Rab GTPases as coordinators of vesicle traffic (original) (raw)
Schwartz, S. L., Cao, C., Pylypenko, O., Rak, A. & Wandinger-Ness, A. Rab GTPases at a glance. J. Cell Sci.120, 3905–3910 (2007). ArticleCASPubMed Google Scholar
Pereira-Leal, J. B. & Seabra, M. C. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol.313, 889–901 (2001). Provides a useful overview of Rab subfamilies in yeast, nematodes, flies and humans, and defines Rab-specific sequence motifs. ArticleCASPubMed Google Scholar
Zerial, M. & McBride, H. Rab proteins as membrane organizers. Nature Rev. Mol. Cell Biol.2, 107–117 (2001). CAS Google Scholar
Pfeffer, S. R. Structural clues to Rab GTPase functional diversity. J. Biol. Chem.280, 15485–15488 (2005). ArticlePubMed Google Scholar
Delprato, A., Merithew, E. & Lambright, D. G. Structure, exchange determinants, and family-wide rab specificity of the tandem helical bundle and Vps9 domains of Rabex-5. Cell118, 607–617 (2004). ArticleCASPubMed Google Scholar
Eathiraj, S., Pan, X., Ritacco, C. & Lambright, D. G. Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature436, 415–419 (2005). ArticleCASPubMedPubMed Central Google Scholar
Haas, A. K. et al. 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 (2007). ArticleCASPubMed Google Scholar
Pan, X., Eathiraj, S., Munson, M. & Lambright, D. G. TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature442, 303–306 (2006). ArticleCASPubMed Google Scholar
Shirane, M. & Nakayama, K. I. Protrudin induces neurite formation by directional membrane trafficking. Science314, 818–821 (2006). ArticleCASPubMed Google Scholar
Matsui, Y. et al. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for smg p25A, a ras p21-like GTP-binding protein. Mol. Cell. Biol.10, 4116–4122 (1990). ArticleCASPubMedPubMed Central Google Scholar
Ullrich, O., Horiuchi, H., Bucci, C. & Zerial, M. Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange. Nature368, 157–160 (1994). ArticleCASPubMed Google Scholar
Ullrich, O. et al. Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J. Biol. Chem.268, 18143–18150 (1993). CASPubMed Google Scholar
Soldati, T., Shapiro, A. D., Svejstrup, A. B. & Pfeffer, S. R. Membrane targeting of the small GTPase Rab9 is accompanied by nucleotide exchange. Nature369, 76–78 (1994). References 12 and 13 show the function of Rab GDI in delivering isoprenylated Rabs to specific membranes. ArticleCASPubMed Google Scholar
Alexandrov, K., Horiuchi, H., Steele-Mortimer, O., Seabra, M. C. & Zerial, M. Rab escort protein-1 is a multifunctional protein that accompanies newly prenylated rab proteins to their target membranes. EMBO J.13, 5262–5273 (1994). ArticleCASPubMedPubMed Central Google Scholar
Seabra, M. C. Nucleotide dependence of Rab geranylgeranylation. Rab escort protein interacts preferentially with GDP-bound Rab. J. Biol. Chem.271, 14398–14404 (1996). ArticleCASPubMed Google Scholar
Shen, F. & Seabra, M. C. Mechanism of digeranylgeranylation of Rab proteins. Formation of a complex between monogeranylgeranyl-Rab and Rab escort protein. J. Biol. Chem.271, 3692–3698 (1996). Shows the function of REP in escorting newly synthesized Rabs to Rab geranylgeranyl transferase. ArticleCASPubMed Google Scholar
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. Cell62, 317–329 (1990). First paper to show the localization of different Rabs to distinct intracellular membranes. ArticleCASPubMed Google Scholar
Sivars, U., Aivazian, D. & Pfeffer, S. R. Yip3 catalyses the dissociation of endosomal Rab–GDI complexes. Nature425, 856–859 (2003). First identification of a Rab GDF. ArticleCASPubMed Google Scholar
Carroll, K. S. et al. Role of Rab9 GTPase in facilitating receptor recruitment by TIP47. Science292, 1373–1376 (2001). ArticleCASPubMed Google Scholar
McLauchlan, H. et al. A novel role for Rab5–GDI in ligand sequestration into calthrin-coated pits. Curr. Biol.8, 34–45 (1998). ArticleCASPubMed Google Scholar
Cremona, O. et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell99, 179–188 (1999). ArticleCASPubMed Google Scholar
Semerdjieva, S. et al. Coordinated regulation of AP2 uncoating from clathrin-coated vesicles by rab5 and hRME-6. J. Cell Biol.183, 499–511 (2008). Provides the first functional mechanisms for a Rab GTPase in vesicle uncoating. CASPubMedPubMed Central Google Scholar
Christoforidis, S. et al. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nature Cell Biol.1, 249–252 (1999). ArticleCASPubMed Google Scholar
Shin, H. W. et al. An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J. Cell Biol.170, 607–618 (2005). ArticleCASPubMedPubMed Central Google Scholar
Arai, S., Noda, Y., Kainuma, S., Wada, I. & Yoda, K. Ypt11 functions in bud-directed transport of the Golgi by linking Myo2 to the coatomer subunit Ret2. Curr. Biol.18, 987–991 (2008). ArticleCASPubMed Google Scholar
Seabra, M. C. & Coudrier, E. Rab GTPases and myosin motors in organelle motility. Traffic5, 393–399 (2004). ArticleCASPubMed Google Scholar
Wu, X. S. et al. Identification of an organelle receptor for myosin-Va. Nature Cell Biol.4, 271–278 (2002). ArticleCASPubMed Google Scholar
Menasche, G. et al. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nature Genet.25, 173–176 (2001). First demonstration that a genetic disease is caused by a Rab mutation. Article Google Scholar
Kuroda, T. S. & Fukuda, M. Rab27A-binding protein Slp2-a is required for peripheral melanosome distribution and elongated cell shape in melanocytes. Nature Cell Biol.6, 1195–1203 (2004). ArticleCASPubMed Google Scholar
Hales, C. M., Vaerman, J. P. & Goldenring, J. R. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J. Biol. Chem.277, 50415–50421 (2002). ArticleCASPubMed Google Scholar
Roland, J. T., Kenworthy, A. K., Peranen, J., Caplan, S. & Goldenring, J. R. Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol. Biol. Cell18, 2828–2837 (2007). ArticleCASPubMedPubMed Central Google Scholar
Echard, A. et al. Interaction of a Golgi-associated kinesin-like protein with Rab6. Science279, 580–585 (1998). ArticleCASPubMed Google Scholar
Fontijn, R. D. et al. The human kinesin-like protein RB6K is under tight cell cycle control and is essential for cytokinesis. Mol. Cell. Biol.21, 2944–2955 (2001). ArticleCASPubMedPubMed Central Google Scholar
Hoepfner, S. et al. Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell121, 437–450 (2005). ArticleCASPubMed Google Scholar
Jordens, I. et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein–dynactin motors. Curr. Biol.11, 1680–1685 (2001). ArticleCASPubMed Google Scholar
Matanis, T. et al. Bicaudal-D regulates COPI-independent Golgi–ER transport by recruiting the dynein–dynactin motor complex. Nature Cell Biol.4, 986–992 (2002). ArticleCASPubMed Google Scholar
Salminen, A. & Novick, P. J. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell49, 527–538 (1987). First demonstration that a Rab GTPase controls vesicle traffic. ArticleCASPubMed Google Scholar
Guo, W., Roth, D., Walch-Solimena, C. & Novick, P. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J.18, 1071–1080 (1999). ArticleCASPubMedPubMed Central Google Scholar
Guo, W., Tamanoi, F. & Novick, P. Spatial regulation of the exocyst complex by Rho1 GTPase. Nature Cell Biol.3, 353–360 (2001). ArticleCASPubMed Google Scholar
Gorvel, J. P., Chavrier, P., Zerial, M. & Gruenberg, J. rab5 controls early endosome fusion in vitro. Cell64, 915–925 (1991). First direct demonstration that a Rab GTPase controls membrane fusion. ArticleCASPubMed Google Scholar
Rubino, M., Miaczynska, M., Lippé, R. & Zerial, M. Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J. Biol. Chem.275, 3745–3748 (2000). ArticleCASPubMed Google Scholar
Stenmark, H. et al. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J.13, 1287–1296 (1994). Identifies the GTP-bound form of a Rab GTPase as the active conformation in membrane fusion. ArticleCASPubMedPubMed Central Google Scholar
Simonsen, A. et al. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature394, 494–498 (1998). ArticleCASPubMed Google Scholar
Nielsen, E. et al. 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 (2000). ArticleCASPubMedPubMed Central Google Scholar
Callaghan, J., Simonsen, A., Gaullier, J.-M., Toh, B.-H. & Stenmark, H. The endosome fusion regulator EEA1 is a dimer. Biochem. J.338, 539–543 (1999). ArticleCASPubMedPubMed Central Google Scholar
Morrison, H. A. et al. Regulation of early endosomal entry by the Drosophila tumor suppressors rabenosyn and Vps45. Mol. Biol. Cell19, 4167–4176 (2008). ArticleCASPubMedPubMed Central Google Scholar
Simonsen, A., Gaullier, J.-M., D'Arrigo, A. & Stenmark, H. The Rab5 effector EEA1 interacts directly with syntaxin-6. J. Biol. Chem.274, 28857–28860 (1999). ArticleCASPubMed Google Scholar
McBride, H. M. et al. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell98, 377–386 (1999). ArticleCASPubMed Google Scholar
Ohya, T. et al. Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 20 May 2009 (doi: 10.1038/nature 08107). First reconstitution of Rab-mediated fusion using liposomes, purified SNAREs and RAB5 effectors.
Fukuda, M. Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J. Biochem.137, 9–16 (2005). ArticleCASPubMed Google Scholar
Tsuboi, T. & Fukuda, M. The Slp4-a linker domain controls exocytosis through interaction with Munc18–1syntaxin-1a complex. Mol. Biol. Cell17, 2101–2112 (2006). ArticleCASPubMedPubMed Central Google Scholar
Gomi, H., Mizutani, S., Kasai, K., Itohara, S. & Izumi, T. Granuphilin molecularly docks insulin granules to the fusion machinery. J. Cell Biol.171, 99–109 (2005). ArticleCASPubMedPubMed Central Google Scholar
Tsuboi, T. & Fukuda, M. The C2B domain of rabphilin directly interacts with SNAP-25 and regulates the docking step of dense core vesicle exocytosis in PC12 cells. J. Biol. Chem.280, 39253–39259 (2005). ArticleCASPubMed Google Scholar
Haas, A., Scheglmann, D., Lazar, T., Gallwitz, D. & Wickner, W. 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 (1995). ArticleCASPubMedPubMed Central Google Scholar
Ungermann, C., Sato, K. & Wickner, W. Defining the functions of _trans_-SNARE pairs. Nature396, 543–548 (1998). ArticleCASPubMed Google Scholar
Allan, B. B., Moyer, B. D. & Balch, W. E. Rab1 recruitment of p115 into a _cis_-SNARE complex: programming budding COPII vesicles for fusion. Science289, 444–448 (2000). ArticleCASPubMed Google Scholar
Moyer, B. D., Allan, B. B. & Balch, W. E. Rab1 interaction with a GM130 effector complex regulates COPII vesicle _cis_-Golgi tethering. Traffic2, 268–276 (2001). ArticleCASPubMed Google Scholar
Stenmark, H., Vitale, G., Ullrich, O. & Zerial, M. Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell83, 423–432 (1995). ArticleCASPubMed Google Scholar
Horiuchi, H. et al. A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell90, 1149–1159 (1997). Shows the inclusion of a Rab GEF in a Rab effector complex. ArticleCASPubMed Google Scholar
Jones, S., Newman, C., Liu, F. & Segev, N. The TRAPP complex is a nucleotide exchanger for Ypt1 and Ypt31/32. Mol. Biol. Cell11, 4403–4411 (2000). ArticleCASPubMedPubMed Central Google Scholar
Cai, Y. et al. The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell133, 1202–1213 (2008). ArticleCASPubMedPubMed Central Google Scholar
Wurmser, A. E., Sato, T. K. & Emr, S. D. 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 (2000). ArticleCASPubMedPubMed Central Google Scholar
Sonnichsen, B., De, R. S., Nielsen, E., Rietdorf, J. & Zerial, M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol.149, 901–914 (2000). Proposes the concept of Rab domains. ArticleCASPubMedPubMed Central Google Scholar
Barbero, P., Bittova, L. & Pfeffer, S. R. Visualization of Rab9-mediated vesicle transport from endosomes to the _trans_-Golgi in living cells. J. Cell Biol.156, 511–518 (2002). ArticleCASPubMedPubMed Central Google Scholar
de Renzis, S., Sonnichsen, B. & Zerial, M. Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nature Cell Biol.4, 124–133 (2002). ArticleCASPubMed Google Scholar
Burguete, A. S., Fenn, T. D., Brunger, A. T. & Pfeffer, S. R. Rab and Arl GTPase family members cooperate in the localization of the golgin GCC185. Cell132, 286–298 (2008). ArticleCASPubMedPubMed Central Google Scholar
Hayes, G. L. et al. Multiple Rab GTPase binding sites in GCC185 suggest a model for vesicle tethering at the _trans_-Golgi. Mol. Biol. Cell20, 209–217 (2009). ArticleCASPubMedPubMed Central Google Scholar
Reddy, J. V. et al. A functional role for the GCC185 golgin in mannose 6-phosphate receptor recycling. Mol. Biol. Cell17, 4353–4363 (2006). ArticleCASPubMedPubMed Central Google Scholar
Sinka, R., Gillingham, A. K., Kondylis, V. & Munro, S. Golgi coiled-coil proteins contain multiple binding sites for Rab family G proteins. J. Cell Biol.183, 607–615 (2008). ArticleCASPubMedPubMed Central Google Scholar
Fukuda, M., Kanno, E., Ishibashi, K. & Itoh, T. Large scale screening for novel Rab effectors reveals unexpected broad Rab binding specificity. Mol. Cell Proteomics7, 1031–1042 (2008). ArticleCASPubMed Google Scholar
Schnatwinkel, C. et al. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol.2, e261 (2004). ArticleCASPubMedPubMed Central Google Scholar
Carlton, J. et al. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high- curvature membranes and 3-phosphoinositides. Curr. Biol.14, 1791–1800 (2004). ArticleCASPubMed Google Scholar
Rojas, R. et al. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol.183, 513–526 (2008). ArticleCASPubMedPubMed Central Google Scholar
Rink, J., Ghigo, E., Kalaidzidis, Y. & Zerial, M. Rab conversion as a mechanism of progression from early to late endosomes. Cell122, 735–749 (2005). Introduces the concept of Rab conversion. ArticleCASPubMed Google Scholar
Conte-Zerial, P. et al. Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol. Syst. Biol.4, 206 (2008). PubMedPubMed Central Google Scholar
Eggenschwiler, J. T., Espinoza, E. & Anderson, K. V. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature412, 194–198 (2001). ArticleCASPubMed Google Scholar
Romero, R. K., Peralta, E. R., Guenther, G. G., Wong, S. Y. & Edinger, A. L. Rab7 activation by growth factor withdrawal contributes to the induction of apoptosis. Mol. Biol. Cell20, 2831–2840 (2009). Article Google Scholar
Barbieri, M. A. et al. Epidermal growth factor and membrane trafficking. EGF receptor activation of endocytosis requires Rab5a. J. Cell Biol.151, 539–550 (2000). ArticleCASPubMedPubMed Central Google Scholar
Tall, G. G., Barbieri, M. A., Stahl, P. D. & Horazdovsky, B. F. Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell1, 73–82 (2001). ArticleCASPubMed Google Scholar
Lanzetti, L., Palamidessi, A., Areces, L., Scita, G. & Di Fiore, P. P. Rab5 is a signalling GTPase involved in actin remodelling by receptor tyrosine kinases. Nature429, 309–314 (2004). ArticleCASPubMed Google Scholar
Lanzetti, L. et al. The Eps8 protein coordinates EGF receptor signalling through Rac and trafficking through Rab5. Nature408, 374–377 (2000). ArticleCASPubMed Google Scholar
Palamidessi, A. et al. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell134, 135–147 (2008). ArticleCASPubMed Google Scholar
Miaczynska, M. et al. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell116, 445–456 (2004). ArticleCASPubMed Google Scholar
Schenck, A. et al. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell133, 486–497 (2008). ArticleCASPubMed Google Scholar
Wang, Y. et al. Regulation of endocytosis via the oxygen-sensing pathway. Nature Med.15, 319–324 (2009). ArticleCASPubMed Google Scholar
Coyne, C. B., Shen, L., Turner, J. R. & Bergelson, J. M. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe2, 181–192 (2007). ArticleCASPubMedPubMed Central Google Scholar
Smith, A. C. et al. A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J. Cell Biol.176, 263–268 (2007). ArticleCASPubMedPubMed Central Google Scholar
Desjardins, M., Huber, L. A., Parton, R. G. & Griffiths, G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol.124, 677–688 (1994). ArticleCASPubMed Google Scholar
Kinchen, J. M. & Ravichandran, K. S. Phagosome maturation: going through the acid test. Nature Rev. Mol. Cell Biol.9, 781–795 (2008). ArticleCAS Google Scholar
Kitano, M., Nakaya, M., Nakamura, T., Nagata, S. & Matsuda, M. Imaging of Rab5 activity identifies essential regulators for phagosome maturation. Nature453, 241–245 (2008). ArticleCASPubMed Google Scholar
Terebiznik, M. R. et al. Helicobacter pylori VacA toxin promotes bacterial intracellular survival in gastric epithelial cells. Infect. Immun.74, 6599–6614 (2006). ArticleCASPubMedPubMed Central Google Scholar
Via, L. E. et al. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J. Biol. Chem.272, 13326–13331 (1997). ArticleCASPubMed Google Scholar
Prada-Delgado, A. et al. Inhibition of Rab5a exchange activity is a key step for Listeria monocytogenes survival. Traffic6, 252–265 (2005). ArticleCASPubMed Google Scholar
Mallo, G. V. et al. SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J. Cell Biol.182, 741–752 (2008). ArticleCASPubMedPubMed Central Google Scholar
Ingmundson, A., Delprato, A., Lambright, D. G. & Roy, C. R. Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature450, 365–369 (2007). ArticleCASPubMed Google Scholar
Machner, M. P. & Isberg, R. R. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science318, 974–977 (2007). ArticleCASPubMed Google Scholar
Polo, S., Pece, S. & Di Fiore, P. P. Endocytosis and cancer. Curr. Opin. Cell Biol.16, 1–6 (2004). ArticleCAS Google Scholar
Bache, K. G., Slagsvold, T. & Stenmark, H. Defective downregulation of receptor tyrosine kinases in cancer. EMBO J.23, 2707–2712 (2004). ArticleCASPubMedPubMed Central Google Scholar
Cheng, K. W. et al. The RAB25 small GTPase determines aggressiveness of ovarian and breast cancers. Nature Med.10, 1251–1256 (2004). ArticleCASPubMed Google Scholar
Wang, X., Kumar, R., Navarre, J., Casanova, J. E. & Goldenring, J. R. Regulation of vesicle trafficking in Madin–Darby canine kidney cells by Rab11a and Rab25. J. Biol. Chem.275, 29138–29146 (2000). ArticleCASPubMed Google Scholar
Caswell, P. T. et al. Rab25 associates with α5β1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell13, 496–510 (2007). ArticleCASPubMed Google Scholar
Pellinen, T. et al. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of β1-integrins. J. Cell Biol.173, 767–780 (2006). ArticleCASPubMedPubMed Central Google Scholar
Pellinen, T. et al. Integrin trafficking regulated by Rab21 is necessary for cytokinesis. Dev. Cell15, 371–385 (2008). ArticleCASPubMed Google Scholar
Bravo-Cordero, J. J. et al. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J.26, 1499–1510 (2007). ArticleCASPubMedPubMed Central Google Scholar
Hou, Q. et al. Integrative genomics identifies RAB23 as an invasion mediator gene in diffuse-type gastric cancer. Cancer Res.68, 4623–4630 (2008). ArticleCASPubMed Google Scholar
Neeft, M. et al. Munc13–4 is an effector of Rab27a and controls secretion of lysosomes in hematopoietic cells. Mol. Biol. Cell16, 731–741 (2005). ArticleCASPubMedPubMed Central Google Scholar
Holt, O. et al. Slp1 and Slp2-a localize to the plasma membrane of CTL and contribute to secretion from the immunological synapse. Traffic9, 446–457 (2008). ArticleCASPubMedPubMed Central Google Scholar
Seabra, M. C., Brown, M. S. & Goldstein, J. L. Retinal degeneration in choroideremia: deficiency of rab geranylgeranyl transferase. Science259, 377–381 (1993). ArticleCASPubMed Google Scholar
Seabra, M. C., Ho, Y. K. & Anant, J. S. Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J. Biol. Chem.270, 24420–24427 (1995). ArticleCASPubMed Google Scholar
Aligianis, I. A. et al. Mutations of the catalytic subunit of RAB3GAP cause Warburg Micro syndrome. Nature Genet.37, 221–223 (2005). ArticleCASPubMed Google Scholar
Aligianis, I. A. et al. Mutation in Rab3 GTPase-activating protein (RAB3GAP) noncatalytic subunit in a kindred with Martsolf syndrome. Am. J. Hum. Genet.78, 702–707 (2006). ArticleCASPubMedPubMed Central Google Scholar
Verhoeven, K. et al. Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy. Am. J. Hum. Genet.72, 722–727 (2003). ArticleCASPubMedPubMed Central Google Scholar
Miinea, C. P. et al. AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem. J.391, 87–93 (2005). ArticleCASPubMedPubMed Central Google Scholar
Roach, W. G., Chavez, J. A., Miinea, C. P. & Lienhard, G. E. Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem. J.403, 353–358 (2007). ArticleCASPubMedPubMed Central Google Scholar
Chadt, A. et al. Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity. Nature Genet.40, 1354–1359 (2008). ArticleCASPubMed Google Scholar
Sano, H., Roach, W. G., Peck, G. R., Fukuda, M. & Lienhard, G. E. Rab10 in insulin-stimulated GLUT4 translocation. Biochem. J.411, 89–95 (2008). ArticleCASPubMed Google Scholar
Jenkins, D. et al. RAB23 mutations in Carpenter syndrome imply an unexpected role for hedgehog signaling in cranial-suture development and obesity. Am. J. Hum. Genet.80, 1162–1170 (2007). ArticleCASPubMedPubMed Central Google Scholar
Kapfhamer, D. et al. Mutations in Rab3a alter circadian period and homeostatic response to sleep loss in the mouse. Nature Genet.32, 290–295 (2002). ArticleCASPubMed Google Scholar
Geppert, M. et al. The role of Rab3A in neurotransmitter release. Nature369, 493–497 (1994). ArticleCASPubMed Google Scholar
Sato, T. et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature448, 366–369 (2007). ArticleCASPubMed Google Scholar
Nielsen, E., Severin, F., Backer, J. M., Hyman, A. A. & Zerial, M. Rab5 regulates motility of early endosomes on microtubules. Nature Cell Biol.1, 376–382 (1999). ArticleCASPubMed Google Scholar
Christoforidis, S., McBride, H. M., Burgoyne, R. D. & Zerial, M. The Rab5 effector EEA1 is a core component of endosome docking. Nature397, 621–626 (1999). ArticleCASPubMed Google Scholar
Chiariello, M., Bruni, C. B. & Bucci, C. The small GTPases Rab5a, Rab5b and Rab5c are differentially phosphorylated in vitro. FEBS Lett.453, 20–24 (1999). ArticleCASPubMed Google Scholar
Ding, J., Soule, G., Overmeyer, J. H. & Maltese, W. A. Tyrosine phosphorylation of the Rab24 GTPase in cultured mammalian cells. Biochem. Biophys. Res. Commun.312, 670–675 (2003). ArticleCASPubMed Google Scholar
van der Sluijs, P. et al. Reversible phosphorylation–dephosphorylation determines the localization of rab4 during the cell cycle. EMBO J.11, 4379–4389 (1992). ArticleCASPubMedPubMed Central Google Scholar
Bailly, E. et al. Phosphorylation of two small GTP-binding proteins of the Rab family by p34cdc2. Nature350, 715–718 (1991). ArticleCASPubMed Google Scholar
Karniguian, A., Zahraoui, A. & Tavitian, A. Identification of small GTP-binding rab proteins in human platelets: thrombin-induced phosphorylation of rab3B, rab6, and rab8 proteins. Proc. Natl Acad. Sci. USA90, 7647–7651 (1993). ArticleCASPubMedPubMed Central Google Scholar
Mace, G., Miaczynska, M., Zerial, M. & Nebreda, A. R. Phosphorylation of EEA1 by p38 MAP kinase regulates mu opioid receptor endocytosis. EMBO J.24, 3235–3246 (2005). ArticleCASPubMedPubMed Central Google Scholar
Mattera, R., Tsai, Y. C., Weissman, A. M. & Bonifacino, J. S. The Rab5 guanine nucleotide exchange factor Rabex-5 binds ubiquitin (Ub) and functions as a Ub ligase through an atypical Ub-interacting motif and a zinc finger domain. J. Biol. Chem.281, 6874–6883 (2006). ArticleCASPubMed Google Scholar
Mattera, R. & Bonifacino, J. S. Ubiquitin binding and conjugation regulate the recruitment of Rabex-5 to early endosomes. EMBO J.27, 2484–2494 (2008). ArticleCASPubMedPubMed Central Google Scholar
Chavez, J. A., Roach, W. G., Keller, S. R., Lane, W. S. & Lienhard, G. E. Inhibition of GLUT4 translocation by Tbc1d1, a Rab GTPase-activating protein abundant in skeletal muscle, is partially relieved by AMP-activated protein kinase activation. J. Biol. Chem.283, 9187–9195 (2008). ArticleCASPubMedPubMed Central Google Scholar
Steele-Mortimer, O., Gruenberg, J. & Clague, M. J. Phosphorylation of GDI and membrane cycling of rab proteins. FEBS Lett.329, 313–318 (1993). ArticleCASPubMed Google Scholar
Vitale, G. et al. Distinct Rab-binding domains mediate the interaction of Rabaptin- 5 with GTP-bound Rab4 and Rab5. EMBO J.17, 1941–1951 (1998). ArticleCASPubMedPubMed Central Google Scholar
Riggs, B. et al. Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J. Cell Biol.163, 143–154 (2003). ArticleCASPubMedPubMed Central Google Scholar
Kouranti, I., Sachse, M., Arouche, N., Goud, B. & Echard, A. Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr. Biol.16, 1719–1725 (2006). ArticleCASPubMed Google Scholar
Yoshimura, S., Egerer, J., Fuchs, E., Haas, A. K. & Barr, F. A. Functional dissection of Rab GTPases involved in primary cilium formation. J. Cell Biol.178, 363–369 (2007). ArticleCASPubMedPubMed Central Google Scholar