Abstract
The endoplasmic reticulum (ER), which is composed of a continuous network of tubules and sheets, forms the most widely distributed membrane system in eukaryotic cells. As a result, it engages a variety of organelles by establishing membrane contact sites (MCSs). These contacts regulate organelle positioning and remodeling, including fusion and fission, facilitate precise lipid exchange, and couple vital signaling events. Here, we systematically review recent advances and converging themes on ER-involved organellar contact. The molecular basis, cellular influence, and potential physiological functions for ER/nuclear envelope contacts with mitochondria, Golgi, endosomes, lysosomes, lipid droplets, autophagosomes, and plasma membrane are summarized.
This is a preview of subscription content, log in via an institution to check access.
References
AhYoung, A.P., Jiang, J., Zhang, J., Khoi Dang, X., Loo, J.A., Zhou, Z.H., and Egea, P.F. (2015). Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci USA 112, E3179–3188.
Allison, R., Edgar, J.R., Pearson, G., Rizo, T., Newton, T., Günther, S., Berner, F., Hague, J., Connell, J.W., Winkler, J., et al. (2017). Defects in ER-endosome contacts impact lysosome function in hereditary spastic paraplegia. J Cell Biol 216, 1337–1355.
Allison, R., Lumb, J.H., Fassier, C., Connell, J.W., Ten Martin, D., Seaman, M.N.J., Hazan, J., and Reid, E. (2013). An ESCRT-spastin interaction promotes fission of recycling tubules from the endosome. J Cell Biol 202, 527–543.
Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., Spiegelhalter, C., Kessler, P., Mathelin, C., Rio, M.C., et al. (2013). STARD3/STARD3NL and VAP make a novel molecular tether between late endosomes and the ER. J Cell Sci 126, jcs.139295.
Alpy, F., and Tomasetto, C. (2014). START ships lipids across interorganelle space. Biochimie 96, 85–95.
Alva, V., and Lupas, A.N. (2016). The TULIP superfamily of eukaryotic lipid-binding proteins as a mediator of lipid sensing and transport. Biochim Biophys Acta 1861, 913–923.
Antonny, B., Bigay, J., and Mesmin, B. (2018). The oxysterol-binding protein cycle: burning off PI(4)P to transport cholesterol. Annu Rev Biochem 87, 809–837.
Appenzeller-Herzog, C., and Hauri, H.P. (2006). The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119, 2173–2183.
Arruda, A.P., Pers, B.M., Parlakgül, G., Güney, E., Inouye, K., and Hotamisligil, G.S. (2014). Chronic enrichment of hepatic endoplasmic reticulum-mitochondria contact leads to mitochondrial dysfunction in obesity. Nat Med 20, 1427–1435.
Atakpa, P., Thillaiappan, N.B., Mataragka, S., Prole, D.L., and Taylor, C.W. (2018). IP3 receptors preferentially associate with ER-lysosome contact sites and selectively deliver Ca2+ to lysosomes. Cell Rep 25, 3180–3193.e7.
Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., Griffiths, G., and Ktistakis, N.T. (2008). Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182, 685–701.
Ba, Q., Raghavan, G., Kiselyov, K., and Yang, G. (2018). Whole-cell scale dynamic organization of lysosomes revealed by spatial statistical analysis. Cell Rep 23, 3591 -3606.
Ballabio, A., and Bonifacino, J.S. (2020). Lysosomes as dynamic regulators of cell and organismal homeostasis. Nat Rev Mol Cell Biol 21, 101–118.
Ban, T., Ishihara, T., Kohno, H., Saita, S., Ichimura, A., Maenaka, K., Oka, T., Mihara, K., and Ishihara, N. (2017). Molecular basis of selective mitochondrial fusion by heterotypic action between OPA1 and cardiolipin. Nat Cell Biol 19, 856–863.
Bannykh, S.I., Rowe, T., and Balch, W.E. (1996). The organization of endoplasmic reticulum export complexes. J Cell Biol 135, 19–35.
Bard, F., Casano, L., Mallabiabarrena, A., Wallace, E., Saito, K., Kitayama, H., Guizzunti, G., Hu, Y., Wendler, F., Dasgupta, R., et al. (2006). Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439, 604–607.
Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M.F., Ravazzola, M., Amherdt, M., et al. (1994). COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895–907.
Barlowe, C.K., and Miller, E.A. (2013). Secretory protein biogenesis and traffic in the early secretory pathway. Genetics 193, 383–410.
Baughman, J.M., Perocchi, F., Girgis, H.S., Plovanich, M., Belcher-Timme, C.A., Sancak, Y., Bao, X.R., Strittmatter, L., Goldberger, O., Bogorad, R.L., et al. (2011). Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341–345.
Baumann, O., and Walz, B. (2001). Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205, 149–214.
Bean, B.D.M., Dziurdzik, S.K., Kolehmainen, K.L., Fowler, C.M.S., Kwong, W.K., Grad, L.I., Davey, M., Schluter, C., and Conibear, E. (2018). Competitive organelle-specific adaptors recruit Vps13 to membrane contact sites. J Cell Biol 217, 3593–3607.
Berridge, M.J., and Irvine, R.F. (1989). Inositol phosphates and cell signalling. Nature 341, 197–205.
Berridge, M.J., Lipp, P., and Bootman, M.D. (2000). The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1, 11–21.
Besprozvannaya, M., Dickson, E., Li, H., Ginburg, K.S., Bers, D.M., Auwerx, J., and Nunnari, J. (2018). GRAM domain proteins specialize functionally distinct ER-PM contact sites in human cells. eLife 7, e31019.
Bian, X., and De Camilli, P. (2019). In vitro assays to measure the membrane tethering and lipid transport activities of the extended synaptotagmins. Methods Mol Biol 1949, 201–212.
Bian, X., Zhang, Z., Xiong, Q., De Camilli, P., and Lin, C. (2019). A programmable DNA-origami platform for studying lipid transfer between bilayers. Nat Chem Biol 15, 830–837.
Bockler, S., and Westermann, B. (2014). Mitochondrial ER contacts are crucial for mitophagy in yeast. Dev Cell 28, 450–458.
Brandizzi, F., and Barlowe, C. (2013). Organization of the ER-Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14, 382–392.
Burkhardt, J.K., Echeverri, C.J., Nilsson, T., and Vallee, R.B. (1997). Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139, 469–484.
Bykov, Y.S., Schaffer, M., Dodonova, S.O., Albert, S., Plitzko, J.M., Baumeister, W., Engel, B.D., and Briggs, J.A. (2017). The structure of the COPI coat determined within the cell. eLife 6, e32493.
Cabukusta, B., and Neefjes, J. (2018). Mechanisms of lysosomal positioning and movement. Traffic 19, 761–769.
Cancela, J.M., Churchill, G.C., and Galione, A. (1999). Coordination of agonist-induced Ca2+-signalling patterns by NAADP in pancreatic acinar cells. Nature 398, 74–76.
Carlton, J.G., Jones, H., and Eggert, U.S. (2020). Membrane and organelle dynamics during cell division. Nat Rev Mol Cell Biol 21, 151–166.
Castellano Brian, M., Thelen, A.M., Moldavski, O., Feltes, M.K., van der Welle, R.E.N., Mydock-McGrane, L., Jiang, X., van Eijkeren, R.J., Davis, O.B., et al. (2017). Lysosomal cholesterol activates mTORC1 via an SLC38A9-Niemann Pick C1 signaling complex. Science 355, 1306–1311.
Champion, L., Linder, M.I., and Kutay, U. (2017). Cellular reorganization during mitotic entry. Trends Cell Biol 27, 26–41.
Chang, C.L., Chen, Y.J., and Liou, J. (2017). ER-plasma membrane junctions: why and how do we study them? Biochim Biophys Acta 1864, 1494–1506.
Chang, C.L., Chen, Y.J., Quintanilla, C.G., Hsieh, T.S., and Liou, J. (2018). EB1 binding restricts STIM1 translocation to ER-PM junctions and regulates store-operated Ca2+ entry. J Cell Biol 217, 2047–2058.
Chang, C.L., Hsieh, T.S., Yang, T.T., Rothberg, K.G., Azizoglu, D.B., Volk, E., Liao, J.C., and Liou, J. (2013). Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep 5, 813–825.
Chang, C.L., and Liou, J. (2015). Phosphatidylinositol 4,5-Bisphosphate homeostasis regulated by Nir2 and nir3 proteins at endoplasmic reticulum-plasma membrane junctions. J Biol Chem 290, 14289–14301.
Chauhan, S., Kumar, S., Jain, A., Ponpuak, M., Mudd, M.H., Kimura, T., Choi, S.W., Peters, R., Mandell, M., et al. (2016). TRIMs and galectins globally cooperate and TRIM16 and Galectin-3 co-direct autophagy in endomembrane damage homeostasis. Dev Cell 39, 13–27.
Chio, U.S., Cho, H., and Shan, S. (2017). Mechanisms of tail-anchored membrane protein targeting and insertion. Annu Rev Cell Dev Biol 33, 417–438.
Chowdhury, S., Otomo, C., Leitner, A., Ohashi, K., Aebersold, R., Lander, G.C., and Otomo, T. (2018). Insights into autophagosome biogenesis from structural and biochemical analyses of the ATG2A-WIPI4 complex. Proc Natl Acad Sci USA 115, E9792–E9801.
Chung, J., Torta, F., Masai, K., Lucast, L., Czapla, H., Tanner, L.B., Narayanaswamy, P., Wenk, M.R., Nakatsu, F., and De Camilli, P. (2015). PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349, 428–432.
Clark, B.J. (2012). The mammalian START domain protein family in lipid transport in health and disease. J Endocrinol 212, 257–275.
Cockcroft, S., Garner, K., Yadav, S., Gomez-Espinoza, E., and Raghu, P. (2016). RdgBa reciprocally transfers PA and PI at ER-PM contact sites to maintain PI(4,5)P2 homoeostasis during phospholipase C signalling in Drosophila photoreceptors. Biochem Soc Trans 44, 286–292.
Cohen, S., Valm, A.M., and Lippincott-Schwartz, J. (2018). Interacting organelles. Curr Opin Cell Biol 53, 84–91.
Collado, J., Kalemanov, M., Campelo, F., Bourgoint, C., Thomas, F., Loewith, R., Martínez-Sánchez, A., Baumeister, W., Stefan, C.J., and Fernández-Busnadiego, R. (2019). Tricalbin-mediated contact sites control ER curvature to maintain plasma membrane integrity. Dev Cell 51, 476–487.e7.
Connelly, S.V., Manzella-Lapeira, J., Levine, Z.C., Brzostowski, J., Krymskaya, L., Rahman, R.S., Ellis, A.C., Amin, S.N., Sa, J.M., Wellems, T.E., et al. (2021). Restructured mitochondrial-nuclear interaction in Plasmodium falciparum dormancy and persister survival after artemisinin exposure. mBio 12, e0075321.
Csordas, G., Weaver, D., and Hajnoczky, G. (2018). Endoplasmic reticulum-mitochondrial contactology: structure and signaling functions. Trends Cell Biol 28, 523–540.
Datta, S., Liu, Y., Hariri, H., Bowerman, J., and Henne, W.M. (2019). Cerebellar ataxia disease-associated Snx14 promotes lipid droplet growth at ER-droplet contacts. J Cell Biol 218, 1335–1351.
de Brito, O.M., and Scorrano, L. (2008). Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456, 605–610.
De Matteis, M.A., and Rega, L.R. (2015). Endoplasmic reticulum-Golgi complex membrane contact sites. Curr Opin Cell Biol 35, 43–50.
De Vos, K.J., Mórotz, G.M., Stoica, R., Tudor, E.L., Lau, K.F., Ackerley, S., Warley, A., Shaw, C.E., and Miller, C.C.J. (2012). VAPB interacts with the mitochondrial protein PTPIP51 to regulate calcium homeostasis. Hum Mol Genet 21, 1299–1311.
Desai, R., East, D.A., Hardy, L., Faccenda, D., Rigon, M., Crosby, J., Alvarez, M.S., Singh, A., Mainenti, M., Hussey, L.K., et al. (2020). Mitochondria form contact sites with the nucleus to couple prosurvival retrograde response. Sci Adv 6, eabc9955.
Di Mattia, T., Wilhelm, L.P., Ikhlef, S., Wendling, C., Spehner, D., Nomine, Y., Giordano, F., Mathelin, C., Drin, G., Tomasetto, C., et al. (2020). Faraway, so close! Functions of Endoplasmic reticulum-Endosome contacts. Biochim Biophys Acta Mol Cell Biol Lipids 1865, 158490.
Di Mattia, T., Wilhelm, L.P., Ikhlef, S., Wendling, C., Spehner, D., Nomine, Y., Giordano, F., Mathelin, C., Drin, G., Tomasetto, C., et al. (2018). Identification of MOSPD2, a novel scaffold for endoplasmic reticulum membrane contact sites. EMBO Rep 19, e45453.
Dimitrov, L., Lam, S.K., and Schekman, R. (2013). The role of the endoplasmic reticulum in peroxisome biogenesis. Cold Spring Harb Perspect Biol 5, a013243.
Ding, L., Yang, X., Tian, H., Liang, J.J., Zhang, F.X., Wang, G.D., Wang, Y.C., Ding, M., Shui, G.H., and Huang, X. (2018). Seipin regulates lipid homeostasis by ensuring calcium-dependent mitochondrial metabolism. EMBO J 37, e97572.
Doghman-Bouguerra, M., Granatiero, V., Sbiera, S., Sbiera, I., Lacas-Gervais, S., Brau, F., Fassnacht, M., Rizzuto, R., and Lalli, E. (2016). FATE1 antagonizes calcium- and drug-induced apoptosis by uncoupling ER and mitochondria. EMBO Rep 17, 1264–1280.
Dong, J., Du, X., Wang, H., Wang, J., Lu, C., Chen, X., Zhu, Z., Luo, Z., Yu, L., Brown, A.J., et al. (2019). Allosteric enhancement of ORP1-mediated cholesterol transport by PI(4,5)P2/PI(3,4)P2. Nat Commun 10, 829.
Dong, R., Saheki, Y., Swarup, S., Lucast, L., Harper, J.W., and De Camilli, P. (2016). Endosome-ER contacts control actin nucleation and retromer function through VAP-dependent regulation of PI4P. Cell 166, 408–423.
Du, X., Kumar, J., Ferguson, C., Schulz, T.A., Ong, Y.S., Hong, W., Prinz, W.A., Parton, R.G., Brown, A.J., and Yang, H. (2011). A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J Cell Biol 192, 121–135.
Du, X., Zhou, L., Aw, Y.C., Mak, H.Y., Xu, Y., Rae, J., Wang, W., Zadoorian, A., Hancock, S.E., Osborne, B., et al. (2020). ORP5 localizes to ER-lipid droplet contacts and regulates the level of PI(4)P on lipid droplets. J Cell Biol 219, e201905162.
Eapen, V.V., Swarup, S., Hoyer, M.J., Paulo, J.A., and Harper, J.W. (2021). Quantitative proteomics reveals the selectivity of ubiquitin-binding autophagy receptors in the turnover of damaged lysosomes by lysophagy. eLife 10, e72328.
Eden, E.R., Sanchez-Heras, E., Tsapara, A., Sobota, A., Levine, T.P., and Futter, C.E. (2016). Annexin A1 tethers membrane contact sites that mediate ER to endosome cholesterol transport. Dev Cell 37, 473–483.
Eden, E.R., White, I.J., Tsapara, A., and Futter, C.E. (2010). Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat Cell Biol 12, 267–272.
Eisenberg-Bord, M., Zung, N., Collado, J., Drwesh, L., Fenech, E.J., Fadel, A., Dezorella, N., Bykov, Y.S., Rapaport, D., Fernandez-Busnadiego, R., et al. (2021). Cnm1 mediates nucleus-mitochondria contact site formation in response to phospholipid levels. J Cell Biol 220, e202104100.
Encinar Del Dedo, J., Fernandez-Golbano, I.M., Pastor, L., Meler, P., Ferrer-Orta, C., Rebollo, E., and Geli, M.I. (2021). Coupled sterol synthesis and transport machineries at ER-endocytic contact sites. J Cell Biol 220, e202010016.
Endo, M. (2009). Calcium-induced calcium release in skeletal muscle. Physiol Rev 89, 1153–1176.
Ercan, B., Naito, T., Koh, D.H.Z., Dharmawan, D., and Saheki, Y. (2021). Molecular basis of accessible plasma membrane cholesterol recognition by the GRAM domain of GRAMD1b. EMBOJ40, e106524.
Faelber, K., Dietrich, L., Noel, J.K., Wollweber, F., Pfitzner, A.K., Mühleip, A., Sanchez, R., Kudryashev, M., Chiaruttini, N., Lilie, H., et al. (2019). Structure and assembly of the mitochondrial membrane remodelling GTPase Mgm1. Nature 571, 429–433.
Farias, G.G., Freal, A., Tortosa, E., Stucchi, R., Pan, X., Portegies, S., Will, L., Altelaar, M., and Hoogenraad, C.C. (2019). Feedback-driven mechanisms between microtubules and the endoplasmic reticulum instruct neuronal polarity. Neuron 102, 184–201.e8.
Fei, W.H., Shui, G.H., Gaeta, B., Du, X.M., Kuerschner, L., Li, P., Brown, A.J., Wenk, M.R., Parton, R.G., and Yang, H. (2008). Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J Cell Biol 180, 473–482.
Feng, Y., He, D., Yao, Z., and Klionsky, D.J. (2014). The machinery of macroautophagy. Cell Res 24, 24–41.
Feng, Z., Yang, K., and Pastor-Pareja, J.C. (2021). Tales of the ER-Golgi Frontier: Drosophila-centric considerations on Tango1 function. Front Cell Dev Biol 8, 619022.
Fernandez-Busnadiego, R., Saheki, Y., and De Camilli, P. (2015). Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. Proc Natl Acad Sci USA 112, E2004-2013.
Ferrari, A., He, C., Kennelly, J.P., Sandhu, J., Xiao, X., Chi, X., Jiang, H., Young, S.G., and Tontonoz, P. (2020). Aster proteins regulate the accessible cholesterol pool in the plasma membrane. Mol Cell Biol 40, e00255–20.
Feske, S., Gwack, Y., Prakriya, M., Srikanth, S., Puppel, S.H., Tanasa, B., Hogan, P.G., Lewis, R.S., Daly, M., and Rao, A. (2006). A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179–185.
Filadi, R., Greotti, E., Turacchio, G., Luini, A., Pozzan, T., and Pizzo, P. (2015). Mitofusin 2 ablation increases endoplasmic reticulum-mitochondria coupling. Proc Natl Acad Sci USA 112, E2174–2181.
Fischer, M.A., Temmerman, K., Ercan, E., Nickel, W., and Seedorf, M. (2009). Binding of plasma membrane lipids recruits the yeast integral membrane protein Ist2 to the cortical ER. Traffic 10, 1084–1097.
Fox, P.D., Haberkorn, C.J., Akin, E.J., Seel, P.J., Krapf, D., and Tamkun, M.M. (2015). Induction of stable ER-plasma-membrane junctions by Kv2.1 potassium channels. J Cell Sci 128, 2096–2105.
Friedman, J.R., DiBenedetto, J.R., West, M., Rowland, A.A., and Voeltz, G.K. (2013). Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol Biol Cell 24, 1030–1040.
Friedman, J.R., Lackner, L.L., West, M., DiBenedetto, J.R., Nunnari, J., and Voeltz, G.K. (2011). ER tubules mark sites of mitochondrial division. Science 334, 358–362.
Fromme, J.C., and Schekman, R. (2005). COPII-coated vesicles: flexible enough for large cargo? Curr Opin Cell Biol 17, 345–352.
Fukasawa, M., Nishijima, M., and Hanada, K. (1999). Genetic evidence for ATP-dependent endoplasmic reticulum-to-Golgi apparatus trafficking of ceramide for sphingomyelin synthesis in Chinese hamster ovary cells. J Cell Biol 144, 673–685.
Galione, A., Morgan, A.J., Arredouani, A., Davis, L.C., Rietdorf, K., Ruas, M., and Parrington, J. (2010). NAADP as an intracellular messenger regulating lysosomal calcium-release channels. Biochem Soc Trans 38, 1424–1431.
Galmes, R., Houcine, A., van Vliet, A.R., Agostinis, P., Jackson, C.L., and Giordano, F. (2016). ORP5/ORP8 localize to endoplasmic reticulum-mitochondria contacts and are involved in mitochondrial function. EMBO Rep 17, 800–810.
Gao, G., Sheng, Y., Yang, H., Chua, B.T., and Xu, L. (2019a). DFCP1 associates with lipid droplets. Cell Biol Int 43, 1492–1504.
Gao, M., Huang, X., Song, B.L., and Yang, H. (2019b). The biogenesis of lipid droplets: lipids take center stage. Prog Lipid Res 75, 100989.
Gatta, A.T., Wong, L.H., Sere, Y.Y., Calderon-Norena, D.M., Cockcroft, S., Menon, A. K., and Levine, T.P. (2015). A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. eLife 4, e07253.
Ge, J., Bian, X., Ma, L., Cai, Y., Li, Y., Yang, J., Karatekin, E., De Camilli, P., and Zhang, Y. (2022). Stepwise membrane binding of extended synaptotagmins revealed by optical tweezers. Nat Chem Biol 18, 313–320.
Ge, L., Melville, D., Zhang, M., and Schekman, R. (2013). The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife 2, e00947.
Ge, L., Zhang, M., Kenny, S.J., Liu, D., Maeda, M., Saito, K., Mathur, A., Xu, K., and Schekman, R. (2017). Remodeling of ER-exit sites initiates a membrane supply pathway for autophagosome biogenesis. EMBO Rep 18, 1586–1603.
Ge, L., Zhang, M., and Schekman, R. (2014). Phosphatidylinositol 3-kinase and COPII generate LC3 lipidation vesicles from the ER-Golgi intermediate compartment. eLife 3, e04135.
Gelmetti, V., De Rosa, P., Torosantucci, L., Marini, E.S., Romagnoli, A., Di Rienzo, M., Arena, G., Vignone, D., Fimia, G.M., and Valente, E.M. (2017). PINK1 and BECN1 relocalize at mitochondria-associated membranes during mitophagy and promote ER-mitochondria tethering and autophagosome formation. Autophagy 13, 654–669.
Gerasimenko, J.V., Charlesworth, R.M., Sherwood, M.W., Ferdek, P.E., Mikoshiba, K., Parrington, J., Petersen, O.H., and Gerasimenko, O.V. (2015). Both RyRs and TPCs are required for NAADP-induced intracellular Ca2+ release. Cell Calcium 58, 237–245.
Ghai, R., Du, X., Wang, H., Dong, J., Ferguson, C., Brown, A.J., Parton, R.G., Wu, J. W., and Yang, H. (2017). ORP5 and ORP8 bind phosphatidylinositol-4,5-biphosphate (PtdIns(4,5)P2) and regulate its level at the plasma membrane. Nat Commun 8, 757.
Ghanbarpour, A., Valverde, D.P., Melia, T.J., and Reinisch, K.M. (2021). A model for a partnership of lipid transfer proteins and scramblases in membrane expansion and organelle biogenesis. Proc Natl Acad Sci USA 118, e2101562118.
Giordano, F., Saheki, Y., Idevall-Hagren, O., Colombo, S.F., Pirruccello, M., Milosevic, I., Gracheva, E.O., Bagriantsev, S.N., Borgese, N., and De Camilli, P. (2013). PI(4,5) P2-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153, 1494–1509.
Golini, L., Chouabe, C., Berthier, C., Cusimano, V., Fornaro, M., Bonvallet, R., Formoso, L., Giacomello, E., Jacquemond, V., and Sorrentino, V. (2011). Junctophilin 1 and 2 proteins interact with the L-type Ca2+ channel dihydropyridine receptors (DHPRs) in skeletal muscle. J Biol Chem 286, 43717–43725.
Gomez-Navarro, N., and Miller, E. (2016). Protein sorting at the ER-Golgi interface. J Cell Biol 215, 769–778.
Gomez-Sanchez, R., Rose, J., Guimaraes, R., Mari, M., Papinski, D., Rieter, E., Geerts, W.J., Hardenberg, R., Kraft, C., Ungermann, C., et al. (2018). Atg9 establishes Atg2-dependent contact sites between the endoplasmic reticulum and phagophores. J Cell Biol 217, 2743–2763.
Gomez-Sanchez, R., Tooze, S.A., and Reggiori, F. (2021). Membrane supply and remodeling during autophagosome biogenesis. Curr Opin Cell Biol 71, 112–119.
Gómez-Suaga, P., Bravo-San Pedro, J.M., González-Polo, R.A., Fuentes, J.M., and Niso-Santano, M. (2018). ER-mitochondria signaling in Parkinson’s disease. Cell Death Dis 9, 337.
Gomez-Suaga, P., Paillusson, S., and Miller, C.C.J. (2017). ER-mitochondria signaling regulates autophagy. Autophagy 13, 1250–1251.
Graef, M., Friedman, J.R., Graham, C., Babu, M., and Nunnari, J. (2013). ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell 24, 2918–2931.
Grippa, A., Buxó, L., Mora, G., Funaya, C., Idrissi, F.Z., Mancuso, F., Gomez, R., Muntanyà, J., Sabidó, E., and Carvalho, P. (2015). The seipin complex Fld1/Ldb16 stabilizes ER-lipid droplet contact sites. J Cell Biol 211, 829–844.
Guardia, C.M., Farias, G.G., Jia, R., Pu, J., and Bonifacino, J.S. (2016). BORC functions upstream of Kinesins 1 and 3 to coordinate regional movement of lysosomes along different microtubule tracks. Cell Rep 17, 1950–1961.
Guillén-Samander, A., Bian, X., and De Camilli, P. (2019). PDZD8 mediates a Rab7-dependent interaction of the ER with late endosomes and lysosomes. Proc Natl Acad Sci USA 116, 22619–22623.
Guillén-Samander, A., and De Camilli, P. (2023). Endoplasmic reticulum membrane contact sites, lipid transport, and neurodegeneration. Cold Spring Harb Perspect Biol 15, a041257.
Guna, A., Stevens, T.A., Inglis, A.J., Replogle, J.M., Esantsi, T.K., Muthukumar, G., Shaffer, K.C.L., Wang, M.L., Pogson, A.N., Jones, J.J., et al. (2022). MTCH2 is a mitochondrial outer membrane protein insertase. Science 378, 317–322.
Guo, Y., Li, D., Zhang, S., Yang, Y., Liu, J.J., Wang, X., Liu, C., Milkie, D.E., Moore, R. P., Tulu, U.S., et al. (2018). Visualizing intracellular organelle and cytoskeletal interactions at nanoscale resolution on millisecond timescales. Cell 175, 1430–1442.e17.
Gutierrez, T., and Simmen, T. (2018). Endoplasmic reticulum chaperones tweak the mitochondrial calcium rheostat to control metabolism and cell death. Cell Calcium 70, 64–75.
Güttinger, S., Laurell, E., and Kutay, U. (2009). Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat Rev Mol Cell Biol 10, 178–191.
Haj, F.G., Verveer, P.J., Squire, A., Neel, B.G., and Bastiaens, P.I.H. (2002). Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science 295, 1708–1711.
Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., et al. (2013). Autophagosomes form at ER-mitochondria contact sites. Nature 495, 389–393.
Hanada, K., Kumagai, K., Yasuda, S., Miura, Y., Kawano, M., Fukasawa, M., and Nishijima, M. (2003). Molecular machinery for non-vesicular trafficking of ceramide. Nature 426, 803–809.
Hancock-Cerutti, W., Wu, Z., Xu, P., Yadavalli, N., Leonzino, M., Tharkeshwar, A.K., Ferguson, S.M., Shadel, G.S., and De Camilli, P. (2022). ER-lysosome lipid transfer protein VPS13C/PARK23 prevents aberrant mtDNA-dependent STING signaling. J Cell Biol 221, e202106046.
Hanna, M.G., Block, S., Frankel, E.B., Hou, F., Johnson, A., Yuan, L., Knight, G., Moresco, J.J., Yates, J.R., Ashton, R., et al. (2017). TFG facilitates outer coat disassembly on COPII transport carriers to promote tethering and fusion with ER-Golgi intermediate compartments. Proc Natl Acad Sci USA 114, E7707–E7716.
Harada, A., Takei, Y., Kanai, Y., Tanaka, Y., Nonaka, S., and Hirokawa, N. (1998). Golgi vesiculation and Lysosome dispersion in cells lacking cytoplasmic dynein. J Cell Biol 141, 51–59.
Hariri, H., Speer, N., Bowerman, J., Rogers, S., Fu, G., Reetz, E., Datta, S., Feathers, J. R., Ugrankar, R., Nicastro, D., et al. (2019). Mdm1 maintains endoplasmic reticulum homeostasis by spatially regulating lipid droplet biogenesis. J Cell Biol 218, 1319–1334.
Hayashi, T., Rizzuto, R., Hajnoczky, G., and Su, T.P. (2009). MAM: more than just a housekeeper. Trends Cell Biol 19, 81–88.
Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 11, 1433–1437.
Helle, S.C.J., Kanfer, G., Kolar, K., Lang, A., Michel, A.H., and Kornmann, B. (2013). Organization and function ofmembrane contact sites. Biochim Biophys Acta 1833, 2526–2541.
Henkart, M., Landis, D.M., and Reese, T.S. (1976). Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J Cell Biol 70, 338–347.
Hirabayashi, Y., Kwon, S.K., Paek, H., Pernice, W.M., Paul, M.A., Lee, J., Erfani, P., Raczkowski, A., Petrey, D.S., Pon, L.A., et al. (2017). ER-mitochondria tethering by PDZD8 regulates Ca2+ dynamics in mammalian neurons. Science 358, 623–630.
Hoffmann, P.C., Bharat, T.A.M., Wozny, M.R., Boulanger, J., Miller, E.A., and Kukulski, W. (2019). Tricalbins contribute to cellular lipid flux and form curved ER-PM contacts that are bridged by rod-shaped structures. Dev Cell 51, 488–502. e8.
Hoglinger, D., Burgoyne, T., Sanchez-Heras, E., Hartwig, P., Colaco, A., Newton, J., Futter, C.E., Spiegel, S., Platt, F.M., and Eden, E.R. (2019). NPC1 regulates ER contacts with endocytic organelles to mediate cholesterol egress. Nat Commun 10, 4276.
Holmes, S.E., O’Hearn, E., Rosenblatt, A., Callahan, C., Hwang, H.S., Ingersoll-Ashworth, R.G., Fleisher, A., Stevanin, G., Brice, A., Potter, N.T., et al. (2001). A repeat expansion in the gene encoding junctophilin-3 is associated with Huntington disease-like 2. Nat Genet 29, 377–378.
Hong, Z., Adlakha, J., Wan, N., Guinn, E., Giska, F., Gupta, K., Melia, T.J., and Reinisch, K.M. (2022). Mitoguardin-2-mediated lipid transfer preserves mitochondrial morphology and lipid droplet formation. J Cell Biol 221, e202207022.
Horenkamp, F.A., Valverde, D.P., Nunnari, J., and Reinisch, K.M. (2018). Molecular basis for sterol transport by StART-like lipid transfer domains. EMBO J 37, e98002.
Hoth, M., and Penner, R. (1992). Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355, 353–356.
Hoyer, M.J., Chitwood, P.J., Ebmeier, C.C., Striepen, J.F., Qi, R.Z., Old, W.M., and Voeltz, G.K. (2018). A novel class of ER membrane proteins regulates ER-associated endosome fission. Cell 175, 254–265.e14.
Hugenroth, M., and Bohnert, M. (2020). Come a little bit closer! Lipid droplet-ER contact sites are getting crowded. Biochim Biophys Acta 1867, 118603.
Hughes, H., Budnik, A., Schmidt, K., Palmer, K.J., Mantell, J., Noakes, C., Johnson, A., Carter, D.A., Verkade, P., Watson, P., et al. (2009). Organisation ofhuman ER-exit sites: requirements for the localisation of Sec16 to transitional ER. J Cell Sci 122, 2924–2934.
Hung, V., Lam, S.S., Udeshi, N.D., Svinkina, T., Guzman, G., Mootha, V.K., Carr, S.A., and Ting, A.Y. (2017). Proteomic mapping of cytosol-facing outer mitochondrial and ER membranes in living human cells by proximity biotinylation. eLife 6, e24463.
Huotari, J., and Helenius, A. (2011). Endosome maturation. EMBO J 30, 3481–3500.
Iaea, D.B., Mao, S., Lund, F.W., and Maxfield, F.R. (2017). Role of STARD4 in sterol transport between the endocytic recycling compartment and the plasma membrane. Mol Biol Cell 28, 1111–1122.
Iaea, D.B., Spahr, Z.R., Singh, R.K., Chan, R.B., Zhou, B., Bareja, R., Elemento, O., Di Paolo, G., Zhang, X., and Maxfield, F.R. (2020). Stable reduction of STARD4 alters cholesterol regulation and lipid homeostasis. Biochim Biophys Acta 1865, 158609.
Idevall-Hagren, O., Lu, A., Xie, B., and De Camilli, P. (2015). Triggered Ca2+ influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering. EMBO J 34, 2291–2305.
Jacquemyn, J., Cascalho, A., and Goodchild, R.E. (2017). The ins and outs of endoplasmic reticulum-controlled lipid biosynthesis. EMBO Rep 18, 1905–1921.
Jansen, M., Ohsaki, Y., Rita Rega, L., Bittman, R., Olkkonen, V.M., and Ikonen, E. (2011). Role of ORPs in sterol transport from plasma membrane to ER and lipid droplets in mammalian cells. Traffic 12, 218–231.
Jensen, D., and Schekman, R. (2011). COPII-mediated vesicle formation at a glance. J Cell Sci 124, 1–4.
Jentsch, J.A., Kiburu, I., Pandey, K., Timme, M., Ramlall, T., Levkau, B., Wu, J., Eliezer, D., Boudker, O., and Menon, A.K. (2018). Structural basis of sterol binding and transport by a yeast StARkin domain. J Biol Chem 293, 5522–5531.
Jeyasimman, D., and Saheki, Y. (2020). SMP domain proteins in membrane lipid dynamics. Biochim Biophys Acta 1865, 158447.
Jha, A., Ahuja, M., Patel, S., Brailoiu, E., and Muallem, S. (2014). Convergent regulation of the lysosomal two-pore channel-2 by Mg2+, NAADP, PI(3,5)P2 and multiple protein kinases. EMBO J 33, 501–511.
Jha, A., Chung, W.Y., Vachel, L., Maleth, J., Lake, S., Zhang, G., Ahuja, M., and Muallem, S. (2019). Anoctamin 8 tethers endoplasmic reticulum and plasma membrane for assembly of Ca2+ signaling complexes at the ER/PM compartment. EMBO J 38, e101452.
Ji, C., Zhao, H., Chen, D., Zhang, H., and Zhao, Y.G. (2021). β-propeller proteins WDR45 and WDR45B regulate autophagosome maturation into autolysosomes in neural cells. Curr Biol 31, 1666–1677.e6.
Jing, J., He, L., Sun, A., Quintana, A., Ding, Y., Ma, G., Tan, P., Liang, X., Zheng, X., Chen, L., et al. (2015). Proteomic mapping of ER-PM junctions identifies STIMATE as a regulator of Ca2+ influx. Nat Cell Biol 17, 1339–1347.
Johannes, L., Jacob, R., and Leffler, H. (2018). Galectins at a glance. J Cell Sci 131, jcs208884.
Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V.M., and Neefjes, J. (2007). Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor βlll spectrin. J Cell Biol 176, 459–471.
John Peter, A.T., Petrungaro, C., Peter, M., and Kornmann, B. (2022). METALIC reveals interorganelle lipid flux in live cells by enzymatic mass tagging. Nat Cell Biol 24, 996–1004.
Johnson, A., Bhattacharya, N., Hanna, M., Pennington, J.G., Schuh, A.L., Wang, L., Otegui, M.S., Stagg, S.M., and Audhya, A. (2015). TFG clusters COPII-coated transport carriers and promotes early secretory pathway organization. EMBO J 34, 811–827.
Johnson, B., Leek, A.N., Solé, L., Maverick, E.E., Levine, T.P., and Tamkun, M.M. (2018). Kv2 potassium channels form endoplasmic reticulum/plasma membrane junctions via interaction with VAPA and VAPB. Proc Natl Acad Sci USA 115, E7331–E7340.
Jongsma, M.L.M., Berlin, I., Wijdeven, R.H.M., Janssen, L., Janssen, G.M.C., Garstka, M.A., Janssen, H., Mensink, M., van Veelen, P.A., Spaapen, R.M., et al. (2016). An ER-associated pathway defines endosomal architecture for controlled cargo transport. Cell 166, 152–166.
Kaiser, S.E., Brickner, J.H., Reilein, A.R., Fenn, T.D., Walter, P., and Brunger, A.T. (2005). Structural basis of FFAT motif-mediated ER targeting. Structure 13, 1035–1045.
Kameoka, S., Adachi, Y., Okamoto, K., Iijima, M., and Sesaki, H. (2018). Phosphatidic acid and cardiolipin coordinate mitochondrial dynamics. Trends Cell Biol 28, 67–76.
Kang, F., Zhou, M., Huang, X., Fan, J., Wei, L., Boulanger, J., Liu, Z., Salamero, J., Liu, Y., and Chen, L. (2019). E-syt1 re-arranges STIM1 clusters to stabilize ring-shaped ER-PM contact sites and accelerate Ca2+ store replenishment. Sci Rep 9, 3975.
Kawasaki, A., Sakai, A., Nakanishi, H., Hasegawa, J., Taguchi, T., Sasaki, J., Arai, H., Sasaki, T., Igarashi, M., and Nakatsu, F. (2022). PI4P/PS countertransport by ORP10 at ER-endosome membrane contact sites regulates endosome fission. J Cell Biol 221, e202103141.
Kawasaki, T., Lange, I., and Feske, S. (2009). A minimal regulatory domain in the C terminus of STIM1 binds to and activates ORAI1 CRAC channels. Biochem Biophys Res Commun 385, 49–54.
Kelu, J.J., Webb, S.E., Parrington, J., Galione, A., and Miller, A.L. (2017). Ca2+ release via two-pore channel type 2 (TPC2) is required for slow muscle cell myofibrillogenesis and myotomal patterning in intact zebrafish embryos. Dev Biol 425, 109–129.
Kilpatrick, B.S., Eden, E.R., Hockey, L.N., Yates, E., Futter, C.E., and Patel, S. (2017). An endosomal NAADP-sensitive two-pore Ca2+ channel regulates ER-endosome membrane contact sites to control growth factor signaling. Cell Rep 18, 1636–1645.
Kilpatrick, B.S., Eden, E.R., Schapira, A.H., Futter, C.E., and Patel, S. (2013). Direct mobilisation of lysosomal Ca2+ triggers complex Ca2+ signals. J Cell Sci 126, 60–66.
Kim, S., Coukos, R., Gao, F., and Krainc, D. (2022). Dysregulation of organelle membrane contact sites in neurological diseases. Neuron 110, 2386–2408.
Kim, S.H., Kedan, A., Marom, M., Gavert, N., Keinan, O., Selitrennik, M., Laufman, O., and Lev, S. (2013). The phosphatidylinositol-transfer protein Nir2 binds phosphatidic acid and positively regulates phosphoinositide signalling. EMBO Rep 14, 891–899.
Kim, Y.J., Guzman-Hernandez, M.L., Wisniewski, E., and Balla, T. (2015). Phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev Cell 33, 549–561.
Kinnaird, A., Zhao, S., Wellen, K.E., and Michelakis, E.D. (2016). Metabolic control of epigenetics in cancer. Nat Rev Cancer 16, 694–707.
Kinnear, N.P., Wyatt, C.N., Clark, J.H., Calcraft, P.J., Fleischer, S., Jeyakumar, L.H., Nixon, G.F., and Evans, A.M. (2008). Lysosomes co-localize with ryanodine receptor subtype 3 to form a trigger zone for calcium signalling by NAADP in rat pulmonary arterial smooth muscle. Cell Calcium 44, 190–201.
Kirmiz, M., Vierra, N.C., Palacio, S., and Trimmer, J.S. (2018). Identification of VAPA and VAPB as Kv2 channel-interacting proteins defining endoplasmic reticulum-plasma membrane junctions in mammalian brain neurons. J Neurosci 38, 7562–7584.
Kleele, T., Rey, T., Winter, J., Zaganelli, S., Mahecic, D., Perreten Lambert, H., Ruberto, F.P., Nemir, M., Wai, T., Pedrazzini, T., et al. (2021). Distinct fission signatures predict mitochondrial degradation or biogenesis. Nature 593, 435–439.
Kopec, K.O., Alva, V., and Lupas, A.N. (2010). Homology of SMP domains to the TULIP superfamily of lipid-binding proteins provides a structural basis for lipid exchange between ER and mitochondria. Bioinformatics 26, 1927–1931.
Kornmann, B., Currie, E., Collins, S.R., Schuldiner, M., Nunnari, J., Weissman, J.S., and Walter, P. (2009). An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477–481.
Korobova, F., Ramabhadran, V., and Higgs, H.N. (2013). An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339, 464–467.
Korzeniowski, M.K., Popovic, M.A., Szentpetery, Z., Varnai, P., Stojilkovic, S.S., and Balla, T. (2009). Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J Biol Chem 284, 21027–21035.
Kotani, T., Kirisako, H., Koizumi, M., Ohsumi, Y., and Nakatogawa, H. (2018). The Atg2-Atg18 complex tethers pre-autophagosomal membranes to the endoplasmic reticulum for autophagosome formation. Proc Natl Acad Sci USA 115, 10363–10368.
Kumagai, K., Kawano, M., Shinkai-Ouchi, F., Nishijima, M., and Hanada, K. (2007). Interorganelle trafficking of ceramide is regulated by phosphorylation-dependent cooperativity between the PH and START domains of CERT. J Biol Chem 282, 17758–17766.
Kumar, N., Leonzino, M., Hancock-Cerutti, W., Horenkamp, F.A., Li, P.Q., Lees, J.A., Wheeler, H., Reinisch, K.M., and De Camilli, P. (2018). VPS13A and VPS13C are lipid transport proteins differentially localized at ER contact sites. J Cell Biol 217, 3625–3639.
Kurokawa, K., Okamoto, M., and Nakano, A. (2014). Contact of cis-Golgi with ER exit sites executes cargo capture and delivery from the ER. Nat Commun 5, 3653.
Kwak, C., Shin, S., Park, J.S., Jung, M., Nhung, T.T.M., Kang, M.G., Lee, C., Kwon, T. H., Park, S.K., Mun, J.Y., et al. (2020). Contact-ID, a tool for profiling organelle contact sites, reveals regulatory proteins of mitochondrial-associated membrane formation. Proc Natl Acad Sci USA 117, 12109–12120.
Labbe, K., Mookerjee, S., Le Vasseur, M., Gibbs, E., Lerner, C., and Nunnari, J. (2021). The modified mitochondrial outer membrane carrier MTCH2 links mitochondrial fusion to lipogenesis. J Cell Biol 220, e202103122.
Lacruz, R.S., and Feske, S. (2015). Diseases caused by mutations in ORAI1 and STIM1. Ann New York Acad Sci 1356, 45–79.
Landstrom, A.P., Beavers, D.L., and Wehrens, X.H.T. (2014). The junctophilin family of proteins: from bench to bedside. Trends Mol Med 20, 353–362.
Lang, A.B., Peter, A.T.J., Walter, P., and Kornmann, B. (2015). ER-mitochondrial junctions can be bypassed by dominant mutations in the endosomal protein Vps13. J Cell Biol 210, 883–890.
Lang, S., Pfeffer, S., Lee, P.H., Cavalié, A., Helms, V., Förster, F., and Zimmermann, R. (2017). An update on Sec61 channel functions, mechanisms, and related diseases. Front Physiol 8, 887.
Laraia, L., Friese, A., Corkery, D.P., Konstantinidis, G., Erwin, N., Hofer, W., Karatas, H., Klewer, L., Brockmeyer, A., Metz, M., et al. (2019). The cholesterol transfer protein GRAMD1A regulates autophagosome biogenesis. Nat Chem Biol 15, 710–720.
Lawrence, R.E., and Zoncu, R. (2019). The lysosome as a cellular centre for signalling, metabolism and quality control. Nat Cell Biol 21, 133–142.
Lee, I., and Hong, W. (2006). Diverse membrane-associated proteins contain a novel SMP domain. FASEB Journal 20, 202–206.
Lees, J.A., Messa, M., Sun, E.W., Wheeler, H., Torta, F., Wenk, M.R., De Camilli, P., and Reinisch, K.M. (2017). Lipid transport by TMEM24 at ER-plasma membrane contacts regulates pulsatile insulin secretion. Science 355, eaah6171.
Levin-Konigsberg, R., Montano-Rendón, F., Keren-Kaplan, T., Li, R., Ego, B., Mylvaganam, S., DiCiccio, J.E., Trimble, W.S., Bassik, M.C., Bonifacino, J.S., et al. (2019). Phagolysosome resolution requires contacts with the endoplasmic reticulum and phosphatidylinositol-4-phosphate signalling. Nat Cell Biol 21, 1234–1247.
Li, G., Su, B., Fu, P., Bai, Y., Ding, G., Li, D., Wang, J., Yang, G., and Chu, B. (2022a). NPC1-regulated dynamic of clathrin-coated pits is essential for viral entry. Sci China Life Sci 65, 341–361.
Li, P., Lees, J.A., Lusk, C.P., and Reinisch, K.M. (2020). Cryo-EM reconstruction of a VPS13 fragment reveals a long groove to channel lipids between membranes. J Cell Biol 219, e202001161.
Li, S., Yan, R., Xu, J., Zhao, S., Ma, X., Sun, Q., Zhang, M., Li, Y., Liu, J.G., Chen, L., et al. (2022b). A new type of ERGIC-ERES membrane contact mediated by TMED9 and SEC12 is required for autophagosome biogenesis. Cell Res 32, 119–138.
Li, W., Zhang, S., and Yang, G. (2021a). Dynamic organization of intracellular organelle networks. WIREs Mech Dis 13, e1505.
Li, Y.E., Wang, Y., Du, X., Zhang, T., Mak, H.Y., Hancock, S.E., McEwen, H., Pandzic, E., Whan, R.M., Aw, Y.C., et al. (2021b). TMEM41B and VMP1 are scramblases and regulate the distribution of cholesterol and phosphatidylserine. J Cell Biol 220, e202103105.
Lim, C.Y., Davis, O.B., Shin, H.R., Zhang, J., Berdan, C.A., Jiang, X., Counihan, J.L., Ory, D.S., Nomura, D.K., and Zoncu, R. (2019). ER-lysosome contacts enable cholesterol sensing by mTORC1 and drive aberrant growth signalling in Niemann-Pick type C. Nat Cell Biol 21, 1206–1218.
Liou, J., Fivaz, M., Inoue, T., and Meyer, T. (2007). Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. Proc Natl Acad Sci USA 104, 9301–9306.
Liou, J., Kim, M.L., Do Heo, W., Jones, J.T., Myers, J.W., Ferrell, J.E. Jr., and Meyer, T. (2005). STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15, 1235–1241.
Litvak, V., Dahan, N., Ramachandran, S., Sabanay, H., and Lev, S. (2005). Maintenance of the diacylglycerol level in the Golgi apparatus by the Nir2 protein is critical for Golgi secretory function. Nat Cell Biol 7, 225–234.
Liu, L., Yang, S., Liu, Y., Li, X., Hu, J., Xiao, L., and Xu, T. (2022). DeepContact: high-throughput quantification of membrane contact sites based on electron microscopy imaging. J Cell Biol 221, e202106190.
Liu, M., Feng, Z., Ke, H., Liu, Y., Sun, T., Dai, J., Cui, W., and Pastor-Pareja, J.C. (2017). Tango1 spatially organizes ER exit sites to control ER export. J Cell Biol 216, 1035–1049.
Liu, N., Zhao, H., Zhao, Y.G., Hu, J., and Zhang, H. (2021). Atlastin 2/3 regulate ER targeting of the ULK1 complex to initiate autophagy. J Cell Biol 220, e202012091.
Liu, X., Guo, X., Niu, L., Li, X., Sun, F., Hu, J., Wang, X., and Shen, K. (2019a). Atlastin-1 regulates morphology and function of endoplasmic reticulum in dendrites. Nat Commun 10, 568.
Liu, Y., Ma, X., Fujioka, H., Liu, J., Chen, S., and Zhu, X. (2019b). DJ-1 regulates the integrity and function of ER-mitochondria association through interaction with IP3R3-Grp75-VDAC1. Proc Natl Acad Sci USA 116, 25322–25328.
Loewen, C.J., Roy, A., and Levine, T.P. (2003). A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J 22, 2025–2035.
Lopez-Sanjurjo, C.I., Tovey, S.C., Prole, D.L., and Taylor, C.W. (2013). Lysosomes shape ins(1,4,5)P3-evoked Ca2+ signals by selectively sequestering Ca2+ released from the endoplasmic reticulum. J Cell Sci 126, 289–300.
Lu, M., van Tartwijk, F.W., Lin, J.Q., Nijenhuis, W., Parutto, P., Fantham, M., Christensen, C.N., Avezov, E., Holt, C.E., Tunnacliffe, A., et al. (2020). The structure and global distribution of the endoplasmic reticulum network are actively regulated by lysosomes. Sci Adv 6, eabc7209.
Lu, Q., Yang, P., Huang, X., Hu, W., Guo, B., Wu, F., Lin, L., Kovacs, A.L., Yu, L., and Zhang, H. (2011). The WD40 repeat PtdIns(3)P-binding protein EPG-6 regulates progression of omegasomes to autophagosomes. Dev Cell 21, 343–357.
Luo, J., Jiang, L., Yang, H., and Song, B. (2017). Routes and mechanisms of postendosomal cholesterol trafficking: a story that never ends. Traffic 18, 209–217.
Luo, J., Jiang, L.Y., Yang, H., and Song, B.L. (2019). Intracellular cholesterol transport by sterol transfer proteins at membrane contact sites. Trends Biochem Sci 44, 273–292.
Luzio, J.P., Pryor, P.R., and Bright, N.A. (2007). Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8, 622–632.
Maeda, K., Anand, K., Chiapparino, A., Kumar, A., Poletto, M., Kaksonen, M., and Gavin, A.C. (2013). Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501, 257–261.
Maeda, M., Katada, T., and Saito, K. (2017). TANGO1 recruits Sec16 to coordinately organize ER exit sites for efficient secretion. J Cell Biol 216, 1731–1743.
Maeda, S., Otomo, C., and Otomo, T. (2019). The autophagic membrane tether ATG2A transfers lipids between membranes. eLife 8, e45777.
Maejima, I., Takahashi, A., Omori, H., Kimura, T., Takabatake, Y., Saitoh, T., Yamamoto, A., Hamasaki, M., Noda, T., Isaka, Y., et al. (2013). Autophagy sequesters damaged lysosomes to control lysosomal biogenesis and kidney injury. EMBO J 32, 2336–2347.
Magré, J., Delépine, M., Khallouf, E., Gedde-Dahl Jr, T., Van Maldergem, L., Sobel, E., Papp, J., Meier, M., Mégarbané, A., BSCL Working Group, et al. (2001). Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nat Genet 28, 365–370.
Malhotra, V., and Erlmann, P. (2015). The pathway of collagen secretion. Annu Rev Cell Dev Biol 31, 109–124.
Manford, A.G., Stefan, C.J., Yuan, H.L., MacGurn, J.A., and Emr, S.D. (2012). ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell 23, 1129–1140.
Manik, M.K., Yang, H., Tong, J., and Im, Y.J. (2017). Structure of yeast OSBP-related protein Osh1 reveals key determinants for lipid transport and protein targeting at the nucleus-vacuole junction. Structure 25, 617–629.e3.
Manor, U., Bartholomew, S., Golani, G., Christenson, E., Kozlov, M., Higgs, H., Spudich, J., and Lippincott-Schwartz, J. (2015). A mitochondria-anchored isoform of the actin-nucleating spire protein regulates mitochondrial division. eLife 4, e08828.
Marek, M., Vincenzetti, V., and Martin, S.G. (2020). Sterol biosensor reveals LAM-family Ltc1-dependent sterol flow to endosomes upon Arp2/3 inhibition. J Cell Biol 219, e202001147.
Markgraf, D.F., Klemm, R.W., Junker, M., Hannibal-Bach, H.K., Ejsing, C.S., and Rapoport, T.A. (2014). An ER protein functionally couples neutral lipid metabolism on lipid droplets to membrane lipid synthesis in the ER. Cell Rep 6, 44–55.
Masone, M.C., Morra, V., and Venditti, R. (2019). Illuminating the membrane contact sites between the endoplasmic reticulum and the trans-Golgi network. FEBS Lett 593, 3135–3148.
Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N.T., Izumi, T., Noda, T., and Yoshimori, T. (2010). Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol 190, 511–521.
Matsushita, M., Tanaka, S., Nakamura, N., Inoue, H., and Kanazawa, H. (2004). A novel kinesin-like protein, KIF1Bβ3 is involved in the movement of lysosomes to the cell periphery in non-neuronal cells. Traffic 5, 140–151.
Mattiazzi Ušaj, M., Brložnik, M., Kaferle, P., Žitnik, M., Wolinski, H., Leitner, F., Kohlwein, S.D., Zupan, B., and Petrovic, U. (2015). Genome-wide localization study of yeast Pex11 identifies peroxisome-mitochondria interactions through the ERMES complex. J Mol Biol 427, 2072–2087.
McCaughey, J., Miller, V.J., Stevenson, N.L., Brown, A.K., Budnik, A., Heesom, K.J., Alibhai, D., and Stephens, D.J. (2016). TFG promotes organization of transitional ER and efficient collagen secretion. Cell Rep 15, 1648–1659.
Medina, D.L., Di Paola, S., Peluso, I., Armani, A., De Stefani, D., Venditti, R., Montefusco, S., Scotto-Rosato, A., Prezioso, C., Forrester, A., et al. (2015). Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol 17, 288–299.
Mesmin, B., Bigay, J., Moser von Filseck, J., Lacas-Gervais, S., Drin, G., and Antonny, B. (2013). A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP. Cell 155, 830–843.
Mesmin, B., Bigay, J., Polidori, J., Jamecna, D., Lacas-Gervais, S., and Antonny, B. (2017). Sterol transfer, PI4P consumption, and control of membrane lipid order by endogenous OSBP. EMBO J 36, 3156–3174.
Mesmin, B., Pipalia, N.H., Lund, F.W., Ramlall, T.F., Sokolov, A., Eliezer, D., and Maxfield, F.R. (2011). STARD4 abundance regulates sterol transport and sensing. Mol Biol Cell 22, 4004–4015.
Mikoshiba, K. (1997). The InsP3 receptor and intracellular Ca2+ signaling. Curr Opin Neurobiol 7, 339–345.
Milligan, S.C., Alb, J.G. Jr., Elagina, R.B., Bankaitis, V.A., and Hyde, D.R. (1997). The phosphatidylinositol transfer protein domain of Drosophila retinal degeneration B protein is essential for photoreceptor cell survival and recovery from light stimulation. J Cell Biol 139, 351–363.
Min, S.W., Chang, W.P., and Südhof, T.C. (2007). E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains. Proc Natl Acad Sci USA 104, 3823–3828.
Mizushima, N. (2018). A brief history of autophagy from cell biology to physiology and disease. Nat Cell Biol 20, 521–527.
Mizushima, N., Yoshimori, T., and Ohsumi, Y. (2011). The role of atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27, 107–132.
Mochizuki, S., Miki, H., Zhou, R., Kido, Y., Nishimura, W., Kikuchi, M., and Noda, Y. (2018). Oxysterol-binding protein-related protein (ORP) 6 localizes to the ER and ER-plasma membrane contact sites and is involved in the turnover of PI4P in cerebellar granule neurons. Exp Cell Res 370, 601–612.
Morgan, A.J., Davis, L.C., Wagner, S.K.T.Y., Lewis, A.M., Parrington, J., Churchill, G. C., and Galione, A. (2013). Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J Cell Biol 200, 789–805.
Morgan, A.J., Platt, F.M., Lloyd-Evans, E., and Galione, A. (2011). Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease. Biochem J 439, 349–378.
Moriguchi, S., Nishi, M., Komazaki, S., Sakagami, H., Miyazaki, T., Masumiya, H., Saito, S., Watanabe, M., Kondo, H., Yawo, H., et al. (2006). Functional uncoupling between Ca2+ release and afterhyperpolarization in mutant hippocampal neurons lacking junctophilins. Proc Natl Acad Sci USA 103, 10811–10816.
Morishita, H., and Mizushima, N. (2019). Diverse cellular roles of autophagy. Annu Rev Cell Dev Biol 35, 453–475.
Moser von Filseck, J., Copie, A., Delfosse, V., Vanni, S., Jackson, C.L., Bourguet, W., and Drin, G. (2015a). Phosphatidylserine transport by ORP/Osh proteins is driven by phosphatidylinositol 4-phosphate. Science 349, 432–436.
Moser von Filseck, J, Vanni, S., Mesmin, B., Antonny, B., and Drin, G. (2015b). A phosphatidylinositol-4-phosphate powered exchange mechanism to create a lipid gradient between membranes. Nat Commun 6, 6671.
Munoz-Braceras, S., Tornero-Ecija, A.R., Vincent, O., and Escalante, R. (2019). VPS13A, a closely associated mitochondrial protein, is required for efficient lysosomal degradation. Dis Model Mech 12, dmm.036681.
Murley, A., Lackner, L.L., Osman, C., West, M., Voeltz, G.K., Walter, P., and Nunnari, J. (2013). ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. eLife 2, e00422.
Naito, T., Ercan, B., Krshnan, L., Triebl, A., Koh, D.H.Z., Wei, F.Y., Tomizawa, K., Torta, F.T., Wenk, M.R., and Saheki, Y. (2019). Movement of accessible plasma membrane cholesterol by the GRAMD1 lipid transfer protein complex. eLife 8, e51401.
Nakata, T., and Hirokawa, N. (1995). Point mutation of adenosine triphosphate-binding motif generated rigor kinesin that selectively blocks anterograde lysosome membrane transport. J Cell Biol 131, 1039–1053.
Nakatogawa, H. (2020). Mechanisms governing autophagosome biogenesis. Nat Rev Mol Cell Biol 21, 439–458.
Nakatsu, F., Baskin, J.M., Chung, J., Tanner, L.B., Shui, G., Lee, S.Y., Pirruccello, M., Hao, M., Ingolia, N.T., Wenk, M.R., et al. (2012). PtdIns4P synthesis by PI4KIIIα at the plasma membrane and its impact on plasma membrane identity. J Cell Biol 199, 1003–1016.
Nath, V.R., Mishra, S., Basak, B., Trivedi, D., and Raghu, P. (2020). Extended synaptotagmin regulates membrane contact site structure and lipid transfer function in vivo. EMBO Rep 21, e50264.
Ngo, M., and Ridgway, N.D. (2009). Oxysterol binding protein-related Protein 9 (ORP9) is a cholesterol transfer protein that regulates Golgi structure and function. Mol Biol Cell 20, 1388–1399.
Nemani, N., Dong, Z., Daw, C.C., Madaris, T.R., Ramachandran, K., Enslow, B.T., Rubannelsonkumar, C.S., Shanmughapriya, S., Mallireddigari, V., Maity, S., et al. (2020). Mitochondrial pyruvate and fatty acid flux modulate MICU1-dependent control of MCU activity. Sci Signal 13, eaaz6206.
Nishimura, T., Tamura, N., Kono, N., Shimanaka, Y., Arai, H., Yamamoto, H., and Mizushima, N. (2017). Autophagosome formation is initiated at phosphatidylinositol synthase-enriched ER subdomains. EMBO J 36, 1719–1735.
Olarte, M.J., Kim, S., Sharp, M.E., Swanson, J.M.J., Farese Jr., R.V., and Walther, T.C. (2020). Determinants of endoplasmic reticulum-to-lipid droplet protein targeting. Dev Cell 54, 471–487.e7.
Orci, L., Ravazzola, M., Le Coadic, M., Shen, W., Demaurex, N., and Cosson, P. (2009). STTM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc Natl Acad Sci USA 106, 19358–19362.
Orci, L., Stamnes, M., Ravazzola, M., Amherdt, M., Perrelet, A., Söllner, T.H., and Rothman, J.E. (1997). Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335–349.
Orrenius, S., Zhivotovsky, B., and Nicotera, P. (2003). Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4, 552–565.
Osawa, T., Ishii, Y., and Noda, N.N. (2020). Human ATG2B possesses a lipid transfer activity which is accelerated by negatively charged lipids and WIPI4. Genes Cells 25, 65–70.
Osawa, T., Kotani, T., Kawaoka, T., Hirata, E., Suzuki, K., Nakatogawa, H., Ohsumi, Y., and Noda, N.N. (2019). Atg2 mediates direct lipid transfer between membranes for autophagosome formation. Nat Struct Mol Biol 26, 281–288.
Özkan, N., Koppers, M., van Soest, I., van Harten, A., Jurriens, D., Liv, N., Klumperman, J., Kapitein, L.C., Hoogenraad, C.C., and Farías, G.G. (2021). ER-lysosome contacts at a pre-axonal region regulate axonal lysosome availability. Nat Commun 12, 4493.
Palade, G. (1975). Intracellular aspects of the process of protein synthesis. Science 189, 347–358.
Palande, K., Roovers, O., Gits, J., Verwijmeren, C., Iuchi, Y., Fujii, J., Neel, B.G., Karisch, R., Tavernier, J., and Touw, I.P. (2011). Peroxiredoxin-controlled G-CSF signalling at the endoplasmic reticulum-early endosome interface. J Cell Sci 124, 3695–3705.
Pallafacchina, G., Zanin, S., and Rizzuto, R. (2021). From the identification to the dissection of the physiological role of the mitochondrial calcium uniporter: an ongoing story. Biomolecules 11, 786.
Palty, R., Raveh, A., Kaminsky, I., Meller, R., and Reuveny, E. (2012). SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149, 425–438.
Pang, Q., Liu, C., Qiao, Y., Zhao, J., Lam, S.M., Mei, M., Shui, G., Bao, S., and Li, Q. (2022). GM130 regulates pulmonary surfactant protein secretion in alveolar type II cells. Sci China Life Sci 65, 193–205.
Pankiv, S., Alemu, E.A., Brech, A., Bruun, J.A., Lamark, T., Øvervatn, A., Bjørkøy, G., and Johansen, T. (2010). FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol 188, 253–269.
Parenti, G., Andria, G., and Ballabio, A. (2015). Lysosomal storage diseases: from pathophysiology to therapy. Annu Rev Med 66, 471–486.
Park, C.Y., Hoover, P.J., Mullins, F.M., Bachhawat, P., Covington, E.D., Raunser, S., Walz, T., Garcia, K.C., Dolmetsch, R.E., and Lewis, R.S. (2009). STTM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136, 876–890.
Park, J.S., and Neiman, A.M. (2012). VPS13 regulates membrane morphogenesis during sporulation in Sflcchflromyces cerevisifle. J Cell Sci 125, jcs.105114.
Park, J.S., Thorsness, M.K., Policastro, R., McGoldrick, L.L., Hollingsworth, N.M., Thorsness, P.E., and Neiman, A.M. (2016). Yeast Vps13 promotes mitochondrial function and is localized at membrane contact sites. Mol Biol Cell 27, 2435–2449.
Park, M.K., Petersen, O.H., and Tepikin, A.V. (2000). The endoplasmic reticulum as one continuous Ca2+ pool: visualization of rapid Ca2+ movements and equilibration. EMBO J 19, 5729–5739.
Pedersen, N.M., Wenzel, E.M., Wang, L., Antoine, S., Chavrier, P., Stenmark, H., and Raiborg, C. (2020). Protrudin-mediated ER-endosome contact sites promote MT1MMP exocytosis and cell invasion. J Cell Biol 219, e202003063.
Penner, R., Matthews, G., and Neher, E. (1988). Regulation of calcium influx by second messengers in rat mast cells. Nature 334, 499–504.
Peotter, J., Kasberg, W., Pustova, I., and Audhya, A. (2019). COPII-mediated trafficking at the ER/ERGIC interface. Traffic 20, 491–503.
Perera, R.M., and Zoncu, R. (2016). The lysosome as a regulatory hub. Annu Rev Cell Dev Biol 32, 223–253.
Petkovic, M., Jemaiel, A., Daste, F., Specht, C.G., Izeddin, I., Vorkel, D., Verbavatz, J.M., Darzacq, X., Triller, A., Pfenninger, K.H., et al. (2014). The SNARE Sec22b has a non-fusogenic function in plasma membrane expansion. Nat Cell Biol 16, 434–444.
Picard, C., McCarl, C.A., Papolos, A., Khalil, S., Lüthy, K., Hivroz, C., LeDeist, F., Rieux-Laucat, F., Rechavi, G., Rao, A., et al. (2009). STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N Engl J Med 360, 1971–1980.
Pietrangelo, A., and Ridgway, N.D. (2018). Golgi-localization of oxysterol binding protein-related protein 4L (ORP4L) is regulated by ligand binding. J Cell Sci 131, jcs.215335.
Porter, K.R., and Palade, G.E. (1957). Studies on the endoplasmic reticulum. J Cell Biol 3, 269–300.
Pottekat, A., Becker, S., Spencer, K.R., Yates, J.R. III, Manning, G., Itkin-Ansari, P., and Balch, W.E. (2013). Insulin biosynthetic interaction network component, TMEM24, facilitates insulin reserve pool release. Cell Rep 4, 921–930.
Prinz, W.A., Toulmay, A., and Balla, T. (2020). The functional universe of membrane contact sites. Nat Rev Mol Cell Biol 21, 7–24.
Protasi, F. (2002). Structural interaction between RYRs and DHPRs in calcium release units of cardiac and skeletal muscle cells. Front Biosci 7, d650-658.
Pu, J., Guardia, C.M., Keren-Kaplan, T., and Bonifacino, J.S. (2016). Mechanisms and functions of lysosome positioning. J Cell Sci 129, jcs.196287.
Putney, J.W. Jr. (1986). A model for receptor-regulated calcium entry. Cell Calcium 7, 1–12.
Putney, J.W Jr. (1990). Capacitative calcium entry revisited. Cell Calcium 11, 611–624.
Qi, H., Li, L., and Shuai, J. (2015). Optimal microdomain crosstalk between endoplasmic reticulum and mitochondria for Ca2+ oscillations. Sci Rep 5, 7984.
Qian, K., Tol, M.J., Wu, J., Uchiyama, L.F., Xiao, X., Cui, L., Bedard, A.H., Weston, T. A., Rajendran, P.S., Vergnes, L., et al. (2023). CLSTN3β enforces adipocyte multilocularity to facilitate lipid utilization. Nature 613, 160–168.
Qian, T., Li, C., He, R., Wan, C., Liu, Y., and Yu, H. (2021). Calcium-dependent and -independent lipid transfer mediated by tricalbins in yeast. J Biol Chem 296, 100729.
Quintana, A., Rajanikanth, V., Farber-Katz, S., Gudlur, A., Zhang, C., Jing, J., Zhou, Y., Rao, A., and Hogan, P.G. (2015). TMEM110 regulates the maintenance and remodeling of mammalian ER-plasma membrane junctions competent for STIMORAI signaling. Proc Natl Acad Sci USA 112, E7083–7092.
Quintanilla, C.G., Lee, W.R., and Liou, J. (2022). Nir1 constitutively localizes at ERPM junctions and promotes Nir2 recruitment for PIP2 homeostasis. Mol Biol Cell 33, br2.
Quon, E., Sere, Y.Y., Chauhan, N., Johansen, J., Sullivan, D.P., Dittman, J.S., Rice, W. J., Chan, R.B., Di Paolo, G., Beh, C.T., et al. (2018). Endoplasmic reticulum-plasma membrane contact sites integrate sterol and phospholipid regulation. PLoS Biol 16, e2003864.
Radulovic, M., Schink, K.O., Wenzel, E.M., Nähse, V., Bongiovanni, A., Lafont, F., and Stenmark, H. (2018). ESCRT-mediated lysosome repair precedes lysophagy and promotes cell survival. EMBO J 37, e99753.
Raiborg, C., Wenzel, E.M., Pedersen, N.M., Olsvik, H., Schink, K.O., Schultz, S.W., Vietri, M., Nisi, V., Bucci, C., Brech, A., et al. (2015). Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth. Nature 520, 234–238.
Rampoldi, L., Dobson-Stone, C., Rubio, J.P., Danek, A., Chalmers, R.M., Wood, N.W., Verellen, C., Ferrer, X., Malandrini, A., Fabrizi, G.M., et al. (2001). A conserved sorting-associated protein is mutant in chorea-acanthocytosis. Nat Genet 28, 119–120.
Raote, I., and Malhotra, V. (2021). Tunnels for protein export from the endoplasmic reticulum. Annu Rev Biochem 90, 605–630.
Raychaudhuri, S., Im, Y.J., Hurley, J.H., and Prinz, W.A. (2006). Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides. J Cell Biol 173, 107–119.
Reinisch, K.M., and De Camilli, P. (2016). SMP-domain proteins at membrane contact sites: structure and function. Biochim Biophys Acta-Mol Cell Biol Lipids 1861, 924–927.
Riegelhaupt, J.J., Waase, M.P., Garbarino, J., Cruz, D.E., and Breslow, J.L. (2010). Targeted disruption of steroidogenic acute regulatory protein D4 leads to modest weight reduction and minor alterations in lipid metabolism. J Lipid Res 51, 1134–1143.
Rizzuto, R., Brini, M., Murgia, M., and Pozzan, T. (1993). Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262, 744–747.
Rocha, N., Kuijl, C., van der Kant, R., Janssen, L., Houben, D., Janssen, H., Zwart, W., and Neefjes, J. (2009). Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150Glued and late endosome positioning. J Cell Biol 185, 1209–1225.
Rodriguez-Agudo, D., Calderon-Dominguez, M., Ren, S., Marques, D., Redford, K., Medina-Torres, M.A., Hylemon, P., Gil, G., and Pandak, W.M. (2011). Subcellular localization and regulation of StarD4 protein in macrophages and fibroblasts. Biochim Biophys Acta 1811, 597–606.
Rodriguez-Agudo, D., Malacrida, L., Kakiyama, G., Sparrer, T., Fortes, C., Maceyka, M., Subler, M.A., Windle, J.J., Gratton, E., Pandak, W.M., et al. (2019). StarD5: an ER stress protein regulates plasma membrane and intracellular cholesterol homeostasis. J Lipid Res 60, 1087–1098.
Roos, J., DiGregorio, P.J., Yeromin, A.V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J.A., Wagner, S.L., Cahalan, M.D., et al. (2005). STM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169, 435–445.
Rosenbluth, J. (1962). Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol 13, 405–421.
Rowland, A.A., Chitwood, P.J., Phillips, M.J., and Voeltz, G.K. (2014). ER contact sites define the position and timing of endosome fission. Cell 159, 1027–1041.
Ruas, M., Rietdorf, K., Arredouani, A., Davis, L.C., Lloyd-Evans, E., Koegel, H., Funnell, T.M., Morgan, A.J., Ward, J.A., Watanabe, K., et al. (2010). Purified TPC isoforms form NAADP receptors with distinct roles for Ca2+ signaling and endolysosomal trafficking. Curr Biol 20, 703–709.
Sabatini, D.D. (1999). George E. Palade: charting the secretory pathway. Trends Cell Biol 9, 413–417.
Saheki, Y., Bian, X., Schauder, C.M., Sawaki, Y., Surma, M.A., Klose, C., Pincet, F., Reinisch, K.M., and De Camilli, P. (2016). Control of plasma membrane lipid homeostasis by the extended synaptotagmins. Nat Cell Biol 18, 504–515.
Saito, K., Chen, M., Bard, F., Chen, S., Zhou, H., Woodley, D., Polischuk, R., Schekman, R., and Malhotra, V. (2009). TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136, 891–902.
Salo, V.T., Belevich, I., Li, S., Karhinen, L., Vihinen, H., Vigouroux, C., Magré, J., Thiele, C., Hölttä-Vuori, M., Jokitalo, E., et al. (2016). Seipin regulates ER-lipid droplet contacts and cargo delivery. EMBO J 35, 2699–2716.
Salo, V.T., Li, S., Vihinen, H., Hölttä-Vuori, M., Szkalisity, A., Horvath, P., Belevich, I., Peränen, J., Thiele, C., Somerharju, P., et al. (2019). Seipin facilitates triglyceride flow to lipid droplet and counteracts droplet ripening via endoplasmic reticulum contact. Dev Cell 50, 478–493.e9.
Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A.L., Nada, S., and Sabatini, D.M. (2010). Ragulator-rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290–303.
Sandhu, J., Li, S., Fairall, L., Pfisterer, S.G., Gurnett, J.E., Xiao, X., Weston, T.A., Vashi, D., Ferrari, A., Orozco, J.L., et al. (2018). Aster proteins facilitate nonvesicular plasma membrane to ER cholesterol transport in mammalian cells. Cell 175, 514–529.e20.
Santos, A.J., Raote, I., Scarpa, M., Brouwers, N., and Malhotra, V. (2015). TANGO1 recruits ERGIC membranes to the endoplasmic reticulum for procollagen export. eLife 4, e10982.
Saraste, J., and Marie, M. (2018). Intermediate compartment (IC): from pre-Golgi vacuoles to a semi-autonomous membrane system. Histochem Cell Biol 150, 407–430.
Schauder, C.M., Wu, X., Saheki, Y., Narayanaswamy, P., Torta, F., Wenk, M.R., de Camilli, P., and Reinisch, K.M. (2014). Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510, 552–555.
Schneider, M.F., and Chandler, W.K. (1973). Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242, 244–246.
Schulz, T.A., Choi, M.G., Raychaudhuri, S., Mears, J.A., Ghirlando, R., Hinshaw, J.E., and Prinz, W.A. (2009). Lipid-regulated sterol transfer between closely apposed membranes by oxysterol-binding protein homologues. J Cell Biol 187, 889–903.
Schutter, M., Giavalisco, P., Brodesser, S., and Graef, M. (2020). Local fatty acid channeling into phospholipid synthesis drives phagophore expansion during autophagy. Cell 180, 135–149.e14.
Sclip, A., Bacaj, T., Giam, L.R., and Sudhof, T.C. (2016). Extended synaptotagmin (ESyt) triple knock-out mice are viable and fertile without obvious endoplasmic reticulum dysfunction. PLoS ONE 11, e0158295.
Scorrano, L., De Matteis, M.A., Emr, S., Giordano, F., Hajnóczky, G., Kornmann, B., Lackner, L.L., Levine, T.P., Pellegrini, L., Reinisch, K., et al. (2019). Coming together to define membrane contact sites. Nat Commun 10, 1287.
Shai, N., Yifrach, E., van Roermund, C.W.T., Cohen, N., Bibi, C., IJlst, L., Cavellini, L., Meurisse, J., Schuster, R., Zada, L., et al. (2018). Systematic mapping of contact sites reveals tethers and a function for the peroxisome-mitochondria contact. Nat Commun 9, 1761.
Sharma, S., Quintana, A., Findlay, G.M., Mettlen, M., Baust, B., Jain, M., Nilsson, R., Rao, A., and Hogan, P.G. (2013). An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry. Nature 499, 238–242.
Shinoda, Y., Fujita, K., Saito, S., Matsui, H., Kanto, Y., Nagaura, Y., Fukunaga, K., Tamura, S., and Kobayashi, T. (2012). Acyl-CoA binding domain containing 3 (ACBD3) recruits the protein phosphatase PPM1L to ER-Golgi membrane contact sites. FEBS Lett 586, 3024–3029.
Shirane, M., Wada, M., Morita, K., Hayashi, N., Kunimatsu, R., Matsumoto, Y., Matsuzaki, F., Nakatsumi, H., Ohta, K., Tamura, Y., et al. (2020). Protrudin and PDZD8 contribute to neuronal integrity by promoting lipid extraction required for endosome maturation. Nat Commun 11, 4576.
Shomron, O., Nevo-Yassaf, I., Aviad, T., Yaffe, Y., Zahavi, E.E., Dukhovny, A., Perlson, E., Brodsky, I., YeheskelA.Pasmanik-Chor, M., Mironov, A., et al. (2021). COPII collar defines the boundary between ER and ER exit site and does not coat cargo containers. J Cell Biol 220, e201907224.
Simoes, I.C.M., Morciano, G., Lebiedzinska-Arciszewska, M., Aguiari, G., Pinton, P., Potes, Y., and Wieckowski, M.R. (2020). The mystery of mitochondria-ER contact sites in physiology and pathology: a cancer perspective. Biochim Biophys Acta Mol Basis Dis 1866, 165834.
Skowyra, M.L., Schlesinger, P.H., Naismith, T.V., and Hanson, P.I. (2018). Triggered recruitment of ESCRT machinery promotes endolysosomal repair. Science 360, eaar5078.
Smirnova, E., Shurland, D.L., Ryazantsev, S.N., and van der Bliek, A.M. (1998). A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 143, 351–358.
Sohn, M., Korzeniowski, M., Zewe, J.P., Wills, R.C., Hammond, G.R.V., Humpolickova, J., Vrzal, L., Chalupska, D., Veverka, V., Fairn, G.D., et al. (2018). PI(4,5)P2 controls plasma membrane PI4P and PS levels via ORP5/8 recruitment to ER-PM contact sites. J Cell Biol 217, 1797–1813.
Song, J., Mizrak, A., Lee, C.W., Cicconet, M., Lai, Z.W., Tang, W.C., Lu, C.H., Mohr, S. E., Farese Jr., R.V., and Walther, T.C. (2022). Identification of two pathways mediating protein targeting from ER to lipid droplets. Nat Cell Biol 24, 1364–1377.
Sonnichsen, B., De Renzis, S., Nielsen, E., Rietdorf, J., and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149, 901–914.
Spits, M., Heesterbeek, I.T., Voortman, L.M., Akkermans, J.J., Wijdeven, R.H., Cabukusta, B., and Neefjes, J. (2021). Mobile late endosomes modulate peripheral endoplasmic reticulum network architecture. EMBO Rep 22, e50815.
Srikanth, S., Jew, M., Kim, K.D., Yee, M.K., Abramson, J., and Gwack, Y. (2012). Junctate is a Ca2+-sensing structural component of Orai1 and stromal interaction molecule 1 (STIM1). Proc Natl Acad Sci USA 109, 8682–8687.
Srikanth, S., Jung, H.J., Kim, K.D., Souda, P., Whitelegge, J., and Gwack, Y. (2010). A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nat Cell Biol 12, 436–446.
Stathopulos, P.B., Zheng, L., and Ikura, M. (2009). Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J Biol Chem 284, 728–732.
Stathopulos, P.B., Zheng, L., Li, G.Y., Plevin, M.J., and Ikura, M. (2008). Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135, 110–122.
Stefan, C.J., Manford, A.G., Baird, D., Yamada-Hanff, J., Mao, Y., and Emr, S.D. (2011). Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144, 389–401.
Stocco, D.M. (2001). StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 63, 193–213.
Stoica, R., De Vos, K.J., Paillusson, S., Mueller, S., Sancho, R.M., Lau, K.F., Vizcay-Barrena, G., Lin, W.L., Xu, Y.F., Lewis, J., et al. (2014). ER-mitochondria associations are regulated by the VAPB-PTPIP51 interaction and are disrupted by ALS/FTD-associated TDP-43. Nat Commun 5, 3996.
Stuible, M., Abella, J.V., Feldhammer, M., Nossov, M., Sangwan, V., Blagoev, B., Park, M., and Tremblay, M.L. (2010). PTP1B targets the endosomal sorting machinery. J Biol Chem 285, 23899–23907.
Sui, X., Arlt, H., Brock, K.P., Lai, Z.W., DiMaio, F., Marks, D.S., Liao, M., Farese, R.V. Jr., and Walther, T.C. (2018). Cryo-electron microscopy structure of the lipid droplet-formation protein seipin. J Cell Biol 217, 4080–4091.
Sun, E.W., Guillén-Samander, A., Bian, X., Wu, Y., Cai, Y., Messa, M., and De Camilli, P. (2019). Lipid transporter TMEM24/C2CD2L is a Ca2+-regulated component of ER-plasma membrane contacts in mammalian neurons. Proc Natl Acad Sci USA 116, 5775 -5784.
Sun, S., Tang, X., Guo, Y., and Hu, J. (2021). Endoplasmic reticulum composition and form: Proteins in and out. Curr Opin Cell Biol 71, 1–6.
Suzuki, K., Akioka, M., Kondo-Kakuta, C., Yamamoto, H., and Ohsumi, Y. (2013). Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J Cell Sci 126, jcs.122960.
Szabadkai, G., Bianchi, K., Várnai, P., De Stefani, D., Wieckowski, M.R., Cavagna, D., Nagy, A.I., Balla, T., and Rizzuto, R. (2006). Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol 175, 901–911.
Szymanski, K.M., Binns, D., Bartz, R., Grishin, N.V., Li, W.P., Agarwal, A.K., Garg, A., Anderson, R.G.W., and Goodman, J.M. (2007). The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology. Proc Natl Acad Sci USA 104, 20890–20895.
Takeshima, H., Komazaki, S., Nishi, M., Iino, M., and Kangawa, K. (2000). Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6, 11–22.
Tan, J.X., and Finkel, T. (2022). A phosphoinositide signalling pathway mediates rapid lysosomal repair. Nature 609, 815–821.
Terasaki, M., Chen, L.B., and Fujiwara, K. (1986). Microtubules and the endoplasmic reticulum are highly interdependent structures. J Cell Biol 103, 1557–1568.
Thyme, S.B., Pieper, L.M., Li, E.H., Pandey, S., Wang, Y., Morris, N.S., Sha, C., Choi, J. W., Herrera, K.J., Soucy, E.R., et al. (2019). Phenotypic landscape of schizophrenia-associated genes defines candidates and their shared functions. Cell 177, 478–491.e20.
Tian, S., Ohta, A., Horiuchi, H., and Fukuda, R. (2018). Oxysterol-binding protein homologs mediate sterol transport from the endoplasmic reticulum to mitochondria in yeast. J Biol Chem 293, 5636–5648.
Tian, Y., Li, Z., Hu, W., Ren, H., Tian, E., Zhao, Y., Lu, Q., Huang, X., Yang, P., Li, X., et al. (2010). C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell 141, 1042–1055.
Tikhomirova, M.S., Kadosh, A., Saukko-Paavola, A.J., Shemesh, T., and Klemm, R.W. (2022). A role for endoplasmic reticulum dynamics in the cellular distribution of microtubules. Proc Natl Acad Sci USA 119, e2104309119.
Tong, J., Manik, M.K., and Im, Y.J. (2018). Structural basis of sterol recognition and nonvesicular transport by lipid transfer proteins anchored at membrane contact sites. Proc Natl Acad Sci USA 115, E856–E865.
Toulmay, A., and Prinz, W.A. (2012). A conserved membrane-binding domain targets proteins to organelle contact sites. J Cell Sci 125, 49–58.
Tremblay, M.G., and Moss, T. (2016). Loss of all 3 extended synaptotagmins does not affect normal mouse development, viability or fertility. Cell Cycle 15, 2360–2366.
Trinh, M.N., Brown, M.S., Goldstein, J.L., Han, J., Vale, G., McDonald, J.G., Seemann, J., Mendell, J.T., and Lu, F. (2020). Last step in the path of LDL cholesterol from lysosome to plasma membrane to ER is governed by phosphatidylserine. Proc Natl Acad Sci USA 117, 18521–18529.
Uemura, T., Yamamoto, M., Kametaka, A., Sou, Y., Yabashi, A., Yamada, A., Annoh, H., Kametaka, S., Komatsu, M., and Waguri, S. (2014). A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol Cell Biol 34, 1695–1706.
Ueno, S., Maruki, Y., Nakamura, M., Tomemori, Y., Kamae, K., Tanabe, H., Yamashita, Y., Matsuda, S., Kaneko, S., and Sano, A. (2001). The gene encoding a newly discovered protein, chorein, is mutated in chorea-acanthocytosis. Nat Genet 28, 121–122.
Ugur, B., Hancock-Cerutti, W., Leonzino, M., and De Camilli, P. (2020). Role of VPS13, a protein with similarity to ATG2, in physiology and disease. Curr Opin Genet Dev 65, 61–68.
Ungricht, R., and Kutay, U. (2017). Mechanisms and functions of nuclear envelope remodelling. Nat Rev Mol Cell Biol 18, 229–245.
Valm, A.M., Cohen, S., Legant, W.R., Melunis, J., Hershberg, U., Wait, E., Cohen, A.R., Davidson, M.W., Betzig, E., and Lippincott-Schwartz, J. (2017). Applying systems-level spectral imaging and analysis to reveal the organelle interactome. Nature 546, 162–167.
Valverde, D.P., Yu, S., Boggavarapu, V., Kumar, N., Lees, J.A., Walz, T., Reinisch, K. M., and Melia, T.J. (2019). ATG2 transports lipids to promote autophagosome biogenesis. J Cell Biol 218, 1787–1798.
Van Petegem, F. (2012). Ryanodine receptors: structure and function. J Biol Chem 287, 31624–31632.
Venditti, R., Masone, M.C., and De Matteis, M.A. (2020). ER-Golgi membrane contact sites. Biochem Soc Trans 48, 187–197.
Venditti, R., Masone, M.C., Rega, L.R., Di Tullio, G., Santoro, M., Polishchuk, E., Serrano, I.C., Olkkonen, V.M., Harada, A., Medina, D.L., et al. (2019a). The activity of Sac1 across ER-TGN contact sites requires the four-phosphate-adaptor-protein-1. J Cell Biol 218, 783–797.
Venditti, R., Rega, L.R., Masone, M.C., Santoro, M., Polishchuk, E., Sarnataro, D., Paladino, S., D’Auria, S., Varriale, A., Olkkonen, V.M., et al. (2019b). Molecular determinants of ER-Golgi contacts identified through a new FRET-FLIM system. J Cell Biol 218, 1055–1065.
Vietri, M., Radulovic, M., and Stenmark, H. (2020). The many functions of ESCRTs. Nat Rev Mol Cell Biol 21, 25–42.
Vig, M., Peinelt, C., Beck, A., Koomoa, D.L., Rabah, D., Koblan-Huberson, M., Kraft, S., Turner, H., Fleig, A., Penner, R., et al. (2006). CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312, 1220–1223.
Vihervaara, T., Uronen, R.L., Wohlfahrt, G., Björkhem, I., Ikonen, E., and Olkkonen, V.M. (2011). Sterol binding by OSBP-related protein 1L regulates late endosome motility and function. Cell Mol Life Sci 68, 537–551.
Voeltz, G.K., Prinz, W.A., Shibata, Y., Rist, J.M., and Rapoport, T.A. (2006). A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573–586.
Wanders, R.J.A., Waterham, H.R., and Ferdinandusse, S. (2016). Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum. Front Cell Dev Biol 3, 83.
Wang, F., Gómez-Sintes, R., and Boya, P. (2018). Lysosomal membrane permeabilization and cell death. Traffic 19, 918–931.
Wang, H., Becuwe, M., Housden, B.E., Chitraju, C., Porras, A.J., Graham, M.M., Liu, X. N., Thiam, A.R., SavageD.B.Agarwal, A.K., et al. (2016). Seipin is required for converting nascent to mature lipid droplets. eLife 5, e16582.
Wang, H., Ma, Q., Qi, Y., Dong, J., Du, X., Rae, J., Wang, J., Wu, W.F., Brown, A.J., Parton, R.G., et al. (2019). ORP2 Delivers Cholesterol to the Plasma Membrane in Exchange for Phosphatidylinositol 4, 5-Bisphosphate (PI(4,5)P2). Mol Cell 73, 458–473.e7.
Wang, X., Zhang, X., Dong, X., Samie, M., Li, X., Cheng, X., Goschka, A., Shen, D., Zhou, Y., Harlow, J., et al. (2012). TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372–383.
Wang, Y., Li, Z., Wang, X., Zhao, Z., Jiao, L., Liu, R., Wang, K., Ma, R., Yang, Y., Chen, G., et al. (2023). Insights into membrane association of the SMP domain of extended synaptotagmin. Nat Commun 14, 1504.
Waterman-Storer, C.M., and Salmon, E.D. (1998). Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol 8, 798–807.
Weigel, A.V., Chang, C.L., Shtengel, G., Xu, C.S., Hoffman, D.P., Freeman, M., Iyer, N., Aaron, J., Khuon, S., Bogovic, J., et al. (2021). ER-to-Golgi protein delivery through an interwoven, tubular network extending from ER. Cell 184, 2412–2429.e16.
Wenzel, E.M., Elfmark, L.A., Stenmark, H., and Raiborg, C. (2022). ER as master regulator of membrane trafficking and organelle function. J Cell Biol 221, e202205135.
West, M., Zurek, N., Hoenger, A., and Voeltz, G.K. (2011). A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J Cell Biol 193, 333–346.
Westrate, L.M., Hoyer, M.J., Nash, M.J., and Voeltz, G.K. (2020). Vesicular and uncoated Rab1-dependent cargo carriers facilitate ER to Golgi transport. J Cell Sci 133, jcs239814.
Westrate, L.M., Lee, J.E., Prinz, W.A., and Voeltz, G.K. (2015). Form follows function: the importance of endoplasmic reticulum shape. Annu Rev Biochem 84, 791–811.
Wilfling, F., Thiam, A.R., Olarte, M.J., Wang, J., Beck, R., Gould, T.J., Allgeyer, E.S., Pincet, F., Bewersdorf, J., Farese, R.V., et al. (2014). Arf1/COPI machinery acts directly on lipid droplets and enables their connection to the ER for protein targeting. eLife 3, e01607.
Wilhelm, L.P., Wendling, C., Vedie, B., Kobayashi, T., Chenard, M.P., Tomasetto, C., Drin, G., and Alpy, F. (2017). STARD3 mediates endoplasmic reticulum-to-endosome cholesterol transport at membrane contact sites. EMBO J 36, 1412–1433.
Witte, K., Schuh, A.L., Hegermann, J., Sarkeshik, A., Mayers, J.R., Schwarze, K., Yates III, J.R., Eimer, S., and Audhya, A. (2011). TFG-1 function in protein secretion and oncogenesis. Nat Cell Biol 13, 550–558.
Wong, L.H., Gatta, A.T., and Levine, T.P. (2019). Lipid transfer proteins: the lipid commute via shuttles, bridges and tubes. Nat Rev Mol Cell Biol 20, 85–101.
Wong, L.H., and Levine, T.P. (2017). Tubular lipid binding proteins (TULIPs) growing everywhere. Biochim Biophys Acta 1864, 1439–1449.
Woo, J.S., Srikanth, S., Nishi, M., Ping, P., Takeshima, H., and Gwack, Y. (2016). Junctophilin-4, a component of the endoplasmic reticulum-plasma membrane junctions, regulates Ca2+ dynamics in T cells. Proc Natl Acad Sci USA 113, 2762–2767.
Wu, H., Carvalho, P., and Voeltz, G.K. (2018). Here, there, and everywhere: the importance of ER membrane contact sites. Science 361, eaan5835.
Wu, H., and Voeltz, G.K. (2021). Reticulon-3 promotes endosome maturation at ER membrane contact sites. Dev Cell 56, 52–66.e7.
Xiao, J., Luo, J., Hu, A., Xiao, T., Li, M., Kong, Z., Jiang, L., Zhou, Z., Liao, Y., Xie, C., et al. (2019). Cholesterol transport through the peroxisome-ER membrane contacts tethered by PI(4,5)P2 and extended synaptotagmins. Sci China Life Sci 62, 1117–1135.
Xiao, X., Kim, Y., Romartinez-Alonso, B., Sirvydis, K., OryD.S.Schwabe, J.W.R., Jung, M.E., and Tontonoz, P. (2021). Selective aster inhibitors distinguish vesicular and nonvesicular sterol transport mechanisms. Proc Natl Acad Sci USA 118, e2024149118.
Xie, B., Nguyen, P.M., and Idevall-Hagren, O. (2019). Feedback regulation of insulin secretion by extended synaptotagmin-1. FASEB J 33, 4716–4728.
Xie, B., Nguyen, P.M., and Idevall-Hagren, O. (2022). The endoplasmic reticulum-plasma membrane tethering protein TMEM24 is a regulator of cellular Ca2+ homeostasis. J Cell Sci 135, jcs259073.
Xu, D., Li, Y., Wu, L., Li, Y., Zhao, D., Yu, J., Huang, T., Ferguson, C., Parton, R.G., Yang, H., et al. (2018). Rab18 promotes lipid droplet (LD) growth by tethering the ER to LDs through SNARE and NRZ interactions. J Cell Biol 217, 975–995.
Xu, H., and Ren, D. (2015). Lysosomal physiology. Annu Rev Physiol 77, 57–80.
Xu, L., Wang, X., and Tong, C. (2020). Endoplasmic reticulum-mitochondria contact sites and neurodegeneration. Front Cell Dev Biol 8, 428.
Xu, N., Zhang, S.O., Cole, R.A., McKinney, S.A., Guo, F., Haas, J.T., Bobba, S., Farese, R.V. Jr., and Mak, H.Y. (2012). The FATP1-DGAT2 complex facilitates lipid droplet expansion at the ER-lipid droplet interface. J Cell Biol 198, 895–911.
Yadav, S., Cockcroft, S., and Raghu, P. (2016). The Drosophila photoreceptor as a model system for studying signalling at membrane contact sites. Biochem Soc Trans 44, 447–451.
Yan, R., Qian, H., Lukmantara, I., Gao, M., Du, X., Yan, N., and Yang, H. (2018). Human seipin binds anionic phospholipids. Dev Cell 47, 248–256.e4.
Yang, K., Liu, M., Feng, Z., Rojas, M., Zhou, L., Ke, H., and Pastor-Pareja, J.C. (2021). ER exit sites in Drosophila display abundant ER-Golgi vesicles and pearled tubes but no megacarriers. Cell Rep 36, 109707.
Yao, Y., Xu, M., Qiao, L., Nie, H., Lu, F., and Huang, X. (2022). BAP60 plays an opposite role to the MRT-NURF complex in regulating lipid droplet size. J Genet Genomics 49, 377–379.
Yeshaw, W.M., van der Zwaag, M., Pinto, F., Lahaye, L.L., Faber, A.I., Gómez-Sánchez, R., Dolga, A.M., Poland, C., Monaco, A.P., van IJzendoorn, S.C., et al. (2019). Human VPS13A is associated with multiple organelles and influences mitochondrial morphology and lipid droplet motility. eLife 8, e43561.
Yla-Anttila, P., Vihinen, H., Jokitalo, E., and Eskelinen, E.L. (2009). 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180–1185.
Yoboue, E.D., Sitia, R., and Simmen, T. (2018). Redox crosstalk at endoplasmic reticulum (ER) membrane contact sites (MCS) uses toxic waste to deliver messages. Cell Death Dis 9, 331.
Yu, H., Liu, Y., Gulbranson, D.R., Paine, A., Rathore, S.S., and Shen, J. (2016). Extended synaptotagmins are Ca2+-dependent lipid transfer proteins at membrane contact sites. Proc Natl Acad Sci USA 113, 4362–4367.
Yuan, J.P., Zeng, W., Dorwart, M.R., Choi, Y.J., Worley, P.F., and Muallem, S. (2009). SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11, 337–343.
Zacharogianni, M., Aguilera-Gomez, A., Veenendaal, T., Smout, J., and Rabouille, C. (2014). A stress assembly that confers cell viability by preserving ERES components during amino-acid starvation. eLife 3, e04132.
Zanetti, G., Pahuja, K.B., Studer, S., Shim, S., and Schekman, R. (2011). COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14, 20–28.
Zervopoulos, S.D., Boukouris, A.E., Saleme, B., Haromy, A., Tejay, S., Sutendra, G., and Michelakis, E.D. (2022). MFN2-driven mitochondria-to-nucleus tethering allows a non-canonical nuclear entry pathway of the mitochondrial pyruvate dehydrogenase complex. Mol Cell 82, 1066–1077.e7.
Zeuschner, D., Geerts, W.J.C., van Donselaar, E., Humbel, B.M., Slot, J.W., Koster, A.J., and Klumperman, J. (2006). Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nat Cell Biol 8, 377–383.
Zhang, D., Bidone, T.C., and Vavylonis, D. (2016). ER-PM contacts define actomyosin kinetics for proper contractile ring assembly. Curr Biol 26, 647–653.
Zhang, D., Vjestica, A., and Oliferenko, S. (2010). The cortical ER network limits the permissive zone for actomyosin ring assembly. Curr Biol 20, 1029–1034.
Zhang, D., Vjestica, A., and Oliferenko, S. (2012). Plasma membrane tethering of the cortical er necessitates its finely reticulated architecture. Curr Biol 22, 2048–2052.
Zhang, H., and Hu, J. (2016). Shaping the endoplasmic reticulum into a social network. Trends Cell Biol 26, 934–943.
Zhang, S.L., Yeromin, A.V., Zhang, X.H.F., Yu, Y., Safrina, O., Penna, A., Roos, J., Stauderman, K.A., and Cahalan, M.D. (2006). Genome-wide RNAi screen of Ca2+ influx identifies genes that regulate Ca2+ release-activated Ca2+ channel activity. Proc Natl Acad Sci USA 103, 9357–9362.
Zhang, S.L., Yu, Y., Roos, J., Kozak, J.A., Deerinck, T.J., Ellisman, M.H., Stauderman, K.A., and Cahalan, M.D. (2005). STM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437, 902–905.
Zhang, X., Gibhardt, C.S., Will, T., Stanisz, H., Körbel, C., Mitkovski, M., Stejerean, I., Cappello, S., Pacheu-Grau, D., Dudek, J., et al. (2019). Redox signals at the ER-mitochondria interface control melanoma progression. EMBO J 38, e100871.
Zhang, Y., Guan, Y., Pan, S., Yan, L., Wang, P., Chen, Z., Shen, Q., Zhao, F., Zhang, X., Li, J., et al. (2020a). Hypothalamic extended synaptotagmin-3 contributes to the development of dietary obesity and related metabolic disorders. Proc Natl Acad Sci USA 117, 20149–20158.
Zhang, Y., Schroeder, L.K., Lessard, M.D., Kidd, P., Chung, J., Song, Y., Benedetti, L., Li, Y., Ries, J., Grimm, J.B., et al. (2020b). Nanoscale subcellular architecture revealed by multicolor three-dimensional salvaged fluorescence imaging. Nat Methods 17, 225–231.
Zhao, H., Li, T., Wang, K., Zhao, F., Chen, J., Xu, G., Zhao, J., Li, T., Chen, L., Li, L., et al. (2019). AMPK-mediated activation of MCU stimulates mitochondrial Ca2+ entry to promote mitotic progression. Nat Cell Biol 21, 476–486.
Zhao, K., Foster, J., and Ridgway, N.D. (2020). Oxysterol-binding protein-related protein 1 variants have opposing cholesterol transport activities from the endolysosomes. Mol Biol Cell 31, 793–802.
Zhao, K., and Ridgway, N.D. (2017). Oxysterol-binding protein-related protein 1L regulates cholesterol egress from the endo-lysosomal system. Cell Rep 19, 1807–1818.
Zhao, Y.G., Chen, Y., Miao, G., Zhao, H., Qu, W., Li, D., Wang, Z., Liu, N., Li, L., Chen, S., et al. (2017). The ER-localized transmembrane protein EPG-3/VMP1 regulates SERCA activity to control ER-isolation membrane contacts for autophagosome formation. Mol Cell 67, 974–989.e6.
Zhao, Y.G., Liu, N., Miao, G., Chen, Y., Zhao, H., and Zhang, H. (2018). The ER contact proteins VAPA/B interact with multiple autophagy proteins to modulate autophagosome biogenesis. Curr Biol 28, 1234–1245.e4.
Zhao, Y.G., and Zhang, H. (2019). Core autophagy genes and human diseases. Curr Opin Cell Biol 61, 117–125.
Zheng, P., Obara, C.J., Szczesna, E., Nixon-Abell, J., Mahalingan, K.K., Roll-Mecak, A., Lippincott-Schwartz, J., and Blackstone, C. (2022). ER proteins decipher the tubulin code to regulate organelle distribution. Nature 601, 132–138.
Zoncu, R., Bar-Peled, L., Efeyan, A., Wang, S., Sancak, Y., and Sabatini, D.M. (2011). mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase. Science 334, 678–683.
Zoncu, R., and Perera, R.M. (2022). Built to last: lysosome remodeling and repair in health and disease. Trends Cell Biol 32, 597–610.
Acknowledgement
JH is supported by the National Natural Science Foundation of China (92254305), the Strategic Priority Research Program (XDB39000000) and Project for Young Scientists in Basic Research (YSBR-075) of the Chinese Academy of Sciences, and the National Key Research and Development Program of China (2021YFA1300800). CZ is supported by the National Natural Science Foundation of China (92254305, 91854204, 32130026). LG is supported by National Natural Science Foundation of China (92254302, 32225013, 32130023), National Key Research and Development Program of China (2021YFA0804802, 2019YFA0508602), Beijing Natural Science Foundation (JQ20028), and New Cornerstone Science Foundation (Xplorer Prize). HC is supported by grants from the National Natural Science Foundation of China (92254303, 32170701), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB37020304), and the National Key Research and Development Program of China (2021YFA1300301). GY is supported by the National Natural Science Foundation of China (91954201,31971289) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB37040402). XH is supported by grants from the National Natural Science Foundation of China (91954207), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA24030205), and the National Key Research and Development Program of China (2018YFA0506902). YGZ is supported by the National Natural Science Foundation of China (32170753). XB is supported by the National Natural Science Foundation of China (32170692, 92154001), the Fundamental Research Funds for the Central Universities (63213104, 63223043), and the Talent Training Project at Nankai University (035-BB042112). SS is supported by grants from the National Natural Science Foundation of China (32101000, 32271273). WL is supported by the Beijing Municipal Science & Technology Commission (5202022). We apologize to the researchers whose studies could not be cited due to space limitations. We thank all of Chuanmao Zhang’s laboratory members for their constructive suggestions. We also thank Yujie Wu for her technical assistance and Siyu Chen during writing this review.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
The author(s) declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Sun, S., Zhao, G., Jia, M. et al. Stay in touch with the endoplasmic reticulum. Sci. China Life Sci. 67, 230–257 (2024). https://doi.org/10.1007/s11427-023-2443-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-023-2443-9