Primate chaperones Hsc70 (constitutive) and Hsp70 (induced) differ functionally in supporting growth and prion propagation in Saccharomyces cerevisiae

Genetics

Volumn 172, Issue 2, 2006, Pages 851-861

  Tutar, Yusuf ^a,b   Song, Youtao ^a,c   Masison, Daniel C ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b CUMHURIYET UNIVERSITY   (Turkey)

^c LIAONING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 70; ISOPROTEIN; VEGETABLE PROTEIN;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ANALYSIS; ENZYME SUBSTRATE COMPLEX; FUNCTIONAL ASSESSMENT; GENETIC CONSERVATION; HETEROLOGOUS EXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIMATE; PRION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ARABIDOPSIS; BLOTTING, WESTERN; CELL PROLIFERATION; HEAT; HEAT-SHOCK PROTEINS; HSC70 HEAT-SHOCK PROTEINS; PRIONS; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SAGUINUS;

EUKARYOTA; PRIMATES; SACCHAROMYCES CEREVISIAE;

EID: 33644749282     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.105.048926     Document Type: Article

References (62)

1. BLATCH, G. L., and M. LASSLE, 1999 The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. BioEssays 21: 932-993.
2. BOEKE, J. D., F. LACROUTE and G. R. FINK, 1984 A positive selection for mutants lacking orotidine-59-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197: 345-346.
3. CARRIGAN, P. E., G. M. NELSON, P. J. ROBERTS, J. STOFFER, D. L. RIGGS et al., 2004 Multiple domains of the co-chaperone Hop are important for Hsp70 binding. J. Biol. Chem. 279: 16185-16193.
4. CHERNOFF, Y. O., S. L. LINDQUIST, B. ONO, S. G. INGE-VECHTOMOV and S. W. LIEBMAN, 1995 Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 268: 880-884.
5. COX, B. S., 1965 "Ψ" a cytoplasmic suppressor of super-suppressor in yeast. Heredity 20: 505-521.
6. CRAIG, E. A., and C. A. GROSS, 1991 Is hsp70 the cellular thermometer? Trends Biochem. Sci. 16: 135-140.
7. DEMAND, J., J. LUDERS and J. HOHFELD, 1998 The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol. Cell. Biol. 18: 2023-2028.
8. DUINA, A. A., J. A. MARSH and R. F. GABER, 1996 Identification of two CyP-40-like cyclophilins in Saccharomyces cerevisiae, one of which is required for normal growth. Yeast 12: 943-952.
9. ESCHER, A., D. J. O'KANE, J. LEE and A. A. SZALAY, 1989 Bacterial luciferase alpha beta fusion protein is fully active as a monomer and highly sensitive in vivo to elevated temperature. Proc. Natl Acad. Sci. USA 86: 6528-6532.
10. FAN, C. Y., S. LEE and D. M. CYR, 2003 Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 8: 309-316.
11. FAN, C. Y., H. Y. REN, P. LEE, A. J. CAPLAN and D. M. CYR, 2005 The type IHsp40 zinc finger-like region is required for Hsp70 to capture non-native polypeptides from Ydj1. J. Biol. Chem. 280: 695-702.
12. FREEMAN, B. C., M. P. MYERS, R. SCHUMACHER and R. I. MORIMOTO, 1995 Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14: 2281-2292.
13. FUNG, K. L., L. HILGENBERG, N. M. WANG and W. J. CHIRICO, 1996 Conformations of the nucleotide and polypeptide binding domains of a cytosolic Hsp70 molecular chaperone are coupled. J. Biol. Chem. 271: 21559-21565.
14. GAO, B. C., J. BIOSCA, E. A. CRAIG, L. E. GREENE and E. EISENBERG, 1991 Uncoating of coated vesicles by yeast hsp70 proteins. J. Biol. Chem. 266: 19565-19571.
15. GASSLER, C. S., A. BUCHBERGER, T. LAUFEN, M. P. MAYER, H. SCHRODER et al., 1998 Mutations in the DnaK chaperone affecting interaction with the DnaJ cochaperone. Proc. Natl. Acad. Sci. USA 95: 15229-15234.
16. GISLER, S. M., E. V. PIERPAOLI and P. CHRISTEN, 1998 Catapult mechanism renders the chaperone action of Hsp70 unidirectional. J. Mol. Biol. 279: 833-840.
17. GLOVER, J. R., and S. LINDQUIST, 1998 Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94: 73-82.
18. GLOVER, J. R., and J. M. TKACH, 2001 Crowbars and ratchets: hsp100 chaperones as tools in reversing protein aggregation. Biochem. Cell Biol. 79: 557-568.
19. GREENE, L. E., R. ZINNER, S. NAFICY and E. EISENBERG, 1995 Effect of nucleotide on the binding of peptides to 70-kDa heat shock protein. J. Biol. Chem. 270: 2967-2973.
20. GREENE, M. K., K. MASKOS and S. J. LANDRY, 1998 Role of the J-domain in the cooperation of Hsp40 with Hsp70. Proc. Natl. Acad. Sci. USA 95: 6108-6113.
21. HA, J. H., U. HELLMAN, E. R. JOHNSON, L. LI, D. B. MCKAY et al., 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: 27796-27803.
22. HAINZL, O., H. WEGELE, K. RICHTER and J. BUCHNER, 2004 Cns1 is an activator of the Ssa1 ATPase activity. J. Biol. Chem. 279: 23267-23273.
23. HAN, W., and P. CHRISTEN, 2004 cis-effect of DnaJ on DnaK in ternary complexes with chimeric DnaK/DnaJ-binding peptides. FEBS Lett. 563: 146-150.
24. HARRISON, C., 2003 GrpE, a nucleotide exchange factor for DnaK. Cell Stress Chaperones 8: 218-224.
25. HARTL, F. U., and M. HAYER-HARTL, 2002 Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858.
26. JAMES, P., C. PFUND and E. A. CRAIG, 1997 Functional specificity among Hsp70 molecular chaperones. Science 275: 387-389.
27. +]. Genetics 163: 495-506.
28. +] prion is impaired by factors that regulate Hsp70 substrate binding. Mol. Cell. Biol. 24: 3928-3937.
29. JUNG, G., and D. C. MASISON, 2001 Guanidine hydrochloride inhibits Hsp104 activity in vivo: a possible explanation for its effect in curing yeast prions. Curr. Microbiol. 43: 7-10.
30. +] as a cellular stress. Genetics 156: 559-570.
31. KABANI, M., J. M. BECKERICH and J. L. BRODSKY, 2002 Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Mol. Cell. Biol. 22: 4677-4689.
32. LAUFEN, T., M. P. MAYER, C. BEISEL, D. KLOSTERMEIER, A. MOGK et al., 1999 Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proc. Natl Acad. Sci. USA 96: 5452-5457.
33. LOPEZ-BUESA, P., C. PFUND and E. A. CRAIG, 1998 The biochemical properties of the ATPase activity of a 70-kDa heat shock protein (Hsp70) are governed by the C-terminal domains. Proc. Natl. Acad. Sci. USA 95: 15253-15258.
34. LU, Z., and D. M. CYR, 1998 The conserved carboxyl terminus and zinc finger-like domain of the co-chaperone Ydj1 assist Hsp70 in protein folding. J. Biol. Chem. 273: 5970-5978.
35. MARSH, J. A., H. M. KALTON and R. F. GABER, 1998 Cns1 is an essential protein associated with the Hsp90 chaperone complex in Saccharomyces cerevisiae that can restore cyclophilin 40-dependent functions in Cpr7Δ cells. Mol. Cell. Biol. 18: 7353-7359.
36. MAYER, M. P., and B. BUKAU, 2005 Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62: 670-684.
37. MAYER, M. P., D. BREHMER, C. S. GASSLER and B. BUKAU, 2001 Hsp70 chaperone machines. Adv. Protein Chem. 59: 1-44.
38. MCCARTY, J. S., A. BUCHBERGER, J. REINSTEIN and B. BUKAU, 1995 The role of ATP in the functional cycle of the DnaK chaperone system. J. Mol. Biol. 249: 126-137.
39. MCCLELLAN, A. J., J. B. ENDRES, J. P. VOGEL, D. PALAZZI, M. D. ROSE et al., 1998 Specific molecular chaperone interactions and an ATP-dependent conformational change are required during posttranslational protein translocation into the yeast ER. Mol. Biol. Cell 9: 3533-3545.
40. NELSON, R. J., T. ZIEGELHOFFER, C. NICOLET, M. WERNER-WASHBURNE and E. A. CRAIG, 1992 The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71: 97-105.
41. NYLANDSTED, J., M. ROHDE, K. BRAND, L. BASTHOLM, F. ELLING et al., 2000 Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc. Natl. Acad. Sci. USA 97: 7871-7876.
42. OKA, M., M. NAKAI, T. ENDO, C. R. LIM, Y. KIMATA et al., 1998 Loss of Hsp70-Hsp40 chaperone activity causes abnormal nuclear distribution and aberrant microtubule formation in M-phase of Saccharomyces cerevisiae. J. Biol. Chem. 273: 29727-29737.
43. PARSELL, D. A., A. S. KOWAL, M. A. SINGER and S. LINDQUIST, 1994 Protein disaggregationmediated by heat-shock protein Hsp104. Nature 372: 475-478.
44. PATINO, M. M., J. J. LIU, J. R. GLOVER and S. LINDQUIST, 1996 Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 273: 622-626.
45. RIEGER, T. R., R. I. MORIMOTO and V. HATZIMANIKATIS, 2005 Mathematical modeling of the eukaryotic heat-shock response: dynamics of the hsp70 promoter. Biophys. J. 88: 1646-1658.
46. ROHDE, M., M. DAUGAARD, M. H. JENSEN, K. HELIN, J. NYLANDSTED et al., 2005 Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev. 19: 570-582.
47. SCHEUFLER, C., A. BRINKER, G. BOURENKOV, S. PEGORARO, L. MORODER et al., 2000 Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101: 199-210.
48. SCHMID, D., A. BAICI, H. GEHRING and P. CHRISTEN, 1994 Kinetics of molecular chaperone action. Science 263: 971-973.
49. +] and [URE3] prions and curing of [URE3] by Hsp70 protein chaperone Ssa1p but not by Ssa2p. Mol. Cell. Biol. 22: 3590-3598.
50. SHERMAN, F., 1994 Getting started with yeast. Methods Enzymol. 194: 3-21.
51. SIKORSKI, R. S., M. S. BOGUSKI, M. GOEBL and P. HIETER, 1990 A repeating amino acid motif in CDC23 defines a family of proteins and a new relationship among genes required for mitosis and RNA synthesis. Cell 60: 307-317.
52. STANSFIELD, I., K.M. JONES, V. V. KUSHNIROV, A. R. DAGKESAMANSKAYA, A. I. POZNYAKOVSKI et al., 1995 The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 14: 4365-4373.
53. STONE, D. E., and E. A. CRAIG, 1990 Self-regulation of 70-kilodalton heat shock proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 1622-1632.
54. SUNG, D. Y., E. VIERLING and C. L. GUY, 2001 Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 126: 789-800.
55. WEGELE, H., M. HASLBECK and J. BUCHNER, 2003a Recombinant expression and purification of Ssa1p (Hsp70) from Saccharomyces cerevisiae using Pichia pastoris. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 786: 109-115.
56. WEGELE, H., M. HASLBECK, J. REINSTEIN and J. BUCHNER, 2003b Sti1 is a novel activator of the Ssa proteins. J. Biol. Chem. 278: 25970-25976.
57. WERNER-WASHBURNE, M., D. E. STONE and E. A. CRAIG, 1987 Complex interactions among members of an essential subfamily of Hsp70 genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 7: 2568-2577.
58. WICKNER, R. B., 1994 Evidence for a prion analog in S. cerevisiae: the [URE3] non-Mendelian genetic element as an altered URE2 protein. Science 264: 566-569.
59. WITTUNG-STAFSHEDE, P., J. GUIDRY, B. E. HORNE and S. J. LANDRY, 2003 The J-domain of Hsp40 couples ATP hydrolysis to substrate capture in Hsp70. Biochemistry 42: 4937-4944.
60. WU, S., S. REN, H. CHEN, R. F. CHUN, M. A. GACAD et al., 2000 Intracellular vitamin D binding proteins: novel facilitators of vitamin D-directed transactivation. Mol. Endocrinol. 14: 1387-1397.
61. YOUNG, J. C., J. M. BARRAL and F. U. HARTL, 2003 More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28: 541-547.
62. ZHOURAVLEVA, G., L. FROLOVA, X. LE GOFF, R. LE GUELLEC, S. INGE-VECHTOMOV et al., 1995 Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J. 14: 4065-4072.