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Multiple Roles of Rab GTPases at the Golgi

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Book cover The Golgi Apparatus and Centriole

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 67))

Abstract

The Golgi apparatus is a central sorting station in the cell. It receives newly synthesized molecules from the endoplasmic reticulum and directs them to different subcellular destinations, such as the plasma membrane or the endocytic pathway. Importantly, in the last few years, it has emerged that the maintenance of Golgi structure is connected to the proper regulation of membrane trafficking. Rab proteins are small GTPases that are considered to be the master regulators of the intracellular membrane trafficking. Several of the over 60 human Rabs are involved in the regulation of transport pathways at the Golgi as well as in the maintenance of its architecture. This chapter will summarize the different roles of Rab GTPases at the Golgi, both as regulators of membrane transport, scaffold, and tethering proteins and in preserving the structure and function of this organelle.

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References

  • Aizawa M, Fukuda M (2015) Small GTPase Rab2B and its specific binding protein Golgi-associated Rab2B interactor-like 4 (GARI-L4) regulate Golgi morphology. J Biol Chem 290:22250–22261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ali BR, Wasmeier C, Lamoreux L, Strom M, Seabra MC (2004) Multiple regions contribute to membrane targeting of Rab GTPases. J Cell Sci 117:6401–6412

    Article  CAS  PubMed  Google Scholar 

  • Allan BB, Moyer BD, Balch WE (2000) Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 289:444–448

    Article  CAS  PubMed  Google Scholar 

  • Alshammari MJ, Al-Otaibi L, Alkuraya FS (2012) Mutation in RAB33B, which encodes a regulator of retrograde Golgi transport, defines a second Dyggve-Melchior-Clausen locus. J Med Genet 49:455–461

    Article  CAS  PubMed  Google Scholar 

  • Andres DA, Seabra MC, Brown MS, Armstrong SA, Smeland TE, Cremers FP, Goldstein JL (1993) cDNA cloning of component A of Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein. Cell 73:1091–1099

    Article  CAS  PubMed  Google Scholar 

  • Ang AL, Taguchi T, Francis S, Folsch H, Murrells LJ, Pypaert M, Warren G, Mellman I (2004) Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J Cell Biol 167:531–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antonny B, Burd C, De Camilli P, Chen E, Daumke O, Faelber K, Ford M, Frolov VA, Frost A, Hinshaw JE, Kirchhausen T, Kozlov MM, Lenz M, Low HH, McMahon H, Merrifield C, Pollard TD, Robinson PJ, Roux A, Schmid S (2016) Membrane fission by dynamin: what we know and what we need to know. EMBO J 35:2270–2284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, Dunn KW (2006) Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 17:3156–3175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker RW, Hughson FM (2016) Chaperoning SNARE assembly and disassembly. Nat Rev Mol Cell Biol 17:465–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bard F, Casano L, Mallabiabarrena A, Wallace E, Saito K, Kitayama H, Guizzunti G, Hu Y, Wendler F, Dasgupta R, Perrimon N, Malhotra V (2006) Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439:604–607

    Article  CAS  PubMed  Google Scholar 

  • Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S (2010) TRAPP complexes in membrane traffic: convergence through a common Rab. Nat Rev Mol Cell Biol 11:759–763

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bombardier JP, Munson M (2015) Three steps forward, two steps back: mechanistic insights into the assembly and disassembly of the SNARE complex. Curr Opin Chem Biol 29:66–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonifacino JS, Hierro A (2011) Transport according to GARP: receiving retrograde cargo at the trans-Golgi network. Trends Cell Biol 21:159–167

    Article  CAS  PubMed  Google Scholar 

  • Borg Distefano M, Hofstad Haugen L, Wang Y, Perdreau-Dahl H, Kjos I, Jia D, Morth JP, Neefjes J, Bakke O, Progida C (2018) TBC1D5 controls the GTPase cycle of Rab7b. J Cell Sci 131. https://doi.org/10.1242/jcs.216630

    Article  PubMed  CAS  Google Scholar 

  • Borg M, Bakke O, Progida C (2014) A novel interaction between Rab7b and actomyosin reveals a dual role in intracellular transport and cell migration. J Cell Sci 127:4927–4939

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Borgese N (2016) Getting membrane proteins on and off the shuttle bus between the endoplasmic reticulum and the Golgi complex. J Cell Sci 129:1537–1545

    Article  CAS  PubMed  Google Scholar 

  • Bucci C, Bakke O, Progida C (2010) Rab7b and receptors trafficking. Commun Integr Biol 3:401–404

    Article  PubMed  PubMed Central  Google Scholar 

  • Bucci C, Bakke O, Progida C (2012) Charcot-Marie-Tooth disease and intracellular traffic. Prog Neurobiol 99:191–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai H, Reinisch K, Ferro-Novick S (2007) Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell 12:671–682

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardoso CM, Jordao L, Vieira OV (2010) Rab10 regulates phagosome maturation and its overexpression rescues Mycobacterium-containing phagosomes maturation. Traffic 11:221–235

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Casey PJ, Seabra MC (1996) Protein prenyltransferases. J Biol Chem 271:5289–5292

    Article  CAS  PubMed  Google Scholar 

  • Ceresa BP, Bahr SJ (2006) rab7 activity affects epidermal growth factor: epidermal growth factor receptor degradation by regulating endocytic trafficking from the late endosome. J Biol Chem 281:1099–1106

    Article  CAS  PubMed  Google Scholar 

  • Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M (1990a) Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317–329

    Article  CAS  PubMed  Google Scholar 

  • Chavrier P, Vingron M, Sander C, Simons K, Zerial M (1990b) Molecular cloning of YPT1/SEC4-related cDNAs from an epithelial cell line. Mol Cell Biol 10:6578–6585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Feng Y, Chen D, Wandinger-Ness A (1998) Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9:3241–3257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Hu J, Yun Y, Wang T (2010) Rab36 regulates the spatial distribution of late endosomes and lysosomes through a similar mechanism to Rab34. Mol Membr Biol 27:23–30

    Article  CAS  PubMed  Google Scholar 

  • Christoforidis S, McBride HM, Burgoyne RD, Zerial M (1999a) The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621–625

    Article  CAS  PubMed  Google Scholar 

  • Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip SC, Waterfield MD, Backer JM, Zerial M (1999b) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1:249–252

    Article  CAS  PubMed  Google Scholar 

  • Chua CEL, Tang BL (2014) Engagement of the small GTPase Rab31 protein and its effector, early endosome antigen 1, is important for trafficking of the ligand-bound epidermal growth factor receptor from the early to the late endosome. J Biol Chem 289:12375–12389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chua CEL, Tang BL (2018) Rab 10-a traffic controller in multiple cellular pathways and locations. J Cell Physiol 233:6483–6494

    Article  CAS  PubMed  Google Scholar 

  • Collins RN (2003) “Getting it on”–GDI displacement and small GTPase membrane recruitment. Mol Cell 12:1064–1066

    Article  CAS  PubMed  Google Scholar 

  • Cottam NP, Ungar D (2012) Retrograde vesicle transport in the Golgi. Protoplasma 249:943–955

    Article  CAS  PubMed  Google Scholar 

  • Cox JV, Kansal R, Whitt MA (2016) Rab43 regulates the sorting of a subset of membrane protein cargo through the medial Golgi. Mol Biol Cell 27:1834–1844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Day PM, Thompson CD, Schowalter RM, Lowy DR, Schiller JT (2013) Identification of a role for the trans-Golgi network in HPV16 pseudovirus infection. J Virol 87:3862–3870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Graaf P, Zwart WT, van Dijken RA, Deneka M, Schulz TK, Geijsen N, Coffer PJ, Gadella BM, Verkleij AJ, van der Sluijs P, van Bergen en Henegouwen PM (2004) Phosphatidylinositol 4-kinasebeta is critical for functional association of rab11 with the Golgi complex. Mol Biol Cell 15:2038–2047

    Article  PubMed  PubMed Central  Google Scholar 

  • de Leeuw HP, Koster PM, Calafat J, Janssen H, van Zonneveld AJ, van Mourik JA, Voorberg J (1998) Small GTP-binding proteins in human endothelial cells. Br J Haematol 103:15–19

    Article  PubMed  Google Scholar 

  • Deen AJ, Rilla K, Oikari S, Karna R, Bart G, Hayrinen J, Bathina AR, Ropponen A, Makkonen K, Tammi RH, Tammi MI (2014) Rab10-mediated endocytosis of the hyaluronan synthase HAS3 regulates hyaluronan synthesis and cell adhesion to collagen. J Biol Chem 289:8375–8389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dejgaard SY, Murshid A, Erman A, Kizilay O, Verbich D, Lodge R, Dejgaard K, Ly-Hartig TB, Pepperkok R, Simpson JC, Presley JF (2008) Rab18 and Rab43 have key roles in ER-Golgi trafficking. J Cell Sci 121:2768–2781

    Article  CAS  PubMed  Google Scholar 

  • Del Nery E, Miserey-Lenkei S, Falguières T, Nizak C, Johannes L, Perez F, Goud B (2006) Rab6A and Rab6A′ GTPases play non-overlapping roles in membrane trafficking. Traffic 7:394–407

    Article  PubMed  CAS  Google Scholar 

  • Diaz E, Schimmoller F, Pfeffer SR (1997) A novel Rab9 effector required for endosome-to-TGN transport. J Cell Biol 138:283–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dippold HC, Ng MM, Farber-Katz SE, Lee SK, Kerr ML, Peterman MC, Sim R, Wiharto PA, Galbraith KA, Madhavarapu S, Fuchs GJ, Meerloo T, Farquhar MG, Zhou H, Field SJ (2009) GOLPH3 bridges phosphatidylinositol-4- phosphate and actomyosin to stretch and shape the Golgi to promote budding. Cell 139:337–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dupuis N, Lebon S, Kumar M, Drunat S, Graul-Neumann LM, Gressens P, El Ghouzzi V (2013) A novel RAB33B mutation in Smith-McCort dysplasia. Hum Mutat 34:283–286

    Article  CAS  PubMed  Google Scholar 

  • Echard A, Opdam FJ, de Leeuw HJ, Jollivet F, Savelkoul P, Hendriks W, Voorberg J, Goud B, Fransen JA (2000) Alternative splicing of the human Rab6A gene generates two close but functionally different isoforms. Mol Biol Cell 11:3819–3833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • English AR, Voeltz GK (2013) Rab10 GTPase regulates ER dynamics and morphology. Nat Cell Biol 15:169–178

    Article  CAS  PubMed  Google Scholar 

  • Epp N, Rethmeier R, Kramer L, Ungermann C (2011) Membrane dynamics and fusion at late endosomes and vacuoles—Rab regulation, multisubunit tethering complexes and SNAREs. Eur J Cell Biol 90:779–785

    Article  CAS  PubMed  Google Scholar 

  • Espinosa EJ, Calero M, Sridevi K, Pfeffer SR (2009) RhoBTB3: a Rho GTPase-family ATPase required for endosome to Golgi transport. Cell 137:938–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faini M, Beck R, Wieland FT, Briggs JA (2013) Vesicle coats: structure, function, and general principles of assembly. Trends Cell Biol 23:279–288

    Article  CAS  PubMed  Google Scholar 

  • Ferraro F, Kriston-Vizi J, Metcalf DJ, Martin-Martin B, Freeman J, Burden JJ, Westmoreland D, Dyer CE, Knight AE, Ketteler R, Cutler DF (2014) A two-tier Golgi-based control of organelle size underpins the functional plasticity of endothelial cells. Dev Cell 29:292–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galea G, Bexiga MG, Panarella A, O’Neill ED, Simpson JC (2015) A high-content screening microscopy approach to dissect the role of Rab proteins in Golgi-to-ER retrograde trafficking. J Cell Sci 128:2339–2349

    Article  CAS  PubMed  Google Scholar 

  • Gallwitz D, Donath C, Sander C (1983) A yeast gene encoding a protein homologous to the human c-has/bas proto-oncogene product. Nature 306:704–707

    Article  CAS  PubMed  Google Scholar 

  • Ganley IG, Carroll K, Bittova L, Pfeffer S (2004) Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. Mol Biol Cell 15:5420–5430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 USA 110:13380–13385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerondopoulos A, Bastos RN, Yoshimura S-I, Anderson R, Carpanini S, Aligianis I, Handley MT, Barr FA (2014) Rab18 and a Rab18 GEF complex are required for normal ER structure. J Cell Biol 205:707–720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gidon A, Bardin S, Cinquin B, Boulanger J, Waharte F, Heliot L, de la Salle H, Hanau D, Kervrann C, Goud B, Salamero J (2012) A Rab11A/myosin Vb/Rab11-FIP2 complex frames two late recycling steps of langerin from the ERC to the plasma membrane. Traffic 13:815–833

    Article  CAS  PubMed  Google Scholar 

  • Gillingham AK, Munro S (2016) Finding the Golgi: Golgin coiled-coil proteins show the way. Trends Cell Biol 26:399–408

    Article  CAS  PubMed  Google Scholar 

  • Gillingham AK, Sinka R, Torres IL, Lilley KS, Munro S (2014) Toward a comprehensive map of the effectors of rab GTPases. Dev Cell 31:358–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Girod A, Storrie B, Simpson JC, Johannes L, Goud B, Roberts LM, Lord JM, Nilsson T, Pepperkok R (1999) Evidence for a COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat Cell Biol 1:423–430

    Article  CAS  PubMed  Google Scholar 

  • Goitre L, Trapani E, Trabalzini L, Retta SF (2014) The Ras superfamily of small GTPases: the unlocked secrets. Methods Mol Biol 1120:1–18

    Article  CAS  PubMed  Google Scholar 

  • Goldenberg NM, Grinstein S, Silverman M (2007) Golgi-bound Rab34 is a novel member of the secretory pathway. Mol Biol Cell 18:4762–4771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goody RS, Muller MP, Wu YW (2017) Mechanisms of action of Rab proteins, key regulators of intracellular vesicular transport. Biol Chem 398:565–575

    Article  CAS  PubMed  Google Scholar 

  • Goud B, Salminen A, Walworth NC, Novick PJ (1988) A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53:753–768

    Article  CAS  PubMed  Google Scholar 

  • Goud B, Liu S, Storrie B (2018) Rab proteins as major determinants of the Golgi complex structure. Small GTPases 9:66–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grigoriev I, Splinter D, Keijzer N, Wulf PS, Demmers J, Ohtsuka T, Modesti M, Maly IV, Grosveld F, Hoogenraad CC, Akhmanova A (2007) Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13:305–314

    Article  CAS  PubMed  Google Scholar 

  • Grigoriev I, Yu KL, Martinez-Sanchez E, Serra-Marques A, Smal I, Meijering E, Demmers J, Peranen J, Pasterkamp RJ, van der Sluijs P, Hoogenraad CC, Akhmanova A (2011) Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers. Curr Biol 21:967–974

    Article  CAS  PubMed  Google Scholar 

  • Gutkowska M, Swiezewska E (2012) Structure, regulation and cellular functions of Rab geranylgeranyl transferase and its cellular partner Rab Escort Protein. Mol Membr Biol 29:243–256

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hanna J, Carroll K, Pfeffer SR (2002) Identification of residues in TIP47 essential for Rab9 binding. Proc Natl Acad Sci USA 99:7450–7454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasanagic M, Waheed A, Eissenberg JC (2015) Different pathways to the lysosome: sorting out alternatives. Int Rev Cell Mol Biol 320:75–101

    Article  CAS  PubMed  Google Scholar 

  • Horgan CP, McCaffrey MW (2011) Rab GTPases and microtubule motors. Biochem Soc Trans 39:1202–1206

    Article  CAS  PubMed  Google Scholar 

  • Horgan CP, Hanscom SR, Jolly RS, Futter CE, McCaffrey MW (2010) Rab11-FIP3 links the Rab11 GTPase and cytoplasmic dynein to mediate transport to the endosomal-recycling compartment. J Cell Sci 123:181–191

    Article  CAS  PubMed  Google Scholar 

  • Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K (1993) Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 123:35–45

    Article  CAS  PubMed  Google Scholar 

  • Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M (2008) Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 19:2916–2925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaarsma D, Hoogenraad CC (2015) Cytoplasmic dynein and its regulatory proteins in Golgi pathology in nervous system disorders. Front Neurosci 9:397

    Article  PubMed  PubMed Central  Google Scholar 

  • Jayson CBK, Arlt H, Fischer AW, Lai ZW, Farese RV, Walther TC, Barr FA (2018) Rab18 is not necessary for lipid droplet biogenesis or turnover in human mammary carcinoma cells. Mol Biol Cell 29:2045–2054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jedd G, Richardson C, Litt R, Segev N (1995) The Ypt1 GTPase is essential for the first two steps of the yeast secretory pathway. J Cell Biol 131:583–590

    Article  CAS  PubMed  Google Scholar 

  • Jia D, Zhang JS, Li F, Wang J, Deng Z, White MA, Osborne DG, Phillips-Krawczak C, Gomez TS, Li H, Singla A, Burstein E, Billadeau DD, Rosen MK (2016) Structural and mechanistic insights into regulation of the retromer coat by TBC1d5. Nat Commun 7:13305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang S, Storrie B (2005) Cisternal rab proteins regulate Golgi apparatus redistribution in response to hypotonic stress. Mol Biol Cell 16:2586–2596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Junutula JR, De Maziére AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, Klumperman J, Scheller RH (2004) Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 15:2218–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly EE, Giordano F, Horgan CP, Jollivet F, Raposo G, McCaffrey MW (2012) Rab30 is required for the morphological integrity of the Golgi apparatus. Biol Cell 104:84–101

    Article  CAS  PubMed  Google Scholar 

  • Kirchhausen T, Owen D, Harrison SC (2014) Molecular structure, function, and dynamics of clathrin-mediated membrane traffic. Cold Spring Harb Perspect Biol 6:a016725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kitt KN, Hernández-Deviez D, Ballantyne SD, Spiliotis ET, Casanova JE, Wilson JM (2008) Rab14 regulates apical targeting in polarized epithelial cells. Traffic 9:1218–1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kjos I, Vestre K, Guadagno NA, Borg Distefano M, Progida C (2018) Rab and Arf proteins at the crossroad between membrane transport and cytoskeleton dynamics. Biochim Biophys Acta 1865:1397–1409

    Article  CAS  Google Scholar 

  • Kloer DP, Rojas R, Ivan V, Moriyama K, van Vlijmen T, Murthy N, Ghirlando R, van der Sluijs P, Hurley JH, Bonifacino JS (2010) Assembly of the biogenesis of lysosome-related organelles complex-3 (BLOC-3) and its interaction with Rab9. J Biol Chem 285:7794–7804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi S, Hida Y, Ishizaki H, Inoue E, Tanaka-Okamoto M, Yamasaki M, Miyazaki T, Fukaya M, Kitajima I, Takai Y, Watanabe M, Ohtsuka T, Manabe T (2016) The active zone protein CAST regulates synaptic vesicle recycling and quantal size in the mouse hippocampus. Eur J Neurosci 44:2272–2284

    Article  PubMed  Google Scholar 

  • Krzewski K, Cullinane AR (2013) Evidence for defective Rab GTPase-dependent cargo traffic in immune disorders. Exp Cell Res 319:2360–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kucera A, Bakke O, Progida C (2016a) The multiple roles of Rab9 in the endolysosomal system. Commun Integr Biol 9:e1204498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kucera A, Borg Distefano M, Berg-Larsen A, Skjeldal F, Repnik U, Bakke O, Progida C (2016b) Spatiotemporal resolution of Rab9 and CI-MPR dynamics in the endocytic pathway. Traffic 17:211–229

    Article  CAS  PubMed  Google Scholar 

  • Lee PL, Ohlson MB, Pfeffer SR (2015) Rab6 regulation of the kinesin family KIF1C motor domain contributes to Golgi tethering. Elife 4. https://doi.org/10.7554/eLife.06029

  • Li F, Yi L, Zhao L, Itzen A, Goody RS, Wu YW (2014) The role of the hypervariable C-terminal domain in Rab GTPases membrane targeting. Proc Natl Acad Sci USA 111:2572–2577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Wei Z, Fan Y, Huang W, Su Y, Li H, Dong Z, Fukuda M, Khater M, Wu G (2017) The GTPase Rab43 controls the anterograde ER-Golgi trafficking and sorting of GPCRs. Cell Rep 21:1089–1101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Storrie B (2012) Are Rab proteins the link between Golgi organization and membrane trafficking? Cell Mol Life Sci 69:4093–4106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Storrie B (2015) How Rab proteins determine Golgi structure. Int Rev Cell Mol Biol 315:1–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Hunt L, Storrie B (2013a) Rab41 is a novel regulator of Golgi apparatus organization that is needed for ER-to-Golgi trafficking and cell growth. PLoS One 8:e71886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Xu XH, Chen Q, Wang T, Deng CY, Song BL, Du JL, Luo ZG (2013b) Myosin Vb controls biogenesis of post-Golgi Rab10 carriers during axon development. Nat Commun 4:2005

    Article  PubMed  CAS  Google Scholar 

  • Liu S, Majeed W, Kudlyk T, Lupashin V, Storrie B (2016) Identification of Rab41/6d effectors provides an explanation for the differential effects of Rab41/6d and Rab6a/a′ on Golgi organization. Front Cell Dev Biol 4:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu H, Wang S, Hang W, Gao J, Zhang W, Cheng Z, Yang C, He J, Zhou J, Chen J, Shi A (2018) LET-413/Erbin acts as a RAB-5 effector to promote RAB-10 activation during endocytic recycling. J Cell Biol 217:299–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lock JG, Stow JL (2005) Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin. Mol Biol Cell 16:1744–1755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorincz P, Toth S, Benko P, Lakatos Z, Boda A, Glatz G, Zobel M, Bisi S, Hegedus K, Takats S, Scita G, Juhasz G (2017) Rab2 promotes autophagic and endocytic lysosomal degradation. J Cell Biol 216:1937–1947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lupashin VV, Waters MG (1997) t-SNARE activation through transient interaction with a rab-like guanosine triphosphatase. Science 276:1255–1258

    Article  CAS  PubMed  Google Scholar 

  • Lurick A, Gao J, Kuhlee A, Yavavli E, Langemeyer L, Perz A, Raunser S, Ungermann C (2017) Multivalent Rab interactions determine tether-mediated membrane fusion. Mol Biol Cell 28:322–332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mahanty S, Ravichandran K, Chitirala P, Prabha J, Jani RA, Setty SR (2016) Rab9A is required for delivery of cargo from recycling endosomes to melanosomes. Pigment Cell Melanoma Res 29:43–59

    Article  CAS  PubMed  Google Scholar 

  • Majeed W, Liu S, Storrie B (2014) Distinct sets of Rab6 effectors contribute to ZW10—and COG-dependent Golgi homeostasis. Traffic 15:630–647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L (2002) Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 156:653–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin S, Driessen K, Nixon SJ, Zerial M, Parton RG (2005) Regulated Localization of Rab18 to lipid droplets: effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J Biol Chem 280:42325–42335

    Article  CAS  PubMed  Google Scholar 

  • Martinez O, Schmidt A, Salamero J, Hoflack B, Roa M, Goud B (1994) The small GTP-binding protein rab6 functions in intra-Golgi transport. J Cell Biol 127:1575–1588

    Article  CAS  PubMed  Google Scholar 

  • Martinez O, Antony C, Pehau-Arnaudet G, Berger EG, Salamero J, Goud B (1997) GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc Natl Acad Sci USA 94:1828–1833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marubashi S, Shimada H, Fukuda M, Ohbayashi N (2016) RUTBC1 functions as a GTPase-activating protein for Rab32/38 and regulates melanogenic enzyme trafficking in melanocytes. J Biol Chem 291:1427–1440

    Article  CAS  PubMed  Google Scholar 

  • Matanis T, Akhmanova A, Wulf P, Del Nery E, Weide T, Stepanova T, Galjart N, Grosveld F, Goud B, De Zeeuw CI, Barnekow A, Hoogenraad CC (2002) Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat Cell Biol 4:986–992

    Article  CAS  PubMed  Google Scholar 

  • Matsuto M, Kano F, Murata M (2015) Reconstitution of the targeting of Rab6A to the Golgi apparatus in semi-intact HeLa cells: a role of BICD2 in stabilizing Rab6A on Golgi membranes and a concerted role of Rab6A/BICD2 interactions in Golgi-to-ER retrograde transport. Biochim Biophys Acta 1853:2592–2609

    Article  CAS  PubMed  Google Scholar 

  • Mayer T, Touchot N, Elazar Z (1996) Transport between cis and medial Golgi cisternae requires the function of the Ras-related protein Rab6. J Biol Chem 271:16097–16103

    Article  CAS  PubMed  Google Scholar 

  • Micaroni M, Stanley AC, Khromykh T, Venturato J, Wong CX, Lim JP, Marsh BJ, Storrie B, Gleeson PA, Stow JL (2013) Rab6a/a′ are important Golgi regulators of pro-inflammatory TNF secretion in macrophages. PLoS One 8:e57034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller VJ, Ungar D (2012) Re’COG’nition at the Golgi. Traffic 13:891–897

    Article  CAS  PubMed  Google Scholar 

  • Miserey-Lenkei S, Waharte F, Boulet A, Cuif MH, Tenza D, El Marjou A, Raposo G, Salamero J, Heliot L, Goud B, Monier S (2007) Rab6-interacting protein 1 links Rab6 and Rab11 function. Traffic 8:1385–1403

    Article  CAS  PubMed  Google Scholar 

  • Miserey-Lenkei S, Chalancon G, Bardin S, Formstecher E, Goud B, Echard A (2010) Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol 12:645–654

    Article  CAS  PubMed  Google Scholar 

  • Miserey-Lenkei S, Bousquet H, Pylypenko O, Bardin S, Dimitrov A, Bressanelli G, Bonifay R, Fraisier V, Guillou C, Bougeret C, Houdusse A, Echard A, Goud B (2017) Coupling fission and exit of RAB6 vesicles at Golgi hotspots through kinesin-myosin interactions. Nat Commun 8:1254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Monier S, Jollivet F, Janoueix-Lerosey I, Johannes L, Goud B (2002) Characterization of novel Rab6-interacting proteins involved in endosome-to-TGN transport. Traffic 3:289–297

    Article  PubMed  Google Scholar 

  • Morimoto S, Nishimura N, Terai T, Manabe S, Yamamoto Y, Shinahara W, Miyake H, Tashiro S, Shimada M, Sasaki T (2005) Rab13 mediates the continuous endocytic recycling of occludin to the cell surface. J Biol Chem 280:2220–2228

    Article  CAS  PubMed  Google Scholar 

  • Moyer BD, Allan BB, Balch WE (2001) Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering. Traffic 2:268–276

    Article  CAS  PubMed  Google Scholar 

  • Muller MP, Goody RS (2017) Molecular control of Rab activity by GEFs, GAPs and GDI. Small GTPases 9:5–21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nakazawa H, Sada T, Toriyama M, Tago K, Sugiura T, Fukuda M, Inagaki N (2012) Rab33a mediates anterograde vesicular transport for membrane exocytosis and axon outgrowth. J Neurosci 32:12712–12725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ng EL, Wang Y, Tang BL (2007) Rab22B’s role in trans-Golgi network membrane dynamics. Biochem Biophys Res Commun 361:751–757

    Article  CAS  PubMed  Google Scholar 

  • Ng EL, Ng JJ, Liang F, Tang BL (2009) Rab22B is expressed in the CNS astroglia lineage and plays a role in epidermal growth factor receptor trafficking in A431 cells. J Cell Physiol 221:716–728

    Article  CAS  PubMed  Google Scholar 

  • Ni X, Ma Y, Cheng H, Jiang M, Guo L, Ji C, Gu S, Cao Y, Xie Y, Mao Y (2002) Molecular cloning and characterization of a novel human Rab ( Rab2B) gene. J Hum Genet 47:548–551

    Article  CAS  PubMed  Google Scholar 

  • Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimizu S (2009) Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461:654–658

    Article  CAS  PubMed  Google Scholar 

  • Nokes RL, Fields IC, Collins RN, Fölsch H (2008) Rab13 regulates membrane trafficking between TGN and recycling endosomes in polarized epithelial cells. J Cell Biol 182:845–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nottingham RM, Ganley IG, Barr FA, Lambright DG, Pfeffer SR (2011) RUTBC1 protein, a Rab9A effector that activates GTP hydrolysis by Rab32 and Rab33B proteins. J Biol Chem 286:33213–33222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nottingham RM, Pusapati GV, Ganley IG, Barr FA, Lambright DG, Pfeffer SR (2012) RUTBC2 protein, a Rab9A effector and GTPase-activating protein for Rab36. J Biol Chem 287:22740–22748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuoffer C, Davidson HW, Matteson J, Meinkoth J, Balch WE (1994) A GDP-bound of rab1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments. J Cell Biol 125:225–237

    Article  CAS  PubMed  Google Scholar 

  • Olkkonen VM, Ikonen E (2006) When intracellular logistics fails—genetic defects in membrane trafficking. J Cell Sci 119:5031–5045

    Article  CAS  PubMed  Google Scholar 

  • Opdam FJ, Echard A, Croes HJ, van den Hurk JA, van de Vorstenbosch RA, Ginsel LA, Goud B, Fransen JA (2000) The small GTPase Rab6B, a novel Rab6 subfamily member, is cell-type specifically expressed and localised to the Golgi apparatus. J Cell Sci 113(Pt 15):2725–2735

    CAS  PubMed  Google Scholar 

  • Osipovich AB, Jennings JL, Lin Q, Link AJ, Ruley HE (2008) Dyggve-Melchior-Clausen syndrome: chondrodysplasia resulting from defects in intracellular vesicle traffic. Proc Natl Acad Sci USA 105:16171–16176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer KJ, Stephens DJ (2004) Biogenesis of ER-to-Golgi transport carriers: complex roles of COPII in ER export. Trends Cell Biol 14:57–61

    Article  CAS  PubMed  Google Scholar 

  • Parmar HB, Duncan R (2016) A novel tribasic Golgi export signal directs cargo protein interaction with activated Rab11 and AP-1-dependent Golgi-plasma membrane trafficking. Mol Biol Cell 27:1320–1331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira-Leal JB, Seabra MC (2000) 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 301:1077–1087

    Article  CAS  PubMed  Google Scholar 

  • Pereira-Leal JB, Seabra MC (2001) Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313:889–901

    Article  CAS  PubMed  Google Scholar 

  • Perrin L, Lacas-Gervais S, Gilleron J, Ceppo F, Prodon F, Benmerah A, Tanti JF, Cormont M (2013) Rab4b controls an early endosome sorting event by interacting with the gamma-subunit of the clathrin adaptor complex 1. J Cell Sci 126:4950–4962

    Article  CAS  PubMed  Google Scholar 

  • Pind SN, Nuoffer C, McCaffery JM, Plutner H, Davidson HW, Farquhar MG, Balch WE (1994) Rab1 and Ca2+ are required for the fusion of carrier vesicles mediating endoplasmic reticulum to Golgi transport. J Cell Biol 125:239–252

    Article  CAS  PubMed  Google Scholar 

  • Plutner H, Cox AD, Pind S, Khosravi-Far R, Bourne JR, Schwaninger R, Der CJ, Balch WE (1991) Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J Cell Biol 115:31–43

    Article  CAS  PubMed  Google Scholar 

  • Progida C, Bakke O (2016) Bidirectional traffic between the Golgi and the endosomes – machineries and regulation. J Cell Sci 129:3971–3982

    CAS  PubMed  Google Scholar 

  • Progida C, Cogli L, Piro F, De Luca A, Bakke O, Bucci C (2010) Rab7b controls trafficking from endosomes to the TGN. J Cell Sci 123:1480–1491

    Article  CAS  PubMed  Google Scholar 

  • Progida C, Nielsen MS, Koster G, Bucci C, Bakke O (2012) Dynamics of Rab7b-dependent transport of sorting receptors. Traffic 13:1273–1285

    Article  CAS  PubMed  Google Scholar 

  • Proikas-Cezanne T, Gaugel A, Frickey T, Nordheim A (2006) Rab14 is part of the early endosomal clathrin-coated TGN microdomain. FEBS Lett 580:5241–5246

    Article  CAS  PubMed  Google Scholar 

  • Pusapati GV, Luchetti G, Pfeffer SR (2012) Ric1-Rgp1 complex is a guanine nucleotide exchange factor for the late Golgi Rab6A GTPase and an effector of the medial Golgi Rab33B GTPase. J Biol Chem 287:42129–42137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puthenveedu MA, Linstedt AD (2001) Evidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130. J Cell Biol 155:227–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pylypenko O, Hammich H, Yu IM, Houdusse A (2018) Rab GTPases and their interacting protein partners: structural insights into Rab functional diversity. Small GTPases 9:22–48

    Article  CAS  PubMed  Google Scholar 

  • Rak A, Pylypenko O, Niculae A, Pyatkov K, Goody RS, Alexandrov K (2004) Structure of the Rab7:REP-1 complex: insights into the mechanism of Rab prenylation and choroideremia disease. Cell 117:749–760

    Article  CAS  PubMed  Google Scholar 

  • Reddy JV, Burguete AS, Sridevi K, Ganley IG, Nottingham RM, Pfeffer SR (2006) A functional role for the GCC185 golgin in mannose 6-phosphate receptor recycling. Mol Biol Cell 17:4353–4363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD (1998) 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 95:6187–6192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riederer MA, Soldati T, Shapiro AD, Lin J, Pfeffer SR (1994) Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J Cell Biol 125:573–582

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Gabin AG, Cammer M, Almazan G, Charron M, Larocca JN (2001) Role of rRAB22b, an oligodendrocyte protein, in regulation of transport of vesicles from trans Golgi to endocytic compartments. J Neurosci Res 66:1149–1160

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Gabin AG, Yin X, Si Q, Larocca JN (2009) Transport of mannose-6-phosphate receptors from the trans-Golgi network to endosomes requires Rab31. Exp Cell Res 315:2215–2230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Gabin AG, Ortiz E, Demoliner K, Si Q, Almazan G, Larocca JN (2010) Interaction of Rab31 and OCRL-1 in oligodendrocytes: its role in transport of mannose 6-phosphate receptors. J Neurosci Res 88:589–604

    CAS  PubMed  PubMed Central  Google Scholar 

  • Romer W, Pontani LL, Sorre B, Rentero C, Berland L, Chambon V, Lamaze C, Bassereau P, Sykes C, Gaus K, Johannes L (2010) Actin dynamics drive membrane reorganization and scission in clathrin-independent endocytosis. Cell 140:540–553

    Article  CAS  PubMed  Google Scholar 

  • Russo AJ, Mathiowetz AJ, Hong S, Welch MD, Campellone KG (2016) Rab1 recruits WHAMM during membrane remodeling but limits actin nucleation. Mol Biol Cell 27:967–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F (2005) Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol 169:285–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salian S, Cho TJ, Phadke SR, Gowrishankar K, Bhavani GS, Shukla A, Jagadeesh S, Kim OH, Nishimura G, Girisha KM (2017) Additional three patients with Smith-McCort dysplasia due to novel RAB33B mutations. Am J Med Genet A 173:588–595

    Article  CAS  PubMed  Google Scholar 

  • Salminen A, Novick PJ (1987) A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49:527–538

    Article  CAS  PubMed  Google Scholar 

  • Sandvig K, Skotland T, van Deurs B, Klokk TI (2013) Retrograde transport of protein toxins through the Golgi apparatus. Histochem Cell Biol 140:317–326

    Article  CAS  PubMed  Google Scholar 

  • Saraste J, Lahtinen U, Goud B (1995) Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway. J Cell Sci 108(Pt 4):1541–1552

    CAS  PubMed  Google Scholar 

  • Sato K, Roboti P, Mironov AA, Lowe M (2015) Coupling of vesicle tethering and Rab binding is required for in vivo functionality of the golgin GMAP-210. Mol Biol Cell 26:537–553

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Satoh A, Wang Y, Malsam J, Beard MB, Warren G (2003) Golgin-84 is a rab1 binding partner involved in Golgi structure. Traffic 4:153–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitt HD, Wagner P, Pfaff E, Gallwitz D (1986) The ras-related YPT1 gene product in yeast: a GTP-binding protein that might be involved in microtubule organization. Cell 47:401–412

    Article  CAS  PubMed  Google Scholar 

  • Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, Mellman I, Simons K (2007) Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 8:47–60

    Article  CAS  PubMed  Google Scholar 

  • Seabra MC, Coudrier E (2004) Rab GTPases and myosin motors in organelle motility. Traffic 5:393–399

    Article  CAS  PubMed  Google Scholar 

  • Sechi S, Frappaolo A, Fraschini R, Capalbo L, Gottardo M, Belloni G, Glover DM, Wainman A, Giansanti MG (2017) Rab1 interacts with GOLPH3 and controls Golgi structure and contractile ring constriction during cytokinesis in Drosophila melanogaster. Open Biol 7. https://doi.org/10.1098/rsob.160257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Segev N, Mulholland J, Botstein D (1988) The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell 52:915–924

    Article  CAS  PubMed  Google Scholar 

  • Short B, Preisinger C, Korner R, Kopajtich R, Byron O, Barr FA (2001) A GRASP55-rab2 effector complex linking Golgi structure to membrane traffic. J Cell Biol 155:877–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Short B, Preisinger C, Schaletzky J, Kopajtich R, Barr FA (2002) The Rab6 GTPase regulates recruitment of the dynactin complex to Golgi membranes. Curr Biol 12:1792–1795

    Article  CAS  PubMed  Google Scholar 

  • Sinka R, Gillingham AK, Kondylis V, Munro S (2008) Golgi coiled-coil proteins contain multiple binding sites for Rab family G proteins. J Cell Biol 183:607–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spang A (2013) Retrograde traffic from the Golgi to the endoplasmic reticulum. Cold Spring Harb Perspect Biol 5. https://doi.org/10.1101/cshperspect.a013391

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spang A (2016) Membrane tethering complexes in the endosomal system. Front Cell Dev Biol 4:35

    Article  PubMed  PubMed Central  Google Scholar 

  • Starr T, Sun Y, Wilkins N, Storrie B (2010) Rab33b and Rab6 are functionally overlapping regulators of Golgi homeostasis and trafficking. Traffic 11:626–636

    Article  CAS  PubMed  Google Scholar 

  • Stein MP, Feng Y, Cooper KL, Welford AM, Wandinger-Ness A (2003) Human VPS34 and p150 are Rab7 interacting partners. Traffic 4:754–771

    Article  CAS  PubMed  Google Scholar 

  • Stenmark H, Valencia A, Martinez O, Ullrich O, Goud B, Zerial M (1994) Distinct structural elements of rab5 define its functional specificity. EMBO J 13:575–583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storrie B (2005) Maintenance of Golgi apparatus structure in the face of continuous protein recycling to the endoplasmic reticulum: making ends meet. Int Rev Cytol 244:69–94

    Article  CAS  PubMed  Google Scholar 

  • Storrie B, Micaroni M, Morgan GP, Jones N, Kamykowski JA, Wilkins N, Pan TH, Marsh BJ (2012) Electron tomography reveals Rab6 is essential to the trafficking of trans-Golgi clathrin and COPI-coated vesicles and the maintenance of Golgi cisternal number. Traffic 13:727–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suchy SF, Olivos-Glander IM, Nussbaum RL (1995) Lowe Syndrome, a deficiency of a phosphatidyl-inositol 4,5-bisphosphate 5-phosphatase in the Golgi apparatus. Hum Mol Genet 4:2245–2250

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Shestakova A, Hunt L, Sehgal S, Lupashin V, Storrie B (2007) Rab6 regulates both ZW10/RINT-1 and conserved oligomeric Golgi complex-dependent Golgi trafficking and homeostasis. Mol Biol Cell 18:4129–4142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szul T, Sztul E (2011) COPII and COPI traffic at the ER-Golgi interface. Physiology (Bethesda) 26:348–364

    CAS  Google Scholar 

  • Takahashi S, Kubo K, Waguri S, Yabashi A, Shin HW, Katoh Y, Nakayama K (2012) Rab11 regulates exocytosis of recycling vesicles at the plasma membrane. J Cell Sci 125:4049–4057

    Article  CAS  PubMed  Google Scholar 

  • Tisdale EJ, Bourne JR, Khosravi-Far R, Der CJ, Balch WE (1992) GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J Cell Biol 119:749–761

    Article  CAS  PubMed  Google Scholar 

  • Touchot N, Zahraoui A, Vielh E, Tavitian A (1989) Biochemical properties of the YPT-related rab1B protein. Comparison with rab1A. FEBS Lett 256:79–84

    Article  CAS  PubMed  Google Scholar 

  • Trahey M, Hay JC (2010) Transport vesicle uncoating: it’s later than you think. F1000 Biol Rep 2:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Ullrich O, Stenmark H, Alexandrov K, Huber LA, Kaibuchi K, Sasaki T, Takai Y, Zerial M (1993) Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J Biol Chem 268:18143–18150

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Urbe S, Huber LA, Zerial M, Tooze SA, Parton RG (1993) Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett 334:175–182

    Article  CAS  PubMed  Google Scholar 

  • Utskarpen A, Slagsvold HH, Iversen TG, Walchli S, Sandvig K (2006) Transport of ricin from endosomes to the Golgi apparatus is regulated by Rab6A and Rab6A′. Traffic 7:663–672

    Article  CAS  PubMed  Google Scholar 

  • Valsdottir R, Hashimoto H, Ashman K, Koda T, Storrie B, Nilsson T (2001) Identification of rabaptin-5, rabex-5, and GM130 as putative effectors of rab33b, a regulator of retrograde traffic between the Golgi apparatus and ER. FEBS Lett 508:201–209

    Article  CAS  PubMed  Google Scholar 

  • Viotti C (2016) ER to Golgi-dependent protein secretion: the conventional pathway. Methods Mol Biol 1459:3–29

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Hong W (2002) Interorganellar regulation of lysosome positioning by the Golgi apparatus through Rab34 interaction with Rab-interacting lysosomal protein. Mol Biol Cell 13:4317–4332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Lou J, Ouyang C, Chen W, Liu Y, Liu X, Cao X, Wang J, Lu L (2010) Ras-related protein Rab10 facilitates TLR4 signaling by promoting replenishment of TLR4 onto the plasma membrane. Proc Natl Acad Sci USA 107:13806–13811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, Ma Z, Xu X, Wang Z, Sun L, Zhou Y, Lin X, Hong W, Wang T (2014) A role of Rab29 in the integrity of the trans-Golgi network and retrograde trafficking of mannose-6-phosphate receptor. PLoS One 9:e96242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang P, Liu H, Wang Y, Liu O, Zhang J, Gleason A, Yang Z, Wang H, Shi A, Grant BD (2016) RAB-10 promotes EHBP-1 bridging of filamentous actin and tubular recycling endosomes. PLoS Genet 12:e1006093

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weide T, Bayer M, Koster M, Siebrasse JP, Peters R, Barnekow A (2001) The Golgi matrix protein GM130: a specific interacting partner of the small GTPase rab1b. EMBO Rep 2:336–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White J, Johannes L, Mallard F, Girod A, Grill S, Reinsch S, Keller P, Tzschaschel B, Echard A, Goud B, Stelzer EH (1999) Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J Cell Biol 147:743–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson BS, Nuoffer C, Meinkoth JL, McCaffery M, Feramisco JR, Balch WE, Farquhar MG (1994) A Rab1 mutant affecting guanine nucleotide exchange promotes disassembly of the Golgi apparatus. J Cell Biol 125:557–571

    Article  CAS  PubMed  Google Scholar 

  • Witkos TM, Lowe M (2017) Recognition and tethering of transport vesicles at the Golgi apparatus. Curr Opin Cell Biol 47:16–23

    Article  CAS  PubMed  Google Scholar 

  • Wong M, Munro S (2014) Membrane trafficking. The specificity of vesicle traffic to the Golgi is encoded in the golgin coiled-coil proteins. Science 346:1256898

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu YW, Tan KT, Waldmann H, Goody RS, Alexandrov K (2007) Interaction analysis of prenylated Rab GTPase with Rab escort protein and GDP dissociation inhibitor explains the need for both regulators. Proc Natl Acad Sci USA 104:12294–12299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu YW, Goody RS, Abagyan R, Alexandrov K (2009) Structure of the disordered C terminus of Rab7 GTPase induced by binding to the Rab geranylgeranyl transferase catalytic complex reveals the mechanism of Rab prenylation. J Biol Chem 284:13185–13192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yadav S, Linstedt AD (2011) Golgi positioning. Cold Spring Harb Perspect Biol 3. https://doi.org/10.1101/cshperspect.a005322

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Young J, Stauber T, del Nery E, Vernos I, Pepperkok R, Nilsson T (2005) Regulation of microtubule-dependent recycling at the trans-Golgi network by Rab6A and Rab6A′. Mol Biol Cell 16:162–177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young J, Menetrey J, Goud B (2010) RAB6C is a retrogene that encodes a centrosomal protein involved in cell cycle progression. J Mol Biol 397:69–88

    Article  CAS  PubMed  Google Scholar 

  • Zhen Y, Stenmark H (2015) Cellular functions of Rab GTPases at a glance. J Cell Sci 128:3171–3176

    Article  CAS  PubMed  Google Scholar 

  • Zheng JY, Koda T, Fujiwara T, Kishi M, Ikehara Y, Kakinuma M (1998) A novel Rab GTPase, Rab33B, is ubiquitously expressed and localized to the medial Golgi cisternae. J Cell Sci 111(Pt 8):1061–1069

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

C. Progida is supported by grants from the Research Council of Norway (grant 287560), the Norwegian Cancer Society (grant 198094), the Anders Jahre Foundation, and the S. G. Sønneland Foundation.

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Progida, C. (2019). Multiple Roles of Rab GTPases at the Golgi. In: Kloc, M. (eds) The Golgi Apparatus and Centriole. Results and Problems in Cell Differentiation, vol 67. Springer, Cham. https://doi.org/10.1007/978-3-030-23173-6_6

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