Mutations in the gene encoding the ancillary pilin subunit of the Streptococcus suis srtF cluster result in pili formed by the major subunit only

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Fittipaldi, Nahuel ^a   Takamatsu, Daisuke ^b   Domínguez Punaro, María De La Cruz ^a   Lecours, Marie Pier ^a   Montpetit, Diane ^c   Osaki, Makoto ^b   Sekizaki, Tsutomu ^d   Gottschalk, Marcelo ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^c AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM PILUS; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; GENE MUTATION; GENETIC CODE; GRAM POSITIVE BACTERIUM; NONHUMAN; NONSENSE MUTATION; PATHOGENESIS; SEPSIS; SEROTYPE; STREPTOCOCCUS SUIS; VASCULAR ENDOTHELIUM; ANIMAL; BACTERIAL GENE; CELL ADHESION; ELECTRON MICROSCOPY; GENETICS; MOUSE; MULTIGENE FAMILY; MUTATION; PATHOGENICITY; TRANSGENIC MOUSE; VIRULENCE; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); MURINAE; POSIBACTERIA; STREPTOCOCCUS SUIS; SUIDAE; SUS;

BACTERIAL PROTEIN; FIMBRIA PROTEIN;

ANIMALS; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL ADHESION; FIMBRIAE PROTEINS; GENES, BACTERIAL; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MULTIGENE FAMILY; MUTATION; SEPSIS; STREPTOCOCCUS SUIS; VIRULENCE;

EID: 77649164355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008426     Document Type: Article

References (68)

1. Higgins R, Gottschalk M (2006) Streptococcocal Diseases. In: Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ, eds. Diseases of swine. Ames, Iowa: Blackwell Publishing Professional. pp 769-783.
2. Gottschalk M, Segura M, Xu J (2007) Streptococcus suis infections in humans: the Chinese experience and the situation in North America. Anim Health Res Rev 8: 29-45.
3. Mai NT, Hoa NT, Nga TV, Linh LD, Chau TT, et al. (2008) Streptococcus suis Meningitis in Adults in Vietnam. Clin Infect Dis 46: 659-667.
4. Suankratay C, Intalapaporn P, Nunthapisud P, Arunyingmongkol K, Wilde H (2004) Streptococcus suis meningitis in Thailand. Southeast Asian J Trop Med Public Health 35: 868-876.
5. Yu H, Jing H, Chen Z, Zheng H, Zhu X, et al. (2006) Human Streptococcus suis outbreak, Sichuan, China. Emerg Infect Dis 12: 914-920.
6. Smith HE, Damman M, van der Velde J, Wagenaar F, Wisselink HJ, et al. (1999) Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 67: 1750-1756.
7. Fittipaldi N, Sekizaki T, Takamatsu D, Dominguez-Punaro Mde L, Harel J, et al. (2008) Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol Microbiol 70: 1120-1135.
8. Fittipaldi N, Sekizaki T, Takamatsu D, Harel J, Dominguez-Punaro Mde L, et al. (2008) D-alanylation of lipoteichoic acid contributes to the virulence of Streptococcus suis. Infect Immun 76: 3587-3594.
9. Baums CG, Kaim U, Fulde M, Ramachandran G, Goethe R, et al. (2006) Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infect Immun 74: 6154-6162.
10. Vanier G, Segura M, Friedl P, Lacouture S, Gottschalk M (2004) Invasion of porcine brain microvascular endothelial cells by Streptococcus suis serotype 2. Infect Immun 72: 1441-1449.
11. Dominguez-Punaro MC, Segura M, Plante MM, Lacouture S, Rivest S, et al. (2007) Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. J Immunol 179: 1842-1854.
12. Tenenbaum T, Papandreou T, Gellrich D, Friedrichs U, Seibt A, et al. (2009) Polar bacterial invasion and translocation of Streptococcus suis across the blood-cerebrospinal fluid barrier in vitro. Cell Microbiol 11: 323-336.
13. Fittipaldi N, Gottschalk M, Vanier G, Daigle F, Harel J (2007) Use of selective capture of transcribed sequences to identify genes preferentially expressed by Streptococcus suis upon interaction with porcine brain microvascular endothelial cells. Appl Environ Microbiol 73: 4359-4364.
14. Holden MT, Hauser H, Sanders M, Ngo TH, Cherevach I, et al. (2009) Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLoS ONE 4: e6072.
15. Dramsi S, Trieu-Cuot P, Bierne H (2005) Sorting sortases: a nomenclature proposal for the various sortases of Gram-positive bacteria. Res Microbiol 156: 289-297.
16. Mandlik A, Swierczynski A, Das A, Ton-That H (2008) Pili in Gram-positive bacteria: assembly, involvement in colonization and biofilm development. Trends Microbiol 16: 33-40.
17. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G (2006) Pili in gram-positive pathogens. Nat Rev Microbiol 4: 509-519.
18. Takamatsu D, Nishino H, Ishiji T, Ishii J, Osaki M, et al. (2009) Genetic organization and preferential distribution of putative pilus gene clusters in Streptococcus suis. Vet Microbiol 138: 132-139.
19. Manetti AG, Zingaretti C, Falugi F, Capo S, Bombaci M, et al. (2007) Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol Microbiol 64: 968-983.
20. 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.
21. 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.
22. Bagnoli F, Moschioni M, Donati C, Dimitrovska V, Ferlenghi I, et al. (2008) A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J Bacteriol 190: 5480-5492.
23. Nelson AL, Ries J, Bagnoli F, Dahlberg S, Falker S, et al. (2007) RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol Microbiol 66: 329-340.
24. Rosch JW, Mann B, Thornton J, Sublett J, Tuomanen E (2008) Convergence of regulatory networks on the pilus locus of Streptococcus pneumoniae. Infect Immun 76: 3187-3196.
25. Maisey HC, Quach D, Hensler ME, Liu GY, Gallo RL, et al. (2008) A group B streptococcal pilus protein promotes phagocyte resistance and systemic virulence. FASEB J 22: 1715-1724.
26. Mora M, Bensi G, Capo S, Falugi F, Zingaretti C, et al. (2005) Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci U S A 102: 15641-15646.
27. 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.
28. Maisey HC, Hensler M, Nizet V, Doran KS (2007) Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. J Bacteriol 189: 1464-1467.
29. Nobbs AH, Rosini R, Rinaudo CD, Maione D, Grandi G, et al. (2008) Sortase A utilizes an ancillary protein anchor for efficient cell wall anchoring of pili in Streptococcus agalactiae. Infect Immun 76: 3550-3560.
30. Jacques M, Gottschalk M, Foiry B, Higgins R (1990) Ultrastructural study of surface components of Streptococcus suis. J Bacteriol 172: 2833-2838.
31. Proft T, Baker EN (2009) Pili in Gram-negative and Gram-positive bacteria - structure, assembly and their role in disease. Cell Mol Life Sci 66: 613-635.
32. Budzik JM, Marraffini LA, Schneewind O (2007) Assembly of pili on the surface of Bacillus cereus vegetative cells. Mol Microbiol 66: 495-510.
33. Zahner D, Scott JR (2008) SipA Is Required for Pilus Formation in Streptococcus pyogenes Serotype M3. J Bacteriol 190: 527-535.
34. 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.
35. King SJ, Leigh JA, Heath PJ, Luque I, Tarradas C, et al. (2002) Development of a multilocus sequence typing scheme for the pig pathogen Streptococcus suis: identification of virulent clones and potential capsular serotype exchange. J Clin Microbiol 40: 3671-3680.
36. Chen C, Tang J, Dong W, Wang C, Feng Y, et al. (2007) A Glimpse of Streptococcal Toxic Shock Syndrome from Comparative Genomics of S. suis 2 Chinese Isolates. PLoS ONE 2: e315.
37. Ye C, Zheng H, Zhang J, Jing H, Wang L, et al. (2008) Clinical, Experimental, and Genomic Differences between Intermediately Pathogenic, Highly Pathogenic, and Epidemic Streptococcus suis. J Infect Dis.
38. Rodriguez-Ortega MJ, Luque I, Tarradas C, Barcena JA (2008) Overcoming function annotation errors in the Gram-positive pathogen Streptococcus suis by a proteomics-driven approach. BMC Genomics 9: 588.
39. Scott JR, Zahner D (2006) Pili with strong attachments: Gram-positive bacteria do it differently. Mol Microbiol 62: 320-330.
40. Dominguez-Punaro Mde L, Segura M, Radzioch D, Rivest S, Gottschalk M (2008) Comparison of the susceptibilities of C57BL/6 and A/J mouse strains to Streptococcus suis serotype 2 infection. Infect Immun 76: 3901-3910.
41. Vanier G, Fittipaldi N, Slater JD, Dominguez-Punaro Mde L, Rycroft AN, et al. (2009) New putative virulence factors of Streptococcus suis involved in invasion of porcine brain microvascular endothelial cells. Microb Pathog 46: 13-20.
42. Vanier G, Sekizaki T, Dominguez-Punaro MC, Esgleas M, Osaki M, et al. (2008) Disruption of srtA gene in Streptococcus suis results in decreased interactions with endothelial cells and extracellular matrix proteins. Vet Microbiol 127: 417-424.
43. Osaki M, Takamatsu D, Shimoji Y, Sekizaki T (2002) Characterization of Streptococcus suis genes encoding proteins homologous to sortase of gram-positive bacteria. J Bacteriol 184: 971-982.
44. Basset A, Trzcinski K, Hermos C, O'Brien KL, Reid R, et al. (2007) Association of the Pneumococcal Pilus with Certain Capsular Serotypes but Not with Increased Virulence. J Clin Microbiol 45: 1684-1689.
45. Aguiar SI, Serrano I, Pinto FR, Melo-Cristino J, Ramirez M (2008) The presence of the pilus locus is a clonal property among pneumococcal invasive isolates. BMC Microbiol 8: 41.
46. Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8: 151-156.
47. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual. New York: Cold Spring Harbor Laboratory Press.
48. Warrens AN, Jones MD, Lechler RI (1997) Splicing by overlap extension by PCR using asymmetric amplification: an improved technique for the generation of hybrid proteins of immunological interest. Gene 186: 29-35.
49. Takamatsu D, Osaki M, Sekizaki T (2001) Thermosensitive suicide vectors for gene replacement in Streptococcus suis. Plasmid 46: 140-148.
50. Takamatsu D, Osaki M, Sekizaki T (2001) Construction and characterization of Streptococcus suis-Escherichia coli shuttle cloning vectors. Plasmid 45: 101-113.
51. Roge J, Betton JM (2005) Use of pIVEX plasmids for protein overproduction in Escherichia coli. Microb Cell Fact 4: 18.
52. Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83: 346-356.
53. Li Y, Martinez G, Gottschalk M, Lacouture S, Willson P, et al. (2006) Identification of a surface protein of Streptococcus suis and evaluation of its immunogenic and protective capacity in pigs. Infect Immun 74: 305-312.
54. McNab R, Jenkinson HF (1998) Lipoproteins and other cell-surface associated proteins in streptococci. Methods in Cell Science 20: 209-216.
55. Vecht U, Wisselink HJ, Jellema ML, Smith HE (1991) Identification of two proteins associated with virulence of Streptococcus suis type 2. Infect Immun 59: 3156-3162.
56. Teifel M, Friedl P (1996) Establishment of the permanent microvascular endothelial cell line PBMEC/C1-2 from porcine brains. Exp Cell Res 228: 50-57.
57. Higgins R, Gottschalk M (1990) An update on Streptococcus suis identification. J Vet Diagn Invest 2: 249-252.
58. Slater JD, Allen AG, May JP, Bolitho S, Lindsay H, et al. (2003) Mutagenesis of Streptococcus equi and Streptococcus suis by transposon Tn917. Vet Microbiol 93: 197-206.
59. Berthelot-Herault F, Gottschalk M, Morvan H, Kobisch M (2005) Dilemma of virulence of Streptococcus suis: Canadian isolate 89-1591 characterized as a virulent strain using a standardized experimental model in pigs. Can J Vet Res 69: 236-240.
60. Vecht U, Arends JP, van der Molen EJ, van Leengoed LA (1989) Differences in virulence between two strains of Streptococcus suis type II after experimentally induced infection of newborn germ-free pigs. Am J Vet Res 50: 1037-1043.
61. de Moor CE (1963) Septicaemic Infections in Pigs, Caused by Haemolytic Streptococci of New Lancefield Groups Designated R, S and T. Antonie van Leewenhoek 29: 272-280.
62. Vecht U, Wisselink HJ, van Dijk JE, Smith HE (1992) Virulence of Streptococcus suis type 2 strains in newborn germfree pigs depends on phenotype. Infect Immun 60: 550-556.
63. Segura M, Vadeboncoeur N, Gottschalk M (2002) CD14-dependent and - independent cytokine and chemokine production by human THP-1 monocytes stimulated by Streptococcus suis capsular type 2. Clin Exp Immunol 127: 243-254.
64. Francois B, Gissot V, Ploy MC, Vignon P (1998) Recurrent septic shock due to Streptococcus suis. J Clin Microbiol 36: 2395.
65. Quessy S, Dubreuil JD, Caya M, Higgins R (1995) Discrimination of virulent and avirulent Streptococcus suis capsular type 2 isolates from different geographical origins. Infect Immun 63: 1975-1979.
66. Munier H, Gilles AM, Glaser P, Krin E, Danchin A, et al. (1991) Isolation and characterization of catalytic and calmodulin-binding domains of Bordetella pertussis adenylate cyclase. Eur J Biochem 196: 469-474.
67. Li Y, Gottschalk M, Esgleas M, Lacouture S, Dubreuil JD, et al. (2007) Immunization with recombinant Sao protein confers protection against Streptococcus suis infection. Clin Vaccine Immunol 14: 937-943.
68. Smith HE, Reek FH, Vecht U, Gielkens AL, Smits MA (1993) Repeats in an extracellular protein of weakly pathogenic strains of Streptococcus suis type 2 are absent in pathogenic strains. Infect Immun 61: 3318-3326.