SSI1 encodes a novel Hsp70 of the Saccharomyces cerevisiae endoplasmic reticulum

Molecular and Cellular Biology

Volumn 16, Issue 11, 1996, Pages 6444-6456

  Baxter, Bonnie K ^a   James, Philip ^a   Evans, Tara ^a   Craig, Elizabeth A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN 70;

ALLELE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; ENDOPLASMIC RETICULUM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0029802682     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.11.6444     Document Type: Article

References (76)

1. Archibald, F. S., and I. Fridovich. 1982. The scavenging of superoxide radical by manganous complexes in vitro. Arch. Biochem. Biophys. 214:452-463.
2. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. G. Seidman, J. Smith, and K. Struhl. 1989. Current protocols in molecular biology. John Wiley and Sons, New York.
3. Baust, E. 1979. Studies on the acceptor specificity of asparagine-N-glycosyl-transferase from rat liver. FEBS Lett. 103:296-336.
4. 2+ cation. J. Am. Them. Soc. 100:1920-1921.
5. Blond-Elguindi, S., S. Cwirla, W. Dower, R. Lipshutz, S. Sprang, J. Sambrook, and M. J. Gething. 1993. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75: 717-728.
6. Bole, D. G., L. M. Hendershot, and J. F. Kearney. 1986. Posttranslational association of immunoglobulin heavy chain binding protein wilh nascent heavy chains in nonsecreting and secreting hybridomas. J. Cell Biol. 102: 1558-1566.
7. Bollag, D. M., and S. J. Edelstein. 1991. Protein methods. Wiley-Liss, Inc., New York.
8. Boorstein, W., and E. A. Craig. 1990. Transcriptional regulation of SSA3, an HSP70 gene from Saccharomyces cerevisiae. Mol. Cell. Biol. 10:3262-3267.
9. Boorstein, W. R., and E. A. Craig. 1990. Structure and regulation of the SSA4 HSP70 gene of Saccharomyces cerevisiae. J. Biol. Chem. 265:18912-18921.
10. Boorstein, W. R., T. Ziegelhoffer, and E. A. Craig. 1994. Molecular evolution of the HSP70 multigene family. J. Mol. Evol. 38:1-17.
11. Brodsky, J., and R. Schekman. 1994. Heat shock cognate proteins and polypeptide translocation across the endoplasmic reticulum membranes, p. 85-110. In R. I. Morimoto, A. Tissieres, and C. Georgopolous (ed.), The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
12. Brodsky, J. L., J. Goeckeler, and R. Schekman. 1995. BiP and Sec63p are required for both co- and posttranslational protein translocation into the yeast endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 92:9643-9646.
13. Brodsky, J. L., and R. Schekman. 1993. A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome. J. Cell Biol. 123:1355-1363.
14. Caplan, A., and M. Douglas. 1991. Characterization of YDJ1: a yeast homologue of the bacterial dnaJ protein. J. Cell Biol. 114:609-621.
15. Chang, E. C., and D. J. Kosman. 1989. Intracellular Mn(II)-associated superoxide scavenging activity protects Cu,Zn superoxide dismutase-deficient Saccharomyces cerevisiae against dioxygen stress. J. Biol. Chem. 264:12172-12178.
16. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
17. Cox, J. S., C. E. Shamu, and P. Walter. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197-12116.
18. Craig, E. A., B. K. Baxter, J. Becker, J. Halladay, and T. Ziegelhoffer. 1994. Cytosolic hsp70s of Saccharomyces cerevisiae: roles in protein synthesis, protein translocation, proteolysis, and regulation, p. 31-52. In R. I. Morimoto, A. Tissieres, and C. Georgopoulos (ed.), The biology of heat shock proteins and molecular chaperones. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
19. Craig, E. A., B. D. Gambill, and R. J. Nelson. 1993. Heat shock proteins: molecular chaperones of protein biogenesis. Microbiol. Rev. 57:4112-414.
20. Craven, R. A., M. Egerton, and C. J. Stirling. 1996. A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J. 15:2640-2650.
21. Flaherty, K. M., C. DeLuca-Flaherty, and D. B. McKay. 1990. Three dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature (London) 346:623-628.
22. Flaherty, K. M., D. B. McKay, W. Kabash, and K. Holmes. 1991. Similarity of the three-dimensional structure of actin and the ATPase fragment of a 70-kDa heat shock cognate protein. Proc. Natl. Acad. Sci. USA 88:5041-5045.
23. Flynn, G., J. Pohl, M. Flocco, and J. Rothman. 1991. Peptide-binding specificity of the molecular chaperone BiP. Nature (London) 353:726-730.
24. Gething, M. J., K. McCammon, and J. Sambrook. 1986. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell 46:939-950.
25. Gietz, R. D., R. H. Schiestl, A. R. Willems, and R. A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11:355-360.
26. Glick, B. S. 1995. Can Hsp70 proteins act as force-generating motors? Cell 80:11-14.
27. Guan, K. L., and J. E. Dixon. 1991. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:262-267.
28. Halladay, J. T., and E. A. Craig. 1995. A heat shock transcription factor with reduced activity suppresses a yeast HSP70 mutant. Mol. Cell. Biol. 15:4890-4897.
29. Haselbeck, A., and R. Schekman. 1986. Interorganelle transfer and glycosylation of yeast invertase in vitro. Proc. Natl. Acad. Sci. USA 83:2017-2021.
30. Hendrick, J. P., T. Langer, T. A. Davis, F. U. Hartl, and M. Wiedmann. 1993. Control of folding and membrane translocation by binding of the chaperone DmU to nascent polypeptides. Proc. Natl. Acad. Sci. USA 90:10216-10220.
31. Herskowitz, I., and R. E. Jensen. 1991. Putting the HO gene to work: practical uses for mating-type switching. Methods Enzymol. 194:132-146.
32. 31a. James, P. Unpublished data.
33. Klionsky, D. J., L. M. Banta, and S. D. Emr. 1988. Intracellular sorting and processing of a yeast vacuolar hydrolase: proteinase A propeptide contains vacuolar targeting information. Mol. Cell. Biol. 8:2105-2116.
34. Kohno, K., K. Normington, J. Sambrook, M.-J. Gething, and K. Mori. 1993. The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell. Biol. 13:877-890.
35. Koppenol, W. H., F. Levine, T. L. Hatmaker, J. Epp, and J. D. Rush. 1986. Catalysis of superoxide dismutase by manganese aminopolycarboxylate complexes. Arch. Biochem. Biophys. 251:594-599.
36. Langer, T., C. Lu, H. Echols, J. Flanagan, M. K. Haver, and F. U. Hartl. 1992. Successive action of DnaK, DnaJ, and GroEL along the pathway of chaperone-mediated protein folding. Nature (London) 356:683-689.
37. Lapinskas, P. J., K. W. Cunningham, X. F. Liu, G. R. Fink, and V. C. Culotta. 1995. Mutations in PMRI suppress oxidative damage in yeast cells lacking superoxide dismutase. Mol. Cell. Biol. 15:1382-1388.
38. Liberek, K., J. Marszalek, D. Ang, and C. Georgopoulos. 1991. Escherichia coli DnaJ and GrpR heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88:2874-2878.
39. Lyman, S. K., and R. Schekman. 1995. Interaction between BiP and Sec63p is required for the completion of protein translocation into the ER of Saccharomyces cerevisiae. J. Cell Biol. 131:1163-1171.
40. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
41. Mori, K., W. Ma, M. J. Gething, and J. Sambrook. 1993. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74:743-756.
42. Mori, K., A. Sant, K. Kohno, K. Normington, M. J. Gething, and J. Sambrook. 1992. A 22-bp cis-acting element is necessary and sufficient for the induction the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11: 2583-2593.
43. Nelson, R. J., and J. Becker. Personal communication.
44. Nelson, R. J., M. Heschl, and E. A. Craig. 1992. Isolation and characterization of extragenic suppressors of mutations in the SSA hsp70 genes of Saccharomyces cerevisiae. Genetics 131:277-285.
45. Nelson, R. J., T. Ziegelhoffer, C. Nicolet, M. Werner-Washburne, and E. A. Craig. 1992. The translation machinery and seventy kilodalton heat shock protein cooperate in protein synthesis. Cell 71:97-105.
46. Normington, K., K. Kohno, Y. Kozutsumi, M. J. Gething, and J. Sambrook. 1989. S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57:1223-1236.
47. Parodi, A. J. 1979. Biosynthesis of yeast mannoproteins. J. Biol. Chem. 254:8343-8352.
48. Partaledis, J. A., and V. Berlin. 1993. The FKB2 gene of Saccharomyces cerevisiae, encoding the immunosuppressant-binding protein FKBP-13, is regulated in response to accumulation of unfolded proteins in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 90:5450-5454.
49. Pelham, H. R. B., K. G. Hardwick, and W. J. Lewis. 1988. Sorting of soluble ER proteins in yeast. EMBO J. 7:1757-1762.
50. Rasmussen, S. W. 1994. Sequence of a 20.7 kb region of yeast chromosome X1 includes the NUP100 gene, an open reading frame (ORF) possibly representing a nucleoside diphosphate kinase gene, tRNAs for IIis, Val and Trp in addition to seven ORFs with weak or no significant similarity to known proteins. Yeast 10:S69-S74.
51. Rose, M., and J. Vogel. 1994. KAR2, p. 41-42. In S. Rothblatt, P. Novick, and T. H. Stevens (ed.), Guidebook to the secretory pathway. Oxford University Press, New York.
52. Rose, M. D., L. M. Misra, and J. P. Vogel. 1989. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57:1211-1221.
53. Rose, M. D., P. Novick, J. H. Thomas, D. Botstein, and G. R. Fink. 1987. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene 60:237-243.
54. Rose, M. D., J. P. Vogel, and M. A. Scidmore. Personal communication.
55. Rothblatt, J., R. Deshaies, S. Sanders, G. Daum, and R. Schekman. 1989. Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum. J. Cell Biol. 109:2641-2652.
56. Sadler, I., A. Chiang, T. Kurihara, J. Rothblatt, J. Way, and P. Silver. 1989. A yeast gene important for protein assembly into the endoplasmic reticulum and the nucleus has homology to DnaJ, an Escherichia coli heat shock protein. J. Cell Biol. 109:2665-2675.
57. Sanders, S. L., K. M. Whitfield, J. P. Vogel, M. D. Rose, and R. W. Schekman. 1992. Sec16p and BiP directly facilitate polypeptide translocation into the ER. Cell 69:353-365.
58. Schilke, B., J. Forster, J. Davis, P. James, W. Walter, S. Laloraya, J. Johnson, B. Miao, and E. Craig. 1996. The cold sensitivity of a mutant of Saccharomyces cerevisiae lacking a mitochondrial heat shock protein 70 is suppressed by loss of mitochondrial DNA. J. Cell Biol. 134:603-613.
59. Schlenstedt, G., S. Harris, B. Risse, R. Lill, and P. A. Silver. 1995. A yeast DnaJ homologue, Scj1p, can function in the endoplasmic reticulum with BiP/Kar2p via a conserved domain that specifies interactions with Hsp70s. J. Cell Biol. 129:979-988.
60. Schmitt, M. E., T. A. Brown, and B. L. Trumpower. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 18:3091-3092.
61. Schroder, H., T. Langer, F.-U. Hartl, and B. Bukau. 1993. DnaK, DnaJ and GrpE form a cellular chaperone machinery capable of repairing heat-induced protein damage. EMBO J. 12:4137-4144.
62. Scidmore, M. A., H. H. Okamura, and M. D. Rose. 1993. Genetic interactions between KAR2 and SEC63, encoding eukaryotic homologues of DnaK and DnaJ in the endoplasmic reticulum. Mol. Biol. Cell 4:1145-1159.
63. Sharp, P. M., and W.-H. Li. 1987. The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 15:1281-1295.
64. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
65. Simons, J. F., S. Ferro-Novick, M. D. Rose, and A. Helenius. 1995. BiP/ Kar2p serves as a molecular chaperone during carboxypeptidase Y folding in yeast. J. Cell Biol. 130:41-49.
66. 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.
67. Stuart, R., D. Cyr, E. A. Craig, and W. Neupert. 1994. Mitochondrial molecular chaperones: their role in protein translocation. Trends Biochem. Sci. 19:87-92.
68. Tachibana, C., and T. H. Stevens. 1992. The yeast EUG1 gene encodes an endoplasmic reticulum protein that is functionally related to protein disulfide isomerase. Mol. Cell. Biol. 12:4601-4611.
69. Tamai, K. T., E. B. Gralla, L. M. Ellerby, J. S. Valentine, and D. J. Thiele. 1993. Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. Proc. Natl. Acad. Sci. USA 90:8013-8017.
70. Thomas, B. J., and R. Rothstein. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619-630.
71. Tokunaga, M., A. Kawamura, and K. Kohno. 1992. Purification and characterization of BiP/Kar2 protein from Saccharomyces cerevisiae. J. Biol. Chem. 267:17553-17559.
72. Vogel, J. P., L. M. Misra, and M. D. Rose. 1990. Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J. Cell Biol. 110:1885-1895.
73. von Heijne, G. 1985. Signal sequences: the limits of variation. J. Mol. Biol. 184:99-105.
74. 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.
75. Zhu, X., X. Zhao, W. Burkholder, A. Gragerov, C. Ogata, M. Gottesman, and W. Hendrickson. 1996. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 272:1606-1614.
76. Ziegelhoffer, T., C. Pfund, and E. Craig. Unpublished data.