Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules

Journal of Cell Science

Volumn 118, Issue 16, 2005, Pages 3663-3673

  Pulipparacharuvil, Suprabha ^a   Akbar, Mohammed Ali ^a   Ray, Sanchali ^a   Sevrioukov, Evgueny A ^a   Haberman, Adam S ^a   Rohrer, Jack ^b   Krämer, Helmut ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Autophagosomes; Endocytic trafficking; Lysosome related organelles; Pigment granules; Vps C genes

Indexed keywords

CELL PROTEIN; LIGAND; PIGMENT; PROTEIN C; PROTEIN SUBUNIT; PROTEIN VPS16A; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL GRANULE; CELL TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; EXPERIMENTATION; EYE; GENE MUTATION; GENETIC CODE; LETHALITY; LYSOSOME; METAZOON; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SEQUENCE HOMOLOGY;

ANIMALS; CELLS, CULTURED; CYTOPLASMIC GRANULES; DNA-BINDING PROTEINS; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOSOMES; EYE; EYE ABNORMALITIES; EYE PROTEINS; LYSOSOMES; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; PIGMENTS, BIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEINS; RNA INTERFERENCE; VESICULAR TRANSPORT PROTEINS;

ANIMALIA; DIANTHUS CARYOPHYLLUS; METAZOA;

EID: 24944583279     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02502     Document Type: Article

References (78)

1. Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F. et al. (2000). The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Struhl, K. (1994). Current Protocols in Molecular Biology. New York, NY, USA: John Wiley & Sons.
3. Baehrecke, E. H. (2003). Autophagic programmed cell death in Drosophila. Cell Death Differ. 10, 940-945.
4. Banta, L. M., Vida, T. A., Herman, P. K. and Emr, S. D. (1990). Characterization of yeast Vps33p, a protein required for vacuolar protein sorting and vacuole biogenesis. Mol. Cell. Biol. 10, 4638-4649.
5. Beadle, G. and Ephrussi, B. (1936). The differentiation of eye pigments in Drosophila as studied by transplantation. Genetics 21, 225-247.
6. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
7. Bunch, T. A., Grinblat, Y. and Goldstein, L. S. (1988). Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells. Nucleic Acids Res. 16, 1043-1061.
8. Cagan, R. L. and Ready, D. F. (1989). The emergence of order in the Drosophila pupal retina. Dev. Biol. 136, 346-362.
9. Caplan, S., Hartnell, L. M., Aguilar, R. C., Naslavsky, N. and Bonifacino, J. S. (2001). Human Vam6p promotes lysosome clustering and fusion in vivo. J. Cell Biol. 154, 109-122.
10. Carr, C. M., Grote, E., Munson, M., Hughson, F. M. and Novick, P. J. (1999). Sec1p binds to SNARE complexes and concentrates at sites of secretion. J. Cell Biol. 146, 333-344.
11. Casso, D., Ramirez-Weber, F. and Kornberg, T. B. (2000). GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech. Dev. 91, 451-454.
12. Chang, H. C., Newmyer, S. L., Hull, M. J., Ebersold, M., Schmid, S. L. and Mellman, I. (2002). Hsc70 is required for endocytosis and clathrin function in Drosophila. J. Cell Biol. 159, 477-487.
13. Ciciotte, S. L., Gwynn, B., Moriyama, K., Huizing, M., Gahl, W. A., Bonifacino, J. S. and Peters, L. L. (2003). Cappuccino, a mouse model of Hermansky-Pudlak syndrome, encodes a novel protein that is part of the pallidin-muted complex (BLOC-1). Blood 101, 4402-4407.
14. Dell'Angelica, E. C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A. and Bonifacino, J. S. (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21.
15. Dulubova, I., Sugita, S., Hill, S., Hosaka, M., Fernandez, I., Sudhof, T. C. and Rizo, J. (1999). A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18, 4372-4382.
16. Dulabova, I., Yamaguchi, T., Wang, Y., Sudhof, T. C. and Rizo, J. (2001). Vam3p structure reveals conserved and divergent properties of syntaxins. Nat. Struct. Biol. 8, 258-264.
17. Eastham, K. M., McKiernan, P. J., Milford, D. V., Ramani, P., Wyllie, J., van't Hoff, W., Lynch, S. A. and Morris, A. A. (2001). ARC syndrome: an expanding range of phenotypes. Arch. Dis. Child. 85, 415-420.
18. Gahl, W. A., Brantly, M., Kaiser-Kupfer, M. I., Iwata, F., Hazelwood, S., Shotelersuk, V., Duffy, L. F., Kuehl, E. M., Troendle, J. and Bernardini, I. (1998). Genetic defects and clinical characteristics of patients with a form of oculocutaneous albinism (Hermansky-Pudlak syndrome). New Engl. J. Med. 338, 1258-1264.
19. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E. et al. (2003). A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736.
20. Gissen, P., Johnson, C. A., Morgan, N. V., Stapelbroek, J. M., Forshew, T., Cooper, W. N., McKiernan, P. J., Klomp, L. W., Morris, A. A., Wraith, J. E. et al. (2004). Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat. Genet. 36, 400-404.
21. Gwynn, B., Martina, J. A., Bonifacino, J. S., Sviderskaya, E. V., Lamoreux, M. L., Bennett, D. C., Moriyama, K., Huizing, M., Helip-Wooley, A., Gahl, W. A. et al. (2004). Reduced pigmentation (rp), a mouse model of Hermansky-Pudlak syndrome, encodes a novel component of the BLOC-1 complex. Blood 104, 3181-3189.
22. Harlow, E. and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
23. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129.
24. Hazelett, D. J., Bourouis, M., Walldorf, U. and Treisman, J. E. (1998). decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125, 3741-3751.
25. Horazdovsky, B. F. and Emr, S. D. (1993). The VPS16 gene product associates with a sedimentable protein complex and is essential for vacuolar protein sorting in yeast. J. Biol. Chem. 268, 4953-4962.
26. Huizing, M. and Gahl, W. A. (2002). Disorders of vesicles of lysosomal lineage: the Hermansky-Pudlak syndromes. Curr Mol. Med. 2, 451-467.
27. Huizing, M., Didier, A., Walenta, J., Anikster, Y., Gahl, W. A. and Krämer, H. (2001). Molecular cloning and characterization of human VPS18, VPS 11, VPS16, and VPS33. Gene 264, 241-247.
28. Jahn, R., Lang, T. and Sudhof, T. C. (2003). Membrane fusion. Cell 112, 519-533.
29. Kim, B. Y., Krämer, H., Yamamoto, A., Kominami, E., Kohsaka, S. and Akazawa, C. (2001). Molecular characterization of mammalian homologues of class C Vps proteins that interact with syntaxin-7. J. Biol. Chem. 276, 29393-29402.
30. Klionsky, D. J. (2005). The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 118, 7-18.
31. Krämer, H. and Phistry, M. (1996). Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies. J. Cell Biol. 133, 1205-1215.
32. Krämer, H., Cagan, R. L. and Zipursky, S. L. (1991). Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature 352, 207-212.
33. Lee, E. C., Hu, X., Yu, S. Y. and Baker, N. E. (1996). The scabrous gene encodes a secreted glycoprotein dimer and regulates proneural development in Drosophila eyes. Mol. Cell. Biol. 16, 1179-1188.
34. Lee, Y. S. and Carthew, R. W. (2003). Making a better RNAi vector for Drosophila: use of intron spacers. Methods 30, 322-329.
35. Li, W., Zhang, Q., Oiso, N., Novak, E. K., Gautam, R., O'Brien, E. P., Tinsley, C. L., Blake, D. J., Spritz, R. A., Copeland, N. G. et al. (2003a). Hermansky-Pudlak syndrome type 7 (HPS-7) results from mutant dysbindin, a member of the biogenesis of lysosome-related organelles complex 1 (BLOC-1). Nat. Genet. 35, 84-89.
36. Li, W., Rusiniak, M. E., Chintala, S., Gautam, R., Novak, E. K. and Swank, R. T. (2004). Murine Hermansky-Pudlak syndrome genes: regulators of lysosome-related organelles. BioEssays 26, 616-628.
37. Li, Y., Fetchko, M., Lai, Z. C. and Baker, N. E. (2003b). Scabrous and Gp150 are endosomal proteins that regulate Notch activity. Development 130, 2819-2827.
38. Marchler-Bauer, A., Anderson, J. B., Cherukuri, P. F., DeWeese-Scott, C., Geer, L. Y., Gwadz, M., He, S., Hurwitz, D. I., Jackson, J. D., Ke, Z. et al. (2005). CDD: a conserved domain database for protein classification. Nucleic Acids Res. 30, D192-D196.
39. Martina, J. A., Moriyama, K. and Bonifacino, J. S. (2003). BLOC-3, a protein complex containing the Hermansky-Pudlak syndrome gene products HPS1 and HPS4. J. Biol. Chem. 278, 29376-29384.
40. Misura, K. M., Scheller, R. H. and Weis, W. I. (2000). Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 404, 355-362.
41. Nazarian, R., Falcon-Perez, J. M. and Dell'Angelica, E. C. (2003). Biogenesis of lysosome-related organelles complex 3 (BLOC-3): a complex containing the Hermansky-Pudlak syndrome (HPS) proteins HPS1 and HPS4. Proc. Natl. Acad. Sci. USA 100, 8770-8775.
42. Nelson, W. J. and Rodriguez-Boulan, E. (2004). Unravelling protein sorting. Nat. Cell Biol. 6, 282-284.
43. Nguyen, T. and Wei, M. L. (2004). Characterization of melanosomes in murine Hermansky-Pudlak syndrome: mechanisms of hypopigmentation. J. Invest. Dermatol. 122, 452-460.
44. Nguyen, T., Novak, E. K., Kermani, M., Fluhr, J., Peters, L. L., Swank, R. T. and Wei, M. L. (2002). Melanosome morphologies in murine models of hermansky-pudlak syndrome reflect blocks in organelle development. J. Invest. Dermatol. 119, 1156-1164.
45. Nickla, H. (1977). Maternal effects determine effective lethal phase of carnation-light synthetic lethal in Drosophila melanogaster. Nature 268, 638-639.
46. 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.
47. Poupon, V., Stewart, A., Gray, S. R., Piper, R. C. and Luzio, J. P. (2003). The role of HmVps18p in clustering, fusion, and intracellular localization of late endocytic organelles. Mol. Biol. Cell 14, 4015-4027.
48. Price, A., Seals, D., Wickner, W. and Ungermann, C. P. (2000). The docking stage 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.
49. Raymond, C. K., Howald-Stevenson, I., Vater, C. A. and Stevens, T. H. (1992). Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E VPS mutants. Mol. Biol. Cell 3, 1389-1402.
50. Richardson, S. C., Winistorfer, S. C., Poupon, V., Luzio, J. P. and Piper, R. C. (2004). Mammalian late vacuole protein sorting orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol. Biol. Cell 15, 1197-1210.
51. 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.
52. Robinson, J. S., Klionsky, D. J., Banta, L. M. and Emr, S. D. (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.
53. Rohrer, J., Schweizer, A., Russell, D. and Kornfeld, S. (1996). The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J. Cell Biol. 132, 565-576.
54. Rojo, E., Gillmor, C. S., Kovaleva, V., Somerville, C. R. and Raikhel, N. V. (2001). VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1, 303-310.
55. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
56. Rubin, G. M., Hong, L., Brokstein, P., Evans-Holm, M., Frise, E., Stapleton, M. and Harvey, D. A. (2000). A Drosophila complementary DNA resource. Science 287, 2222-2224.
57. Rusten, T. E., Lindmo, K., Juhasz, G., Sass, M., Seglen, P. O., Brech, A. and Stenmark, H. (2004). Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 7, 179-192.
58. 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.
59. Scott, R. C., Schuldiner, O. and Neufeld, T. P. (2004). Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7, 167-178.
60. Seals, D. F., Eitzen, G., Margolis, N., Wickner, W. T. and 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.
61. Sevrioukov, E. A., He, J. P., Moghrabi, N., Sunio, A. and Krämer, H. (1999). A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Mol. Cell 4, 479-486.
62. Shestopal, S. A., Makunin, I. V., Belyaeva, E. S., Ashburner, M. and Zhimulev, I. F. (1997). Molecular characterization of the deep orange (dor) gene of Drosophila melanogaster. Mol. Gen. Genet. 253, 642-648.
63. Spritz, R. A. and Oh, J. (1999). HPS gene mutations in Hermansky-Pudlak syndrome. Am. J. Hum. Genet. 64, 658.
64. Sriram, V., Krishnan, K. S. and Mayor, S. (2003). deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster. J. Cell Biol. 161, 593-607.
65. Srivastava, A., Woolford, C. A. 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.
66. Starcevic, M. and Dell'Angelica, E. C. (2004). Identification of snapin and three novel proteins (BLOS1, BLOS2 and BLOS3/reduced pigmentation) as subunits of biogenesis of lysosome-related organelles complex-1 (BLOC-1). J. Biol. Chem. 279, 28393-28401.
67. Stinchcombe, J., Bossi, G. and Griffiths, G. M. (2004). Linking albinism and immunity: the secrets of secretory lysosomes. Science 305, 55-59.
68. Subramanian, S., Woolford, C. A. and Jones, E. W. (2004). The Sec1/Munc18 protein, Vps33p, functions at the endosome and the vacuole of Saccharomyces cerevisiae. Mol. Biol. Cell 15, 2593-2605.
69. Sunio, A., Metcalf, A. B. and Krämer, 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.
70. Suzuki, T., Oiso, N., Gautam, R., Novak, E. K., Panthier, J. J., Suprabha, P. G., Vida, T., Swank, R. T. and Spritz, R. A. (2003). The mouse organellar biogenesis mutant buff results from a mutation in Vps33a, a homologue of yeast vps33 and Drosophila carnation. Proc. Natl. Acad. Sci. USA 100, 1146-1150.
71. Toonen, R. F. and Verhage, M. (2003). Vesicle trafficking: pleasure and pain from SM genes. Trends Cell Biol. 13, 177-186.
72. Van Vactor, D. L., Jr, Cagan, R. L., Krämer, H. and Zipursky, S. L. (1991). Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell. Cell 67, 1145-1155.
73. Walenta, J. H., Didier, A. J., Liu, X. and Krämer, H. (2001). The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152, 923-934.
74. Warner, T. S., Sinclair, D. A., Fitzpatrick, K. A., Singh, M., Devlin, R. H. and Honda, B. M. (1998). The light gene of Drosophila melanogaster encodes a homologue of VPS41, a yeast gene involved in cellular-protein trafficking. Genome 41, 236-243.
75. White, J. G. (1982). Membrane defects in inherited disorders of platelet function. Am. J. Pediatr Hematol. Oncol. 4, 83-94.
76. Wodarz, A., Hinz, U., Engelbert, M. and Knust, E. (1995). Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76.
77. Wu, M. N., Littleton, J. T., Bhat, M. A., Prokop, A. and Bellen, H. J. (1998). ROP, the Drosophila Sec1 homolog, interacts with syntaxin and regulates neurotransmitter release in a dosage-dependent manner. EMBO J. 17, 127-139.
78. 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 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151, 551-562.