Abstract
In vitro, anionic phospholipids can reactivate inactivated DnaA protein, which is essential for initiation of DNA replication at the oriC site of Escherichia coli [Sekimizu, K. & Kornberg, A. (1988) J. Biol. Chem. 263, 7131-7135]. Mutations in the pgsA gene (encoding phosphatidylglycerophosphate synthase) limit the synthesis of the major anionic phospholipids and lead to arrest of cell growth. We report herein that a mutation in the rnhA gene (encoding RNase H) that bypasses the need for the DnaA protein through induction of constitutive stable DNA replication [Kogoma, T. & von Meyenburg, K. (1983) EMBO J. 2, 463-468] also suppressed the growth arrest phenotype of a pgsA mutant. The maintenance of plasmids dependent on an oriC site for replication, and therefore DnaA protein, was also compromised under conditions of limiting anionic phospholipid synthesis. These results provide support for the involvement of anionic phospholipids in normal initiation of DNA replication at oriC in vivo by the DnaA protein.
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Selected References
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- Abe M. Replication of ColE1 plasmid deoxyribonucleic acid in a thermosensitive dnaA mutant of Escherichia coli. J Bacteriol. 1980 Mar;141(3):1024–1030. doi: 10.1128/jb.141.3.1024-1030.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Asai Y., Katayose Y., Hikita C., Ohta A., Shibuya I. Suppression of the lethal effect of acidic-phospholipid deficiency by defective formation of the major outer membrane lipoprotein in Escherichia coli. J Bacteriol. 1989 Dec;171(12):6867–6869. doi: 10.1128/jb.171.12.6867-6869.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bachmann B. J., Low K. B. Linkage map of Escherichia coli K-12, edition 6. Microbiol Rev. 1980 Mar;44(1):1–56. doi: 10.1128/mr.44.1.1-56.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bell R. M., Burns D. J. Lipid activation of protein kinase C. J Biol Chem. 1991 Mar 15;266(8):4661–4664. [PubMed] [Google Scholar]
- Cox M. M., Lehman I. R. Enzymes of general recombination. Annu Rev Biochem. 1987;56:229–262. doi: 10.1146/annurev.bi.56.070187.001305. [DOI] [PubMed] [Google Scholar]
- Crooke E., Castuma C. E., Kornberg A. The chromosome origin of Escherichia coli stabilizes DnaA protein during rejuvenation by phospholipids. J Biol Chem. 1992 Aug 25;267(24):16779–16782. [PubMed] [Google Scholar]
- Firshein W. Role of the DNA/membrane complex in prokaryotic DNA replication. Annu Rev Microbiol. 1989;43:89–120. doi: 10.1146/annurev.mi.43.100189.000513. [DOI] [PubMed] [Google Scholar]
- Fralick J. A., Lark K. G. Evidence for the involvement of unsaturated fatty acids in initiating chromosome replication in Escherichia coli. J Mol Biol. 1973 Nov 5;80(3):459–475. doi: 10.1016/0022-2836(73)90416-6. [DOI] [PubMed] [Google Scholar]
- Frey J., Chandler M., Caro L. The initiation of chromosome replication in a dnaAts46 and a dnaA+ strain at various temperatures. Mol Gen Genet. 1981;182(2):364–366. doi: 10.1007/BF00269686. [DOI] [PubMed] [Google Scholar]
- Gopalakrishnan A. S., Chen Y. C., Temkin M., Dowhan W. Structure and expression of the gene locus encoding the phosphatidylglycerophosphate synthase of Escherichia coli. J Biol Chem. 1986 Jan 25;261(3):1329–1338. [PubMed] [Google Scholar]
- Heacock P. N., Dowhan W. Alteration of the phospholipid composition of Escherichia coli through genetic manipulation. J Biol Chem. 1989 Sep 5;264(25):14972–14977. [PubMed] [Google Scholar]
- Heacock P. N., Dowhan W. Construction of a lethal mutation in the synthesis of the major acidic phospholipids of Escherichia coli. J Biol Chem. 1987 Sep 25;262(27):13044–13049. [PubMed] [Google Scholar]
- Hendrick J. P., Wickner W. SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J Biol Chem. 1991 Dec 25;266(36):24596–24600. [PubMed] [Google Scholar]
- Horiuchi T., Maki H., Maruyama M., Sekiguchi M. Identification of the dnaQ gene product and location of the structural gene for RNase H of Escherichia coli by cloning of the genes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3770–3774. doi: 10.1073/pnas.78.6.3770. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horiuchi T., Maki H., Sekiguchi M. RNase H-defective mutants of Escherichia coli: a possible discriminatory role of RNase H in initiation of DNA replication. Mol Gen Genet. 1984;195(1-2):17–22. doi: 10.1007/BF00332717. [DOI] [PubMed] [Google Scholar]
- Hwang D. S., Crooke E., Kornberg A. Aggregated dnaA protein is dissociated and activated for DNA replication by phospholipase or dnaK protein. J Biol Chem. 1990 Nov 5;265(31):19244–19248. [PubMed] [Google Scholar]
- Kanaya S., Crouch R. J. DNA sequence of the gene coding for Escherichia coli ribonuclease H. J Biol Chem. 1983 Jan 25;258(2):1276–1281. [PubMed] [Google Scholar]
- Kogoma T., Skarstad K., Boye E., von Meyenburg K., Steen H. B. RecA protein acts at the initiation of stable DNA replication in rnh mutants of Escherichia coli K-12. J Bacteriol. 1985 Aug;163(2):439–444. doi: 10.1128/jb.163.2.439-444.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kogoma T., von Meyenburg K. The origin of replication, oriC, and the dnaA protein are dispensable in stable DNA replication (sdrA) mutants of Escherichia coli K-12. EMBO J. 1983;2(3):463–468. doi: 10.1002/j.1460-2075.1983.tb01445.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kusters R., Dowhan W., de Kruijff B. Negatively charged phospholipids restore prePhoE translocation across phosphatidylglycerol-depleted Escherichia coli inner membranes. J Biol Chem. 1991 May 15;266(14):8659–8662. [PubMed] [Google Scholar]
- Lill R., Dowhan W., Wickner W. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell. 1990 Jan 26;60(2):271–280. doi: 10.1016/0092-8674(90)90742-w. [DOI] [PubMed] [Google Scholar]
- Løbner-Olesen A., Atlung T., Rasmussen K. V. Stability and replication control of Escherichia coli minichromosomes. J Bacteriol. 1987 Jun;169(6):2835–2842. doi: 10.1128/jb.169.6.2835-2842.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miki T., Ebina Y., Kishi F., Nakazawa A. Organization of the lexA gene of Escherichia coli and nucleotide sequence of the regulatory region. Nucleic Acids Res. 1981 Feb 11;9(3):529–543. doi: 10.1093/nar/9.3.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parks W. A., Couper C. L., Low R. L. Phosphatidylcholine and phosphatidylethanolamine enhance the activity of the mammalian mitochondrial endonuclease in vitro. J Biol Chem. 1990 Feb 25;265(6):3436–3439. [PubMed] [Google Scholar]
- Raetz C. R., Dowhan W. Biosynthesis and function of phospholipids in Escherichia coli. J Biol Chem. 1990 Jan 25;265(3):1235–1238. [PubMed] [Google Scholar]
- Rando R. R. Regulation of protein kinase C activity by lipids. FASEB J. 1988 May;2(8):2348–2355. doi: 10.1096/fasebj.2.8.3282960. [DOI] [PubMed] [Google Scholar]
- Ryter A. Association of the nucleus and the membrane of bacteria: a morphological study. Bacteriol Rev. 1968 Mar;32(1):39–54. doi: 10.1128/br.32.1.39-54.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sankaran K., Wu H. C. Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J Biol Chem. 1994 Aug 5;269(31):19701–19706. [PubMed] [Google Scholar]
- Sekimizu K., Kornberg A. Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J Biol Chem. 1988 May 25;263(15):7131–7135. [PubMed] [Google Scholar]
- Sekimizu K., Yung B. Y., Kornberg A. The dnaA protein of Escherichia coli. Abundance, improved purification, and membrane binding. J Biol Chem. 1988 May 25;263(15):7136–7140. [PubMed] [Google Scholar]
- Skarstad K., Boye E. Perturbed chromosomal replication in recA mutants of Escherichia coli. J Bacteriol. 1988 Jun;170(6):2549–2554. doi: 10.1128/jb.170.6.2549-2554.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stuitje A. R., Meijer M. Maintenance and incompatibility of plasmids carrying the replication origin of the Escherichia coli chromosome: evidence for a control region of replication between oriC and asnA. Nucleic Acids Res. 1983 Aug 25;11(16):5775–5791. doi: 10.1093/nar/11.16.5775. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Torrey T. A., Atlung T., Kogoma T. dnaA suppressor (dasF) mutants of Escherichia coli are stable DNA replication (sdrA/rnh) mutants. Mol Gen Genet. 1984;196(2):350–355. doi: 10.1007/BF00328070. [DOI] [PubMed] [Google Scholar]
- Torrey T. A., Kogoma T. Genetic analysis of constitutive stable DNA replication in rnh mutants of Escherichia coli K12. Mol Gen Genet. 1987 Jul;208(3):420–427. doi: 10.1007/BF00328133. [DOI] [PubMed] [Google Scholar]
- Wang Y., MacDonald J. I., Kent C. Regulation of CTP:phosphocholine cytidylyltransferase in HeLa cells. Effect of oleate on phosphorylation and intracellular localization. J Biol Chem. 1993 Mar 15;268(8):5512–5518. [PubMed] [Google Scholar]
- Witkin E. M. RecA protein in the SOS response: milestones and mysteries. Biochimie. 1991 Feb-Mar;73(2-3):133–141. doi: 10.1016/0300-9084(91)90196-8. [DOI] [PubMed] [Google Scholar]
- Wu H. C., Tokunaga M., Tokunaga H., Hayashi S., Giam C. Z. Posttranslational modification and processing of membrane lipoproteins in bacteria. J Cell Biochem. 1983;22(3):161–171. doi: 10.1002/jcb.240220305. [DOI] [PubMed] [Google Scholar]
- Yoshida S., Tamiya-Koizumi K., Kojima K. Interaction of DNA polymerases with phospholipids. Biochim Biophys Acta. 1989 Jan 23;1007(1):61–66. doi: 10.1016/0167-4781(89)90130-9. [DOI] [PubMed] [Google Scholar]
- Yung B. Y., Kornberg A. Membrane attachment activates dnaA protein, the initiation protein of chromosome replication in Escherichia coli. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7202–7205. doi: 10.1073/pnas.85.19.7202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Massy B., Fayet O., Kogoma T. Multiple origin usage for DNA replication in sdrA(rnh) mutants of Escherichia coli K-12. Initiation in the absence of oriC. J Mol Biol. 1984 Sep 15;178(2):227–236. doi: 10.1016/0022-2836(84)90141-4. [DOI] [PubMed] [Google Scholar]
- de Vrije T., de Swart R. L., Dowhan W., Tommassen J., de Kruijff B. Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature. 1988 Jul 14;334(6178):173–175. doi: 10.1038/334173a0. [DOI] [PubMed] [Google Scholar]