Mammalian Late Vacuole Protein Sorting Orthologues Participate in Early Endosomal Fusion and Interact with the Cytoskeleton

Molecular Biology of the Cell

Volumn 15, Issue 3, 2004, Pages 1197-1210

  Richardson, Simon C W ^a   Winistorfer, Stanley C ^a   Poupon, Viviane ^b   Luzio, J Paul ^b   Piper, Robert C ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CELL PROTEIN; PROTEIN MVAM2P; PROTEIN MVAM6; PROTEIN MVPS11; PROTEIN MVPS16; PROTEIN MVPS18; PROTEIN MVPS45; SYNAPTOBREVIN; SYNAPTOBREVIN 13; SYNAPTOBREVIN 6; SYNAPTOBREVIN 7; SYNTAXIN; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BIOGENESIS; CELL VACUOLE; CONTROLLED STUDY; CYTOSKELETON; ENDOSOME; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

ANIMALS; CERCOPITHECUS AETHIOPS; CHO CELLS; CRICETINAE; CRICETULUS; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; ENDOSOMES; MEMBRANE FUSION; PROTEIN TRANSPORT; RATS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLES; VERO CELLS; VESICULAR TRANSPORT PROTEINS;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS; MAMMALIA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 1542283806     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-06-0358     Document Type: Article

References (75)

1. Accoceberry, I., Thellier, M., Datry, A., Desportes-Livage, I., Biligui, S., Danis, M., and Santaelli, X (2001). One-step purification of Enterocytozoon bieneusi from human stools by immunoaffinity expanded bed adsorption. J. Clin. Microbiol. 39, 1947-1951.
2. Allen, V. (1995). Membrane traffic motors. FEBS Lett. 369, 101-106.
3. Antonin, W., Dulubova, I., Arac, D., Pabst, S., Plitzner, J., Rizo, J., and Jahn, R. (2002). The N-terminal domains of Syn7 and Vti1b form three-helix bundles that differ in their ability to regulate SNARE complex assembly. J. Biol. Chem. 277, 36449-36456.
4. Apodacia, G. (2001). Endocytic traffic in polarized epithelial cells: role of the actin and Microtubule cytoskeleton. Traffic 2, 149-159.
5. Bogdanovic, A., Bennett, N., Kieffer, S., Louwagie, M., Morio, T., Garin, J., Satre, M., and Bruckert, F. (2002). Syn7, Syn 8, Vti1 and Vamp7 (vesicle-associated membrane protein 7) form an active S.N.A.R.E. complex for early macropinocytic compartment fusion in Dictyostelium discoideum. Biochem. J. 368, 29-39.
6. Caplan, S., Hartnell, L.M., Aguilar, R.C., Naslavsky, N., and Bonifacino, J. (2001). Human Vam6p promotes lysosomal clustering and fusion in vivo. J. Cell Biol. 154, 109-121.
7. Chen, Y.A., and Scheller, R.H. (2001). SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2, 98-106.
8. Chimini, G., and Chavrier, P. (2000). Function of Rho family proteins in actin dynamics during phagocytosis and engulfment. Nat. Cell Biol. 2, E191-E196.
9. Christoforidis, S., Mcbride, H., Burgoyne, R.D., and Zerial, M. 1999. The Rab5 effectors EEA1 is a core component of endosome docking. Nature 397, 621-625.
10. Cordonnier, M.-N., Dauzonne, D., Louvard, D., and Coudrier, E. (2001). Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell 12, 4013-4029.
11. de Renzis, S., Sonnichsen, B., and Zerial, M. (2002). Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes. Nat. Cell Biol. 4, 124-133.
12. Eitzen, G., Thorngren, N., and Wickner, W. (2001). Rho1p and CDC42p act after Ypt7p to regulate vacuole docking. EMBO J. 20, 5650-5656.
13. Eitzen, G., Wang, L., Thorngren, N., and Wickner, W. (2002). Remodeling of organelle-bound actin is required for yeast vacuole fusion. J. Cell Biol. 158, 669-679.
14. Eitzen, G. (2003). Actin remodeling to facilitate membrane fusion. Biochim. Biophys. Acta 1641, 175-181.
15. Ellis, S., and Mellor, H. (2000). Regulation of endocytic traffic by rho family GTPases. Trends Cell Biol. 10, 85-88.
16. Falcon-Perez, J.M., Starcevic, M., Gautam, R., and Dell'Angelica, E.C. (2002). BLOC-1, a novel complex containing the pallidin and muted proteins involved in the biogenesis of melanosomes and platelet-dense granules. J. Biol. Chem. 277, 28191-28199.
17. Fucini, R.V., Navarrete, A., Vadakkan, C., Lacomis, L., Erdjument-Bromage, H., Tempst, P., and Stamnes, M. (2000). Activated ADP-ribosylation factor assembles distinct pools of actin on Golgi membranes. J. Biol. Chem. 275, 18824-18829.
18. Gaullier, J.M., Simonsen, A., D'Arrigo, A., Bremnes, B., and Stenmark, H. (1999). FYVE finger protein as effectors of phosphatidylinositol 3-phosphate. Chem. Physiol. Lipids 98, 87-94.
19. Gorvel, J.-P., Chavrier, P., Zerial, M., and Gruenberg, J. (1991). Rab5 controls early endosome fusion in vitro. Cell 64, 915-925.
20. Gough, N.R., Zweifel, M.E., Martinez-Augustin, O., Aguilar, R.C., Bonifacino, J.S., and Fambourgh, D.M. (1999). Utilization of the indirect lysosomal targeting pathway by lysosome-associated membrane proteins (LAMPs) is influenced largely by the C-terminal residue of their GYXXf targeting signals. J. Cell Sci. 112, 4257-4269.
21. Gruenberg, J., Griffiths, G., Howell, K.E. (1989). Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316.
22. Hay, J.C. (2001). SNARE complex structure and function. Exp. Cell Res. 271, 10-21.
23. Horazdovsky, B.F., Cowles, C.R., Mustol, P., Holmes, M., and Emr, S.D. (1996). A novel RING finger protein, Vps8p, functionally interacts with the small GTPase, Vps21p, to facilitate soluble vacuolar protein localization. J. Biol. Chem. 271, 33607-33615.
24. Jahraus, A., Egeberg, M., Hinner, B., Habermann, A., Sackman, E., Pralle, A., Faulstich, H., Rybin, V., Defacque, H., and Griffiths, G. (2001). ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol. Biol. Cell 12, 155-170.
25. Kelly, R.B. (1990). Associations between microtubules and intracellular organelles. Curr. Opin. Cell Biol. 2, 105-108.
26. Kim, B.Y., Kramer, H., Yamamoto, A., and Kominami, E. (2001). Molecular characterization of mammalian homologues of class C Vps proteins that interact with Syn-7. J. Biol. Chem. 276, 29393-29402.
27. Kramer, H., and Phistry, M. (1999). Genetic Analysis of hook, a gene required for endocytic trafficking in Drosophila. Genetics 151, 675-684.
28. Langford, G.M. (2002). Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3, 859-865.
29. Yi, Z., Yokota, H., Torii, S., Aoki, T., Hosaka, M., Zhao, S., Takata, K., Takeuchi, T., and Izumi, T. (2002). The Rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol. Cell Biol. 22, 1858-1867.
30. Lipschutz, J.H., and Mostov, K.E. (2002). Exocytosis: the many masters of the exocyst. Curr. Biol. 12, R212-R214.
31. Lloyd, V., Ramaswami, M., and Kramer, H. (1998). Not just pretty eyes: Drosophila eye-color mutations and lysosomal delivery. Trends Cell Biol. 8, 257-259.
32. McBride, H.M., Rybin, V., Murphy, C., Giner, A., Teasdale, R., and Zerial, M. (1999). Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and Syn 13. Cell 98, 377-386.
33. McVey Ward, D., Pevsner, J., Scullion, M. A., Vaughn, M. and Kaplan. J. (2000). Syn7 and VAMP-7 are soluble N-ethylmaleimide-sensitive factor attachment protein receptors required for late endosome-lysosome and homotypic lysosome fusion in alveolar macrophages. Mol. Biol. Cell 11, 2327-2333.
34. McVey Ward, D., Radisky, D., Scullion, M.A., Tuttle, M.S., Vaughn, M., and Kaplan, J. (2001). hVPS41 is expressed in multiple isoforms and can associate with vesicles through a RING-H2 finger motif. Exp. Cell Res. 267, 126-134.
35. Metzelaar, M.J., Wijngaard, P.L., Peters, P.J., Sixma, J.J., Nieuwenhuis, H.K., and Clevers, H.C. (1991). CD63 antigen. A novel lysosomal membrane glycoprotein, cloned by a screening procedure for intracellular antigens in eukaryotic cells. J. Biol. Chem. 266, 3239-3245.
36. Mills, I.G., Urbe, S., and Clague, M.J. (2001). Relationships between EEA1 binding partners and their role in endosome fusion. J. Cell Sci. 114,1959-1965.
37. Muller, O., Johnson, D.I., and Mayer, A. (2001). Cdc42p functions at the docking stage of yeast vacuole membrane fusion. EMBO J. 20, 5657-65.
38. Mullock, B.M., Smith, C.W., Bright, N.A., Ihrke, G., Lindsay, M., Parton, R.G., James, D.E., Luzio, J.P., and Piper, R.C. (2000). Syn 7 is localized to late endosomes compartments, associated with Vamp 8, and is required for endosome, lysosome fusion. Mol. Biol. Cell 11, 3137-3153.
39. Murphy, C., Saffrich, R., Grummt, M., Gournier, H., Rybin, V., Rubino, M., Auvinen, P., Lütcke, A., Parton, R.G., and Zerial, M. (1996). Endosome dynamics regulated by a Rho protein. Nature 384, 427-432.
40. Narayanan, R., Kramer, H., and Ramaswami, M. (2000). Drosophila endosomal proteins Hook and Deep Orange regulate synapse size but not synaptic vesicle recycling. J. Neurobiol. 45, 105-119.
41. Nielsen, E., Christoforidis, S., Uttenweiler-Joseph, S., Miaczynska, M., Dewitte, F., Wilm, M., Hoflack, B., and Zerial, M. (2000). Rabenosyn-5, a novel Rab5 effecter, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J. Cell Biol. 151, 601-612.
42. Prekeris, R., Klumperman, J., Chen, Y.A., and Scheller, R.H. (1998). Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J. Cell Biol. 143, 957-971.
43. Prekeris, R., Yang, B., Oorschot, V., Klumperman, J., and Scheller, R.H. (1999). Differential roles of Syntaxin7 and Syntaxin8 during endosomal trafficking. Mol. Biol. Cell 10, 3891-908.
44. Peterson, M.R., Burd, C.G., and Emr, S.D. (1999). Vac1p coordinates Vps21 Rab GTPase and Vps34 PtdIns 3-kinase signaling, essential for Pep12- and Vps45p-dependent vesicle docking/fusion at the endosome. Curr. Biol. 9, 159-162.
45. Peterson, M.R., and Emr, S.D. (2001). The class C Vps complex functions at multiple stages of the vacuolar transport pathway. Traffic 2, 476-486.
46. Poupon, V., Stewart, A., Gray, S.R., Piper, R.C., and Luzio, J.P. (2003). The role of mVps18 in clustering, fusion, and intracellular localization of late endocytic organelles. Mol. Biol. Cell 14, 4015-4027.
47. Price, A., Seals, D., Wickner, W., and Ungerman, C. (2000). The docking stages of yeast vacuole fusion requires the transfer of proteins from a cis-SNARE complex to a Rab/Ypt protein. J. Cell Biol. 148, 1231-1238.
48. Qualmann, B., Kessels, M.M., and Kelly, R. (2000). Molecular links between endocytosis and the actin cytoskeleton. J. Cell Biol. 150, F111-F116.
49. Rieder, S.E., and Emr, S.D. (1997). A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol. Biol. Cell 8, 2307-2327.
50. Roberts, R.L., Barbieri, K.M., Pryse, K.M., Chua, M., Morisaki, J.H., and Stahl, P.D. (1999). Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112, 3667-3675.
51. Rogers, S.L., and Gelfand, V.I. (2000). Membrane trafficking, organelle transport and the cytoskeleton. Curr. Opin. Cell Biol. 12, 57-62.
52. Sato, T.K., Rehling, P., Peterson, M.R., and Emr, S.D. (2000). Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Mol. Cell 6, 661-671.
53. Schroer, T.A. (2000). Motors, clutches and breaks for membrane traffic: a commemorative review in honor of Thomas Kreis. Traffic 1, 3-10.
54. Seals, D.F., Eitzen, G., Margolis, N., Wickner, W., and Price, A. (2000). A Ypt/Rab effecter complex containing the Sec1 homologue Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. USA 97, 9402-9407.
55. Sevrioukov, E.A., He, J.-P. Moghabi, N., Sunio, A., and Kramer, H. (1999). A role for the Deep Orange and Carnation eye color genes in lysosomal delivery in Drosophila. Mol. Cell 4, 479-486.
56. Shin, C.S., Hong, M. S. Cheon, S.B., and Jeewon, L. (1997). Enhanced production of human mini-proinsulin in fed-batch cultures at high cell density of Escherchia coli BL21(DE3) [pET-3aT2M2]. Biotechnol. Prog. 13, 249-257.
57. Stoorvogel, W. (1993). Arguments in favor of endosomal maturation. Biochem. Soc. Trans. 3, 711-715.
58. Short, B., Preisinger, C., Schaletzky, J., Kopajtich, J., and Barr, F.A. (2002). The Rab6 GTPase regulates recruitment of the dynactin complex to Golgi membranes. Curr. Biol. 12, 1792-1795.
59. Simonsen, A., Gaullier, J.-M. D'Arrigo, A., and Stenmark, H. (1999). The Rab5 effecter EEA1 interacts directly with Syn-6. J. Cell Biol. 247, 28857-28860.
60. Sollner, T.H. (2003). Regulated exocytosis and SNARE function. Mol. Membr. Biol. 20, 209-220.
61. Srivastava, A., Woolford, C., and Jones, E.W. (2000). Pep3p/Pep5p complex: a putative docking factor at multiple steps of vesicular transport to the vacuole of Saccharomyces cerevisiae. Genetics 156, 105-122.
62. Sunio, A., Metcalf, A.B., and Kramer, H. (1999). Genetic dissection of endocytic trafficking in Drosophila using a horseradish peroxidase-bride of sevenless chimera: hook is required for normal maturation of multivesicular endosomes. Mol. Biol. Cell 10, 847-859.
63. Tellam, J.T., James, D.E., Stevens, T.H., and Piper, R.C. (1997). Identification of mammalian Golgi Sec1p-like protein mVps45. J. Biol. Chem. 272, 6187-6193.
64. Wade, N., Bryant, N.J., Connolly, L.M., Simpson, R.J., Luzio, J.P., Piper, R.C., and James, D.E. (2001). Syn 7 complexes with mouse Vps10 tail interactor 1b, Syn 6, vesicle associated membrane protein (Vamp) 8 and Vamp7 in B16 melanoma cells. J. Biol. Chem. 276, 19820-19827.
65. Walenta, J.H., Didier, A.J., Liu, X., and Kraymer, H. (2001). The Golgi-associated Hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152, 923-934.
66. Wang, L., Merz, A.J., Collins, K.M., and Wickner, W. (2003). Hierarchy of proteins assembly at the vertex ring domain for yeast vacuole docking and fusion. Mol. Biol. Cell 160, 365-374.
67. Waters, G.M., and Hughson, F.M. (2000). Membrane tethering and fusion in the secretory and endocytic pathways. Traffic 1, 588-597.
68. Waters, G.M., and Pfeffer, S.R. (1999). Membrane tethering in intracellular transport. Curr. Opin. Cell Biol. 11, 453-459.
69. Wattenberg, B.W., and Rothman, I.E. (1986). Multiple cytosolic components promote intra-Golgi protein transport: resolution of a protein acting at a late stage, prior to membrane fusion. J. Biol. Chem. 261, 2208-2213.
70. Wendler, F., and Tooze, S. (2001). Syn 6, The promiscuous behavior of a SNARE protein. Traffic 2, 606-611.
71. Whyte, J.R.C., and Munro, S. (2002). Vesicle tethering complexes in membrane traffic. J. Cell Sci. 115, 2627-2637.
72. Wickner, W., and Haas, A. (2000). Yeast homotypic vacuole fusion: a window in organelle trafficking mechanisms, Annu. Rev. Biochem. 69, 247-275.
73. Woolford, C.A., Bounoutas, G.S., Frew, S.E., and Jones, E.W. (1998). Genetic interaction with vps8-200 allows partial suppression of the vestigial vacuole phenotype caused by a PEP5 mutation in Saccharomyces cerevisiae. Genetics 148, 71-83.
74. Wurmser, A.E., Sato, T.K., and Emr, S.D. (2000). New component of the vacuolar class c-VPS complex couples nucleotide exchange on the Ypt7 GT-Pase to SNARE-dependent docking and fusion. J. Cell Biol. 151, 551-562.
75. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-119.