The replication checkpoint control in Bacillus subtilis: Identification of a novel RTP-binding sequence essential for the replication fork arrest after induction of the stringent response

Molecular Microbiology

Volumn 31, Issue 6, 1999, Pages 1665-1679

  Autret, S ^a,c   Levine, A ^a   Vannier, F ^a   Fujita, Y ^b   Seror S J ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b FUKUYAMA UNIVERSITY   (Japan)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; REPLICATION TERMINATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL GENETICS; BINDING SITE; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA FOOTPRINTING; DNA HYBRIDIZATION; DNA REPLICATION; DNA SYNTHESIS; GENE DELETION; GENE MAPPING; GENE SEQUENCE; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DNA BINDING;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 0032991566     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01299.x     Document Type: Article

References (58)

1. Ahn, K.S., Malo, M.S., Smith, M.T., and Wake, R.G. (1993) Autoregulation of the gene encoding the replication terminator protein of Bacillus subtilis. Gene 132: 7-13.
2. Aviv, M., Giladi, H., Schreiber, G., Oppenheim, A.B., and Glaser, G. (1994) Expression of the genes coding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation. Mol Microbiol 14: 1021-1031.
3. Baker, T.A. (1995) Replication arrest. Cell 80: 521-524.
4. Boulanger, P., le Maire, M., Bonhivers, M., Dubois, S., Desmadril, M., and Letellier, L. (1996) Purification and structural and functional characterization of FhuA, a transporter of the Escherichia coli outer membrane. Biochemistry 25: 14216-14224.
5. Bruand, C., Ehrlich, S.D., and Janniere, L. (1991) Unidirectional theta replication of the structurally stable Enterococcus faecalis plasmid pAMβ1. EMBO J 10: 2171-2177.
6. Bussiere, D.E., Bastia, D., and White, S.W. (1995) Crystal structure of the replication terminator protein from B. subtilis at 2.6Ȧ. Cell 80: 651-660.
7. Carrigan, C.M., Haarsma, J.A., Smith, M.T., and Wake, R.G. (1987) Sequence features of the replication terminus of the Bacillus subtilis chromosome. Nucleic Acids Res 15: 8501-8509.
8. Carrigan, C.M., Pack, R.A., Smith, M.T., and Wake, R.G. (1991) Normal terC-region of the Bacillus subtilis chromosome acts in a polar manner to arrest the clockwise replication fork. J Mol Biol 222: 197-207.
9. Cashel, M., Gentry, D.R., Hernandez, V.J., and Vinella, D. (1996) The stringent response. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, 2nd edn. Neidhardt, F.C., Ingraham, J.L., Low, K.B., Magasanik, B., Schaechter, M., and Umbarger, H.E. (eds). Washington, DC: American Society for Microbiology Press, pp. 1410-1438.
10. Chiaramello, A.E., and Zyskind, J.W. (1990) Coupling of DNA replication to growth rate in Escherichia coli: a possible role for guanosine tetraphosphate. J Bacteriol 172: 2013-2019.
11. Dijkwel, P.A., Vaughn, J.P., and Hamlin, J.L. (1991) Mapping of replication initiation sites in mammalian genomes by two-dimensional gel analysis: stabilization and enrichment of replication intermediates by isolation on the nuclear matrix. Mol Cell Biol 11: 3850-3859.
12. Franks, A.H., Griffiths, A.A., and Wake, R.G. (1995) Identification and characterization of new DNA replication terminators in Bacillus subtilis. Mol Microbiol 17: 13-23.
13. Gentry, D.R., and Cashel, M. (1996) Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol Microbiol 19: 1373-1384.
14. S, is positively regulated by ppGpp. J Bacteriol 175: 7982-7989.
15. Harris, B.Z., Kaiser, D., and Singer, M. (1998) The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes Dev 12: 1022-1035.
16. Henckes, G., Harper, F., Levine, A., Vannier, F., and Séror, S.J. (1989) Over-replication of the origin region in the dnaB37 mutant of Bacillus subtilis: post-initiation control of chromosomal replication. Proc Natl Acad Sci USA 86: 8660-8663.
17. Herman, A., and Wegrzyn, G. (1995). Effect of increased ppGpp concentration on DNA replication of different replicons in Escherichia coli. J Basic Microbiol 35: 33-39.
18. Hernandez, V.J., and Bremer, H. (1991) Escherichia coli ppGpp synthetase II activity requires spoT. J Biol Chem 266: 5991-5999.
19. Hill, T.M. (1992) Arrest of bacterial DNA replication. Annu Rev Microbiol 46: 603-633.
20. Horiuchi, T., Hidaka, M., Akiyama, M., Nishitani, H., and Sekiguchi, M. (1987) Replication intermediate of a hybrid plasmid carrying the replication terminus (ter) site of R6K as revealed by agarose gel electrophoresis. Mol Gen Genet 210: 394-398.
21. Kaul, S., Mohanty, B.K., Sahoo, T., Patel, I., Khan, S.A., and Bastia, D. (1994) The replication terminator protein of the Gram-positive bacterium Bacillus subtilis functions as a polar contrahelicase in Gram-negative Escherichia coli. Proc Natl Acad Sci USA 91: 11143-11147.
22. Khatri, G.S., MacAllister, T., Sista, P.R., and Bastia, D. (1989) The replication terminator protein of E. coli is a DNA sequence-specific contra-helicase. Cell 59: 667-674.
23. Kralicek, A.V., Wilson, P.K., Ralston, G.B., Wake, R.G., and King, G.F. (1997) Reorganization of the terminator DNA upon binding replication terminator protein: implications for the functional replication fork arrest complex. Nucleic Acids Res 25: 590-596.
24. Kunst, F., Msadek, T., Bignon, J., and Rapoport, G. (1994) The DegS/DegU and ComP/ComA two-component systems are part of a network controlling degradative enzyme synthesìs and competence in Bacillus subtilis. Res Microbiol 145: 393-402.
25. Langley, D.B., Smith, M.T., Lewis, P.J., and Wake, R.G. (1993) Protein-nucleoside contacts in the interaction between the replication terminator protein of Bacillus subtilis and the DNA terminator. Mol Microbiol 10: 771-779.
26. Laurent, S.J., and Vannier, F. (1973) Temperature-sensitive initiation of chromosome replication in a mutant of Bacillus subtilis. J Bacteriol 114: 474-484.
27. Lee, E.H., Kornberg, A., Hidaka, M., Kobayashi, T., and Horiuchi, T. (1989) Escherichia coli replication termination protein impedes the action of helicases. Proc Natl Acad Sci USA 86: 9104-9108.
28. Levine, A., Henckes, G., Vannier, F., and Séror, S.J. (1987) Chromosomal initiation in Bacillus subtilis may involve two closely linked origins. Mol Gen Genet 208: 37-44.
29. Levine, A., Vannier, F., Dehbi, M., Henckes, G., and Séror, S.J. (1991) The stringent response blocks DNA replication outside the ori region in Bacillus subtilis and at the origin in Escherichia coli. J Mol Biol 219: 605-613.
30. Levine, A., Autret, S., and Séror, S.J. (1995) A checkpoint involving RTP, the replication terminator protein, arrests replication downstream ot the origin during the stringent response in Bacillus subtilis. Mol Microbiol 15: 287-295.
31. Lewis, P.J., Ralston, G.B., Christopherson, R.I., and Wake, R.G. (1990) Identification of the replication terminator protein binding sites in the terminus region of the Bacillus subtilis chromosome and stoichiometry of the binding. J Mol Biol 214: 73-84.
32. Manna, A.C., Pai, K.S., Bussiere, D.E., White, S.W., and Bastia, D. (1996a) The dimer-dimer interaction surface of the replication terminator protein of Bacillus subtilis and termination of DNA replication. Proc Natl Acad Sci USA 93: 3253-3258.
33. Manna, A.C., Pai, K.S., Bussiere, D.E., Davies, C., White, S.W., and Bastia, D. (1996b) Helicase-contrahelicase interaction and the mechanism of termination of DNA replication. Cell 87: 881-891.
34. Mohanty, B.K., Sahoo, T., and Bastia, D. (1996) The relation between sequence-specific termination of DNA replication and transcription. EMBO J 15: 2530-2539.
35. Ninnemann, O., Koch, C., and Kahmann, R. (1992) The E. coli fis promoter is subject to stringent control and autoregulation. EMBO J 11: 1075-1083.
36. Nishimura, A., Moriya, S., Ukai, H., Nagai, K., Wachi, M., and Yamada, Y. (1997) Diadenosine 5′, 5‴-P1,P4 - tetraphosphate (Ap4A) controls the timing of cell division in Escherichia coli. Genes Cells 2: 401-413.
37. Ogawa, T., and Okazaki, T. (1991) Concurrent transcription from the gid and mioC promoters activates replication of an Escherichia coli minichromosome. Mol Gen Genet 230: 193-200.
38. Otter, T., King, S.M., and Witman, G.M. (1987) A two step procedure for efficient electrotransfer of both high molecular weight (400 000) and low molecular weight (20 000) proteins. Anal Biochem 162: 370-377.
39. Pai, K.S., Bussiere, D.E., Wang, F., Hutchison, III, C.A., White, S.W., and Bastia, D. (1996) The structure and function of the replication protein of Bacillus subtilis: identification of the 'winged helix' DNA-binding domain. EMBO J 15: 3164-3173.
40. Rokeach, L.A., Kassavetis, G.A., and Zyskind, J.W. (1987) RNA Polymerase pauses in vitro within the Escherichia coli origin of replication at the same sites where termination occurs in vivo. J Biol Chem 262: 7264-7272.
41. Sahoo, T., Mohanty, B.D., Patel, I., and Bastia, D. (1995a) Termination of DNA replication in vitro: requirement for stereospecific interaction between two dimers of the replication terminator protein of Bacillus subtilis and with the terminator site to elicit polar contrahelicase and fork impedance. EMBO J 14: 619-628.
42. Sahoo, T., Mohanty, B.K., Lobert, M., Manna, A.C., and Bastia, D. (1995b) The contrahelicase activities of the replication terminator proteins of Escherichia coli and Bacillus subtilis are helicase-specific and impede both helicase translocation and authentic DNA unwinding. J Biol Chem 270: 29138-29144.
43. Schreiber, G., Metzger, S., Aizenman, E., Roza, S., Cashel, M., and Glaser, G. (1991) Overexpression of the relA gene in Escherichia coli. J Biol Chem 266: 3760-3767.
44. Schreiber, G., Ron, E.Z., and Glaser, G. (1995) ppGpp-mediated regulation of DNA replication and cell division in Escherichia coli. Curr Microbiol 30: 27-32.
45. Séror, S.J., Vannier, F., Levine, A., and Henckes, G. (1986) Stringent control of initiation of chromosomal replication in B. subtilis. Nature 321: 709-710.
46. Séror, S.J., Levine, A., and Vannier, F. (1991) Post-initiation control of chromosomal replication in Bacillus subtilis: a mechanism for limiting over-replication or duplicating key growth and sporulation genes? Res Microbiol 142: 861-867.
47. Sharpe, M.E., and Errington, J. (1998) A fixed distance for separation of newly replicated copies of oriC in Bacillus subtilis: implications for co-ordination of chromosome segregation and cell division. Mol Microbiol 28: 981-990.
48. Smith, M.T., and Wake, R.G. (1988) DNA sequence requirements of replication fork arrest at terC in Bacillus subtilis. J Bacteriol 170: 4083-4090.
49. Smith, M.T., and Wake, R.G. (1992) Definition and polarity of action of DNA replication terminators in Bacillus subtilis. J Mol Biol 227: 648-657.
50. Smith, M.T., Langley, D.B., Young, P.A., and Wake, R.G. (1994) The minimal sequence needed to define a functional DNA terminator in Bacillus subtilis. J Mol Biol 241: 335-340.
51. Smith, M.T., de Vries, C.J., Langley, D.B., King, G.F., and Wake, R.G. (1996) The Bacillus subtilis DNA replication terminator. J Mol Biol 260: 54-69.
52. Spizizen, J. (1958) Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA 48: 1072-1078.
53. Stragier, P., Bonamy, C., and Karmazyn-Campelli, C. (1988) Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell 52: 697-704.
54. Szalewska-Palasz, A., Wegrzyn, A., Herman, A., and Wergrzyn, G. (1994) The mechanism of the stringent control of λ plasmid DNA replication. EMBO J 13: 5779-5785.
55. Wegrzyn, G., and Taylor, K. (1992) Inheritance of the replication complex by one of two daughter copies during λ plasmid replication in Escherichia coli. J Mol Biol 226: 681-688.
56. Wendrich, T.M., and Marahiel, M.A. (1997) Cloning and characterization of a relA/spoThomologue from Bacillus subtilis. Mol Microbiol 26: 65-79.
57. Wröbel, B., and Wegrzyn, G. (1998) Replication regulation of ColE1-like plasmids in amino acid-starved Escherichia coli. Plasmid 39: 48-62.
58. Yoshida, K., Sano, H., Miwa, Y., Ogasawara, N., and Fujita, Y. (1994) Cloning and nucleotide sequencing of a 15 kb region of the Bacillus subtilis genome containing the iol operon. Microbiology 140: 2289-2298.