Nucleotide binding and hydrolysis properties of Neurospora crassa cytosolic molecular chaperones, Hsp70 and Hsp80, heat-inducible members of the eukaryotic stress-70 and stress-90 families

Biochemistry and Cell Biology

Volumn 77, Issue 2, 1999, Pages 89-99

  Ouimet, P M ^a,b   Kapoor, M ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b MONSANTO COMPANY   (United States)

Author keywords

ATPase; Hsp70; Hsp80; Molecular chaperones; Neurospora

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ADIPIMIDIC ACID DIMETHYL ESTER; CYTIDINE TRIPHOSPHATE; DIMER; GLUTARALDEHYDE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; NICOTINAMIDE ADENINE DINUCLEOTIDE; NUCLEOTIDE; OLIGOMER; PROTEIN SUBUNIT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUBERIMIDIC ACID DIMETHYL ESTER; SULFONIC ACID DERIVATIVE;

ARTICLE; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROLYSIS; HYDROPHOBICITY; MOLECULAR DYNAMICS; NEUROSPORA CRASSA; NONHUMAN; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DETERMINATION; PROTEIN FAMILY; PROTEIN TERTIARY STRUCTURE; REACTION ANALYSIS; STRUCTURE ANALYSIS;

ADENOSINE TRIPHOSPHATASES; CROSS-LINKING REAGENTS; CYTOSOL; DIMETHYL ADIPIMIDATE; DIMETHYL SUBERIMIDATE; FLUORESCENT DYES; FUNGAL PROTEINS; GLUTARAL; HEAT-SHOCK PROTEINS; HEATING; HSP70 HEAT-SHOCK PROTEINS; HYDROLYSIS; NAPHTHALENESULFONATES; NEUROSPORA CRASSA; NUCLEOTIDES; SUBSTRATE SPECIFICITY;

EUKARYOTA; NEUROSPORA; NEUROSPORA CRASSA;

EID: 0032841126     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/bcb-77-2-89     Document Type: Article

References (45)

1. Aligue, R., Akhavan-Niak, H., and Russell, P. 1994. A role for Hsp90 in cell cycle control: Weel tyrosine kinase activity requires interaction with Hsp90. EMBO J. 13: 6099-6106.
2. Boston, R.S., Vitanen, P.V., and Vierling, E. 1996. Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32: 191-222.
3. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
4. Carlino, A., Toledo, H., Skaleris, D., DeLisio, R., Weissbach, H., and Brot, N. 1992. Interaction of liver Grp78 and Escherichia coli recombinant Grp78 ATP: multiple species and disaggregation. Proc. Natl. Acad. Sci U.S.A. 89: 2081-2085.
5. Craig, E.A., Gambill, B.D., and Nelson, R.J. 1993. Heat shock proteins: molecular chaperones of protein biogenesis. Microbiol. Rev. 57: 402-414.
6. Csermely, P., Kjtar, J., Hollos, I.M., Jalsovsky, G., Holly, S., Kahn, C.R., Gergely, P., Soti, C., Mihaly, K., and Somogyi, J. 1993. ATP induces a conformational change of the 90-kDa heat-shock protein (HSP90). J. Biol. Chem. 268: 1901-1907.
7. Edelman, G.M., and McClure, W.O. 1968. Accounts Chem. Res. 1: 65-70
8. Flaherty, F.M., DeLuca-Flaherty, C., and McKay, D.B. 1990. Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature (London), 346: 623-628.
9. Freitag, D.G., Ouimet, P.M., Girvitz, T.L., and Kapoor, M. 1997. Heat shock protein 80 of Neurospora crassa, a cytosolic molecular chaperone of the eukaryotic stress 90 family, interacts directly with heat shock protein 70. Biochemistry, 36: 10 221-10 229.
10. Gao, B., Eisenberg, E., and Greene, L. 1996. Effect of constitutive 70-kDa heat shock protein polymerization on its interaction with protein substrate. J. Biol. Chem. 271: 16 792-16 797.
11. Garcia-Cardena, G., Fan, R., Shah, V., Sorrentino, R., Cirino, G., Papapetropoulos, A., and Sessa, W.C. 1998. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature (London), 392: 821-824.
12. Hartl, F.U. 1996. Molecular chaperones in cellular protein folding. Nature (London), 381: 571-580.
13. Hendricks, J.P., and Hartl, F.U. 1993. Molecular chaperone functions of heat shock proteins. Annu. Rev. Biochem. 62: 349-384.
14. Hiromura, M., Yano, M., Mori, H., Inoue, M., and Kido, H. 1998. Intrinsic ADP-ATP exchange activity is a novel function of the molecular chaperone, Hsp70. J. Biol. Chem. 273: 5435-5438.
15. Hunter, M.J., and Ludwig, M.L. 1972. Amidination. In Methods in enzymology. Vol. 25. Edited by C.H.W. Hirs and S.N. Timasheff. Academic Press, New York. pp. 585-596.
16. Hutchinson, K.A., Dittmar, K.D., Czar, M.J., and Pratt, W.B. 1994. Proof that HSP70 is required for assembly of the glucocorticoid receptor into a heterocomplex with HSP90. J. Biol. Chem. 269: 5043-5049.
17. Jakob, U., and Buchner, J. 1994. Assisting spontaneity: the role of Hsp90 and small Hsps as molecular chaperones. Trends Biochem. Sci. 19: 205-211.
18. Jakob, U., Scheibel, T., Bose, S., Renstein, J., and Buchner, J. 1996. Assessment of the ATP binding properties of Hsp90. J. Biol. Chem. 271: 10 035-10 041.
19. Kapoor, M., and Lewis, J. 1987. Alteration of protein synthesis pattern in Neurospora crassa cells by hyperthermal and oxidative stress. Can. J. Microbiol. 22: 162-168.
20. Kapoor, M., and O'Brien, M.D. 1977. Investigations of the quaternary structure of Neurospora pyruvate kinase by cross-linking with bifunctional reagents: the effect of substrates and allosteric ligands. Can. J. Biochem. 55: 43-49.
21. Kapoor, M., Curle, C.A., and Runham, C. 1995. The hsp70 gene family of Neurospora crassa: cloning, sequence analysis, expression, and genetic mapping of the major stress-inducible member. J. Bacteriol. 177: 212-221.
22. King, C., Eisenberg, E., and Greene, L. 1995. Polymerization of 70-kDa heat shock protein by yeast DnaJ in ATP. J. Biol. Chem. 270: 22 535-22 540.
23. Laemmli, U.K. 1970. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature (London), 227: 680-685.
24. Loubradou, G., Begueret, J., and Turcq, B. 1997. A mutation in an HSP90 gene affects the sexual cycle and suppresses vegetative incompatibility in the fungus Podospora anserina. Genetics, 147: 581-588.
25. Miernyk, J.A., and Hayman, G.T. 1996. ATPase activity and molecular chaperone function of the stress 70 proteins. Plant Physiol. 110: 419-424.
26. Minami, Y., Hohfeld, J., Ohtsuka, K., and Hartl, F.-U. 1996. Regulation of the heat shock protein 70 reaction cycle by the mammalian DnaJ homolog, Hsp40. J. Biol.Chem. 271: 19 617-19 624.
27. Nadeau, K., Das, A., and Walsh, C.T. 1993a. Hsp90 chaperonins possess ATPase activity and bind heat-shock transcription factors and peptidyl prolyl isomerases. J. Biol. Chem. 268: 1479-1487.
28. Nadeau, K., Sullivan, M.A., Bradley, M., Engman, D.M., and Walsh, C.T. 1993b. 83-kilodalton heat-shock proteins of Trypanosomes are potent peptide-stimulated ATPases. Prot. Sci. 1: 970-979.
29. Ouimet, P.M., and Kapoor, M. 1998. Analysis of complex formation between Hsp80 and Hsp70, cytosolic molecular chaperones of Neurospora crassa, by enzyme-linked immunosorbent assays (ELISA). Biochem. Cell Biol. 76: 97-106.
30. 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 (London), 365: 664-665.
31. Palleros, D.R., Shi, L., Reid, K.L., and Fink, A.L. 1994. hsp70-protein complexes. Complex stability and conformation of bound substrate. J. Biol. Chem. 269: 13 107-13 114.
32. Pratt, W.B. 1993. The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 268: 21 455-21 458.
33. Prodromou, C., Roe, S.M., O'Brien, R., Ladbury, J.E., Piper, P.W., and Pearl, L.H. 1997. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell, 90: 65-75.
34. Rassow, J., von Ahsen, O., Bomer, U., and Pfanner, N. 1997. Molecular chaperones: towards a characterization of the heat-shock protein 70 family. Trends Cell Biol. 7: 129-133.
35. Roychowdhury H.S., Wong, D., and Kapoor, M. 1992. Hsp80 of Neurospora crassa: cDNA cloning, gene mapping, and studies of mRNA accumulation under stress. Biochem. Cell Biol. 70: 1356-1367.
36. Scheibel, T., Neuhofen, S., Weikl, T., Mayr, C., Reinstein, C., Vogel, P.D., and Buchner, J. 1997. ATP-binding properties of human Hsp90. J. Biol. Chem. 272: 18 608-18 613.
37. Scheibel, T., Weikl, T., and Buchner, J. 1998. Two chaperone sites in Hsp90 differing in substrate specificity and ATP dependence. Proc. Natl. Acad. Sci. U.S.A. 95: 1495-1499.
38. Schmid, S.L., Braell, W.A., and Rothman, J.E. 1985. ATP catalyses the sequestration of clathrin during enzymatic uncoating. J. Biol. Chem. 260: 10 057-10 062.
39. Schonfield, H.-J., Schmidt, D., Schroder, H., and Bukau, B. 1995. The DnaK chaperone system of Escherichia coli: quaternary structures and interactions of DnaK and GropE components. J. Biol. Chem. 270: 2183-2189.
40. Stepanova, L., Leng, X., Parker, S.B., and Harper, J.W. 1996. Mammalian p50cdc37 is a protein kinase targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev. 10: 1491-1502.
41. Sullivan, W., Stensgard, B., Caucutt, G., Bartha, B., McMahon, N., Alnemri, E.S., Litwack, G., and Toft, D. 1997. Nucleotides and two functional states of hsp90. J. Biol. Chem. 272: 8007-8012.
42. Toledo, H., Carlino, A., Vidal, V, Redfield, B., Nettleton, M., Kocham, J., Brot, N., and Weissbach, H. 1993. Dissociation of glucose-regulated protein Grp78 and Grp78-IgG E Fc complexes by ATP. Proc. Natl. Acad. Sci. U.S.A. 90: 2505-2508.
43. Vogel, H.J. 1956. A convenient growth medium for Neurospora crassa (N medium). Microb. Genet. Bull. 13: 42-43.
44. Xu, Y., and Lindquist, S.1993. Heat shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. U.S.A. 90: 7074-7078.
45. Zhu, X., Zhao, X., Burkholder, W.F., Gragerov, A., Ogata, C.M., Gottesman, M.E., and Hendrickson, W.A. 1996. Structural analysis of substrate binding by the molecular chaperone DnaK. Science (Washington, D.C.), 272: 1606-1614.