Regulation of the heat-shock response in bacteria

Annual Review of Microbiology

Volumn 47, Issue , 1993, Pages 321-350

  Yura, T ^a,c   Nagai, H ^b   Mori, H ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

^c Kyoto Research Park ^*  (Japan)

Author keywords

Escherichia coli; heat shock protein; stress response; translational control; factor

Indexed keywords

MATING HORMONE ALPHA FACTOR;

ESCHERICHIA COLI; HEAT STROKE; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS; TRANSLATION REGULATION;

ESCHERICHIA COLI;

EID: 0027385183     PISSN: 00664227     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.mi.47.100193.001541     Document Type: Review

References (122)

1. Allan, B., Linseman, M., McDonald, L. A., Lam, J. S., Kropinski, A. M. 1988. Heat shock response of Pseudomonas aeruginosa. J. Bacteriol. 170: 3668-74
2. Allen, S. P., Polazzi, J. O., Gierse, J, K., Easton, A. M. 1992. Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli. J. Bacteriol. 174:6938-47
3. 32 by the phage λ cIII protein. Genes Dev. 1:57-64
4. Baker, T. A., Grossman, A. D., Gross, C A. 1984. A gene regulating the heat shock response in Escherichia coli also affects proteolysis. Proc. Natl. Acad. Sci. USA 81:6779-83
5. Bloom, M., Skelly, S., VanBogelen, R., Neidhardt, F., Brot, N., Weissbach, H. 1986. In vitro effect of the Escherichia coli heat shock regulatory protein on expression of heat shock genes. J. Bacteriol. 166:380-84
6. Bochkareva, E. S., Lisson, Girshovich, A. S. 1988. Transient association of newly synthesized unfolded proteins with the heat-shock GroEL protein. Nature 336:254-57
7. Bukau, B., Walker, G. C. 1989. Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J. Bacteriol. 171:2337-46
8. Bukau, B., Walker, G. C. 1990. Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the DnaK chaperone. EMBO J. 9:4027-36
9. 32. J. Bacteriol. 170:3479-84
10. Cooper, S., Ruettinger, T. 1975. A temperature sensitive nonsense mutation affecting the synthesis of a major protein of Escherichia coli K12. Mol. Gen. Genet. 139:167-76
11. Cowing, D. W., Bardwell, J. C. A., Craig, E. A., Woolford, C., Hendrix, R. W., Gross, C. A. 1985. Consensus sequence for Escherichia coli heat shock gene promoters. Proc. Natl. Acad. Sci. USA 82:2679-83
12. Craig, E. A., Gross, C. A. 1991. Is hsp70 the cellular thermometer? TIBS 16:135-40
13. Crickmore, N., Salmond, G. P. C. 1986. The Escherichia coli heat shock regulatory gene is immediately downstream of a cell division operon: the fam mutation is allelic with rpoH. Mol. Gen. Genet. 205:535-39
14. DiDomenico, B. J., Bugaisky, G. E., Lindquist, S. 1982. The heat shock response is self-regulated at both the transcriptional and posttranscriptional levels. Cell 31:593-603
15. Donnelly, C., Walker, G. C. 1989. groE mutants of Escherichia coli are defective in umuDC-dependent UV mutagenesis. J. Bacteriol. 171:6117-25
16. Drahos, D. J., Hendrix, R. W. 1982. Effect of bacteriophage lambda infection on synthesis of groE protein and other Escherichia coli proteins. J. Bacteriol. 149:1050-63
17. Ellis, R. J., van der Vies, S. M. 1991. Molecular chaperones. Annu. Rev. Biochem. 60:321-47
18. E subunit of Escherichia coli RNA polymerase: a second alternate σ factor involved in high-temperature gene expression. Genes Dev. 3:1462-71
19. Erickson, J. W., Vaughn, V., Walter, W. A., Neidhardt, F. C., Gross, C. A. 1987. Regulation of the promoters and transcripts of rpoH, the Escherichia coli heat shock regulaory gene. Genes Dev. 1:419-32
20. Faxen, M., Plumbridge, J., Isaksson, L. A. 1991. Codon choice and potential complementarity between mRNA downstream of the initiation codon and bases 1471-1480 in 16S ribosomal RNA affects expression of glnS. Nucleic Acids Res. 19:5247-51
21. Fujita, N., Ishihama, A. 1987. Heat-shock induction of RNA polymerase sigma-32 synthesis in Escherichia coli: transcriptional control and multiple promoter system. Mol. Gen. Genet. 210: 10-15
22. Fujita, N., Ishihama, A., Nagasawa, Y., Ueda, S. 1987. RNA polymerase sigma-related proteins in Escherichia coli: detection by antibodies against a synthetic peptide. Mol. Gen. Genet. 210:5-9
23. Fujita, N., Nomura, T., Ishihama, A. 1987. Promoter selectivity of Escherichia coli RNA polymerase: purification and properties of holoenzyme containing the heat-shock σ subunit. J. Biol. Chem. 262:1855-59
24. Gaitanaris, G. A., Papavassiliou, A. G., Rubock, P., Silverstein, S. J., Gottesman, M. E. 1990. Renaturation of denatured λ repressor requires heat shock proteins. Cell 61:1013-20
25. 32. Cell 69:833-42
26. Garvin, L. D., Hardies, S. C. 1989. Nucleotide sequence for the htpR gene from Citrobacter freundii. Nucleic Acids Res. 17:4889
27. Georgopoulos, C., Ang, D., Liberek, K., Zylicz, M. 1990. Properties of the Escherichia coli heat shock proteins and their role in bacteriophage λ growth. See Ref. 62, pp. 191-221
28. Georgopoulos, C., Ang, D., Maddock, A., Raina, S., Lipinska, B., Zylicz, M. 1990. Heat shock response of Escherichia coli. In The Bacterial Chromosome, ed. K. Drlica, M. Riley, pp. 405-19. Washington, DC: Am. Soc. Microbiol.
29. Goff, S. A., Casson, L. P., Goldberg, A. L. 1984. Heat shock regulatory gene htpR influences rates of protein degradation and expression of the Ion gene in Escherichia coli. Proc. Natl. Acad. Sci. USA 81:6647-51
30. Goff, S. A., Goldberg, A. L. 1985. Production of abnormal proteins in E. coli stimulates transcription of Ion and other heat shock genes. Cell 41:587-95
31. Gross, C. A., Straus, D. B., Erickson, J. W., Yura, T. 1990. The function and regulation of heat shock proteins in Escherichia coli. See Ref. 62, pp. 167-89
32. Grossman, A. D., Erickson, J. W., Gross, C. A. 1984. The htpR gene product of E. coli is a sigma factor for heat-shock promoters. Cell 38:383-90
33. 32 synthesis can regulate the synthesis of heat shock proteins in Escherichia coli. Genes Dev. 1:179-84
34. Grossman, A. D., Taylor, W. E., Burton, Z. F., Burgess, R. R., Gross, C. A. 1985. Stringent response in Escherichia coli induces expression of heat shock proteins. J. Mol. Biol. 186: 357-65
35. Herendeen, S. L., VanBogelen, R. A., Neidhardt, F. C. 1979. Levels of major proteins of Escherichia coli during growth at different temperatures. J. Bacteriol. 139:185-94
36. Jaeger, J. A., Turner, D. H., Zuker, M. 1989. Improved predictions of secondary structures for RNA. Proc. Natl. Acad. Sci. USA 86:7706-10
37. Jenkins, D. E., Auger, E. A., Matin, A. 1991. Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J. Bacteriol. 173:1992-96
38. Johnson, W. C., Moran, C. P. Jr., Losick, R. 1983. Two RNA polymerase sigma factors from Bacillus subtilis discriminate between overlapping promoters for a developmentally regulated gene. Nature 302:800-4
39. 32 synthesis: requirement for an internal control element. J. Bacteriol. 173: 3904-6
40. Kanemori, M., Yura, T. 1991. Physiological functions of the GroE heat shock proteins: effects of decreased levels of GroE. Annu. Meet. Mol. Biol. Soc. Jpn. Abstr. p. 196
41. Keller, J. A., Simon, L. D. 1988. Divergent effects of a dnaK mutation on abnormal protein degradation in Escherichia coli. Mol. Micorbiol. 2:31-41
42. 32). J. Bacteriol. 173:4247-53
43. Kochan, J., Murialdo, H. 1982. Stimulation of groE synthesis in Escherichia coli by bacteriophage lambda infection. J. Bacteriol. 149:1166-70
44. 32-dependent heat shock protein F21.5. J. Bacteriol. 172:6026-34
45. +-dependent fashion. Proc. Natl. Acad. Sci. USA 81:1499-1503
46. Kusukawa, N., Yura, T. 1988. Heat shock protein GroE of Escherichia coli: key protective roles against thermal stress. Genes Dev. 2:874-82
47. Landick, R., Vaughn, V., Lau, E. T., VanBogelen, R. A., Erickson, J. W., Neidhardt, F. C. 1984. Nucleotide sequence of the heat shock regulatory gene of E. coli suggests its protein product may be a transcription factor. Cell 38:175-82
48. Langer, T., Lu, C., Echols, H., Flanagan, J., Hayer, M. K., Hartl, F. U. 1992. Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356:683-89
49. LaRossa, R. A., Van Dyk, T. K. 1991. Physiological roles of the DnaK and GroE stress proteins: catalysts of protein folding or macromolecular sponges? Mol. Microbiol. 5:529-34
50. Lemaux, P. G., Herendeen, S. L., Bloch, P. L., Neidhardt, F. C. 1978. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell 13:427-34
51. 70: localization of a region involved in the interaction with core RNA polymerase. Biochemistry 28:7728-34
52. Lesley, S. A., Jovanovich, S. B., Tse-Dinh, Y.-C., Burgess, R. R. 1990. Identification of a heat shock promoter in the topA gene of Escherichia coli. J. Bacteriol. 172:6871-74
53. 32 by the use of monoclonal antibodies. J. Biol. Chem. 262:5404-7
54. 32 transcription factor. Proc. Natl. Acad. Sci. USA 89:3516-20
55. Lipinska, B., Fayet, O., Baird, L., Georgopoulos, C. 1989. Identification, characterization and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J. Bacteriol. 171:1574-84
56. Lipinska, B., King, J., Ang, D., Georgopoulos, C. 1988. Sequence analysis and transcriptional regulation of the Escherichia coli grpE gene, encoding a heat shock protein. Nucleic Acids Res. 16:7545-62
57. 32-independent mechanism of heat-inducible transcription. Nucleic Acids Res. 16:10053-67
58. 70 family: sequence conservation and evolutionary relationships. J. Bacteriol. 174:3843-49
59. Maurizi, M. R., Clark, W. P., Katayama, Y., Rudikoff, S., Pumphrey, J., Bowers, B., Gottesman, S. 1990. Sequence and structure of ClpP, the proteolytic component of the ATP-dependent CIp protease of Escherichia coli. J. Biol. Chem. 265: 12536-45
60. McCarty, J. S., Walker, G. C. 1991. DnaK as a thermometer: threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc. Natl. Acad. Sci. USA 88:9513-17
61. Mizobata, T., Akiyama, Y., Ito, K., Yumoto, N., Kawata, Y. 1992. Effects of the chaperonin GroE on the refolding of tryptophanase from Escherichia coli: refolding is enhanced in the presence of ADP. J. Biol. Chem. 267:17773-79
62. Morimoto, R., Tissières, A., Georgopoulos, C., eds. 1990. Stress Proteins in Biology and Medicine. Cold Spring Harbor, NY: Cold Spring Harbor Lab. 450 pp.
63. Nagai, H., Yano, R., Erickson, J. W., Yura, T. 1990. Transcriptional regulation of the heat shock regulatory gene rpoH in Escherichia coli: involvement of a novel catabolite-sensitive promoter. J. Bacteriol. 172:2710-15
64. 32 synthesis during the heat shock response of Escherichia coli. Proc. Natl. Acad. Sci. USA 88:10515-19
65. 32 synthesis. Biochimie 73:1473-79
66. 32 synthesis. Presented at Meeting on Translational Control, Cold Spring Harbor, N.Y.
67. Narberhaus, F., Bahl, H. 1992. Cloning, sequencing, and molecular analysis of the groESL operon of Clostridium acetobutylicum. J. Bacteriol. 174: 3282-89
68. Neidhardt, F. C., VanBogelen, R. A. 1981. Positive regulatory gene for temperature-controlled proteins in Escherichia coli. Biochem. Biophys. Res. Commun. 100:894-900
69. Neidhardt, F. C., VanBogelen, R. A. 1987. Heat shock response. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, ed. F. C. Neidhardt, J. E. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, H. E. Umbarger, pp. 1334-45. Washington, DC: Am. Soc. Microbiol.
70. Neidhardt, F. C., VanBogelen, R. A., Lau, E. T. 1983. Molecular cloning and expression of a gene that controls the high-temperature regulon of Escherichia coli. J. Bacteriol. 153:597-603
71. Neidhardt, F. C., VanBogelen, R. A., Vaughn, V. 1984. The genetics and regulation ot heat-shock proteins. Annu. Rev. Genet. 18:295-29
72. Neuwald, A. F., York, J. D., Majerus, P. W. 1991. Diverse proteins homologous to inositol monophosphatase. FEBS Lett. 294:16-18
73. 32) in vitro. J. Bacteriol. 175:661-68
74. Obukowicz, M. G., Slater, N. R., Krivi, G. G. 1992. Enhanced heterologous gene expression in novel rpoH mutants of Escherichia coli. Appl. Environ. Microbiol. 58:1511-23
75. Osawa, T., Yura, T. 1981. Effects of reduced amount of RNA polymerase sigma factor on gene expression and growth of Escherichia coli: studies of the rpoD40 (amber) mutation. Mol. Gen. Genet. 184:166-73
76. Paek, K.-H., Walker, G. C. 1987. Escherichia coli dnaK null mutants are inviable at high temperature. J. Bacteriol. 169:283-90
77. Parsell, D. A., Sauer, R. T. 1989. Induction of a heat shock-like response by unfolded protein in Escherichia coli: dependence on protein level not protein degradation. Genes Dev. 3:1226-32
78. Pelham, H. R. B. 1986. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46:959-61
79. Raina, S., Georgopoulos, C. 1990. A new Escherichia coli heat shock gene, hlrC, whose product is essential for viability only at high temperatures. J. Bacteriol. 172:3417-26
80. Schultz, J. E., Latter, G. I., Matin, A. 1988. Differential regulation by cyclic AMP of starvation protein synthesis in Escherichia coli. J. Bacteriol. 170:3903-9
81. Shean, C. S., Gottesman, M. E. 1992. Translation of the prophage λ cI transcript. Cell 70:513-22
82. Shi, W., Zhou, Y., Wild, J., Adler, J., Gross, C. A. 1992. DnaK, DnaJ, and GrpE are required for flagellum synthesis in Escherichia coli. J. Bacteriol. 174:6256-63
83. Skelly, S., Coleman, T., Fu, C.-F., Brot, N., Weissbach, H. 1987. Correlation between the 32-kDa σ factor levels and in vitro expression of Escherichia coli heat shock genes. Proc. Natl. Acad. Sci. USA 84:8365-69
84. Skowyra, D., Georgopoulos, C., Zylicz, M. 1990. The E. coli dnaK gene product, the hsp70 homolog, can reactivate heat-inactivated RNA polymerase in an ATP hydrolysis-dependent manner. Cell 62:939-44
85. Sprengart, M. L., Falscher, H. P., Fuchs, E. 1990. The initiation of translation in E. coli: apparent base pairing between the 16S rRNA and downstream sequences of the mRNA. Nucleic Acids Res. 18:1719-23
86. Squires, C. L., Pedersen, S., Ross, B. M., Squires, C. 1991. ClpB is the Escherichia coli heat shock protein F84.1. J. Bacteriol. 173:4254-62
87. Strauch, K. L., Johnson, K., Beckwith, J. 1989. Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171:2689-96
88. 32. Nature 329: 348-51
89. Straus, D. B., Walter, W. A., Gross, C. A. 1988. Escherichia coli heat shock gene mutants are defective in proteolysis. Genes Dev. 2:1851-58
90. 32 is reduced under conditions of excess heat shock protein production in Escherichia coli. Genes Dev. 3:2003-10
91. 32. Genes Dev. 4:2202-9
92. Taglicht, D., Padan, E., Oppenheim, A. B., Schuldiner, S. 1987. An alkaline shift induces the heat shock response in Escherichia coli. J. Bacteriol. 169: 885-87
93. Tatti, K. M., Moran C. P. Jr. 1985. Utilization of one promoter by two forms of RNA polymerase from Bacillus subtilis. Nature 314: 190-92
94. Taura, T., Kusukawa, N., Yura, T., Ito, K. 1989. Transient shutoff of Escherichia coli heat shock protein synthesis upon temperature shift down. Biochem. Biophys. Res. Commun. 163: 438-43
95. Taylor, W. E., Straus, D. B., Grossman, A. D., Burton, Z. F., Gross, C. A., Burgess, R. 1984. Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38:371-81
96. Tilly, K., Erickson, J., Sharma, S., Georgopoulos, C. 1986. Heat shock regulatory gene rpoH mRNA level increases after heat shock in Escherichia coli. J. Bacteriol. 168:1155-58
97. Tilly, K., McKittrick, N., Zylicz, M., Georgopoulos, C. 1983. The dnaK protein modulates the heat-shock response of Escherichia coli. Cell 34:641-46
98. 32. J. Bacteriol. 171: 1585-89
99. Tobe, T., Ito, K., Yura, T. 1984. Isolation and physical mapping of temperature-sensitive mutants defective in heat-shock induction of proteins in Escherichia coli. Mol. Gen. Genet. 195: 10-16
100. Travers, A. A. 1982. The heat-shock phenomenon in bacteria - a protection against DNA relaxation? In Heat Shock from Bacteria to Man, ed. M. J. Schlesinger, M. Ashbumer, A. Tissieres, pp. 127-30. Cold Spring Harbor, NY: Cold Spring Harbor Lab. 440 pp.
101. Tsuchido, T., VanBogelen, R. A., Neidhardt, F. C. 1986. Heat shock response in Escherichia coli influences cell division. Proc. Natl. Acad. Sci. USA 83:6959-63
102. VanBogelen, R. A., Acton, M. A., Neidhardt, F. C. 1987. Induction of the heat shock regulon does not produce thermotolerance in Escherichia coli. Genes Dev. 1:525-31
103. VanBogelen, R. A., Neidhardt, F. C. 1990. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:5589-93
104. Van Dyk, T. K., Gatenby, A. A., LaRossa, R. A. 1989. Demonstration by genetic suppression of interaction of GroE products with many proteins. Nature 342:451-53
105. 32 in transcription of mini-F replication initiator gene. Proc. Natl. Acad. Sci. USA 84:8849-53
106. 37 RNA polymerase holoenzymes during growth and stationary phases. J. Biol. Chem. 259: 8619-25
107. Wang, Q., Kaguni, J. M. 1989. DnaA protein regulates transcription of the rpoH gene of Escherichia coli. J. Biol. Chem. 264:7338-44
108. Wang, Q., Kaguni, J. M. 1989. A novel sigma factor is involved in expression of the rpoH gene of Escherichia coli. J. Bacteriol. 171: 4248-53
109. Welch, W. J., Georgopoulos, C. 1993. Function and regulation of heat shock proteins. Annu. Rev. Cell Biol. In press
110. Wetzstein, M., Völker, U., Dedio, J., Löbau, S., Zuber, U., et al. 1992. Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis. J. Bacteriol. 174:3300-10
111. Wild, J., Kamath-Loeb, A., Ziegelhoffer, E., Lonetto, M., Kawasaki, Y., 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 89:7139-43
112. Yamamori, T., Ito, K., Nakamura, Y., Yura, T. 1978. Transient regulation of protein synthesis in Escherichia coli upon shift-up of growth temperature. J. Bacteriol. 134:1133-40
113. Yamamori, T., Yura, T. 1980. Temperature-induced synthesis of specific proteins in Escherichia coli: evidence for transcriptional control. J. Bacteriol. 142:843-51
114. Yamamori, T., Yura, T. 1982. Genetic control of heat-shock protein synthesis and its bearing on growth and thermal resistance in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 79:860-64
115. 32 and suppresses temperature-sensitive growth of the rpoH15 mutant of Escherichia coli. J. Bacteriol. 172:2124-30
116. Yura, T., Tobe, T., Ito, K., Osawa, T. 1984. Heat shock regulatory gene (htpR) of Escherichia coli is required for growth at high temperature but is dispensable at low temperature. Proc. Natl. Acad. Sci. USA 81:6803-7
117. Yura, T., Yamamori, T., Osawa, T. 1983. Transcriptional control of heat shock-inducible operons in Escherichia coli. In Microbiology - 1983, ed. D. Schlessinger, pp. 14-17. Washington, DC: Am. Soc. Microbiol.
118. 32 synthesis mediated by alternative mRNA secondary structures: a primary step of the heat shock response in Escherichia coli. Presented at Meeting on Translational Control, Cold Spring Harbor, N.Y.
119. Zeilstra-Ryalls, J., Fayet, O., Georgopoulos, C. 1991. The universally conserved GroE (Hsp60) chaperonins. Annu. Rev. Microbiol. 45: 301-25
120. 32. J. Bacteriol. 170:3640-49
121. 32 with a small deletion in conserved region 3 of σ has reduced affinity for core RNA polymerase. J. Bacteriol. 174:5005-12
122. Zylicz, M., Yamamoto, T., McKittrick, N., Sell, S., Georgopoulos, C. 1985. Purification and properties of the DnaJ replication protein of Escherichia coli. J. Biol. Chem. 260:7591-98