Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality

Molecular Biology of the Cell

Volumn 10, Issue 7, 1999, Pages 2101-2117

  Elefant, Felice ^a,b   Palter, Karen B ^a  

^a Temple University   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; HEAT SHOCK PROTEIN 70; MUTANT PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING SITE; CELL MATURATION; CONFORMATIONAL TRANSITION; CYTOTOXICITY; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HYDROLYSIS; LARVAL DEVELOPMENT; MESODERM; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INDUCTION; TISSUE SPECIFICITY;

ANIMALIA; DROSOPHILA; DROSOPHILA MELANOGASTER; HEXAPODA; MAMMALIA; MELANOGASTER;

EID: 0032837196     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.7.2101     Document Type: Article

References (58)

1. Blond-Elguindi, S., Fourie, A.M., Sambrook J.F., and Gething, M.J. (1993). Peptide-dependent stimulation of the ATPase activity of the molecular chaperone BiP is the result of conversion of oligomers to active monomers. J. Biol. Chem. 268, 12730-12735.
2. Brand, A.H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 18, 401-415.
3. Braun, A., Lemaitre, B., Lanot, R., Zachary, D., and Meister, M. (1997). Drosophila immunity: analysis of larval hemocytes by P-element-mediated enhancer trap. Genetics 347, 623-634.
4. Buchberger, A., Theyssen H., Schroder, H., McCarty, J.S., Virgallita, G., Milkereit, P., Reinstein, J., and Bukau, B. (1995). Nucleotideinduced conformational changes in the ATPase and substrate binding domains of the DnaK chaperone provide evidence for interdomain communication. J. Biol. Chem. 270, 16903-16910.
5. Buchberger, A., Valencia, A., Mcmacken, R., Sander, C., and Bukau, B. (1994). The chaperone function of DnaK requires the coupling of ATPase activity with substrate binding through residue E171. EMBO J. 13, 1687-1695.
6. Bukau, B., and Horwich, A.L. (1998). The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
7. Chappell, T.G., Welch, W.J., Schlossman, D.M., Palter, K.B., Schlesinger, M.J., and Rothman, J.E. (1986). Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45, 3-13.
8. Chirico, W.J., Water, M.G., and Blobel, G. (1988). 70 K heat shock related proteins stimulate protein translocation into microsomes. Nature 332, 805-810.
9. Craig, E.A., and Gross, C.A. (1991). Is hsp70 the cellular thermometer? Trends Biochem. Sci. 10, 135-140.
10. Craig, E.A., Kramer, J., and Kosic-Smithers, J. (1987). SSC1, a member of the 70-kDa heat shock protein multigene family of Saccharomyces cerevisiae, is essential for growth. Proc. Natl. Acad. Sci. USA 84, 4156-4160.
11. Deshaies, R.J., Kock, B.D., Werner-Washburne, M., Craig, E.A., and Schekman, R. (1988). A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature 332, 800-810.
12. Drysdale, R., Rushton, E., and Bate, M. (1993). Genes required for embryonic muscle development in Drosophila melanogaster. Roux's Arch. Dev. Biol. 202, 282-295.
13. Elguindie, S., Fourie, A.M., Sambrook, J.F., and Gething, M.J. (1993). Peptide-dependent stimulation of the ATPase activity of the molecular chaperone BiP is the result of conversion of oligomers to active monomers. J. Biol. Chem. 268, 12730-12735.
14. Flaherty, K.M., DeLuca-Flaherty, C., and McKay, D.B. (1990). Three-dimensional structure of the ATPase fragment of a 70K heat shock cognate protein. Nature 34, 623-628.
15. Flaherty, K.M., Wilbanks, S.M., DeLuca-Flaherty, C., and McKay, D.B. (1994). Structural basis of the 70-kilodalton heat shock cognate protein ATP hydrolytic activity. J. Biol. Chem. 269, 12899-12907.
16. Flynn, G.C., Chappell, T.G., and Rothman, S.E. (1989). Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 245, 385-390.
17. Fyrberg, E.A., Bernstein, S.I., and VijayRaghavan, K. (1994). Basic methods for Drosophila muscle biology. Methods Cell Biol. 44, 237-256.
18. Gao, B., Greene, L., and Eisenberg, E. (1994). Characterization of nucleotide-free uncoating ATPase and its binding to ATP, ADP, and ATP analogues. Biochemistry 33, 2048-2053.
19. Gething, M.J., and Sambrook, J. (1992). Protein folding in the cell. Nature 355, 33-34.
20. Ha, J., and McKay, D.B. (1995). Kinetics of nucleotide-induced changes in the tryptophan fluorescence of the molecular chaperone Hsc70 and its subfragments suggest the ATP-induced conformational change follows initial ATP binding. Biochemistry 34, 11635-11644.
21. Ha, J.H., Hellman, U., Johnson, E.R., Li, L, McKay, D.B., Sousa, M.C., Takeda, S., Wernstedt, C., and Wilbanks, S.M. (1997). Destabilization of peptide binding and interdomain communication by an E543K mutation in the bovine 70-kDa heat shock cognate protein, a molecular chaperone. J. Biol. Chem. 272, 27796-277803.
22. Hartl, F.U. (1996), Molecular chaperones in cellular protein folding. Nature 381, 571-579.
23. Hendershot, L.M., Wei, J., Gaut, J.R., Lawson, B., Freiden, P.J., and Murti, K.G. (1995). In vivo expression of mammalian BiP ATPase mutants causes disruption of the endoplasmic reticulum. Mol. Biol. Cell 6, 283-296.
24. Hendrick, J.P., and Hartl, F.U. (1993). Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62, 349-384.
25. Hendrick, J.P., and Hartl, F.U. (1993). Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 6, 349-384.
26. Herskowitz, I. (1987). Functional inactivation of genes by dominant negative mutation. Nature 329, 219-222.
27. Holtzman, D.M., and Mobley, W.C. (1991). Molecular studies in Alzheimer's disease. Trends Biochem. Sci. 259,140-144.
28. Jan, L.Y., and Jan, Y.N. (1982). Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc. Natl. Acad. Sci. USA 7, 2700-27004.
29. Kamath-Loeb, A.S., Zen Iu, C., Suh, W.C., Lonetto, M.A., and Gross, C.A. (1995). Analysis of three DnaK mutant proteins suggests that progression through the ATPase cycle requires conformational changes. J. Biol. Chem. 270, 30051-30059.
30. Laemmli, U.K. (1970). Cleavage of the structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680-685.
31. Liberek, K., Skowyra, S., Zylicz, M., Johnson, C., and Georgopolous, C. (1991). The Escherickia coli DnaK chaperone, the 70-kDa heat shock protein eukaryotic equivalent, changes conformation upon ATP hydrolysis, thus triggering its dissociation from a bound target protein. J. Biol. Chem. 22, 14491-14496.
32. Lindquist, S., and Craig, E.A. (1988). The heat shock proteins. Annu. Rev. Genet. 22, 631-677.
33. Lis, J., and Wu, C. (1993). Proteins traffic on the heat shock promoter, parking, stalling and trucking along. Cell 74,1-4.
34. Manseau, L., Baradaran, A., Brower, S., Budhu, A., Elefant, F., Philip, A.P., Glover, D., Kaiser, K., Palter, K.B., and Selleck, S. (1997). GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev. Dyn. 209, 310-322.
35. Mehta, A. (1993). Functional Properties and Protein Binding Studies of Drosophila 70 kDa Heat Shock Cognate Proteins. Ph.D. Thesis. Philadelphia, PA: Temple University.
36. Morimoto, R.F. (1993). Cells in stress: transcriptional activation of heat shock genes. Science 259, 1404-1410.
37. Morris, J.A., Dorner, A.J., Edward, C.A., Hendershot, L.M., and Kaufman, R.J. (1997). Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J. Biol. Chem. 272, 4327-4334.
38. Normington, K., Kohno, K., Kozutsumi, Y., Gething, M.J., and Sambrook, J. (1989). S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57, 1223-1236.
39. O'Brien, M.C., Flaherty, K.M., and McKay, D.B. (1996). Lysine 71 of the chaperone protein Hsc70 is essential for ATP hydrolysis. J. Biol. Chem. 273, 74-15878.
40. O'Farrell, P.H. (1974). High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
41. Palleros, D.R., Reid, K.L., Shi, L, Welch, W.J., and Fink, A.L. (1993). ATP-induced protein-Hsp70 complex dissociation requires K+ but not ATP hydrolysis. Nature 365, 664-666.
42. Palter, K.B., Watanabe, M., Stinson, L., Mahowald, A.P., and Craig, E.A. (1986). Expression and localization of Drosophila melanogaster hsp70 cognate proteins. Mol. Cell. Biol. 6, 1187-1203.
43. Perkins, L.A., Doctor, J.S., Zhang, K., Stinson, L., Perrimon, N., and Craig, E.A. (1990). Molecular and developmental characterization of the heat shock cognate gene 4 of Drosophila melanogaster. Mol. Cell. Biol. 30, 3232-3238.
44. Perrimon, N., Lanjuin, A., Arnold, C., and Noll, E. (1996). Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics 344, 1681-1692.
45. Robertson, H.M., Preston, C.R., Philllis, R.W., and Sclitz-Johnson, D.M. (1988). A stable source of P-element transposase in Drosophila. Genetics 318, 120-128.
46. Rubin, D.M. (1993). Biochemical and Genetic Analysis of Drosophila Heat Shock Cognate 70 Proteins with Substitutions of Amino Acid Implicated in ATP Binding and Hydrolysis. Ph.D. Thesis. Philadelphia, PA: Temple University.
47. Rubin, D.M., Mehta, A.D., Zhu, J., Shoham, S., Chen, X., Wells, Q.R., and Palter, K.B. (1993). Genomic structure and sequence analysis of Drosophila melanogaster HSC70 genes. Gene 128, 155-163.
48. Sadis, S., and Hightower, L.E. (1992). Unfolded proteins stimulate molecular chaperone Hsc70 ATPase by accelerating ADP/ATP exchange. Biochemistry 33, 9406-9412.
49. Schmid, D., Baici, A., Gehring, H., and Christe, P. (1994). Kinetics of molecular chaperone action. Science 263, 971-973.
50. Schmucker, D., Jackle, H., and Gaul, U. (1997). Genetic analysis of the larval optic nerve projection in Drosophila. Development 124, 937-948.
51. Shamu, C.E., Cox, J.S., and Walter, P. (1994). The unfolded-protein-response pathway in yeast. Trends Cell Biol. 4, 56-60.
52. Vogel, J.P., Misra, L.M., and Rose, M.R. (1990). Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J. Biol. Chem. 110, 1885-1895.
53. Wei, J., Gaut, J.R., and Hendershot, L.M. (1995). In vitro dissociation of BiP-peptide complexes requires a conformational change in BiP after ATP binding but does not require ATP hydrolysis. J. Biol. Chem. 270, 26677-26682.
54. Wei, J., and Hendershot, L.M. (1995). Characterization of the nucleotide binding properties and ATPase activity of recombinant hamster BiP purified from bacteria. J. Biol Chem. 270, 26670-26676.
55. Werner-Washburne, M., Stone, D.E., and Craig, E.A. (1987). Complex interactions among members of an essential subfamily of HSP70 genes in Saccharomyces cerevisae. Mol. Cell. Biol. 7, 2568-2577.
56. Wilbanks, S.M., DeLuca-Flaherty, C., and McKay, D.B. (1994). Structural basis of the 70-kilodalton heat shock cognate protein ATP hydrolytic activity. J. Biol. Chem. 269, 12893-12898.
57. Wild, J., Kamath-Loeb A., Ziegelhoffer, E., Lonetto, M., Kawasaki, Y., and Gross, C.A. (1992). Partial loss of function mutations in DnaK, the Escherichia coli homologue of the 70-kDa heat shock proteins, affect highly conserved amino acids implicated in ATP binding and hydrolysis. Proc. Natl. Acad. Sci. USA 89, 7139-7143.
58. Zylicz, M., and Georgopoulos, G. (1984). Purification and properties of the Escherichia coli DnaK replication protein. J. Biol. Chem. 14, 8820-8825.