Identification of a Rab GTPase-activating protein cascade that controls recycling of the Rab5 GTPase Vps21 from the vacuole

Molecular Biology of the Cell

Volumn 26, Issue 13, 2015, Pages 2535-2549

  Rana, Meenakshi ^a   Lachmann, Jens ^a   Ungermann, Christian ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN BLOC 1; PROTEIN MSB3; PROTEIN VPS21; PROTEIN YPT7; RAB PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; CCZ1 PROTEIN, S CEREVISIAE; MON1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; VESICULAR TRANSPORT PROTEIN; VPS21 PROTEIN, S CEREVISIAE; YPT7 PROTEIN, S CEREVISIAE;

ARTICLE; CELL VACUOLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; LYSOSOME; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; COMPARATIVE STUDY; ENZYMOLOGY; METABOLISM; SACCHAROMYCES CEREVISIAE;

ENDOSOMES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84934325667     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-02-0062     Document Type: Article

References (57)

1. 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.
2. Arlt H, Auffarth K, Kurre R, Lisse D, Piehler J, Ungermann C (2015a). Spatio-temporal dynamics of membrane remodeling and fusion proteins during endocytic transport. Mol Biol Cell 26, 1357-1370.
3. Arlt H, Reggiori F, Ungermann C (2015b). Retromer and the dynamin Vps1 cooperate in the retrieval of transmembrane proteins from vacuoles. J Cell Sci 128, 645-655.
4. Auffarth K, Arlt H, Lachmann J, Cabrera M, Ungermann C (2014). Tracking of the dynamic localization of the Rab-specific HOPS subunits reveal their distinct interaction with Ypt7 and vacuoles. Cell Logistics 4, e29191.
5. Balderhaar HJK, Arlt H, Ostrowicz CW, Bröcker C, Sündermann F, Brandt R, Babst M, Ungermann C (2010). The Rab GTPase Ypt7 is linked to retromer-mediated receptor recycling and fusion at the yeast late endosome. J Cell Sci 123, 4085-4094.
6. Balderhaar HJK, Lachmann J, Yavavli E, Bröcker C, Lürick A, Ungermann C (2013). The CORVET complex promotes tethering and fusion of Rab5/Vps21-positive membranes. Proc Natl Acad Sci USA 110, 3823-3828.
7. Balderhaar HJK, Ungermann C (2013). CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion. J Cell Sci 126, 1307-1316.
8. Barr F, Lambright DG (2010). Rab GEFs and GAPs. Curr Opin Cell Biol 22, 461-470.
9. Barr FA (2013). Rab GTPases and membrane identity: causal or inconsequential? J Cell Biol 202, 191-199.
10. Bean BDM, Davey M, Snider J, Jessulat M, Deineko V, Tinney M, Stagljar I, Babu M, Conibear E (2015). Rab5-family guanine nucleotide exchange factors bind retromer and promote its recruitment to endosomes. Mol Biol Cell 26, 1119-1128.
11. Bröcker C, Kuhlee A, Gatsogiannis C, Kleine Balderhaar HJ, Hönscher C, Engelbrecht-Vandré S, Ungermann C, Raunser S (2012). Molecular architecture of the multisubunit homotypic fusion and vacuole protein sorting (HOPS) tethering complex. Proc Natl Acad Sci USA 109, 1991-1996.
12. Cabrera M, Arlt H, Epp N, Lachmann J, Griffith J, Perz A, Reggiori F, Ungermann C (2013). Functional separation of endosomal fusion factors and the class C core vacuole/endosome tethering (CORVET) complex in endosome biogenesis. J Biol Chem 288, 5166-5175.
13. Cabrera M, Langemeyer L, Mari M, Rethmeier R, Orban I, Perz A, Bröcker C, Griffith J, Klose D, Steinhoff H-J, et al. (2010). Comment on: phosphorylation of a membrane curvature-sensing motif switches function of the HOPS subunit Vps41 in membrane tethering. J Cell Biol 191,845-859.
14. Cabrera M, Nordmann M, Perz A, Schmedt D, Gerondopoulos A, Barr F, Piehler J, Engelbrecht-Vandré S, Ungermann C (2014). The Mon1-Ccz1 GEF activates the Rab7 GTPase Ypt7 via a longin-fold-Rab interface and association with PI3P-positive membranes. J Cell Sci 127, 1043-1051.
15. Cabrera M, Ungermann C (2013). Guanine nucleotide exchange factors (GEFs) have a critical but not exclusive role in organelle localization of Rab GTPases. J Biol Chem 288, 28704-287
16. del Conte-Zerial P, Brusch L, Rink JC, Collinet C, Kalaidzidis Y, Zerial M, Deutsch A (2008). Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol Syst Biol 4, 206.
17. Di Pietro SM, Falcón-Pérez JM, Tenza D, Setty SRG, Marks MS, Raposo G, Dell'Angelica EC (2006). BLOC-1 interacts with BLOC-2 and the AP-3 complex to facilitate protein trafficking on endosomes. Mol Biol Cell 17, 4027-4038.
18. Epp N, Ungermann C (2013). The N-terminal domains of Vps3 and Vps8 are critical for localization and function of the CORVET tethering complex on endosomes. PLoS One 8, e67307.
19. Gao X-D, Albert S, Tcheperegine SE, Burd CG, Gallwitz D, Bi E (2003). The GAP activity of Msb3p and Msb4p for the Rab GTPase Sec4p is required for efficient exocytosis and actin organization. J Cell Biol 162, 635-646.
20. Gautreau A, Oguievetskaia K, Ungermann C (2014). Function and regulation of the endosomal fusion and fission machineries. CSH Perspect Biology 6, a016832.
21. Haas A (1995). A quantitative assay to measure homotypic vacuole fusion in vitro. Methods Cell Sci 17, 283-294.
22. Haas AK, Fuchs E, Kopajtich R, Barr FA (2005). A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol 7, 887-893.
23. Hayes MJ, Bryon K, Satkurunathan J, Levine TP (2011). Yeast homologues of three BLOC-1 subunits highlight KxDL proteins as conserved interactors of BLOC-1. Traffic 12, 260-268.
24. Huotari J, Helenius A (2011). Endosome maturation. EMBO J 30, 3481-3500.
25. Hutagalung AH, Novick PJ (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91, 119-149.
26. Itzen A, Goody RS (2011). GTPases involved in vesicular trafficking: structures and mechanisms. Semin Cell Dev Biol 22, 48-56.
27. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, et al. (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
28. John Peter AT, Lachmann J, Rana M, Bunge M, Cabrera M, Ungermann C (2013). The BLOC-1 complex promotes endosomal maturation by recruiting the Rab5 GTPase-activating protein Msb3. J Cell Biol 201, 97-111.
29. Kucharczyk R, Kierzek AM, Slonimski PP, Rytka J (2001). The Ccz1 protein interacts with Ypt7 GTPase during fusion of multiple transport intermediates with the vacuole in S. cerevisiae. J Cell Sci 114, 3137-3145.
30. Lachmann J, Barr FA, Ungermann C (2012). The Msb3/Gyp3 GAP controls the activity of the Rab GTPases Vps21 and Ypt7 at endosomes and vacuoles. Mol Biol Cell 23, 2516-2526.
31. Lachmann J, Ungermann C, Engelbrecht-Vandré S (2011). Rab GTPases and tethering in the yeast endocytic pathway. Small GTPases 2, 182-186.
32. LaGrassa TJ, Ungermann C (2005). The vacuolar kinase Yck3 maintains organelle fragmentation by regulating the HOPS tethering complex. J Cell Biol 168, 401-414.
33. Lee HH, Nemecek D, Schindler C, Smith WJ, Ghirlando R, Steven AC, Bonifacino JS, Hurley JH (2012). Assembly and architecture of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J Biol Chem 287, 5882-5890.
34. Liu T-T, Gomez TS, Sackey BK, Billadeau DD, Burd CG (2012). Rab GTPase regulation of retromer-mediated cargo export during endosome maturation. Mol Biol Cell 23, 2505-2515.
35. Markgraf DF, Ahnert F, Arlt H, Mari M, Peplowska K, Epp N, Griffith J, Reggiori F, Ungermann C (2009). The CORVET subunit Vps8 cooperates with the Rab5 homolog Vps21 to induce clustering of late endosomal compartments. Mol Biol Cell 20, 5276-5289.
36. Nickerson DP, Russell MRG, Lo S-Y, Chapin HC, Milnes JM, Merz AJ (2012). Termination of isoform-selective Vps21/Rab5 signaling at endolysosomal organelles by Msb3/Gyp3. Traffic 13, 1411-1428.
37. Nordmann M, Cabrera M, Perz A, Bröcker C, Ostrowicz CW, Engelbrecht-Vandré S, Ungermann C (2010). The Mon1-Ccz1 complex is the GEF of the late endosomal Rab7 homolog Ypt7. Curr Biol 20, 1654-1659.
38. 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.
39. 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.
40. Ostrowicz CW, Bröcker C, Ahnert F, Nordmann M, Lachmann J, Peplowska K, Perz A, Auffarth K, Engelbrecht-Vandré S, Ungermann C (2010). Defined subunit arrangement and Rab interactions are required for functionality of the HOPS tethering complex. Traffic 11, 1334-1346.
41. Peplowska K, Markgraf DF, Ostrowicz CW, Bange G, Ungermann C (2007). The CORVET tethering complex interacts with the yeast Rab5 homolog Vps21 and is involved in endo-lysosomal biogenesis. Dev Cell 12, 739-750.
42. Plemel RL, Lobingier BT, Brett CL, Angers CG, Nickerson DP, Paulsel A, Sprague D, Merz AJ (2011). Subunit organization and Rab interactions of Vps-C protein complexes that control endolysosomal membrane traffic. Mol Biol Cell 22, 1353-1363.
43. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010). Identification of the switch in early-to-late endosome transition. Cell 141, 497-508.
44. Rak A, Pylypenko O, Durek T, Watzke A, Kushnir S, Brunsveld L, Waldmann H, Goody RS, Alexandrov K (2003). Structure of Rab GDP-dissociation inhibitor in complex with prenylated YPT1 GTPase. Science 302, 646-650.
45. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749.
46. Rivera-Molina FE, Novick PJ (2009). A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc Natl Acad Sci USA 106, 14408-14413.
47. Robinson JS, Klionsky DJ, Banta LM, Emr SD (1988). Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 8, 4936-4948.
48. Rojas R, van Vlijmen T, Mardones GA, Prabhu Y, Rojas AL, Mohammed S, Heck AJ, Raposo G, van der Sluijs P, Bonifacino JS (2008). Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J Cell Biol 183, 513-526.
49. Salazar G, Craige B, Styers ML, Newell-Litwa KA, Doucette MM, Wainer BH, Falcon-Perez JM, Dell'Angelica EC, Peden AA, Werner E, et al. (2006). BLOC-1 complex deficiency alters the targeting of adaptor protein complex-3 cargoes. Mol Biol Cell 17, 4014-4026.
50. Seals D, Eitzen G, Margolis N, Wickner W, Price A (2000). A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc Natl Acad Sci USA 97, 9402-9407.
51. Setty SRG, Tenza D, Truschel ST, Chou E, Sviderskaya EV, Theos AC, Lamoreux ML, Di Pietro SM, Starcevic M, Bennett DC, et al. (2007). BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol Biol Cell 18, 768-780.
52. Singh MK, Krüger F, Beckmann H, Brumm S, Vermeer JEM, Munnik T, Mayer U, Stierhof Y-D, Grefen C, Schumacher K, et al. (2014). Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion. Curr Biol 24, 1383-1389.
53. Solinger JA, Spang A (2014). Loss of the Sec1/Munc18-family proteins VPS-33.2 and VPS-33.1 bypasses a block in endosome maturation in Caenorhabditis elegans. Mol Biol Cell 25, 3909-3925.
54. Sot B, Behrmann E, Raunser S, Wittinghofer A (2013). Ras GTPase activating (RasGAP) activity of the dual specificity GAP protein Rasal requires colocalization and C2 domain binding to lipid membranes. Proc Natl Acad Sci USA 110, 111-116.
55. Suda Y, Kurokawa K, Hirata R, Nakano A (2013). Rab GAP cascade regulates dynamics of Ypt6 in the Golgi traffic. Proc Natl Acad Sci USA 110, 18976-18981.
56. Sung M-K, Huh W-K (2007). Bimolecular fluorescence complementation analysis system for in vivo detection of protein-protein interaction in Saccharomyces cerevisiae. Yeast 24, 767-775.
57. Wurmser AE, Sato TK, Emr SD (2000). 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.