The J-domain protein Rme-8 interacts with Hsc70 to control clathrin-dependent endocytosis in Drosophila

Journal of Cell Biology

Volumn 164, Issue 7, 2004, Pages 1055-1064

  Chang, Henry C ^a   Hull, Michael ^a   Mellman, Ira ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Clathrin; Endocytosis; Hsc70; J domain; Rme 8

Indexed keywords

AUXILIN; BRIDE OF SEVENLESS PROTEIN; CHAPERONE; CLATHRIN; COCHAPERONE; DYNAMIN; HEAT SHOCK COGNATE PROTEIN 70; J DOMAIN PROTEIN; MUTANT PROTEIN; PROTEIN; RME 8 PROTEIN; TRACER; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; DROSOPHILA; ENDOCYTOSIS; GENE; HSC70 4 GENE; INTERNALIZATION; LARVA; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RME 8 GENE;

ANIMALS; BASE SEQUENCE; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CLATHRIN; CLONING, MOLECULAR; CROSSES, GENETIC; DNA PRIMERS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; HSC70 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MUTAGENESIS; POLYMERASE CHAIN REACTION; RETINA; TRANSCRIPTION, GENETIC;

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; HEXAPODA;

EID: 1842561557     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200311084     Document Type: Article

References (49)

1. Brand, A.H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:401-415.
2. Bukau, B., and A.L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cell. 92:351-366.
3. Cagan, R.L., H. Kramer, A.C. Hart, and S.L. Zipursky. 1992. The bride of sevenless and sevenless interaction: internalization of a transmembrane ligand. Cell. 69:393-399.
4. Campbell, R.E., O. Tour, A.E. Palmer, P.A. Steinbach, G.S. Baird, D.A. Zacharias, and R.Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:7877-7882.
5. Chang, H.C., S.L. Newmyer, M.J. Hull, M. Ebersold, S.L. Schmid, and I. Mellman. 2002. Hsc70 is required for endocytosis and clathrin function in Drosophila. J. Cell Biol. 159:477-487.
6. Chappell, T.G., W.J. Welch, D.M. Schlossman, K.B. Palter, M.J. Schlesinger, and J.E. Rothman. 1986. Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell. 45:3-13.
7. Chen, B., T. Chu, E. Harms, J.P. Gergen, and S. Strickland. 1998. Mapping of Drosophila mutations using site-specific male recombination. Genetics. 149: 157-163.
8. Damke, H., D.D. Binns, H. Ueda, S.L. Schmid, and T. Baba. 2001. Dynamin GTPase domain mutants block endocytic vesicle formation at morphologically distinct stages. Mol. Biol. Cell. 12:2578-2589.
9. Dockendorff, T.C., S.E. Robertson, D.L. Faulkner, and T.A. Jongens. 2000. Genetic characterization of the 44D-45B region of the Drosophila melanogaster genome based on an F2 lethal screen. Mol. Gen. Genet. 263:137-143.
10. Elefant, F., and K.B. Palter. 1999. Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality. Mol. Biol. Cell. 10:2101-2117.
11. Entchev, E.V., A. Schwabedissen, and M. González-Gaitán. 2000. Gradient formation of the TGF-β homolog Dpp. Cell. 103:981-991.
12. Gall, W.E., M.A. Higginbotham, C. Chen, M.F. Ingram, D.M. Cyr, and T.R. Graham. 2000. The auxilin-like phosphoprotein Swa2p is required for clathrin function in yeast. Curr. Biol. 10:1349-1358.
13. Ghosh, P., and S. Kornfeld. 2003. AP-1 binding to sorting signals and release from clathrin-coated vesicles is regulated by phosphorylation. J. Cell Biol. 160: 699-708.
14. González-Gaitán, M., and H. Jackie. 1997. Role of Drosophila α-adaptin in presynaptic vesicle recycling. Cell. 88:767-776.
15. Gteener, T., B. Grant, Y. Zhang, X. Wu, L.E. Greene, D. Hirsh, and E. Eisenberg. 2001. Caenorhabditis elegans auxilin: a J-domain protein essential for clathrin-mediated endocytosis in vivo. Nat. Cell Biol. 3:215-219.
16. Hannan, L.A., S.L. Newmyer, and S.L. Schmid. 1998. ATP- and cytosol-dependent release of adaptor proteins from clathrin-coated vesicles: A dual role for Hsc70. Mol. Biol. Cell. 9:2217-2229.
17. Hay, B.A., T. Wolff, and G.M. Rubin. 1994. Expression of baculovirus P35 prevents cell death in Drosophila. Development. 120:2121-2129.
18. Holstein, S.E., H. Ungewickell, and E. Ungewickell. 1996. Mechanism of clathrin basket dissociation: separate functions of protein domains of the DnaJ homologue auxilin. J. Cell Biol. 135:925-937.
19. Honing, S., G. Kreimer, H. Robenek, and B.M. Jockusch. 1994. Receptor-mediated endocytosis is sensitive to antibodies against the uncoating ATPase (hsc70). J. Cell Sci. 107:1185-1196.
20. Jiang, R., B. Gao, K. Prasad, L.E. Greene, and E. Eisenberg. 2000. Hsc70 chaperones clathrin and primes it to interact with vesicle membranes. J. Biol. Chem. 275:8439-8447.
21. Kelley, W.L. 1999. Molecular chaperones: How J domains turn on Hsp70s. Curr. Biol. 9:R305-R308.
22. Kirchhausen, T. 2000. Three ways to make a vesicle. Nat. Rev. Mol. Cell Biol. 1:187-198.
23. ts1. J. Cell Biol. 97:499-507.
24. Kramer, H., and M. Phistry. 1996. Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies. J. Cell Biol. 133:1205-1215.
25. Lloyd, T.E., R. Atkinson, M.N. Wu, Y. Zhou, G. Pennetta, and H.J. Bellen. 2002. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila. Cell. 108:261-269.
26. Morgan, J.R., K. Prasad, W. Hao, G.J. Augustine, and E.M. Lafer. 2000. A conserved clathrin assembly motif essential for synaptic vesicle endocytosis. J. Neurosci. 20:8667-8676.
27. Morgan, J.R., K. Prasad, S. Jin, G.J. Augustine, and E.M. Lafer. 2001. Uncoating of clathrin-coated vesicles in presynaptic terminals: roles for Hsc70 and auxilin. Neuron. 32:289-300.
28. Narayanan, R., and M. Ramaswami. 2003. Regulation of dynamin by nucleoside diphosphate kinase. J. Bioenerg. Biomembr. 35:49-55.
29. Newmyer, S.L., A. Christensen, and S. Sever. 2003. Auxilin-dynamin interactions link the uncoating ATPase chaperone machinery with vesicle formation, Dev. Cell. 4:929-940.
30. Newmyer, S.L., and S.L. Schmid. 2001. Dominant-interfering Hsc70 mutants disrupt multiple stages of the clathrin-coated vesicle cycle in vivo. J. Cell Biol. 152:607-620.
31. Pishvaee, B., G. Costaguta, B.G. Yeung, S. Ryazantsev, T. Greener, L.E. Greene, E. Eisenberg, J.M. McCaffery, and G.S. Payne. 2000. A yeast DNA J protein required for uncoating of clathrin-coated vesicles in vivo. Nat. Cell Biol. 2:958-963.
32. Poodry, C.A., and L. Edgar. 1979. Reversible alteration in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire. J. Cell Biol. 81:520-527.
33. Poodry, C.A., L. Hall, and D.T. Suzuki. 1973. Developmental properties of Shibire: a pleiotropic mutation affecting larval and adult locomotion and development. Dev. Biol. 32:373-386.
34. Robinow, S., and K. White. 1988. The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev. Biol. 126:294-303.
35. Rubin, G.M., and A.C. Spradling. 1982. Genetic transformation of Drosophila with transposable element vectors. Science. 218:348-353.
36. Rubin, G.M., L. Hong, P. Brokstein, M. Evans-Holm, E. Frise, M. Stapleton, and D.A. Harvey. 2000. A Drosophila complementary DNA resource. Science. 287:2222-2224.
37. Schlossman, D.M., S.L. Schmid, W.A. Braell, and J.E. Rothman. 1984. An enzyme that removes clathrin coats: purification of an uncoating ATPase. J. Cell Biol. 99:723-733.
38. Schmid, S.L. 1997. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66:511-548.
39. Spradling, A.C., D.M. Stern, I. Kiss, J. Roote, T. Laverty, and G.M. Rubin. 1995. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA. 92:10824-10830.
40. Spradling, A.C., D. Stern, A. Beaton, E.J. Rhem, T. Laverty, N. Mozden, S. Misra, and G.M. Rubin. 1999. The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 153:135-177.
41. Sunio, A., A.B. Metcalf, and H. Kramer. 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.
42. Tomancak, P., A. Beaton, R. Weiszmann, E. Kwan, S. Shu, S.E. Lewis, S. Richards, M. Ashburner, V. Hartenstein, S.E. Celniker, and G.M. Rubin. 2002., Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol. 3:research0088.1-0088.14.
43. Umeda, A., A. Meyerholz, and E. Ungewickell. 2000. Identification of the universal cofactor (auxilin 2) in clathrin coat dissociation. Eur. J. Cell Biol. 79:336-342.
44. Ungewickell, E., H. Ungewickell, S.E. Holstein, R. Lindner, K. Prasad, W. Barouch, B. Martin, L.E. Greene, and E. Eisenberg. 1995. Role of auxilin in uncoating clathrin-coated vesicles. Nature. 378:632-635.
45. van der Bliek, A.M., and E.M. Meyerowitz. 1991. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature. 351: 411-414.
46. Wolff, T. 2000. Histological techniques for the Drosophila eye. Parts I and II. In Drosophila Protocols. W. Sullivan, M. Ashburner, and R.S. Hawley, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 201-244.
47. Wucherpfennig, T., M. Wilsch-Brauninger, and M. Gonzá lez-Gaitán. 2003. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161:609-624.
48. Xu, T., and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 117:1223-1237.
49. Zhang, Y., B. Grant, and D. Hirsh. 2001. RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol. Biol. Cell. 12: 2011-2021.