Function and regulation of the endosomal fusion and fission machineries

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 3, 2014, Pages

  Gautreau, Alexis ^a   Oguievetskaia, Ksenia ^a   Ungermann, Christian ^b  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RAB PROTEIN;

ARTICLE; BIOLOGICAL MODEL; CYTOSKELETON; ENDOCYTOSIS; ENDOSOME; MEMBRANE FUSION; METABOLISM; PHYSIOLOGY;

CYTOSKELETON; ENDOCYTOSIS; ENDOSOMES; MEMBRANE FUSION; MODELS, BIOLOGICAL; RAB GTP-BINDING PROTEINS;

EID: 84897584040     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016832     Document Type: Article

References (129)

1. Akbar MA, Tracy C, Kahr WHA, Kramer H. 2011. The fullof-bacteria gene is required for phagosome maturation during immune defense in Drosophila. J Cell Biol 192: 383-390.
2. Bacia K, Schwille P, Kurzchalia T. 2005. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc Natl Acad Sci 102: 3272-3277.
3. Balderhaar HJK, Arlt H, Ostrowicz CW, Brocker C, Sundermann F, Brandt R, Babst M, Ungermann C. 2010. The Rab GTPase Ypt7 is linked to retromer-mediated receptor recycling and fusion at the yeast late endosome. J Cell Sci 123: 4085-4094.
4. Balderhaar HJK, Lachmann J, Yavavli E, Brocker C, Lurick A, Ungermann C. 2013. The CORVET complex promotes tethering and fusion of Rab5/Vps21-positive membranes. Proc Natl Acad Sci 110: 3823-3828.
5. Bananis E, Murray JW, Stockert RJ, Satir P, Wolkoff AW. 2003. Regulation of early endocytic vesicle motility and fission in a reconstituted system. J Cell Sci 116: 2749-2761.
6. Barr FA. 2013. Rab GTPases and membrane identity: Causal or inconsequential? J Cell Biol 202: 191-199.
7. Barr F, Lambright DG. 2010. Rab GEFs and GAPs. Curr Opin Cell Biol 22: 461-470.
8. Baumgart T, Hess ST, Webb WW. 2003. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425: 821-824.
9. Bonifacino JS, Glick BS. 2004. The mechanisms of vesicle budding and fusion. Cell 116: 153-166.
10. Bonifacino JS, Hurley JH. 2008. Retromer. Curr Opin Cell Biol 20: 427-436.
11. Braun A, Pinyol R, Dahlhaus R, Koch D, Fonarev P, Grant BD, Kessels MM, Qualmann B. 2005. EHD proteins associatewith syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 16: 3642-3658.
12. Brocker C, Kuhlee A, Gatsogiannis C, Kleine Balderhaar HJ, Honscher C, Engelbrecht-Vandre S, Ungermann C, Raunser S. 2012. Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc Natl Acad Sci 109: 1991-1996.
13. Cabrera M, Arlt H, Epp N, Lachmann J, Griffith J, Perz A, Reggiori F, Ungermann C. 2013. Functional separation of endosomal fusion factors and the class C core vacuole/ endosome tethering (CORVET) complex in endosome biogenesis. J Biol Chem 288: 5166-5175.
14. Cai L, Makhov AM, Schafer DA, Bear JE. 2008. Coronin 1B antagonizes cortactin and remodels Arp2/3-containing actin branches in lamellipodia. Cell 134: 828-842.
15. Carnell M, Zech T, Calaminus SD, Ura S, Hagedorn M, Johnston SA, May RC, Soldati T, Machesky LM, Insall RH. 2011. Actin polymerization driven by WASH causes V-ATPase retrieval and vesicle neutralization before exocytosis. J Cell Biol 193: 831-839.
16. Carpentier S, N'kuli F, Grieco G, Van Der Smissen P, Janssens V, Emonard H, Bilanges B, Vanhaesebroeck B, Gaide Chevronnay HP, Pierreux CE, et al. 2013. Class III phosphoinositide 3-kinase/VPS34 and dynamin are critical for apical endocytic recycling. Traffic 14: 933-948.
17. Christoforidis S, McBride H, Burgoyne R, Zerial M. 1999. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397: 621-625.
18. Collins K, Thorngren N, Fratti R, Wickner W. 2005. Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J 24: 1775-1786.
19. Collins A, Warrington A, Taylor KA, Svitkina T. 2011. Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis. Curr Biol 21: 1167-1175.
20. Cullen PJ. 2008. Endosomal sorting and signalling: An emerging role for sorting nexins. Nat Rev Mol Cell Biol 9: 574-582.
21. Cullinane AR, Straatman-Iwanowska A, Zaucker A, Wakabayashi Y, Bruce CK, Luo G, Rahman F, Gurakan F, Utine E, Ozkan TB, et al. 2010. Mutations in VIPAR cause an arthrogryposis, renal dysfunction and cholestasis syndrome phenotype with defects in epithelial polarization. Nat Genet 42: 303-312.
22. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJG, McMahon HT. 2007. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449: 923-927.
23. de Figueiredo P, Doody A, Polizotto RS, Drecktrah D, Wood S, Banta M, Strang MS, Brown WJ. 2001. Inhibition of transferrin recycling and endosome tubulation by phospholipase A2 antagonists. J Biol Chem 276: 47361-47370.
24. 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.
25. Derivery E, Gautreau A. 2010. Evolutionary conservation of the WASH complex, an actin polymerization machine involved in endosomal fission. Commun Integr Biol 3: 227-230.
26. Derivery E, Sousa C, Gautier JJ, Lombard B, Loew D, Gautreau A. 2009. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev Cell 17: 712-723.
27. Derivery E, Helfer E, Henriot V, Gautreau A. 2012. Actin polymerization controls the organization of WASH domains at the surface of endosomes. PLoS ONE 7: e39774.
28. Dion PA, Daoud H, Rouleau GA. 2009. Genetics of motor neuron disorders: New insights into pathogenic mechanisms. Nat Rev Genet 10: 769-782.
29. Di Pietro SM, Falcon-Perez JM, Tenza D, Setty SRG, Marks MS, Raposo G, Dell'Angelica EC. 2006. BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes. Mol Biol Cell 17: 4027-4038.
30. Drengk A, Fritsch J, Schmauch C, Ruhling H, Maniak M. 2003. A coat of filamentous actin prevents clustering of late-endosomal vacuoles in vivo. Curr Biol 13: 1814-1819.
31. Duleh SN, Welch MD. 2010. WASH and the Arp2/3 complex regulate endosome shape and trafficking. Cytoskeleton (Hoboken) 67: 193-206.
32. Duleh SN, Welch MD. 2012. Regulation of integrin trafficking, cell adhesion, and cell migration by WASH and the Arp2/3 complex. Cytoskeleton (Hoboken) 69: 1047-1058.
33. Egami Y, Araki N. 2008. Characterization of Rab21-positive tubular endosomes induced by PI3K inhibitors. Exp Cell Res 314: 729-737.
34. Epp N, Ungermann C. 2013. The N-terminal domains of Vps3 and Vps8 are critical for localization and function of the CORVET tethering complex on endosomes. PLoS ONE 8: e67307.
35. Fouraux M, Deneka M, Ivan V, van der Heijden A, Raymackers J, van Suylekom D, van Venrooij W, van der Sluijs P, Pruijn G. 2004. rabip40 is an effector of rab5 and rab4 and regulates transport through early endosomes. Mol Biol Cell 15: 611-624.
36. Fuchs E, Haas AK, Spooner RA, Yoshimura S-I, Lord JM, Barr FA. 2007. Specific Rab GTPase-activating proteins define the Shiga toxin and epidermal growth factor uptake pathways. J Cell Biol 177: 1133-1143.
37. Galvez T, Gilleron J, Zerial M, O'Sullivan GA. 2012. Snap-Shot: Mammalian Rab proteins in endocytic trafficking. Cell 151: 234-234. e2.
38. Gao X-D, Albert S, Tcheperegine SE, Burd CG, Gallwitz D, Bi E. 2003. The GAPactivity of Msb3p and Msb4p for the Rab GTPase Sec4p is required for efficient exocytosis and actin organization. J Cell Biol 162: 635-646.
39. Gerondopoulos A, Langemeyer L, Liang J-R, Linford A, Barr FA. 2012. BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr Biol 1-5.
40. Gokool S, Tattersall D, Seaman MNJ. 2007. EHD1 interacts with retromer to stabilize SNX1 tubules and facilitate endosome-to-Golgi retrieval. Traffic 8: 1873-1886.
41. Gomez TS, Billadeau DD. 2009. AFAM21-containingWASH complex regulates retromer-dependent sorting. Dev Cell 17: 699-711.
42. Gomez TS, Gorman JA, de Narvajas AA-M, Koenig AO, Billadeau DD. 2012. Trafficking defects inWASH-knock-out fibroblasts originate from collapsed endosomal and lysosomal networks. Mol Biol Cell 23: 3215-3228.
43. Haas A, Conradt B, Wickner W. 1994. G-protein ligands inhibit in vitro reactions of vacuole inheritance. J Cell Biol 126: 87-97.
44. Haas A, Scheglmann D, Lazar T, Gallwitz D, Wickner W. 1995. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. EMBO J 14: 5258-5270.
45. Haas AK, Fuchs E, Kopajtich R, Barr FA. 2005. A GTPaseactivating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 7: 887-893.
46. Haas AK, Yoshimura S-I, Stephens DJ, Preisinger C, Fuchs E, Barr FA. 2007. Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. J Cell Sci 120: 2997-3010.
47. Hama H, Tall G, Horazdovsky B. 1999. Vps9p is a guanine nucleotide exchange factor involved in vesicle-mediated vacuolar protein transport. J Biol Chem 274: 15284-15291.
48. Hao Y-H, Doyle JM, Ramanathan S, Gomez TS, Jia D, Xu M, Chen ZJ, Billadeau DD, Rosen MK, Potts PR. 2013. Regulation of WASH-dependent actin polymerization and protein trafficking by ubiquitination. Cell 152: 1051-1064.
49. Harbour ME, Breusegem SYA, Antrobus R, Freeman C, Reid E, Seaman MNJ. 2010. The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J Cell Sci 123: 3703-3717.
50. Helfer E, Harbour ME, Henriot V, Lakisic G, Sousa-Blin C, Volceanov L, Seaman MNJ, Gautreau A. 2013. Endosomal recruitment of theWASH complex: Active sequences and mutations impairing interaction with the retromer. Biol Cell 105: 191-207.
51. Hernandez-Valladares M, Kim T, Kannan B, Tung A, Aguda AH, Larsson M, Cooper JA, Robinson RC. 2010. Structural characterization of a capping protein interaction motif defines a family of actin filament regulators. Nat Struct Mol Biol 17: 497-503.
52. Hickey CM, Wickner W. 2010. HOPS initiates vacuole docking by tethering membranes before trans-SNARE complex assembly. Mol Biol Cell 21: 2297-2305.
53. Horiuchi H, Lippe R, McBride H, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M, et al. 1997. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90: 1149-1159.
54. Huotari J, Helenius A. 2011. Endosome maturation. EMBO J 30: 3481-3500.
55. Itzen A, Goody RS. 2011. GTPases involved in vesicular trafficking: Structures and mechanisms. Semin Cell Dev Biol 22: 48-56.
56. Jahn R, Scheller R. 2006. SNAREs-Engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643.
57. Jakobsson J, Ackermann F, Andersson F, Larhammar D, Low P, Brodin L. 2011. Regulation of synaptic vesicle budding and dynamin function by an EHD ATPase. J Neurosci 31: 13972-13980.
58. Jia D, Gomez TS, Metlagel Z, Umetani J, Otwinowski Z, Rosen MK, Billadeau DD. 2010. WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes. Proc Natl Acad Sci 107: 10442-10447.
59. Jia D, Gomez TS, Billadeau DD, Rosen MK. 2012. Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer. Mol Biol Cell 23: 2352-2361.
60. Johannes L, Wunder C, Bassereau P. 2014. Bending "on the rocks"-A cocktail of biophysical modules to build endocytic pathways. Cold Spring Harb Perspect Biol 6: a016741.
61. 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 GTPaseactivating protein Msb3. J Cell Biol 201: 97-111.
62. Julicher F, Lipowsky R. 1993. Domain-induced budding of vesicles. Phys Rev Lett 70: 2964-2967.
63. Kim B, Kramer H, Yamamoto A, Kominami E, Kohsaka S, Akazawa C. 2001. Molecular characterization of mammalian homologues of class C Vps proteins that interact with syntaxin-7. J Biol Chem 276: 29393-29402.
64. Kinchen JM, Ravichandran KS. 2010. Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464: 778-782.
65. Kramer L, Ungermann C. 2011. HOPS drives vacuole fusion by binding the vacuolar SNARE complex and the Vam7 PX domain via two distinct sites. Mol Biol Cell 22: 2601-2611.
66. Lachmann J, Ungermann C, Engelbrecht-Vandre S. 2011. Rab GTPases and tethering in the yeast endocytic pathway. Small GTPases 2: 182-186.
67. Lachmann J, Barr FA, Ungermann C. 2012. The Msb3/Gyp3 GAP controls the activity of the Rab GTPases Vps21 and Ypt7 at endosomes and vacuoles. Mol Biol Cell 23: 2516-2526.
68. Lanzetti L, Rybin V, Malabarba MG, Christoforidis S, Scita G, Zerial M, Di Fiore PP. 2000. The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature 408: 374-377.
69. Lanzetti L, Palamidessi A, Areces L, Scita G, Di Fiore PP. 2004. Rab5 is a signalling GTPase involved in actin remodeling by receptor tyrosine kinases. Nature 429: 309-314.
70. Liu AP, Fletcher DA. 2006. Actin polymerization serves as a membrane domain switch in model lipid bilayers. Biophys J 91: 4064-4070.
71. Liu J, Kaksonen M, Drubin DG, Oster G. 2006. Endocytic vesicle scission by lipid phase boundary forces. Proc Natl Acad Sci 103: 10277-10282.
72. Liu T-T, Gomez TS, Sackey BK, Billadeau DD, Burd CG. 2012. Rab GTPase regulation of retromer-mediated cargo export during endosome maturation. Mol Biol Cell 23: 2505-2515.
73. Lobingier BT, Merz AJ. 2012. Sec1/Munc18 protein Vps33 binds to SNARE domains and the quaternary SNARE complex. Mol Biol Cell 23: 4611-4622.
74. Markgraf DF, Ahnert F, Arlt H, Mari M, Peplowska K, Epp N, Griffith J, Reggiori F, Ungermann C. 2009. The CORVET subunit Vps8 cooperates with the Rab5 homolog Vps21 to induce clustering of late endosomal compartments. Mol Biol Cell 20: 5276-5289.
75. Mayor S, Presley JF, Maxfield FR. 1993. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J Cell Biol 121: 1257-1269.
76. McMahon HT, Gallop JL. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438: 590-596.
77. McNiven MA, Kim L, Krueger EW, Orth JD, Cao H, Wong TW. 2000. Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151: 187-198.
78. Merrifield CJ, Kaksonen M. 2014. Endocytic accessory factors and regulation of clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016733.
79. Mima J, Wickner W. 2009. Phosphoinositides and SNARE chaperones synergistically assemble and remodel SNARE complexes for membrane fusion. Proc Natl Acad Sci 106: 16191-16196.
80. Morel E, Parton RG, Gruenberg J. 2009. Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev Cell 16: 445-457.
81. Morrison HA, Dionne H, Rusten TE, Brech A, Fisher WW, Pfeiffer BD, Celniker SE, Stenmark H, Bilder D. 2008. Regulation of early endosomal entry by the Drosophila tumor suppressors Rabenosyn and Vps45. Mol Biol Cell 19: 4167-4176.
82. Murray JW, Sarkar S, Wolkoff AW. 2008. Single vesicle analysis of endocytic fission on microtubules in vitro. Traffic 9: 833-847.
83. Nickerson DP, Brett CL, Merz AJ. 2009. Vps-C complexes: Gatekeepers of endolysosomal traffic. Curr Opin Cell Biol 21: 543-551.
84. Nickerson DP, Russell MRG, Lo S-Y, Chapin HC, Milnes JM, Merz AJ. 2012. Termination of isoform-selective Vps21/Rab5 signaling at endolysosomal organelles by Msb3/Gyp3. Traffic 13: 1411-1428.
85. Nielsen E, Christoforidis S, Uttenweiler-Joseph S, Miaczynska M, Dewitte F, Wilm M, Hoflack B, Zerial M. 2000. Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol 151: 601-612.
86. Nordmann M, Cabrera M, Perz A, Brocker C, Ostrowicz CW, Engelbrecht-Vandre S, Ungermann C. 2010. The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 20: 1654-1659.
87. Ohya T, Miaczynska M, Coskun U, Lommer B, Runge A, Drechsel D, Kalaidzidis Y, Zerial M. 2009. Reconstitution of Rab-and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459: 1091-1097.
88. Ostrowicz CW, Brocker C, Ahnert F, Nordmann M, Lachmann J, Peplowska K, Perz A, Auffarth K, Engelbrecht-Vandre S, Ungermann C. 2010. Defined subunit arrangement and rab interactions are required for functionality of the HOPS tethering complex. Traffic 11: 1334-1346.
89. Pant S, Sharma M, Patel K, Caplan S, Carr CM, Grant BD. 2009. AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 11: 1399-1410.
90. Park L, Thomason PA, Zech T, King JS, Veltman DM, Carnell M, Ura S, Machesky LM, Insall RH. 2013. Cyclical action of the WASH complex: FAM21 and capping protein drive WASH recycling, not initial recruitment. Dev Cell 24: 169-181.
91. Peplowska K, Markgraf DF, Ostrowicz CW, Bange G, Ungermann C. 2007. The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Cell 12: 739-750.
92. Peterson MR, Burd CG, Emr SD. 1999. Vac1p coordinates Rab and phosphatidylinositol 3-kinase signaling in Vps45p-dependent vesicle docking/fusion at the endosome. Curr Biol 9: 159-162.
93. Piotrowski JT, Gomez TS, Schoon RA, Mangalam AK, Billadeau DD. 2013. WASH knockout T cells demonstrate defective receptor trafficking, proliferation, and effector function. Mol Cell Biol 33: 958-973.
94. Plemel RL, Lobingier BT, Brett CL, Angers CG, Nickerson DP, Paulsel A, Sprague D, Merz AJ. 2011. Subunit organization and Rab interactions of Vps-C protein complexes that control endolysosomal membrane traffic. Mol Biol Cell 22: 1353-1363.
95. Pols MS, ten Brink C, Gosavi P, Oorschot V, Klumperman J. 2012. The HOPS proteins hVps41 and hVps39 are required for homotypic and heterotypic late endosome fusion. Traffic 14: 219-232.
96. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A. 2010. Identification of the switch in early-to-late endosome transition. Cell 141: 497-508.
97. Pulipparacharuvil S, Akbar MA, Ray S, Sevrioukov EA, Haberman AS, Rohrer J, Kramer H. 2005. Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J Cell Sci 118: 3663-3673.
98. 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.
99. Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, Fein A, Caplan S, Joyner AL, Horowitz M. 2006. Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7: 52-60.
100. Richardson S, Winistorfer S, Poupon V, Luzio J, Piper R. 2004. Mammalian late vacuole protein sorting orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol Biol Cell 15: 1197-1210.
101. 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.
102. Rojas R, van Vlijmen T, Mardones GA, Prabhu Y, Rojas AL, Mohammed S, Heck AJ, Raposo G, van der Sluijs P, Bonifacino JS. 2008. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 183: 513-526.
103. Romer W, Pontani L-L, Sorre B, Rentero C, Berland L, Chambon V, Lamaze C, Bassereau P, Sykes C, Gaus K, et al. 2010. Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 140: 540-553.
104. Ropers F, Derivery E, Hu H, Garshasbi M, Karbasiyan M, Herold M, Nurnberg G, Ullmann R, Gautreau A, Sperling K, et al. 2011. Identification of a novel candidate gene for non-syndromic autosomal recessive intellectual disability: The WASH complex member SWIP. Hum Mol Genet 20: 2585-2590.
105. Rubino M, Miaczynska M, Lippe R, Zerial M. 2000. Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem 275: 3745-3748.
106. Seals D, Eitzen G, Margolis N, Wickner W, Price A. 2000. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc Natl Acad Sci 97: 9402-9407.
107. Seaman MNJ. 2012. The retromer complex-Endosomal protein recycling and beyond. J Cell Sci 125: 4693-4703.
108. Seaman MNJ, 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: 2371-2382.
109. Seaman MNJ, Gautreau A, Billadeau DD. 2013. Retromermediated endosomal protein sorting: All WASHed up! Trends Cell Biol 23: 522-528.
110. Setty SRG, Tenza D, Truschel ST, Chou E, Sviderskaya EV, Theos AC, Lamoreux ML, Di Pietro SM, Starcevic M, Bennett DC, et al. 2007. BLOC-1 is required for cargospecific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol Biol Cell 18: 768-780.
111. Simonsen A, Lippe R, Christoforidis S, Gaullier J, Brech A, Callaghan J, Toh B, Murphy C, Zerial M, Stenmark H. 1998. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion [see comments]. Nature 394: 494-498.
112. Soldati T, Schliwa M. 2006. Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 7: 897-908.
113. 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.
114. Steinberg F, Gallon M, Winfield M, Thomas E, 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: 1-13.
115. Stroupe C, Collins K, Fratti R, Wickner W. 2006. Purification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p. EMBO J 25: 1579-1589.
116. Stroupe C, Hickey CM, Mima J, Burfeind AS, Wickner W. 2009. Minimal membrane docking requirements revealed by reconstitution of RabGTPase-dependent membrane fusion from purified components. Proc Natl Acad Sci 106: 17626-17633.
117. Subramanian S, Woolford CA, Jones EW. 2004. The Sec1/Munc18 protein, Vps33p, functions at the endosome and the vacuole of Saccharomyces cerevisiae. Mol Biol Cell 15: 2593-2605.
118. Suetsugu S, Gautreau A. 2012. Synergistic BAR-NPF interactions in actin-driven membrane remodeling. Trends Cell Biol 22: 141-150.
119. Tall G, Hama H, DeWald D, Horazdovsky B. 1999. The phosphatidylinositol 3-phosphate binding protein Vac1p interacts with a Rab GTPase and a Sec1p homologue to facilitate vesicle-mediated vacuolar protein sorting. Mol Biol Cell 10: 1873-1889.
120. Temkin P, Lauffer B, Jager S, Cimermancic P, Krogan NJ, Zastrow von M. 2011. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat Cell Biol 13: 715-721.
121. van Dam EM, Broeke Ten T, Jansen K, Spijkers P, Stoorvogel W. 2002. Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem 277: 48876-48883.
122. Vonderheit A, Helenius A. 2005. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 3: e233.
123. Wickner W. 2010. Membrane fusion: Five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu Rev Cell Dev Biol 26: 115-136.
124. Wurmser AE, Sato TK, Emr SD. 2000. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J Cell Biol 151: 551-562.
125. 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: 1583-1594.
126. Yu I-M, Hughson FM. 2010. Tethering factors as organizers of intracellular vesicular traffic. Annu Rev Cell Dev Biol 26: 137-156.
127. Zech T, Calaminus SDJ, Caswell P, Spence HJ, Carnell M, Insall RH, Norman J, Machesky LM. 2011. The Arp2/3 activatorWASH regulates a5b1-integrin-mediated invasive migration. J Cell Sci 124: 3753-3759.
128. 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 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485: 465-470.
129. Zick M, Wickner W. 2012. Phosphorylation of the effector complex HOPS by the vacuolar kinase Yck3p confers Rab nucleotide specificity for vacuole docking and fusion. Mol Biol Cell 23: 3429-3437.