Genetic analysis of lysosomal trafficking in Caenorhabditis elegans

Molecular Biology of the Cell

Volumn 16, Issue 7, 2005, Pages 3273-3288

  Hermann, Greg J ^a   Schroeder, Lena K ^a   Hieb, Caroline A ^a   Kershner, Aaron M ^a   Rabbitts, Beverley M ^a   Fonarev, Paul ^b   Grant, Barth D ^b   Priess, James R ^c,d,e  

^a LEWIS AND CLARK COLLEGE   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; PROTEIN AP 3; PROTEIN GLO 1; PROTEIN SUBUNIT; PROTEIN VPS 16; PROTEIN VPS 41; RAB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; CELL GRANULE; CELL ORGANELLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENETIC ANALYSIS; INTESTINE CELL; LYSOSOME; MAMMAL; MELANOSOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ACRIDINE ORANGE; ALLELES; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; BODY SIZE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; DROSOPHILA; EPISTASIS, GENETIC; GENES, HELMINTH; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; GTP PHOSPHOHYDROLASES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INTESTINES; LYSOSOMES; MELANOSOMES; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE; TRANSCRIPTION FACTORS;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 22044453367     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-01-0060     Document Type: Article

References (92)

1. Alto, N. M., Soderling, J., and Scott, J. D. (2002). Rab32 is an A-kinase anchoring protein and participates in mitochondrial dynamics. J. Cell Biol. 158, 659-668.
2. Babu, P. (1974). Biochemical genetics of Caenorhabditis elegans. Mol. Gen. Genet. 135, 39-44.
3. Bankaitis, V. A., Johnson, L. M., and Emr, S. D. (1986). Isolation of yeast mutants defective in protein targeting to the vacuole. Proc. Natl. Acad. Sci. USA 83, 9075-9079.
4. Banta, L. M., Robinson, J. S., Klionsky, D. J., and Emr, S. D. (1988). Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J. Cell Biol. 107, 1369-1383.
5. Blott, E. J., and Griffiths, G. M. (2002). Secretory lysosomes. Nat. Rev. Mol. Cell. Biol. 3, 122-131.
6. Boehm, M., and Bonifacino, J. S. (2001). Adaptins: the final recount. Mol. Biol. Cell 12, 2907-2920.
7. Boehm, M., and Bonifacino, J. S. (2002). Genetic analyses of adaptin function from yeast to mammals. Gene 286, 175-186.
8. Bonangelino, C. J., Chavez, E. M., and Bonifacino, J. S. (2002). Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2486-2501.
9. Bonifacino, J. S., and Traub, L. M. (2003). Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447.
10. Bourne, H. R., Sanders, D. A., and McCormick, F. (1991). The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127.
11. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
12. Bryant, N. J., and Stevens, T. H. (1998). Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol. Mol. Biol. Rev. 62, 230-247.
13. Burd, C. G., Babst, M., and Emr, S. D. (1998). Novel pathways, membrane coats and PI kinase regulation in yeast lysosomal trafficking. Semin. Cell Dev. Biol. 9, 527-533.
14. Chitwood, B. G., and Chitwood, M. B. (1974). Introduction to Nematology, Baltimore, MD: University Park Press.
15. Clokey, G. V., and Jacobson, L. A. (1986). The autofluorescent "lipofuscin granules" in the intestinal cells of Caenorhabditis elegans are secondary lysosomes. Mech. Ageing Dev. 35, 79-94.
16. Cohen-Solal, K. A., Sood, R., Marin, Y., Crespo-Carbone, S. M., Sinsimer, D., Martino, J. J., Robbins, C., Makalowska, I., Trent, J., and Chen, S. (2003). Identification and characterization of mouse Rab32 by mRNA and protein expression analysis. Biochem. Biophys. Acta 1651, 68-75.
17. Collins, R. N., and Brennwald, P. (2000). Rab. In: GTPases, ed. A. Hall, New York: Oxford University Press, 137-175.
18. Conibear, E., and Stevens, T. H. (1998). Multiple sorting pathways between late Golgi and the vacuole in yeast. Biochim. Biophys. Acta 1404, 211-230.
19. Dang, H., Li, Z., Skolnik, E. Y., and Fares, H. (2004). Disease-related myotubularins function in endocytic traffic in Caenorhabditis elegans. Mol. Biol. Cell 15, 189-196.
20. Dell'Angelica, E. C. (2004). The building BLOC(k)s of lysosomes and related organelles. Curr. Opin. Cell Biol. 16, 458-464.
21. Dell'Angelica, E. C., Aguilar, R. C., Wolins, N., Hazelwood, S., Gahl, W. A., and Bonifacino, J. S. (2000a). Molecular characterization of the protein encoded by the Hermansky-Pudlak syndrome type 1 gene. J. Biol. Chem. 275, 1300-1306.
22. Dell'Angelica, E. C., Mullins, C., Caplan, S., and Bonifacino, J. S. (2000b). Lysosome-related organelles. FASEB J. 14, 1265-1278.
23. 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 β3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21.
24. Fares, H., and Greenwald, I. (2001a). Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159, 133-145.
25. Fares, H., and Greenwald, I. (2001b). Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat. Genet. 28, 64-68.
26. Fujikawa, K., Satoh, A. K., Kawamura, S., and Ozaki, K. (2002). Molecular and functional characterization of a unique Rab protein, RABRP1, containing the WDIAGQE sequence in a GTPase motif. Zool. Sci. 19, 981-993.
27. Grant, B., and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
28. Grant, B., Zhang, Y., Paupard, M.-C, Lin, S. X., Hall, D., and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579.
29. Hersh, B. M., Hartwig, E., and Horvitz, H. R. (2002). The Caenorhabditis elegans mucolipin-like gene cup-5 is essential for viability and regulates lysosomes in multiple cell types. Proc. Natl. Acad. Sci. USA 99, 4355-4360.
30. Hobart, O. (2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728-730.
31. Jacobson, L. A., Jen-Jacobson, L., Hawdon, J. M., Owens, G. P., Bolanowski, M. A., Emmons, S. W., Shah, M. V., Pollock, R. A., and Conklin, D. S. (1988). Identification of a putative structural gene for cathepsin D in Caenorhabditis elegans. Genetics 119, 355-363.
32. Johnstone, I. L. (2000). Cuticle collagen genes: expression in C. elegans. Trends Genet. 16, 21-27.
33. Jones, E. W. (1977). Proteinase mutants of Saccharomyces cerevisiae. Genetics 85, 23-33.
34. King, S. M., and Reed, G. L. (2002). Development of platelet secretory granules. Semin. Cell Dev. Biol. 13, 293-302.
35. Kontani, K., Moskowitz, I.P.G., and Rothman, J. H. (2005). Repression of cell-cell fusion by components of the C. elegans vacuolar ATPase complex. Dev. Cell 8, 787-794.
36. Kornfeld, S., and Mellman, I. (1989). The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5, 483-525.
37. Kostich, M., Fire, A., and Fambrough, D. M. (2000). Identification and molecular-genetic characterization of a LAMP/CD68-like protein from Caenorhabditis elegans. J. Cell Sci. 113, 2595-2606.
38. Kramer, H., and Phistry, M. (1996). Mutations in the Drosophila hook gene inhibit endocytosis of the Boss transmembrane ligands into multivesicular bodies. J. Cell Biol. 133, 1205-1215.
39. Lamitina, S. T., Morrison, R., Moeckel, G. W., and Strange, S. (2004). Adaptation of the nematode Caenorhabditis elegans to extreme osmotic stress. Am. J. Physiol. 286, C785-C791.
40. Laufer, J. S., Bazzicalupo, P., and Wood, W. B. (1980). Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell 19, 569-577.
41. Le Borne, R., Alconada, A., Bauer, U., and Hoflack, B. (1998). The mammalian AP-3 adaptor-like complex mediates the intracellular transport of lysosomal membrane glycoproteins. J. Biol. Chem. 273, 29451-29461.
42. Lemmon, S. K., and Traub, L. M. (2000). Sorting in the endosomal system in yeast and animal cells. Curr. Opin. Cell Biol. 12, 457-466.
43. Leung, B., Hermann, G. J., and Priess, J. R. (1999). Organogenesis of the Caenorhabditis elegans intestine. Dev. Biol. 216, 114-134.
44. 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.
45. 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.
46. Loftus, S. K., Larson, D. M., Baxter, L. L., Antonellis, A., Chen, Y., Wu, X., Jiang, Y., Bittner, M., Hammer, J. A., and Pavan, W. J. (2002). Mutation of melanosome protein RAB38 in chocolate mice. Proc. Natl. Acad. Sci. USA 99, 4471-4476.
47. Malone, C. J., Misner, L., Le Bot, N., Tsai, M. C., Campbell, J. M., Ahringer, J., and White, J. G. (2003). The C. elegans Hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115, 825-836.
48. Marks, M. S., and Seabra, M. C. (2001). The melanosome: membrane dynamics in black and white. Nat. Rev. Mol. Cell. Biol. 2, 738-748.
49. McKim, K. S., and Rose, A. M. (1990). Chromosome I duplications in Caenorhabditis elegans. Genetics 124, 115-132.
50. Mullins, C., and Bonifacino, J. S. (2001). The molecular machinery for lysosome biogenesis. Bioessays 23, 333-343.
51. Nelson, F. K., and Riddle, D. L. (1984). Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J. Exp. Zool. 231, 45-56.
52. Nonet, M. L., Staunton, J. E., Kilgard, M. P., Fergestad, T., Hartweig, E., Horvitz, H. R., Jorgensen, E. M., and Meyer, B. J. (1997). Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17, 8061-8073.
53. Odorizzi, G., Cowles, C. R., and Emr, S. D. (1998). The AP-3 complex: a coat of many colours. Trends Cell Biol. 8, 282-288.
54. Oiso, N., Riddle, S. R., Serikawa, T., Kuramoto, T., and Spritz, R. A. (2004). The rat Ruby (R) locus is Rab38: identical mutations in Fawn-hooded and Tester-Moriyama rats derived from an ancestral Long Evans rat sub-strain. Mamm. Genome 15, 307-314.
55. Oka, T., and Futai, M. (2000). Requirement of V-ATPase for ovulation and embryogenesis in Caenorhabditis elegans. J. Biol. Chem. 275, 29556-29561.
56. +-ATPase. J. Biol. Chem. 276, 33079-33085.
57. Pereira-Leal, J. B., and Seabra, M. C. (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.
58. Pereira-Leal, J. B., and Seabra, M. C. (2001). Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313, 889-901.
59. 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.
60. Piper, R. C., and Luzio, J. P. (2004). CUPpling calcium to lysosomal biogenesis. Trends Cell Biol. 24, 471-473.
61. Poupon, V., Stewart, A., Gray, S. R., Piper, R. C., and Luzio, J. P. (2003). The role of mVps18p in clustering, fusion, and intracellular localization of late endocytic organelles. Mol. Biol. Cell 14, 4015-4027.
62. Priess, J. R., and Hirsh, D. I. (1986). Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev. Biol. 117, 156-173.
63. Priess, J. R., Schnabel, H., and Schnabel, R. (1987). The glp-1locus and cellular interactions in early C. elegans embryos. Cell 51, 601-611.
64. Pujol, N., Bonnerot, C., Ewbank, J. J., Kohara, Y., and Thierry-Mieg, D. (2001). The Caenorhabditis elegans unc-32gene encodes alternative forms of a vacuolar ATPase a subunit. J. Biol. Chem. 276, 11913-11921.
65. Raiborg, C., Rusten, T. E., and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15, 446-455.
66. Raposo, G., and Marks, M. S. (2002). The dark side of lysosome-related organelles: specialization of the endocytic pathway for melanosome biogenesis. Traffic 3, 237-248.
67. Richardson, S.C.W., 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.
68. 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.
69. Roggo, L., Bernard, V., Kovacs, A. L., Rose, A. M., Savoy, F., Zetka, M., Wymann, M. P., and Muller, F. (2002). Membrane transport in Caenorhabditis elegans: an essential role for VPS34 at the nuclear membrane. EMBO J. 21, 1673-1683.
70. Rothman, J. H., and Stevens, T. H. (1986). Protein sorting in yeast: mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the secretory pathway. Cell 47, 1041-1051.
71. Rous, B. A., Reaves, B. J., Ihrke, G., Briggs, J.A.G., Gray, S. R., Stephens, D. J., Banting, G., and Luzio, J. P. (2002). Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol. Biol. Cell 13, 1071-1082.
72. Sambade, M., and Kane, P. M. (2004). The yeast vacuolar proton-translocating ATPase contains a subunit homologous to the Manduca sexta and bovine e subunits that is essential for function. J. Biol. Chem. 279, 17361-17365.
73. Sannerud, R., Saraste, J., and Goud, B. (2003). Retrograde traffic in the biosynthetic-secretory route: pathways and machinery. Curr. Opin. Cell Biol. 15, 438-445.
74. Seabra, M. C. (1998). Membrane association and targeting of prenylated Ras-like GTPases. Cell Signal. 10, 167-172.
75. Segev, N. (2001). Ypt and Rab GTPases: insight into functions through novel interactions. Curr. Opin. Cell Biol. 13, 500-511.
76. Sevrioukov, E. A., He, J. P., Moghrabi, 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.
77. Siddiqui, S. S., and Babu, P. (1980). Kynurenine hydroxylase mutants of the nematode Caenorhabditis elegans. Mol. Gen. Genet. 179, 21-24.
78. Spritz, R. A. (1999). Multi-organellar disorders of pigmentation: intracellular traffic jams in mammals, flies and yeast. Trends Genet. 15, 337-340.
79. Sriram, V. S., 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.
80. Stinchcombe, J., Bossi, G., and Griffiths, G. M. (2004). Linking albinism and immunity: the secrets of secretory lysosomes. Science 305, 55-59.
81. Sulston, J. E., Schierenberg, E., White, J. G., and Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
82. 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.
83. Tappel, A. L. (1969). Lysosomal Enzymes and Other Components, Amsterdam: North-Holland Publishing Co.
84. Treusch, S., Knuth, S., Slaugenhaupt, S. A., Goldin, E., Grant, B. D., and Fares, H. (2004). Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc. Natl. Acad. Sci. USA 13, 4483-4488.
85. Tschopp, T. B., and Zucker, M. B. (1972). Hereditary defect in platelet function in rats. Blood 40, 217-226.
86. Valencia, A., Chardin, P., Wittinghofer, A., and Sander, C. (1991). The ras protein family: evolutionary tree and role of conserved amino acids. Biochemistry 30, 4637-4648.
87. Van der Keyl, H., Kim, H., Oke, C. V., and Edwards, M. K. (1994). Caenorhabditis elegans sqt-3 mutants have mutations in the col-1collagen gene. Dev. Dyn. 201, 86-94.
88. Walenta, J. H., Didier, A. J., and Kramer, H. (2001). The Golgi-associated Hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152, 923-934.
89. Winter, A. D., and Page, A. P. (2000). Prolyl 4-hydroxylase is an essential procollagen-modifying enzyme required for exoskeleton formation and the maintenance of body shape in the nematode Caenorhabditis elegans. Mol. Cell. Biol. 20, 4084-4093.
90. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2, 107-117.
91. Zhang, Y., Grant, B., and Hirsh, D. (2001). RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol. Biol. Cell 12, 2011-2021.
92. Zhu, J., Hill, R. J., Heid, P. J., Fukuyama, M., Sugimoto, A., Priess, J. R., and Rothman, J. H. (1997). end-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos. Genes Dev. 11, 2883-2896.