Single Cell Stochastic Regulation of Pilus Phase Variation by an Attenuation-like Mechanism

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Danne, Camille ^a,b,c   Dubrac, Sarah ^a,b   Trieu Cuot, Patrick ^a,b   Dramsi, Shaynoor ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIMBRIA PROTEIN;

BACTERIAL ENDOCARDITIS; BIOSYNTHESIS; FIMBRIA; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; STATISTICS; STREPTOCOCCUS; ULTRASTRUCTURE;

ENDOCARDITIS, BACTERIAL; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; STOCHASTIC PROCESSES; STREPTOCOCCUS;

EID: 84893754582     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003860     Document Type: Article

References (46)

1. Klein RS, Recco RA, Catalano MT, Edberg SC, Casey JI, et al. (1977) Association of Streptococcus bovis with carcinoma of the colon. N Engl J Med 297: 800-802.
2. Abdulamir AS, Hafidh RR, Bakar FA, (2010) Molecular detection, quantification, and isolation of Streptococcus gallolyticus bacteria colonizing colorectal tumors: inflammation-driven potential of carcinogenesis via IL-1, COX-2, and IL-8. Mol Cancer 9: 249.
3. Boleij A, Schaeps RM, Tjalsma H, (2009) Association between Streptococcus bovis and colon cancer. J Clin Microbiol 47: 516.
4. Boleij A, Muytjens CM, Bukhari SI, Cayet N, Glaser P, et al. (2011) Novel clues on the specific association of Streptococcus gallolyticus subsp gallolyticus with colorectal cancer. J Infect Dis 203: 1101-1109.
5. Rusniok C, Couve E, Da Cunha V, El Gana R, Zidane N, et al. (2010) Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol 192: 2266-2276.
6. Sillanpaa J, Nallapareddy SR, Qin X, Singh KV, Muzny DM, et al. (2009) A collagen-binding adhesin, Acb, and ten other putative MSCRAMM and pilus family proteins of Streptococcus gallolyticus subsp. gallolyticus (Streptococcus bovis Group, biotype I). J Bacteriol 191: 6643-6653.
7. Danne C, Entenza JM, Mallet A, Briandet R, Debarbouille M, et al. (2011) Molecular characterization of a Streptococcus gallolyticus genomic island encoding a pilus involved in endocarditis. J Infect Dis 204: 1960-1970.
8. Takai S, Yanagawa R, Kitamura Y, (1980) pH-dependent adhesion of piliated Corynebacterium renale to bovine bladder epithelial cells. Infect Immun 28: 669-674.
9. Ito H, Ono E, Yanagawa R, (1987) Comparison of surface hydrophobicity of piliated and non-piliated clones of Corynebacterium renale and Corynebacterium pilosum. Vet Microbiol 14: 165-171.
10. Hiramune T, Onishi K, Kikuchi N, Yanagawa R, (1991) Phase variation of pili of Corynebacterium pilosum. Zentralbl Veterinarmed B 38: 303-305.
11. Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, et al. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci U S A 103: 2857-2862.
12. Basset A, Turner KH, Boush E, Sayeed S, Dove SL, et al. (2011) Expression of the type 1 pneumococcal pilus is bistable and negatively regulated by the structural component RrgA. Infect Immun 79: 2974-2983.
13. De Angelis G, Moschioni M, Muzzi A, Pezzicoli A, Censini S, et al. (2011) The Streptococcus pneumoniae pilus-1 displays a biphasic expression pattern. PLoS One 6: e21269.
14. Nakata M, Koller T, Moritz K, Ribardo D, Jonas L, et al. (2009) Mode of expression and functional characterization of FCT-3 pilus region-encoded proteins in Streptococcus pyogenes serotype M49. Infect Immun 77: 32-44.
15. Bourgogne A, Thomson LC, Murray BE, (2007) Bicarbonate enhances expression of the endocarditis and biofilm associated pilus locus, ebpR-ebpABC, in Enterococcus faecalis. BMC Microbiol 10: 17.
16. Nallapareddy SR, Singh KV, Sillanpaa J, Garsin DA, Hook M, et al. (2006) Endocarditis and biofilm-associated pili of Enterococcus faecalis. J Clin Invest 116: 2799-2807.
17. Danne C, Dramsi S, (2012) Pili of gram-positive bacteria: roles in host colonization. Res Microbiol 163: 645-658.
18. Basset A, Turner KH, Boush E, Sayeed S, Dove SL, et al. (2011) An epigenetic switch mediates bistable expression of the type 1 pilus genes in Streptococcus pneumoniae. J Bacteriol 194: 1088-1091.
19. Hava DL, Hemsley CJ, Camilli A, (2003) Transcriptional regulation in the Streptococcus pneumoniae rlrA pathogenicity islet by RlrA. J Bacteriol 185: 413-421.
20. Nallapareddy SR, Singh KV, Sillanpaa J, Zhao M, Murray BE, (2011) Relative contributions of Ebp Pili and the collagen adhesin ace to host extracellular matrix protein adherence and experimental urinary tract infection by Enterococcus faecalis OG1RF. Infect Immun 79: 2901-2910.
21. Molhoj M, Degan FD, (2004) Leader sequences are not signal peptides. Nat Biotechnol 22: 1502.
22. Boleij A, Roelofs R, Danne C, Bellais S, Dramsi S, et al. (2012) Selective Antibody Response to Streptococcus gallolyticus Pilus Proteins in Colorectal Cancer Patients. Cancer Prevention Research 5: 260-265.
23. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G, (2006) Pili in gram-positive pathogens. Nat Rev Microbiol 4: 509-519.
24. Maione D, Margarit I, Rinaudo CD, Masignani V, Mora M, et al. (2005) Identification of a universal Group B streptococcus vaccine by multiple genome screen. Science 309: 148-150.
25. Yanofsky C, (1981) Attenuation in the control of expression of bacterial operons. Nature 289: 751-758.
26. Naville M, Gautheret D, (2009) Transcription attenuation in bacteria: theme and variations. Brief Funct Genomic Proteomic 8: 482-492.
27. Hallet B, (2001) Playing Dr Jekyll and Mr Hyde: combined mechanisms of phase variation in bacteria. Curr Opin Microbiol 4: 570-581.
28. van der Woude MW, (2011) Phase variation: how to create and coordinate population diversity. Curr Opin Microbiol 14: 205-211.
29. Dawid S, Barenkamp SJ, St Geme JW 3rd, (1999) Variation in expression of the Haemophilus influenzae HMW adhesins: a prokaryotic system reminiscent of eukaryotes. Proc Natl Acad Sci U S A 96: 1077-1082.
30. van Ham SM, van Alphen L, Mooi FR, van Putten JP, (1993) Phase variation of Haemophilus influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell 73: 1187-1196.
31. Zaleski P, Wojciechowski M, Piekarowicz A, (2005) The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. Microbiology 151: 3361-3369.
32. Ritz D, Lim J, Reynolds CM, Poole LB, Beckwith J, (2001) Conversion of a peroxiredoxin into a disulfide reductase by a triplet repeat expansion. Science 294: 158-160.
33. Silverman M, Zieg J, Hilmen M, Simon M, (1979) Phase variation in Salmonella: genetic analysis of a recombinational switch. Proc Natl Acad Sci U S A 76: 391-395.
34. Linton D, Gilbert M, Hitchen PG, Dell A, Morris HR, et al. (2000) Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol Microbiol 37: 501-514.
35. Stern A, Brown M, Nickel P, Meyer TF, (1986) Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47: 61-71.
36. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
37. Moxon R, Bayliss C, Hood D, (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40: 307-333.
38. Moxon ER, Rainey PB, Nowak MA, Lenski RE, (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4: 24-33.
39. Eisenstein BI, (1981) Phase variation of type 1 fimbriae in Escherichia coli is under transcriptional control. Science 214: 337-339.
40. Murphy GL, Connell TD, Barritt DS, Koomey M, Cannon JG, (1989) Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56: 539-547.
41. Bayliss CD, Hoe JC, Makepeace K, Martin P, Hood DW, et al. (2008) Neisseria meningitidis escape from the bactericidal activity of a monoclonal antibody is mediated by phase variation of lgtG and enhanced by a mutator phenotype. Infect Immun 76: 5038-5048.
42. Tauseef I, Ali YM, Bayliss CD, (2013) Phase Variation of PorA, a Major Outer Membrane Protein, Mediates Escape of Bactericidal Antibodies by Neisseria meningitidis. Infect Immun 81: 1374-1380.
43. Kuipers OP, de Ruyter PGGA, Kleerebezem M, de Vos WM, (1998) Quorum sensing-controlled gene expression in lactic acid bacteria. Journal of Biotechnology 64: 15-21.
44. Konto-Ghiorghi Y, Mairey E, Mallet A, Dumenil G, Caliot E, et al. (2009) Dual role for pilus in adherence to epithelial cells and biofilm formation in Streptococcus agalactiae. PLoS Pathog 5: e1000422.
45. Dubrac S, Boneca IG, Poupel O, Msadek T, (2007) New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J Bacteriol 189: 8257-8269.
46. Dramsi S, Caliot E, Bonne I, Guadagnini S, Prevost MC, et al. (2006) Assembly and role of pili in group B streptococci. Mol Microbiol 60: 1401-1413.