Skip to main content
SpringerLink
Log in
Book cover

Organelle Contact Sites pp 1–12Cite as

Organelle Communication at Membrane Contact Sites (MCS): From Curiosity to Center Stage in Cell Biology and Biomedical Research

  • Chapter
  • First Online:

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 997))

Abstract

Cell biology has long recognized that organelles can communicate with each other. Initially, such communication was thought to occur primarily via vesicular trafficking between biochemically distinct organelles. However, studies starting in the 1970s on lipid metabolism have unearthed another way how organelles can communicate and have spawned the field of membrane contact sites (MCS). While, initially, MCS had been recognized as fluid entities that mediate lipid and ion transport in an ad hoc manner, more recently MCS have been found to depend on protein–protein interactions that control themselves a variety of MCS functions. As a result, the cell biological definition of an intracellular organelle as an isolated membrane compartment is now being revised. Accordingly, the organelle definition now describes organelles as dynamic membrane compartments that function in a milieu of coordinated contacts with other organelles. Through these mercurial functions, MCS dictate the function of organelles to a large extent but also play important roles in a number of diseases, including type 2 diabetes, neurodegenerative diseases, infections, and cancer. This book assembles reviews that describe our quickly evolving knowledge about organellar communication on MCS and the significance of MCS for disease.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Alford SC, Ding Y, Simmen T, Campbell RE (2012) Dimerization-dependent green and yellow fluorescent proteins. ACS Synth Biol 1:569–575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson RG, Brown MS, Goldstein JL (1977) Role of the coated endocytic vesicle in the uptake of receptor-bound low density lipoprotein in human fibroblasts. Cell 10:351–364

    Article  CAS  PubMed  Google Scholar 

  • Barone V, Randazzo D, Del Re V, Sorrentino V, Rossi D (2015) Organization of junctional sarcoplasmic reticulum proteins in skeletal muscle fibers. J Muscle Res Cell Motil 36:501–515

    Article  CAS  PubMed  Google Scholar 

  • Bernhard W, Haguenau F, Gautier A, Oberling C (1952) Submicroscopical structure of cytoplasmic basophils in the liver, pancreas and salivary gland; study of ultrafine slices by electron microscope. Z Zellforsch Mikrosk Anat 37:281–300

    Article  CAS  PubMed  Google Scholar 

  • Bhuvanendran S, Salka K, Rainey K, Sreetama SC, Williams E, Leeker M, Prasad V, Boyd J, Patterson GH, Jaiswal JK et al (2014) Superresolution imaging of human cytomegalovirus vMIA localization in sub-mitochondrial compartments. Virus 6:1612–1636

    Article  CAS  Google Scholar 

  • Bonifacino JS (2014) Vesicular transport earns a Nobel. Trends Cell Biol 24:3–5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booth DM, Enyedi B, Geiszt M, Varnai P, Hajnoczky G (2016) Redox nanodomains are induced by and control calcium signaling at the ER-mitochondrial interface. Mol Cell 63:240–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brdiczka D, Bucheler K, Kottke M, Adams V, Nalam VK (1990) Characterization and metabolic function of mitochondrial contact sites. Biochim Biophys Acta 1018:234–238

    Article  CAS  PubMed  Google Scholar 

  • Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang KT et al (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459:596–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardenas C, Miller RA, Smith I, Bui T, Molgo J, Muller M, Vais H, Cheung KH, Yang J, Parker I et al (2010) Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142:270–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cherradi N, Rossier MF, Vallotton MB, Capponi AM (1996) Calcium stimulates intramitochondrial cholesterol transfer in bovine adrenal glomerulosa cells. J Biol Chem 271:25971–25975

    Article  CAS  PubMed  Google Scholar 

  • Chu BB, Liao YC, Qi W, Xie C, Du X, Wang J, Yang H, Miao HH, Li BL, Song BL (2015) Cholesterol transport through lysosome-peroxisome membrane contacts. Cell 161:291–306

    Article  CAS  PubMed  Google Scholar 

  • Colberg-Poley AM, Patterson GH, Salka K, Bhuvanendran S, Yang D, Jaiswal JK (2015) Superresolution imaging of viral protein trafficking. Med Microbiol Immunol 204:449–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colombini M, Blachly-Dyson E, Forte M (1996) VDAC, a channel in the outer mitochondrial membrane. Ion Channels 4:169–202

    Article  CAS  PubMed  Google Scholar 

  • Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG, Balla T, Hajnoczky G (2010) Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell 39:121–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, Sorensen JB, Verhage M (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138:935–946

    Article  PubMed  CAS  Google Scholar 

  • Du X, Kumar J, Ferguson C, Schulz TA, Ong YS, Hong W, Prinz WA, Parton RG, Brown AJ, Yang H (2011) A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. J Cell Biol 192:121–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisner V, Csordas G, Hajnoczky G (2013) Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle – pivotal roles in Ca2+ and reactive oxygen species signaling. J Cell Sci 126:2965–2978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisner V, Lenaers G, Hajnoczky G (2014) Mitochondrial fusion is frequent in skeletal muscle and supports excitation-contraction coupling. J Cell Biol 205:179–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • English AR, Voeltz GK (2013) Endoplasmic reticulum structure and interconnections with other organelles. Cold Spring Harb Perspect Biol 5:a013227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fernandez-Busnadiego R, Saheki Y, De Camilli P (2015) Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. Proc Natl Acad Sci U S A 112:E2004–E2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK (2011) ER tubules mark sites of mitochondrial division. Science 334:358–362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritz S, Rapaport D, Klanner E, Neupert W, Westermann B (2001) Connection of the mitochondrial outer and inner membranes by Fzo1 is critical for organellar fusion. J Cell Biol 152:683–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatta AT, Levine TP (2017) Piecing together the patchwork of contact sites. Trends Cell Biol 27(3):214–229

    Article  CAS  PubMed  Google Scholar 

  • Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, Stevens CF, Südhof TC (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79:717–727

    Article  CAS  PubMed  Google Scholar 

  • Gerasimenko JV, Charlesworth RM, Sherwood MW, Ferdek PE, Mikoshiba K, Parrington J, Petersen OH, Gerasimenko OV (2015) Both RyRs and TPCs are required for NAADP-induced intracellular Ca2+ release. Cell Calcium 58:237–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giacomello M, Pellegrini L (2016) The coming of age of the mitochondria-ER contact: a matter of thickness. Cell Death Differ 23:1417–1427

    Article  CAS  PubMed  Google Scholar 

  • Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P2-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:1494–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein JL, Brown MS (2015) A century of cholesterol and coronaries: from plaques to genes to statins. Cell 161:161–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein JL, Anderson RG, Brown MS (1979) Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279:679–685

    Article  CAS  PubMed  Google Scholar 

  • Goldstein JL, DeBose-Boyd RA, Brown MS (2006) Protein sensors for membrane sterols. Cell 124:35–46

    Article  CAS  PubMed  Google Scholar 

  • Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC et al (2008) STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 18:177–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hackenbrock CR (1968) Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. Proc Natl Acad Sci U S A 61:598–605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harner M, Korner C, Walther D, Mokranjac D, Kaesmacher J, Welsch U, Griffith J, Mann M, Reggiori F, Neupert W (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30:4356–4370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi T, Su TP (2003) Sigma-1 receptors (sigma(1) binding sites) form raft-like microdomains and target lipid droplets on the endoplasmic reticulum: roles in endoplasmic reticulum lipid compartmentalization and export. J Pharmacol Exp Ther 306:718–725

    Article  CAS  PubMed  Google Scholar 

  • Helle SC, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B (2013) Organization and function of membrane contact sites. Biochim Biophys Acta 1833:2526–2541

    Article  CAS  PubMed  Google Scholar 

  • Herdman C, Moss T (2016) Extended-Synaptotagmins (E-Syts); the extended story. Pharmacol Res 107:48–56

    Article  CAS  PubMed  Google Scholar 

  • Holtzman E, Novikoff AB, Villaverde H (1967) Lysosomes and GERL in normal and chromatolytic neurons of the rat ganglion nodosum. J Cell Biol 33:419–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honscher C, Ungermann C (2014) A close-up view of membrane contact sites between the endoplasmic reticulum and the endolysosomal system: from yeast to man. Crit Rev Biochem Mol Biol 49:262–268

    Article  PubMed  CAS  Google Scholar 

  • Jacobs JL, Coyne CB (2013) Mechanisms of MAVS regulation at the mitochondrial membrane. J Mol Biol 425:5009–5019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim TH, Zhao Y, Ding WX, Shin JN, He X, Seo YW, Chen J, Rabinowich H, Amoscato AA, Yin XM (2004) Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome C release. Mol Biol Cell 15:3061–3072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim BJ, Park KH, Yim CY, Takasawa S, Okamoto H, Im MJ, Kim UH (2008) Generation of nicotinic acid adenine dinucleotide phosphate and cyclic ADP-ribose by glucagon-like peptide-1 evokes Ca2+ signal that is essential for insulin secretion in mouse pancreatic islets. Diabetes 57:868–878

    Article  CAS  PubMed  Google Scholar 

  • Kornmann B, Walter P (2010) ERMES-mediated ER-mitochondria contacts: molecular hubs for the regulation of mitochondrial biology. J Cell Sci 123:1389–1393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kottke M, Adam V, Riesinger I, Bremm G, Bosch W, Brdiczka D, Sandri G, Panfili E (1988) Mitochondrial boundary membrane contact sites in brain: points of hexokinase and creatine kinase location, and control of Ca2+ transport. Biochim Biophys Acta 935:87–102

    Article  CAS  PubMed  Google Scholar 

  • Krols M, van Isterdael G, Asselbergh B, Kremer A, Lippens S, Timmerman V, Janssens S (2016) Mitochondria-associated membranes as hubs for neurodegeneration. Acta Neuropathol 131:505–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levental I, Lingwood D, Grzybek M, Coskun U, Simons K (2010) Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci U S A 107:22050–22054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levine T (2004) Short-range intracellular trafficking of small molecules across endoplasmic reticulum junctions. Trends Cell Biol 14:483–490

    Article  CAS  PubMed  Google Scholar 

  • Levine TP, Patel S (2016) Signalling at membrane contact sites: two membranes come together to handle second messengers. Curr Opin Cell Biol 39:77–83

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Ge M, Ciani L, Kuriakose G, Westover EJ, Dura M, Covey DF, Freed JH, Maxfield FR, Lytton J et al (2004) Enrichment of endoplasmic reticulum with cholesterol inhibits sarcoplasmic-endoplasmic reticulum calcium ATPase-2b activity in parallel with increased order of membrane lipids: implications for depletion of endoplasmic reticulum calcium stores and apoptosis in cholesterol-loaded macrophages. J Biol Chem 279:37030–37039

    Article  CAS  PubMed  Google Scholar 

  • Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luik RM, Wu MM, Buchanan J, Lewis RS (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174:815–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynes EM, Simmen T (2011) Urban planning of the endoplasmic reticulum (ER): how diverse mechanisms segregate the many functions of the ER. Biochim Biophys Acta 1813:1893–1905

    Article  CAS  PubMed  Google Scholar 

  • Lynes EM, Bui M, Yap MC, Benson MD, Schneider B, Ellgaard L, Berthiaume LG, Simmen T (2012) Palmitoylated TMX and calnexin target to the mitochondria-associated membrane. EMBO J 31:457–470

    Article  CAS  PubMed  Google Scholar 

  • Lynes EM, Raturi A, Shenkman M, Ortiz Sandoval C, Yap MC, Wu J, Janowicz A, Myhill N, Benson MD, Campbell RE et al (2013) Palmitoylation is the switch that assigns calnexin to quality control or ER Ca2+ signaling. J Cell Sci 126:3893–3903

    Article  CAS  PubMed  Google Scholar 

  • Marchi S, Giorgi C, Oparka M, Duszynski J, Wieckowski MR, Pinton P (2014) Oncogenic and oncosuppressive signal transduction at mitochondria-associated endoplasmic reticulum membranes. Mol Cell Oncol 1:e956469

    Article  PubMed  PubMed Central  Google Scholar 

  • Maxfield FR, Wustner D (2002) Intracellular cholesterol transport. J Clin Invest 110:891–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McMurray WC, Dawson RM (1969) Phospholipid exchange reactions within the liver cell. Biochem J 112:91–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mercer JC, Dehaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney JW Jr (2006) Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem 281:24979–24990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikoshiba K (2007) The IP3 receptor/Ca2+ channel and its cellular function. Biochem Soc Symp 74:9–22

    Article  CAS  Google Scholar 

  • Missiroli S, Bonora M, Patergnani S, Poletti F, Perrone M, Gafa R, Magri E, Raimondi A, Lanza G, Tacchetti C, Kroemer G, Pandolfi PP, Pinton P, Giorgi C (2016) PML at mitochondria-associated membranes is critical for the repression of autophagy and cancer development. Cell Rep 16:2415–2427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munoz P, Rosemblatt M, Testar X, Palacin M, Zorzano A (1995) Isolation and characterization of distinct domains of sarcolemma and T-tubules from rat skeletal muscle. Biochem J 307:273–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375–2390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neuspiel M, Schauss AC, Braschi E, Zunino R, Rippstein P, Rachubinski RA, Andrade-Navarro MA, McBride HM (2008) Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biol 18:102–108

    Article  CAS  PubMed  Google Scholar 

  • Nixon-Abell J, Obara CJ, Weigel AV, Li D, Legant WR, Xu CS, Pasolli HA, Harvey K, Hess HF, Betzig E et al (2016) Increased spatiotemporal resolution reveals highly dynamic dense tubular matrices in the peripheral ER. Science 354:aaf3928

    Article  PubMed  CAS  Google Scholar 

  • Novick P, Schekman R (1979) Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 76:1858–1862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Novick P, Field C, Schekman R (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21:205–215

    Article  CAS  PubMed  Google Scholar 

  • Novikoff AB (1976) The endoplasmic reticulum: a cytochemist’s view (a review). Proc Natl Acad Sci U S A 73:2781–2787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189:347–358

    Article  CAS  PubMed  Google Scholar 

  • Park Y, Seo JB, Fraind A, Perez-Lara A, Yavuz H, Han K, Jung SR, Kattan I, Walla PJ, Choi M et al (2015) Synaptotagmin-1 binds to PIP2-containing membrane but not to SNAREs at physiological ionic strength. Nat Struct Mol Biol 22:815–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parrington J, Lear P, Hachem A (2015) Calcium signals regulated by NAADP and two-pore channels-their role in development, differentiation and cancer. Int J Dev Biol 59:341–535

    Article  CAS  PubMed  Google Scholar 

  • Patergnani S, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E, Giorgi C, Marchi S, Missiroli S, Poletti F et al (2011) Calcium signaling around mitochondria associated membranes (MAMs). Cell Commun Signal 9:19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peinelt C, Vig M, Koomoa DL, Beck A, Nadler MJ, Koblan-Huberson M, Lis A, Fleig A, Penner R, Kinet JP (2006) Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol 8:771–773

    Article  CAS  PubMed  Google Scholar 

  • Perez-Lara A, Jahn R (2015) Extended synaptotagmins (E-Syts): architecture and dynamics of membrane contact sites revealed. Proc Natl Acad Sci U S A 112:4837–4838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perin MS, Fried VA, Mignery GA, Jahn R, Südhof TC (1990) Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345:260–263

    Article  CAS  PubMed  Google Scholar 

  • Perkins G, Renken C, Martone ME, Young SJ, Ellisman M, Frey T (1997) Electron tomography of neuronal mitochondria: three-dimensional structure and organization of cristae and membrane contacts. J Struct Biol 119:260–272

    Article  CAS  PubMed  Google Scholar 

  • Phillips MJ, Voeltz GK (2016) Structure and function of ER membrane contact sites with other organelles. Nat Rev Mol Cell Biol 17:69–82

    Article  CAS  PubMed  Google Scholar 

  • Phimister AJ, Lango J, Lee EH, Ernst-Russell MA, Takeshima H, Ma J, Allen PD, Pessah IN (2007) Conformation-dependent stability of junctophilin 1 (JP1) and ryanodine receptor type 1 (RyR1) channel complex is mediated by their hyper-reactive thiols. J Biol Chem 282:8667–8677

    Article  CAS  PubMed  Google Scholar 

  • Pichler H, Gaigg B, Hrastnik C, Achleitner G, Kohlwein SD, Zellnig G, Perktold A, Daum G (2001) A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur J Biochem 268:2351–2361

    Article  CAS  PubMed  Google Scholar 

  • Pike LJ (2003) Lipid rafts: bringing order to chaos. J Lipid Res 44:655–667

    Article  CAS  PubMed  Google Scholar 

  • Pon L, Moll T, Vestweber D, Marshallsay B, Schatz G (1989) Protein import into mitochondria: ATP-dependent protein translocation activity in a submitochondrial fraction enriched in membrane contact sites and specific proteins. J Cell Biol 109:2603–2616

    Article  CAS  PubMed  Google Scholar 

  • Porter KR, Palade GE (1957) Studies on the endoplasmic reticulum. III Its form and distribution in striated muscle cells J Biophys Biochem Cytol 3:269–300

    CAS  PubMed  Google Scholar 

  • Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230–233

    Article  CAS  PubMed  Google Scholar 

  • Quintana A, Pasche M, Junker C, Al-Ansary D, Rieger H, Kummerow C, Nunez L, Villalobos C, Meraner P, Becherer U et al (2011) Calcium microdomains at the immunological synapse: how ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation. EMBO J 30:3895–3912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS (2008) Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: a delicate balance. Cell Metab 8:512–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raturi A, Gutierrez T, Ortiz-Sandoval C, Ruangkittisakul A, Herrera-Cruz MS, Rockley JP, Gesson K, Ourdev D, Lou PH, Lucchinetti E et al (2016) TMX1 determines cancer cell metabolism as a thiol-based modulator of ER-mitochondria Ca2+ flux. J Cell Biol 214:433–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhart MP, Billheimer JT, Faust JR, Gaylor JL (1987) Subcellular localization of the enzymes of cholesterol biosynthesis and metabolism in rat liver. J Biol Chem 262:9649–9655

    CAS  PubMed  Google Scholar 

  • Reinisch KM, De Camilli P (2016) SMP-domain proteins at membrane contact sites: structure and function. Biochim Biophys Acta 1861:924–927

    Article  CAS  PubMed  Google Scholar 

  • Rizzuto R, Brini M, Murgia M, Pozzan T (1993) Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262:744–747

    Article  CAS  PubMed  Google Scholar 

  • Rothman JE, Fine RE (1980) Coated vesicles transport newly synthesized membrane glycoproteins from endoplasmic reticulum to plasma membrane in two successive stages. Proc Natl Acad Sci U S A 77:780–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rothman JE, Bursztyn-Pettegrew H, Fine RE (1980) Transport of the membrane glycoprotein of vesicular stomatitis virus to the cell surface in two stages by clathrin-coated vesicles. J Cell Biol 86:162–171

    Article  CAS  PubMed  Google Scholar 

  • Rowland AA, Chitwood PJ, Phillips MJ, Voeltz GK (2014) ER contact sites define the position and timing of endosome fission. Cell 159:1027–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudolf R, Mongillo M, Magalhaes PJ, Pozzan T (2004) In vivo monitoring of Ca2+ uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol 166:527–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rusinol AE, Cui Z, Chen MH, Vance JE (1994) A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins. J Biol Chem 269:27494–27502

    CAS  PubMed  Google Scholar 

  • Rutter GA, Pinton P (2014) Mitochondria-associated endoplasmic reticulum membranes in insulin signaling. Diabetes 63:3163–3165

    Article  CAS  PubMed  Google Scholar 

  • Sala-Vila A, Navarro-Lerida I, Sanchez-Alvarez M, Bosch M, Calvo C, Lopez JA, Calvo E, Ferguson C, Giacomello M, Serafini A et al (2016) Interplay between hepatic mitochondria-associated membranes, lipid metabolism and caveolin-1 in mice. Sci Rep 6:27351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauner MT, Levy M (1971) Study of the transfer of phospholipids from the endoplasmic reticulum to the outer and inner mitochondrial membranes. J Lipid Res 12:71–75

    CAS  PubMed  Google Scholar 

  • Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, Wenk MR, De Camilli P, Reinisch KM (2014) Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510:552–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schrader M (2001) Tubulo-reticular clusters of peroxisomes in living COS-7 cells: dynamic behavior and association with lipid droplets. J Histochem Cytochem 49:1421–1429

    Article  CAS  PubMed  Google Scholar 

  • Schultz ML, Krus KL, Lieberman AP (2016) Lysosome and endoplasmic reticulum quality control pathways in Niemann-Pick type C disease. Brain Res 1649:181–188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwaiger M, Herzog V, Neupert W (1987) Characterization of translocation contact sites involved in the import of mitochondrial proteins. J Cell Biol 105:235–246

    Article  CAS  PubMed  Google Scholar 

  • Shiao YJ, Lupo G, Vance JE (1995) Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine. J Biol Chem 270:11190–11198

    Article  CAS  PubMed  Google Scholar 

  • Shoshan-Barmatz V, Zalk R, Gincel D, Vardi N (2004) Subcellular localization of VDAC in mitochondria and ER in the cerebellum. Biochim Biophys Acta 1657:105–114

    Article  CAS  PubMed  Google Scholar 

  • Simbeni R, Pon L, Zinser E, Paltauf F, Daum G (1991) Mitochondrial membrane contact sites of yeast. Characterization of lipid components and possible involvement in intramitochondrial translocation of phospholipids. J Biol Chem 266:10047–10049

    CAS  PubMed  Google Scholar 

  • Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458:1131–1145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith JJ, Aitchison JD (2013) Peroxisomes take shape. Nat Rev Mol Cell Biol 14:803–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–324

    Article  PubMed  Google Scholar 

  • Stathopulos PB, Zheng L, Li GY, Plevin MJ, Ikura M (2008) Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135:110–122

    Article  CAS  PubMed  Google Scholar 

  • Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6:11–22

    CAS  PubMed  Google Scholar 

  • Thomson M (2003) Does cholesterol use the mitochondrial contact site as a conduit to the steroidogenic pathway? BioEssays 25:252–258

    Article  CAS  PubMed  Google Scholar 

  • Tubbs E, Theurey P, Vial G, Bendridi N, Bravard A, Chauvin MA, Ji-Cao J, Zoulim F, Bartosch B, Ovize M et al (2014) Mitochondria-associated endoplasmic reticulum membrane (MAM) integrity is required for insulin signaling and is implicated in hepatic insulin resistance. Diabetes 63:3279–3294

    Article  CAS  PubMed  Google Scholar 

  • van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, Willig KI, Hubrich BE, Dier M, Hell SW, Grubmuller H, Diederichsen U et al (2011a) Membrane protein sequestering by ionic protein-lipid interactions. Nature 479:552–555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van den Bogaart G, Thutupalli S, Risselada JH, Meyenberg K, Holt M, Riedel D, Diederichsen U, Herminghaus S, Grubmuller H, Jahn R (2011b) Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation. Nat Struct Mol Biol 18:805–812

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Zutphen T, Todde V, de Boer R, Kreim M, Hofbauer HF, Wolinski H, Veenhuis M, van der Klei IJ, Kohlwein SD (2014) Lipid droplet autophagy in the yeast Saccharomyces cerevisiae. Mol Biol Cell 25:290–301

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vance JE (1990) Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 265:7248–7256

    CAS  PubMed  Google Scholar 

  • Vance JE (1991) Newly made phosphatidylserine and phosphatidylethanolamine are preferentially translocated between rat liver mitochondria and endoplasmic reticulum. J Biol Chem 266:89–97

    CAS  PubMed  Google Scholar 

  • Vance JE (2015) Phospholipid synthesis and transport in mammalian cells. Traffic 16:1–18

    Article  CAS  PubMed  Google Scholar 

  • Varnai P, Toth B, Toth DJ, Hunyady L, Balla T (2007) Visualization and manipulation of plasma membrane-endoplasmic reticulum contact sites indicates the presence of additional molecular components within the STIM1-Orai1 complex. J Biol Chem 282:29678–29690

    Article  CAS  PubMed  Google Scholar 

  • Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573–586

    Article  CAS  PubMed  Google Scholar 

  • Wang HJ, Guay G, Pogan L, Sauve R, Nabi IR (2000) Calcium regulates the association between mitochondria and a smooth subdomain of the endoplasmic reticulum. J Cell Biol 150:1489–1498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver D, Eisner V, Liu X, Varnai P, Hunyady L, Gross A, Hajnoczky G (2014) Distribution and apoptotic function of outer membrane proteins depend on mitochondrial fusion. Mol Cell 54:870–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westermann B (2015) The mitochondria-plasma membrane contact site. Curr Opin Cell Biol 35:1–6

    Article  CAS  PubMed  Google Scholar 

  • Wideman JG, Gawryluk RM, Gray MW, Dacks JB (2013) The ancient and widespread nature of the ER-mitochondria encounter structure. Mol Biol Evol 30:2044–2049

    Article  CAS  PubMed  Google Scholar 

  • Wilfling F, Haas JT, Walther TC, Farese RV Jr (2014) Lipid droplet biogenesis. Curr Opin Cell Biol 29:39–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wirtz KW, Zilversmit DB (1968) Exchange of phospholipids between liver mitochondria and microsomes in vitro. J Biol Chem 243:3596–3602

    CAS  PubMed  Google Scholar 

  • Wozniak MJ, Bola B, Brownhill K, Yang YC, Levakova V, Allan VJ (2009) Role of kinesin-1 and cytoplasmic dynein in endoplasmic reticulum movement in VERO cells. J Cell Sci 122:1979–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu MM, Buchanan J, Luik RM, Lewis RS (2006) Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 174:803–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu P, Lu J, Li Z, Yu X, Chen L, Xu T (2006) Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun 350:969–976

    Article  CAS  PubMed  Google Scholar 

  • Züchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, Zappia M, Nelis E, Patitucci A, Senderek J et al (2004) Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 36:449–451

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Maria Sol Herrera for the design of the figure and critical reading of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Medicine and Dentistry, Department of Cell Biology, University of Alberta, Edmonton, T6G2H7, Canada

    Thomas Simmen

  2. School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Hachioji, Tokyo, 192-0392, Japan

    Mitsuo Tagaya

Authors
  1. Thomas Simmen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mitsuo Tagaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Simmen .

Editor information

Editors and Affiliations

  1. School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, Hachioji, Tokyo, Japan

    Mitsuo Tagaya

  2. Department of Cell Biology, University of Alberta, Edmonton, Alberta, Canada

    Thomas Simmen

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Simmen, T., Tagaya, M. (2017). Organelle Communication at Membrane Contact Sites (MCS): From Curiosity to Center Stage in Cell Biology and Biomedical Research. In: Tagaya, M., Simmen, T. (eds) Organelle Contact Sites. Advances in Experimental Medicine and Biology, vol 997. Springer, Singapore. https://doi.org/10.1007/978-981-10-4567-7_1

Download citation

Publish with us

Policies and ethics

Search

Navigation