Loss of Capsule in Streptococcus suis

Main Article Content

Nattakan Meekhanon

Abstract

Streptococcus (S.) suis is an important zoonotic pathogen. It can cause various diseases, particularly meningitis in swine and human. Most patients recovering from meningitis further develop permanent deaf. Among the proposed virulence factors described so far, capsule is thought to be a significant factor contributing to severe diseases. According to the antigenicity of the capsular polysaccharides, S. suis can be classified into different serotypes. However, the nontypeable S. suis has increasingly been reported. The loss of capsule in S. suis, which results in being the nontypeable strain, can be caused by the alteration of gene(s) in a group of capsular polysaccharide synthesis genes. In addition, the non-encapsulated cells were reported to have greater adherence and biofilm formation abilities than those of the encapsulated cells. Since the adherence to host cell has been considered as the initial step for the pathogenesis of S. suis infection, the loss of capsule in S. suis may play an important role in the severe infection in both swine and human.

Article Details

Section
Review Article

References

Arai, S., Tohya, M., Yamada, R., Osawa, R., Nomoto, R., Kawamura, Y. and Sekizaki, T. 2015. Development of loop-mediated isothermal amplification to detect Streptococcus suis and its application to retail pork meat in Japan. Int. J. Food Microbiol. 208: 35-42.
Arends, J.P., Hartwig, N., Rudolphy, M. and Zanen, H.C. 1984. Carrier rate of Streptococcus suis capsular type 2 in palatine tonsils of slaughtered pigs. J. Clin. Microbiol. 20(5): 945-947.
Baums, C.G. and Valentin-Weigand, P. 2009. Surface-associated and secreted factors of Streptococcus suis in epidemiology, pathogenesis and vaccine development. Anim. Health Res. Rev. 10(1): 65-83.
Benga, L., Friedl, P. and Valentin-Weigand, P. 2005. Adherence of Streptococcus suis to porcine endothelial cells. J. Vet. Med. B. Infect. Dis. Vet. Public Health. 52(9): 392-395.
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. Cell. Microbiol. 6(9): 867-881.
Bonifait, L., Gottschalk, M. and Grenier, D. 2010. Cell surface characteristics of nontypeable isolates of Streptococcus suis. FEMS Microbiol. Lett. 311(2): 160-166.
Charland, N., Harel, J., Kobisch, M., Lacasse, S. and Gottschalk, M. 1998. Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology. 144: 325-332.
Choi, S.M., Cho, B.H., Choi, K.H., Nam, T.S., Kim, J.T., Park, M.S., Kim, B.C., Kim, M.K. and Cho, K.H. 2012. Meningitis caused by Streptococcus suis: case report and review of the literature. J. Clin. Neurol. 8(1): 79-82.
Clifton-Hadley, F.A., Alexander, T.J. and Enright, M.R. 1986. Monitoring herds for Streptococcus suis type 2: chance contamination of slaughter pigs. Vet. Rec. 118(10): 274.
Cloutier, G., D'Allaire, S., Martinez, G., Surprenant, C., Lacouture, S. and Gottschalk, M. 2003. Epidemiology of Streptococcus suis serotype 5 infection in a pig herd with and without clinical disease. Vet. Microbiol. 97(1-2), 135-151.
Corbett, D. and Roberts, I.S. 2009. The role of microbial polysaccharides in host-pathogen interaction. F1000 Biol. Rep. 1: 30.
Costa, A.T., Lobato, F.C., Abreu, V.L., Assis, R.A., Reis, R. and Uzal, F.A. 2005. Serotyping and evaluation of the virulence in mice of Streptococcus suis strains isolated from diseased pigs. Rev. Inst. Med. Trop. Sao Paulo 47(2): 113-115.
Crum, N. F., Barrozo, C. P., Chapman, F. A., Ryan, M. A. and Russell, K. L. 2004. An outbreak of conjunctivitis due to a novel unencapsulated Streptococcus pneumoniae among military trainees. Clin. Infect. Dis. 39(8): 1148-1154.
Fittipaldi, N., Segura, M., Grenier, D. and Gottschalk, M. 2012. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol. 7(2): 259-279.
Fongcom, A., Pruksakorn, S., Netsirisawan, P., Pongprasert, R. and Onsibud, P. 2009. Streptococcus suis infection: a prospective study in northern Thailand. Southeast Asian J. Trop. Med. Public Health. 40(3): 511-517.
Gottschalk, M., Higgins, R., Jacques, M., Mittal, K.R. and Henrichsen, J. 1989. Description of 14 new capsular types of Streptococcus suis. J. Clin. Microbiol. 27(12): 2633-2636.
Gottschalk, M., Lacouture, S., Bonifait, L., Roy, D., Fittipaldi, N. and Grenier, D. 2013. Characterization of Streptococcus suis isolates recovered between 2008 and 2011 from diseased pigs in Quebec, Canada. Vet. Microbiol. 162(2-4): 819-825.
Gottschalk, M. and Segura, M. 2000. The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Vet. Microbiol. 76(3): 259-272.
Gottschalk, M., Segura, M. and Xu, J. 2007. Streptococcus suis infections in humans: the Chinese experience and the situation in North America. Anim. Health. Res. Rev. 8(1): 29-45.
Goyette-Desjardins, G., Auger, J.P., Xu, J., Segura, M. and Gottschalk, M. 2014. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg. Microbes Infect. 3(6): e45.
Higgins, R. and Gottschalk, M. 2006. Diseases of Swine. Blackwell publishing, Ames, Iowa.
Hill, J.E., Gottschalk, M., Brousseau, R., Harel, J., Hemmingsen, S.M. and Goh, S.H. 2005. Biochemical analysis, cpn60 and 16S rDNA sequence data indicate that Streptococcus suis serotypes 32 and 34, isolated from pigs, are Streptococcus orisratti. Vet. Microbiol. 107(1-2): 63-69.
Houde, M., Gottschalk, M., Gagnon, F., Van Calsteren, M.R. and Segura, M. 2012. Streptococcus suis capsular polysaccharide inhibits phagocytosis through destabilization of lipid microdomains and prevents lactosylceramide-dependent recognition. Infect. Immun. 80(2): 506-517.
Ip, M., Fung, K.S., Chi, F., Cheuk, E.S., Chau, S.S., Wong, B.W., Lui, S., Hui, M., Lai, R.W. and Chan, P.K. 2007. Streptococcus suis in Hong Kong. Diagn. Microbiol. Infect. Dis. 57(1): 15-20.
Ishida, S., Tien le, H.T., Osawa, R., Tohya, M., Nomoto, R., Kawamura, Y., Takahashi, T., Kikuchi, N., Kikuchi, K. and Sekizaki, T. 2014. Development of an appropriate PCR system for the reclassification of Streptococcus suis. J. Microbiol. Methods. 107: 66-70.
Katsumi, M., Kataoka, Y., Takahashi, T., Kikuchi, N. and Hiramune, T. 1997. Bacterial isolation from slaughtered pigs associated with endocarditis, especially the isolation of Streptococcus suis. J. Vet. Med. Sci. 59(1): 75-78.
Kerdsin, A., Dejsirilert, S., Sawanpanyalert, P., Boonnark, A., Noithachang, W., Sriyakum, D., Simkum, S., Chokngam, S., Gottschalk, M., Akeda, Y. and Oishi, K. 2011. Sepsis and spontaneous bacterial peritonitis in Thailand. Lancet. 378(9794): 960.
Kerdsin, A., Akeda, Y., Hatrongjit, R., Detchawna, U., Sekizaki, T., Hamada, S., Gottschalk, M. and Oishi, K. 2014. Streptococcus suis serotyping by a new multiplex PCR. J. Med. Microbiol. 63: 824-830.
Lakkitjaroen, N., Takamatsu, D., Okura, M., Sato, M., Osaki, M. and Sekizaki, T. 2011. Loss of capsule among Streptococcus suis isolates from porcine endocarditis and its biological significance. J. Med. Microbiol. 60: 1669-1676.
Lakkitjaroen, N., Takamatsu, D., Okura, M., Sato, M., Osaki, M. and Sekizaki, T. 2014. Capsule loss or death: the position of mutations among capsule genes sways the destiny of Streptococcus suis. FEMS Microbiol. Lett. 354(1): 46-54.
Liu, Z., Zheng, H., Gottschalk, M., Bai, X., Lan, R., Ji, S., Liu, H. and Xu, J. 2013. Development of multiplex PCR assays for the identification of the 33 serotypes of Streptococcus suis. PLoS One. 8(8): e72070.
Lun, Z.R., Wang, Q.P., Chen, X.G., Li, A.X. and Zhu, X.Q. 2007. Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect. Dis. 7(3): 201-209.
Meijerink, M., Ferrando, M.L., Lammers, G., Taverne, N., Smith, H.E. and Wells, J.M. 2012. Immunomodulatory effects of Streptococcus suis capsule type on human dendritic cell responses, phagocytosis and intracellular survival. PLoS One. 7(4): e35849.
Melchiorre, S., Camilli, R., Pietrantoni, A., Moschioni, M., Berti, F., Del Grosso, M., Superti, F., Barocchi, M. A. and Pantosti, A. 2012. Point mutations in wchA are responsible for the non-typability of two invasive Streptococcus pneumoniae isolates. Microbiology. 158: 338-344.
Nghia, H.D., Hoa, N.T., Linh le, D., Campbell, J., Diep, T.S., Chau, N.V., Mai, N.T., Hien, T.T., Spratt, B., Farrar, J. and Schultsz, C. 2008. Human case of Streptococcus suis serotype 16 infection. Emerg. Infect. Dis. 14(1): 155-157.
Nghia, H.D., Tu le, T.P., Wolbers, M., Thai, C.Q., Hoang, N.V., Nga, T.V., Thao le, T.P., Phu, N.H., Chau, T.T., Sinh, D.X., Diep, T.S., Hang, H.T., Truong, H., Campbell, J., Chau, N.V., Chinh, N.T., Dung, N.V., Hoa, N.T., Spratt, B.G., Hien, T.T., Farrar, J. and Schultsz, C. 2011. Risk factors of Streptococcus suis infection in Vietnam. A case-control study. PLoS One. 6(3): e17604.
Nomoto, R., Maruyama, F., Ishida, S., Tohya, M., Sekizaki, T. and Osawa R. 2015. Reappraisal of the taxonomy of Streptococcus suis serotypes 20, 22 and 26: Streptococcus parasuis sp. nov. Int. J. Syst. Evol. Microbiol. 65: 438-443.
Okura, M., Lachance, C., Osaki, M., Sekizaki, T., Maruyama, F., Nozawa, T., Nakagawa, I., Hamada, S., Rossignol, C., Gottschalk, M. and Takamatsu, D. 2014. Development of a two-step multiplex PCR assay for typing of capsular polysaccharide synthesis gene clusters of Streptococcus suis. J. Clin. Microbiol. 52(5): 1714-1719.
Okwumabua, O., O'Connor, M. and Shull, E. 2003. A polymerase chain reaction (PCR) assay specific for Streptococcus suis based on the gene encoding the glutamate dehydrogenase. FEMS Microbiol. Lett. 218(1): 79-84.
Padungtod, P., Tharavichitkul, P., Junya, S., Chaisowong, W., Kadohira, M., Makino, S. and Sthitmatee, N. 2010. Incidence and presence of virulence factors of Streptococcus suis infection in slaughtered pigs from Chiang Mai, Thailand. Southeast Asian J. Trop. Med. Public Health. 41(6): 1454-1461.
Perch, B., Pedersen, K.B. and Henrichsen, J. 1983. Serology of capsulated streptococci pathogenic for pigs: six new serotypes of Streptococcus suis. J. Clin. Microbiol. 17(6): 993-996.
Princivalli, M.S., Palmieri, C., Magi, G., Vignaroli, C., Manzin, A., Camporese, A., Barocci, S., Magistrali, C. and Facinelli, B. 2009. Genetic diversity of Streptococcus suis clinical isolates from pigs and humans in Italy (2003-2007). Euro Surveill. 14(33): pii: 19310.
Salasia, S. I., Lammler, C. and Herrmann, G. 1995. Properties of a Streptococcus suis isolate of serotype 2 and two capsular mutants. Vet. Microbiol. 45(2-3): 151-156.
Segura, M. 2009. Streptococcus suis: an emerging human threat. J. Infect. Dis. 199(1): 4-6.
Segura, M. and Gottschalk, M. 2002. Streptococcus suis interactions with the murine macrophage cell line J774: adhesion and cytotoxicity. Infect. Immun. 70(8): 4312-4322.
Smith, H. E., Damman, M., van der Velde, J., Wagenaar, F., Wisselink, H. J., Stockhofe-Zurwieden, N. and Smits, M. A. 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(4): 1750-1756.
Staats, J.J., Feder, I., Okwumabua, O. and Chengappa, M.M. 1997. Streptococcus suis: past and present. Vet. Res. Commun. 21(6): 381-407.
Sullam, P. M., Bayer, A. S., Foss, W. M. and Cheung, A. L. 1996. Diminished platelet binding in vitro by Staphylococcus aureus is associated with reduced virulence in a rabbit model of infective endocarditis. Infect. Immun. 64(12): 4915-4921.
Takeuchi, D., Kerdsin, A., Pienpringam, A., Loetthong, P., Samerchea, S., Luangsuk, P., Khamisara, K., Wongwan, N., Areeratana, P., Chiranairadul, P., Lertchayanti, S., Petcharat, S., Yowang, A., Chaiwongsaen, P., Nakayama, T., Akeda, Y., Hamada, S., Sawanpanyalert, P., Dejsirilert, S. and Oishi, K. 2012. Population-based study of Streptococcus suis infection in humans in Phayao Province in northern Thailand. PLoS One. 7(2): e31265.
Tan, J.H., Yeh, B.I. and Seet, C.S. 2010. Deafness due to haemorrhagic labyrinthitis and a review of relapses in Streptococcus suis meningitis. Singapore Med. J. 51(2): e30-33.
Tanabe, S., Bonifait, L., Fittipaldi, N., Grignon, L., Gottschalk, M. and Grenier, D. 2010. Pleiotropic effects of polysaccharide capsule loss on selected biological properties of Streptococcus suis. Can. J. Vet. Res. 74(1): 65-70.
Tien le, H.T., Nishibori, T., Nishitani, Y., Nomoto, R. and Osawa, R. 2013. Reappraisal of the taxonomy of Streptococcus suis serotypes 20, 22, 26, and 33 based on DNA-DNA homology and sodA and recN phylogenies. Vet. Microbiol. 162(2-4): 842-849.
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. Vet. Microbiol. 137(1-2): 196-201.
Wertheim, H.F., Nghia, H.D., Taylor, W. and Schultsz, C. 2009. Streptococcus suis: an emerging human pathogen. Clin. Infect. Dis. 48(5): 617-625.
Wisselink, H.J., Reek, F.H., Vecht, U., Stockhofe-Zurwieden, N., Smits, M.A. and Smith, H.E. 1999. Detection of virulent strains of Streptococcus suis type 2 and highly virulent strains of Streptococcus suis type 1 in tonsillar specimens of pigs by PCR. Vet. Microbiol. 67(2): 143-157.
Wisselink, H.J., Smith, H.E., 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. Vet. Microbiol. 74(3): 237-248.
Yu, H., Jing, H., Chen, Z., Zheng, H., Zhu, X., Wang, H., Wang, S., Liu, L., Zu, R., Luo, L., Xiang, N., Liu, H., Liu, X., Shu, Y., Lee, S.S., Chuang, S.K., Wang, Y., Xu, J. and Yang, W. 2006. Human Streptococcus suis outbreak, Sichuan, China. Emerg. Infect. Dis. 12(6): 914-920.