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Integration of the Endocytic System into the Network of Cellular Functions

  • Noga Budick-Harmelin
  • Marta Miaczynska
Chapter
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 57)

Abstract

Maintenance of physiologic cellular functions and homeostasis requires highly coordinated interactions between different cellular compartments. In this regard, the endocytic system, which plays a key role in cargo internalization and trafficking within the cell, participates in upkeep of intracellular dynamics, while communicating with multiple organelles. This chapter will discuss the function of endosomes from a standpoint of cellular integration. We will present examples of different types of interactions between endosomes and other cellular compartments, such as the endoplasmic reticulum (ER), mitochondria, the plasma membrane (PM), and the nuclear envelope. In addition, we will describe the incorporation of endocytic components, such as endosomal sorting complexes required for transport (ESCRT) proteins and Rab small GTPases, into cellular processes that operate outside of the endolysosomal pathway. The significance of endosomal interactions for processes such as signaling regulation, intracellular trafficking, organelle dynamics, metabolic control, and homeostatic responses will be reviewed. Accumulating data indicate that beyond its involvement in cargo transport, the endocytic pathway is comprehensively integrated into other systems of the cell and plays multiple roles in the complex net of cellular functions.

References

  1. Alonso YAM, Migliano SM, Teis D (2016) ESCRT-III and Vps4: a dynamic multipurpose tool for membrane budding and scission. FEBS J 283(18):3288–3302.  https://doi.org/10.1111/febs.13688CrossRefGoogle Scholar
  2. Alpy F, Rousseau A, Schwab Y, Legueux F, Stoll I, Wendling C, Spiegelhalter C, Kessler P, Mathelin C, Rio MC, Levine TP, Tomasetto C (2013) STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER. J Cell Sci 126(Pt 23):5500–5512.  https://doi.org/10.1242/jcs.139295 jcs.139295 [pii]CrossRefPubMedGoogle Scholar
  3. Antonescu CN, McGraw TE, Klip A (2014) Reciprocal regulation of endocytosis and metabolism. Cold Spring Harb Perspect Biol 6(7):a016964.  https://doi.org/10.1101/cshperspect.a016964 a016964, /7/a016964 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barth JM, Kohler K (2014) How to take autophagy and endocytosis up a notch. Biomed Res Int 2014:960803.  https://doi.org/10.1155/2014/960803CrossRefPubMedPubMedCentralGoogle Scholar
  5. Berg TO, Fengsrud M, Stromhaug PE, Berg T, Seglen PO (1998) Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 273(34):21883–21892CrossRefPubMedGoogle Scholar
  6. Biazik J, Yla-Anttila P, Vihinen H, Jokitalo E, Eskelinen EL (2015) Ultrastructural relationship of the phagophore with surrounding organelles. Autophagy 11(3):439–451.  https://doi.org/10.1080/15548627.2015.1017178CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bogan JS (2012) Regulation of glucose transporter translocation in health and diabetes. Annu Rev Biochem 81:507–532.  https://doi.org/10.1146/annurev-biochem-060109-094246CrossRefPubMedGoogle Scholar
  8. Brahimi-Horn MC, Lacas-Gervais S, Adaixo R, Ilc K, Rouleau M, Notte A, Dieu M, Michiels C, Voeltzel T, Maguer-Satta V, Pelletier J, Ilie M, Hofman P, Manoury B, Schmidt A, Hiller S, Pouyssegur J, Mazure NM (2015) Local mitochondrial-endolysosomal microfusion cleaves voltage-dependent anion channel 1 to promote survival in hypoxia. Mol Cell Biol 35(9):1491–1505.  https://doi.org/10.1128/MCB.01402-14 MCB.01402-14 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brewer PD, Habtemichael EN, Romenskaia I, Coster AC, Mastick CC (2016a) Rab14 limits the sorting of Glut4 from endosomes into insulin-sensitive regulated secretory compartments in adipocytes. Biochem J 473(10):1315–1327.  https://doi.org/10.1042/BCJ20160020 BCJ20160020 [pii]CrossRefPubMedGoogle Scholar
  10. Brewer PD, Habtemichael EN, Romenskaia I, Mastick CC, Coster AC (2016b) Glut4 is sorted from a Rab10 GTPase-independent constitutive recycling pathway into a highly insulin-responsive Rab10 GTPase-dependent sequestration pathway after adipocyte differentiation. J Biol Chem 291(2):773–789.  https://doi.org/10.1074/jbc.M115.694919 M115.694919 [pii]CrossRefPubMedGoogle Scholar
  11. Calore F, Genisset C, Casellato A, Rossato M, Codolo G, Esposti MD, Scorrano L, de Bernard M (2010) Endosome-mitochondria juxtaposition during apoptosis induced by H. pylori VacA. Cell Death Differ 17(11):1707–1716.  https://doi.org/10.1038/cdd.2010.42 cdd201042 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cendrowski J, Maminska A, Miaczynska M (2016) Endocytic regulation of cytokine receptor signaling. Cytokine Growth Factor Rev.  https://doi.org/10.1016/j.cytogfr.2016.07.002 S1359-6101(16)30086-7 [pii]CrossRefPubMedGoogle Scholar
  13. Chan SN, Tang BL (2013) Location and membrane sources for autophagosome formation—from ER-mitochondria contact sites to Golgi-endosome-derived carriers. Mol Membr Biol 30(8):394–402.  https://doi.org/10.3109/09687688.2013.850178CrossRefPubMedGoogle Scholar
  14. Charman M, Kennedy BE, Osborne N, Karten B (2010) MLN64 mediates egress of cholesterol from endosomes to mitochondria in the absence of functional Niemann-Pick Type C1 protein. J Lipid Res 51(5):1023–1034.  https://doi.org/10.1194/jlr.M002345 jlr.M002345 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chen Y, Wang Y, Zhang J, Deng Y, Jiang L, Song E, Wu XS, Hammer JA, Xu T, Lippincott-Schwartz J (2012) Rab10 and myosin-Va mediate insulin-stimulated GLUT4 storage vesicle translocation in adipocytes. J Cell Biol 198(4):545–560.  https://doi.org/10.1083/jcb.201111091 jcb.201111091 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chen Y, Zhou F, Zou S, Yu S, Li S, Li D, Song J, Li H, He Z, Hu B, Bjorn LO, Lipatova Z, Liang Y, Xie Z, Segev N (2014) A Vps21 endocytic module regulates autophagy. Mol Biol Cell 25(20):3166–3177.  https://doi.org/10.1091/mbc.E14-04-0917 mbc.E14-04-0917 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chevallier J, Chamoun Z, Jiang G, Prestwich G, Sakai N, Matile S, Parton RG, Gruenberg J (2008) Lysobisphosphatidic acid controls endosomal cholesterol levels. J Biol Chem 283(41):27871–27880.  https://doi.org/10.1074/jbc.M801463200 M801463200 [pii]CrossRefPubMedGoogle Scholar
  18. Christ L, Raiborg C, Wenzel EM, Campsteijn C, Stenmark H (2016) Cellular functions and molecular mechanisms of the ESCRT membrane-scission machinery. Trends Biochem Sci.  https://doi.org/10.1016/j.tibs.2016.08.016 S0968-0004(16)30146-3 [pii]CrossRefPubMedGoogle Scholar
  19. 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(2):291–306.  https://doi.org/10.1016/j.cell.2015.02.019 10.1016/j.cell.2015.02.019CrossRefPubMedGoogle Scholar
  20. Chua CE, Tang BL (2015) Role of Rab GTPases and their interacting proteins in mediating metabolic signalling and regulation. Cell Mol Life Sci 72(12):2289–2304.  https://doi.org/10.1007/s00018-015-1862-xCrossRefPubMedGoogle Scholar
  21. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, Habermann B, Buchholz F, Henschel R, Mueller MS, Nagel WE, Fava E, Kalaidzidis Y, Zerial M (2010) Systems survey of endocytosis by multiparametric image analysis. Nature 464(7286):243–249.  https://doi.org/10.1038/nature08779 nature08779 [pii]CrossRefPubMedGoogle Scholar
  22. Daniele T, Schiaffino MV (2016) Lipid transfer and metabolism across the endolysosomal-mitochondrial boundary. Biochim Biophys Acta 1861(8 Pt B):880–894.  https://doi.org/10.1016/j.bbalip.2016.02.001 S1388-1981(16)30020-8 [pii]
  23. Das A, Nag S, Mason AB, Barroso MM (2016) Endosome-mitochondria interactions are modulated by iron release from transferrin. J Cell Biol 214(7):831–845.  https://doi.org/10.1083/jcb.201602069 jcb.201602069 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  24. Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K, Lammerding J (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352(6283):353–358.  https://doi.org/10.1126/science.aad7297 science.aad7297 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  25. Djeddi A, Michelet X, Culetto E, Alberti A, Barois N, Legouis R (2012) Induction of autophagy in ESCRT mutants is an adaptive response for cell survival in C. elegans. J Cell Sci 125(Pt 3):685–694.  https://doi.org/10.1242/jcs.091702 125/3/685 [pii]
  26. Eden ER (2016) The formation and function of ER-endosome membrane contact sites. Biochim Biophys Acta 1861(8 Pt B):874–879.  https://doi.org/10.1016/j.bbalip.2016.01.020 S1388-1981(16)30019-1 [pii]
  27. Eden ER, White IJ, Tsapara A, Futter CE (2010) Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat Cell Biol 12(3):267–272.  https://doi.org/10.1038/ncb2026 ncb2026 [pii]CrossRefPubMedGoogle Scholar
  28. Eden ER, Sanchez-Heras E, Tsapara A, Sobota A, Levine TP, Futter CE (2016) Annexin A1 tethers membrane contact sites that mediate ER to endosome cholesterol transport. Dev Cell 37(5):473–483.  https://doi.org/10.1016/j.devcel.2016.05.005 S1534-5807(16)30282-9 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  29. Edgar JR, Manna PT, Nishimura S, Banting G, Robinson MS (2016) Tetherin is an exosomal tether. Elife 5.  https://doi.org/10.7554/elife.17180 e17180 [pii]
  30. 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 S1534-5807(14)00378-5 [pii]CrossRefPubMedGoogle Scholar
  31. Esk C, Chen CY, Johannes L, Brodsky FM (2010) The clathrin heavy chain isoform CHC22 functions in a novel endosomal sorting step. J Cell Biol 188(1):131–144.  https://doi.org/10.1083/jcb.200908057 jcb.200908057 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  32. Fader CM, Colombo MI (2009) Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16(1):70–78.  https://doi.org/10.1038/cdd.2008.168 cdd2008168 [pii]CrossRefPubMedGoogle Scholar
  33. Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerod L, Fisher EM, Isaacs A, Brech A, Stenmark H, Simonsen A (2007) Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol 179(3):485–500.  https://doi.org/10.1083/jcb.200702115 jcb.200702115 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 mbc.E12-10-0733 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ganley IG, Wong PM, Gammoh N, Jiang X (2011) Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 42(6):731–743.  https://doi.org/10.1016/j.molcel.2011.04.024 S1097-2765(11)00370-4 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 e15887 [pii]
  37. Glick D, Barth S, Macleod KF (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221(1):3–12.  https://doi.org/10.1002/path.2697CrossRefPubMedPubMedCentralGoogle Scholar
  38. Haj FG, Verveer PJ, Squire A, Neel BG, Bastiaens PI (2002) Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science 295(5560):1708–1711.  https://doi.org/10.1126/science.1067566CrossRefPubMedGoogle Scholar
  39. Hamdi A, Roshan TM, Kahawita TM, Mason AB, Sheftel AD, Ponka P (2016) Erythroid cell mitochondria receive endosomal iron by a “kiss-and-run” mechanism. Biochim Biophys Acta 1863(12):2859–2867.  https://doi.org/10.1016/j.bbamcr.2016.09.008 S0167-4889(16)30228-2 [pii]CrossRefPubMedGoogle Scholar
  40. 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 ncomms14050 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  41. Henne WM (2016) Organelle remodeling at membrane contact sites. J Struct Biol 196(1):15–19.  https://doi.org/10.1016/j.jsb.2016.05.003 S1047-8477(16)30088-0 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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 S1534-5807(14)00377-3 [pii]CrossRefPubMedGoogle Scholar
  43. Huberts DH, van der Klei IJ (2010) Moonlighting proteins: an intriguing mode of multitasking. Biochim Biophys Acta 1803(4):520–525.  https://doi.org/10.1016/j.bbamcr.2010.01.022CrossRefPubMedGoogle Scholar
  44. Ikonen E (2008) Cellular cholesterol trafficking and compartmentalization. Nat Rev Mol Cell Biol 9(2):125–138.  https://doi.org/10.1038/nrm2336 nrm2336 [pii]CrossRefPubMedGoogle Scholar
  45. Imai K, Hao F, Fujita N, Tsuji Y, Oe Y, Araki Y, Hamasaki M, Noda T, Yoshimori T (2016) Atg9A trafficking through the recycling endosomes is required for autophagosome formation. J Cell Sci 129(20):3781–3791.  https://doi.org/10.1242/jcs.196196 jcs.196196 [pii]CrossRefPubMedGoogle Scholar
  46. Ishikura S, Klip A (2008) Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am J Physiol Cell Physiol 295(4):C1016–C1025.  https://doi.org/10.1152/ajpcell.00277.2008 00277.2008 [pii]CrossRefPubMedGoogle Scholar
  47. Jeffery CJ (1999) Moonlighting proteins. Trends Biochem Sci 24(1):8–11CrossRefPubMedGoogle Scholar
  48. Jiang P, Nishimura T, Sakamaki Y, Itakura E, Hatta T, Natsume T, Mizushima N (2014) The HOPS complex mediates autophagosome-lysosome fusion through interaction with syntaxin 17. Mol Biol Cell 25(8):1327–1337.  https://doi.org/10.1091/mbc.E13-08-0447 mbc.E13-08-0447 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  49. Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, Perez F (2014) ESCRT machinery is required for plasma membrane repair. Science 343(6174):1247136.  https://doi.org/10.1126/science.1247136 science.1247136 [pii]CrossRefPubMedGoogle Scholar
  50. Kandror KV, Pilch PF (2011) The sugar is sIRVed: sorting Glut4 and its fellow travelers. Traffic 12(6):665–671.  https://doi.org/10.1111/j.1600-0854.2011.01175.xCrossRefPubMedGoogle Scholar
  51. 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 jcs.118836 [pii]CrossRefPubMedGoogle Scholar
  52. Korolchuk VI, Saiki S, Lichtenberg M, Siddiqi FH, Roberts EA, Imarisio S, Jahreiss L, Sarkar S, Futter M, Menzies FM, O’Kane CJ, Deretic V, Rubinsztein DC (2011) Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol 13(4):453–460.  https://doi.org/10.1038/ncb2204 ncb2204 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kozik P, Hodson NA, Sahlender DA, Simecek N, Soromani C, Wu J, Collinson LM, Robinson MS (2013) A human genome-wide screen for regulators of clathrin-coated vesicle formation reveals an unexpected role for the V-ATPase. Nat Cell Biol 15(1):50–60.  https://doi.org/10.1038/ncb2652 ncb2652 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lam AK, Galione A (2013) The endoplasmic reticulum and junctional membrane communication during calcium signaling. Biochim Biophys Acta 1833(11):2542–2559.  https://doi.org/10.1016/j.bbamcr.2013.06.004 S0167-4889(13)00227-9 [pii]CrossRefPubMedGoogle Scholar
  55. Lang MJ, Martinez-Marquez JY, Prosser DC, Ganser LR, Buelto D, Wendland B, Duncan MC (2014) Glucose starvation inhibits autophagy via vacuolar hydrolysis and induces plasma membrane internalization by down-regulating recycling. J Biol Chem 289(24):16736–16747.  https://doi.org/10.1074/jbc.M113.525782 M113.525782 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lee JA, Beigneux A, Ahmad ST, Young SG, Gao FB (2007) ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr Biol 17(18):1561–1567.  https://doi.org/10.1016/j.cub.2007.07.029 S0960-9822(07)01707-1 [pii]CrossRefPubMedGoogle Scholar
  57. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C, Jung JU (2008) Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10(7):776–787.  https://doi.org/10.1038/ncb1740 ncb1740 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  58. Lim CY, Zoncu R (2016) The lysosome as a command-and-control center for cellular metabolism. J Cell Biol 214(6):653–664.  https://doi.org/10.1083/jcb.201607005CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lindmo K, Simonsen A, Brech A, Finley K, Rusten TE, Stenmark H (2006) A dual function for deep orange in programmed autophagy in the Drosophila melanogaster fat body. Exp Cell Res 312(11):2018–2027.  https://doi.org/10.1016/j.yexcr.2006.03.002 S0014-4827(06)00088-7 [pii]CrossRefPubMedGoogle Scholar
  60. Liou W, Geuze HJ, Geelen MJ, Slot JW (1997) The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J Cell Biol 136(1):61–70CrossRefPubMedPubMedCentralGoogle Scholar
  61. Longatti A, Lamb CA, Razi M, Yoshimura S, Barr FA, Tooze SA (2012) TBC1D14 regulates autophagosome formation via Rab11- and ULK1-positive recycling endosomes. J Cell Biol 197(5):659–675.  https://doi.org/10.1083/jcb.201111079 jcb.201111079 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  62. Lopez Sanjurjo CI, Tovey SC, Taylor CW (2014) Rapid recycling of Ca2+ between IP3-sensitive stores and lysosomes. PLoS ONE 9(10):e111275.  https://doi.org/10.1371/journal.pone.0111275 PONE-D-14-31104 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  63. Lopez-Sanjurjo CI, Tovey SC, Prole DL, Taylor CW (2013) Lysosomes shape Ins(1,4,5) P3-evoked Ca2+ signals by selectively sequestering Ca2+ released from the endoplasmic reticulum. J Cell Sci 126(Pt 1):289–300.  https://doi.org/10.1242/jcs.116103 jcs.116103 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  64. Luo J, Jiang L, Yang H, Song BL (2017) Routes and mechanisms of post-endosomal cholesterol trafficking: a story that never ends. Traffic.  https://doi.org/10.1111/tra.12471CrossRefPubMedGoogle Scholar
  65. Majumder P, Chakrabarti O (2015) Mahogunin regulates fusion between amphisomes/MVBs and lysosomes via ubiquitination of TSG101. Cell Death Dis 6:e1970.  https://doi.org/10.1038/cddis.2015.257 cddis2015257 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  66. Matheoud D, Sugiura A, Bellemare-Pelletier A, Laplante A, Rondeau C, Chemali M, Fazel A, Bergeron JJ, Trudeau LE, Burelle Y, Gagnon E, McBride HM, Desjardins M (2016) Parkinson’s disease-related proteins PINK1 and Parkin repress mitochondrial antigen presentation. Cell 166(2):314–327.  https://doi.org/10.1016/j.cell.2016.05.039 S0092-8674(16)30590-6 [pii]CrossRefPubMedGoogle Scholar
  67. McLelland GL, Soubannier V, Chen CX, McBride HM, Fon EA (2014) Parkin and PINK1 function in a vesicular trafficking pathway regulating mitochondrial quality control. EMBO J 33(4):282–295.  https://doi.org/10.1002/embj.201385902 embj.201385902 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  68. McLelland GL, Lee SA, McBride HM, Fon EA (2016) Syntaxin-17 delivers PINK1/parkin-dependent mitochondrial vesicles to the endolysosomal system. J Cell Biol 214(3):275–291.  https://doi.org/10.1083/jcb.201603105 jcb.201603105 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  69. Morgan AJ, Davis LC, Wagner SK, Lewis AM, Parrington J, Churchill GC, Galione A (2013) Bidirectional Ca2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J Cell Biol 200(6):789–805.  https://doi.org/10.1083/jcb.201204078 jcb.201204078 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  70. Muller M, Schmidt O, Angelova M, Faserl K, Weys S, Kremser L, Pfaffenwimmer T, Dalik T, Kraft C, Trajanoski Z, Lindner H, Teis D (2015) The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation. Elife 4:e07736.  https://doi.org/10.7554/eLife.07736CrossRefPubMedPubMedCentralGoogle Scholar
  71. Muretta JM, Romenskaia I, Mastick CC (2008) Insulin releases Glut4 from static storage compartments into cycling endosomes and increases the rate constant for Glut4 exocytosis. J Biol Chem 283(1):311–323.  https://doi.org/10.1074/jbc.M705756200 M705756200 [pii]CrossRefPubMedGoogle Scholar
  72. Murrow L, Malhotra R, Debnath J (2015) ATG12-ATG3 interacts with Alix to promote basal autophagic flux and late endosome function. Nat Cell Biol 17(3):300–310.  https://doi.org/10.1038/ncb3112 ncb3112 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  73. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015) ESCRT-III controls nuclear envelope reformation. Nature 522(7555):236–239.  https://doi.org/10.1038/nature14503 nature14503 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  74. Oshima R, Hasegawa T, Tamai K, Sugeno N, Yoshida S, Kobayashi J, Kikuchi A, Baba T, Futatsugi A, Sato I, Satoh K, Takeda A, Aoki M, Tanaka N (2016) ESCRT-0 dysfunction compromises autophagic degradation of protein aggregates and facilitates ER stress-mediated neurodegeneration via apoptotic and necroptotic pathways. Sci Rep 6:24997.  https://doi.org/10.1038/srep24997 srep24997 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  75. Palande K, Roovers O, Gits J, Verwijmeren C, Iuchi Y, Fujii J, Neel BG, Karisch R, Tavernier J, Touw IP (2011) Peroxiredoxin-controlled G-CSF signalling at the endoplasmic reticulum-early endosome interface. J Cell Sci 124(Pt 21):3695–3705.  https://doi.org/10.1242/jcs.089656 jcs.089656 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  76. Pfisterer SG, Peranen J, Ikonen E (2016) LDL-cholesterol transport to the endoplasmic reticulum: current concepts. Curr Opin Lipidol 27(3):282–287.  https://doi.org/10.1097/MOL.0000000000000292CrossRefPubMedPubMedCentralGoogle Scholar
  77. Platta HW, Stenmark H (2011) Endocytosis and signaling. Curr Opin Cell Biol 23(4):393–403.  https://doi.org/10.1016/j.ceb.2011.03.008 S0955-0674(11)00025-1 [pii]CrossRefPubMedGoogle Scholar
  78. Popovic D, Akutsu M, Novak I, Harper JW, Behrends C, Dikic I (2012) Rab GTPase-activating proteins in autophagy: regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol Cell Biol 32(9):1733–1744.  https://doi.org/10.1128/MCB.06717-11 MCB.06717-11 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  79. Prinz WA (2014) Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J Cell Biol 205(6):759–769.  https://doi.org/10.1083/jcb.201401126 jcb.201401126 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  80. Pyrzynska B, Pilecka I, Miaczynska M (2009) Endocytic proteins in the regulation of nuclear signaling, transcription and tumorigenesis. Mol Oncol 3(4):321–338.  https://doi.org/10.1016/j.molonc.2009.06.001 S1574-7891(09)00081-7 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  81. Raab M, Gentili M, de Belly H, Thiam HR, Vargas P, Jimenez AJ, Lautenschlaeger F, Voituriez R, Lennon-Dumenil AM, Manel N, Piel M (2016) ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352(6283):359–362.  https://doi.org/10.1126/science.aad7611 science.aad7611 [pii]CrossRefPubMedGoogle Scholar
  82. Raiborg C, Wenzel EM, Pedersen NM, Olsvik H, Schink KO, Schultz SW, Vietri M, Nisi V, Bucci C, Brech A, Johansen T, Stenmark H (2015a) Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth. Nature 520(7546):234–238.  https://doi.org/10.1038/nature14359 nature14359 [pii]CrossRefPubMedGoogle Scholar
  83. Raiborg C, Wenzel EM, Stenmark H (2015b) ER-endosome contact sites: molecular compositions and functions. EMBO J 34(14):1848–1858.  https://doi.org/10.15252/embj.201591481 embj.201591481 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  84. Raiborg C, Wenzel EM, Pedersen NM, Stenmark H (2016) ER-endosome contact sites in endosome positioning and protrusion outgrowth. Biochem Soc Trans 44(2):441–446.  https://doi.org/10.1042/BST20150246 BST20150246 [pii]CrossRefPubMedGoogle Scholar
  85. Reed SE, Hodgson LR, Song S, May MT, Kelly EE, McCaffrey MW, Mastick CC, Verkade P, Tavare JM (2013) A role for Rab14 in the endocytic trafficking of GLUT4 in 3T3-L1 adipocytes. J Cell Sci 126(Pt 9):1931–1941.  https://doi.org/10.1242/jcs.104307 jcs.104307 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  86. Rocha N, Kuijl C, van der Kant R, Janssen L, Houben D, Janssen H, Zwart W, Neefjes J (2009) Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning. J Cell Biol 185(7):1209–1225.  https://doi.org/10.1083/jcb.200811005 jcb.200811005 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  87. 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 S0092-8674(14)01311-7 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  88. Rusten TE, Stenmark H (2009) How do ESCRT proteins control autophagy? J Cell Sci 122(Pt 13):2179–2183.  https://doi.org/10.1242/jcs.050021 122/13/2179 [pii]CrossRefPubMedGoogle Scholar
  89. Rusten TE, Vaccari T, Lindmo K, Rodahl LM, Nezis IP, Sem-Jacobsen C, Wendler F, Vincent JP, Brech A, Bilder D, Stenmark H (2007) ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol 17(20):1817–1825.  https://doi.org/10.1016/j.cub.2007.09.032 S0960-9822(07)01991-4 [pii]CrossRefPubMedGoogle Scholar
  90. Sheftel AD, Zhang AS, Brown C, Shirihai OS, Ponka P (2007) Direct interorganellar transfer of iron from endosome to mitochondrion. Blood 110(1):125–132.  https://doi.org/10.1182/blood-2007-01-068148 blood-2007-01-068148 [pii]CrossRefPubMedGoogle Scholar
  91. Soubannier V, Rippstein P, Kaufman BA, Shoubridge EA, McBride HM (2012) Reconstitution of mitochondria derived vesicle formation demonstrates selective enrichment of oxidized cargo. PLoS ONE 7(12):e52830.  https://doi.org/10.1371/journal.pone.0052830 PONE-D-12-27184 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  92. Steinbusch LK, Wijnen W, Schwenk RW, Coumans WA, Hoebers NT, Ouwens DM, Diamant M, Bonen A, Glatz JF, Luiken JJ (2010) Differential regulation of cardiac glucose and fatty acid uptake by endosomal pH and actin filaments. Am J Physiol Cell Physiol 298(6):C1549–C1559.  https://doi.org/10.1152/ajpcell.00334.2009 ajpcell.00334.2009 [pii]CrossRefPubMedGoogle Scholar
  93. Stuible M, Abella JV, Feldhammer M, Nossov M, Sangwan V, Blagoev B, Park M, Tremblay ML (2010) PTP1B targets the endosomal sorting machinery: dephosphorylation of regulatory sites on the endosomal sorting complex required for transport component STAM2. J Biol Chem 285(31):23899–23907.  https://doi.org/10.1074/jbc.M110.115295 M110.115295 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  94. Sun Y, Bilan PJ, Liu Z, Klip A (2010) Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc Natl Acad Sci U S A 107(46):19909–19914.  https://doi.org/10.1073/pnas.1009523107 1009523107 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  95. Sun Y, Chiu TT, Foley KP, Bilan PJ, Klip A (2014) Myosin Va mediates Rab8A-regulated GLUT4 vesicle exocytosis in insulin-stimulated muscle cells. Mol Biol Cell 25(7):1159–1170.  https://doi.org/10.1091/mbc.E13-08-0493 mbc.E13-08-0493 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  96. Sun Y, Jaldin-Fincati J, Liu Z, Bilan PJ, Klip A (2016) A complex of Rab13 with MICAL-L2 and alpha-actinin-4 is essential for insulin-dependent GLUT4 exocytosis. Mol Biol Cell 27(1):75–89.  https://doi.org/10.1091/mbc.E15-05-0319 mbc.E15-05-0319 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  97. 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 mbc.E13-10-0574 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  98. Tooze SA, Abada A, Elazar Z (2014) Endocytosis and autophagy: exploitation or cooperation? Cold Spring Harb Perspect Biol 6(5):a018358.  https://doi.org/10.1101/cshperspect.a018358 a018358, /5/a018358 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  99. Urano Y, Watanabe H, Murphy SR, Shibuya Y, Geng Y, Peden AA, Chang CC, Chang TY (2008) Transport of LDL-derived cholesterol from the NPC1 compartment to the ER involves the trans-Golgi network and the SNARE protein complex. Proc Natl Acad Sci U S A 105(43):16513–16518.  https://doi.org/10.1073/pnas.0807450105 0807450105 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  100. Valm AM, Cohen S, Legant WR, Melunis J, Hershberg U, Wait E, Cohen AR, Davidson MW, Betzig E, Lippincott-Schwartz J (2017) Applying systems-level spectral imaging and analysis to reveal the organelle interactome. Nature 546(7656):162–167.  https://doi.org/10.1038/nature22369CrossRefPubMedPubMedCentralGoogle Scholar
  101. van der Kant R, Zondervan I, Janssen L, Neefjes J (2013) Cholesterol-binding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1. J Lipid Res 54(8):2153–2165.  https://doi.org/10.1194/jlr.M037325 jlr.M037325 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  102. Ventimiglia LN, Martin-Serrano J (2016) ESCRT machinery: damage control at the nuclear membrane. Cell Res 26(6):641–642.  https://doi.org/10.1038/cr.2016.52 cr201652 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  103. Vietri M, Schink KO, Campsteijn C, Wegner CS, Schultz SW, Christ L, Thoresen SB, Brech A, Raiborg C, Stenmark H (2015) Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522(7555):231–235.  https://doi.org/10.1038/nature14408 nature14408 [pii]CrossRefPubMedGoogle Scholar
  104. Wang W, Wang X, Fujioka H, Hoppel C, Whone AL, Caldwell MA, Cullen PJ, Liu J, Zhu X (2016) Parkinson’s disease-associated mutant VPS35 causes mitochondrial dysfunction by recycling DLP1 complexes. Nat Med 22(1):54–63.  https://doi.org/10.1038/nm.3983 nm.3983 [pii]CrossRefPubMedGoogle Scholar
  105. Wartosch L, Gunesdogan U, Graham SC, Luzio JP (2015) Recruitment of VPS33A to HOPS by VPS16 is required for lysosome fusion with endosomes and autophagosomes. Traffic 16(7):727–742.  https://doi.org/10.1111/tra.12283CrossRefPubMedPubMedCentralGoogle Scholar
  106. Webster BM, Colombi P, Jager J, Lusk CP (2014) Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159(2):388–401.  https://doi.org/10.1016/j.cell.2014.09.012 S0092-8674(14)01161-1 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  107. Wilhelm LP, Wendling C, Vedie B, Kobayashi T, Chenard MP, Tomasetto C, Drin G, Alpy F (2017) STARD3 mediates endoplasmic reticulum-to-endosome cholesterol transport at membrane contact sites. EMBO J 36(10):1412–1433.  https://doi.org/10.15252/embj.201695917CrossRefPubMedPubMedCentralGoogle Scholar
  108. Xu Y, Rubin BR, Orme CM, Karpikov A, Yu C, Bogan JS, Toomre DK (2011) Dual-mode of insulin action controls GLUT4 vesicle exocytosis. J Cell Biol 193(4):643–653.  https://doi.org/10.1083/jcb.201008135 jcb.201008135 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  109. Zavodszky E, Seaman MN, Moreau K, Jimenez-Sanchez M, Breusegem SY, Harbour ME, Rubinsztein DC (2014) Mutation in VPS35 associated with Parkinson’s disease impairs WASH complex association and inhibits autophagy. Nat Commun 5:3828.  https://doi.org/10.1038/ncomms4828 ncomms4828 [pii]CrossRefPubMedPubMedCentralGoogle Scholar
  110. Zeigerer A, Bogorad RL, Sharma K, Gilleron J, Seifert S, Sales S, Berndt N, Bulik S, Marsico G, D’Souza RC, Lakshmanaperumal N, Meganathan K, Natarajan K, Sachinidis A, Dahl A, Holzhutter HG, Shevchenko A, Mann M, Koteliansky V, Zerial M (2015) Regulation of liver metabolism by the endosomal GTPase Rab5. Cell Rep 11(6):884–892.  https://doi.org/10.1016/j.celrep.2015.04.018 S2211-1247(15)00405-2 [pii]CrossRefPubMedGoogle Scholar
  111. Zhang M, Liu P, Dwyer NK, Christenson LK, Fujimoto T, Martinez F, Comly M, Hanover JA, Blanchette-Mackie EJ, Strauss JF 3rd (2002) MLN64 mediates mobilization of lysosomal cholesterol to steroidogenic mitochondria. J Biol Chem 277(36):33300–33310.  https://doi.org/10.1074/jbc.M200003200 M200003200 [pii]CrossRefPubMedGoogle Scholar
  112. Zhang AS, Sheftel AD, Ponka P (2005) Intracellular kinetics of iron in reticulocytes: evidence for endosome involvement in iron targeting to mitochondria. Blood 105(1):368–375.  https://doi.org/10.1182/blood-2004-06-2226 2004-06-2226 [pii]CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratory of Cell BiologyInternational Institute of Molecular and Cell BiologyWarsawPoland
  2. 2.Cell Research and Immunology Department, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

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