Group B Streptococcus and Streptococcus suis capsular polysaccharides induce chemokine production by dendritic cells via Toll-like receptor 2-and MyD88-dependent and -independent pathways

Infection and Immunity

Volumn 81, Issue 9, 2013, Pages 3106-3118

  Calzas, Cynthia ^a   Goyette Desjardins, Guillaume ^a   Lemire, Paul ^a   Gagnon, Fleur ^b   Lachance, Claude ^a   Van Calsteren, Marie Rose ^b   Segura, Mariela ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b FOOD RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; MYELOID DIFFERENTIATION FACTOR 88; POLYSACCHARIDE; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMORAL IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SEROTYPE; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS SUIS;

EID: 84884262828     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00113-13     Document Type: Article

References (92)

1. Edwards MS, Baker CJ. 2005. Group B streptococcal infections in elderly adults. Clin. Infect. Dis. 41:839-847.
2. Koenig JM, Keenan WJ. 2009. Group B Streptococcus and early-onset sepsis in the era of maternal prophylaxis. Pediatr. Clin. North Am. 56:689-708.
3. Blumberg HM, Stephens DS, Modansky M, Erwin M, Elliot J, Facklam RR, Schuchat A, Baughman W, Farley MM. 1996. Invasive group B streptococcal disease: the emergence of serotype V. J. Infect. Dis. 173:365-373.
4. 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.
5. Segura M. 2009. Streptococcus suis: an emerging human threat. J. Infect. Dis. 199:4-6.
6. 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.
7. Kerdsin A, Oishi K, Sripakdee S, Boonkerd N, Polwichai P, Nakamura S, Uchida R, Sawanpanyalert P, Dejsirilert S. 2009. Clonal dissemination of human isolates of Streptococcus suis serotype 14 in Thailand. J. Med. Microbiol. 58:1508-1513.
8. Cieslewicz MJ, Chaffin D, Glusman G, Kasper D, Madan A, Rodrigues S, Fahey J, Wessels MR, Rubens CE. 2005. Structural and genetic diversity of group B Streptococcus capsular polysaccharides. Infect. Immun. 73:3096-3103.
9. 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.
10. 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.
11. Van Calsteren MR, 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.
12. Lecours MP, Gottschalk M, Houde M, Lemire P, Fittipaldi N, Segura M. 2011. Critical role for Streptococcus suis cell wall modifications and suilysin in resistance to complement-dependent killing by dendritic cells. J. Infect. Dis. 204:919-929.
13. Lemire P, Houde M, Lecours MP, Fittipaldi N, Segura M. 2012. Role of capsular polysaccharide in group B Streptococcus interactions with dendritic cells. Microbes Infect. 14:1064-1076.
14. Segura MA, Cleroux P, Gottschalk M. 1998. Streptococcus suis and group B Streptococcus differ in their interactions with murine macrophages. FEMS Immunol. Med. Microbiol. 21:189-195.
15. 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.
16. Takahashi S, Aoyagi Y, Adderson EE, Okuwaki Y, Bohnsack JF. 1999. Capsular sialic acid limits C5a production on type III group B streptococci. Infect. Immun. 67:1866-1870.
17. Crocker PR, Paulson JC, Varki A. 2007. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7:255-266.
18. Chaffin DO, Mentele LM, Rubens CE. 2005. Sialylation of group B streptococcal capsular polysaccharide is mediated by cpsK and is required for optimal capsule polymerization and expression. J. Bacteriol. 187:4615-4626.
19. 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.
20. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820.
21. Steinman RM. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271-296.
22. Mond JJ, Vos Q, Lees A, Snapper CM. 1995. T cell independent antigens. Curr. Opin. Immunol. 7:349-354.
23. Weintraub A. 2003. Immunology of bacterial polysaccharide antigens. Carbohydr. Res. 338:2539-2547.
24. Simpson SQ, Singh R, Bice DE. 1994. Heat-killed pneumococci and pneumococcal capsular polysaccharides stimulate tumor necrosis factor-α production by murine macrophages. Am. J. Respir. Cell Mol. Biol. 10:284-289.
25. Wang Q, McLoughlin RM, Cobb BA, Charrel-Dennis M, Zaleski KJ, Golenbock D, Tzianabos AO, Kasper DL. 2006. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 203:2853-2863.
26. d'Empaire G, Baer MT, Gibson FC, 3rd. 2006. The K1 serotype capsular polysaccharide of Porphyromonas gingivalis elicits chemokine production from murine macrophages that facilitates cell migration. Infect. Immun. 74:6236-6243.
27. Zughaier SM. 2011. Neisseria meningitidis capsular polysaccharides induce inflammatory responses via TLR2 and TLR4-MD-2. J. Leukoc. Biol. 89:469-480.
28. Soell M, Diab M, Haan-ArchipoffG, Beretz A, Herbelin C, Poutrel B, Klein JP. 1995. Capsular polysaccharide types 5 and 8 of Staphylococcus aureus bind specifically to human epithelial (KB) cells, endothelial cells, and monocytes and induce release of cytokines. Infect. Immun. 63:1380-1386.
29. Litinskiy MB, Nardelli B, Hilbert DM, He B, Schaffer A, Casali P, Cerutti A. 2002. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3:822-829.
30. Craxton A, Magaletti D, Ryan EJ, Clark EA. 2003. Macrophage- and dendritic cell-dependent regulation of human B-cell proliferation requires the TNF family ligand BAFF. Blood 101:4464-4471.
31. Jacques M, Gottschalk M, Foiry B, Higgins R. 1990. Ultrastructural study of surface components of Streptococcus suis. J. Bacteriol. 172:2833-2838.
32. 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.
33. Kuypers JM, Heggen LM, Rubens CE. 1989. Molecular analysis of a region of the group B Streptococcus chromosome involved in type III capsule expression. Infect. Immun. 57:3058-3065.
34. Michon F. June 2001. Procedures for the extraction and isolation of bacterial capsular polysaccharides for use as vaccines or linked to proteins as conjugate vaccines. US patent 6,248,570 B1.
35. Brandrup J, Immergut EH, Grulke EA. 2005. Polymer handbook, 4th ed. John Wiley&Sons, New York, NY.
36. Gornik O, Lauc G. 2007. Enzyme linked lectin assay (ELLA) for direct analysis of transferrin sialylation in serum samples. Clin. Biochem. 40:718-723.
37. Shibuya N, Goldstein IJ, Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ. 1987. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(α2-6)Gal/GalNAc sequence. J. Biol. Chem. 262:1596-1601.
38. Geisler C, Jarvis DL. 2011. Effective glycoanalysis with Maackia amurensis lectins requires a clear understanding of their binding specificities. Glycobiology 21:988-993.
39. Miller RL, Collawn JF, Jr, Fish WW. 1982. Purification and macromolecular properties of a sialic acid-specific lectin from the slug Limax flavus. J. Biol. Chem. 257:7574-7580.
40. Charland N, Jacques M, Lacouture S, Gottschalk M. 1997. Characterization and protective activity of a monoclonal antibody against a capsular epitope shared by Streptococcus suis serotypes 1, 2 and 1/2. Microbiology 143:3607-3614.
41. Higgins R, Gottschalk M. 1990. An update on Streptococcus suis identification. J. Vet. Diagn. Invest. 2:249-252.
42. Animal Welfare Committee of the Université de Montréal. 2012. Guide for the care and use of laboratory animals. Animal Welfare Committee of the Université de Montréal, Montréal, Canada.
43. Segura M, Su Z, Piccirillo C, Stevenson MM. 2007. Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. Eur. J. Immunol. 37:1887-1904.
44. van den Berg TK, Kraal G. 2005. A function for the macrophage F4/80 molecule in tolerance induction. Trends Immunol. 26:506-509.
45. MacDonald AS, Straw AD, Bauman B, Pearce EJ. 2001. CD8-dendritic cell activation status plays an integral role in influencing Th2 response development. J. Immunol. 167:1982-1988.
46. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, Schuler G. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223:77-92.
47. -ΔΔCT method. Methods 25:402-408.
48. Deng L, Kasper DL, Krick TP, Wessels MR. 2000. Characterization of the linkage between the type III capsular polysaccharide and the bacterial cell wall of group B Streptococcus. J. Biol. Chem. 275:7497-7504.
49. Gonzalez-Outeirino J, Kadirvelraj R, Woods RJ. 2005. Structural elucidation of type III group B Streptococcus capsular polysaccharide using molecular dynamics simulations: the role of sialic acid. Carbohydr. Res. 340:1007-1018.
50. Guttormsen HK, Paoletti LC, Mansfield KG, Jachymek W, Jennings HJ, Kasper DL. 2008. Rational chemical design of the carbohydrate in a glycoconjugate vaccine enhances IgM-to-IgG switching. Proc. Natl. Acad. Sci. U. S. A. 105:5903-5908.
51. Jennings HJ, Lugowski C, Kasper DL. 1981. Conformational aspects critical to the immunospecificity of the type III group B streptococcal polysaccharide. Biochemistry 20:4511-4518.
52. Knibbs RN, Goldstein IJ, Ratcliffe RM, Shibuya N. 1991. Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J. Biol. Chem. 266:83-88.
53. Graveline R, Segura M, Radzioch D, Gottschalk M. 2007. TLR2-dependent recognition of Streptococcus suis is modulated by the presence of capsular polysaccharide which modifies macrophage responsiveness. Int. Immunol. 19:375-389.
54. Lecours MP, Segura M, Fittipaldi N, Rivest S, Gottschalk M. 2012. Immune receptors involved in Streptococcus suis recognition by dendritic cells. PLoS One 7:e44746. doi:10.1371/journal.pone.0044746.
55. Draper DW, Bethea HN, He YW. 2006. Toll-like receptor 2-dependent and -independent activation of macrophages by group B streptococci. Immunol. Lett. 102:202-214.
56. Henneke P, Takeuchi O, van Strijp JA, Guttormsen HK, Smith JA, Schromm AB, Espevik TA, Akira S, Nizet V, Kasper DL, Golenbock DT. 2001. Novel engagement of CD14 and multiple Toll-like receptors by group B streptococci. J. Immunol. 167:7069-7076.
57. Um SH, Rhee DK, Pyo S. 2002. Involvement of protein kinase C and tyrosine kinase in tumoricidal activation of macrophage induced by Streptococcus pneumoniae type II capsular polysaccharide. Int. Immunopharmacol. 2:129-137.
58. Kanswal S, Katsenelson N, Allman W, Uslu K, Blake MS, Akkoyunlu M. 2011. Suppressive effect of bacterial polysaccharides on BAFF system is responsible for their poor immunogenicity. J. Immunol. 186:2430-2443.
59. Kim HA, Jeon SH, Seo GY, Park JB, Kim PH. 2008. TGF-β1 and IFN-γ stimulate mouse macrophages to express BAFF via different signaling pathways. J. Leukoc. Biol. 83:1431-1439.
60. Nardelli B, Belvedere O, Roschke V, Moore PA, Olsen HS, Migone TS, Sosnovtseva S, Carrell JA, Feng P, Giri JG, Hilbert DM. 2001. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 97:198-204.
61. Courtney AH, Puffer EB, Pontrello JK, Yang ZQ, Kiessling LL. 2009. Sialylated multivalent antigens engage CD22 in trans and inhibit B cell activation. Proc. Natl. Acad. Sci. U. S. A. 106:2500-2505.
62. Elliott SD, Clifton-Hadley F, 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. J. Hyg. (Lond.) 85:275-285.
63. Baums CG, Kock C, Beineke A, Bennecke K, Goethe R, Schroder C, Waldmann KH, Valentin-Weigand P. 2009. Streptococcus suis bacterin and subunit vaccine immunogenicities and protective efficacies against serotypes 2 and 9. Clin. Vaccine Immunol. 16:200-208.
64. del Campo Sepulveda EM, Altman E, Kobisch M, D'Allaire S, Gottschalk M. 1996. Detection of antibodies against Streptococcus suis capsular type 2 using a purified capsular polysaccharide antigen-based indirect ELISA. Vet. Microbiol. 52:113-125.
65. Heath PT. 2011. An update on vaccination against group B Streptococcus. Expert Rev. Vaccines 10:685-694.
66. Baker CJ, Kasper DL. 1976. Correlation of maternal antibody deficiency with susceptibility to neonatal group B streptococcal infection. N. Engl. J. Med. 294:753-756.
67. Avci FY, Kasper DL. 2010. How bacterial carbohydrates influence the adaptive immune system. Annu. Rev. Immunol. 28:107-130.
68. Wessels MR, Paoletti LC, Rodewald AK, Michon F, DiFabio J, Jennings HJ, Kasper DL. 1993. Stimulation of protective antibodies against type Ia and Ib group B streptococci by a type Ia polysaccharide-tetanus toxoid conjugate vaccine. Infect. Immun. 61:4760-4766.
69. Finne J, Leinonen M, Makela PH. 1983. Antigenic similarities between brain components and bacteria causing meningitis. Implications for vaccine development and pathogenesis. Lancet ii:355-357.
70. Moe GR, Bhandari TS, Flitter BA. 2009. Vaccines containing de-N-acetyl sialic acid elicit antibodies protective against Neisseria meningitidis groups B and C. J. Immunol. 182:6610-6617.
71. Meijerink M, Ferrando ML, Lammers G, Taverne N, Smith HE, Wells JM. 2012. Immunomodulatory effects of Streptococcus suis capsule type on human dendritic cell responses, phagocytosis and intracellular survival. PLoS One 7:e35849. doi:10.1371/journal.pone.0035849.
72. Segura M, Vanier G, Al-Numani D, Lacouture S, Olivier M, Gottschalk M. 2006. Proinflammatory cytokine and chemokine modulation by Streptococcus suis in a whole-blood culture system. FEMS Immunol. Med. Microbiol. 47:92-106.
73. Segura M, Stankova J, Gottschalk M. 1999. Heat-killed Streptococcus suis capsular type 2 strains stimulate tumor necrosis factor alpha and interleukin-6 production by murine macrophages. Infect. Immun. 67:4646-4654.
74. Vallejo JG, Baker CJ, Edwards MS. 1996. Roles of the bacterial cell wall and capsule in induction of tumor necrosis factor alpha by type III group B streptococci. Infect. Immun. 64:5042-5046.
75. Vallejo JG, Baker CJ, Edwards MS. 1996. Interleukin-6 production by human neonatal monocytes stimulated by type III group B streptococci. J. Infect. Dis. 174:332-337.
76. Meltzer U, Goldblatt D. 2006. Pneumococcal polysaccharides interact with human dendritic cells. Infect. Immun. 74:1890-1895.
77. Kocabas C, Katsenelson N, Kanswal S, Kennedy MN, Cui X, Blake MS, Segal DM, Akkoyunlu M. 2007. Neisseria meningitidis type C capsular polysaccharide inhibits lipooligosaccharide-induced cell activation by binding to CD14. Cell. Microbiol. 9:1297-1310.
78. Carlin AF, Uchiyama S, Chang YC, Lewis AL, Nizet V, Varki A. 2009. Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 113:3333-3336.
79. Ando M, Tu W, Nishijima K, Iijima S. 2008. Siglec-9 enhances IL-10 production in macrophages via tyrosine-based motifs. Biochem. Biophys. Res. Commun. 369:878-883.
80. Deshmane SL, Kremlev S, Amini S, Sawaya BE. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29:313-326.
81. Maurer M, von Stebut E. 2004. Macrophage inflammatory protein-1. Int. J. Biochem. Cell Biol. 36:1882-1886.
82. Lahrtz F, Piali L, Spanaus KS, Seebach J, Fontana A. 1998. Chemokines and chemotaxis of leukocytes in infectious meningitis. J. Neuroimmunol. 85:33-43.
83. 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.
84. Okazaki K, Kondo M, Kato M, Nishida A, Takahashi H, Noda M, Kimura H. 2008. Temporal alterations in concentrations of sera cytokines/chemokines in sepsis due to group B Streptococcus infection in a neonate. Jpn. J. Infect. Dis. 61:382-385.
85. i proteins. Immunology 122:116-123.
86. Lemire P, Houde M, Segura M. 2012. Encapsulated group B Streptococcus modulates dendritic cell functions via lipid rafts and clathrin-mediated endocytosis. Cell. Microbiol. 14:1707-1719.
87. Mogensen TH, Paludan SR, Kilian M, Ostergaard L. 2006. Live Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis activate the inflammatory response through Toll-like receptors 2, 4, and 9 in species-specific patterns. J. Leukoc. Biol. 80:267-277.
88. Mitchell D, Olive C. 2010. Regulation of Toll-like receptor-induced chemokine production in murine dendritic cells by mitogen-activated protein kinases. Mol. Immunol. 47:2065-2073.
89. Zamze S, Martinez-Pomares L, Jones H, Taylor PR, Stillion RJ, Gordon S, Wong SY. 2002. Recognition of bacterial capsular polysaccharides and lipopolysaccharides by the macrophage mannose receptor. J. Biol. Chem. 277:41613-41623.
90. Moon EY, Lee JH, Oh SY, Ryu SK, Kim HM, Kwak HS, Yoon WK. 2006. Reactive oxygen species augment B-cell-activating factor expression. Free Radic. Biol. Med. 40:2103-2111.
91. Houde M, Gottschalk M, Gagnon F, Van Calsteren MR, Segura M. 2012. Streptococcus suis capsular polysaccharide inhibits phagocytosis through destabilization of lipid microdomains and prevents lactosylceramide-dependent recognition. Infect. Immun. 80:506-517.
92. Segura M, Gottschalk M, Olivier M. 2004. Encapsulated Streptococcus suis inhibits activation of signaling pathways involved in phagocytosis. Infect. Immun. 72:5322-5330.