Rab Proteins and the Compartmentalization of the Endosomal system

Cold Spring Harbor Perspectives in Biology

Volumn 6, Issue 11, 2014, Pages 1-25

  Wandinger Ness, Angela ^a   Zerial, Marino ^b  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903772646     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a016162     Document Type: Article

References (231)

1. Agola JO, Jim PA, Ward HH, Basuray S, Wandinger-Ness A. 2011. Rab GTPases as regulators of endocytosis, targets of disease and therapeutic opportunities. Clin Genet 80: 305-318.
2. Aloisi AL, Bucci C. 2013. Rab GTPases-cargo direct interactions: Fine modulators of intracellular trafficking. Histol Histopathol 28: 839-849.
3. Alpy F, Rousseau A, Schwab Y, Legueux F, Stoll I, Wendling C, Spiegelhalter C, Kessler P, Mathelin C, Rio MC, et al. 2013. STARD3/STARD3NL and VAP make a novel molecular tether between late endosomes and the ER. J Cell Sci 126: 5500-5512.
4. Ambrosio AL, Boyle JA, Di Pietro SM. 2012. Mechanism of platelet dense granule biogenesis: Study of cargo transport and function of Rab32 and Rab38 in a model system. Blood 120: 4072-4081.
5. Arjonen A, Alanko J, Veltel S, Ivaska J. 2012. Distinct recycling of active and inactive beta1 integrins. Traffic 13: 610-625.
6. Babbey CM, Bacallao RL, Dunn KW. 2010. Rab10 associates with primary cilia and the exocyst complex in renal epithelial cells. Am J Physiol Renal Physiol 299: F495-F506.
7. Bananis E, Nath S, Gordon K, Satir P, Stockert RJ, Murray JW, Wolkoff AW. 2004. Microtubule-dependent movement of late endocytic vesicles in vitro: Requirements for Dynein and Kinesin. Mol Biol Cell 15: 3688-3697.
8. Banta LM, Robinson JS, Klionsky DJ, Emr SD. 1988. Organelle assembly in yeast: Characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J Cell Biol 107: 1369-1383.
9. Barbero P, Buell E, Zulley S, Pfeffer SR. 2001. TIP47 is not a component of lipid droplets. J Biol Chem 276: 24348-24351.
10. Barbero P, Bittova L, Pfeffer SR. 2002.Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J Cell Biol 156: 511-518.
11. Barbieri MA, Roberts RL, Gumusboga A, Highfield H, Alvarez-Dominguez C, Wells A, Stahl PD. 2000. Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a. J Cell Biol 151: 539-550.
12. Barr FA. 2013. Review series: Rab GTPases and membrane identity: Causal or inconsequential? J Cell Biol 202: 191-199.
13. BasuRay S, Mukherjee S, Romero E, Wilson MC, Wandinger-Ness A. 2010. Rab7 mutants associated with Charcot-Marie-Tooth disease exhibit enhanced NGFstimulated signaling. PLoS ONE 5: e15351.
14. BasuRay S, Agola J, Jim PA, Seaman MN, Wandinger-Ness A. 2012. Rab7 in endocytosis and signaling. In The encyclopedia of signaling molecules (ed. Choi S), pp. 1536-1547.
15. Springer, Heidelberg, BasuRay S, Mukherjee S, Romero EG, Seaman MN, Wandinger-Ness A. 2013. Rab7 mutants associated with Charcot-Marie-Tooth disease cause delayed growth factor receptor transport and altered endosomal and nuclear signaling. J Biol Chem 288: 1135-1149.
16. Bhagatji P, Leventis R, Rich R, Lin CJ, Silvius JR. 2010. Multiple cellular proteins modulate the dynamics of Kras association with the plasma membrane. Biophys J 99: 3327-3335.
17. Blumer J, Wu YW, Goody RS, Itzen A. 2012. Specific localization of Rabs at intracellular membranes. Biochem Soc Trans 40: 1421-1425.
18. Blumer J, Rey J, Dehmelt L, Mazel T, Wu YW, Bastiaens P, Goody RS, Itzen A. 2013. RabGEFs are a major determinant for specific Rab membrane targeting. J Cell Biol 200: 287-300.
19. Bohdanowicz M, Balkin DM, De Camilli P, Grinstein S. 2012. Recruitment of OCRL and Inpp5B to phagosomes by Rab5 and APPL1 depletes phosphoinositides and attenuates Akt signaling. Mol Biol Cell 23: 176-187.
20. Bucci C, Parton RG, Mather IH, Stunnenberg H, Simons K, Hoflack B, Zerial M. 1992. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70: 715-728.
21. Bucci C, De Gregorio L, Bruni CB. 2001. Expression analysis and chromosomal assignment of PRA1 and RILP genes. Biochem Biophys Res Commun 286: 815-819.
22. Bulankina AV, Deggerich A, Wenzel D, Mutenda K, Wittmann JG, Rudolph MG, Burger KN, Honing S. 2009. TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 185: 641-655.
23. Bultema JJ, Ambrosio AL, Burek CL, Di Pietro SM. 2012. BLOC-2, AP-3, and AP-1 proteins function in concert with Rab38 and Rab32 proteins to mediate protein trafficking to lysosome-related organelles. J Biol Chem 287: 19550-19563.
24. Buranda T, BasuRay S, Swanson S, Agola J, Bondu V, Wandinger-Ness A. 2013. Rapid parallel flowcytometry assays of active GTPases using effector beads. Anal Biochem 442: 149-157.
25. Burd C, Cullen PJ. 2014. Retromer: A master conductor of endosome sorting. Cold Spring Harb Perspect Biol 6: a016774.
26. Burguete AS, Fenn TD, Brunger AT, Pfeffer SR. 2008. Rab and Arl GTPase family members cooperate in the localization of the golgin GCC185. Cell 132: 286-298.
27. Cantalupo G, Alifano P, Roberti V, Bruni CB, Bucci C. 2001. Rab-interacting lysosomal protein (RILP): The Rab7 effector required for transport to lysosomes. EMBO J 20:683-693.
28. Cao C, Backer JM, Laporte J, Bedrick EJ, Wandinger-Ness A. 2008. Sequential actions of myotubularin lipid phosphatases regulate endosomal PI3Pand growth factor receptor trafficking. Mol Biol Cell 19: 3334-3346.
29. Carlton JG, Cullen PJ. 2005. Coincidence detection in phosphoinositide signaling. Trends Cell Biol 15: 540-547.
30. Carr CM, Rizo J. 2010. At the junction of SNARE and SM protein function. Curr Opin Cell Biol 22: 488-495.
31. Carroll KS, Hanna J, Simon I, Krise J, Barbero P, Pfeffer SR. 2001. Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science 292:1373-1376.
32. Carvalho FA, Carneiro FA, Martins IC, Assuncao-Miranda I, Faustino AF, Pereira RM, Bozza PT, Castanho MA, Mohana-Borges R, Da Poian AT, et al. 2012. Dengue virus capsid protein binding to hepatic lipid droplets (LD) is potassium ion dependent and is mediated by LD surface proteins. J Virol 86: 2096-2108.
33. Chavrier P, Goud B. 1999. The role of ARF and Rab GTPases in membrane transport. Curr Opin Cell Biol 11: 466-475.
34. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62: 317-329.
35. Chavrier P, Gorvel JP, Stelzer E, Simons K, Gruenberg J, Zerial M. 1991. Hypervariable C-terminal domain of Rab proteins acts as a targeting signal. Nature 353: 769-772.
36. Chen Y, Lippincott-Schwartz J. 2013. Rab10 delivers GLUT4 storage vesicles to the plasma membrane. Commun Integr Biol 6: e23779.
37. Chen H, Yang J, Low PS, Cheng JX. 2008. Cholesterol level regulates endosome motility via Rab proteins. Biophys J 94: 1508-1520.
38. Chen PI, Kong C, Su X, Stahl PD. 2009a. Rab5 isoforms differentially regulate the trafficking and degradation of epidermal growth factor receptors. J Biol Chem 284: 30328-30338.
39. Chen Y, Honeychurch KM, Yang G, Byrd CM, Harver C, Hruby DE, Jordan R. 2009b. Vaccinia virus p37 interacts with host proteins associated with LE-derived transport vesicle biogenesis. Virol J 6: 44.
40. 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: 545-560.
41. Cheng J, Liu W, Duffney LJ, Yan Z. 2013. SNARE proteins are essential in the potentiation of NMDA receptors by group II metabotropic glutamate receptors. J Physiol 591: 3935-3947.
42. Choudhury A, Sharma DK, Marks DL, Pagano RE. 2004. Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit Rab4 and perturb membrane recycling. Mol Biol Cell 15: 4500-4511.
43. Christoforidis S, McBride H., Burgoyne RD, Zerial M. 1999. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397: 621-625.
44. Cocucci E, Aguet F, Boulant S, Kirchhausen T. 2012. The first five seconds in the life of a clathrin-coated pit. Cell 150: 495-507.
45. Cossart P, Helenius A. 2014. Endocytosis of viruses and bacteria. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016972.
46. Cui Z, Zhang S. 2013. Regulation of the human ether-a-gogo-related gene (hERG) channel by Rab4 protein through neural precursor cell-expressed developmentally downregulated protein 4-2 (Nedd4-2). J Biol Chem 288: 21876-21886.
47. deCurtis I, Meldolesi J. 2012. Cell surface dynamics—How Rho GTPases orchestrate the interplay between the plasma membrane and the cortical cytoskeleton. J Cell Sci 125: 4435-4444.
48. 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.
49. de Renzis S, Sonnichsen B, Zerial M.. 2002. Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes.Nat Cell Biol 4: 124-133.
50. Dickison VM, Richmond AM, Abu Irqeba A, Martak JG, Hoge SC, Brooks MJ, Othman MI, Khanna R, Mears AJ, Chowdhury AY, et al. 2012. A role for prenylated rab acceptor 1 in vertebrate photoreceptor development. BMC Neurosci 13: 152.
51. Diekmann Y, Seixas E, Gouw M, Tavares-Cadete F, Seabra MC, Pereira-Leal JB. 2011. Thousands of rab GTPases for the cell biologist. PLoS Comput Biol 7: e1002217.
52. Di Fiore PP, De Camilli P. 2001. Endocytosis and signaling. an inseparable partnership. Cell 106: 1-4.
53. Di Fiore PP, von Zastrow M. 2014. Endocytosis, signaling and beyond. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016865.
54. Dirac-Svejstrup AB, Sumizawa T, Pfeffer SR. 1997. Identification of a GDI displacement factor that releases endosomal Rab GTPases from Rab-GDI. EMBO J 16: 465-472.
55. Dong B, Kakihara K, Otani T, Wada H, Hayashi S. 2013. Rab9 and retromer regulate retrograde trafficking of luminal protein required for epithelial tube length control. Nat Commun 4: 1358.
56. Erdmann KS, Mao Y, McCrea HJ, Zoncu R, Lee S, Paradise S, Modregger J, Biemesderfer D, Toomre D, De Camilli P. 2007. A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway. Dev Cell 13: 377-390.
57. Esters H, Alexandrov K, Iakovenko A, Ivanova T, Thoma N, Rybin V, Zerial M, Scheidig AJ, Goody RS. 2001. Vps9, Rabex-5 and DSS4: Proteins with weak but distinct nucleotide-exchange activities for Rab proteins. J Mol Biol 310: 141-156.
58. Feng Y, Press B, Wandinger-Ness A. 1995. Rab 7: An important regulator of late endocytic membrane traffic. J Cell Biol 131: 1435-1452.
59. Freeman C, Seaman MN, Reid E. 2013. The hereditary spastic paraplegia protein strumpellin: Characterisation in neurons and of the effect of disease mutations on WASH complex assembly and function. Biochim Biophys Acta 1832: 160-173.
60. 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.
61. Fukuda M. 2003. Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J Biol Chem 278: 15373-15380.
62. Fukuda M. 2013. Rab27 effectors, pleiotropic regulators in secretory pathways. Traffic 14: 949-963.
63. Ganley IG, Pfeffer SR. 2006. Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells. J Biol Chem 281: 17890-17899.
64. Garg S, Sharma M, Ung C, Tuli A, Barral DC, Hava DL, Veerapen N, Besra GS, Hacohen N, Brenner MB. 2011. Lysosomal trafficking, antigen presentation, and microbial killing are controlled by the Arf-like GTPase Arl8b. Immunity 35: 182-193.
65. Gaullier JM, Simonsen A, D’Arrigo A, Bremnes B, Stenmark H, Aasland R. 1998. FYVE fingers bind PtdIns(3)P. Nature 394: 432-433.
66. Gautreau A, Oguievetskaia K, Ungermann C. 2014. Function and regulation of the endsomal fusion and fission. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect. a016832.
67. Gavriljuk K, Itzen A, Goody RS, Gerwert K, Kotting C. 2013. Membrane extraction of Rab proteins by GDP dissociation inhibitor characterized using attenuated total reflection infrared spectroscopy. Proc Natl Acad Sci 110: 13380-13385.
68. Gillooly DJ, Morrow IC, Lindsay M, Gould R, Bryant NJ, Gaullier JM, Parton RG, Stenmark H. 2000. Localization of phosphatidylinositol-3-phosphate in yeast and mammalian cells. EMBO J 19: 4577-4588.
69. Gonzalez Gaitan M, Jülicher F. 2014. The role of endocytosis during morphogenetic signaling. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016881.
70. Gorvel JP, Chavrier P, Zerial M, Gruenberg J. 1991. Rab5 controls early endosome fusion in vitro. Cell 64: 915-925.
71. Goueli BS, Powell MB, Finger EC, Pfeffer SR. 2012. TBC1D16 is a Rab4A GTPase activating protein that regulates receptor recycling and EGF receptor signaling. Proc Natl Acad Sci 109: 15787-15792.
72. Grosshans BL, Ortiz D, Novick P. 2006. Rabs and their effectors: Achieving specificity in membrane traffic. Proc Natl Acad Sci 103: 11821-11827.
73. Guo Z, Hou X, Goody RS, Itzen A. 2013. Intermediates in the guanine nucleotide exchange reaction of Rab8 protein catalyzed by guanine nucleotide exchange factors Rabin8 and GRAB. J Biol Chem 288: 32466-32474.
74. Gutierrez MG, Munafo DB, Beron W, Colombo MI. 2004. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 117: 2687-2697.
75. Haas AK, Fuchs E, Kopajtich R, Barr FA. 2005. A GTPaseactivating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 7: 887-893.
76. Haas AK, Yoshimura S, 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.
77. Hall A. 2012. Rho family GTPases. Biochem Soc Trans 40: 1378-1382.
78. Hayes GL, Brown FC, Haas AK, Nottingham RM, Barr FA, Pfeffer SR. 2009. Multiple Rab GTPase binding sites in GCC185 suggest a model for vesicle tethering at the trans-Golgi. Mol Biol Cell 20:209-217.
79. Hellberg C, Schmees C, Karlsson S, Ahgren A, Heldin CH. 2009. Activation of protein kinase Ca is necessary for sorting the PDGFb-receptor to Rab4a-dependent recycling. Mol Biol Cell 20: 2856-2863.
80. Henry RM, Hoppe AD, Joshi N, Swanson JA. 2004. The uniformity of phagosome maturation in macrophages. J Cell Biol 164: 185-194.
81. 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.
82. Holtta-Vuori M, Tanhuanpaa K, Mobius W, Somerharju P, Ikonen E. 2002.Modulation of cellular cholesterol transport and homeostasis by Rab11. Mol Biol Cell 13: 3107-3122.
83. 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.
84. Hume AN, Collinson LM, Rapak A, Gomes AQ, Hopkins CR, Seabra MC. 2001. Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J Cell Biol 152: 795.
85. Huotari J, Helenius A. 2011. Endosome maturation. EMBO J 30: 3481-3500.
86. Hutagalung AH, Novick PJ. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119-149.
87. Hynson RM, Jeffries CM, Trewhella J, Cocklin S. 2012. Solution structure studies of monomeric human TIP47/perilipin-3 reveal a highly extended conformation. Proteins 80: 2046-2055.
88. Hyvola N, Diao A, McKenzie E, Skippen A, Cockcroft S, Lowe M. 2006. Membrane targeting and activation of the Lowe syndrome protein OCRL1 by rab GTPases. EMBO J 25: 3750-3761.
89. Jackson LK, Nawabi P, Hentea C, Roark EA, Haldar K. 2008. The Salmonella virulence protein SifA is a G protein antagonist. Proc Natl Acad Sci 105: 14141-14146.
90. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, Eskelinen EL. 2004. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 117: 4837-4848.
91. Jahn R, Scheller RH. 2006. SNAREs—Engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643.
92. Jing J, Prekeris R. 2009. Polarized endocytic transport: The roles of Rab11 and Rab11-FIPs in regulating cell polarity. Histol Histopathol 24: 1171-1180.
93. Johansson M, Rocha N, Zwart W, Jordens I, Janssen L, Kuijl C, Olkkonen VM, Neefjes J. 2007. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor bIII spectrin. J Cell Biol 176: 459-471.
94. 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-dynactin motors. Curr Biol 11: 1680-1685.
95. Kelly EE, Horgan CP, McCaffrey MW. 2012. Rab11 proteins in health and disease. Biochem Soc Trans 40: 1360-1367.
96. Kerr MC, Lindsay MR, Luetterforst R, Hamilton N, Simpson F, Parton RG, Gleeson PA, Teasdale RD. 2006. Visualisation of macropinosome maturation by the recruitment of sorting nexins. J Cell Sci 119: 3967-3980.
97. Kinsella BT, Maltese WA. 1992. Rab GTP-binding proteins with three different carboxyl-terminal cysteine motifs are modified in vivo by 20-carbon isoprenoids. J Biol Chem 267: 3940-3945.
98. Klopper TH, Kienle N, Fasshauer D, Munro S. 2012. Untangling the evolution of Rab G proteins: Implications of a comprehensive genomic analysis. BMC Biol 10: 71.
99. Klumperman J, Raposo G. 2014. The complex ultrastructure of the endolysosomal system. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a016857.
100. Kotting C, Gerwert K. 2013. The dynamics of the catalytic site in small GTPases, variations on a common motif. FEBS Lett 587: 2025-2027.
101. Lane KT, Beese LS. 2006. Thematic review series: Lipid posttranslational modifications. Structural biology of protein farnesyltransferase and geranylgeranyltransferase type I. J Lipid Res 47: 681-699.
102. 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.
103. Lanzetti L, Palamidessi A, Areces L, Scita G, Di Fiore PP. 2004. Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases.Nature 429: 309-314.
104. Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance DWJ, Mercer JA, Bahler M, Goldenring JR. 2001. Myosin Vb is associated with plasma membrane recycling systems. Mol Biol Cell 12: 1843-1857.
105. Lawe DC, Patki V, Heller-Harrison R, Lambright D, Corvera S. 2000. The FYVE domain of earlyendosome antigen 1 is required for both phosphatidylinositol-3-phosphate and Rab5 binding. Critical role of this dual interaction for endosomal localization. J Biol Chem 275: 3699-3705.
106. Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, Mayran N, Faure J, Gruenberg J. 2002. Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J 21: 1289-1300.
107. Lindsay AJ, Hendrick AG, Cantalupo G, Senic-Matuglia F, Goud B, Bucci C, McCaffrey MW. 2002. Rab coupling protein (RCP), a novel Rab4 and Rab11 effector protein. J Biol Chem 277: 12190-12199.
108. Lindsay AJ, Jollivet F, Horgan CP, Khan AR, Raposo G, McCaffrey MW, Goud B. 2013. Identification and characterization of multiple novel Rab-myosin Va interactions. Mol Biol Cell 24: 3420-3434.
109. Lo SY, Brett CL, Plemel RL, Vignali M, Fields S, Gonen T, Merz AJ. 2012. Intrinsic tethering activity of endosomal Rab proteins. Nat Struct Mol Biol 19: 40-47.
110. Lombardi D, Soldati T, Riederer MA, Goda Y, Zerial M, Pfeffer SR. 1993. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J 12: 677-682.
111. Longatti A, Tooze SA. 2009. Vesicular trafficking and autophagosome formation. Cell Death Differ 16:956-965.
112. 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: 659-675.
113. Mao X, Kikani CK, Riojas RA, Langlais P, Wang L, Ramos FJ, Fang Q, Christ-Roberts CY, Hong JY, Kim RY, et al. 2006. APPL1 binds to adiponectin receptors and mediates adiponectin signalling and function. Nat Cell Biol 8: 516-523.
114. Marijuan PC, del Moral R, Navarro J. 2013. On eukaryotic intelligence: Signaling system’s guidance in the evolution of multicellular organization. BioSystems 114: 8-24.
115. Matesic LE, Yip R, Reuss AE, Swing DA, O’Sullivan TN, Fletcher CF, Copeland NG, Jenkins NA. 2001. Mutations in Mlph, encoding a member of the Rab effector family, cause the melanosome transport defects observed in leaden mice. Proc Natl Acad Sci 98: 10238-10243.
116. Matsui T, Ohbayashi N, Fukuda M. 2012. The Rab interacting lysosomal protein (RILP) homology domain functions as a novel effector domain for small GTPase Rab36: Rab36 regulates retrograde melanosome transport in melanocytes. J Biol Chem 287: 28619-28631.
117. Mayer A, Wickner W. 1997. Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). J Cell Biol 136: 307-317.
118. Mazelova J, Astuto-Gribble L, Inoue H, Tam BM, Schonteich E, Prekeris R, Moritz OL, Randazzo PA, Deretic D. 2009. Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J 28:183-192.
119. McBride H., Rybin V, Murphy C, Giner A, Teasdale R, Zerial M. 1999. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98: 377-386.
120. McCray BA, Skordalakes E, Taylor JP. 2010. Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation. Hum Mol Genet 19: 1033-1047.
121. McGourty K, Thurston TL, Matthews SA, Pinaud L, Mota LJ, Holden DW. 2012. Salmonella inhibits retrograde trafficking of mannose-6-phosphate receptors and lysosome function. Science 338: 963-967.
122. McLauchlan H, Newell J, Morrice N, Osborne A, West M, Smythe E. 1998. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr Biol 8: 34-45.
123. McNew JA, Weber T, Parlati F, Johnston RJ, Melia TJ, Sollner TH, Rothman JE. 2000. Close is not enough: SNAREdependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J Cell Biol 150: 105-117.
124. Menasche G, Pastural E, Feldmann J, Certain S, Ersoy F, Dupuis S, Wulffraat N, Bianchi D, Fischer A, Le Deist F, et al. 2000. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat Genet 25: 173-176.
125. Miaczynska MS, Christoforidis A, Giner A, Shevchenko S, Uttenweiler-Joseph B, Habermann M, Wilm RG, Parton, Zerial M. 2004. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 116: 445-456.
126. Mishra A, Eathiraj S, Corvera S, Lambright DG. 2010. Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of Early endosomal autoantigen 1 (EEA1). Proc Natl Acad Sci 107: 0866-10871.
127. Mitra S, Cheng KW, Mills GB. 2012. Rab25 in cancer: A brief update. Biochem Soc Trans 40: 1404-1408.
128. Mizuno-Yamasaki E, Rivera-Molina F, Novick P. 2012. GTPase networks in membrane traffic. Annu Rev Biochem 81: 637-659.
129. 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.
130. Murphy S, Martin S, Parton RG. 2009. Lipid droplet-organelle interactions; sharing the fats. Biochim Biophys Acta 1791: 441-447.
131. Murray JT, Panaretou C, Stenmark H, Miaczynska M, Backer JM. 2002. Role of Rab5 in the recruitment of hVps34/p150 to the early endosome. Traffic 3: 416-427.
132. Murray JL, Mavrakis M, McDonald NJ, Yilla M, Sheng J, Bellini WJ, Zhao L, Le Doux JM, Shaw MW, Luo CC, et al. 2005. Rab9 GTPase is required for replication of human immunodeficiency virus type 1, filoviruses, and measles virus. J Virol 79: 11742-11751.
133. Nagashima K, Torii S, Yi Z, Igarashi M, Okamoto K, Takeuchi T, Izumi T. 2002.Melanophilin directly links Rab27a and myosin Va through its distinct coiled-coil regions. FEBS Lett 517: 233-238.
134. Nielsen E, Severin F, Backer JM, Hyman AA, Zerial M. 1999. Rab5 regulates motility of early endosomes on microtubules. Nat Cell Biol 1: 376-382.
135. 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.
136. Novick P, Zerial M. 1997. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 9: 496-504.
137. Numrich J, Ungermann C. 2013. Endocytic Rabs in membrane trafficking and signaling. Biol Chem doi: 10.1515/hsz-2013-0258.
138. Oesterlin LK, Goody RS, Itzen A. 2012. Posttranslational modifications of Rab proteins cause effective displacement of GDP dissociation inhibitor. Proc Natl Acad Sci 109: 5621-5626.
139. 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.
140. Ortiz D, Medkova M, Walch-Solimena C, Novick P. 2002. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J Cell Biol 157: 1005-1015.
141. Pal A, Severin F, Lommer B, Shevchenko A, Zerial M. 2006. Huntingtin-HAP40 complex is a novel Rab5 effector that regulates early endosome motility and is up-regulated in Huntington’s disease. J Cell Biol 172: 605-618.
142. Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, Diaspro A, Lanzetti L, Scita G, Di Fiore PP. 2008. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134: 135-147.
143. Panzeri C, De Palma C, Martinuzzi A, Daga A, De Polo G, Bresolin N, Miller CC, Tudor EL, Clementi E, Bassi MT. 2006. The first ALS2 missense mutation associated with JPLS reveals new aspects of alsin biological function. Brain 129: 1710-1719.
144. Park HH. 2013. Structural basis of membrane trafficking by Rab family small G protein. Int J Mol Sci 14: 8912-8923.
145. Pelkmans L, Burli T, Zerial M, Helenius A. 2004. Caveolinstabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118: 767-780.
146. 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.
147. Pfeffer SR. 2011. Entry at the trans-face of the Golgi. Cold Spring Harb Perspect Biol 3: a005272.
148. Pfeffer SR. 2012. Rab GTPase localization and Rab cascades in Golgi transport. Biochem Soc Trans 40: 1373-1377.
149. Pfeffer SR. 2013a. Rab GTPase regulation of membrane identity. Curr Opin Cell Biol 25: 414-419.
150. Pfeffer SR. 2013b. A nexus for receptor recycling. Nat Cell Biol 15: 446-448.
151. Pfeffer S, Aivazian D. 2004. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 5: 886-896.
152. Platta HW, Stenmark H. 2011. Endocytosis and signaling. Curr Opin Cell Biol 23: 393-403.
153. 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.
154. Posor Y, Eichhorn-Gruenig M, Puchkov D, Schoneberg J, Ullrich A, Lampe A, Muller R, Zarbakhsh S, Gulluni F, Hirsch E, et al. 2013. Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499: 233-237.
155. Rasineni K, McVicker BL, Tuma DJ, McNiven MA, Casey CA. 2013. Rab GTPases associatewith isolated lipid droplets (LDs) and show altered content after ethanol administration: Potential role in alcohol-impaired LD metabolism. Alcohol Clin Exp Res doi: 10.1111/acer.12271.
156. 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: 1931-1941.
157. 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.
158. Rizo J, Sudhof TC. 2012. The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices— Guilty as charged? Annu Rev Cell Dev Biol 28: 279-308.
159. 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-p150Glued and late endosome positioning. J Cell Biol 185: 1209-1225.
160. Rojas AM, Fuentes G, Rausell A, Valencia A. 2012. The Ras protein superfamily: Evolutionary tree and role of conserved amino acids. J Cell Biol 196: 189-201.
161. Rush JS, Ceresa BP. 2013. RAB7 and TSG101 are required for the constitutive recycling of unliganded EGFRs via distinct mechanisms. Mol Cell Endocrinol 381: 188-197.
162. Sano H, Roach WG, Peck GR, Fukuda M, Lienhard GE. 2008. Rab10 in insulin-stimulated GLUT4 translocation. Biochem J 411: 89-95.
163. Sasaki T, Kikuchi A, Araki S, Hata Y, Isomura M, Kuroda S, Takai Y. 1990. Purification and characterization from bovine brain cytosol of a protein that inhibits the dissociation of GDP from and the subsequent binding of GTP to smg p25A, a ras p21-like GTP-binding protein. J Biol Chem 265: 2333-2337.
164. Saxena S, Bucci C, Weis J, Kruttgen A. 2005. The small GTPase Rab7 controls the endosomal trafficking and neuritogenic signaling of the nerve growth factor receptor TrkA. J Neurosci 25: 10930-10940.
165. Schmid SL, Mettlen M. 2013. Cell biology: Lipid switches and traffic control. Nature 499: 161-162.
166. Schnatwinkel C, Christoforidis S, Lindsay MR, Uttenweiler-Joseph S, Wilm M, Parton RG, Zerial M. 2004. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol 2: 1363-1380.
167. Schoebel S, Oesterlin LK, Blankenfeldt W, Goody RS, Itzen A. 2009. RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Mol Cell 36: 1060-1072.
168. Schu PV, Takegawa K, Fry MJ, Stack JH, Waterfield MD, Emr SD. 1993. Phosphatidylinositol-3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260: 88-91.
169. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A. 2007. Rab GTPases at a glance. J Cell Sci 120: 3905.
170. Seabra MC, Wasmeier C. 2004. Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol 16: 451-457.
171. Seabra MC, Reiss Y, Casey PJ, Brown MS, Goldstein JL. 1991. Protein farnesyltransferase and geranylgeranyltransferase share a common a subunit. Cell 65: 429-434.
172. Seabra MC, Mules EH, Hume AN. 2002. Rab GTPases, intracellular traffic and disease. Trends Mol Med 8: 23-30.
173. Seals DF, Eitzen G, Margolis N, Wickner W., Price A. 2000. AYpt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc Natl Acad Sci 97: 9402-9407.
174. Seaman MN. 2012. The retromer complex—Endosomal protein recycling and beyond. J Cell Sci 125: 4693-4702.
175. Seaman MN, Gautreau A, Billadeau DD. 2013. Retromermediated endosomal protein sorting: All WASHed up! Trends Cell Biol 23: 522-528.
176. Shin HW, Hayashi M, Christoforidis S, Lacas-Gervais S, Hoepfner S, Wenk MR, Modregger J, Uttenweiler-Joseph S, Wilm M, Nystuen A, et al. 2005. An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 170: 607-618.
177. Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M, Stenmark H. 1998. EEA1 links PI3K function to Rab5 regulation of endosome fusion. Nature 394: 494-498.
178. Simonsen A, Gaullier JM, D’Arrigo A, Stenmark H. 1999. The Rab5 effector EEA1 interacts directly with syntaxin-6. J Biol Chem 274: 28857-28860.
179. Sivars U, Aivazian D, Pfeffer S. 2005. Purification and properties of Yip3/PRA1 as a Rab GDI displacement factor. Methods Enzymol 403: 348-356.
180. Soldati T, Schliwa M. 2006. Powering membrane traffic in endocytosis and recycling. Nat Rev Mol Cell Biol 7: 897-908.
181. Solinger JA, Spang A. 2013. Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J 280: 2743-2757.
182. Somsel Rodman J, Wandinger-Ness A. 2000. Rab GTPases coordinate endocytosis. J Cell Sci 113: 183-192.
183. 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.
184. Stein MP, Feng Y, Cooper KL, Welford AM, Wandinger-Ness A. 2003. Human VPS34 and p150 are Rab7 interacting partners. Traffic 4: 754-771.
185. Stein MP, Cao C, Tessema M, Feng Y, Romero E, Welford A, Wandinger-Ness A. 2005. Interaction and functional analyses of human VPS34/p150 phosphatidylinositol-3-kinase complex with Rab7. Methods Enzymol 403: 628-649.
186. Stein M, Pilli M, Bernauer S, Habermann BH, Zerial M, Wade RC. 2012a. The interaction properties of the human Rab GTPase family—Comparative analysis reveals determinants of molecular binding selectivity. PLoSONE 7: e34870.
187. Stein MP, Muller MP, Wandinger-Ness A. 2012b. Bacterial pathogens commandeer Rab GTPases to establish intracellular niches. Traffic 13: 1565-1588.
188. Stenmark H. 2009.Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10: 513-525.
189. Stenmark H, Aasland R, Toh BH, D’Arrigo A. 1996. Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J Biol Chem 271: 24048-24054.
190. Stinchcombe JC, Barral DC, Mules EH, Booth S, Hume AN, Machesky LM, Seabra MC, Griffiths GM. 2001. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152: 825-834.
191. Stockli J, Davey JR, Hohnen-Behrens C, Xu A, James DE, Ramm G. 2008. Regulation of glucose transporter 4 translocation by the Rab guanosine triphosphatase-activating protein AS160/TBC1D4: Role of phosphorylation and membrane association. Mol Endocrinol 22: 2703-2715.
192. Strom M, Hume AN, Tarafder AK, Barkagianni E, Seabra MC. 2002. A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J Biol Chem 277: 25423-25430.
193. Stroupe C, Hickey CM, Mima J, Burfeind AS, Wickner W. 2009. Minimal membrane docking requirements revealed by reconstitution of Rab GTPase-dependent membrane fusion from purified components. Proc Natl Acad Sci 106: 17626-17633.
194. Tall GG, Barbieri MA, Stahl PD, Horazdovsky BF. 2001. Rasactivated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev Cell 1: 73-82.
195. Taub N, Teis D, Ebner HL, Hess MW, Huber LA. 2007. Late endosomal traffic of the epidermal growth factor receptor ensures spatial and temporal fidelity of mitogen-activated protein kinase signaling. Mol Biol Cell 18: 4698-4710.
196. Ullrich O, Stenmark H, Alexandrov K, Huber LA, Kaibuchi K, Sasaki T, Takai Y, Zerial M. 1993.
197. Rab GDP dissociation inhibitor as a general regulator for the membrane association of Rab proteins. J Biol Chem 268: 18143-18150.
198. 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.
199. Ungermann C, Price A, Wickner W. 2000. A new role for a SNARE protein as a regulator of the Ypt7/Rab-dependent stage of docking. Proc Natl Acad Sci 97: 8889-8891.
200. van der Kant R, Fish A, Janssen L, Janssen H, Krom S, Ho N, Brummelkamp T, Carette J, Rocha N, Neefjes J. 2013. Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J Cell Sci 126: 3462-3474.
201. Van Der Sluijs P, Hull M, Zahraoui A, Tavitian A, Goud B, Mellman I. 1991. The small GTP-binding protein Rab4 is associated with early endosomes. Proc Natl Acad Sci 88: 6313-6317.
202. van der Sluijs P, Hull M, Webster P, Māle P, Goud B, Mellman I. 1992. The small GTP-binding protein Rab4 controls an early sorting event on the endocytic pathway. Cell 70: 729-740.
203. van IJzendoorn SC, Tuvim MJ, Weimbs T, Dickey BF, Mostov KE. 2002. Direct interaction between Rab3b and the polymeric immunoglobulin receptor controls ligandstimulated transcytosis in epithelial cells. Dev Cell 2: 219-228.
204. Vardarajan BN, Bruesegem SY, Harbour ME, Inzelberg R, Friedland R, St George-Hyslop P, Seaman MN, Farrer LA. 2012. Identification of Alzheimer disease-associated variants in genes that regulate retromer function. Neurobiol Aging 33: 2231.e15-2231.e30.
205. Vieira OV, Bucci C, Harrison RE, Trimble WS, Lanzetti L, Gruenberg J, Schreiber AD, Stahl PD, Grinstein S. 2003. Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol-3-kinase. Mol Cell Biol 23: 2501-2514.
206. Vitale G, Rybin V, Christoforidis S, Thornqvist P, McCaffrey M, Stenmark H, Zerial M. 1998. Distinct Rab-binding domains mediate the interaction of Rabaptin-5 with GTP-bound Rab4 and Rab5. EMBO J 17: 1941-1951.
207. Vitelli R, Santillo M, Lattero D, Chiariello M, Bifulco M, Bruni CB, Bucci C. 1997. Role of the small GTPase Rab7 in the late endocytic pathway. J Biol Chem 272: 4391-4397.
208. Vogt DA, Camus G, Herker E, Webster BR, Tsou CL, Greene WC, Yen TS, Ott M. 2013. Lipid droplet-binding protein TIP47 regulates hepatitis C Virus RNA replication through interaction with the viral NS5A protein. PLoS Pathog 9: e1003302.
209. 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.
210. Wang L, Merz AJ, Collins KM, Wickner W. 2003. Hierarchy of protein assembly at the vertex ring domain for yeast vacuole docking and fusion. J Cell Biol 160: 365-374.
211. Wang J, Morita Y, Mazelova J, Deretic D. 2012. The Arf GAP ASAP1 provides a platform to regulate Arf4-and Rab11-Rab8-mediated ciliary receptor targeting. EMBO J 31: 4057-4071.
212. Ward HH, Brown-Glaberman U, Wang J, Morita Y, Alper SL, Bedrick EJ, Gattone VHn, Deretic D, Wandinger-Ness A. 2011. A conserved signal and GTPase complex are required for the ciliary transport of polycystin-1. Mol Biol Cell 22: 3289-3305.
213. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE. 1998. SNAREpins: Minimal machinery for membrane fusion. Cell 92: 759-772.
214. 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 (TRAPPII) complex-dependent trafficking of Rabin8 to the centrosome. Proc Natl Acad Sci 108: 2759-2764.
215. Wickner W, Schekman R. 2008. Membrane fusion. Nat Struct Mol Biol 15: 658-664.
216. Wideman J, Leung KF, Field MC, Dacks JB. 2014. The cell biology of the endocytic system from an evolutionary perspective. Cold Spring Harb Perspect Biol doi: 10. 1101/cshperspect.a016998.
217. Wiley HS. 2003. Trafficking of the ErbB receptors and its influence on signaling. Exp Cell Res 284: 78-88.
218. Wilson SM, Yip R, Swing DA, O’Sullivan TN, Zhang Y, Novak EK, Swank RT, Russell LB, Copeland NG, Jenkins NA. 2000. A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc Natl Acad Sci 97: 7933.
219. Wittinghofer A, Franken SM, Scheidig AJ, Rensland H, Lautwein A, Pai EF, Goody RS. 1993. Three-dimensional structure and properties of wild-type and mutant H-ras-encoded p21. Ciba Found Symp 176: 6-21.
220. Wu X, Rao K, Bowers MB, Copeland NG, Jenkins NA, Hammer JA. 2001. Rab27a enables myosin Va-dependent melanosome capture by recruiting the myosin to the organelle. J Cell Sci 114: 1091-1100.
221. Wu X, Wang F, Rao K, Sellers JR, Hammer JA, III. 2002a. Rab27a is an essential component of melanosome receptor for myosin Va. Mol Biol Cell 13:1735.
222. Wu XS, Rao K, Zhang H, Wang F, Sellers JR, Matesic LE, Copeland NG, Jenkins NA, Hammer JA. 2002b. Identification of an organelle receptor for myosin-Va. Nat Cell Biol 4: 271-278.
223. Wu YW, Oesterlin LK, Tan KT, Waldmann H, Alexandrov K, Goody RS. 2010.Membrane targeting mechanism of Rab GTPases elucidated by semisynthetic protein probes. Nat Chem Biol 6: 534-540.
224. Wu X, Bradley MJ, Cai Y, Kummel D, De La Cruz EM, Barr FA, Reinisch KM. 2011. Insights regarding guanine nucleotide exchange from the structure of a DENN-domain protein complexed with its Rab GTPase substrate. Proc Natl Acad Sci 108: 18672-18677.
225. Yang M, Chen T, Han C, Li N, Wan T, Cao X. 2004. Rab7b, a novel lysosome-associated small GTPase, is involved in monocytic differentiation of human acute promyelocytic leukemia cells. Biochem Biophys Res Commun 318: 792-799.
226. Yoshimura S, Gerondopoulos A, Linford A, Rigden DJ, Barr FA. 2010. Family-wide characterization of the DENN domain Rab GDP-GTP exchange factors. J Cell Biol 191: 367-381.
227. 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.
228. Zerial M, McBride H. 2001. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117.
229. Zick M, Wickner W. 2013. The tethering complex HOPS catalyzes assembly of the soluble SNARE Vam7 into fusogenic trans-SNARE complexes. Mol Biol Cell 24: 3746-3753.
230. Zimmerberg J, Gawrisch K. 2006. The physical chemistry of biological membranes. Nat Chem Biol 2: 564-567.
231. Zoncu R, Perera RM, Balkin DM, Pirruccello M, Toomre D, De Camilli P. 2009. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136: 1110-1121.