Structural biology of arf and rab GTPases' effector recruitment and specificity

Structure

Volumn 21, Issue 8, 2013, Pages 1284-1297

  Khan, Amir R ^a   Ménétrey, Julie ^b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; AUTOANTIGEN; BART PROTEIN; CHOLERA TOXIN; COAT PROTEIN COMPLEX I; DENND5 PROTEIN; EARLY ENDOSOMAL AUTOANTIGEN 1; FAMILY INTERACTING PROTEIN; GOLGIN 245; GRIP AND COILED DOMAIN CONTAINING PROTEIN 185; JANUS KINASE; JANUS KINASE INTERACTING PROTEIN 4; KINESIN; MEMBRANE PROTEIN; MITOTIC KINESIN LIKE PROTEIN 1; OCULOCEREBRORENAL SYNDROME OF LOWE PROTEIN 1; PHOSPHODIESTERASE; PHOSPHODIESTERASE DELTA; PROTEIN; RAB INTERACTING LYSOSOMAL PROTEIN; RAB PROTEIN; RABAPTIN 5; RABENOSYN 5; UNC119 PROTEIN; UNCLASSIFIED DRUG;

BINDING AFFINITY; CELL FUNCTION; CRYSTAL STRUCTURE; CRYSTALLIZATION; GOLGI COMPLEX; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; REVIEW;

EID: 84881414181     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.06.016     Document Type: Review

References (101)

1. D.F. Anthony, Y.Y. Sin, S. Vadrevu, N. Advant, J.P. Day, A.M. Byrne, M.J. Lynch, G. Milligan, M.D. Houslay, and G.S. Baillie β-Arrestin 1 inhibits the GTPase-activating protein function of ARHGAP21, promoting activation of RhoA following angiotensin II type 1A receptor stimulation Mol. Cell. Biol. 31 2011 1066 1075
2. K.S. Barcellos, C.L. Bigarella, M.V. Wagner, K.P. Vieira, M. Lazarini, P.R. Langford, J.A. Machado-Neto, S.G. Call, D.M. Staley, and J.Y. Chung ARHGAP21 protein, a new partner of α-tubulin involved in cell-cell adhesion formation and essential for epithelial-mesenchymal transition J. Biol. Chem. 288 2013 2179 2189
3. F.A. Barr, and B. Short Golgins in the structure and dynamics of the Golgi apparatus Curr. Opin. Cell Biol. 15 2003 405 413
4. J.S. Bonifacino The GGA proteins: adaptors on the move Nat. Rev. Mol. Cell Biol. 5 2004 23 32
5. A.S. Burguete, T.D. Fenn, A.T. Brunger, and S.R. Pfeffer Rab and Arl GTPase family members cooperate in the localization of the golgin GCC185 Cell 132 2008 286 298
6. J. Callaghan, S. Nixon, C. Bucci, B.H. Toh, and H. Stenmark Direct interaction of EEA1 with Rab5b Eur. J. Biochem. 265 1999 361 366
7. J. Callaghan, A. Simonsen, J.M. Gaullier, B.H. Toh, and H. Stenmark The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer Biochem. J. 338 1999 539 543
8. P.T. Caswell, H.J. Spence, M. Parsons, D.P. White, K. Clark, K.W. Cheng, G.B. Mills, M.J. Humphries, A.J. Messent, and K.I. Anderson Rab25 associates with alpha5beta1 integrin to promote invasive migration in 3D microenvironments Dev. Cell 13 2007 496 510
9. L.M. Chavas, K. Ihara, M. Kawasaki, S. Torii, T. Uejima, R. Kato, T. Izumi, and S. Wakatsuki Elucidation of Rab27 recruitment by its effectors: structure of Rab27a bound to Exophilin4/Slp2-a Structure 16 2008 1468 1477
10. P. Chavrier, and J. Ménétrey Toward a structural understanding of Arf family:effector specificity Structure 18 2010 1552 1558
11. K.W. Cheng, J.P. Lahad, W.L. Kuo, A. Lapuk, K. Yamada, N. Auersperg, J. Liu, K. Smith-McCune, K.H. Lu, and D. Fishman The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers Nat. Med. 10 2004 1251 1256
12. R. Choudhury, A. Diao, F. Zhang, E. Eisenberg, A. Saint-Pol, C. Williams, A. Konstantakopoulos, J. Lucocq, L. Johannes, and C. Rabouille Lowe syndrome protein OCRL1 interacts with clathrin and regulates protein trafficking between endosomes and the trans-Golgi network Mol. Biol. Cell 16 2005 3467 3479
13. S. Christoforidis, H.M. McBride, R.D. Burgoyne, and M. Zerial The Rab5 effector EEA1 is a core component of endosome docking Nature 397 1999 621 625
14. B.G. Coon, D. Mukherjee, C.B. Hanna, D.J. Riese 2nd, M. Lowe, and R.C. Aguilar Lowe syndrome patient fibroblasts display OCRL1-specific cell migration defects that cannot be rescued by the homologous Inpp5b phosphatase Hum. Mol. Genet. 18 2009 4478 4491
15. M.C. Derby, Z.Z. Lieu, D. Brown, J.L. Stow, B. Goud, and P.A. Gleeson The trans-Golgi network golgin, GCC185, is required for endosome-to-Golgi transport and maintenance of Golgi structure Traffic 8 2007 758 773
16. J.G. Donaldson, and C.L. Jackson ARF family G proteins and their regulators: roles in membrane transport, development and disease Nat. Rev. Mol. Cell Biol. 12 2011 362 375
17. C. D'Souza-Schorey, and P. Chavrier ARF proteins: roles in membrane traffic and beyond Nat. Rev. Mol. Cell Biol. 7 2006 347 358
18. T. Dubois, O. Paléotti, A.A. Mironov, V. Fraisier, T.E.B. Stradal, M.A. De Matteis, M. Franco, and P. Chavrier Golgi-localized GAP for Cdc42 functions downstream of ARF1 to control Arp2/3 complex and F-actin dynamics Nat. Cell Biol. 7 2005 353 364
19. S. Eathiraj, X. Pan, C. Ritacco, and D.G. Lambright Structural basis of family-wide Rab GTPase recognition by rabenosyn-5 Nature 436 2005 415 419
20. S. Eathiraj, A. Mishra, R. Prekeris, and D.G. Lambright Structural basis for Rab11-mediated recruitment of FIP3 to recycling endosomes J. Mol. Biol. 364 2006 121 135
21. M. Franco, P. Chardin, M. Chabre, and S. Paris Myristoylation is not required for GTP-dependent binding of ADP-ribosylation factor ARF1 to phospholipids J. Biol. Chem. 268 1993 24531 24534
22. M.J. Fritzler, J.C. Hamel, R.L. Ochs, and E.K. Chan Molecular characterization of two human autoantigens: unique cDNAs encoding 95- and 160-kD proteins of a putative family in the Golgi complex J. Exp. Med. 178 1993 49 62
23. M. Fukuda Distinct Rab27 binding affinities of Slp2-a and Slac2-a/melanophilin: hierarchy of Rab27A effectors Biochem. Biophys. Res. Commun. 343 2006 666 674
24. A.K. Gillingham, A.H. Tong, C. Boone, and S. Munro The GTPase Arf1p and the ER to Golgi cargo receptor Erv14p cooperate to recruit the golgin Rud3p to the cis-Golgi J. Cell Biol. 167 2004 281 292
25. J.R. Goldenring, and K.T. Nam Rab25 as a tumour suppressor in colon carcinogenesis Br. J. Cancer 104 2011 33 36
26. H. Gournier, H. Stenmark, V. Rybin, R. Lippé, and M. Zerial Two distinct effectors of the small GTPase Rab5 cooperate in endocytic membrane fusion EMBO J. 17 1998 1930 1940
27. B.L. Grosshans, D. Ortiz, and P. Novick Rabs and their effectors: achieving specificity in membrane traffic Proc. Natl. Acad. Sci. USA 103 2006 11821 11827
28. M. Hanzal-Bayer, L. Renault, P. Roversi, A. Wittinghofer, and R.C. Hillig The complex of Arl2-GTP and PDE delta: from structure to function EMBO J. 21 2002 2095 2106
29. R.E. Harrison, C. Bucci, O.V. Vieira, T.A. Schroer, and S. Grinstein Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP Mol. Cell. Biol. 23 2003 6494 6506
30. W.D. Heo, T. Inoue, W.S. Park, M.L. Kim, B.O. Park, T.J. Wandless, and T. Meyer PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane Science 314 2006 1458 1461
31. X. Hou, N. Hagemann, S. Schoebel, W. Blankenfeldt, R.S. Goody, K.S. Erdmann, and A. Itzen A structural basis for Lowe syndrome caused by mutations in the Rab-binding domain of OCRL1 EMBO J. 30 2011 1659 1670
32. F.J. Houghton, P.L. Chew, S. Lodeho, B. Goud, and P.A. Gleeson The localization of the Golgin GCC185 is independent of Rab6A/A′ and Arl1 Cell 138 2009 787 794
33. N. Hyvola, A. Diao, E. McKenzie, A. Skippen, S. Cockcroft, and M. Lowe Membrane targeting and activation of the Lowe syndrome protein OCRL1 by rab GTPases EMBO J. 25 2006 3750 3761
34. T. Isabet, G. Montagnac, K. Regazzoni, B. Raynal, F. El Khadali, P. England, M. Franco, P. Chavrier, A. Houdusse, and J. Ménétrey The structural basis of Arf effector specificity: the crystal structure of ARF6 in a complex with JIP4 EMBO J. 28 2009 2835 2845
35. S.A. Ismail, Y.X. Chen, A. Rusinova, A. Chandra, M. Bierbaum, L. Gremer, G. Triola, H. Waldmann, P.I. Bastiaens, and A. Wittinghofer Arl2-GTP and Arl3-GTP regulate a GDI-like transport system for farnesylated cargo Nat. Chem. Biol. 7 2011 942 949
36. S.A. Ismail, Y.X. Chen, M. Miertzschke, I.R. Vetter, C. Koerner, and A. Wittinghofer Structural basis for Arl3-specific release of myristoylated ciliary cargo from UNC119 EMBO J. 31 2012 4085 4094
37. A. Itzen, and R.S. Goody Key determinants of Rab specificity Structure 16 2008 1437 1439
38. W.N. Jagoe, A.J. Lindsay, R.J. Read, A.J. McCoy, M.W. McCaffrey, and A.R. Khan Crystal structure of rab11 in complex with rab11 family interacting protein 2 Structure 14 2006 1273 1283
39. R. Jahn, and D. Fasshauer Molecular machines governing exocytosis of synaptic vesicles Nature 490 2012 201 207
40. A. Joshi, H. Garg, K. Nagashima, J.S. Bonifacino, and E.O. Freed GGA and Arf proteins modulate retrovirus assembly and release Mol. Cell 30 2008 227 238
41. A.R. Khan Oligomerization of rab/effector complexes in the regulation of vesicle trafficking Prog. Mol. Biol. Transl. Sci. 117 2013 579 614
42. R.A. Kahn, and A.G. Gilman The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein J. Biol. Chem. 261 1986 7906 7911
43. M. Kawasaki, K. Nakayama, and S. Wakatsuki Membrane recruitment of effector proteins by Arf and Rab GTPases Curr. Opin. Struct. Biol. 15 2005 681 689
44. J. Kooy, B.H. Toh, J.M. Pettitt, R. Erlich, and P.A. Gleeson Human autoantibodies as reagents to conserved Golgi components. Characterization of a peripheral, 230-kDa compartment-specific Golgi protein J. Biol. Chem. 267 1992 20255 20263
45. S.P. Koushika "JIP"ing along the axon: the complex roles of JIPs in axonal transport Bioessays 30 2008 10 14
46. M. Kukimoto-Niino, A. Sakamoto, E. Kanno, K. Hanawa-Suetsugu, T. Terada, M. Shirouzu, M. Fukuda, and S. Yokoyama Structural basis for the exclusive specificity of Slac2-a/melanophilin for the Rab27 GTPases Structure 16 2008 1478 1490
47. M.C. Lee, E.A. Miller, J. Goldberg, L. Orci, and R. Schekman Bi-directional protein transport between the ER and Golgi Annu. Rev. Cell Dev. Biol. 20 2004 87 123
48. K.F. Leung, R. Baron, and M.C. Seabra Thematic review series: lipid posttranslational modifications. geranylgeranylation of Rab GTPases J. Lipid Res. 47 2006 467 475
49. Y.C. Lin, T.C. Chiang, Y.T. Liu, Y.T. Tsai, L.T. Jang, and F.J. Lee ARL4A acts with GCC185 to modulate Golgi complex organization J. Cell Sci. 124 2011 4014 4026
50. H. Makyio, M. Ohgi, T. Takei, S. Takahashi, H. Takatsu, Y. Katoh, A. Hanai, T. Ueda, Y. Kanaho, and Y. Xie Structural basis for Arf6-MKLP1 complex formation on the Flemming body responsible for cytokinesis EMBO J. 31 2012 2590 2603
51. T. Matsui, N. Ohbayashi, and M. Fukuda 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 2012 28619 28631
52. G. Ménasché, E. Pastural, J. Feldmann, S. Certain, F. Ersoy, S. Dupuis, N. Wulffraat, D. Bianchi, A. Fischer, F. Le Deist, and G. de Saint Basile Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome Nat. Genet. 25 2000 173 176
53. J. Ménétrey, M. Perderiset, J. Cicolari, T. Dubois, N. Elkhatib, F. El Khadali, M. Franco, P. Chavrier, and A. Houdusse Structural basis for ARF1-mediated recruitment of ARHGAP21 to Golgi membranes EMBO J. 26 2007 1953 1962
54. E. Merithew, S. Hatherly, J.J. Dumas, D.C. Lawe, R. Heller-Harrison, and D.G. Lambright Structural plasticity of an invariant hydrophobic triad in the switch regions of Rab GTPases is a determinant of effector recognition J. Biol. Chem. 276 2001 13982 13988
55. S. Miserey-Lenkei, F. Waharte, A. Boulet, M.H. Cuif, D. Tenza, A. El Marjou, G. Raposo, J. Salamero, L. Héliot, B. Goud, and S. Monier Rab6-interacting protein 1 links Rab6 and Rab11 function Traffic 8 2007 1385 1403
56. A. Mishra, S. Eathiraj, S. Corvera, and D.G. Lambright Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of Early Endosomal Autoantigen 1 (EEA1) Proc. Natl. Acad. Sci. USA 107 2010 10866 10871
57. E. Mizuno-Yamasaki, M. Medkova, J. Coleman, and P. Novick Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p Dev. Cell 18 2010 828 840
58. G. Montagnac, J.-B. Sibarita, S. Loubéry, L. Daviet, M. Romao, G. Raposo, and P. Chavrier ARF6 Interacts with JIP4 to control a motor switch mechanism regulating endosome traffic in cytokinesis Curr. Biol. 19 2009 184 195
59. I. Moore, J. Schell, and K. Palme Subclass-specific sequence motifs identified in Rab GTPases Trends Biochem. Sci. 20 1995 10 12
60. S. Munro The golgin coiled-coil proteins of the Golgi apparatus Cold Spring Harb Perspect Biol. 3 2011 a005256
61. R. Muromoto, Y. Sekine, S. Imoto, O. Ikeda, T. Okayama, N. Sato, and T. Matsuda BART is essential for nuclear retention of STAT3 Int. Immunol. 20 2008 395 403
62. D.M. Navaroli, K.D. Bellvé, C. Standley, L.M. Lifshitz, J. Cardia, D. Lambright, D. Leonard, K.E. Fogarty, and S. Corvera Rabenosyn-5 defines the fate of the transferrin receptor following clathrin-mediated endocytosis Proc. Natl. Acad. Sci. USA 109 2012 E471 E480
63. E. Nielsen, S. Christoforidis, S. Uttenweiler-Joseph, M. Miaczynska, F. Dewitte, M. Wilm, B. Hoflack, and M. Zerial Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain J. Cell Biol. 151 2000 601 612
64. C.J. Noakes, G. Lee, and M. Lowe The PH domain proteins IPIP27A and B link OCRL1 to receptor recycling in the endocytic pathway Mol. Biol. Cell 22 2011 606 623
65. T. Ohya, M. Miaczynska, U. Coskun, B. Lommer, A. Runge, D. Drechsel, Y. Kalaidzidis, and M. Zerial Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes Nature 459 2009 1091 1097
66. C.J. O'Neal, E.I. Amaya, M.G. Jobling, R.K. Holmes, and W.G. Hol Crystal structures of an intrinsically active cholera toxin mutant yield insight into the toxin activation mechanism Biochemistry 43 2004 3772 3782
67. C.J. O'Neal, M.G. Jobling, R.K. Holmes, and W.G.J. Hol Structural basis for the activation of cholera toxin by human ARF6-GTP Science 309 2005 1093 1096
68. C. Ostermeier, and A.T. Brunger Structural basis of Rab effector specificity: crystal structure of the small G protein Rab3A complexed with the effector domain of rabphilin-3A Cell 96 1999 363 374
69. B. Panic, O. Perisic, D.B. Veprintsev, R.L. Williams, and S. Munro Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus Mol. Cell 12 2003 863 874
70. S. Pasqualato, L. Renault, and J. Cherfils Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication EMBO Rep. 3 2002 1035 1041
71. J.B. Pereira-Leal, and M.C. Seabra The mammalian Rab family of small GTPases: definition of family and subfamily sequence motifs suggests a mechanism for functional specificity in the Ras superfamily J. Mol. Biol. 301 2000 1077 1087
72. J.B. Pereira-Leal, A.N. Hume, and M.C. Seabra Prenylation of Rab GTPases: molecular mechanisms and involvement in genetic disease FEBS Lett. 498 2001 197 200
73. S. Pfeffer Membrane domains in the secretory and endocytic pathways Cell 112 2003 507 517
74. R. Puertollano, P.A. Randazzo, J.F. Presley, L.M. Hartnell, and J.S. Bonifacino The GGAs promote ARF-dependent recruitment of clathrin to the TGN Cell 105 2001 93 102
75. R. Recacha, A. Boulet, F. Jollivet, S. Monier, A. Houdusse, B. Goud, and A.R. Khan Structural basis for recruitment of Rab6-interacting protein 1 to Golgi via a RUN domain Structure 17 2009 21 30
76. J.V. Reddy, A.S. Burguete, K. Sridevi, I.G. Ganley, R.M. Nottingham, and S.R. Pfeffer A functional role for the GCC185 golgin in mannose 6-phosphate receptor recycling Mol. Biol. Cell 17 2006 4353 4363
77. M. Ren, G. Xu, J. Zeng, C. De Lemos-Chiarandini, M. Adesnik, and D.D. Sabatini Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes Proc. Natl. Acad. Sci. USA 95 1998 6187 6192
78. E. Schonteich, M. Pilli, G.C. Simon, H.T. Matern, J.R. Junutula, D. Sentz, R.K. Holmes, and R. Prekeris Molecular characterization of Rab11-FIP3 binding to ARF GTPases Eur. J. Cell Biol. 86 2007 417 431
79. J.D. Sharer, J.F. Shern, H. Van Valkenburgh, D.C. Wallace, and R.A. Kahn ARL2 and BART enter mitochondria and bind the adenine nucleotide transporter Mol. Biol. Cell 13 2002 71 83
80. T. Shiba, M. Kawasaki, H. Takatsu, T. Nogi, N. Matsugaki, N. Igarashi, M. Suzuki, R. Kato, K. Nakayama, and S. Wakatsuki Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport Nat. Struct. Biol. 10 2003 386 393
81. T. Shiba, H. Koga, H.W. Shin, M. Kawasaki, R. Kato, K. Nakayama, and S. Wakatsuki Structural basis for Rab11-dependent membrane recruitment of a family of Rab11-interacting protein 3 (FIP3)/Arfophilin-1 Proc. Natl. Acad. Sci. USA 103 2006 15416 15421
82. B. Short, A. Haas, and F.A. Barr Golgins and GTPases, giving identity and structure to the Golgi apparatus Biochim. Biophys. Acta 1744 2005 383 395
83. A. Simonsen, R. Lippé, S. Christoforidis, J.M. Gaullier, A. Brech, J. Callaghan, B.H. Toh, C. Murphy, M. Zerial, and H. Stenmark EEA1 links PI(3)K function to Rab5 regulation of endosome fusion Nature 394 1998 494 498
84. H. Stenmark, G. Vitale, O. Ullrich, and M. Zerial Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion Cell 83 1995 423 432
85. C. Stroupe, and A.T. Brunger Crystal structures of a Rab protein in its inactive and active conformations J. Mol. Biol. 304 2000 585 598
86. Y. Takai, T. Sasaki, and T. Matozaki Small GTP-binding proteins Physiol. Rev. 81 2001 153 208
87. S. Takamori, M. Holt, K. Stenius, E.A. Lemke, M. Grønborg, D. Riedel, H. Urlaub, S. Schenck, B. Brügger, and P. Ringler Molecular anatomy of a trafficking organelle Cell 127 2006 831 846
88. K. Taniuchi, S. Iwasaki, and T. Saibara BART inhibits pancreatic cancer cell invasion by inhibiting ARL2-mediated RhoA inactivation Int. J. Oncol. 39 2011 1243 1252
89. G. Vitale, V. Rybin, S. Christoforidis, P. Thornqvist, M. McCaffrey, H. Stenmark, and M. Zerial Distinct Rab-binding domains mediate the interaction of Rabaptin-5 with GTP-bound Rab4 and Rab5 EMBO J. 17 1998 1941 1951
90. L. Wang, E.S. Seeley, W. Wickner, and A.J. Merz Vacuole fusion at a ring of vertex docking sites leaves membrane fragments within the organelle Cell 108 2002 357 369
91. G.M. Wilson, A.B. Fielding, G.C. Simon, X. Yu, P.D. Andrews, R.S. Hames, A.M. Frey, A.A. Peden, G.W. Gould, and R. Prekeris The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis Mol. Biol. Cell 16 2005 849 860
92. K.J. Wright, L.M. Baye, A. Olivier-Mason, S. Mukhopadhyay, L. Sang, M. Kwong, W. Wang, P.R. Pretorius, V.C. Sheffield, and P. Sengupta An ARL3-UNC119-RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium Genes Dev. 25 2011 2347 2360
93. M. Wu, L. Lu, W. Hong, and H. Song Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Arl1 Nat. Struct. Mol. Biol. 11 2004 86 94
94. M. Wu, T. Wang, E. Loh, W. Hong, and H. Song Structural basis for recruitment of RILP by small GTPase Rab7 EMBO J. 24 2005 1491 1501
95. Z. Yi, H. Yokota, S. Torii, T. Aoki, M. Hosaka, S. Zhao, K. Takata, T. Takeuchi, and T. Izumi The Rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules Mol. Cell. Biol. 22 2002 1858 1867
96. X. Yu, M. Breitman, and J. Goldberg A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes Cell 148 2012 530 542
97. M. Zerial, and H. McBride Rab proteins as membrane organizers Nat. Rev. Mol. Cell Biol. 2 2001 107 117
98. T. Zhang, S. Li, Y. Zhang, C. Zhong, Z. Lai, and J. Ding Crystal structure of the ARL2-GTP-BART complex reveals a novel recognition and binding mode of small GTPase with effector Structure 17 2009 602 610
99. H. Zhang, R. Constantine, S. Vorobiev, Y. Chen, J. Seetharaman, Y.J. Huang, R. Xiao, G.T. Montelione, C.D. Gerstner, and M.W. Davis UNC119 is required for G protein trafficking in sensory neurons Nat. Neurosci. 14 2011 874 880
100. G. Zhu, P. Zhai, J. Liu, S. Terzyan, G. Li, and X.C. Zhang Structural basis of Rab5-Rabaptin5 interaction in endocytosis Nat. Struct. Mol. Biol. 11 2004 975 983
101. H. Zhu, G. Zhu, J. Liu, Z. Liang, X.C. Zhang, and G. Li Rabaptin-5-independent membrane targeting and Rab5 activation by Rabex-5 in the cell Mol. Biol. Cell 18 2007 4119 4128