SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae

Molecular Microbiology

Volumn 81, Issue 3, 2011, Pages 676-688

  Minnen, Anita ^a   Attaiech, Laetitia ^a   Thon, Maria ^a   Gruber, Stephan ^b   Veening, Jan Willem ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; CIPROFLOXACIN; CONDENSIN; DNA BINDING PROTEIN; GYRASE INHIBITOR; NORFLOXACIN; NOVOBIOCIN; PROTEIN PARB; STREPTOCOCCUS PNEUMONIAE CONDENSIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; CENTROMERE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA REPLICATION ORIGIN; DNA SEQUENCE; GENE DELETION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; DNA-BINDING PROTEINS; GENE DELETION; ORIGIN RECOGNITION COMPLEX; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); STREPTOCOCCUS PNEUMONIAE;

EID: 79960708973     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07722.x     Document Type: Article

References (62)

1. Avery, A.T., MacLeod, C.M., and McCarty, M. (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a desoxyribonucleic acid fraction isolated from Pneumococcus type III. J Exp Med 79: 137-158.
2. Baerends, R.J., Smits, W.K., de Jong, A., Hamoen, L.W., Kok, J., and Kuipers, O.P. (2004) Genome2D: a visualization tool for the rapid analysis of bacterial transcriptome data. Genome Biol 5: R37.
3. Bloom, K., and Joglekar, A. (2010) Towards building a chromosome segregation machine. Nature 463: 446-456.
4. Bouthier de la Tour, C., Toueille, M., Jolivet, E., Nguyen, H.H., Servant, P., Vannier, F., and Sommer, S. (2009) The Deinococcus radiodurans SMC protein is dispensable for cell viability yet plays a role in DNA folding. Extremophiles 13: 827-837.
5. Britton, R.A., Lin, D.C., and Grossman, A.D. (1998) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12: 1254-1259.
6. Dagkessamanskaia, A., Moscoso, M., Henard, V., Guiral, S., Overweg, K., Reuter, M., etal. (2004) Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51: 1071-1086.
7. Danilova, O., Reyes-Lamothe, R., Pinskaya, M., Sherratt, D., and Possoz, C. (2007) MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 65: 1485-1492.
8. Eberhardt, A., Wu, L.J., Errington, J., Vollmer, W., and Veening, J.W. (2009) Cellular localization of choline-utilization proteins in Streptococcus pneumoniae using novel fluorescent reporter systems. Mol Microbiol 74: 395-408.
9. Errington, J. (2010) From spores to antibiotics via the cell cycle. Microbiology 156: 1-13.
10. Fadda, D., Santona, A., D'Ulisse, V., Ghelardini, P., Ennas, M.G., Whalen, M.B., and Massidda, O. (2007) Streptococcus pneumoniae DivIVA: localization and interactions in a MinCD-free context. J Bacteriol 189: 1288-1298.
11. Ferrandiz, M.J., Martin-Galiano, A.J., Schvartzman, J.B., and de la Campa, A.G. (2010) The genome of Streptococcus pneumoniae is organized in topology-reacting gene clusters. Nucleic Acids Res 38: 3570-3581.
12. Fogel, M.A., and Waldor, M.K. (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20: 3269-3282.
13. Gasc, A.M., Giammarinaro, P., Ton-Hoang, B., Geslin, P., van der Giezen, M., and Sicard, M. (1997) Structural organization of the Streptococcus pneumoniae chromosome and relatedness of penicillin-sensitive and -resistant strains in type 9V. Microb Drug Resist 3: 65-72.
14. Gerdes, K., Howard, M., and Szardenings, F. (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141: 927-942.
15. Glaser, P., Sharpe, M.E., Raether, B., Perego, M., Ohlsen, K., and Errington, J. (1997) Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev 11: 1160-1168.
16. Graumann, P.L., and Knust, T. (2009) Dynamics of the bacterial SMC complex and SMC-like proteins involved in DNA repair. Chromosome Res 17: 265-275.
17. Gruber, S., and Errington, J. (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137: 685-696.
18. Guthlein, C., Wanner, R.M., Sander, P., Bottger, E.C., and Springer, B. (2008) A mycobacterial smc null mutant is proficient in DNA repair and long-term survival. J Bacteriol 190: 452-456.
19. Halfmann, A., Kovacs, M., Hakenbeck, R., and Bruckner, R. (2007) Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol Microbiol 66: 110-126.
20. Hendriksen, W.T., Bootsma, H.J., Estevao, S., Hoogenboezem, T., de Jong, A., de Groot, R., etal. (2008) CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization. J Bacteriol 190: 590-601.
21. Hoskins, J., Alborn, W.E., Jr, Arnold, J., Blaszczak, L.C., Burgett, S., DeHoff, B.S., etal. (2001) Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 183: 5709-5717.
22. Hudson, D.F., Marshall, K.M., and Earnshaw, W.C. (2009) Condensin: architect of mitotic chromosomes. Chromosome Res 17: 131-144.
23. Hui, M.P., Galkin, V.E., Yu, X., Stasiak, A.Z., Stasiak, A., Waldor, M.K., and Egelman, E.H. (2010) ParA2, a Vibrio cholerae chromosome partitioning protein, forms left-handed helical filaments on DNA. Proc Natl Acad Sci USA 107: 4590-4595.
24. Ireton, K., Gunther, N.W., and Grossman, A.D. (1994) spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176: 5320-5329.
25. Jun, S., and Mulder, B. (2006) Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA 103: 12388-12393.
26. Jun, S., and Wright, A. (2010) Entropy as the driver of chromosome segregation. Nat Rev Microbiol 8: 600-607.
27. Katayama, T., Ozaki, S., Keyamura, K., and Fujimitsu, K. (2010) Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8: 163-170.
28. Kloosterman, T.G., Hendriksen, W.T., Bijlsma, J.J., Bootsma, H.J., van Hijum, S.A., Kok, J., etal. (2006) Regulation of glutamine and glutamate metabolism by GlnR and GlnA in Streptococcus pneumoniae. J Biol Chem 281: 25097-25109.
29. Kornberg, A., and Baker, T.A. (1992) DNA Replication. New York: W.H. Freeman and Co.
30. Lanie, J.A., Ng, W.L., Kazmierczak, K.M., Andrzejewski, T.M., Davidsen, T.M., Wayne, K.J., etal. (2007) Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189: 38-51.
31. Leenhouts, K., Buist, G., Bolhuis, A., ten Berge, A., Kiel, J., Mierau, I., etal. (1996) A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol Gen Genet 253: 217-224.
32. Lin, D.C., Levin, P.A., and Grossman, A.D. (1997) Bipolar localization of a chromosome partition protein in Bacillus subtilis. Proc Natl Acad Sci USA 94: 4721-4726.
33. Lindow, J.C., Britton, R.A., and Grossman, A.D. (2002) Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo. J Bacteriol 184: 5317-5322.
34. Livny, J., Yamaichi, Y., and Waldor, M.K. (2007) Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189: 8693-8703.
35. Lynch, J.P., 3rd, and Zhanel, G.G. (2010) Streptococcus pneumoniae: epidemiology and risk factors, evolution of antimicrobial resistance, and impact of vaccines. Curr Opin Pulm Med 16: 217-225.
36. Martin, B., Garcia, P., Castanie, M.P., and Claverys, J.P. (1995) The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol Microbiol 15: 367-379.
37. Mascarenhas, J., Soppa, J., Strunnikov, A.V., and Graumann, P.L. (2002) Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 21: 3108-3118.
38. Mitchell, A.M., and Mitchell, T.J. (2010) Streptococcus pneumoniae: virulence factors and variation. Clin Microbiol Infect 16: 411-418.
39. Moriya, S., Tsujikawa, E., Hassan, A.K., Asai, K., Kodama, T., and Ogasawara, N. (1998) A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 29: 179-187.
40. Mott, M.L., and Berger, J.M. (2007) DNA replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 5: 343-354.
41. Murray, H., and Errington, J. (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135: 74-84.
42. Nasmyth, K., and Haering, C.H. (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525-558.
43. O'Brien, K.L., Wolfson, L.J., Watt, J.P., Henkle, E., Deloria-Knoll, M., McCall, N., etal. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893-902.
44. Onn, I., Heidinger-Pauli, J.M., Guacci, V., Unal, E., and Koshland, D.E. (2008) Sister chromatid cohesion: a simple concept with a complex reality. Annu Rev Cell Dev Biol 24: 105-129.
45. van der Poll, T., and Opal, S.M. (2009) Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 374: 1543-1556.
46. Ptacin, J.L., Lee, S.F., Garner, E.C., Toro, E., Eckart, M., Comolli, L.R., etal. (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12: 791-798.
47. Reyes-Lamothe, R., Wang, X., and Sherratt, D. (2008) Escherichia coli and its chromosome. Trends Microbiol 16: 238-245.
48. Ringgaard, S., van Zon, J., Howard, M., and Gerdes, K. (2009) Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 106: 19369-19374.
49. Salje, J. (2010) Plasmid segregation: how to survive as an extra piece of DNA. Crit Rev Biochem Mol Biol 45: 296-317.
50. Sambrook, J. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
51. Schofield, W.B., Lim, H.C., and Jacobs-Wagner, C. (2010) Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J 29: 3068-3081.
52. Scholefield, G., Veening, J.W., and Murray, H. (2011) DnaA and ORC: more than DNA replication initiators. Trends Cell Biol 21: 188-194.
53. Sebert, M.E., Palmer, L.M., Rosenberg, M., and Weiser, J.N. (2002) Microarray-based identification of htrA, a Streptococcus pneumoniae gene that is regulated by the CiaRH two-component system and contributes to nasopharyngeal colonization. Infect Immun 70: 4059-4067.
54. Soppa, J., Kobayashi, K., Noirot-Gros, M.F., Oesterhelt, D., Ehrlich, S.D., Dervyn, E., etal. (2002) Discovery of two novel families of proteins that are proposed to interact with prokaryotic SMC proteins, and characterization of the Bacillus subtilis family members ScpA and ScpB. Mol Microbiol 45: 59-71.
55. Sullivan, N.L., Marquis, K.A., and Rudner, D.Z. (2009) Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137: 697-707.
56. Terzaghi, B.E., and Sandine, W.E. (1975) Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 29: 807-813.
57. Thanbichler, M. (2009) Closing the ring: a new twist to bacterial chromosome condensation. Cell 137: 598-600.
58. Toro, E., and Shapiro, L. (2010) Bacterial chromosome organization and segregation. Cold Spring Harb Perspect Biol 2: a000349.
59. Weiser, J.N. (2010) The pneumococcus: why a commensal misbehaves. J Mol Med 88: 97-102.
60. Yu, W., Herbert, S., Graumann, P.L., and Gotz, F. (2010) Contribution of SMC (structural maintenance of chromosomes) and SpoIIIE to chromosome segregation in Staphylococci. J Bacteriol 192: 4067-4073.
61. Zakrzewska-Czerwinska, J., Jakimowicz, D., Zawilak-Pawlik, A., and Messer, W. (2007) Regulation of the initiation of chromosomal replication in bacteria. FEMS Microbiol Rev 31: 378-387.
62. Zhao, S., and Fernald, R.D. (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12: 1047-1064.