{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T22:12:17Z","timestamp":1780524737104,"version":"3.54.1"},"reference-count":34,"publisher":"American Society for Microbiology","issue":"12","license":[{"start":{"date-parts":[[1992,6,1]],"date-time":"1992-06-01T00:00:00Z","timestamp":707356800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["J Bacteriol"],"published-print":{"date-parts":[[1992,6]]},"abstract":"<jats:p>Temperature downshifts of Escherichia coli throughout its growth range resulted in transient growth inhibition and a cold shock response consisting of transient induction of several proteins, repression of heat shock proteins, and, despite the growth lag, continued synthesis of proteins involved in transcription and translation. The paradoxical synthesis of the latter proteins, which are normally repressed when growth is arrested, was explored further. First, by means of a nutritional downshift, a natural stringent response was induced in wild-type cells immediately prior to a shift from 37 to 10 degrees C. These cells displayed decreased synthesis of transcriptional and translational proteins and decreased induction of cold shock proteins; also, adaptation for growth at 10 degrees C was delayed, even after restoration of the nutrient supplementation. Next, the contribution of guanosine 5'-triphosphate-3'-diphosphate and guanosine 5'-diphosphate-3'-diphosphate, collectively abbreviated (p)ppGpp, to the alteration in cold shock response was studied with the aid of a mutant strain in which overproduction of these nucleotides can be artificially induced. Induction of (p)ppGpp synthesis immediately prior to shifting this strain from 37 to 10 degrees C produced results differing only in a few details from those described above for nutritional downshift of the wild-type strain. Finally, shifting a relA spoT mutant, which cannot synthesize (p)ppGpp, from 24 to 10 degrees C resulted in a greater induction of the cold shock proteins, increased synthesis of transcriptional and translational proteins, decreased synthesis of a major heat shock protein, and faster adaptation to growth than for the wild-type strain. Our results indicate that the previously reported decrease in the (p)ppGpp level following temperature downshift plays a physiological role in the regulation of gene expression and adaptation for growth at low temperature.<\/jats:p>","DOI":"10.1128\/jb.174.12.3903-3914.1992","type":"journal-article","created":{"date-parts":[[2016,11,4]],"date-time":"2016-11-04T20:13:33Z","timestamp":1478290413000},"page":"3903-3914","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":104,"title":["Function of a relaxed-like state following temperature downshifts in Escherichia coli"],"prefix":"10.1128","volume":"174","author":[{"given":"P G","family":"Jones","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor 48109-0620."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"M","family":"Cashel","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor 48109-0620."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"G","family":"Glaser","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor 48109-0620."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"F C","family":"Neidhardt","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor 48109-0620."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"p_1","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1128\/JB.134.3.861-874.1978","article-title":"Effects of low temperature on in vivo and in vitro protein synthesis in Escherichia coli and Pseudomonas fluorescens","volume":"134","author":"Broeze R. J.","year":"1978","unstructured":"Broeze , R. J. , C. J. Solomon , and D. H. Pope . 1978 . Effects of low temperature on in vivo and in vitro protein synthesis in Escherichia coli and Pseudomonas fluorescens . J. Bacteriol. 134 : 861 - 874 .","journal-title":"J. Bacteriol."},{"key":"p_2","unstructured":"Cashel M. and K. E. Rudd. 1987. The stringent response p. 1410-1438. In F. C. Neidhardt J. L. Ingraham K. B. Low B. Magasanik M. Schaechter and H. E. Umbarger (ed.) Escherichia coli and Salmonella typhimurium: cellular and molecular biology vol. 2. American Society for Microbiology Washington D.C."},{"key":"p_3","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1016\/0006-291X(83)91688-1","article-title":"Effects of aminoglycoside antibiotics on the coupling of protein and RNA synthesis in Escherichia coli","volume":"112","author":"Cortay J. C.","year":"1983","unstructured":"Cortay , J. C. , and A. J. Cozzone . 1983 . Effects of aminoglycoside antibiotics on the coupling of protein and RNA synthesis in Escherichia coli . Biochem. Biophys. Res. Commun. 112 : 801 - 808 .","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"p_4","doi-asserted-by":"crossref","first-page":"7322","DOI":"10.1073\/pnas.85.19.7322","article-title":"Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II box","volume":"85","author":"Didier D. K.","year":"1988","unstructured":"Didier , D. K. , J. Schiffenbauer , S. L. Woulfe , M. Zacheis , and B. D. Schwatz . 1988 . Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II box . Proc. Natl. Acad. Sci. USA 85 : 7322 - 7326 .","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"p_5","unstructured":".Gage D. Unpublished data."},{"key":"p_6","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1073\/pnas.87.1.283","article-title":"Major cold shock protein of Escherichia coli","volume":"87","author":"Goldstein J.","year":"1990","unstructured":"Goldstein , J. , N. S. Pollitt , and M. Inouye . 1990 . Major cold shock protein of Escherichia coli . Proc. Natl. Acad. Sci. USA 87 : 283 - 287 .","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"p_7","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1038\/344682a0","article-title":"Transcriptional silencing and thermoregulation of gene expression in Escherichia coli","volume":"344","author":"Goransson M.","year":"1990","unstructured":"Goransson , M. , B. Sonden , P. Nilsson , B. Dagberg , K. Fosman , K. Emanuelsson , and B. E. Uhlin . 1990 . Transcriptional silencing and thermoregulation of gene expression in Escherichia coli . Nature (London) 344 : 682 - 685 .","journal-title":"Nature (London)"},{"key":"p_8","doi-asserted-by":"crossref","first-page":"2336","DOI":"10.1128\/JB.172.5.2336-2342.1990","article-title":"Identification of a second promoter for the metY-nusA-infB operon of Escherichia coli","volume":"172","author":"Granston A. E.","year":"1990","unstructured":"Granston , A. E. , D. L. Thompson , and D. I. Friedman . 1990 . Identification of a second promoter for the metY-nusA-infB operon of Escherichia coli . J. Bacteriol. 172 : 2336 - 2342 .","journal-title":"J. Bacteriol."},{"key":"p_9","unstructured":"Grunberg-Manago M. 1987. Regulation of the expression of aminoacyl-tRNA synthetases and translation factors p. 1386-1409. In F. C. Neidhardt J. L. Ingraham K. B. Low B. Magasanik M. Schaechter and H. E. Umbarger (ed.) Escherichia coli and Salmonella typhimurium: cellular and molecular biology vol. 2. American Society for Microbiology Washington D.C."},{"key":"p_10","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1128\/JB.139.1.185-194.1979","article-title":"Levels of major proteins of Escherichia coli during growth at different temperatures","volume":"139","author":"Herendeen S. L.","year":"1979","unstructured":"Herendeen , S. L. , R. A. VanBogelen , and F. C. Neidhardt . 1979 . Levels of major proteins of Escherichia coli during growth at different temperatures . J. Bacteriol. 139 : 185 - 194 .","journal-title":"J. Bacteriol."},{"key":"p_11","doi-asserted-by":"crossref","first-page":"5991","DOI":"10.1016\/S0021-9258(19)67695-7","article-title":"Escherichia coli ppGpp synthetase II activity requires spoT","volume":"266","author":"Hernandez V. J.","year":"1991","unstructured":"Hernandez , V. J. , and H. Bremer . 1991 . Escherichia coli ppGpp synthetase II activity requires spoT . J. Biol. Chem. 266 : 5991 - 5999 .","journal-title":"J. Biol. Chem."},{"key":"p_12","doi-asserted-by":"crossref","first-page":"2092","DOI":"10.1128\/JB.169.5.2092-2095.1987","article-title":"Induction of proteins in response to low temperature in Eschenichia coli","volume":"169","author":"Jones P. G.","year":"1987","unstructured":"Jones , P. G. , R. A. VanBogelen , and F. C. Neidhardt . 1987 . Induction of proteins in response to low temperature in Eschenichia coli . J. Bacteriol. 169 : 2092 - 2095 .","journal-title":"J. Bacteriol."},{"key":"p_13","doi-asserted-by":"crossref","first-page":"10907","DOI":"10.1073\/pnas.88.23.10907","article-title":"Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS","volume":"88","author":"La Teana A.","year":"1991","unstructured":"La Teana , A. , A. Brandi , M. Falconi , R. Spurio , C. L. Pon , and C. 0. Gualerzi . 1991 . Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS . Proc. Natl. Acad. Sci. USA 88 : 10907 - 10911 .","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"p_14","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1007\/BF00327639","article-title":"Correlation between RNA synthesis and ppGpp content in Eschenichia coli during temperature shifts","volume":"192","author":"Mackow E. R.","year":"1983","unstructured":"Mackow , E. R. , and F. N. Chang . 1983 . Correlation between RNA synthesis and ppGpp content in Eschenichia coli during temperature shifts . Mol. Gen. Genet. 192 : 5 - 9 .","journal-title":"Mol. Gen. Genet."},{"key":"p_15","doi-asserted-by":"crossref","first-page":"9122","DOI":"10.1016\/S0021-9258(18)60500-9","article-title":"Protein sequences encoded by the relA and the spoT genes of Eschenichia coli are interrelated","volume":"264","author":"Metzger S.","year":"1989","unstructured":"Metzger , S. , E. Sarubbi , G. Glaser , and M. Cashel . 1989 . Protein sequences encoded by the relA and the spoT genes of Eschenichia coli are interrelated . J. Biol. Chem. 264 : 9122 - 9125 .","journal-title":"J. Biol. Chem."},{"key":"p_16","doi-asserted-by":"crossref","first-page":"21146","DOI":"10.1016\/S0021-9258(19)30059-6","article-title":"Characterization of the reL41 mutation and a comparison of the relAl with new relA null alleles in Escherichia coli","volume":"264","author":"Metzger S.","year":"1989","unstructured":"Metzger , S. , G. Schreiber , E. Aizenman , M. Cashel , and G. Glaser . 1989 . Characterization of the reL41 mutation and a comparison of the relAl with new relA null alleles in Escherichia coli . J. Biol. Chem. 264 : 21146 - 21152 .","journal-title":"J. Biol. Chem."},{"key":"p_17","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1128\/jb.119.3.736-747.1974","article-title":"Culture medium for enterobacteria","volume":"119","author":"Neidhardt F. C.","year":"1974","unstructured":"Neidhardt , F. C. , P. L. Bloch , and D. F. Smith . 1974 . Culture medium for enterobacteria . J. Bacteriol. 119 : 736 - 747 .","journal-title":"J. Bacteriol."},{"key":"p_18","unstructured":"Neidhardt F. C. J. L. Ingraham and M. Schaechter. 1990. Physiology of the bacterial cell: a molecular approach. Sinauer Associates Inc. Sunderland Mass."},{"key":"p_19","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1128\/JB.84.2.331-339.1962","article-title":"Damage and derepression in Escherichia coli resulting from growth at low temperatures","volume":"84","author":"Ng H.","year":"1962","unstructured":"Ng , H. , J. L. Ingraham , and A. G. Marr . 1962 . Damage and derepression in Escherichia coli resulting from growth at low temperatures . J. Bacteriol. 84 : 331 - 339 .","journal-title":"J. Bacteriol."},{"key":"p_20","doi-asserted-by":"crossref","first-page":"4007","DOI":"10.1016\/S0021-9258(19)41496-8","article-title":"High resolution of two dimensional electrophoresis of proteins","volume":"250","author":"O'Farrell P. H.","year":"1975","unstructured":"O'Farrell , P. H. 1975 . High resolution of two dimensional electrophoresis of proteins . J. Biol. Chem. 250 : 4007 - 4021 .","journal-title":"J. Biol. Chem."},{"key":"p_21","doi-asserted-by":"crossref","first-page":"2252","DOI":"10.1016\/S0021-9258(19)69769-3","article-title":"Stringent control of RNA synthesis in the absence of guanosine 5'-diphosphate-3'-diphosphate","volume":"256","author":"Pao C. C.","year":"1981","unstructured":"Pao , C. C. , and B. T. Dyess . 1981 . Stringent control of RNA synthesis in the absence of guanosine 5'-diphosphate-3'-diphosphate . J. Biol. Chem. 256 : 2252 - 2257 .","journal-title":"J. Biol. Chem."},{"key":"p_22","doi-asserted-by":"crossref","first-page":"6493","DOI":"10.1128\/jb.171.12.6493-6502.1989","article-title":"Effect of variation of charged and uncharged tRNATrP levels on ppGpp synthesis in Escherichia coli","volume":"171","author":"Rojiani M. V.","year":"1989","unstructured":"Rojiani , M. V. , H. Jakubowski , and E. Goldman . 1989 . Effect of variation of charged and uncharged tRNATrP levels on ppGpp synthesis in Escherichia coli . J. Bacteriol. 171 : 6493 - 6502 .","journal-title":"J. Bacteriol."},{"key":"p_23","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.1073\/pnas.87.4.1511","article-title":"Relationship between protein synthesis and concentrations of charged and uncharged tRNA Trp in Escherichia coli","volume":"87","author":"Rojiani M. V.","year":"1990","unstructured":"Rojiani , M. V. , H. Jakubowski , and E. Goldman . 1990 . Relationship between protein synthesis and concentrations of charged and uncharged tRNA Trp in Escherichia coli . Proc. Natl. Acad. Sci. USA 87 : 1511 - 1515 .","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"p_24","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1128\/JB.151.2.879-887.1982","article-title":"Temperature dependence of RNA synthesis parameters in Escherichia coli","volume":"151","author":"Ryals J.","year":"1982","unstructured":"Ryals , J. , R. Little , and H. Bremer . 1982 . Temperature dependence of RNA synthesis parameters in Escherichia coli . J. Bacteriol. 151 : 879 - 887 .","journal-title":"J. Bacteriol."},{"key":"p_25","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1128\/JB.151.3.1261-1268.1982","article-title":"Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate","volume":"151","author":"Ryals J.","year":"1982","unstructured":"Ryals , J. , R. Little , and H. Bremer . 1982 . Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate . J. Bacteriol. 151 : 1261 - 1268 .","journal-title":"J. Bacteriol."},{"key":"p_26","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/0378-1119(88)90514-8","article-title":"Two human genes isolated by a novel method encode DNA-binding proteins containing a region of homology","volume":"73","author":"Sakura H.","year":"1988","unstructured":"Sakura , H. , T. Maekawa , F. Imamoto , K. Yusuda , and S. Ishii . 1988 . Two human genes isolated by a novel method encode DNA-binding proteins containing a region of homology . Gene 73 : 499 - 507 .","journal-title":"Gene"},{"key":"p_27","doi-asserted-by":"crossref","first-page":"3760","DOI":"10.1016\/S0021-9258(19)67860-9","article-title":"Overexpression of the relA gene in Escherichia coli","volume":"266","author":"Schreiber G.","year":"1991","unstructured":"Schreiber , G. , S. Metzger , E. Aizenman , S. Roza , M. Cashel , and G. Glaser . 1991 . Overexpression of the relA gene in Escherichia coli . J. Biol. Chem. 266 : 3760 - 3767 .","journal-title":"J. Biol. Chem."},{"key":"p_28","doi-asserted-by":"crossref","first-page":"9028","DOI":"10.1073\/pnas.87.22.9028","article-title":"Xenopus Y-box transcription factors: molecular cloning, functional analysis, and developmental regulation","volume":"87","author":"Tafuri S. R.","year":"1990","unstructured":"Tafuri , S. R. , and A. P. Wolffe . 1990 . Xenopus Y-box transcription factors: molecular cloning, functional analysis, and developmental regulation . Proc. Natl. Acad. Sci. USA 87 : 9028 - 9032 .","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"p_29","doi-asserted-by":"crossref","first-page":"7289","DOI":"10.1093\/nar\/13.20.7289","article-title":"Attenuation and processing of RNA from the rpsO-pnp transcription unit of Escherichia coli","volume":"13","author":"Takata R.","year":"1985","unstructured":"Takata , R. , T. Mukai , and K. Hori . 1985 . Attenuation and processing of RNA from the rpsO-pnp transcription unit of Escherichia coli . Nucleic Acids Res. 13 : 7289 - 7296 .","journal-title":"Nucleic Acids Res."},{"key":"p_30","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1016\/0006-291X(89)92155-4","article-title":"Transient shut off of Eschenichia coli heat shock protein synthesis upon temperature shift down","volume":"163","author":"Taura T.","year":"1989","unstructured":"Taura , T. , N. Kusukawa , T. Yura , and K. Ito . 1989 . Transient shut off of Eschenichia coli heat shock protein synthesis upon temperature shift down . Biochem. Biophys. Res. Commun. 163 : 438 - 443 .","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"p_31","doi-asserted-by":"crossref","first-page":"5589","DOI":"10.1073\/pnas.87.15.5589","article-title":"Ribosomes as sensors of heat and cold shock in Escherichia coli","volume":"87","author":"VanBogelen R. A.","year":"1990","unstructured":"VanBogelen , R. A. , and F. C. Neidhardt . 1990 . Ribosomes as sensors of heat and cold shock in Escherichia coli . Proc. Natl. Acad. Sci. USA 87 : 5589 - 5593 .","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"p_32","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1128\/JB.130.1.212-222.1977","article-title":"Physiological regulation of a decontrolled lac operon","volume":"130","author":"Wanner B. L.","year":"1977","unstructured":"Wanner , B. L. , R. Kodaira , and F. C. Neidhardt . 1977 . Physiological regulation of a decontrolled lac operon . J. Bacteriol. 130 : 212 - 222 .","journal-title":"J. Bacteriol."},{"key":"p_33","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1038\/344823c0","article-title":"Cold shock and DNA binding","volume":"344","author":"Wistow G.","year":"1990","unstructured":"Wistow , G. 1990 . Cold shock and DNA binding . Nature (London) 344 : 823 - 824 . (Letter tc the editor.)","journal-title":"Nature (London)"},{"key":"p_34","doi-asserted-by":"crossref","first-page":"5980","DOI":"10.1016\/S0021-9258(19)67694-5","article-title":"Residual guanosine 3',5'-bispyrophosphate synthetic activity of reLA null mutants can be eliminated by spoT null mutations","volume":"266","author":"Xiao H.","year":"1991","unstructured":"Xiao , H. , M. Kalman , K. Ikehara , S. Zemel , G. Glaser , and M. Cashel . 1991 . Residual guanosine 3',5'-bispyrophosphate synthetic activity of reLA null mutants can be eliminated by spoT null mutations . J. Biol. Chem. 266 : 5980 - 5990 .","journal-title":"J. Biol. Chem."}],"container-title":["Journal of Bacteriology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/jb.174.12.3903-3914.1992","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/jb.174.12.3903-3914.1992","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,29]],"date-time":"2021-07-29T17:47:00Z","timestamp":1627580820000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/jb.174.12.3903-3914.1992"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1992,6]]},"references-count":34,"journal-issue":{"issue":"12","published-print":{"date-parts":[[1992,6]]}},"alternative-id":["10.1128\/jb.174.12.3903-3914.1992"],"URL":"https:\/\/doi.org\/10.1128\/jb.174.12.3903-3914.1992","relation":{},"ISSN":["0021-9193","1098-5530"],"issn-type":[{"value":"0021-9193","type":"print"},{"value":"1098-5530","type":"electronic"}],"subject":[],"published":{"date-parts":[[1992,6]]},"assertion":[{"value":"2021-02-02","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}