Abstract
Endocytosis is a means for the cell to sample its environment for nutrients and regulate plasma membrane (PM) composition and area. Whereas the majority of internalized cargo is recycled back to the cell surface, select material is sent to the lysosome for degradation. Endosomes further play major roles in central cell activities as diverse as establishment of cell polarity and signaling, lysosomal storage and immunity. The complexity of endosomal functions is reflected by the extensive changes to endosome properties as they mature. The identity of individual endosomes is influenced by the presence of specific Rab GTPases and phosphoinositides (PIPs), which coordinate membrane traffic and facilitate endosomal functions. Motors and tethers direct the endosomes to the required locations and moderate fusion with other organelles. The maintenance of the elaborate endosomal network is supported by the ER and the trans-Golgi network (TGN), which promote the exchange of membrane components, provide enzymes, and assist with signaling. Additionally, V-ATPase is emerging as an underappreciated coordinator of endosome maturation and cell signaling. The inputs of the various mediators of endosome maturation are tightly regulated and coordinated to ensure appropriate maintenance and functioning of endosomes at each stage of the maturation process. Perturbations in endosome maturation are implicated in devastating diseases, such as neurodegeneration and cancer, and the endosome maturation processes are manipulated and exploited by intracellular pathogens to meet their own needs. A greater understanding of coordination and fine-tuning of endosome maturation will help us address various pathologies more effectively.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- EE:
-
Early endosome
- CI-M6PR:
-
Cation-independent mannose-6-phosphate receptor
- ILV:
-
Intra luminal vesicle
- LE:
-
Late endosome
- MVB:
-
Multivesicular body
- PIP:
-
Phosphoinositide phosphate
- PM:
-
Plasma membrane
- TfR:
-
Transferrin receptor
- TGN:
-
Trans-Golgi network
References
Abenza JF, Galindo A, Pinar M, Pantazopoulou A, de los Rios V, Penalva MA (2012) Endosomal maturation by Rab conversion in Aspergillus nidulans is coupled to dynein-mediated basipetal movement. Mol Biol Cell 23(10):1889–1901. https://doi.org/10.1091/mbc.E11-11-0925
Adell MA, Vogel GF, Pakdel M, Muller M, Lindner H, Hess MW, Teis D (2014) Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation. J Cell Biol 205(1):33–49. https://doi.org/10.1083/jcb.201310114
Akbar MA, Mandraju R, Tracy C, Hu W, Pasare C, Kramer H (2016) ARC syndrome-linked Vps33B protein is required for inflammatory endosomal maturation and signal termination. Immunity 45(2):267–279. https://doi.org/10.1016/j.immuni.2016.07.010
Amaya C, Militello RD, Calligaris SD, Colombo MI (2016) Rab24 interacts with the Rab7/Rab interacting lysosomal protein complex to regulate endosomal degradation. Traffic 17(11):1181–1196. https://doi.org/10.1111/tra.12431
Andrews NW, Corrotte M, Castro-Gomes T (2015) Above the fray: surface remodeling by secreted lysosomal enzymes leads to endocytosis-mediated plasma membrane repair. Semin Cell Dev Biol 45:10–17. https://doi.org/10.1016/j.semcdb.2015.09.022
Antonescu CN, Aguet F, Danuser G, Schmid SL (2011) Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol Biol Cell 22(14):2588–2600. https://doi.org/10.1091/mbc.E11-04-0362
Ao X, Zou L, Wu Y (2014) Regulation of autophagy by the Rab GTPase network. Cell Death Differ 21(3):348–358. https://doi.org/10.1038/cdd.2013.187
Armstrong J (2010) Yeast vacuoles: more than a model lysosome. Trends Cell Biol 20(10):580–585. https://doi.org/10.1016/j.tcb.2010.06.010
Bach H, Papavinasasundaram KG, Wong D, Hmama Z, Av-Gay Y (2008) Mycobacterium tuberculosis virulence is mediated by PtpA dephosphorylation of human vacuolar protein sorting 33B. Cell Host Microbe 3(5):316–322. https://doi.org/10.1016/j.chom.2008.03.008
Balderhaar HJ, Ungermann C (2013) CORVET and HOPS tethering complexes—coordinators of endosome and lysosome fusion. J Cell Sci 126(Pt 6):1307–1316. https://doi.org/10.1242/jcs.107805
Baravalle G, Schober D, Huber M, Bayer N, Murphy RF, Fuchs R (2005) Transferrin recycling and dextran transport to lysosomes is differentially affected by bafilomycin, nocodazole, and low temperature. Cell Tissue Res 320(1):99–113. https://doi.org/10.1007/s00441-004-1060-x
Bean BD, Davey M, Conibear E (2017) Cargo selectivity of yeast sorting nexins. Traffic 18(2):110–122. https://doi.org/10.1111/tra.12459
Ben-Sahra I, Manning BD (2017) mTORC1 signaling and the metabolic control of cell growth. Curr Opin Cell Biol 45:72–82. https://doi.org/10.1016/j.ceb.2017.02.012
Bissig C, Hurbain I, Raposo G, van Niel G (2017) PIKfyve activity regulates reformation of terminal storage lysosomes from endolysosomes. Traffic 18(11):747–757. https://doi.org/10.1111/tra.12525
Boal F, Mansour R, Gayral M, Saland E, Chicanne G, Xuereb JM, Marcellin M, Burlet-Schiltz O, Sansonetti PJ, Payrastre B, Tronchere H (2015) TOM1 is a PI5P effector involved in the regulation of endosomal maturation. J Cell Sci 128(4):815–827. https://doi.org/10.1242/jcs.166314
Boes M, Cuvillier A, Ploegh H (2004) Membrane specializations and endosome maturation in dendritic cells and B cells. Trends Cell Biol 14(4):175–183. https://doi.org/10.1016/j.tcb.2004.02.004
Bohdanowicz M, Grinstein S (2013) Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis. Physiol Rev 93(1):69–106. https://doi.org/10.1152/physrev.00002.2012
Borland H, Vilhardt F (2017) Prelysosomal compartments in the unconventional secretion of amyloidogenic seeds. Int J Mol Sci 18(1). https://doi.org/10.3390/ijms18010227
Bouchez I, Pouteaux M, Canonge M, Genet M, Chardot T, Guillot A, Froissard M (2015) Regulation of lipid droplet dynamics in Saccharomyces cerevisiae depends on the Rab7-like Ypt7p, HOPS complex and V1-ATPase. Biol Open 4(7):764–775. https://doi.org/10.1242/bio.20148615
Broniarczyk J, Pim D, Massimi P, Bergant M, Gozdzicka-Jozefiak A, Crump C, Banks L (2017) The VPS4 component of the ESCRT machinery plays an essential role in HPV infectious entry and capsid disassembly. Sci Rep 7:45159. https://doi.org/10.1038/srep45159
Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11(2):467–480
Buckley CM, King JS (2017) Drinking problems: mechanisms of macropinosome formation and maturation. FEBS J. https://doi.org/10.1111/febs.14115
Candiello E, Kratzke M, Wenzel D, Cassel D, Schu P (2016) AP-1/σ1A and AP-1/σ1B adaptor-proteins differentially regulate neuronal early endosome maturation via the Rab5/Vps34-pathway. Sci Rep 6:29950. https://doi.org/10.1038/srep29950
Cao Q, Zhong XZ, Zou Y, Murrell-Lagnado R, Zhu MX, Dong XP (2015) Calcium release through P2X4 activates calmodulin to promote endolysosomal membrane fusion. J Cell Biol 209(6):879–894. https://doi.org/10.1083/jcb.201409071
Cardoso CM, Jordao L, Vieira OV (2010) Rab10 regulates phagosome maturation and its overexpression rescues Mycobacterium-containing phagosomes maturation. Traffic 11(2):221–235. https://doi.org/10.1111/j.1600-0854.2009.01013.x
Caviglia S, Brankatschk M, Fischer EJ, Eaton S, Luschnig S (2016) Staccato/Unc-13-4 controls secretory lysosome-mediated lumen fusion during epithelial tube anastomosis. Nat Cell Biol 18(7):727–739. https://doi.org/10.1038/ncb3374
Chen PI, Kong C, Su X, Stahl PD (2009) Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors. J Biol Chem 284(44):30328–30338. https://doi.org/10.1074/jbc.M109.034546
Chen SH, Bubb MR, Yarmola EG, Zuo J, Jiang J, Lee BS, Lu M, Gluck SL, Hurst IR, Holliday LS (2004) Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem 279(9):7988–7998. https://doi.org/10.1074/jbc.M305351200
Chirivino D, Del Maestro L, Formstecher E, Hupe P, Raposo G, Louvard D, Arpin M (2011) The ERM proteins interact with the HOPS complex to regulate the maturation of endosomes. Mol Biol Cell 22(3):375–385. https://doi.org/10.1091/mbc.E10-09-0796
Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip SC, Waterfield MD, Backer JM, Zerial M (1999) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1(4):249–252. https://doi.org/10.1038/12075
Clague MJ, Hammond DE (2006) Membrane traffic: catching the lysosome express. Current Biol CB 16(11):R416–R418. https://doi.org/10.1016/j.cub.2006.05.009
Clarke M, Maddera L, Engel U, Gerisch G (2010) Retrieval of the vacuolar H-ATPase from phagosomes revealed by live cell imaging. PLoS ONE 5(1):e8585. https://doi.org/10.1371/journal.pone.0008585
Cogli L, Progida C, Bramato R, Bucci C (2013) Vimentin phosphorylation and assembly are regulated by the small GTPase Rab7a. Biochem Biophys Acta 1833(6):1283–1293. https://doi.org/10.1016/j.bbamcr.2013.02.024
Colacurcio DJ, Nixon RA (2016) Disorders of lysosomal acidification—the emerging role of v-ATPase in aging and neurodegenerative disease. Age Res Rev 32:75–88. https://doi.org/10.1016/j.arr.2016.05.004
Compagnon J, Gervais L, Roman MS, Chamot-Boeuf S, Guichet A (2009) Interplay between Rab5 and PtdIns(4,5)P2 controls early endocytosis in the Drosophila germline. J Cell Sci 122(Pt 1):25–35. https://doi.org/10.1242/jcs.033027
Compton LM, Ikonomov OC, Sbrissa D, Garg P, Shisheva A (2016) Active vacuolar H+ATPase and functional cycle of Rab5 are required for the vacuolation defect triggered by PtdIns(3,5)P2 loss under PIKfyve or Vps34 deficiency. Am J Physiol Cell Physiol 311(3):C366–C377. https://doi.org/10.1152/ajpcell.00104.2016
Cotter K, Stransky L, McGuire C, Forgac M (2015) Recent Insights into the structure, regulation, and function of the V-ATPases. Trends Biochem Sci 40(10):611–622. https://doi.org/10.1016/j.tibs.2015.08.005
Currinn H, Wassmer T (2016) The amyloid precursor protein (APP) binds the PIKfyve complex and modulates its function. Biochem Soc Trans 44(1):185–190. https://doi.org/10.1042/BST20150179
D’Costa VM, Braun V, Landekic M, Shi R, Proteau A, McDonald L, Cygler M, Grinstein S, Brumell JH (2015) Salmonella disrupts host endocytic trafficking by SopD2-mediated inhibition of Rab7. Cell Rep 12(9):1508–1518. https://doi.org/10.1016/j.celrep.2015.07.063
D’Souza RS, Semus R, Billings EA, Meyer CB, Conger K, Casanova JE (2014) Rab4 orchestrates a small GTPase cascade for recruitment of adaptor proteins to early endosomes. Current Biol CB 24(11):1187–1198. https://doi.org/10.1016/j.cub.2014.04.003
Danson C, Brown E, Hemmings OJ, McGough IJ, Yarwood S, Heesom KJ, Carlton JG, Martin-Serrano J, May MT, Verkade P, Cullen PJ (2013) SNX15 links clathrin endocytosis to the PtdIns3P early endosome independently of the APPL1 endosome. J Cell Sci 126(Pt 21):4885–4899. https://doi.org/10.1242/jcs.125732
Dayam RM, Saric A, Shilliday RE, Botelho RJ (2015) The Phosphoinositide-gated lysosomal Ca(2+) channel, TRPML1, is required for phagosome maturation. Traffic 16(9):1010–1026. https://doi.org/10.1111/tra.12303
de Armas-Rillo L, Valera MS, Marrero-Hernandez S, Valenzuela-Fernandez A (2016) Membrane dynamics associated with viral infection. Rev Med Virol 26(3):146–160. https://doi.org/10.1002/rmv.1872
De Luca M, Bucci C (2014) A new V-ATPase regulatory mechanism mediated by the Rab interacting lysosomal protein (RILP). Commun Integr Biol 7(5). https://doi.org/10.4161/cib.29616
De Luca M, Cogli L, Progida C, Nisi V, Pascolutti R, Sigismund S, Di Fiore PP, Bucci C (2014) RILP regulates vacuolar ATPase through interaction with the V1G1 subunit. J Cell Sci 127(Pt 12):2697–2708. https://doi.org/10.1242/jcs.142604
Del Conte-Zerial P, Brusch L, Rink JC, Collinet C, Kalaidzidis Y, Zerial M, Deutsch A (2008) Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol Syst Biol 4:206. https://doi.org/10.1038/msb.2008.45
Desfougeres Y, Vavassori S, Rompf M, Gerasimaite R, Mayer A (2016) Organelle acidification negatively regulates vacuole membrane fusion in vivo. Sci Rep 6:29045. https://doi.org/10.1038/srep29045
Dieckmann R, Gueho A, Monroy R, Ruppert T, Bloomfield G, Soldati T (2012) The balance in the delivery of ER components and the vacuolar proton pump to the phagosome depends on myosin IK in Dictyostelium. Mol Cell Proteomics MCP 11(10):886–900. https://doi.org/10.1074/mcp.M112.017608
Dill BD, Gierlinski M, Hartlova A, Arandilla AG, Guo M, Clarke RG, Trost M (2015) Quantitative proteome analysis of temporally resolved phagosomes following uptake via key phagocytic receptors. Mol Cell Proteomics MCP 14(5):1334–1349. https://doi.org/10.1074/mcp.M114.044594
Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. https://doi.org/10.1146/annurev.biochem.78.081307.110540
Dolat L, Spiliotis ET (2016) Septins promote macropinosome maturation and traffic to the lysosome by facilitating membrane fusion. J Cell Biol 214(5):517–527. https://doi.org/10.1083/jcb.201603030
Dong XP, Shen D, Wang X, Dawson T, Li X, Zhang Q, Cheng X, Zhang Y, Weisman LS, Delling M, Xu H (2010) PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 1:38. https://doi.org/10.1038/ncomms1037
Dove SK, Dong K, Kobayashi T, Williams FK, Michell RH (2009) Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve underPPIn endo-lysosome function. Biochem J 419(1):1–13. https://doi.org/10.1042/BJ20081950
Driskell OJ, Mironov A, Allan VJ, Woodman PG (2007) Dynein is required for receptor sorting and the morphogenesis of early endosomes. Nat Cell Biol 9(1):113–120. https://doi.org/10.1038/ncb1525
Duleh SN, Welch MD (2010) WASH and the Arp2/3 complex regulate endosome shape and trafficking. Cytoskeleton 67(3):193–206. https://doi.org/10.1002/cm.20437
Elbaz-Alon Y, Rosenfeld-Gur E, Shinder V, Futerman AH, Geiger T, Schuldiner M (2014) A dynamic interface between vacuoles and mitochondria in yeast. Dev Cell 30(1):95–102. https://doi.org/10.1016/j.devcel.2014.06.007
Endo Y, Furuta A, Nishino I (2015) Danon disease: a phenotypic expression of LAMP-2 deficiency. Acta Neuropathol 129(3):391–398. https://doi.org/10.1007/s00401-015-1385-4
Fairn GD, Grinstein S (2012) How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33(8):397–405. https://doi.org/10.1016/j.it.2012.03.003
Fili N, Calleja V, Woscholski R, Parker PJ, Larijani B (2006) Compartmental signal modulation: endosomal phosphatidylinositol 3-phosphate controls endosome morphology and selective cargo sorting. Proc Natl Acad Sci USA 103(42):15473–15478. https://doi.org/10.1073/pnas.0607040103
Freeman SA, Grinstein S (2014) Phagocytosis: receptors, signal integration, and the cytoskeleton. Immunol Rev 262(1):193–215. https://doi.org/10.1111/imr.12212
Friedman JR, Dibenedetto JR, West M, Rowland AA, Voeltz GK (2013) Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol Biol Cell 24(7):1030–1040. https://doi.org/10.1091/mbc.E12-10-0733
Gao N, Kaestner KH (2010) Cdx2 regulates endo-lysosomal function and epithelial cell polarity. Genes Dev 24(12):1295–1305. https://doi.org/10.1101/gad.1921510
Garg S, Sharma M, Ung C, Tuli A, Barral DC, Hava DL, Veerapen N, Besra GS, Hacohen N, Brenner MB (2011) Lysosomal trafficking, antigen presentation, and microbial killing are controlled by the Arf-like GTPase Arl8b. Immunity 35(2):182–193. https://doi.org/10.1016/j.immuni.2011.06.009
Garrity AG, Wang W, Collier CM, Levey SA, Gao Q, Xu H (2016) The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes. eLife 5. https://doi.org/10.7554/elife.15887
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11(9):1143–1149. https://doi.org/10.1038/ncb1929
Gopaldass N, Patel D, Kratzke R, Dieckmann R, Hausherr S, Hagedorn M, Monroy R, Kruger J, Neuhaus EM, Hoffmann E, Hille K, Kuznetsov SA, Soldati T (2012) Dynamin A, Myosin IB and Abp1 couple phagosome maturation to F-actin binding. Traffic 13(1):120–130. https://doi.org/10.1111/j.1600-0854.2011.01296.x
Granger E, McNee G, Allan V, Woodman P (2014) The role of the cytoskeleton and molecular motors in endosomal dynamics. Semin Cell Dev Biol 31:20–29. https://doi.org/10.1016/j.semcdb.2014.04.011
Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10(9):597–608. https://doi.org/10.1038/nrm2755
Griffiths GM (2016) Secretion from myeloid cells: secretory lysosomes. Microbiol Spectr 4(4). https://doi.org/10.1128/microbiolspec.mchd-0030-2016
Grimm C, Butz E, Chen CC, Wahl-Schott C, Biel M (2017) From mucolipidosis type IV to Ebola: TRPML and two-pore channels at the crossroads of endo-lysosomal trafficking and disease. Cell Calcium. https://doi.org/10.1016/j.ceca.2017.04.003
Gschweitl M, Ulbricht A, Barnes CA, Enchev RI, Stoffel-Studer I, Meyer-Schaller N, Huotari J, Yamauchi Y, Greber UF, Helenius A, Peter M (2016) A SPOPL/Cullin-3 ubiquitin ligase complex regulates endocytic trafficking by targeting EPS15 at endosomes. eLife 5:e13841. https://doi.org/10.7554/elife.13841
Guerra F, Bucci C (2016) Multiple roles of the small GTPase Rab7. Cells 5(3). https://doi.org/10.3390/cells5030034
Gutierrez MG (2013) Functional role(s) of phagosomal Rab GTPases. Small GTPases 4(3):148–158. https://doi.org/10.4161/sgtp.25604
Hammerling BC, Najor RH, Cortez MQ, Shires SE, Leon LJ, Gonzalez ER, Boassa D, Phan S, Thor A, Jimenez RE, Li H, Kitsis RN, Dorn Ii GW, Sadoshima J, Ellisman MH, Gustafsson AB (2017) A Rab5 endosomal pathway mediates Parkin-dependent mitochondrial clearance. Nat Commun 8:14050. https://doi.org/10.1038/ncomms14050
Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 23(18):6494–6506
Hay JC (2007) Calcium: a fundamental regulator of intracellular membrane fusion? EMBO Rep 8(3):236–240. https://doi.org/10.1038/sj.embor.7400921
He J, Johnson JL, Monfregola J, Ramadass M, Pestonjamasp K, Napolitano G, Zhang J, Catz SD (2016) Munc13-4 interacts with syntaxin 7 and regulates late endosomal maturation, endosomal signaling, and TLR9-initiated cellular responses. Mol Biol Cell 27(3):572–587. https://doi.org/10.1091/mbc.E15-05-0283
Hegedus K, Takats S, Boda A, Jipa A, Nagy P, Varga K, Kovacs AL, Juhasz G (2016) The Ccz1-Mon1-Rab7 module and Rab5 control distinct steps of autophagy. Mol Biol Cell 27(20):3132–3142. https://doi.org/10.1091/mbc.E16-03-0205
Hirano T, Munnik T, Sato MH (2015) Phosphatidylinositol 3-phosphate 5-kinase, FAB1/PIKfyve Kinase mediates endosome maturation to establish endosome-cortical microtubule interaction in Arabidopsis. Plant Physiol 169(3):1961–1974. https://doi.org/10.1104/pp.15.01368
Honscher C, Mari M, Auffarth K, Bohnert M, Griffith J, Geerts W, van der Laan M, Cabrera M, Reggiori F, Ungermann C (2014) Cellular metabolism regulates contact sites between vacuoles and mitochondria. Dev Cell 30(1):86–94. https://doi.org/10.1016/j.devcel.2014.06.006
Hsu F, Hu F, Mao Y (2015) Spatiotemporal control of phosphatidylinositol 4-phosphate by Sac2 regulates endocytic recycling. J Cell Biol 209(1):97–110. https://doi.org/10.1083/jcb.201408027
Hu YB, Dammer EB, Ren RJ, Wang G (2015) The endosomal-lysosomal system: from acidification and cargo sorting to neurodegeneration. Transl Neurodegeneration 4:18. https://doi.org/10.1186/s40035-015-0041-1
Huang C, Chang A (2011) pH-dependent cargo sorting from the Golgi. J Biol Chem 286(12):10058–10065. https://doi.org/10.1074/jbc.M110.197889
Hubner M, Peter M (2012) Cullin-3 and the endocytic system: new functions of ubiquitination for endosome maturation. Cell Logistics 2(3):166–168. https://doi.org/10.4161/cl.20372
Huotari J, Helenius A (2011) Endosome maturation. EMBO J 30(17):3481–3500. https://doi.org/10.1038/emboj.2011.286
Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada GH, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V (2006) V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 8(2):124–136. https://doi.org/10.1038/ncb1348
Huynh KK, Eskelinen EL, Scott CC, Malevanets A, Saftig P, Grinstein S (2007) LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 26(2):313–324. https://doi.org/10.1038/sj.emboj.7601511
Issman-Zecharya N, Schuldiner O (2014) The PI3K class III complex promotes axon pruning by downregulating a Ptc-derived signal via endosome-lysosomal degradation. Dev Cell 31(4):461–473. https://doi.org/10.1016/j.devcel.2014.10.013
Jaber N, Mohd-Naim N, Wang Z, DeLeon JL, Kim S, Zhong H, Sheshadri N, Dou Z, Edinger AL, Du G, Braga VM, Zong WX (2016) Vps34 regulates Rab7 and late endocytic trafficking through recruitment of the GTPase-activating protein Armus. J Cell Sci 129(23):4424–4435. https://doi.org/10.1242/jcs.192260
Jacomin AC, Fauvarque MO, Taillebourg E (2016) A functional endosomal pathway is necessary for lysosome biogenesis in Drosophila. BMC cell biology 17(1):36. https://doi.org/10.1186/s12860-016-0115-7
Jean S, Kiger AA (2012) Coordination between RAB GTPase and phosphoinositide regulation and functions. Nat Rev Mol Cell Biol 13(7):463–470. https://doi.org/10.1038/nrm3379
Jefferies KC, Cipriano DJ, Forgac M (2008) Function, structure and regulation of the vacuolar (H+)-ATPases. Arch Biochem Biophys 476(1):33–42. https://doi.org/10.1016/j.abb.2008.03.025
Jeschke A, Zehethofer N, Lindner B, Krupp J, Schwudke D, Haneburger I, Jovic M, Backer JM, Balla T, Hilbi H, Haas A (2015) Phosphatidylinositol 4-phosphate and phosphatidylinositol 3-phosphate regulate phagolysosome biogenesis. Proc Natl Acad Sci USA 112(15):4636–4641. https://doi.org/10.1073/pnas.1423456112
Jiang P, Mizushima N (2014) Autophagy and human diseases. Cell Res 24(1):69–79. https://doi.org/10.1038/cr.2013.161
Jimenez-Orgaz A, Kvainickas A, Nagele H, Denner J, Eimer S, Dengjel J, Steinberg F (2017) Control of RAB7 activity and localization through the retromer-TBC1D5 complex enables RAB7-dependent mitophagy. EMBO J. https://doi.org/10.15252/embj.201797128
Jin N, Lang MJ, Weisman LS (2016) Phosphatidylinositol 3,5-bisphosphate: regulation of cellular events in space and time. Biochem Soc Trans 44(1):177–184. https://doi.org/10.1042/BST20150174
John Peter AT, Lachmann J, Rana M, Bunge M, Cabrera M, Ungermann C (2013) The BLOC-1 complex promotes endosomal maturation by recruiting the Rab5 GTPase-activating protein Msb3. J Cell Biol 201(1):97–111. https://doi.org/10.1083/jcb.201210038
Johnson DE, Ostrowski P, Jaumouille V, Grinstein S (2016) The position of lysosomes within the cell determines their luminal pH. J Cell Biol 212(6):677–692. https://doi.org/10.1083/jcb.201507112
Jongsma ML, Berlin I, Wijdeven RH, Janssen L, Janssen GM, Garstka MA, Janssen H, Mensink M, van Veelen PA, Spaapen RM, Neefjes J (2016) An ER-associated pathway defines endosomal architecture for controlled cargo transport. Cell 166(1):152–166. https://doi.org/10.1016/j.cell.2016.05.078
Kalaidzidis I, Miaczynska M, Brewinska-Olchowik M, Hupalowska A, Ferguson C, Parton RG, Kalaidzidis Y, Zerial M (2015) APPL endosomes are not obligatory endocytic intermediates but act as stable cargo-sorting compartments. J Cell Biol 211(1):123–144. https://doi.org/10.1083/jcb.201311117
Kalin S, Hirschmann DT, Buser DP, Spiess M (2015) Rabaptin5 is recruited to endosomes by Rab4 and Rabex5 to regulate endosome maturation. J Cell Sci 128(22):4126–4137. https://doi.org/10.1242/jcs.174664
Kamalesh K, Trivedi D, Toscano S, Sharma S, Kolay S, Raghu P (2017) Phosphatidylinositol 5-phosphate 4-kinase regulates early endosomal dynamics during clathrin-mediated endocytosis. J Cell Sci 130(13):2119–2133. https://doi.org/10.1242/jcs.202259
Kane PM (2006) The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol Mol Biol Rev MMBR 70(1):177–191. https://doi.org/10.1128/MMBR.70.1.177-191.2006
Karim MA, Brett CL (2017) The Na(+)(K(+))/H(+) exchanger Nhx1 controls multivesicular body-vacuolar lysosome fusion. Mol Biol Cell. https://doi.org/10.1091/mbc.E17-08-0496
Kasmapour B, Gronow A, Bleck CK, Hong W, Gutierrez MG (2012) Size-dependent mechanism of cargo sorting during lysosome-phagosome fusion is controlled by Rab34. Proc Natl Acad Sci USA 109(50):20485–20490. https://doi.org/10.1073/pnas.1206811109
Katzmann DJ, Stefan CJ, Babst M, Emr SD (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J Cell Biol 162(3):413–423. https://doi.org/10.1083/jcb.200302136
Ketel K, Krauss M, Nicot AS, Puchkov D, Wieffer M, Muller R, Subramanian D, Schultz C, Laporte J, Haucke V (2016) A phosphoinositide conversion mechanism for exit from endosomes. Nature 529(7586):408–412. https://doi.org/10.1038/nature16516
Kharitidi D, Apaja PM, Manteghi S, Suzuki K, Malitskaya E, Roldan A, Gingras MC, Takagi J, Lukacs GL, Pause A (2015) Interplay of endosomal pH and ligand occupancy in integrin α5β1 ubiquitination, endocytic sorting, and cell migration. Cell Rep 13(3):599–609. https://doi.org/10.1016/j.celrep.2015.09.024
Kharkwal H, Smith CG, Wilson DW (2016) Herpes simplex virus capsid localization to ESCRT-VPS4 complexes in the presence and absence of the large tegument protein UL36p. J Virol 90(16):7257–7267. https://doi.org/10.1128/JVI.00857-16
Kilpatrick BS, Eden ER, Schapira AH, Futter CE, Patel S (2013) Direct mobilisation of lysosomal Ca2+ triggers complex Ca2+ signals. J Cell Sci 126(Pt 1):60–66. https://doi.org/10.1242/jcs.118836
Kim GH, Dayam RM, Prashar A, Terebiznik M, Botelho RJ (2014) PIKfyve inhibition interferes with phagosome and endosome maturation in macrophages. Traffic 15(10):1143–1163. https://doi.org/10.1111/tra.12199
Kim HJ, Li Q, Tjon-Kon-Sang S, So I, Kiselyov K, Soyombo AA, Muallem S (2008) A novel mode of TRPML3 regulation by extracytosolic pH absent in the varitint-waddler phenotype. EMBO J 27(8):1197–1205. https://doi.org/10.1038/emboj.2008.56
Kim YM, Jung CH, Seo M, Kim EK, Park JM, Bae SS, Kim DH (2015) mTORC1 phosphorylates UVRAG to negatively regulate autophagosome and endosome maturation. Mol Cell 57(2):207–218. https://doi.org/10.1016/j.molcel.2014.11.013
King JS, Gueho A, Hagedorn M, Gopaldass N, Leuba F, Soldati T, Insall RH (2013) WASH is required for lysosomal recycling and efficient autophagic and phagocytic digestion. Mol Biol Cell 24(17):2714–2726. https://doi.org/10.1091/mbc.E13-02-0092
Kirkbride KC, Hong NH, French CL, Clark ES, Jerome WG, Weaver AM (2012) Regulation of late endosomal/lysosomal maturation and trafficking by cortactin affects Golgi morphology. Cytoskeleton 69(9):625–643. https://doi.org/10.1002/cm.21051
Kissing S, Hermsen C, Repnik U, Nesset CK, von Bargen K, Griffiths G, Ichihara A, Lee BS, Schwake M, De Brabander J, Haas A, Saftig P (2015) Vacuolar ATPase in phagosome-lysosome fusion. J Biol Chem 290(22):14166–14180. https://doi.org/10.1074/jbc.M114.628891
Kojima A, Toshima JY, Kanno C, Kawata C, Toshima J (2012) Localization and functional requirement of yeast Na+/H+ exchanger, Nhx1p, in the endocytic and protein recycling pathway. Biochem Biophys Acta 1823(2):534–543. https://doi.org/10.1016/j.bbamcr.2011.12.004
Kriegel A, Andres Z, Medzihradszky A, Kruger F, Scholl S, Delang S, Patir-Nebioglu MG, Gute G, Yang H, Murphy AS, Peer WA, Pfeiffer A, Krebs M, Lohmann JU, Schumacher K (2015) Job sharing in the endomembrane system: vacuolar acidification requires the combined activity of V-ATPase and V-PPase. Plant Cell 27(12):3383–3396. https://doi.org/10.1105/tpc.15.00733
Kummel D, Ungermann C (2014) Principles of membrane tethering and fusion in endosome and lysosome biogenesis. Curr Opin Cell Biol 29:61–66. https://doi.org/10.1016/j.ceb.2014.04.007
Kvainickas A, Jimenez-Orgaz A, Nagele H, Hu Z, Dengjel J, Steinberg F (2017) Cargo-selective SNX-BAR proteins mediate retromer trimer independent retrograde transport. J Cell Biol 216(11):3677–3693. https://doi.org/10.1083/jcb.201702137
Lakadamyali M, Rust MJ, Zhuang X (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124(5):997–1009. https://doi.org/10.1016/j.cell.2005.12.038
Law F, Seo JH, Wang Z, DeLeon JL, Bolis Y, Brown A, Zong WX, Du G, Rocheleau CE (2017) The VPS-34 PI3 kinase negatively regulates RAB-5 during endosome maturation. J Cell Sci. https://doi.org/10.1242/jcs.194746
Lawrence G, Brown CC, Flood BA, Karunakaran S, Cabrera M, Nordmann M, Ungermann C, Fratti RA (2014) Dynamic association of the PI3P-interacting Mon1-Ccz1 GEF with vacuoles is controlled through its phosphorylation by the type 1 casein kinase Yck3. Mol Biol Cell 25(10):1608–1619. https://doi.org/10.1091/mbc.E13-08-0460
Lelouvier B, Puertollano R (2011) Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway. J Biol Chem 286(11):9826–9832. https://doi.org/10.1074/jbc.M110.169185
Levin R, Grinstein S, Schlam D (2015) Phosphoinositides in phagocytosis and macropinocytosis. Biochem Biophys Acta 1851(6):805–823. https://doi.org/10.1016/j.bbalip.2014.09.005
Liegeois S, Benedetto A, Garnier JM, Schwab Y, Labouesse M (2006) The V0-ATPase mediates apical secretion of exosomes containing hedgehog-related proteins in Caenorhabditis elegans. Journal Cell Biol 173(6):949–961. https://doi.org/10.1083/jcb.200511072
Lin X, Zhang J, Chen L, Chen Y, Xu X, Hong W, Wang T (2017) Tyrosine phosphorylation of Rab7 by Src kinase. Cell Signal 35:84–94. https://doi.org/10.1016/j.cellsig.2017.03.006
Liu P, Bartz R, Zehmer JK, Ying YS, Zhu M, Serrero G, Anderson RG (2007) Rab-regulated interaction of early endosomes with lipid droplets. Biochem Biophys Acta 1773(6):784–793. https://doi.org/10.1016/j.bbamcr.2007.02.004
Liu TT, Gomez TS, Sackey BK, Billadeau DD, Burd CG (2012) Rab GTPase regulation of retromer-mediated cargo export during endosome maturation. Mol Biol Cell 23(13):2505–2515. https://doi.org/10.1091/mbc.E11-11-0915
Liu G, Sanghavi P, Bollinger KE, Perry L, Marshall B, Roon P, Tanaka T, Nakamura A, Gonsalvez GB (2015) Efficient endocytic uptake and maturation in Drosophila oocytes requires dynamitin/p50. Genetics 201(2):631–649. https://doi.org/10.1534/genetics.115.180018
Liu J, Ji Y, Zhou J, Xing D (2016) Phosphatidylinositol 3-Kinase promotes activation and vacuolar acidification and delays methyl jasmonate-induced leaf senescence. Plant Physiol 170(3):1714–1731. https://doi.org/10.1104/pp.15.00744
Liu K, Xing R, Jian Y, Gao Z, Ma X, Sun X, Li Y, Xu M, Wang X, Jing Y, Guo W, Yang C (2017) WDR91 is a Rab7 effector required for neuronal development. J Cell Biol 216(10):3307–3321. https://doi.org/10.1083/jcb.201705151
Lloyd-Evans E, Platt FM (2011) Lysosomal Ca(2+) homeostasis: role in pathogenesis of lysosomal storage diseases. Cell Calcium 50(2):200–205. https://doi.org/10.1016/j.ceca.2011.03.010
Lodge R, Descoteaux A (2005) Modulation of phagolysosome biogenesis by the lipophosphoglycan of Leishmania. Clin Immunol 114(3):256–265. https://doi.org/10.1016/j.clim.2004.07.018
Luzio JP, Bright NA, Pryor PR (2007) The role of calcium and other ions in sorting and delivery in the late endocytic pathway. Biochem Soc Trans 35(Pt 5):1088–1091. https://doi.org/10.1042/BST0351088
Luzio JP, Gray SR, Bright NA (2010) Endosome-lysosome fusion. Biochem Soc Trans 38(6):1413–1416. https://doi.org/10.1042/BST0381413
MacDonald C, Piper RC (2016) Cell surface recycling in yeast: mechanisms and machineries. Biochem Soc Trans 44(2):474–478. https://doi.org/10.1042/BST20150263
Mani M, Lee UH, Yoon NA, Kim HJ, Ko MS, Seol W, Joe Y, Chung HT, Lee BJ, Moon CH, Cho WJ, Park JW (2016) Developmentally regulated GTP-binding protein 2 coordinates Rab5 activity and transferrin recycling. Mol Biol Cell 27(2):334–348. https://doi.org/10.1091/mbc.E15-08-0558
Marchant JS, Patel S (2015) Two-pore channels at the intersection of endolysosomal membrane traffic. Biochem Soc Trans 43(3):434–441. https://doi.org/10.1042/BST20140303
Marion S, Hoffmann E, Holzer D, Le Clainche C, Martin M, Sachse M, Ganeva I, Mangeat P, Griffiths G (2011) Ezrin promotes actin assembly at the phagosome membrane and regulates phago-lysosomal fusion. Traffic 12(4):421–437. https://doi.org/10.1111/j.1600-0854.2011.01158.x
Marwaha R, Arya SB, Jagga D, Kaur H, Tuli A, Sharma M (2017) The Rab7 effector PLEKHM1 binds Arl8b to promote cargo traffic to lysosomes. J Cell Biol 216(4):1051–1070. https://doi.org/10.1083/jcb.201607085
Matsumoto R, Suzuki K, Ohya Y (2013) Organelle acidification is important for localisation of vacuolar proteins in Saccharomyces cerevisiae. Protoplasma 250(6):1283–1293. https://doi.org/10.1007/s00709-013-0510-2
Matsuo H, Chevallier J, Mayran N, Le Blanc I, Ferguson C, Faure J, Blanc NS, Matile S, Dubochet J, Sadoul R, Parton RG, Vilbois F, Gruenberg J (2004) Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303(5657):531–534. https://doi.org/10.1126/science.1092425
Mauvezin C, Nagy P, Juhasz G, Neufeld TP (2015) Autophagosome-lysosome fusion is independent of V-ATPase-mediated acidification. Nat Commun 6:7007. https://doi.org/10.1038/ncomms8007
Maxson ME, Grinstein S (2014) The vacuolar-type H(+)-ATPase at a glance—more than a proton pump. J Cell Sci 127(Pt 23):4987–4993. https://doi.org/10.1242/jcs.158550
Mayor S, Pagano RE (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8(8):603–612. https://doi.org/10.1038/nrm2216
McDermott H, Kim K (2015) Molecular dynamics at the endocytic portal and regulations of endocytic and recycling traffics. Eur J Cell Biol 94(6):235–248. https://doi.org/10.1016/j.ejcb.2015.04.003
McKnight NC, Zhong Y, Wold MS, Gong S, Phillips GR, Dou Z, Zhao Y, Heintz N, Zong WX, Yue Z (2014) Beclin 1 is required for neuron viability and regulates endosome pathways via the UVRAG-VPS34 complex. PLoS Genet 10(10):e1004626. https://doi.org/10.1371/journal.pgen.1004626
McNally KE, Faulkner R, Steinberg F, Gallon M, Ghai R, Pim D, Langton P, Pearson N, Danson CM, Nagele H, Morris LL, Singla A, Overlee BL, Heesom KJ, Sessions R, Banks L, Collins BM, Berger I, Billadeau DD, Burstein E, Cullen PJ (2017) Retriever is a multiprotein complex for retromer-independent endosomal cargo recycling. Nat Cell Biol 19(10):1214–1225. https://doi.org/10.1038/ncb3610
Medina DL, Di Paola S, Peluso I, Armani A, De Stefani D, Venditti R, Montefusco S, Scotto-Rosato A, Prezioso C, Forrester A, Settembre C, Wang W, Gao Q, Xu H, Sandri M, Rizzuto R, De Matteis MA, Ballabio A (2015) Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol 17(3):288–299. https://doi.org/10.1038/ncb3114
Menard L, Parker PJ, Kermorgant S (2014) Receptor tyrosine kinase c-Met controls the cytoskeleton from different endosomes via different pathways. Nat Commun 5:3907. https://doi.org/10.1038/ncomms4907
Merz AJ (2015) What are the roles of V-ATPases in membrane fusion? Proc Natl Acad Sci USA 112(1):8–9. https://doi.org/10.1073/pnas.1422280112
Min SH, Suzuki A, Stalker TJ, Zhao L, Wang Y, McKennan C, Riese MJ, Guzman JF, Zhang S, Lian L, Joshi R, Meng R, Seeholzer SH, Choi JK, Koretzky G, Marks MS, Abrams CS (2014) Loss of PIKfyve in platelets causes a lysosomal disease leading to inflammation and thrombosis in mice. Nat Commun 5:4691. https://doi.org/10.1038/ncomms5691
Miura E, Hasegawa T, Konno M, Suzuki M, Sugeno N, Fujikake N, Geisler S, Tabuchi M, Oshima R, Kikuchi A, Baba T, Wada K, Nagai Y, Takeda A, Aoki M (2014) VPS35 dysfunction impairs lysosomal degradation of α-synuclein and exacerbates neurotoxicity in a Drosophila model of Parkinson’s disease. Neurobiol Dis 71:1–13. https://doi.org/10.1016/j.nbd.2014.07.014
Modica G, Lefrancois S (2017) Post-translational modifications: how to modulate Rab7 functions. Small GTPases:0. https://doi.org/10.1080/21541248.2017.1387686
Modica G, Skorobogata O, Sauvageau E, Vissa A, Yip CM, Kim PK, Wurtele H, Lefrancois S (2017) Rab7 palmitoylation is required for efficient endosome-to-TGN trafficking. J Cell Sci 130(15):2579–2590. https://doi.org/10.1242/jcs.199729
Muriel O, Tomas A, Scott CC, Gruenberg J (2016) Moesin and cortactin control actin-dependent multivesicular endosome biogenesis. Mol Biol Cell 27(21):3305–3316. https://doi.org/10.1091/mbc.E15-12-0853
Nagel BM, Bechtold M, Rodriguez LG, Bogdan S (2017) Drosophila WASH is required for integrin-mediated cell adhesion, cell motility and lysosomal neutralization. J Cell Sci 130(2):344–359. https://doi.org/10.1242/jcs.193086
Nannapaneni S, Wang D, Jain S, Schroeder B, Highfill C, Reustle L, Pittsley D, Maysent A, Moulder S, McDowell R, Kim K (2010) The yeast dynamin-like protein Vps1: vps1 mutations perturb the internalization and the motility of endocytic vesicles and endosomes via disorganization of the actin cytoskeleton. Eur J Cell Biol 89(7):499–508. https://doi.org/10.1016/j.ejcb.2010.02.002
Naufer A, Hipolito VEB, Ganesan S, Prashar A, Zaremberg V, Botelho RJ, Terebiznik MR (2017) pH of endophagosomes controls association of their membranes with Vps34 and PtdIns(3)P levels. J Cell Biol. https://doi.org/10.1083/jcb.201702179
Nicot AS, Fares H, Payrastre B, Chisholm AD, Labouesse M, Laporte J (2006) The phosphoinositide kinase PIKfyve/Fab1p regulates terminal lysosome maturation in Caenorhabditis elegans. Mol Biol Cell 17(7):3062–3074. https://doi.org/10.1091/mbc.E06-12-1120
Nicot AS, Laporte J (2008) Endosomal phosphoinositides and human diseases. Traffic 9(8):1240–1249. https://doi.org/10.1111/j.1600-0854.2008.00754.x
Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M (1999) Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1(6):376–382. https://doi.org/10.1038/14075
Nordmann M, Cabrera M, Perz A, Brocker C, Ostrowicz C, Engelbrecht-Vandre S, Ungermann C (2010) The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol CB 20(18):1654–1659. https://doi.org/10.1016/j.cub.2010.08.002
Pankiv S, Alemu EA, Brech A, Bruun JA, Lamark T, Overvatn A, Bjorkoy G, 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(2):253–269. https://doi.org/10.1083/jcb.200907015
Pei G, Repnik U, Griffiths G, Gutierrez MG (2014) Identification of an immune-regulated phagosomal Rab cascade in macrophages. J Cell Sci 127(Pt 9):2071–2082. https://doi.org/10.1242/jcs.144923
Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, Wolff NC, Tran TA, Zou L, Xie XJ, Corey DR, Brugarolas J (2011) Regulation of TFEB and V-ATPases by mTORC1. EMBO J 30(16):3242–3258. https://doi.org/10.1038/emboj.2011.257
Peters LZ, Hazan R, Breker M, Schuldiner M, Ben-Aroya S (2013) Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. J Cell Biol 201(5):663–671. https://doi.org/10.1083/jcb.201211146
Piccinotti S, Kirchhausen T, Whelan SP (2013) Uptake of rabies virus into epithelial cells by clathrin-mediated endocytosis depends upon actin. J Virol 87(21):11637–11647. https://doi.org/10.1128/JVI.01648-13
Pizarro-Cerda J, Kuhbacher A, Cossart P (2015) Phosphoinositides and host-pathogen interactions. Biochem Biophys Acta 1851(6):911–918. https://doi.org/10.1016/j.bbalip.2014.09.011
Posor Y, Eichhorn-Gruenig M, Puchkov D, Schoneberg J, Ullrich A, Lampe A, Muller R, Zarbakhsh S, Gulluni F, Hirsch E, Krauss M, Schultz C, Schmoranzer J, Noe F, Haucke V (2013) Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499(7457):233–237. https://doi.org/10.1038/nature12360
Posor Y, Eichhorn-Grunig M, Haucke M (2015) Phosphoinositides in endocytosis. Biochem Biophys Acta 1851(6):794–804. https://doi.org/10.1016/j.bbalip.2014.09.014
Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141(3):497–508. https://doi.org/10.1016/j.cell.2010.03.011
Prasad H, Rao R (2015) The Na +/H + exchanger NHE6 modulates endosomal pH to control processing of amyloid precursor protein in a cell culture model of Alzheimer disease. J Biol Chem 290(9):5311–5327. https://doi.org/10.1074/jbc.M114.602219
Progida C, Bakke O (2016) Bidirectional traffic between the Golgi and the endosomes—machineries and regulation. J Cell Sci 129(21):3971–3982. https://doi.org/10.1242/jcs.185702
Progida C, Cogli L, Piro F, De Luca A, Bakke O, Bucci C (2010) Rab7b controls trafficking from endosomes to the TGN. J Cell Sci 123(Pt 9):1480–1491. https://doi.org/10.1242/jcs.051474
Purushothaman LK, Arlt H, Kuhlee A, Raunser S, Ungermann C (2017) Retromer-driven membrane tubulation separates endosomal recycling from Rab7/Ypt7-dependent fusion. Mol Biol Cell 28(6):783–791. https://doi.org/10.1091/mbc.E16-08-0582
Raiborg C, Wenzel EM, Pedersen NM, Olsvik H, Schink KO, Schultz SW, Vietri M, Nisi V, Bucci C, Brech A, Johansen T, Stenmark H (2015) Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth. Nature 520(7546):234–238. https://doi.org/10.1038/nature14359
Ramanathan HN, Zhang G, Ye Y (2013) Monoubiquitination of EEA1 regulates endosome fusion and trafficking. Cell Biosci 3(1):24. https://doi.org/10.1186/2045-3701-3-24
Rana M, Lachmann J, Ungermann C (2015) Identification of a Rab GTPase-activating protein cascade that controls recycling of the Rab5 GTPase Vps21 from the vacuole. Mol Biol Cell 26(13):2535–2549. https://doi.org/10.1091/mbc.E15-02-0062
Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122(5):735–749. https://doi.org/10.1016/j.cell.2005.06.043
Rowland AA, Chitwood PJ, Phillips MJ, Voeltz GK (2014) ER contact sites define the position and timing of endosome fission. Cell 159(5):1027–1041. https://doi.org/10.1016/j.cell.2014.10.023
Sandhoff K (2016) Neuronal sphingolipidoses: membrane lipids and sphingolipid activator proteins regulate lysosomal sphingolipid catabolism. Biochimie 130:146–151. https://doi.org/10.1016/j.biochi.2016.05.004
Sandri C, Caccavari F, Valdembri D, Camillo C, Veltel S, Santambrogio M, Lanzetti L, Bussolino F, Ivaska J, Serini G (2012) The R-Ras/RIN2/Rab5 complex controls endothelial cell adhesion and morphogenesis via active integrin endocytosis and Rac signaling. Cell Res 22(10):1479–1501. https://doi.org/10.1038/cr.2012.110
Santiago-Tirado FH, Bretscher A (2011) Membrane-trafficking sorting hubs: cooperation between PI4P and small GTPases at the trans-Golgi network. Trends Cell Biol 21(9):515–525. https://doi.org/10.1016/j.tcb.2011.05.005
Sarantis H, Grinstein S (2012) Subversion of phagocytosis for pathogen survival. Cell Host Microbe 12(4):419–431. https://doi.org/10.1016/j.chom.2012.09.001
Satoh N, Yamada H, Yamazaki O, Suzuki M, Nakamura M, Suzuki A, Ashida A, Yamamoto D, Kaku Y, Sekine T, Seki G, Horita S (2016) A pure chloride channel mutant of CLC-5 causes Dent’s disease via insufficient V-ATPase activation. Pflugers Arch 468(7):1183–1196. https://doi.org/10.1007/s00424-016-1808-7
Sautin YY, Lu M, Gaugler A, Zhang L, Gluck SL (2005) Phosphatidylinositol 3-kinase-mediated effects of glucose on vacuolar H+-ATPase assembly, translocation, and acidification of intracellular compartments in renal epithelial cells. Mol Cell Biol 25(2):575–589. https://doi.org/10.1128/MCB.25.2.575-589.2005
Scheuring D, Viotti C, Kruger F, Kunzl F, Sturm S, Bubeck J, Hillmer S, Frigerio L, Robinson DG, Pimpl P, Schumacher K (2011) Multivesicular bodies mature from the trans-Golgi network/early endosome in Arabidopsis. Plant Cell 23(9):3463–3481. https://doi.org/10.1105/tpc.111.086918
Schindler C, Chen Y, Pu J, Guo X, Bonifacino JS (2015) EARP is a multisubunit tethering complex involved in endocytic recycling. Nat Cell Biol 17(5):639–650. https://doi.org/10.1038/ncb3129
Schink KO, Raiborg C, Stenmark H (2013) Phosphatidylinositol 3-phosphate, a lipid that regulates membrane dynamics, protein sorting and cell signalling. BioEssays News Rev Mol Cell Dev Biol 35(10):900–912. https://doi.org/10.1002/bies.201300064
Schlam D, Bagshaw RD, Freeman SA, Collins RF, Pawson T, Fairn GD, Grinstein S (2015) Phosphoinositide 3-kinase enables phagocytosis of large particles by terminating actin assembly through Rac/Cdc42 GTPase-activating proteins. Nat Commun 6:8623. https://doi.org/10.1038/ncomms9623
Schmidt O, Teis D (2012) The ESCRT machinery. Current Biol CB 22(4):R116–R120. https://doi.org/10.1016/j.cub.2012.01.028
Schmitz G, Robenek H, Lohmann U, Assmann G (1985) Interaction of high density lipoproteins with cholesteryl ester-laden macrophages: biochemical and morphological characterization of cell surface receptor binding, endocytosis and resecretion of high density lipoproteins by macrophages. EMBO J 4(3):613–622
Schreij AM, Fon EA, McPherson PS (2016) Endocytic membrane trafficking and neurodegenerative disease. Cell Mol Life Sci CMLS 73(8):1529–1545. https://doi.org/10.1007/s00018-015-2105-x
Seaman MN, Harbour ME, Tattersall D, Read E, Bright N (2009) Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J Cell Sci 122(Pt 14):2371–2382. https://doi.org/10.1242/jcs.048686
Shaw JD, Hama H, Sohrabi F, DeWald DB, Wendland B (2003) PtdIns(3,5)P2 is required for delivery of endocytic cargo into the multivesicular body. Traffic 4(7):479–490
Sherr GL, LaMassa N, Li E, Phillips G, Shen CH (2017) Pah1p negatively regulates the expression of V-ATPase genes as well as vacuolar acidification. Biochem Biophys Res Commun 491(3):693–700. https://doi.org/10.1016/j.bbrc.2017.07.127
Shin HW, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, Frankel WN, Solimena M, De Camilli P, Zerial M (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 170(4):607–618. https://doi.org/10.1083/jcb.200505128
Shin D, Na W, Lee JH, Kim G, Baek J, Park SH, Choi CY, Lee S (2017) Site-specific monoubiquitination downregulates Rab5 by disrupting effector binding and guanine nucleotide conversion. eLife 6. https://doi.org/10.7554/elife.29154
Shinde SR, Maddika S (2016) PTEN modulates EGFR late endocytic trafficking and degradation by dephosphorylating Rab7. Nat Commun 7:10689. https://doi.org/10.1038/ncomms10689
Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP (2008) Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell 15(2):209–219. https://doi.org/10.1016/j.devcel.2008.06.012
Simonetti B, Danson CM, Heesom KJ, Cullen PJ (2017) Sequence-dependent cargo recognition by SNX-BARs mediates retromer-independent transport of CI-MPR. J Cell Biol 216(11):3695–3712. https://doi.org/10.1083/jcb.201703015
Smardon AM, Diab HI, Tarsio M, Diakov TT, Nasab ND, West RW, Kane PM (2014) The RAVE complex is an isoform-specific V-ATPase assembly factor in yeast. Mol Biol Cell 25(3):356–367. https://doi.org/10.1091/mbc.E13-05-0231
Smith GA, Howell GJ, Phillips C, Muench SP, Ponnambalam S, Harrison MA (2016) Extracellular and luminal pH regulation by vacuolar H+-ATPase isoform expression and targeting to the plasma membrane and endosomes. J Biol Chem 291(16):8500–8515. https://doi.org/10.1074/jbc.M116.723395
Sobota JA, Back N, Eipper BA, Mains RE (2009) Inhibitors of the V0 subunit of the vacuolar H+-ATPase prevent segregation of lysosomal- and secretory-pathway proteins. J Cell Sci 122(Pt 19):3542–3553. https://doi.org/10.1242/jcs.034298
Solinger JA, Spang A (2013) Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J 280(12):2743–2757. https://doi.org/10.1111/febs.12151
Solinger JA, Spang A (2014) Loss of the Sec1/Munc18-family proteins VPS-33.2 and VPS-33.1 bypasses a block in endosome maturation in Caenorhabditis elegans. Mol Biol Cell 25(24):3909–3925. https://doi.org/10.1091/mbc.E13-12-0710
Soria FN, Pampliega O, Bourdenx M, Meissner WG, Bezard E, Dehay B (2017) Exosomes, an unmasked culprit in neurodegenerative diseases. Front Neurosci 11:26. https://doi.org/10.3389/fnins.2017.00026
Spang A (2015) The road not taken: less traveled roads from the TGN to the plasma membrane. Membranes 5(1):84–98. https://doi.org/10.3390/membranes5010084
Spang A (2016) Membrane tethering complexes in the endosomal system. Front Cell Dev Biol 4:35. https://doi.org/10.3389/fcell.2016.00035
Sreelatha A, Bennett TL, Carpinone EM, O’Brien KM, Jordan KD, Burdette DL, Orth K, Starai VJ (2015) Vibrio effector protein VopQ inhibits fusion of V-ATPase-containing membranes. Proc Natl Acad Sci USA 112(1):100–105. https://doi.org/10.1073/pnas.1413764111
Stasyk T, Huber LA (2016) Spatio-temporal parameters of endosomal signaling in cancer: implications for new treatment options. J Cell Biochem 117(4):836–843. https://doi.org/10.1002/jcb.25418
Stransky LA, Forgac M (2015) Amino acid availability modulates vacuolar H+-ATPase assembly. J Biol Chem 290(45):27360–27369. https://doi.org/10.1074/jbc.M115.659128
Sun-Wada GH, Tabata H, Kawamura N, Aoyama M, Wada Y (2009) Direct recruitment of H+-ATPase from lysosomes for phagosomal acidification. J Cell Sci 122(Pt 14):2504–2513. https://doi.org/10.1242/jcs.050443
Sun Q, Westphal W, Wong KN, Tan I, Zhong Q (2010) Rubicon controls endosome maturation as a Rab7 effector. Proc Natl Acad Sci USA 107(45):19338–19343. https://doi.org/10.1073/pnas.1010554107
Szatmari Z, Kis V, Lippai M, Hegedus K, Farago T, Lorincz P, Tanaka T, Juhasz G, Sass M (2014) Rab11 facilitates cross-talk between autophagy and endosomal pathway through regulation of Hook localization. Mol Biol Cell 25(4):522–531. https://doi.org/10.1091/mbc.E13-10-0574
Takatori S, Tatematsu T, Cheng J, Matsumoto J, Akano T, Fujimoto T (2016) Phosphatidylinositol 3,5-bisphosphate-rich membrane domains in endosomes and lysosomes. Traffic 17(2):154–167. https://doi.org/10.1111/tra.12346
Tan X, Thapa N, Choi S, Anderson RA (2015) Emerging roles of PtdIns(4,5)P2–beyond the plasma membrane. J Cell Sci 128(22):4047–4056. https://doi.org/10.1242/jcs.175208
Tang BL (2016) Rab, Arf, and Arl-regulated membrane traffic in cortical neuron migration. J Cell Physiol 231(7):1417–1423. https://doi.org/10.1002/jcp.25261
Teixeira V, Medeiros TC, Vilaca R, Ferreira J, Moradas-Ferreira P, Costa V (2016) Ceramide signaling targets the PP2A-like protein phosphatase Sit4p to impair vacuolar function, vesicular trafficking and autophagy in Isc1p deficient cells. Biochem Biophys Acta 1861(1):21–33. https://doi.org/10.1016/j.bbalip.2015.10.004
Tornieri K, Zlatic SA, Mullin AP, Werner E, Harrison R, L’Hernault SW, Faundez V (2013) Vps33b pathogenic mutations preferentially affect VIPAS39/SPE-39-positive endosomes. Hum Mol Genet 22(25):5215–5228. https://doi.org/10.1093/hmg/ddt378
Urbanska A, Sadowski L, Kalaidzidis Y, Miaczynska M (2011) Biochemical characterization of APPL endosomes: the role of annexin A2 in APPL membrane recruitment. Traffic 12(9):1227–1241. https://doi.org/10.1111/j.1600-0854.2011.01226.x
Vale-Costa S, Amorim MJ (2016) Recycling endosomes and viral infection. Viruses 8(3):64. https://doi.org/10.3390/v8030064
van der Kant R, Neefjes J (2014) Small regulators, major consequences—Ca(2)(+) and cholesterol at the endosome-ER interface. J Cell Sci 127(Pt 5):929–938. https://doi.org/10.1242/jcs.137539
van der Kant R, Jonker CT, Wijdeven RH, Bakker J, Janssen L, Klumperman J, Neefjes J (2015) Characterization of the mammalian CORVET and HOPS Complexes and their modular restructuring for endosome specificity. J Biol Chem 290(51):30280–30290. https://doi.org/10.1074/jbc.M115.688440
van Deurs B, Holm PK, Sandvig K (1996) Inhibition of the vacuolar H(+)-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in HEp-2 cells. Eur J Cell Biol 69(4):343–350
van Weering JR, Verkade P, Cullen PJ (2012) SNX-BAR-mediated endosome tubulation is co-ordinated with endosome maturation. Traffic 13(1):94–107. https://doi.org/10.1111/j.1600-0854.2011.01297.x
Vieira OV, Bucci C, Harrison RE, Trimble WS, Lanzetti L, Gruenberg J, Schreiber AD, Stahl PD, Grinstein S (2003) Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol Cell Biol 23(7):2501–2514
Villasenor R, Kalaidzidis Y, Zerial M (2016) Signal processing by the endosomal system. Curr Opin Cell Biol 39:53–60. https://doi.org/10.1016/j.ceb.2016.02.002
Wang C, Wang Y, Li Y, Bodemann B, Zhao T, Ma X, Huang G, Hu Z, DeBerardinis RJ, White MA, Gao J (2015) A nanobuffer reporter library for fine-scale imaging and perturbation of endocytic organelles. Nat Commun 6:8524. https://doi.org/10.1038/ncomms9524
Waugh MG (2015) PIPs in neurological diseases. Biochem Biophys Acta 1851(8):1066–1082. https://doi.org/10.1016/j.bbalip.2015.02.002
Williamson WR, Hiesinger PR (2010) On the role of v-ATPase V0a1-dependent degradation in Alzheimer disease. Communicative Integr Biol 3(6):604–607. https://doi.org/10.4161/cib.3.6.13364
Wong D, Bach H, Sun J, Hmama Z, Av-Gay Y (2011) Mycobacterium tuberculosis protein tyrosine phosphatase (PtpA) excludes host vacuolar-H+-ATPase to inhibit phagosome acidification. Proc Natl Acad Sci USA 108(48):19371–19376. https://doi.org/10.1073/pnas.1109201108
Xinhan L, Matsushita M, Numaza M, Taguchi A, Mitsui K, Kanazawa H (2011) Na+/H+ exchanger isoform 6 (NHE6/SLC9A6) is involved in clathrin-dependent endocytosis of transferrin. Am J Physiol Cell Physiol 301(6):C1431–C1444. https://doi.org/10.1152/ajpcell.00154.2011
Xu T, Forgac M (2001) Microtubules are involved in glucose-dependent dissociation of the yeast vacuolar [H+]-ATPase in vivo. J Biol Chem 276(27):24855–24861. https://doi.org/10.1074/jbc.M100637200
Xu L, Shen X, Bryan A, Banga S, Swanson MS, Luo ZQ (2010) Inhibition of host vacuolar H+ -ATPase activity by a Legionella pneumophila effector. PLoS Pathog 6(3):e1000822. https://doi.org/10.1371/journal.ppat.1000822
Yasuda S, Morishita S, Fujita A, Nanao T, Wada N, Waguri S, Schiavo G, Fukuda M, Nakamura T (2016) Mon1-Ccz1 activates Rab7 only on late endosomes and dissociates from the lysosome in mammalian cells. J Cell Sci 129(2):329–340. https://doi.org/10.1242/jcs.178095
Yousefian J, Troost T, Grawe F, Sasamura T, Fortini M, Klein T (2013) Dmon1 controls recruitment of Rab7 to maturing endosomes in Drosophila. J Cell Sci 126(Pt 7):1583–1594. https://doi.org/10.1242/jcs.114934
Zajac AL, Goldman YE, Holzbaur EL, Ostap EM (2013) Local cytoskeletal and organelle interactions impact molecular-motor- driven early endosomal trafficking. Current Biol CB 23(13):1173–1180. https://doi.org/10.1016/j.cub.2013.05.015
Zeigerer A, Gilleron J, Bogorad RL, Marsico G, Nonaka H, Seifert S, Epstein-Barash H, Kuchimanchi S, Peng CG, Ruda VM, Del Conte-Zerial P, Hengstler JG, Kalaidzidis Y, Koteliansky V, Zerial M (2012) Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485(7399):465–470. https://doi.org/10.1038/nature11133
Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2(2):107–117. https://doi.org/10.1038/35052055
Zhou A, Bu Y, Takano T, Zhang X, Liu S (2016) Conserved V-ATPase c subunit plays a role in plant growth by influencing V-ATPase-dependent endosomal trafficking. Plant Biotechnol J 14(1):271–283. https://doi.org/10.1111/pbi.12381
Zhu H, Liang Z, Li G (2009) Rabex-5 is a Rab22 effector and mediates a Rab22-Rab5 signaling cascade in endocytosis. Mol Biol Cell 20(22):4720–4729. https://doi.org/10.1091/mbc.E09-06-0453
Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM (2011) mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 334(6056):678–683. https://doi.org/10.1126/science.1207056
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Podinovskaia, M., Spang, A. (2018). The Endosomal Network: Mediators and Regulators of Endosome Maturation. In: Lamaze, C., Prior, I. (eds) Endocytosis and Signaling. Progress in Molecular and Subcellular Biology, vol 57. Springer, Cham. https://doi.org/10.1007/978-3-319-96704-2_1
Download citation
DOI: https://doi.org/10.1007/978-3-319-96704-2_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-96703-5
Online ISBN: 978-3-319-96704-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)