Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-22T08:40:47.415Z Has data issue: false hasContentIssue false

Surface-associated and secreted factors of Streptococcus suis in epidemiology, pathogenesis and vaccine development

Published online by Cambridge University Press:  29 June 2009

Christoph Georg Baums*
Affiliation:
Institut für Mikrobiologie, Zentrum für Infektionsmedizin, Stiftung Tierärztliche Hochschule Hannover, D-30173 Hannover, Germany
Peter Valentin-Weigand
Affiliation:
Institut für Mikrobiologie, Zentrum für Infektionsmedizin, Stiftung Tierärztliche Hochschule Hannover, D-30173 Hannover, Germany
*
*Corresponding author. E-mail: [email protected]

Abstract

Streptococcus suis is an invasive porcine pathogen associated with meningitis, arthritis, bronchopneumonia and other diseases. The pathogen constitutes a major health problem in the swine industry worldwide. Furthermore, S. suis is an important zoonotic agent causing meningitis and other diseases in humans exposed to pigs or pork. Current knowledge on pathogenesis is limited, despite the enormous amount of data generated by ‘omics’ research. Accordingly, immunprophylaxis (in pigs) is hampered by lack of a cross-protective vaccine against virulent strains of this diverse species. This review focuses on bacterial factors, both surface-associated and secreted ones, which are considered to contribute to S. suis interaction(s) with host factors and cells. Factors are presented with respect to (i) their identification and features, (ii) their distribution among S. suis and (iii) their significance for virulence, immune response and vaccination. This review also shows the enormous progress made in research on S. suis over the last few years, and it emphasizes the numerous challenging questions remaining to be answered in the future.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aarestrup, FM, Jorsal, SE and Jensen, NE (1998). Serological characterization and antimicrobial susceptibility of Streptococcus suis isolates from diagnostic samples in Denmark during 1995 and 1996. Veterinary Microbiology 60: 5966.CrossRefGoogle ScholarPubMed
Allen, AG, Bolitho, S, Lindsay, H, Khan, S, Bryant, C, Norton, P, Ward, P, Leigh, J, Morgan, J, Riches, H, Eastty, S and Maskell, D (2001). Generation and characterization of a defined mutant of Streptococcus suis lacking suilysin. Infection and Immunity 69: 27322735.CrossRefGoogle ScholarPubMed
Allen, AG, Lindsay, H, Seilly, D, Bolitho, S, Peters, SE and Maskell, DJ (2004). Identification and characterisation of hyaluronate lyase from Streptococcus suis. Microbial Pathogenesis 36: 327335.CrossRefGoogle ScholarPubMed
Aranda, J, Garrido, ME, Cortes, P, Llagostera, M and Barbe, J (2008). Analysis of the protective capacity of three Streptococcus suis proteins induced under divalent-cation-limited conditions. Infection and Immunity 76: 15901598.CrossRefGoogle ScholarPubMed
Arends, JP and Zanen, HC (1988). Meningitis caused by Streptococcus suis in humans. Reviews of Infectious Diseases 10: 131137.CrossRefGoogle ScholarPubMed
Baele, M, Chiers, K, Devriese, LA, Smith, HE, Wisselink, HJ, Vaneechoutte, M and Haesebrouck, F (2001). The Gram-positive tonsillar and nasal flora of piglets before and after weaning. Journal of Applied Microbiology 91: 9971003.CrossRefGoogle ScholarPubMed
Barocchi, MA, Ries, J, Zogaj, X, Hemsley, C, Albiger, B, Kanth, A, Dahlberg, S, Fernebro, J, Moschioni, M, Masignani, V, Hultenby, K, Taddei, AR, Beiter, K, Wartha, F, von Euler, A, Covacci, A, Holden, DW, Normark, S, Rappuoli, R and Henriques-Normark, B (2006). A pneumococcal pilus influences virulence and host inflammatory responses. Proceedings of the National Academy of Sciences, USA 103: 28572862.CrossRefGoogle ScholarPubMed
Baums, CG, Kaim, U, Fulde, M, Ramachandran, G, Goethe, R and Valentin-Weigand, P (2006). Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infection and Immunity 74: 61546162.CrossRefGoogle ScholarPubMed
Baums, CG, Verkühlen, GJ, Rehm, T, Silva, LM, Beyerbach, M, Pohlmeyer, K and Valentin-Weigand, P (2007). Prevalence of Streptococcus suis genotypes in wild boars of Northwestern Germany. Applied and Environmental Microbiology 73: 711717.CrossRefGoogle ScholarPubMed
Baums, CG, Kock, C, Beineke, A, Bennecke, K, Goethe, R, Schroder, C, Waldmann, KH and Valentin-Weigand, P (2009). Streptococcus suis bacterin and subunit vaccine immunogenicities and protective efficacies against serotypes 2 and 9. Clinical and Vaccine Immunology 16: 200208.CrossRefGoogle Scholar
Beineke, A, Bennecke, K, Neis, C, Schröder, C, Waldmann, KH, Baumgartner, W, Valentin-Weigand, P and Baums, CG (2008). Comparative evaluation of virulence and pathology of Streptococcus suis serotypes 2 and 9 in experimentally infected growers. Veterinary Microbiology 128: 423430.CrossRefGoogle ScholarPubMed
Benga, L, Goethe, R, Rohde, M and Valentin-Weigand, P (2004). Non-encapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cellular Microbiology 6: 867881.CrossRefGoogle ScholarPubMed
Benga, L, Fulde, M, Neis, C, Goethe, R and Valentin-Weigand, P (2008). Polysaccharide capsule and suilysin contribute to extracellular survival of Streptococcus suis co-cultivated with primary porcine phagocytes. Veterinary Microbiology 132: 211219.CrossRefGoogle ScholarPubMed
Brassard, J, Gottschalk, M and Quessy, S (2001). Decrease of the adhesion of Streptococcus suis serotype 2 mutants to embryonic bovine tracheal cells and porcine tracheal rings. Canadian Journal of Veterinary Research 65: 156160.Google ScholarPubMed
Brassard, J, Gottschalk, M and Quessy, S (2004). Cloning and purification of the Streptococcus suis serotype 2 glyceraldehyde-3-phosphate dehydrogenase and its involvement as an adhesin. Veterinary Microbiology 102: 8794.CrossRefGoogle ScholarPubMed
Campo Sepulveda, EM, Altman, E, Kobisch, M, D'Allaire, S and Gottschalk, M (1996). Detection of antibodies against Streptococcus suis capsular type 2 using a purified capsular polysaccharide antigen-based indirect ELISA. Veterinary Microbiology 52: 113125.CrossRefGoogle ScholarPubMed
Chabot-Roy, G, Willson, P, Segura, M, Lacouture, S and Gottschalk, M (2006). Phagocytosis and killing of Streptococcus suis by porcine neutrophils. Microbial Pathogenesis 41: 2132.CrossRefGoogle ScholarPubMed
Charland, N, Kobisch, M, Martineau-Doize, B, Jacques, M and Gottschalk, M (1996). Role of capsular sialic acid in virulence and resistance to phagocytosis of Streptococcus suis capsular type 2. FEMS Immunology and Medical Microbiology 14: 195203.CrossRefGoogle ScholarPubMed
Charland, N, Harel, J, Kobisch, M, Lacasse, S and Gottschalk, M (1998). Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology 144 (Pt 2): 325332.CrossRefGoogle ScholarPubMed
Charland, N, Nizet, V, Rubens, CE, Kim, KS, Lacouture, S and Gottschalk, M (2000). Streptococcus suis serotype 2 interactions with human brain microvascular endothelial cells. Infection and Immunity 68: 637643.CrossRefGoogle ScholarPubMed
Chen, C, Tang, J, Dong, W, Wang, C, Feng, Y, Wang, J, Zheng, F, Pan, X, Liu, D, Li, M, Song, Y, Zhu, X, Sun, H, Feng, T, Guo, Z, Ju, A, Ge, J, Dong, Y, Sun, W, Jiang, Y, Wang, J, Yan, J, Yang, H, Wang, X, Gao, GF, Yang, R, Wang, J and Yu, J (2007). A glimpse of streptococcal toxic shock syndrome from comparative genomics of Streptococcussuis 2 Chinese isolates. PLoS ONE 2: e315.CrossRefGoogle Scholar
Clifton-Hadley, FA and Alexander, TJ (1980). The carrier site and carrier rate of Streptococcus suis type II in pigs. Veterinary Record 107: 4041.CrossRefGoogle ScholarPubMed
Courtney, HS, Hasty, DL, Li, Y, Chiang, HC, Thacker, JL and Dale, JB (1999). Serum opacity factor is a major fibronectin-binding protein and a virulence determinant of M type 2 Streptococcus pyogenes. Molecular Microbiology 32: 8998.CrossRefGoogle Scholar
Cunin, R, Glansdorff, N, Pierard, A and Stalon, V (1986). Biosynthesis and metabolism of arginine in bacteria. Microbiological Reviews 50: 314352.CrossRefGoogle ScholarPubMed
de Greeff, A, Buys, H, Verhaar, R, Dijkstra, J, van Alphen, L and Smith, HE (2002). Contribution of fibronectin-binding protein to pathogenesis of Streptococcus suis serotype 2. Infection and Immunity 70: 13191325.CrossRefGoogle ScholarPubMed
de Greeff, A, Hamilton, A, Sutcliffe, IC, Buys, H, van Alphen, L and Smith, HE (2003). Lipoprotein signal peptidase of Streptococcus suis serotype 2. Microbiology 149: 13991407.CrossRefGoogle ScholarPubMed
Degnan, BA, Fontaine, MC, Doebereiner, AH, Lee, JJ, Mastroeni, P, Dougan, G, Goodacre, JA and Kehoe, MA (2000). Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein. Infection and Immunity 68: 24412448.CrossRefGoogle ScholarPubMed
Dominguez-Punaro, MC, Segura, M, Plante, MM, Lacouture, S, Rivest, S and Gottschalk, M (2007). Streptococcus suis serotype 2, an important swine and human pathogen, induces strong systemic and cerebral inflammatory responses in a mouse model of infection. Journal of Immunology 179: 18421854.CrossRefGoogle Scholar
Dramsi, S, Trieu-Cuot, P and Bierne, H (2005). Sorting sortases: a nomenclature proposal for the various sortases of Gram-positive bacteria. Research in Microbiology 156: 289297.CrossRefGoogle ScholarPubMed
Elliott, SD and Tai, JY (1978). The type-specific polysaccharides of Streptococcus suis. Journal of Experimental Medicine 148: 16991704.CrossRefGoogle ScholarPubMed
Elliott, SD, McCarty, M and Lancefield, RC (1977). Teichoic acids of group D streptococci with special reference to strains from pig meningitis (Streptococcus suis). Journal of Experimental Medicine 145: 490499.CrossRefGoogle Scholar
Elliott, SD, Clifton-Hadley, F and Tai, J (1980). Streptococcal infection in young pigs. V. An immunogenic polysaccharide from Streptococcus suis type 2 with particular reference to vaccination against streptococcal meningitis in pigs. Journal of Hygiene (London) 85: 275285.CrossRefGoogle Scholar
Esgleas, M, Lacouture, S and Gottschalk, M (2005). Streptococcus suis serotype 2 binding to extracellular matrix proteins. FEMS Microbiology Letters 244: 3340.CrossRefGoogle ScholarPubMed
Esgleas, M, Li, Y, Hancock, MA, Harel, J, Dubreuil, JD and Gottschalk, M (2008). Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154: 26682679.CrossRefGoogle ScholarPubMed
Esgleas, M, Dominguez-Punaro, MC, Li, Y, Hancock, MA, Harel, J, Dubreuil, JD and Gottschalk, M (2009). Immunization with SsEno fails to protect mice against challenge with Streptococcus suis serotype 2. FEMS Microbiology Letters 294: 8288.CrossRefGoogle ScholarPubMed
Feng, Y, Zheng, F, Pan, X, Sun, W, Wang, C, Dong, Y, Ju, AP, Ge, J, Liu, D, Liu, C, Yan, J, Tang, J and Gao, GF (2007). Existence and characterization of allelic variants of Sao, a newly identified surface protein from Streptococcus suis. FEMS Microbiology Letters 275: 8088.CrossRefGoogle Scholar
Feng, Y, Li, M, Zhang, H, Zheng, B, Han, H, Wang, C, Yan, J, Tang, J and Gao, GF (2008). Functional definition and global regulation of Zur, a zinc uptake regulator in a Streptococcus suis serotype 2 strain causing streptococcal toxic shock syndrome. Journal of Bacteriology 190: 75677578.CrossRefGoogle Scholar
Fittipaldi, N, Gottschalk, M, Vanier, G, Daigle, F and 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. Applied and Environmental Microbiology 73: 43594364.Google ScholarPubMed
Fittipaldi, N, Sekizaki, T, Takamatsu, D, Dominguez-Punaro, ML, Harel, J, Bui, NK, Vollmer, W and Gottschalk, M (2008a). Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Molecular Microbiology 70: 11201135.CrossRefGoogle Scholar
Fittipaldi, N, Sekizaki, T, Takamatsu, D, Harel, J, Dominguez-Punaro, ML, Von Aulock, S, Draing, C, Marois, C, Kobisch, M and Gottschalk, M (2008b). D-alanylation of lipoteichoic acid contributes to the virulence of Streptococcus suis. Infection and Immunity 76: 35873594.Google Scholar
Fontaine, MC, Perez-Casal, J and Willson, PJ (2004). Investigation of a novel DNase of Streptococcus suis serotype 2. Infection and Immunity 72: 774781.CrossRefGoogle ScholarPubMed
Galina, L, Vecht, U, Wisselink, HJ and Pijoan, C (1996). Prevalence of various phenotypes of Streptococcus suis isolated from swine in the U.S.A. based on the presence of muraminidase-released protein and extracellular factor. Canadian Journal of Veterinary Research 60: 7274.Google ScholarPubMed
Geng, H, Zhu, L, Yuan, Y, Zhang, W, Li, W, Wang, J, Zheng, Y, Wei, K, Cao, W, Wang, H and Jiang, Y (2008). Identification and characterization of novel immunogenic proteins of Streptococcus suis serotype 2. Journal of Proteome Research 7: 41324142.CrossRefGoogle ScholarPubMed
Gottschalk, M and Segura, M (2000). The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Veterinary Microbiology 76: 259272.CrossRefGoogle ScholarPubMed
Gottschalk, MG, Lacouture, S and Dubreuil, JD (1995). Characterization of Streptococcus suis capsular type 2 haemolysin. Microbiology 141: 189195.CrossRefGoogle ScholarPubMed
Gottschalk, M, Lebrun, A, Wisselink, H, Dubreuil, JD, Smith, H and Vecht, U (1998). Production of virulence-related proteins by Canadian strains of Streptococcus suis capsular type 2. Canadian Journal of Veterinary Research–Revue Canadienne de Recherche Veterinaire 62: 7579.Google ScholarPubMed
Gottschalk, M, Higgins, R and Quessy, S (1999). Dilemma of the virulence of Streptococcus suis strains. Journal of Clinical Microbiology 37: 42024203.CrossRefGoogle Scholar
Gottschalk, M, Segura, M and Xu, J (2007). Streptococcus suis infections in humans: the Chinese experience and the situation in North America. Animal Health Research Reviews 8: 2945.CrossRefGoogle ScholarPubMed
Graveline, R, Segura, M, Radzioch, D and Gottschalk, M (2007). TLR2-dependent recognition of Streptococcus suis is modulated by the presence of capsular polysaccharide which modifies macrophage responsiveness. International Immunology 19: 375389.CrossRefGoogle ScholarPubMed
Gruening, P, Fulde, M, Valentin-Weigand, P and Goethe, R (2006). Structure, regulation, and putative function of the arginine deiminase system of Streptococcus suis. Journal of Bacteriology 188: 361369.CrossRefGoogle ScholarPubMed
Haataja, S, Tikkanen, K, Hytonen, J and Finne, J (1996). The Gal alpha 1–4 Gal-binding adhesin of Streptococcus suis, a gram-positive meningitis-associated bacterium. Advances in Experimental Medicine and Biology 408: 2534.CrossRefGoogle ScholarPubMed
Higgins, R and Gottschalk, M (2005). Streptococcal diseases. In: Straw, B, Allaire, SD, Mengeling, W and Taylor, D (eds) Diseases of Swine. Ames, IA: Iowa State University Press, pp. 769783.Google Scholar
Hutchings, MI, Palmer, T, Harrington, DJ and Sutcliffe, IC (2009). Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold 'em, knowing when to fold 'em. Trends in Microbiology 17: 1321.CrossRefGoogle ScholarPubMed
Jacobs, AAC, Loeffen, PLW, vandenBerg, AJG and Storm, PK (1994). Identification, purification, and characterization of a thiol-activated hemolysin (suilysin) of Streptococcus suis. Infection and Immunity 62: 17421748.CrossRefGoogle ScholarPubMed
Jacobs, AAC, vandenBerg, AJG and Loeffen, PLW (1996). Protection of experimentally infected pigs by suilysin, the thiol-activated haemolysin of Streptococcus suis. Veterinary Record 139: 225228.CrossRefGoogle ScholarPubMed
Jacques, M, Gottschalk, M, Foiry, B and Higgins, R (1990). Ultrastructural study of surface components of Streptococcus suis. Journal of Bacteriology 172: 28332838.CrossRefGoogle ScholarPubMed
Jiang, H, Fan, HJ and Lu, CP (2009). Identification and distribution of putative virulent genes in strains of Streptococcus suis serotype 2. Veterinary Microbiology 133: 309316.CrossRefGoogle ScholarPubMed
Jobin, MC and Grenier, D (2003). Identification and characterization of four proteases produced by Streptococcus suis. FEMS Microbiology Letters 220: 113119.CrossRefGoogle ScholarPubMed
Jobin, MC, Brassard, J, Quessy, S, Gottschalk, M and Grenier, D (2004). Acquisition of host plasmin activity by the swine pathogen Streptococcus suis serotype 2. Infection and Immunity 72: 606610.CrossRefGoogle ScholarPubMed
Jobin, MC, Fortin, J, Willson, PJ, Gottschalk, M and Grenier, D (2005a). Acquisition of plasmin activity and induction of arachidonic acid release by Streptococcus suis in contact with human brain microvascular endothelial cells. FEMS Microbiology Letters 252: 105111.CrossRefGoogle ScholarPubMed
Jobin, MC, Martinez, G, Motard, J, Gottschalk, M and Grenier, D (2005b). Cloning, purification, and enzymatic properties of dipeptidyl peptidase IV from the swine pathogen Streptococcus suis. Journal of Bacteriology 187: 795799.CrossRefGoogle ScholarPubMed
King, SJ, Heath, PJ, Luque, I, Tarradas, C, Dowson, CG and Whatmore, AM (2001). Distribution and genetic diversity of suilysin in Streptococcus suis isolated from different diseases of pigs and characterization of the genetic basis of suilysin absence. Infection and Immunity 69: 75727582.CrossRefGoogle ScholarPubMed
King, SJ, Allen, AG, Maskell, DJ, Dowson, CG and Whatmore, AM (2004). Distribution, genetic diversity, and variable expression of the gene encoding hyaluronate lyase within the Streptococcus suis population. Journal of Bacteriology 186: 47404747.CrossRefGoogle ScholarPubMed
Kock, C, Beineke, A, Seitz, M, Ganter, M, Waldmann, K, Valentin-Weigand, P and Baums, CG (2009). Intranasal immunization with a live Streptococcus suis isogenic ofs mutant elicited suilysin-neutralization titers but failed to induce opsonizing antibodies and protection. Veterinary Immunology and Immunopathology in press.CrossRefGoogle ScholarPubMed
Lalonde, M, Segura, M, Lacouture, S and Gottschalk, M (2000). Interactions between Streptococcus suis serotype 2 and different epithelial cell lines. Microbiology 146: 19131921.CrossRefGoogle ScholarPubMed
Li, M, Wang, C, Feng, Y, Pan, X, Cheng, G, Wang, J, Ge, J, Zheng, F, Cao, M, Dong, Y, Liu, D, Wang, J, Lin, Y, Du, H, Gao, GF, Wang, X, Hu, F and Tang, J (2008). SalK/SalR, a two-component signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2. PLoS ONE 3: e2080.CrossRefGoogle ScholarPubMed
Li, W, Liu, L, Chen, H and Zhou, R (2009). Identification of Streptococcus suis genes preferentially expressed under iron starvation by selective capture of transcribed sequences. FEMS Microbiology Letters 292: 123133.CrossRefGoogle ScholarPubMed
Li, Y, Martinez, G, Gottschalk, M, Lacouture, S, Willson, P, Dubreuil, JD, Jacques, M and Harel, J (2006). Identification of a surface protein of Streptococcus suis and evaluation of its immunogenic and protective capacity in pigs. Infection and Immunity 74: 305312.CrossRefGoogle ScholarPubMed
Li, Y, Gottschalk, M, Esgleas, M, Lacouture, S, Dubreuil, JD, Willson, P and Harel, J (2007). Immunization with recombinant Sao protein confers protection against Streptococcus suis infection. Clinical and Vaccine Immunology 14: 937943.CrossRefGoogle ScholarPubMed
Liu, L, Cheng, G, Wang, C, Pan, X, Cong, Y, Pan, Q, Wang, J, Zheng, F, Hu, F and Tang, J (2009). Identification and experimental verification of protective antigens against Streptococcus suis serotype 2 based on genome sequence analysis. Current Microbiology 58: 1117.CrossRefGoogle ScholarPubMed
Liukkonen, J, Haataja, S, Tikkanen, K, Kelm, S and Finne, J (1992). Identification of N-acetylneuraminyl alpha 2–>3 poly-N-acetyllactosamine glycans as the receptors of sialic acid-binding Streptococcus suis strains. Journal of Biological Chemistry 267: 2110521111.CrossRefGoogle Scholar
Lun, S and Willson, PJ (2005). Putative mannose-specific phosphotransferase system component IID represses expression of suilysin in serotype 2 Streptococcus suis. Veterinary Microbiology 105: 169180.CrossRefGoogle ScholarPubMed
Lun, SC, Perez-Casal, J, Connor, W and Willson, PJ (2003). Role of suilysin in pathogenesis of Streptococcus suis capsular serotype 2. Microbial Pathogenesis 34: 2737.CrossRefGoogle ScholarPubMed
Lun, ZR, Wang, QP, Chen, XG, Li, AX and Zhu, XQ (2007). Streptococcus suis: an emerging zoonotic pathogen. Lancet Infectious Diseases 7: 201209.CrossRefGoogle ScholarPubMed
Madsen, LW, Svensmark, B, Elvestad, K, Aalbaek, B and Jensen, HE (2002). Streptococcus suis serotype 2 infection in pigs: new diagnostic and pathogenetic aspects. Journal of Comparative Pathology 126: 5765.CrossRefGoogle ScholarPubMed
Mai, NT, Hoa, NT, Nga, TV, Linh, LD, Chau, TT, Sinh, DX, Phu, NH, Chuong, LV, Diep, TS, Campbell, J, Nghia, HD, Minh, TN, Chau, NV, de Jong, MD, Chinh, NT, Hien, TT, Farrar, J and Schultsz, C (2008). Streptococcus suis meningitis in adults in Vietnam. Clinical Infectious Diseases 46: 659667.Google ScholarPubMed
Malley, R, Henneke, P, Morse, SC, Cieslewicz, MJ, Lipsitch, M, Thompson, CM, Kurt-Jones, E, Paton, JC, Wessels, MR and Golenbock, DT (2003). Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proceedings of the National Academy of Sciences, USA 100: 19661971.CrossRefGoogle ScholarPubMed
Marques, MB, Kasper, DL, Pangburn, MK and Wessels, MR (1992). Prevention of C3 deposition by capsular polysaccharide is a virulence mechanism of type III group B streptococci. Infection and Immunity 60: 39863993.CrossRefGoogle ScholarPubMed
Martinez, G, de Castro, AFP, Pagnani, KJR, Nakazato, G, da Silveira, WD and Gottschalk, M (2003). Clonal distribution of an atypical MRP+, EF*, and suilysin(+) phenotype of virulent Streptococcus suis serotype 2 strains in Brazil. Canadian Journal of Veterinary Research–Revue Canadienne de Recherche Veterinaire 67: 5255.Google ScholarPubMed
Mazmanian, SK, Liu, G, Ton-That, H and Schneewind, O (1999). Staphylococcus aureus sortase, an enzyme that anchors surface proteins to the cell wall. Science 285: 760763.CrossRefGoogle ScholarPubMed
Melancon, D and Grenier, D (2003). Production and properties of bacteriocin-like inhibitory substances from the swine pathogen Streptococcus suis serotype 2. Applied and Environmental Microbiology 69: 44824488.CrossRefGoogle ScholarPubMed
Messier, S, Lacouture, S and Gottschalk, M (2008). Distribution of Streptococcus suis capsular types from 2001 to 2007. Canadian Veterinary Journal 49: 461462.Google ScholarPubMed
Norton, PM, Rolph, C, Ward, PN, Bentley, RW and Leigh, JA (1999). Epithelial invasion and cell lysis by virulent strains of Streptococcus suis is enhanced by the presence of suilysin. FEMS Immunology and Medical Microbiology 26: 2535.CrossRefGoogle ScholarPubMed
Okwumabua, O and Chinnapapakkagari, S (2005). Identification of the gene encoding a 38-kilodalton immunogenic and protective antigen of Streptococcus suis. Clinical and Diagnostic Laboratory Immunology 12: 484490.Google ScholarPubMed
Osaki, M, Takamatsu, D, Shimoji, Y and Sekizaki, T (2002). Characterization of Streptococcus suis genes encoding proteins homologous to sortase of Gram-positive bacteria. Journal of Bacteriology 184: 971982.CrossRefGoogle ScholarPubMed
Osaki, M, Takamatsu, D, Shimoji, Y and Sekizaki, T (2003). Allelic variation in srtAs of Streptococcus suis strains. FEMS Microbiology Letters 219: 195201.CrossRefGoogle ScholarPubMed
Pan, X, Ge, J, Li, M, Wu, B, Wang, C, Wang, J, Feng, Y, Yin, Z, Zheng, F, Cheng, G, Sun, W, Ji, H, Hu, D, Shi, P, Feng, X, Hao, X, Dong, R, Hu, F and Tang, J (2009). The orphan response regulator CovR: a globally negative modulator of virulence in Streptococcus suis serotype 2. Journal of Bacteriology 191: 26012612.CrossRefGoogle ScholarPubMed
Pancholi, V and Fischetti, VA (1992). A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. Journal of Experimental Medicine 176: 415426.CrossRefGoogle Scholar
Pancholi, V and Fischetti, VA (1998). alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. Journal of Biological Chemistry 273: 1450314515.CrossRefGoogle ScholarPubMed
Perch, B, Pedersen, KB and Henrichsen, J (1983). Serology of capsulated streptococci pathogenic for pigs: six new serotypes of Streptococcus suis. Journal of Clinical Microbiology 17: 993996.CrossRefGoogle ScholarPubMed
Quessy, S, Dubreuil, JD, Jacques, M, Malouin, F and Higgins, R (1994). Increase of capsular material thickness following in vivo growth of virulent Streptococcus suis serotype 2 strains. FEMS Microbiology Letters 115: 1926.CrossRefGoogle ScholarPubMed
Quessy, S, Busque, P, Higgins, R, Jacques, M and Dubreuil, JD (1997). Description of an albumin binding activity for Streptococcus suis serotype 2. FEMS Microbiology Letters 147: 245250.CrossRefGoogle ScholarPubMed
Segers, RPAM, Kenter, T, de Haan, LAM and Jacobs, AAC (1998). Characterisation of the gene encoding suilysin from Streptococcus suis and expression in field strains. FEMS Microbiology Letters 167: 255261.CrossRefGoogle ScholarPubMed
Segura, M and Gottschalk, M (2002). Streptococcus suis interactions with the murine macrophage cell line J774: adhesion and cytotoxicity. Infection and Immunity 70: 43124322.CrossRefGoogle ScholarPubMed
Segura, MA, Cleroux, P and Gottschalk, M (1998). Streptococcus suis and group B Streptococcus differ in their interactions with murine macrophages. FEMS Immunology and Medical Microbiology 21: 189195.CrossRefGoogle ScholarPubMed
Segura, M, Gottschalk, M and Olivier, M (2004). Encapsulated Streptococcus suis inhibits activation of signaling pathways involved in phagocytosis. Infection and Immunity 72: 53225330.CrossRefGoogle ScholarPubMed
Segura, M, Vanier, G, Al Numani, D, Lacouture, S, Olivier, M and Gottschalk, M (2006). Proinflammatory cytokine and chemokine modulation by Streptococcus suis in a whole-blood culture system. FEMS Immunology and Medical Microbiology 47: 92106.CrossRefGoogle Scholar
Serhir, B, Higgins, R, Foiry, B and Jacques, M (1993). Detection of immunoglobulin-G-binding proteins in Streptococcus suis. Journal of General Microbiology 139: 29532958.CrossRefGoogle ScholarPubMed
Serhir, B, Dubreuil, D, Higgins, R and Jacques, M (1995). Purification and characterization of a 52-kilodalton immunoglobulin G-binding protein from Streptococcus suis capsular type 2. Journal of Bacteriology 177: 38303836.CrossRefGoogle ScholarPubMed
Silva, LM, Baums, CG, Rehm, T, Wisselink, HJ, Goethe, R and Valentin-Weigand, P (2006). Virulence-associated gene profiling of Streptococcus suis isolates by PCR. Veterinary Microbiology 115: 117127.CrossRefGoogle ScholarPubMed
Smith, HE, Vecht, U, Gielkens, ALJ and Smits, MA (1992). Cloning and nucleotide-sequence of the gene encoding the 136-kilodalton surface protein (muramidase-released protein) of Streptococcus suis type-2. Infection and Immunity 60: 23612367.CrossRefGoogle ScholarPubMed
Smith, HE, Reek, FH, Vecht, U, Gielkens, ALJ and Smits, MA (1993). Repeats in an extracellular protein of weakly pathogenic strains of Streptococcus suis type-2 are absent in pathogenic strains. Infection and Immunity 61: 33183326.CrossRefGoogle Scholar
Smith, HE, Vecht, U, Wisselink, HJ, StockhofeZurwieden, N, Biermann, Y and Smits, MA (1996). Mutants of Streptococcus suis types 1 and 2 impaired in expression of muramidase-released protein and extracellular protein induce disease in newborn germfree pigs. Infection and Immunity 64: 44094412.CrossRefGoogle ScholarPubMed
Smith, HE, Damman, M, van der Velde, J, Wagenaar, F, Wisselink, HJ, Stockhofe-Zurwieden, N and Smits, MA (1999). Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infection and Immunity 67: 17501756.CrossRefGoogle ScholarPubMed
Smith, HE, de Vries, R, van't Slot, R and Smits, MA (2000). The cps locus of Streptococcus suis serotype 2: genetic determinant for the synthesis of sialic acid. Microbial Pathogenesis 29: 127134.CrossRefGoogle ScholarPubMed
Smith, HE, Buijs, H, de Vries, RR, Wisselink, HJ, Stockhofe-Zurwieden, N and Smits, MA (2001). Environmentally regulated genes of Streptococcus suis: identification by the use of iron-restricted conditions in vitro and by experimental infection of piglets. Microbiology 147: 271280.CrossRefGoogle ScholarPubMed
Song, L and Pachter, JS (2004). Monocyte chemoattractant protein-1 alters expression of tight junction-associated proteins in brain microvascular endothelial cells. Microvascular Research 67: 7889.CrossRefGoogle ScholarPubMed
Staats, JJ, Plattner, BL, Stewart, GC and Chengappa, MM (1999). Presence of the Streptococcus suis suilysin gene and expression of MRP and EF correlates with high virulence in Streptococcus suis type 2 isolates. Veterinary Microbiology 70: 201211.CrossRefGoogle ScholarPubMed
Su, Y, Yao, W, Perez-Gutierrez, ON, Smidt, H and Zhu, WY (2008). Changes in abundance of Lactobacillus spp. and Streptococcus suis in the stomach, jejunum and ileum of piglets after weaning. FEMS Microbiology Ecology 66: 546555.CrossRefGoogle ScholarPubMed
Takamatsu, D, Osaki, M and Sekizaki, T (2002). Evidence for lateral transfer of the suilysin gene region of Streptococcus suis. Journal of Bacteriology 184: 20502057.CrossRefGoogle ScholarPubMed
Takamatsu, D, Osaki, M, Tharavichitkul, P, Takai, S and Sekizaki, T (2008). Allelic variation and prevalence of serum opacity factor among the Streptococcus suis population. Journal of Medical Microbiology 57: 488494.Google ScholarPubMed
Takamatsu, D, Nishino, H, Ishiji, T, Ishii, J, Osaki, M, Fittipaldi, N, Gottschalk, M, Tharavichitkul, P, Takai, S and Sekizaki, T (2009). Genetic organization and preferential distribution of putative pilus gene clusters in Streptococcus suis. Veterinary Microbiology 138: 132139.CrossRefGoogle ScholarPubMed
Tan, C, Fu, S, Liu, M, Jin, M, Liu, J, Bei, W and Chen, H (2008a). Cloning, expression and characterization of a cell wall surface protein, 6-phosphogluconate-dehydrogenase, of Streptococcus suis serotype 2. Veterinary Microbiology 130: 363370.CrossRefGoogle ScholarPubMed
Tan, C, Liu, M, Jin, M, Liu, J, Chen, Y, Wu, T, Fu, T, Bei, W and Chen, H (2008b). The key virulence-associated genes of Streptococcus suis type 2 are upregulated and differentially expressed in vivo. FEMS Microbiology Letters 278: 108114.CrossRefGoogle ScholarPubMed
Tan, C, Liu, M, Liu, J, Yuan, F, Fu, S, Liu, Y, Jin, M, Bei, W and Chen, H (2009). Vaccination with Streptococcus suis serotype 2 recombinant 6PGD protein provides protection against S. suis infection in swine. FEMS Microbiology Letters 296: 7883.CrossRefGoogle ScholarPubMed
Tang, J, Wang, C, Feng, Y, Yang, W, Song, H, Chen, Z, Yu, H, Pan, X, Zhou, X, Wang, H, Wu, B, Wang, H, Zhao, H, Lin, Y, Yue, J, Wu, Z, He, X, Gao, F, Khan, AH, Wang, J, Zhao, GP, Wang, Y, Wang, X, Chen, Z and Gao, GF (2006). Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Medicine 3: e151.CrossRefGoogle ScholarPubMed
Telford, JL, Barocchi, MA, Margarit, I, Rappuoli, R and Grandi, G (2006). Pili in gram-positive pathogens. Nature Reviews Microbiology 4: 509519.CrossRefGoogle ScholarPubMed
Tenenbaum, T, Papandreou, T, Gellrich, D, Friedrichs, U, Seibt, A, Adam, R, Wewer, C, Galla, HJ, Schwerk, C and Schroten, H (2009). Polar bacterial invasion and translocation of Streptococcus suis across the blood-cerebrospinal fluid barrier in vitro. Cellular Microbiology 11: 323336.CrossRefGoogle ScholarPubMed
Tian, Y, Aarestrup, FM and Lu, CP (2004). Characterization of Streptococcus suis serotype 7 isolates from diseased pigs in Denmark. Veterinary Microbiology 103: 5562.CrossRefGoogle ScholarPubMed
Tikkanen, K, Haataja, S, Francois-Gerard, C and Finne, J (1995). Purification of a galactosyl-alpha 1–4-galactose-binding adhesin from the Gram-positive meningitis-associated bacterium Streptococcus suis. Journal of Biological Chemistry 270: 2887428878.Google ScholarPubMed
Tikkanen, K, Haataja, S and Finne, J (1996). The galactosyl-(alpha 1–4-galactose-binding adhesin of Streptococcus suis: occurrence in strains of different hemagglutination activities and induction of opsonic antibodies. Infection and Immunity 64: 36593665.CrossRefGoogle ScholarPubMed
Ton-That, H, Liu, G, Mazmanian, SK, Faull, KF and Schneewind, O (1999). Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proceedings of the National Academy of Sciences, USA 96: 1242412429.CrossRefGoogle ScholarPubMed
Ton-That, H, Marraffini, LA and Schneewind, O (2004). Sortases and pilin elements involved in pilus assembly of Corynebacterium diphtheriae. Molecular Microbiology 53: 251261.CrossRefGoogle ScholarPubMed
Vadeboncoeur, N, Segura, M, Al Numani, D, Vanier, G and Gottschalk, M (2003). Pro-inflammatory cytokine and chemokine release by human brain microvascular endothelial cells stimulated by Streptococcus suis serotype 2. FEMS Immunology and Medical Microbiology 35: 4958.CrossRefGoogle ScholarPubMed
Vanier, G, Segura, M, Friedl, P, Lacouture, S and Gottschalk, M (2004). Invasion of porcine brain microvascular endothelial cells by Streptococcus suis serotype 2. Infection and Immunity 72: 14411449.CrossRefGoogle ScholarPubMed
Vanier, G, Segura, M and Gottschalk, M (2007). Characterization of the invasion of porcine endothelial cells by Streptococcus suis serotype 2. Canadian Journal of Veterinary Research 71: 8189.Google ScholarPubMed
Vanier, G, Sekizaki, T, Dominguez-Punaro, MC, Esgleas, M, Osaki, M, Takamatsu, D, Segura, M and Gottschalk, M (2008). Disruption of srtA gene in Streptococcus suis results in decreased interactions with endothelial cells and extracellular matrix proteins. Veterinary Microbiology 127: 417424.CrossRefGoogle ScholarPubMed
Vanier, G, Fittipaldi, N, Slater, JD, Dominguez-Punaro, ML, Rycroft, AN, Segura, M, Maskell, DJ and Gottschalk, M (2009). New putative virulence factors of Streptococcus suis involved in invasion of porcine brain microvascular endothelial cells. Microbial Pathogenesis 46: 1320.CrossRefGoogle ScholarPubMed
Vecht, U, Wisselink, HJ, Jellema, ML and Smith, HE (1991). Identification of 2 proteins associated with virulence of Streptococcus suis type-2. Infection and Immunity 59: 31563162.CrossRefGoogle ScholarPubMed
Vecht, U, Wisselink, HJ, van Dijk, JE and Smith, HE (1992). Virulence of Streptococcus suis type 2 strains in newborn germfree pigs depends on phenotype. Infection and Immunity 60: 550556.CrossRefGoogle ScholarPubMed
Vecht, U, Stockhofe-Zurwieden, N, Tetenburg, BJ, Wisselink, HJ and Smith, HE (1997). Murine and pig models of Streptococcus suis type 2 infections are incompatible. Streptococci and the Host 418: 827829.CrossRefGoogle ScholarPubMed
Vollmer, W (2008). Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiology Reviews 32: 287306.CrossRefGoogle ScholarPubMed
Vollmer, W, Blanot, D and de Pedro, MA (2008). Peptidoglycan structure and architecture. FEMS Microbiology Reviews 32: 149167.CrossRefGoogle ScholarPubMed
Wang, C, Li, M, Feng, Y, Zheng, F, Dong, Y, Pan, X, Cheng, G, Dong, R, Hu, D, Feng, X, Ge, J, Liu, D, Wang, J, Cao, M, Hu, F and Tang, J (2009). The involvement of sortase A in high virulence of STSS-causing Streptococcus suis serotype 2. Archives of Microbiology 191: 2333.CrossRefGoogle ScholarPubMed
Wei, Z, Li, R, Zhang, A, He, H, Hua, Y, Xia, J, Cai, X, Chen, H and Jin, M (2009). Characterization of Streptococcus suis isolates from the diseased pigs in China between 2003 and 2007. Veterinary Microbiology 137: 196201.CrossRefGoogle Scholar
Wertheim, HF, Nghia, HD, Taylor, W and Schultsz, C (2009). Streptococcus suis: an emerging human pathogen. Clinical Infectious Diseases 48: 617625.CrossRefGoogle ScholarPubMed
Wibawan, IW and Lammler, C (1994). Relation between encapsulation and various properties of Streptococcus suis. Zentralblatt Veterinarmedizin RheineB 41: 453459.Google ScholarPubMed
Williams, AE and Blakemore, WF (1990). Pathology of Streptococcal meningitis following intravenous intracisternal and natural routes of infection. Neuropathology and Applied Neurobiology 16: 345356.CrossRefGoogle ScholarPubMed
Winterhoff, N, Goethe, R, Gruening, P, Rohde, M, Kalisz, H, Smith, HE and Valentin-Weigand, P (2002). Identification and characterization of two temperature-induced surface-associated proteins of Streptococcus suis with high homologies to members of the arginine deiminase system of Streptococcus pyogenes. Journal of Bacteriology 184: 67686776.CrossRefGoogle ScholarPubMed
Wisselink, HJ, Smith, HE, Stockhofe-Zurwieden, N, Peperkamp, K and Vecht, U (2000). Distribution of capsular types and production of muramidase-released protein (MRP) and extracellular factor (EF) of Streptococcus suis strains isolated from diseased pigs in seven European countries. Veterinary Microbiology 74: 237248.CrossRefGoogle ScholarPubMed
Wisselink, HJ, Vecht, U, Stockhofe-Zurwieden, N and Smith, HE (2001). Protection of pigs against challenge with virulent Streptococcus suis serotype 2 strains by a muramidase-released protein and extracellular factor vaccine. The Veterinary Record 148: 473477.CrossRefGoogle ScholarPubMed
Wisselink, HJ, Joosten, JJ and Smith, HE (2002). Multiplex PCR assays for simultaneous detection of six major serotypes and two virulence-associated phenotypes of Streptococcus suis in tonsillar specimens from pigs. Journal of Clinical Microbiology 40: 29222929.CrossRefGoogle ScholarPubMed
Wu, Z, Zhang, W and Lu, C (2008a). Comparative proteome analysis of secreted proteins of Streptococcus suis serotype 9 isolates from diseased and healthy pigs. Microbial Pathogenesis 45: 159166.CrossRefGoogle ScholarPubMed
Wu, Z, Zhang, W and Lu, C (2008b). Immunoproteomic assay of surface proteins of Streptococcus suis serotype 9. FEMS Immunology and Medical Microbiology 53: 5259.CrossRefGoogle ScholarPubMed
Ye, C, Zhu, X, Jing, H, Du, H, Segura, M, Zheng, H, Kan, B, Wang, L, Bai, X, Zhou, Y, Cui, Z, Zhang, S, Jin, D, Sun, N, Luo, X, Zhang, J, Gong, Z, Wang, X, Wang, L, Sun, H, Li, Z, Sun, Q, Liu, H, Dong, B, Ke, C, Yuan, H, Wang, H, Tian, K, Wang, Y, Gottschalk, M and Xu, J (2006). Streptococcus suis sequence type 7 outbreak, Sichuan, China. Emerging Infectious Disease 12: 12031208.CrossRefGoogle ScholarPubMed
Yuste, J, Botto, M, Paton, JC, Holden, DW and Brown, JS (2005). Additive inhibition of complement deposition by pneumolysin and PspA facilitates Streptococcus pneumoniae septicemia. Journal of Immunology 175: 18131819.CrossRefGoogle ScholarPubMed
Zhang, A, Chen, B, Mu, X, Li, R, Zheng, P, Zhao, Y, Chen, H and Jin, M (2009). Identification and characterization of a novel protective antigen, enolase of Streptococcus suis serotype 2. Vaccine 27: 13481353.CrossRefGoogle ScholarPubMed
Zhang, W and Lu, CP (2007). Immunoproteomics of extracellular proteins of Chinese virulent strains of Streptococcus suis type 2. Proteomics 7: 44684476.CrossRefGoogle ScholarPubMed
Zuniga, M, Perez, G and Gonzalez-Candelas, F (2002). Evolution of arginine deiminase (ADI) pathway genes. Molecular and Phylogenetic Evolution 25: 429444.CrossRefGoogle ScholarPubMed