Genetic dissection of endocytic trafficking in drosophila using a horseradish peroxidase-Bride of Sevenless chimera: hook is required for normal maturation of multivesicular endosomes

Molecular Biology of the Cell

Volumn 10, Issue 4, 1999, Pages 847-859

  Sunio, Arisa ^b   Metcalf, Anne B ^a,b   Krämer, Helmut ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; HORSERADISH PEROXIDASE; LIGAND;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DROSOPHILA; ENDOCYTOSIS; ENDOSOME; GENE MUTATION; GENETIC ANALYSIS; IMAGINAL DISC; INTERNALIZATION; INTRACELLULAR TRANSPORT; LYSOSOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REGULATORY MECHANISM;

ANIMALIA; ARMORACIA RUSTICANA;

EID: 0032961825     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.4.847     Document Type: Article

References (54)

1. 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: John Wiley & Sons.
2. Bailey, C.H., Chen, M., Keller, F., and Kandel, E.R. (1992). Serotonin-mediated endocytosis of apCAM: an early step of learning-related synaptic growth in Aplysia. Science 256, 645-649.
3. Cagan, R.L., Krämer, H., Hart, A.C., and Zipursky, S.L. (1992). The bride of sevenless and sevenless interaction: internalization of a trans-membrane ligand. Cell 69, 393-399.
4. Chen, C.S., Bach, G., and Pagano, R.E. (1998). Abnormal transport along the lysosomal pathway in mucolipidosis, type IV disease. Proc. Natl. Acad. Sci. USA 95, 6373-6378.
5. Chen, M.S., Obar, R.A., Schroeder, C.C., Austin, T.W., Poodry, C.A., Wadsworth, S.C., and Vallee, R.B. (1991). Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583-586.
6. Connolly, C.N., Futter, C.E., Gibson, A., Hopkins, C.R., and Cutler, D.F. (1994). Transport into and out of the Golgi complex studied by transfecting cells with cDNAs encoding horseradish peroxidase. J. Cell Biol. 127, 641-652.
7. Couso, J.P., Knust, E., and Arias, A.M. (1995). Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol. 5, 1437-1448.
8. Damke, H., Baba, T., van der Bliek, A.M., and Schmid, S.L. (1995). Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J. Cell Biol 131, 69-80.
9. Damke, H., Baba, T., Warnock, D.E., and Schmid, S.L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
10. Dunn, K.W., and Maxfield, F.R. (1992). Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes. J. Cell Biol. 117, 301-310.
11. Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J., and Hopkins, C.R. (1990). Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell 61, 623-634.
12. Futter, C.E., Pearse, A., Hewlett, L.J., and Hopkins, C.R. (1996). Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132, 1011-1123.
13. Ghosh, R.N., Gelman, D.L., and Maxfield, F.R. (1994). Quantification of low density lipoprotein and transferrin endocytic sorting HEp2 cells using confocal microscopy. J. Cell Sci. 107, 2177-2189.
14. Gruenberg, J., and Maxfield, F.R. (1995). Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
15. Hart, A.C., Harrison, S.D., Van Vactor, D.L.J., Rubin, G.M., and Zipursky, S.L. (1993a). The interaction of bride of sevenless with sevenless is conserved between Drosophila virilis and Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 90, 5047-5051.
16. Hart, A.C., Krämer, H., Van Vactor, D.L.J., Paidhungat, M., and Zipursky, S.L. (1990). Induction of cell fate in the Drosophila retina: the bride of sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments. Genes & Dev. 4, 1835-1847.
17. Hart, A.C., Krämer, H., and Zipursky, S.L. (1993b). Extracellular domain of the boss transmembrane ligand acts as an antagonist of the sev receptor. Nature 362, 732-736.
18. Hartmann, C., and Ortiz de Montellano, P.R. (1992). Baculovirus expression and characterization of catalytically active horseradish peroxidase. Arch. Biochem. Biophys. 297, 61-72.
19. Henderson, S.T., Gao, D., Lambie, E.J., and Kimble, J. (1994). lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. elegans. Development 120, 2913-2924.
20. Hirst, J., Futter, C.E., and Hopkins, C.R. (1998). The kinetics of mannose 6-phosphate receptor trafficking in the endocytic pathway in HEp-2 cells: the receptor enters and rapidly leaves multivesicular endosomes without accumulating in a prelysosomal compartment. Mol. Biol. Cell 9, 809-816.
21. Horazdovsky, B.F., Busch, G.R., and Emr, S.D. (1994). VPS21 encodes a rab5-like GTP binding protein that is required for the sorting of yeast vacuolar proteins. EMBO J. 13, 1297-1309.
22. Klueg, K.M., Parody, T.R., and Muskavitch, M.A.T. (1998). Complex proteolytic processing acts on δ, a transmembrane ligand for Notch, during Drosophila development. Mol. Biol. Cell 9, 1709-1723.
23. Kosaka, T., and Ikeda, K. (1983a). Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila. J. Neurobiol. 14, 207-225.
24. ts1. J. Cell Biol. 97, 499-507.
25. 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.
26. 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, 1205-1216.
27. Krämer, H., and Phistry, M. (1999). Genetic analysis of hook, a gene required for endocytic trafficking in Drosophila. Genetics 151, 675-684.
28. Lindsley, D.L., and Zimm, G.G. (1992). The Genome of Drosophila melanogaster, San Diego: Academic Press.
29. Lloyd, V., Ramaswami, M., and Krämer, H. (1998). Not just pretty eyes: Drosophila eye-color mutations and lysosomal delivery. Trends Cell Biol. 8, 257-259.
30. Mayor, S., Presley, J.F., and Maxfield, F.R. (1993). Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol. 121, 1257-1269.
31. Mukherjee, S., Ghosh, R.N., and Maxfield, F.R. (1997). Endocytosis. Physiol. Rev. 77, 759-803.
32. Mullock, B.M., Bright, N.A., Fearon, C.W., Gray, S.R., and Luzio, J.P. (1998). Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. J. Cell Biol. 240, 591-601.
33. Odorizzi, G., Cowles, C.R., and Emr, S.D. (1998). The AP-3 complex: a coat of many colors. Trends Cell Biol. 8, 282-288.
34. Press, B., Feng, Y., Hoflack, B., and Wandinger-Ness, A. (1998). Mutant Rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J. Cell Biol. 140, 1075-1089.
35. Ramaswami, M., Rao, S., van der Bliek, A., Kelly, R.B., and Krishnan, K.S. (1993). Genetic studies on dynamin function in Drosophila. J. Neurogenet. 9, 73-87.
36. Riezman, H. (1993). Yeast endocytosis. Trends Cell Biol. 3, 273-277.
37. Rubin, G.M., and Spradling, A.C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
38. Sato, T.K., Darsow, T., and Emr, S.D. (1998). Vam7p, a SNAP-25-like molecule, and vam3p, a syntaxin homolog, function together in yeast vacuolar protein trafficking. Mol. Cell. Biol. 28, 5308-5319.
39. Seugnet, L., Simpson, P., and Haenlin, M. (1997). Requirement for dynamin during Notch signaling in Drosophila neurogenesis. Dev. Biol. 192, 585-598.
40. Sevrioukov, E., Walenta, J.H., Phistry, M., Sunio, A., and Krämer, H. (1998). Oligomerization of the extracellular domain of Boss enhances its binding to the Sevenless receptor and its antagonistic effect on R7 induction. J. Cell Sci. 111, 737-747.
41. Stack, J.H., Horazdovsky, B., and Emr, S.D. (1995). Receptor-mediated protein sorting to the vacuole in yeast: roles for a protein kinase, a lipid kinase and GTP-binding proteins. Annu. Rev. Cell Dev. Biol. 11, 1-33.
42. Stinchcombe, J.C., Nomoto, H., Cutler, D.F., and Hopkins, C.R. (1995). Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex. J. Cell Biol. 733, 1387-1401.
43. Stoorvogel, W., Strous, G.J., Geuze, H.J., Oorschot, V., and Schwartz, A.L. (1991). Late endosomes derive from early endosomes by maturation. Cell 65, 417-427.
44. Sweitzer, S.M., and Hinshaw, J.E. (1998). Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93, 1021-1029.
45. Takei, K., Haucke, V., Slepnev, V., Farsad, K., Salazar, M., Chen, H., and De Camilli, P. (1998). Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94, 131-141.
46. Thummel, C.S., and Pirrotta, V. (1992). New pCaSpeR P element vectors. Dros. Info. Service 71, 150.
47. Tomlinson, A., Bowtell, D.D., Hafen, E., and Rubin, G.M. (1987). Localization of the sevenless protein, a putative receptor for positional information, in the eye imaginai disk of Drosophila. Cell 51, 143-150.
48. Tsuruhara, T., Koenig, J.H., and Ikeda, K. (1990). Synchronized endocytosis studied in the oocyte of a temperature-sensitive mutant of Drosophila melanogaster. Cell Tissue Res. 259, 199-207.
49. van der Bliek, A.M., and Meyerowitz, E.M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414.
50. van Deurs, B., Holm, P.K., Kayser, L., and Sandvig, K. (1995). Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. Eur. J. Cell Biol. 66, 309-323.
51. van Deurs, B., Holm, P.K., Kayser, L., Sandvig, K., and Hansen, S.H. (1993). Multivesicular bodies in HEp-2 cells are maturing endosomes. Eur. J. Cell Biol. 61, 208-224.
52. Van Vactor, D.L.J., 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.
53. Wendland, B., Emr, S.D., and Riezman, H. (1998). Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol. 10, 513-522.
54. Wolff, T., and Ready, D.F. (1993). Pattern formation in the Drosophila retina. In: The Development of Drosophila melanogaster, ed. M. Bate and A. Martinez-Arias, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1277-1325.