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. 1986 Dec;168(3):1408–1414. doi: 10.1128/jb.168.3.1408-1414.1986

Expression of the adenylate cyclase gene during cell elongation in Escherichia coli K-12.

R Utsumi, M Kawamukai, H Aiba, M Himeno, T Komano
PMCID: PMC213653  PMID: 3536877

Abstract

Expression of the adenylate cyclase gene (cya) in synchronized Escherichia coli cells was investigated by using the cya-lacZ protein and operon fusion plasmids. The regulation of cya expression during the cell cycle is characterized as follows: cya is expressed during cell elongation; expression is repressed during cell division; regulation is exerted at the transcriptional level. To test cya expression during cell elongation, we constructed a plasmid (pLCR1) in which the lacUV5 promoter operator was fused to the structural gene of cya and investigated the effect of cya expression by isopropyl-beta-D-thiogalactopyranoside (IPTG) on the cell division of cells containing pLCR1. By the addition of IPTG, cell division was inhibited and filaments were formed. Such an inhibitory effect was antagonized by adding cyclic GMP to the culture medium and was not observed in the crp mutant.

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Selected References

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  1. Abe M., Tomizawa J. Chromosome replication in Escherichia coli K12 mutant affected in the process of DNA initiation. Genetics. 1971 Sep;69(1):1–15. doi: 10.1093/genetics/69.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aiba H. Autoregulation of the Escherichia coli crp gene: CRP is a transcriptional repressor for its own gene. Cell. 1983 Jan;32(1):141–149. doi: 10.1016/0092-8674(83)90504-4. [DOI] [PubMed] [Google Scholar]
  3. Aiba H., Kawamukai M., Ishihama A. Cloning and promoter analysis of the Escherichia coli adenylate cyclase gene. Nucleic Acids Res. 1983 Jun 11;11(11):3451–3465. doi: 10.1093/nar/11.11.3451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aiba H. Transcription of the Escherichia coli adenylate cyclase gene is negatively regulated by cAMP-cAMP receptor protein. J Biol Chem. 1985 Mar 10;260(5):3063–3070. [PubMed] [Google Scholar]
  5. Backman K., Ptashne M., Gilbert W. Construction of plasmids carrying the cI gene of bacteriophage lambda. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4174–4178. doi: 10.1073/pnas.73.11.4174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casadaban M. J., Chou J., Cohen S. N. In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals. J Bacteriol. 1980 Aug;143(2):971–980. doi: 10.1128/jb.143.2.971-980.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. De Robertis E. M., Jr, Judewicz R. D., Torres H. N. On the control mechanism of bacterial growth by cyclic adenosine 3',5'-monophosphate. Biochem Biophys Res Commun. 1973 Dec 10;55(3):758–764. doi: 10.1016/0006-291x(73)91209-6. [DOI] [PubMed] [Google Scholar]
  9. Emmer M., deCrombrugghe B., Pastan I., Perlman R. Cyclic AMP receptor protein of E. coli: its role in the synthesis of inducible enzymes. Proc Natl Acad Sci U S A. 1970 Jun;66(2):480–487. doi: 10.1073/pnas.66.2.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hartmann R., Höltje J. V., Schwarz U. Targets of penicillin action in Escherichia coli. Nature. 1972 Feb 25;235(5339):426–429. doi: 10.1038/235426a0. [DOI] [PubMed] [Google Scholar]
  11. Kawamukai M., Kishimoto J., Utsumi R., Himeno M., Komano T., Aiba H. Negative regulation of adenylate cyclase gene (cya) expression by cyclic AMP-cyclic AMP receptor protein in Escherichia coli: studies with cya-lac protein and operon fusion plasmids. J Bacteriol. 1985 Nov;164(2):872–877. doi: 10.1128/jb.164.2.872-877.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kumar S., Agarwal K. N., Hazela S. Regulation of envelope-growth in Escherichia coli: horizontal envelope-growth by a process under cyclic AMP control. Indian J Exp Biol. 1981 Jul;19(7):640–642. [PubMed] [Google Scholar]
  13. Kumar S., Prakash N., Sharma V. K. Control of minicell producing cell division by cAMP-receptor protein complex in Escherichia coli. Mol Gen Genet. 1979 Nov;176(3):449–450. doi: 10.1007/BF00333110. [DOI] [PubMed] [Google Scholar]
  14. LENNOX E. S. Transduction of linked genetic characters of the host by bacteriophage P1. Virology. 1955 Jul;1(2):190–206. doi: 10.1016/0042-6822(55)90016-7. [DOI] [PubMed] [Google Scholar]
  15. Louarn J., Patte J., Louarn J. M. Evidence for a fixed termination site of chromosome replication in Escherichia coli K12. J Mol Biol. 1977 Sep 25;115(3):295–314. doi: 10.1016/0022-2836(77)90156-5. [DOI] [PubMed] [Google Scholar]
  16. Matin A., Matin M. K. Cellular levels, excretion, and synthesis rates of cyclic AMP in Escherichia coli grown in continuous culture. J Bacteriol. 1982 Mar;149(3):801–807. doi: 10.1128/jb.149.3.801-807.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matsumoto K., Uno I., Oshima Y., Ishikawa T. Isolation and characterization of yeast mutants deficient in adenylate cyclase and cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2355–2359. doi: 10.1073/pnas.79.7.2355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Movva R. N., Green P., Nakamura K., Inouye M. Interaction of cAMP receptor protein with the ompA gene, a gene for a major outer membrane protein of Escherichia coli. FEBS Lett. 1981 Jun 15;128(2):186–190. doi: 10.1016/0014-5793(81)80077-4. [DOI] [PubMed] [Google Scholar]
  19. Musso R. E., Di Lauro R., Adhya S., de Crombrugghe B. Dual control for transcription of the galactose operon by cyclic AMP and its receptor protein at two interspersed promoters. Cell. 1977 Nov;12(3):847–854. doi: 10.1016/0092-8674(77)90283-5. [DOI] [PubMed] [Google Scholar]
  20. Pastan I. H., Johnson G. S., Anderson W. B. Role of cyclic nucleotides in growth control. Annu Rev Biochem. 1975;44:491–522. doi: 10.1146/annurev.bi.44.070175.002423. [DOI] [PubMed] [Google Scholar]
  21. Pastan I., Johnson G. S. Cyclic AMP and the transformation of fibroblasts. Adv Cancer Res. 1974;19(0):303–329. doi: 10.1016/s0065-230x(08)60057-3. [DOI] [PubMed] [Google Scholar]
  22. Paznokas J. L., Sypherd P. S. Respiratory capacity, cyclic adenosine 3',5'-monophosphate, and morphogenesis of Mucor racemosus. J Bacteriol. 1975 Oct;124(1):134–139. doi: 10.1128/jb.124.1.134-139.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Reddy P., Peterkofsky A., McKenney K. Translational efficiency of the Escherichia coli adenylate cyclase gene: mutating the UUG initiation codon to GUG or AUG results in increased gene expression. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5656–5660. doi: 10.1073/pnas.82.17.5656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roy A., Haziza C., Danchin A. Regulation of adenylate cyclase synthesis in Escherichia coli: nucleotide sequence of the control region. EMBO J. 1983;2(5):791–797. doi: 10.1002/j.1460-2075.1983.tb01502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schwarz U., Ryter A., Rambach A., Hellio R., Hirota Y. Process of cellular division in Escherichia coli: differention of growth zones in the Sacculus. J Mol Biol. 1975 Nov 15;98(4):749–759. doi: 10.1016/s0022-2836(75)80008-8. [DOI] [PubMed] [Google Scholar]
  26. Silverman P. M., Epstein P. M. Cyclic nucleotide metabolism coupled to cytodifferentiation of Blastocladiella emersonii. Proc Natl Acad Sci U S A. 1975 Feb;72(2):442–446. doi: 10.1073/pnas.72.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Thorner J. An essential role for cyclic AMP in growth control: the case for yeast. Cell. 1982 Aug;30(1):5–6. doi: 10.1016/0092-8674(82)90004-6. [DOI] [PubMed] [Google Scholar]
  28. Toda T., Uno I., Ishikawa T., Powers S., Kataoka T., Broek D., Cameron S., Broach J., Matsumoto K., Wigler M. In yeast, RAS proteins are controlling elements of adenylate cyclase. Cell. 1985 Jan;40(1):27–36. doi: 10.1016/0092-8674(85)90305-8. [DOI] [PubMed] [Google Scholar]
  29. Utsumi R., Kawamukai M., Obata K., Morita J., Himeno M., Komano T. Identification of a membrane protein induced concurrently with cell filamentation by cyclic AMP in an Escherichia coli K-12 fic mutant. J Bacteriol. 1983 Jul;155(1):398–401. doi: 10.1128/jb.155.1.398-401.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Utsumi R., Nakamoto Y., Kawamukai M., Himeno M., Komano T. Involvement of cyclic AMP and its receptor protein in filamentation of an Escherichia coli fic mutant. J Bacteriol. 1982 Aug;151(2):807–812. doi: 10.1128/jb.151.2.807-812.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Utsumi R., Tanabe H., Nakamoto Y., Kawamukai M., Sakai H., Himeno M., Komano T., Hirota Y. Inhibitory effect of adenosine 3',5'-phosphate on cell division of Escherichia coli K-12 mutant derivatives. J Bacteriol. 1981 Sep;147(3):1105–1109. doi: 10.1128/jb.147.3.1105-1109.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

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