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. 1996 Aug;143(4):1521–1532. doi: 10.1093/genetics/143.4.1521

Overproduction of Three Genes Leads to Camphor Resistance and Chromosome Condensation in Escherichia Coli

K H Hu 1, E Liu 1, K Dean 1, M Gingras 1, W DeGraff 1, N J Trun 1
PMCID: PMC1207417  PMID: 8844142

Abstract

We isolated and characterized three genes, crcA, cspE and crcB, which when present in high copy confer camphor resistance on a cell and suppress mutations in the chromosomal partition gene mukB. Both phenotypes require the same genes. Unlike chromosomal camphor resistant mutants, high copy number crcA, cspE and crcB do not result in an increase in the ploidy of the cells. The cspE gene has been previously identified as a cold shock-like protein with homologues in all organisms tested. We also demonstrate that camphor causes the nucleoids to decondense in vivo and when the three genes are present in high copy, the chromosomes do not decondense. Our results implicate camphor and mukB mutations as interfering with chromosome condensation and high copy crcA, cspE and crcB as promoting or protecting chromosome folding.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Armstrong K. A., Acosta R., Ledner E., Machida Y., Pancotto M., McCormick M., Ohtsubo H., Ohtsubo E. A 37 X 10(3) molecular weight plasmid-encoded protein is required for replication and copy number control in the plasmid pSC101 and its temperature-sensitive derivative pHS1. J Mol Biol. 1984 May 25;175(3):331–348. doi: 10.1016/0022-2836(84)90352-8. [DOI] [PubMed] [Google Scholar]
  3. Av-Gay Y., Aharonowitz Y., Cohen G. Streptomyces contain a 7.0 kDa cold shock like protein. Nucleic Acids Res. 1992 Oct 25;20(20):5478–5478. doi: 10.1093/nar/20.20.5478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  5. Casadaban M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976 Jul 5;104(3):541–555. doi: 10.1016/0022-2836(76)90119-4. [DOI] [PubMed] [Google Scholar]
  6. Chang A. C., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. doi: 10.1128/jb.134.3.1141-1156.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chuang P. T., Albertson D. G., Meyer B. J. DPY-27:a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell. 1994 Nov 4;79(3):459–474. doi: 10.1016/0092-8674(94)90255-0. [DOI] [PubMed] [Google Scholar]
  8. Cohen S. S., Flaks J. G., Barner H. D., Loeb M. R., Lichtenstein J. THE MODE OF ACTION OF 5-FLUOROURACIL AND ITS DERIVATIVES. Proc Natl Acad Sci U S A. 1958 Oct 15;44(10):1004–1012. doi: 10.1073/pnas.44.10.1004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Daneo-Moore L., Higgins M. L. Morphokinetic reaction of Streptococcus faecalis (ATCC 9790) cells to the specific inhibition of macromolecular synthesis: nucleoid condensation on the inhibition of protein synthesis. J Bacteriol. 1972 Mar;109(3):1210–1220. doi: 10.1128/jb.109.3.1210-1220.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Evdokimova V. M., Wei C. L., Sitikov A. S., Simonenko P. N., Lazarev O. A., Vasilenko K. S., Ustinov V. A., Hershey J. W., Ovchinnikov L. P. The major protein of messenger ribonucleoprotein particles in somatic cells is a member of the Y-box binding transcription factor family. J Biol Chem. 1995 Feb 17;270(7):3186–3192. doi: 10.1074/jbc.270.7.3186. [DOI] [PubMed] [Google Scholar]
  11. Funnell B. E., Gagnier L. Partition of P1 plasmids in Escherichia coli mukB chromosomal partition mutants. J Bacteriol. 1995 May;177(9):2381–2386. doi: 10.1128/jb.177.9.2381-2386.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldstein J., Pollitt N. S., Inouye M. Major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A. 1990 Jan;87(1):283–287. doi: 10.1073/pnas.87.1.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hirano T., Mitchison T. J. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell. 1994 Nov 4;79(3):449–458. doi: 10.1016/0092-8674(94)90254-2. [DOI] [PubMed] [Google Scholar]
  14. Jones P. G., VanBogelen R. A., Neidhardt F. C. Induction of proteins in response to low temperature in Escherichia coli. J Bacteriol. 1987 May;169(5):2092–2095. doi: 10.1128/jb.169.5.2092-2095.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LUCKE W. H., SARACHEK A. X-ray inactivation of polyploid Saccharomyces. Nature. 1953 Jun 6;171(4362):1014–1015. doi: 10.1038/1711014a0. [DOI] [PubMed] [Google Scholar]
  16. Marck C. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 1988 Mar 11;16(5):1829–1836. doi: 10.1093/nar/16.5.1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. McClure W. R., Cech C. L. On the mechanism of rifampicin inhibition of RNA synthesis. J Biol Chem. 1978 Dec 25;253(24):8949–8956. [PubMed] [Google Scholar]
  18. Morgan C., Rosenkranz H. S., Carr H. S., Rose H. M. Electron microscopy of chloramphenicol-treated Escherichia coli. J Bacteriol. 1967 Jun;93(6):1987–2002. doi: 10.1128/jb.93.6.1987-2002.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Murray M. T., Schiller D. L., Franke W. W. Sequence analysis of cytoplasmic mRNA-binding proteins of Xenopus oocytes identifies a family of RNA-binding proteins. Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):11–15. doi: 10.1073/pnas.89.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Newkirk K., Feng W., Jiang W., Tejero R., Emerson S. D., Inouye M., Montelione G. T. Solution NMR structure of the major cold shock protein (CspA) from Escherichia coli: identification of a binding epitope for DNA. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5114–5118. doi: 10.1073/pnas.91.11.5114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. OGG J. E., ZELLE M. R. Isolation and characterization of a large cell possibly polyploid strain of Escherichia coli. J Bacteriol. 1957 Oct;74(4):477–484. doi: 10.1128/jb.74.4.477-484.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Oberto J., Drlica K., Rouvière-Yaniv J. Histones, HMG, HU, IHF: Même combat. Biochimie. 1994;76(10-11):901–908. doi: 10.1016/0300-9084(94)90014-0. [DOI] [PubMed] [Google Scholar]
  23. Obokata J., Ohme M., Hayashida N. Nucleotide sequence of a cDNA clone encoding a putative glycine-rich protein of 19.7 kDa in Nicotiana sylvestris. Plant Mol Biol. 1991 Oct;17(4):953–955. doi: 10.1007/BF00037080. [DOI] [PubMed] [Google Scholar]
  24. Peterson C. L. The SMC family: novel motor proteins for chromosome condensation? Cell. 1994 Nov 4;79(3):389–392. doi: 10.1016/0092-8674(94)90247-x. [DOI] [PubMed] [Google Scholar]
  25. Pettijohn D. E. Histone-like proteins and bacterial chromosome structure. J Biol Chem. 1988 Sep 15;263(26):12793–12796. [PubMed] [Google Scholar]
  26. ROPER J. A. Production of heterozygous diploids in filamentous fungi. Experientia. 1952 Jan 15;8(1):14–15. doi: 10.1007/BF02168881. [DOI] [PubMed] [Google Scholar]
  27. Schindelin H., Jiang W., Inouye M., Heinemann U. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5119–5123. doi: 10.1073/pnas.91.11.5119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Skehel P. A., Bartsch D. Characterization of a Y-Box factor from Aplysia californica. Gene. 1994 Aug 5;145(2):231–235. doi: 10.1016/0378-1119(94)90011-6. [DOI] [PubMed] [Google Scholar]
  29. Strunnikov A. V., Larionov V. L., Koshland D. SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol. 1993 Dec;123(6 Pt 2):1635–1648. doi: 10.1083/jcb.123.6.1635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tafuri S. R., Wolffe A. P. DNA binding, multimerization, and transcription stimulation by the Xenopus Y box proteins in vitro. New Biol. 1992 Apr;4(4):349–359. [PubMed] [Google Scholar]
  31. Trun N. J., Gottesman S. Characterization of Escherichia coli mutants with altered ploidy. Res Microbiol. 1991 Feb-Apr;142(2-3):195–200. doi: 10.1016/0923-2508(91)90030-e. [DOI] [PubMed] [Google Scholar]
  32. Trun N. J., Gottesman S., Løbner-Olesen A. Analysis of Escherichia coli mutants with altered DNA content. Cold Spring Harb Symp Quant Biol. 1991;56:353–358. doi: 10.1101/sqb.1991.056.01.042. [DOI] [PubMed] [Google Scholar]
  33. Trun N. J., Gottesman S. On the bacterial cell cycle: Escherichia coli mutants with altered ploidy. Genes Dev. 1990 Dec;4(12A):2036–2047. doi: 10.1101/gad.4.12a.2036. [DOI] [PubMed] [Google Scholar]
  34. Trun N. J., Silhavy T. J. Characterization and in vivo cloning of prlC, a suppressor of signal sequence mutations in Escherichia coli K12. Genetics. 1987 Aug;116(4):513–521. doi: 10.1093/genetics/116.4.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. WON W. D. The production of "giant" cells of Pasteurella pestis by treatment with camphor. J Bacteriol. 1950 Jul;60(1):102–104. doi: 10.1128/jb.60.1.102-104.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Willimsky G., Bang H., Fischer G., Marahiel M. A. Characterization of cspB, a Bacillus subtilis inducible cold shock gene affecting cell viability at low temperatures. J Bacteriol. 1992 Oct;174(20):6326–6335. doi: 10.1128/jb.174.20.6326-6335.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wistow G. Cold shock and DNA binding. Nature. 1990 Apr 26;344(6269):823–824. doi: 10.1038/344823c0. [DOI] [PubMed] [Google Scholar]
  38. Wolffe A. P., Tafuri S., Ranjan M., Familari M. The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol. 1992 Apr;4(4):290–298. [PubMed] [Google Scholar]
  39. Yamanaka K., Mitani T., Feng J., Ogura T., Niki H., Hiraga S. Two mutant alleles of mukB, a gene essential for chromosome partition in Escherichia coli. FEMS Microbiol Lett. 1994 Oct 15;123(1-2):27–31. doi: 10.1111/j.1574-6968.1994.tb07196.x. [DOI] [PubMed] [Google Scholar]
  40. de Oliveira D. E., Seurinck J., Inzé D., Van Montagu M., Botterman J. Differential expression of five Arabidopsis genes encoding glycine-rich proteins. Plant Cell. 1990 May;2(5):427–436. doi: 10.1105/tpc.2.5.427. [DOI] [PMC free article] [PubMed] [Google Scholar]

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