Capsular sialic acid of streptococcus suis serotype 2 binds to swine influenza virus and enhances bacterial interactions with virus-infected tracheal epithelial cells

Infection and Immunity

Volumn 81, Issue 12, 2013, Pages 4498-4508

  Wang, Yingchao ^a,b   Gagnon, Carl A ^a   Savard, Christian ^a   Music, Nedzad ^a   Srednik, Mariela ^a   Segura, Mariela ^a   Lachance, Claude ^a   Bellehumeur, Christian ^a   Gottschalk, Marcelo ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b JILIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; CAPSULAR POLYSACCHARIDE; CHEMOKINE; COMPLEMENTARY DNA; CYTOKINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; COLONY FORMING UNIT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPITHELIUM CELL; GENE SEQUENCE; HEMAGGLUTINATION INHIBITION TEST; INFLAMMATION; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; MIXED INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY TRACT INFECTION; SCANNING ELECTRON MICROSCOPY; STREPTOCOCCUS SUIS; SWINE DISEASE; SWINE INFLUENZA VIRUS; TRACHEA MUCOSA; TRANSMISSION ELECTRON MICROSCOPY; VIRUS INFECTION; ZOONOSIS;

ANIMALS; BACTERIAL ADHESION; CELL LINE; EPITHELIAL CELLS; INFLUENZA A VIRUS, H1N1 SUBTYPE; N-ACETYLNEURAMINIC ACID; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS SUIS; SWINE; TRACHEA;

EID: 84890236144     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00818-13     Document Type: Article

References (57)

1. Gottschalk M. 2012. Streptococcocis, p 841-855. In Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ (ed), Diseases of swine, 10th ed. Blackwell Publishing, Ames, IA.
2. Gottschalk M, Xu J, Calzas C, Segura M. 2010. Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol. 5:371-391.
3. Ye C, Zheng H, Zhang J, Jing H, Wang L, Xiong Y, Wang W, Zhou Z, Sun Q, Luo X, Du H, Gottschalk M, Xu J. 2009. Clinical, experimental, and genomic differences between intermediately pathogenic, highly pathogenic, and epidemic Streptococcus suis. J. Infect. Dis. 199:97-107.
4. Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ. 2007. Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect. Dis. 7:201-209.
5. Wertheim HF, Nghia HD, Taylor W, Schultsz C. 2009. Streptococcus suis: an emerging human pathogen. Clin. Infect. Dis. 48:617-625.
6. Fittipaldi N, Segura M, Grenier D, Gottschalk M. 2012. Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol. 7:259-279.
7. Ferrando ML, Fuentes S, de GreeffA, Smith H, Wells JM. 2010. ApuA, a multifunctional alpha-glucan-degrading enzyme of Streptococcus suis, mediates adhesion to porcine epithelium and mucus. Microbiology 156:2818-2828.
8. Van Calsteren MR, Gagnon F, Lacouture S, Fittipaldi N, Gottschalk M. 2010. Structure determination of Streptococcus suis serotype 2 capsular polysaccharide. Biochem. Cell Biol. 88:513-525.
9. Benga L, Goethe R, Rohde M, Valentin-Weigand P. 2004. Nonencapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cell Microbiol. 6:867-881.
10. Lalonde M, Segura M, Lacouture S, Gottschalk M. 2000. Interactions between Streptococcus suis serotype 2 and different epithelial cell lines. Microbiology 146:1913-1921.
11. Baums CG, Valentin-Weigand P. 2009. Surface-associated and secreted factors of Streptococcus suis in epidemiology, pathogenesis and vaccine development. Anim. Health Res. Rev. 10:65-83.
12. Smith AM, Adler FR, Ribeiro RM, Gutenkunst RN, McAuley JL, Mc-Cullers JA, Perelson AS. 2013. Kinetics of coinfection with influenza A virus and Streptococcus pneumoniae. PLoS Pathog. 9:e1003238. doi:10.1371/journal.ppat.1003238.
13. Jung K, Ha Y, Chae C. 2005. Pathogenesis of swine influenza virus subtype H1N2 infection in pigs. J. Comp. Pathol. 132:179-184.
14. Loving CL, Brockmeier SL, Vincent AL, Palmer MV, Sacco RE, Nicholson TL. 2010. Influenza virus coinfection with Bordetella bronchiseptica enhances bacterial colonization and host responses exacerbating pulmonary lesions. Microb. Pathog. 49:237-245.
15. Opriessnig T, Gimenez-Lirola LG, Halbur PG. 2011. Polymicrobial respiratory disease in pigs. Anim. Health Res. Rev. 12:133-148.
16. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y. 1998. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72:7367-7373.
17. 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.
18. Lun S, Perez-Casal J, Connor W, Willson PJ. 2003. Role of suilysin in pathogenesis of Streptococcus suis capsular serotype 2. Microb. Pathog. 34:27-37.
19. Fittipaldi N, Harel J, D'Amours B, Lacouture S, Kobisch M, Gottschalk M. 2007. Potential use of an unencapsulated and aromatic amino acidauxotrophic Streptococcus suis mutant as a live attenuated vaccine in swine. Vaccine 25:3524-3535.
20. Fittipaldi N, Sekizaki T, Takamatsu D, Harel J, Dominguez-Punaro Mde L, Von Aulock S, Draing C, Marois C, Kobisch M, Gottschalk M. 2008. D-alanylation of lipoteichoic acid contributes to the virulence of Streptococcus suis. Infect. Immun. 76:3587-3594.
21. Fittipaldi N, Sekizaki T, Takamatsu D, Dominguez-Punaro Mde L, Harel J, Bui NK, Vollmer W, Gottschalk M. 2008. Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol. Microbiol. 70:1120-1135.
22. Bikour MH, Frost EH, Deslandes S, Talbot B, Elazhary Y. 1995. Persistence of a 1930 swine influenzaA(H1N1) virus in Quebec. J. Gen. Virol. 76:2539-2547.
23. Ferrari M, Scalvini A, Losio MN, Corradi A, Soncini M, Bignotti E, Milanesi E, Ajmone-Marsan P, Barlati S, Bellotti D, Tonelli M. 2003. Establishment and characterization of two new pig cell lines for use in virological diagnostic laboratories. J. Virol. Methods 107:205-212.
24. Bouchet B, Vanier G, Jacques M, Auger E, Gottschalk M. 2009. Studies on the interactions of Haemophilus parasuis with porcine epithelial tracheal cells: limited role of LOS in apoptosis and pro-inflammatory cytokine release. Microb. Pathog. 46:108-113.
25. Tremblay D, Allard V, Doyon JF, Bellehumeur C, Spearman JG, Harel J, Gagnon CA. 2011. Emergence of a new swine H3N2 and pandemic (H1N1) 2009 influenza A virus reassortant in two Canadian animal populations, mink and swine. J. Clin. Microbiol. 49:4386-4390.
26. Lecours MP, Fittipaldi N, Takamatsu D, Okura M, Segura M, Goyette-Desjardins G, Van Calsteren MR, Gottschalk M. 2012. Sialylation of Streptococcus suis serotype 2 is essential for capsule expression but is not responsible for the main capsular epitope. Microbes Infect. 14:941-950.
27. Higgins R, Gottschalk M. 1990. An update on Streptococcus suis identification. J. Vet. Diagn. Investig. 2:249-252.
28. Lecours MP, Segura M, Lachance C, Mussa T, Surprenant C, Montoya M, Gottschalk M. 2011. Characterization of porcine dendritic cell response to Streptococcus suis. Vet. Res. 42:72.
29. Jacques M, Gottschalk M, Foiry B, Higgins R. 1990. Ultrastructural study of surface components of Streptococcus suis. J. Bacteriol. 172:2833-2838.
30. Van Calsteren MR, Gagnon F, Calzas C, Goyette-Desjardins G, Okura M, Takamatsu D, Gottschalk M, Segura M. 2013. Structure determination of Streptococcus suis serotype 14 capsular polysaccharide. Biochem. Cell Biol. 91:49-58.
31. Charland N, Kellens JT, Caya F, Gottschalk M. 1995. Agglutination of Streptococcus suis by sialic acid-binding lectins. J. Clin. Microbiol. 33:2220-2221.
32. Smith HE, de Vries R, van't Slot R, Smits MA. 2000. The cps locus of Streptococcus suis serotype 2: genetic determinant for the synthesis of sialic acid. Microb. Pathog. 29:127-134.
33. Okura M, Takamatsu D, Maruyama F, Nozawa T, Nakagawa I, Osaki M, Sekizaki T, Gottschalk M, Kumagai Y, Hamada S. 2013. Genetic analysis of capsular polysaccharide synthesis gene clusters from all serotypes of Streptococcus suis: potential mechanisms for the generation of capsular variation. Appl. Environ. Microbiol. 79:2796-2806.
34. Berthelot-Herault F, Gottschalk M, Labbe A, Cariolet R, Kobisch M. 2001. Experimental airborne transmission of Streptococcus suis capsular type 2 in pigs. Vet. Microbiol. 82:69-80.
35. Dominguez-Punaro MC, Koedel U, Hoegen T, Demel C, Klein M, Gottschalk M. 2012. Severe cochlear inflammation and vestibular syndrome in an experimental model of Streptococcus suis infection in mice. Eur. J. Clin. Microbiol. Infect. Dis. 31:2391-2400.
36. Pallares FJ, Halbur PG, Opriessnig T, Sorden SD, Villar D, Janke BH, Yaeger MJ, Larson DJ, Schwartz KJ, Yoon KJ, Hoffman LJ. 2002. Porcine circovirus type 2 (PCV-2) coinfections in US field cases of postweaning multisystemic wasting syndrome (PMWS). J. Vet. Diagn. Investig. 14:515-519.
37. Schmitt CS, Halbur PG, Roth JA, Kinyon JM, Kasorndorkbua C, Thacker B. 2001. Influence of ampicillin, ceftiofur, attenuated live PRRSV vaccine, and reduced dose Streptococcus suis exposure on disease associated with PRRSV and S. suis coinfection. Vet. Microbiol. 78:29-37.
38. Williamson SM, Tucker AW, McCrone IS, Bidewell CA, Brons N, Habernoll H, Essen SC, Brown IH, Cosi Wood JL. 2012. Descriptive clinical and epidemiological characteristics of influenza A H1N1 2009 virus infections in pigs in England. Vet. Rec. 171:271.
39. Avadhanula V, Rodriguez CA, Devincenzo JP, Wang Y, Webby RJ, Ulett GC, Adderson EE. 2006. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J. Virol. 80:1629-1636.
40. Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. 2013. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog. 9:e1003057. doi:10.1371/journal.ppat.1003057.
41. Pittet LA, Hall-Stoodley L, Rutkowski MR, Harmsen AG. 2010. Influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am. J. Resp. Cell Mol. Biol. 42:450-460.
42. McCullers JA, Bartmess KC. 2003. Role of neuraminidase in lethal synergism between influenza virus and Streptococcus pneumoniae. J. Infect. Dis. 187:1000-1009.
43. Nishikawa T, Shimizu K, Tanaka T, Kuroda K, Takayama T, Yamamoto T, Hanada N, Hamada Y. 2012. Bacterial neuraminidase rescues influenza virus replication from inhibition by a neuraminidase inhibitor. PLoS One 7:e45371. doi:10.1371/journal.pone.0045371.
44. Okamoto S, Kawabata S, Terao Y, Fujitaka H, Okuno Y, Hamada S. 2004. The Streptococcus pyogenes capsule is required for adhesion of bacteria to virus-infected alveolar epithelial cells and lethal bacterial-viral superinfection. Infect. Immun. 72:6068-6075.
45. Swildens B, Stockhofe-Zurwieden N, van der Meulen J, Wisselink HJ, Nielen M, Niewold TA. 2004. Intestinal translocation of Streptococcus suis type 2 EF+ in pigs. Vet. Microbiol. 103:29-33.
46. Hosaka Y, Kuroda K, Ikeura A, Iwamoto T, Suzuki Y. 1998. Binding of influenza and paramyxoviruses to group B Streptococcus with the terminal sialyl-galactose linkage. J. Electron Microsc. 47:169-174.
47. Rameix-Welti MA, Zarantonelli ML, Giorgini D, Ruckly C, Marasescu M, van der Werf S, Alonso JM, Naffakh N, Taha MK. 2009. Influenza A virus neuraminidase enhances meningococcal adhesion to epithelial cells through interaction with sialic acid-containing meningococcal capsules. Infect. Immun. 77:3588-3595.
48. Passariello C, Nencioni L, Sgarbanti R, Ranieri D, Torrisi MR, Ripa S, Garaci E, Palamara AT. 2011. Viral hemagglutinin is involved in promoting the internalisation of Staphylococcus aureus into human pneumocytes during influenza A H1N1 virus infection. Int. J. Med. Microbiol. 301:97-104.
49. Lam WY, Yeung AC, Chu IM, Chan PK. 2010. Profiles of cytokine and chemokine gene expression in human pulmonary epithelial cells induced by human and avian influenza viruses. Virol. J. 7:344.
50. Tong HH, Long JP, Shannon PA, DeMaria TF. 2003. Expression of cytokine and chemokine genes by human middle ear epithelial cells induced by influenza A virus and Streptococcus pneumoniae opacity variants. Infect. Immun. 71:4289-4296.
51. Dominguez-Punaro MC, Segura M, Plante MM, Lacouture S, Rivest S, 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. J. Immunol. 179:1842-1854.
52. Schwerk C, Adam R, Borkowski J, Schneider H, Klenk M, Zink S, Quednau N, Schmidt N, Stump C, Sagar A, Spellerberg B, Tenenbaum T, Koczan D, Klein-Hitpass L, Schroten H. 2011. In vitro transcriptome analysis of porcine choroid plexus epithelial cells in response to Streptococcus suis: release of pro-inflammatory cytokines and chemokines. Microb. Infect. 13:953-962.
53. Vadeboncoeur N, Segura M, Al-Numani D, Vanier G, Gottschalk M. 2003. Pro-inflammatory cytokine and chemokine release by human brain microvascular endothelial cells stimulated by Streptococcus suis serotype 2. FEMS Immun. Med. Microbiol. 35:49-58.
54. Wareing MD, Lyon AB, Lu B, Gerard C, Sarawar SR. 2004. Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J. Leukoc. Biol. 76:886-895.
55. Smith HE, Damman M, van der Velde J, Wagenaar F, Wisselink HJ, Stockhofe-Zurwieden N, 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. Infect. Immun. 67:1750-1756.
56. Charland N, Kobisch M, Martineau-Doize B, Jacques M, Gottschalk M. 1996. Role of capsular sialic acid in virulence and resistance to phagocytosis of Streptococcus suis capsular type 2. FEMS Immun. Med. Microbiol. 14:195-203.
57. Gottschalk M, Higgins R, Jacques M, Mittal KR, Henrichsen J. 1989. Description of 14 new capsular types of Streptococcus suis. J. Clin. Microbiol. 27:2633-2636.