Rab proteins

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1404, Issue 1-2, 1998, Pages 101-112

  Martinez, Olivier ^a   Goud, Bruno ^a  

^a INSTITUT CURIE   (France)

Author keywords

Golgi apparatus; Intracellular transport; Rab GTPase

Indexed keywords

RAB PROTEIN;

ENDOCYTOSIS; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; REVIEW;

EUKARYOTA;

EID: 0032516809     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4889(98)00050-0     Document Type: Article

References (106)

1. Gallwitz D., Donath C., Sander C. A yeast gene encoding a protein homologous to the human c-has/bas proto-oncogene product. Nature. 306:1983;704-707.
2. Rothman J.E. Mechanisms of intracellular protein transport. Nature. 372:1994;55-63.
3. Darchen F., Zahraoui A., Hammel F., Monteils M.P., Tavitian A., Scherman D. Association of the GTP-binding protein Rab3A with bovine adrenal chromaffin granules. Proc. Natl. Acad. Sci. USA. 87:1990;5692-5696.
4. Fischer von Mollard G., Mignery G.A., Baumert M., Perin M.S., Hanson T.J., Burger P.M., Jahn R., Südhof T.C. rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. Natl. Acad. Sci. USA. 87:1990;1988-1992.
5. Lutcke A., Jansson S., Parton R.G., Chavrier P., Valencia A., Huber L.A., Lehtonen E., Zerial M. Rab17, a novel small GTPase, is specific for epithelial cells and is induced during cell polarization. J. Cell Biol. 121:1993;553-564.
6. Moya M., Roberts D., Novick P. DSS4-1 is a dominant suppressor of sec4-8 that encodes a nucleotide exchange protein that aids Sec4p function. Nature. 361:1993;460-463.
7. Burton J., Roberts D., Montaldi M., Novick P., De Camilli P. A mammalian guanine-nucleotide-releasing protein enhances function of yeast secretory protein Sec4. Nature. 361:1993;464-467.
8. Burton J.L., Burns M.E., Gatti E., Augustine G.J., De Camilli P. Specific interactions of Mss4 with members of the Rab GTPase subfamily. EMBO J. 13:1994;5547-5558.
9. Wada M., Nakanishi H., Satoh A., Hirano H., Obaishi H., Matsuura Y., Takai Y. Isolation and characterization of a GDP/GTP exchange protein specific for the Rab3 subfamily small G proteins. J. Biol. Chem. 272:1997;3875-3878.
10. Walch-Solimena C., Collins R.N., Novick P.J. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J. Cell Biol. 137:1997;1495-1509.
11. Brondyk W.H., McKiernan C.J., Fortner K.A., Stabila P., Holz R.W., Macara I.G. Interaction cloning of Rabin3, a novel protein that associates with the Ras-like GTPase Rab3A. Mol. Cell. Biol. 15:1995;1137-1143.
12. Horiuchi H., Lippé R., McBride H., Rubino M., Woodman P., Stenmark H., Rybin V., Wilm M., Ashman K., Mann M., Zerial M. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell. 90:1997;1149-1159.
13. rab3A. Proc. Natl. Acad. Sci. USA. 89:1992;1154-1158.
14. Tan T.J., Vollmer P., Gallwitz D. Identification and partial purification of GTPase-activating proteins from yeast and mammalian cells that preferentially act on Ypt1/Rab1 proteins. FEBS Lett. 291:1991;322-326.
15. Walworth N.C., Brennwald P., Kabcenell A.K., Garrett M., Novick P. Hydrolysis of GTP by Sec4 protein plays an important role in vesicular transport and is stimulated by a GTPase-activating protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:1992;2017-2028.
16. Strom M., Vollmer P., Tan T.J., Gallwitz D. A yeast GTPase-activating protein that interacts specifically with a member of the Ypt/Rab family. Nature. 361:1993;736-739.
17. Fukui K., Sasaki T., Imazumi K., Matsuura Y., Nakanishi H., Takai Y. Isolation and characterization of a GTPase activating protein specific for the Rab3 subfamily of small G proteins. J. Biol. Chem. 272:1997;4655-4658.
18. Garrett M.D., Zahner J.E., Cheney C.M., Novick P.J. GDI1 encodes a GDP dissociation inhibitor that plays an essential role in the yeast secretory pathway. EMBO J. 13:1994;1718-1728.
19. Nishimura N., Nakamura H., Takai Y., Sano K. Molecular cloning and characterization of two rab GDI species from rat brain: brain-specific and ubiquitous types. J. Biol. Chem. 269:1994;14191-14198.
20. Shisheva A., Sudhof T.C., Czech M.P. Cloning, characterization, and expression of a novel GDP dissociation inhibitor isoform from skeletal muscle. Mol. Cell. Biol. 14:1994;3459-3468.
21. Janoueix-Lerosey I., Jollivet F., Camonis J., Marche P.N., Goud B. Two-hybrid system screen with the small GTP-binding protein Rab6. Identification of a novel mouse GDP dissociation inhibitor isoform and two other potential partners of Rab6. J. Biol. Chem. 270:1995;14801-14808.
22. Ullrich O., Horiuchi H., Bucci C., Zerial M. Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange [see comments]. Nature. 368:1994;157-160.
23. Soldati T., Shapiro A.D., Svejstrup A.B., Pfeffer S.R. Membrane targeting of the small GTPase Rab9 is accompanied by nucleotide exchange [see comments]. Nature. 369:1994;76-78.
24. Dirac-Svejstrup A.B., Sumizawa T., Pfeffer S.R. Identification of a GDI displacement factor that releases endosomal Rab GTPases from Rab-GDI. EMBO J. 16:1997;465-472.
25. Chavrier P., Gorvel J.P., Stelzer E., Simons K., Gruenberg J., Zerial M. Hypervariable C-terminal domain of rab proteins acts as a targeting signal. Nature. 353:1991;769-772.
26. Ayad N., Hull M., Mellman I. Mitotic phosphorylation of rab4 prevents binding to a specific receptor on endosomes membranes. EMBO J. 16:1997;4497-4507.
27. Shirataki H., Yamamoto T., Hagi S., Miura H., Oishi H., Jin-no Y., Senbonmatsu T., Takai Y. Rabphilin-3A is associated with synaptic vesicles through a vesicle protein in a manner independent of Rab3A. J. Biol. Chem. 269:1994;32717-32720.
28. Mizoguchi A., Yano Y., Hamaguchi H., Yanagida H., Ide C., Zahraoui A., Shirataki H., Sasaki T., Takai Y. Localization of Rabphilin-3A on the synaptic vesicle. Biochem. Biophys Res. Commun. 202:1994;1235-1243.
29. Geppert M., Bolshakov V.Y., Siegelbaum S.A., Takei K., De Camilli P., Hammer R.E., Sudhof T.C. The role of Rab3A in neurotransmitter release. Nature. 369:1994;493-497.
30. Kishida S., Shirataki H., Sasaki T., Kato M., Kaibuchi K., Takai Y. Rab3A GTPase-activating protein-inhibiting activity of Rabphilin-3A, a putative Rab3A target protein. J. Biol. Chem. 268:1993;22259-22261.
31. Stahl B., Chou J.H., Li C., Sudhof T.C., Jahn R. Rab3 reversibly recruits rabphilin to synaptic vesicles by a mechanism analogous to raf recruitment by ras. EMBO J. 15:1996;1799-1809.
32. Kato M., Sakaki T., Ohya T., Nakanishi H., Nishioka H., Imamura M., Takai Y. Physical and functional interaction of rabphilin-3A with alpha-actinin. J. Biol. Chem. 271:1996;31775-31778.
33. Stenmark H., Vitale G., Ullrich O., Zerial M. Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell. 83:1995;423-432.
34. Ren M., Zeng J., De Lemos-Chiarandini C., Rosenfeld M., Adesnik M., Sabatini D.D. In its active form, the GTP-binding protein rab8 interacts with a stress-activated protein kinase. Proc. Natl. Acad. Sci. USA. 93:1996;5151-5155.
35. Wang Y., Okamoto M., Schmitz F., Hofmann K., Sudhorf T. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature. 388:1997;593-598.
36. Diaz E., Schimmoller F., Pfeffer S. A novel rab9 effector required for endosome to TGN transport. J. Cell Biol. 138:1997;283-290.
37. Echard A., Jollivet F., Martinez O., Lacapère J.-J., Rousselet A., Janoueix-Lerosey I., Goud B. Interaction of a Golgi-associated kinesin-like protein with Rab6. Science. 79:1998;580-587.
38. Dascher C., Ossig R., Gallwitz D., Schmitt H.D. Identification and structure of four yeast genes (SLY) that are able to suppress the functional loss of YPT1, a member of the RAS superfamily. Mol. Cell. Biol. 11:1991;872-885.
39. Sogaard M., Tani K., Ye R.R., Geromanos S., Tempst P., Kirchhausen T., Rothman J.E., Sollner T. A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell. 78:1994;937-948.
40. Lian J.P., Ferro-Novick S. Bos1p, an integral membrane protein of the endoplasmic reticulum to Golgi transport vesicles, is required for their fusion competence. Cell. 73:1993;735-745.
41. Lian J.P., Stone S., Jiang Y., Lyons P., Ferro-Novick S. Ypt1p implicated in v-SNARE activation. Nature. 372:1994;698-701.
42. Søgaard M., Tani K., Ye R.R., Geromanos S., Tempst P., Kirchhausen T., Rothman J.E., Söllner T. A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell. 78:1994;937-948.
43. Lupashin V.V., Waters G. t-SNARE activation through transient interaction with a Rab-like GTPase. Science. 276:1997;1255-1258.
44. Brennwald P., Kearns B., Champion K., Keranen S., Bankaitis V., Novick P. Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis. Cell. 79:1994;245-258.
45. Saraste J., Lahtinen U., Goud B. Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway. J. Cell Sci. 108:1995;1541-1552.
46. Plutner H., Cox A.D., Pind S., Khovravi-Far R., Bourne J.R., Schwaninger R., Der C.J., Balch W.E. Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J. Cell Biol. 115:1991;31-43.
47. Tisdale E.J., Bourne J.R., Khosravi-Far R., Der C.J., Balch W.E. GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J. Cell Biol. 119:1992;749-761.
48. Jedd G., Richardson C., Litt R., Segev N. The Ypt1 GTPase is essential for the first two steps of the yeast secretory pathway. J. Cell Biol. 131:1995;583-590.
49. Nuoffer C., Davidson H.W., Metteson J., Meinkoth J., Balch W.E. A GDP-bond form of rab1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments. J. Cell Biol. 125:1994;225-237.
50. Hengst L., Lehmeier T., Gallwitz D. The ryh1 gene in the fission yeast Schizosaccharomyces pombe encoding a GTP-binding protein related to ras, rho and ypt: structure, expression and identification of its human homologue. EMBO J. 9:1990;1949-1955.
51. L. Hengst, PhD Thesis, Philipps-Universität Marburg/Lahn, 1992.
52. Bednarek S.Y., Reynolds T.L., Schroeder M., Grabowski R., Hengst L., Gallwitz D., Raikhel N.V. A small GTP-binding protein from Arabidopsis thaliana functionally complements the yeast YPT6 null mutant. Plant Physiol. 104:1994;591-596.
53. Alves de Castro F., Ward G.E., Jambou R., Attal G., Mayau V., Jaureguiberry G., Braun-Breton C., Chakrabarti D., Langsley G. A family of Rab G-proteins in Plasmodium falciparum. Mol. Biochem. Parasitol. 80:1996;77-78.
54. Goud B., Zahraoui A., Tavitian A., Saraste J. Small GTP-binding protein associated with Golgi cisternae. Nature. 345:1990;553-556.
55. Antony C., Cibert C., Geraud G., Santa Maria A., Maro B., Mayau V., Goud B. The small GTP-binding protein rab6p is distributed from medial Golgi to the trans-Golgi network as determined by a confocal microscopic approach. J. Cell Sci. 103:1992;785-796.
56. Feldmann G., Durand-Schneider A.-M., Goud B. Behaviour of the small GTP-binding protein rab6 in the liver of normal rats and rats presenting an acute inflammatory reaction. Biol. Cell. 83:1995;121-125.
57. Deretic D., Papermaster D.S. Rab6 is associated with a compartment that transport rhodopsin from the trans-Golgi to the site of rod outer segment disk formation in retinal photoreceptors. J. Cell Sci. 106:1993;803-813.
58. Jasmin B., Goud B., Camus G., Cartaud J. The low molecular weight guanosine triphosphate-binding protein Rab6p associates with distinct post-Golgi vesicles in Torpedo marmorata electrocytes. Neuroscience. 49:1992;849-855.
59. Tixier-Vidal A., Barret A., Picart R., Mayau V., Voqt D., Wiedenman B., Goud B. The small GTP-binding protein rab6p is associated with both Golgi and post-Golgi synaptophysin-containing membranes during synaptogenesis of hypothalamic neurones in culture. J. Cell Sci. 105:1993;935-947.
60. Jones S.M., Crosby J.R., Salamero J., Howell K.E. A cytosolic complex of p62 and rab6 associates with TGN38/41 and is involved in budding of exocytic vesicles from the trans-Golgi network. J. Cell Biol. 122:1993;775-788.
61. Martinez O., Schmidt A., Salamero J., Hoflack B., Roa M., Goud B. The small GTP-binding protein rab6 functions in intra-Golgi transport. J. Cell Biol. 127:1994;1575-1588.
62. Mayer T., Touchot N., Elazar Z. Transport between cis and medial Golgi cisternae requires the function of the Ras-related GTPase Rab6. J. Biol. Chem. 271:1996;16097-16103.
63. Martinez O., Antony C., Pehau-Arnaudet G., Berger E.G., Salamero J., Goud B. GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 94:1997;1828-1833.
64. Johannes D., Tenza D., Antony C., Goud B. Retrograde transport of KDEL-bearing B-fragment of Shiga toxin. J. Biol. Chem. 272:1997;19554-19561.
65. Li B., Warner J.R. Mutation of the Rab6 homologue of Saccharomyces cerevisiae, YPT6, inhibits both early Golgi function and ribosome biosynthesis. J. Biol. Chem. 271:1996;16813-16819.
66. Benli M., Doring F., Robinson D.G., Yang X., Gallwitz D. Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J. 15:1996;6460-6475.
67. Tsukada M., Gallwitz D. isolation and characterization of SYS genes from yeast, multicopy suppressors of the functional loss of the transport GTPase Ypt6p. J. Cell Sci. 109:1996;2471-2481.
68. Chen Y.T., Holcomb C., Moore H.P. Expression and localization of two low molecular weight GTP-binding proteins, Rab8 and Rab10, by epitope tag. Proc. Natl. Acad. Sci. USA. 90:1993;6508-6512.
69. Bourne H.R. Do GTPases direct membrane traffic in secretion? Cell. 55:1988;59-61.
70. Brennwald P., Novick P. Interactions of three domains distinguishing the ras-related GTP-binding proteins Ypt1 and Sec4. Nature. 362:1993;560-563.
71. Johannes L., Doussau F., Clabecq A., Henry J.-P., Darchen F., Poulain B. Evidence for a functional link between Rab3 and the SNARE complex. J. Cell Sci. 109:1996;2875-2884.
72. Goud B., Salminen A., Walworth N.C., Novick P.J. A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell. 53:1988;753-768.
73. Salminen A., Novick P.J. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell. 49:1987;527-538.
74. Walworth N., Goud B., Kabcenell A., Novick P. Mutational analysis of SEC4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J. 8:1989;1685-1693.
75. Segev N., Mulholland J., Botstein D. The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell. 52:1988;915-924.
76. Baker D., Wuestehube L., Schekman R., Botstein D., Segev N. GTP-binding Ypt1 protein and Ca2+ function independently in a cell-free protein transport reaction. Proc. Natl. Acad. Sci. USA. 87:1990;355-359.
77. Singer-Kruger B., Stenmark H., Dusterhoft A., Philippsen P., Yoo J.S., Gallwitz D., Zerial M. Role of three rab5-like GTPases, Ypt51p, Ypt52p, and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast. J. Cell Biol. 125:1994;283-298.
78. Wichmann H., Hengst L., Gallwitz D. Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p). Cell. 71:1992;1131-1142.
79. Schimmoller F., Riezman H. Involvement of Ypt7p, a small GTPase, in traffic from late endosome to the vacuole in yeast. J. Cell Sci. 106:1993;823-830.
80. Mayer A., Wickner W. Docking of yeast vacuoles is catalyzed by the ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). J. Cell Biol. 136:1997;307-317.
81. Plutner H., Davidson H.W., Saraste J., Balch W.E. Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the P58 containing compartment. J. Cell Biol. 119:1992;1097-1116.
82. 2+ are required for the fusion of carrier vesicles mediating endoplasmic reticulum to Golgi transport. J. Cell Biol. 125:1994;239-252.
83. Wilson B.S., Nuoffer C., Meinkoth J.L., McCaffery M., Feramisco J.R., Balch W.E., Farquhar M.G. A Rab1 mutant affecting guanine nucleotide exchange promotes disassembly of the Golgi apparatus. J. Cell Biol. 125:1994;557-571.
84. Chavrier P., Parton R.G., Hauri H.P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 62:1990;317-329.
85. Holz R.W., Brondyk W.H., Senter R.A., Kuizon L., Macara I.G. Evidence for the involvement of Rab3A in Ca(2+)-dependent exocytosis from adrenal chromaffin cells. J. Biol. Chem. 269:1994;10229-10234.
86. Johannes L., Lledo P.M., Roa M., Vincent J.D., Henry J.P., Darchen F. The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J. 13:1994;2029-2037.
87. 2+-dependant exocytosis in rat anterior pituitary cells. Nature. 364:1993;540-544.
88. Weber E., Berta G., Tousson A., St John P., Green M.W., Gopalokrishnan U., Jilling T., Sorscher E.J., Elton T.S., Abrahamson D.R., et al. Expression and polarized targeting of a rab3 isoform in epithelial cells. J. Cell Biol. 125:1994;583-594.
89. Fischer von Mollard G., Stahl B., Khokhlatchev A., Sudhof T.C., Jahn R. Rab3C is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis. J. Biol. Chem. 269:1994;10971-10974.
90. van der Sluijs P., Hull M., Webster P., Male P., Goud B., Mellman I. The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell. 70:1992;729-740.
91. Gorvel J., Chavrier P., Zerial M., Gruenberg J. Rab5 controls early endosome fusion in vitro. Cell. 64:1991;915-925.
92. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell. 70:1992;715-728.
93. Li G.P., Stahl P.D. Structure-function relationship of the small GTPase rab5. J. Biol. Chem. 268:1993;24475-24480.
94. Stenmark H., Parton R.G., Steele-Mortimer O., Lutcke A., Gruenberg J., Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13:1994;1287-1296.
95. Horiuchi H., Giner A., Hoflack B., Zerial M. A GDP/GTP exchange-stimulatory activity for the Rab5-RabGDI complex on clathrin-coated vesicles from bovine brain. J. Biol. Chem. 270:1995;11257-11262.
96. Chavrier P., Vingron M., Sander C., Simons K., Zerial M. Molecular cloning of YPT1/SEC4-related cDNAs from an epithelial cell line. Mol. Cell. Biol. 10:1990;6578-6585.
97. Papini E., Satin B., Bucci C., de Bernard M., Telford J.L., Manetti R., Rappuoli R., Zerial M., Montecucco C. The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J. 16:1997;15-24.
98. Huber L.A., Pimplikar S., Parton R.G., Virta H., Zerial M., Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J. Cell Biol. 123:1993;35-45.
99. Peranen J., Auvinen P., Virta H., Wepf R., Simons K. Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J. Cell. Biol. 135:1996;153-167.
100. Lombardi D., Soldati T., Riederer M.A., Goda Y., Zerial M., Pfeffer S.R. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12:1993;677-682.
101. Riederer M.A., Soldati T., Shapiro A.D., Lin J., Pfeffer S.R. Lysosome biogenesis requires rab9 function and receptor recycling from endosomes to the trans-Golgi network. J. Cell Biol. 125:1994;573-582.
102. Urbe S., Huber L.A., Zerial M., Tooze S.A., Parton R.G. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett. 334:1993;175-182.
103. Ullrich O., Reinsch S., Urbe S., Zerial M., Parton R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:1996;913-924.
104. Olkkonen V.M., Dupree P., Killisch I., Lutcke A., Zerial M., Simons K. Molecular cloning and subcellular localization of three GTP-binding proteins of the rab subfamily. J. Cell Sci. 106:1993;1249-1261.
105. Zahraoui A., Joberty G., Arpin M., Fontaine J.-J., Hellio R., Tavitian A., Louvard D. A small rab GTPase is distributed in cytoplasmic vesicles in non polarized cells but colocalizes with the tight junction marker ZO-1 in polarized epithelial cells. J. Cell Biol. 124:1994;101-115.
106. Seabra M.C., Ho Y.K., Anant J.S. Deficient geranylgeranylation of Ram/Rab27 in choroidemia. J. Biol. Chem. 270:1995;24420-24427.