The complex ultrastructure of the endolysosomal system

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 10, 2014, Pages

  Klumperman, Judith ^a   Raposo, Graça ^b,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b INSTITUT CURIE   (France)

^c INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MODEL; COATED VESICLE; ENDOPLASMIC RETICULUM; ENDOSOME; HEPG2 CELL LINE; HUMAN; IMMUNOELECTRON MICROSCOPY; LYSOSOME; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

CLATHRIN-COATED VESICLES; ENDOPLASMIC RETICULUM; ENDOSOMES; HEP G2 CELLS; HUMANS; LYSOSOMES; MICROSCOPY, IMMUNOELECTRON; MODELS, BIOLOGICAL;

EID: 84903745685     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016857     Document Type: Article

References (178)

1. Allen RD, Fok AK. 1980. Membrane recycling and endocy-tosis in Paramecium confirmed by horseradish peroxi-dase pulse-chase studies. J Cell Sci 45: 131–145.
2. Almeida CG, Yamada A, Tenza D, Louvard D, Raposo G, Coudrier E. 2011. Myosin 1b promotes the formation of post-Golgi carriers by regulating actin assembly and membrane remodelling at the trans-Golgi network. Nat Cell Biol 13: 779–789.
3. Anderson RGW, Falck JR, Goldstein JL, Brown MS. 1984. Visualization of acidic organelles in intact cells by electron microscopy. Proc Natl Acad Sci 81: 4838–4842.
4. Babst M, Wendland B, Estepa EJ, Emr SD. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17: 2982–2993.
5. Bainton DF. 1981. The discovery of lysosomes. J Cell Biol 91: 66s–76s.
6. Bhisey AN, Freed JJ. 1971. Altered movement of endosomes in colchicine-treated cultured macrophages. Exp Cell Res 64: 430–438.
7. Bissig C, Gruenberg J. 2013. Lipid sorting and multivesicu-lar endosome biogenesis. Cold Spring Harb Perspect Biol 5: a016816.
8. Bonifacino JS, Rojas R. 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat Rev Mol Cell Biol 7: 568–579.
9. Bonifacino JS, Traub LM. 2003. Signals for sorting of trans-membrane proteins to endosomes and lysosomes. Annu Rev Biochem 72: 395–447.
10. Bright NA, Lindsay MR, Stewart A, Luzio JP. 2001. The relationship between lumenal and limiting membranes in swollen late endocytic compartments formed after wortmannin treatment or sucrose accumulation. Traffic 2: 631–642.
11. Bright NA, Gratian MJ, Luzio JP. 2005. Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells. Curr Biol 15: 360–365.
12. Burd C, Cullen PJ. 2014. Retromer: A master conductor of endosome sorting. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016774.
13. Buschow SI, Nolte-’t Hoen EN, van Niel G, Pols MS, ten Broeke T, Lauwen M, Ossendorp F, Melief CJ, Raposo G, Wubbolts R, et al. 2009. MHC II in dendritic cells is targeted to lysosomes or T cell–induced exosomes via distinct multivesicular body pathways. Traffic 10: 1528–1542.
14. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M. 1999. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the b2-adrenergic receptor. Nature 401: 286–290.
15. Carlton JG, Cullen PJ. 2005. Sorting nexins. Curr Biol 15: R819–R820.
16. Chapuy B, Tikkanen R, Muhlhausen C, Wenzel D, von Fi-gura K, Honing S. 2008. AP-1 and AP-3 mediate sorting of melanosomal and lysosomal membrane proteins into distinct post-Golgi trafficking pathways. Traffic 9: 1157–1172.
17. Chow A, Toomre D, Garrett W, Mellman I. 2002. Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418: 988–994.
18. Cossart P, Helenius A. 2014. Endocytosis of viruses and bacteria. Cold Spring Harb Perspect Biol doi: 10.1101/ cshperspect.a016972.
19. Cullen PJ, Korswagen HC. 2012. Sorting nexins provide diversity for retromer-dependent trafficking events. Nat Cell Biol 14: 29–37.
20. Delevoye C, Hurbain I, Tenza D, Sibarita JB, Uzan-Gafsou S, Ohno H, Geerts WJ, Verkleij AJ, Salamero J, Marks MS, et al. 2009. AP-1 and KIF13A coordinate endosomal sorting and positioning during melanosome biogenesis. J Cell Biol 187: 247–264.
21. Delevoye C, Miserey-Lenkei S, Montagnac G, Gilles-Mar-sens F, Paul Gilloteaux P, Giordano F, Waharte F, Marks MS, Goud B, Raposo G. 2014. Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Rep 6: 1–10.
22. Dell’Angelica EC, Klumperman J, Stoorvogel W, Bonifacino JS. 1998. Association of the AP-3 adaptor complex with clathrin. Science 280: 431–434.
23. De Maziere AM, Muehlethaler K, Van Donselaar E, Salvi S, Davoust J, Cerottini JC, Levy F, Slot JW, Rimoldi D. 2002. The melanocytic protein Melan-A/MART-1 has a sub-cellular localization distinct from typical melanosomal proteins. Traffic 3: 678–693.
24. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gau-treau A. 2009. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17: 712–723.
25. Duleh SN, Welch MD. 2010. WASH and the Arp2/3 complex regulate endosome shape and trafficking. Cytoskele-ton 67: 193–206.
26. 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: 267–272.
27. Eskelinen EL, Reggiori F, Baba M, Kovacs AL, Seglen PO. 2011. Seeing is believing: The impact of electron microscopy on autophagy research. Autophagy 7: 935–956.
28. Folsch H, Pypaert M, Schu P, Mellman I. 2001. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J Cell Biol 152: 595–606.
29. 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: 1030–1040.
30. Futter CE, Pearse A, Hewlett LJ, Hopkins CR. 1996. Multi-vesicular endosomes containing internalized EGF–EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 132: 1011–1023.
31. Futter CE, Gibson A, Allchin EH, Maxwell S, Ruddock LJ, Odorizzi G, Domingo D, Trowbridge IS, Hopkins CR. 1998. In polarized MDCK cells basolateral vesicles arise from clathrin-g-adaptin-coated domains on endosomal tubules. J Cell Biol 141: 611–623.
32. Futter CE, Collinson LM, Backer JM, Hopkins CR. 2001. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 155: 1251–1264.
33. 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 micro-bial killing are controlled by the Arf-like GTPase Arl8b. Immunity 35: 182–193.
34. Geuze HJ, Slot JW, Scheffer RCT, Van der Ley PA. 1981. Use of colloidal gold particles in double-labeling immuno-electron microscopy of ultrathin frozen tissue sections. J Cell Biol 89: 653–665.
35. Geuze HJ, Slot JW, Strous GJ, Lodish HF, Schwartz AL. 1983. Intracellular site of asialoglycoprotein receptor-ligand uncoupling: Double label immunoelectron microscopy during receptor-mediated endocytosis. Cell 32: 277–287.
36. Giordano F, Simoes S, Raposo G. 2011. The ocular albinism type 1 (OA1) GPCR is ubiquitinated and its traffic requires endosomal sorting complex responsible for transport (ESCRT) function. Proc Natl Acad Sci 108: 11906–11911.
37. Gomez TS, Gorman JA, de Narvajas AA, Koenig AO, Bill-adeau DD. 2012. Trafficking defects in WASH-knockout fibroblasts originate from collapsed endosomal and lyso-somal networks. Mol Biol Cell 23: 3215–3228.
38. Gonatas NK, Kim SU, Stieber A, Avrameas S. 1977. Inter-nalization of lectins in neuronal GERL. J Cell Biol 73: 1–13.
39. Gorvel JP, Chavrier P, Zerial M, Gruenberg J. 1991. rab5 Controls early endosome fusion in vitro. Cell 64: 915–925.
40. Goud B, Legrain P, Antoine JC, Avrameas S, Buttin G. 1981. Cross-linking of surface immunoglobulins and endocy-tosis of antigen are not sufficient to suppress antibody production of two hybridoma cell lines. J Recept Res 2: 63–85.
41. Gould GW, Lippincott-Schwartz J. 2009. New roles for en-dosomes: From vesicular carriers to multi-purpose platforms. Nat Rev Mol Cell Biol 10: 287–292.
42. Grant BD, Donaldson JG. 2009. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10: 597–608.
43. Griffiths G. 1993. Fine structure immunocytochemistry. Springer, New York.
44. Gruenberg J, Stenmark H. 2004. The biogenesis of multi-vesicular endosomes. Nat Rev Mol Cell Biol 5: 317–323.
45. Hanson PI, Cashikar A. 2012. Multivesicular body morphogenesis. Ann Rev Cell Dev Biol 28: 337–362.
46. Hawes P, Netherton CL, Mueller M, Wileman T, Monaghan P. 2007. Rapid freeze-substitution preserves membranes in high-pressure frozen tissue culture cells. J Microsc 226: 182–189.
47. Henne WM, Stenmark H, Emr SD. 2013. Molecular mechanisms of the membrane sculpting ESCRT pathway. Cold Spring Harb Perspect Biol 5: a016766.
48. Hirst J, Borner GH, Antrobus R, Peden AA, Hodson NA, Sahlender DA, Robinson MS. 2012. Distinct and overlapping roles for AP-1 and GGAs revealed by the “knock-sideways” system. Curr Biol 22: 1711–1716.
49. Hoepfner S, Severin F, Cabezas A, Habermann B, Runge A, Gillooly D, Stenmark H, Zerial M. 2005. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121: 437–450.
50. Hunt SD, Townley AK, Danson CM, Cullen PJ, Stephens DJ. 2013. Microtubule motors mediate endosomal sorting by maintaining functional domain organization. J Cell Sci 126: 2493–2501.
51. Huotari J, Helenius A. 2011. Endosome maturation. EMBO J 30: 3481–3500.
52. Hurbain I, Geerts WJ, Boudier T, Marco S, Verkleij AJ, Marks MS, Raposo G. 2008. Electron tomography of early melanosomes: Implications for melanogenesis and the generation of fibrillar amyloid sheets. Proc Natl Acad Sci 105: 19726–19731.
53. Glued, ORP1L, and the receptor bIII spectrin. J Cell Biol 176: 459–471.
54. Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, Janssen H, Wubbolts R, Neefjes J. 2001. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynac-tin motors. Curr Biol 11: 1680–1685.
55. Kaniuk NA, Canadien V, Bagshaw RD, Bakowski M, Braun V, Landekic M, Mitra S, Huang J, Heo WD, Meyer T, et al. 2011. Salmonella exploits Arl8B-directed kinesin activity to promote endosome tubulation and cell-to-cell transfer. Cell Microbiol 13: 1812–1823.
56. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ. 1997. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 139: 639–649.
57. Kleijmeer M, Ramm G, Schuurhuis D, Griffith J, Rescigno M, Ricciardi-Castagnoli P, Rudensky AY, Ossendorp F, Melief CJ, Stoorvogel W, et al. 2001a. Reorganization of multivesicular bodies regulates MHC class IIantigen presentation by dendritic cells. J Cell Biol 155: 53–63.
58. Kleijmeer MJ, Escola JM, UytdeHaag FG, Jakobson E, Griffith JM, Osterhaus AD, Stoorvogel W, Melief CJ, Ra-bouille C, Geuze HJ. 2001b. Antigen loading of MHC class I molecules in the endocytic tract. Traffic 2: 124–137.
59. Klumperman J. 2011. Architecture of the mammalian Golgi. Cold Spring Harb Perspect Biol 3: a005181.
60. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J. 1998. A lipid associated with the antiphos-pholipid syndrome regulates endosome structure and function. Nature 392: 193–197.
61. Kolter T, Sandhoff K. 2010. Lysosomal degradation of membrane lipids. FEBS Lett 584: 1700–1712.
62. Konig P, Braunfeld MB, Sedat JW, Agard DA. 2007. The three-dimensional structure of in vitro reconstituted Xenopus laevis chromosomes by EM tomography. Chro-mosoma 116: 349–372.
63. Koster AJ, Klumperman J. 2003. Electron microscopy in cell biology: Integrating structure and function. Nat Rev Mol Cell Biol SS6–S10.
64. Kukulski W, Schorb M, Kaksonen M, Briggs JA. 2012a. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150: 508–520.
65. Kukulski W, Schorb M, Welsch S, Picco A, Kaksonen M, Briggs JA. 2012b. Precise, correlated fluorescence microscopy and electron tomography of lowicryl sections using fluorescent fiducial markers. Method Cell Biol 111: 235–257.
66. Lapierre LA, Goldenring JR. 2005. Interactions of Myosin Vb with Rab11 family members and cargoes traversing the plasma membrane recycling system. Method Enzymol 403: 715–723.
67. Lauffer BE, Melero C, Temkin P, Lei C, Hong W, Kortemme T, von Zastrow M. 2010. SNX27 mediates PDZ-directed sorting from endosomes to the plasma membrane. J Cell Biol 190: 565–574.
68. Louvard D, Morris C, Warren G, Stanley K, Winkler F, Reg-gio H. 1983. Amonoclonal antibody to the heavy chain of clathrin. EMBO J 2: 1655–1664.
69. Luzio JP, Gray SR, Bright NA. 2010. Endosome–lysosome fusion. Biochem Soc Trans 38: 1413–1416.
70. Mallard F, Antony C, Tenza D, Salamero J, Goud B, Johannes L. 1998. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport. J Cell Biol 143: 973–990.
71. Marbet P, Rahner C, Stieger B, Landmann L. 2006. Quantitative microscopy reveals 3D organization and kinetics of endocytosis in rat hepatocytes. Microsc Res Tech 69: 693–707.
72. Mari M, Bujny MV, Zeuschner D, Geerts WJ, Griffith J, Petersen CM, Cullen PJ, Klumperman J, Geuze HJ. 2008. SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic 9: 380–393.
73. Marks MS, Heijnen HF, Raposo G. 2013. Lysosome-related organelles: Unusual compartments become mainstream. Curr Opin Cell Biol 25: 495–505.
74. Marsh M, Griffiths G, Dean GE, Mellman I, Helenius A. 1986. Three-dimensional structure of endosomes in BHK-21 cells. Proc Natl Acad Sci 83: 2899–2903.
75. Matsuo H, Chevallier J, Mayran N, Le Blanc I, Ferguson C, Faure J, Blanc NS, Matile S, Dubochet J, Sadoul R, et al. 2004. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303: 531–534.
76. Maxfield FR. 2014. Role of endosomes and lysosomes in human disease. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016931.
77. Maxfield FR, McGraw TE. 2004. Endocytic recycling. Nat Rev Mol Cell Biol 5: 121–132.
78. Mayor S, Pagano RE. 2007. Pathways of clathrin-indepen-dent endocytosis. Nat Rev Mol Cell Biol 8: 603–612.
79. Mayor S, Parton RG, Donaldson JG. 2014. Clathrin-inde-pendent pathways of endocytosis. Cold Spring Harb Per-spect Biol doi: 10.1101/cshperspect.a016758.
80. McDermott R, Ziylan U, Spehner D, Bausinger H, Lipsker D, Mommaas M, Cazenave JP, Raposo G, Goud B, de la Salle H, et al. 2002. Birbeck granules are subdomains of endosomal recycling compartment in human epidermal Langerhans cells, which form where Langerin accumulates. Mol Biol Cell 13: 317–335.
81. Menager MM, Menasche G, Romao M, Knapnougel P, Ho CH, Garfa M, Raposo G, Feldmann J, Fischer A, de Saint Basile G. 2007. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat Immunol 8: 257–267.
82. Mesa R, Salomon C, Roggero M, Stahl PD, Mayorga LS. 2001. Rab22a affects the morphology and function of the endocytic pathway. J Cell Sci 114: 4041–4049.
83. Mesaki K, Tanabe K, Obayashi M, Oe N, Takei K. 2011. Fission of tubular endosomes triggers endosomal acidification and movement. PLoS ONE 6: e19764.
84. Meyer C, Eskelinen EL, Guruprasad MR, von Figura K, Schu P. 2001. Mu 1A deficiency induces a profound increase in MPR300/IGF-II receptor internalization rate. J Cell Sci 114: 4469–4476.
85. Mironov AA, Beznoussenko GV. 2012. Correlative light-electron microscopy a potent tool for the imaging of rare or unique cellular and tissue events and structures. Methods Enzymol 504: 201–219.
86. Miserey-Lenkei S, Chalancon G, Bardin S, Formstecher E, Goud B, Echard A.2010. Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol 12: 645–654.
87. Möbius W, Ohno-Iwashita Y, van Donselaar EG, Oorschot VM, Shimada Y, Fujimoto T, Heijnen HF, Geuze HJ, Slot JW. 2002. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfrin-golysin O. J Histochem Cytochem 50: 43–55.
88. Möbius W, van Donselaar E, Ohno-Iwashita Y, Shimada Y, Heijnen HF, Slot JW, Geuze HJ. 2003. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 4: 222–231.
89. Montagnac G, Chavrier P. 2008. Endosome positioning during cytokinesis. Biochem Soc Trans 36: 442–443.
90. Mrakovic A, Kay JG, Furuya W, Brumell JH, Botelho RJ. 2012. Rab7 and Arl8 GTPases are necessary for lysosome tubulation in macrophages. Traffic 13: 1667–1679.
91. Muller-Reichert T, Verkade P. 2012. Introduction to correlative light and electron microscopy. Method Cell Biol 111: xvii–xix.
92. Muller-Reichert T, Hohenberg H, O’Toole ET, McDonald K. 2003. Cryoimmobilization and three-dimensional visualization of C. elegans ultrastructure. J Microsc 212: 71–80.
93. Mullock BM, Bright NA, Fearon CW, Gray SR, Luzio JP. 1998. Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J Cell Biol 140: 591–601.
94. Murk J, Humbel BM, Zlese U, Griffith J, Posthuma G, Slot JW, Koster A, Verkleij H, Geuze H, Kleijmeer MJ. 2003a. Endosomal comparttimentalization inthree dimensions: Implications for membrane fusion. Proc Natl Acad Sci 100: 13332–13337.
95. Murk JL, Posthuma G, Koster AJ, Geuze HJ, Verkleij AJ, Kleijmeer MJ, Humbel BM. 2003b. Influence of aldehyde fixation on the morphology of endosomes and lyso-somes: Quantitative analysis and electron tomography. J Microsc 212: 81–90.
96. Murk JL, Lebbink MN, Humbel BM, Geerts WJ, Griffith JM, Langenberg DM, Verreck FA, Verkleij AJ, Koster AJ, Geuze HJ, Kleijmeer MJ. 2004. 3-D Structure of multi-laminar lysosomes in antigen presenting cells reveals trapping of MHC II on the internal membranes. Traffic 12: 936–945.
97. Nakagawa T, Setou M, Seog D, Ogasawara K, Dohmae N, Takio K, Hirokawa N. 2000. A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex. Cell 103: 569–581.
98. Naslavsky N, Caplan S.2011. EHD proteins: Key conductors of endocytic transport. Trend Cell Biol 21: 122–131.
99. Novikoff AB, Novikoff PM. 1977. Cytochemical contributions to differentiating GERL from the Golgi apparatus. Histochem J 9: 525–551.
100. Novikoff AB, Beaufay H, De Duve C. 1956. Electron microscopy of lysosomerich fractions from rat liver. J Biophys Biochem Cytol 2: 179–184.
101. Odorizzi G, Babst M, Emr SD. 1998. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multi-vesicular body. Cell 95: 847–858.
102. Parton RG, Dotti CG, Bacallao R, Kurtz I, Simons K, Prydz K. 1991. pH-induced microtubule-dependent redistribution of late endosomes in neuronal and epithelial cells. J Cell Biol 113: 261–274.
103. Paul P, van den Hoorn T, Jongsma ML, Bakker MJ, Henge-veld R, Janssen L, Cresswell P, Egan DA, van Ham M, Ten Brinke A, et al. 2011. A genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 145: 268–283.
104. Peden AA, Oorschot V, Hesser BA, Austin CD, Scheller RH, Klumperman J. 2004. Localization of the AP-3 adaptor complex definesanovel endosomal exit site for lysosomal membrane proteins. J Cell Biol 164: 1065–1076.
105. Pfeffer SR. 2013. Rab GTPase regulation of membrane identity. Curr Opin Cell Biol 25: 414–419.
106. Polishchuk RS, Polishchuk EV, Luini A. 2012. Visualizing live dynamics and ultrastructure of intracellular organ-elles with preembedding correlative light-electron microscopy. Method Cell Biol 111: 21–35.
107. Pols MS, Klumperman J. 2009. Trafficking and function of the tetraspanin CD63. Exp Cell Res 315: 1584–1592.
108. Pols MS, van Meel E, Oorschot V, ten Brink C, Fukuda M, Swetha MG, Mayor S, Klumperman J. 2013. hVps41 and VAMP7 function in direct TGN to late endosome transport of lysosomal membrane proteins. Nat Commun 4: 1361.
109. Popoff V, Mardones GA, Tenza D, Rojas R, Lamaze C, Bo-nifacino JS, Raposo G, Johannes L. 2007. The retromer complex and clathrin define an early endosomal retrograde exit site. J Cell Sci 120: 2022–2031.
110. Prekeris R, Klumperman J, Chen YA, Scheller RH. 1998. Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J Cell Biol 143: 957–971.
111. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, Taunton J, Weiner OD, Parton RG, von Zastrow M. 2010. Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143: 761–773.
112. Raiborg C, Bache KG, Mehlum A, Stang E, Stenmark H. 2001. Hrs recruits clathrin to early endosomes. EMBO J 20: 5008–5021.
113. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H. 2002. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol 4: 394–398.
114. Ranftler C, Auinger A, Meisslitzer-Ruppitsch C, Neumüller J, Ellinger A, Pavelka M. 2013. Electron microscopy of endocytic pathways. In Cell imaging techniques: Methods and protocols, 2nd ed. (ed. Taatjes DJ, Roth J), pp. 437–447. Humana, Totowa, NJ.
115. Raposo G, Stoorvogel W. 2013. Extracellular vesicles: Exo-somes, microvesicles, and friends. J Cell Biol 200: 373–383.
116. Raposo G, Kleijmeer MJ, Posthuma G, Slot JW, Geuze HJ. 1997. Immunogold labeling of ultrathin cryosections: Application in immunology. In Weir’s handbook of experimental immunology, immunochemistry and molecular immunology (ed. Weir DM), Chap. 208, pp. 1–11. Wiley, New York.
117. Raposo G, Cordonnier MN, Tenza D, Menichi B, Durrbach A, Louvard D, Coudrier E. 1999. Association of myosin Ia with endosomes and lysosomes in mammalian cells. Mol Biol Cell 10: 1477–1494.
118. Raposo G, Tenza D, Murphy DM, Berson JF, Marks MS. 2001. Distinct protein sorting and localization to preme-lanosomes, melanosomes, and lysosomes in pigmented melanocytic cells. J Cell Biol 152: 809–824.
119. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. 1998. Hydrolysis of GTP on Rab11 is required for the direct delivery of transferrin from the peri-centriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci 95: 6187–6192.
120. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. 2005. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735–749.
121. Glued and late endosome positioning. J Cell Biol 185: 1209–1225.
122. Rojas R, van Vlijmen T, Mardones GA, Prabhu Y, Rojas AL, Mohammed S, Heck AJ, Raposo G, van der Sluijs P, Bo-nifacino JS. 2008. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 183: 513–526.
123. Romao M, Tanaka K, Sibarita JB, Ly-Hartig NT, Tanaka TU, Antony C. 2008. Three-dimensional electron microscopy analysis of ndc10-1 mutant reveals an aberrant organization of the mitotic spindle and spindle pole body defects in Saccharomyces cerevisiae. J Struct Biol 163: 18–28.
124. Rong Y, McPhee CK, Deng S, Huang L, Chen L, Liu M, Tracy K, Baehrecke EH, Yu L, Lenardo MJ. 2011. Spinster is required for autophagic lysosome reformation and mTOR reactivation following starvation. Proc Natl Acad Sci 108: 7826–7831.
125. Rybin V, Ullrich O, Rubino M, Alexandrov K, Simon I, Seabra MC, Goody R, Zerial M. 1996. GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature 383: 266–269.
126. Sachse M, Ramm G, Strous G, Klumperman J. 2002a. En-dosomes: Multipurpose designs for integrating housekeeping and specialized tasks. Histochem Cell Biol 117: 91–104.
127. Sachse M, Urbe S, Oorschot V, Strous GJ, Klumperman J. 2002b. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell 13: 1313–1328.
128. Sachse M, Strous GJ, Klumperman J. 2004. ATPase-deficient hVPS4 impairs formation of internal endosomal vesicles and stabilizes bilayered clathrin coats on endosomal vac-uoles. J Cell Sci 117: 1699–1708.
129. Saftig P, Klumperman J. 2009. Lysosome biogenesis and lysosomal membrane proteins: Trafficking meets function. Nat Rev Mol Cell Biol 10: 623–635.
130. Salas-Cortes L, Ye F, Tenza D, Wilhelm C, Theos A, Louvard D, Raposo G, Coudrier E. 2005. Myosin Ib modulates the morphology and the protein transport within multi-vesicular sorting endosomes. J Cell Sci 118: 4823–4832.
131. Schonteich E, Wilson GM, Burden J, Hopkins CR, Anderson K, Goldenring JR, Prekeris R. 2008. The Rip11/ Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J Cell Sci 121: 3824–3833.
132. Seaman MN, Gautreau A, Billadeau DD. 2013. Retromer-mediated endosomal protein sorting: All WASHed up! Trend Cell Biol 23: 522–528.
133. Sheff DR, Daro EA, Hull M, Mellman I. 1999. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 145: 123–139.
134. Shio H, Farquhar MG, de Duve C. 1974. Lysosomes of the arterial wall. IV. Cytochemical localization of acid phos-phatase and catalase in smooth muscle cells and foam cells from rabbit atheromatous aorta. Am J Pathol 76: 1–16.
135. Shu X, Lev-Ram V, Deerinck TJ, Qi Y, Ramko EB, Davidson MW, Jin Y, Ellisman MH, Tsien RY. 2011. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol 9: e1001041.
136. Slot JW, Geuze HJ. 1981. Sizing of protein A–colloidal gold probes for immunoelectron microscopy. J Cell Biol 90: 533–536.
137. Slot JW, Geuze HJ. 2007. Cryosectioning and immunolab-eling. Nat Protoc 2: 2480–2491.
138. Slot JW, Posthuma G, Chang L, Crapo JD, Geuze HJ. 1988. Quantitative assessment ofimmuno-gold labeling in cry-osections. In Immuno-gold labeling in cell biology (ed. Verleij AJ, Leunissen JLM), pp. 135–156. CRC, Boca Raton, FL.
139. Sonnichsen B, De Renzis S, Nielsen E, Rietdorf J, Zerial M. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J Cell Biol 149: 901–914.
140. Sotelo JR, Porter KR. 1959. An electron microscope study of the rat ovum. J Biophys Biochem Cytol 5: 327–342.
141. Steinberg F, Gallon M, Winfield M, Thomas EC, Bell AJ, Heesom KJ, Tavare JM, Cullen PJ. 2013. A global analysis of SNX27–retromer assembly and cargo specificity reveals a function in glucose and metal ion transport. Nat Cell Biol 15: 461–471.
142. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell 10: 513–525.
143. Stoorvogel W, Strous GJ, Geuze HJ, Oorschot V, Schwartz AL. 1991. Late endosomes derive from early endosomes by maturation. Cell 65: 417–427.
144. Stoorvogel W, Oorschot V, Geuze HJ. 1996. A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol 132: 21–33.
145. Studer D, Graber W, Al-Amoudi A, Eggli P. 2001. A new approach for cryofixation by high pressure freezing. J Microsc 203: 285–294.
146. Stuffers S, Sem Wegner C, Stenmark H, Brech A. 2009. Multivesicular endosome biogenesis in the absence of ESCRTs. Traffic 10: 925–937.
147. Swanson J, Bushnell A, Silverstein SC. 1987. Tubular lyso-some morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules. Proc Natl Acad Sci 84: 1921-1925.
148. Taguchi T. 2013. Emerging roles of recycling endosomes. J Biochem 153: 505-510.
149. Ten Broeke T, Wubbolts R, Stoorvogel W. 2013. MHC class II antigen presentation by dendritic cells regulated through endosomal sorting. Cold Spring Harb Perspect Biol 5: a016873.
150. Theos AC, Tenza D, Martina JA, Hurbain I, Peden AA, Svi-derskaya EV, Stewart A, Robinson MS, Bennett DC, Cutler DF, et al. 2005. Functions of AP-3 and AP-1 in tyrosinase sorting from endosomes to melanosomes. Mol Biol Cell 16: 5356-5372.
151. Theos AC, Truschel ST, Tenza D, Hurbain I, Harper DC, Berson JF, Thomas PC, Raposo G, Marks MS. 2006. A lumenal domain-dependent pathway for sorting to intra-lumenal vesicles of multivesicular endosomes involved in organelle morphogenesis. Dev Cell 10: 343–354.
152. Tooze J, Hollinshead M. 1991. Tubular early endosomal networks in AtT20 and other cells. J Cell Biol 115: 635–653.
153. Tooze SA, Abada A, Elazar Z. 2014. Endocytosis and au-tophagy. Exploitation or cooperation? Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a018358.
154. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M. 2008. Cer-amide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244–1247.
155. Traub LM, Bannykh SI, Rodel JE, Aridor M, Balch WE, Kornfeld S. 1996. AP-2-containing clathrin coats assemble on mature lysosomes. J Cell Biol 135: 1801–1814.
156. Trowbridge IS. 1991. Endocytosis and signals for internalization. Curr Opin Cell Biol 3: 634-641.
157. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135: 913–924.
158. Urbe S, Sachse M, Row PE, Preisinger C, Barr FA, Strous G, Klumperman J, Clague MJ. 2003. The UIM domain of Hrs couples receptor sorting to vesicle formation. J Cell Sci 116: 4169–4179.
159. van Dam EM, Stoorvogel W. 2002. Dynamin dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol Biol Cell 13: 169–182.
160. Van der Sluijs P, Hull P, Webster P, Male P, Goud B, Zerial M. 1992. The small GTP-binding protein Rab4 controls an early sorting event on the endocytic pathway. Cell 70: 729–740.
161. van Niel G, Wubbolts R, ten Broeke T, Buschow SI, Ossen-dorp FA, Melief CJ, Raposo G, van Balkom BW, Stoorvogel W 2006. Dendritic cells regulate exposure of MHC class II at their plasma membrane by oligoubiquitination. Immunity 25: 885-894.
162. van Niel G, Charrin S, Simoes S, Romao M, Rochin L, Saftig P, Marks MS, Rubinstein E, Raposo G. 2011. The Tetra-spanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 21: 708–721.
163. van Rijnsoever C, Oorschot V, Klumperman J. 2008. Correlative light-electron microscopy (CLEM) combining live-cell imaging and immunolabeling of ultrathin cryo-sections. Nat Methods 5: 973–980.
164. van Weering JR, Brown E, Sharp TH, Mantell J, Cullen PJ, Verkade P. 2010. Intracellular membrane traffic at high resolution. Meth Cell Biol 96: 619–648.
165. van Weering JR, Sessions RB, Traer CJ, Kloer DP, Bhatia VK, Stamou D, Carlsson SR, Hurley JH, Cullen PJ. 2012. Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J 31: 4466–4480.
166. Wandinger-Ness A, Zerial M. 2014. Rab proteins and the compartmentalization of the endosomal system. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect. a022616.
167. Westlake CJ, Baye LM, Nachury MV, Wright KJ, Ervin KE, Phu L, Chalouni C, Beck JS, Kirkpatrick DS, Slusarski DC, et al. 2011. Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAP-PII) complex-dependent trafficking of Rabin8 to the cen-trosome. Proc Natl Acad Sci 108: 2759–2764.
168. White IJ, Bailey LM, Aghakhani MR, Moss SE, Futter CE. 2006. EGF stimulates annexin 1–dependent inward ve-siculation in a multivesicular endosome subpopulation. EMBO J 25: 1–12.
169. Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J. 2000. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol 151: 1207–1220.
170. Willingham MC, Pastan I. 1980. The receptosome: An intermediate organelle of receptor mediated endocytosis in cultured fibroblasts. Cell 21: 67–77.
171. Willingham MC, Pastan I. 1983. Formation of receptosomes from plasma membrane coated pits during endocytosis: Analysis by serial sections with improved membrane labeling and preservation techniques. Proc Natl Acad Sci 80: 5617–5621.
172. Willingham MC, Hanover JA, Dickson RB, Pastan I. 1984. Morphologic characterization of the pathway of transfer-rin endocytosis and recycling in human KB cells. Proc Natl Acad Sci 81: 175–179.
173. Yamashiro DJ, Tycko B, Fluss SR, Maxfield FR. 1984. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37: 789–800.
174. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, Mi N, Zhao Y, Liu Z, Wan F, et al. 2010. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 465: 942–946.
175. Yudowski GA, Puthenveedu MA, Henry AG, vonZastrow M. 2009. Cargo-mediated regulation of a rapid Rab4-depen-dent recycling pathway. Mol Biol Cell 20: 2774–2784.
176. Zeigerer A, Gilleron J, Bogorad RL, Marsico G, Nonaka H, Seifert S, Epstein-Barash H, Kuchimanchi S, Peng CG, Ruda VM, et al. 2012. Rab5 isnecessary for the biogenesis of the endolysosomal system in vivo. Nature 485: 465–470.
177. Zerial M, McBride H. 2001. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107–119.
178. Zeuschner D, Geerts WJ, van Donselaar E, Humbel BM, Slot JW, Koster AJ, Klumperman J. 2006. Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nat Cell Biol 8: 377–383.