TLR2-dependent recognition of Streptococcus suis is modulated by the presence of capsular polysaccharide which modifies macrophage responsiveness

International Immunology

Volumn 19, Issue 4, 2007, Pages 375-389

  Graveline, Richard ^a   Segura, Mariela ^b   Radzioch, Danuta ^b   Gottschalk, Marcelo ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; CD14 ANTIGEN; CHEMOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BACTERIAL CELL WALL; C57BL MOUSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MOLECULAR RECOGNITION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS SUIS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD14; CELL LINE; CELL LINE, TUMOR; CELL WALL; CHEMOKINE CCL2; GENE EXPRESSION; HUMANS; IMMUNITY, NATURAL; INTERLEUKINS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; OLIGOPEPTIDES; POLYSACCHARIDES, BACTERIAL; RNA, MESSENGER; STREPTOCOCCUS SUIS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34047113955     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxm003     Document Type: Article

References (71)

1. Gottschalk, M. and Segura, M. 2000. The pathogenesis of the meningitis caused by Streptococcus suis: The unresolved questions. Vet. Microbiol. 75:59.
2. Higgins, R. and Gottschalk, M. 2005. Streptococal diseases. In Straw, B. E., D'Allaire, S., Mengeling, W. L. and Taylor, D. J., eds, Diseases of Swine, p. 769. Iowa State University, Ames.
3. Sriskandan, S. and Slater, J. D. 2006. Invasive disease and toxic shock due to zoonotic Streptococcus suis: An emerging infection in the East? PLoS Med. 3:e187.
4. Tang, J., Wang, C., Feng, Y. et al. 2006. Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med. 3:e151.
5. Yu, H., Jing, H., Chen, Z. et al. 2006. Human Streptococcus suis outbreak, Sichuan, China. Emerg. Infect. Dis. 12:914.
6. Smith, H. E., Damman, M., Van der Velde, J. 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.
7. Segura, M., Gottschalk, M. and Olivier, M. 2004. Encapsulated Streptococcus suis inhibits activation of signaling pathways involved in phagocytosis. Infect. Immun. 72:5322.
8. Charland, N., Harel, J., Kobish, M., Lacasse, S. and Gottschalk, M. 1998. Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology 144:325.
9. de Greeff, A., Buys, H., Verhaar, R., Dijkstra, J., van Alphen, L. and Smith, H. E. 2002. Contribution of fibronectin-binding protein to pathogenesis of Streptococcus suis serotype 2. Infect. Immun. 70:1319.
10. Smith, H. E., Wisselink, H. J., Stockhofe-Zurwieden, N., Vecht, U. and Smits, M. M. 1997. Virulence markers of Streptococcus suis type 1 and 2. In Horaud, A., ed., Streptococci and the Host, p. 651. Plenum Press, New York.
11. Jobin, M. C., Fortin, J., Willson, P. J., Gottschalk, M. and Grenier, D. 2005. Acquisition of plasmin activity and induction of arachidonic acid release by Streptococcus suis in contact with human brain microvascular endothelial cells. FEMS Microbiol. Lett. 252:105.
12. Winterhoff, N., Goethe, R., Gruening, P. et al. 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. J. Bacteriol. 184:6768.
13. Valentin-Weigand, P. 2004. Intracellular invasion and persistence: survival strategies of Streptococcus suis and Mycobacterium avium ssp. paratuberculosis. Berl. Muench. Tieraerztl. Wochenschr. 117:459.
14. Lun, S. and Willson, P. J. 2004. Expression of green fluorescent protein and its application in pathogenesis studies of serotype 2 Streptococcus suis. J. Microbiol. Methods 56:401.
15. Segura, M. A., Cléroux, P. and Gottschalk, M. 1998. Streptococcus suis and group B Streptococcus differ in their interactions with murine macrophages. FEMS Immunol. Med. Microbiol. 21:189.
16. Chabot-Roy, G., Willson, P., Segura, M., Lacouture, S. and Gottschalk, M. 2006. Phagocytosis and killing of Streptococcus suis by porcine neutrophils. Microb. Pathog. 41:21.
17. Vanier, G., Segura, M., Friedl, P., Lacouture, S. and Gottschalk, M. 2004. Invasion of porcine brain microvascular endothelial cells by Streptococcus suis serotype 2. Infect. Immun. 72:1441.
18. 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 52:392.
19. Adam, R., Tenenbaum, T., Valentin-Weigand, P. et al. 2004. Porcine choroid plexus epithelial cells induce Streptococcus suis bacteriostasis in vitro. Infect. Immun. 72:3084.
20. 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 Immunol. Med. Microbiol. 35:49.
21. Tenenbaum, T., Adam, R., Eggelnpohler, I. et al. 2005. Strain-dependent disruption of blood-cerebrospinal fluid barrier by Streptoccocus suis in vitro. FEMS Immunol. Med. Microbiol. 44:25.
22. Segura, M., Stankova, J. and 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.
23. Segura, M., Vadeboncoeur, N. and 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.
24. Segura, M., Vanier, G., Lacouture, S., Olivier, M. and Gottschalk, M. 2006. Pro-inflammatory cytokine and chemokine modulation by Streptococcus suis serotype 2 in a porcine whole blood culture system. FEMS Immunol. Med. Microbiol. 47:92.
25. Al-Numani, D., Segura, M., Doré, M. and Gottschalk, M. 2002. Up-regulation of ICAM-1, CD11a/CD18 and CD11c/CD18 on human THP-1 monocytes stimulated by Streptococcus suis serotype 2. Clin. Exp. Immunol. 133:67.
26. Wright, S. M., Ramos, R. A., Tobias, P. S., Ulevitch, R. J. and Mathison, J. C. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431.
27. Wright, S. M. 1995. CD14 and innate recognition of bacteria. J. Immunol. 155:6.
28. Moreillon, P. and Majcherczyk, P. A. 2003. Proinflammatory activity of cell-wall constituents from gram-positive bacteria. Scand. J. Infect. Dis. 35:632.
29. Akira, S. and Takeda, K. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499.
30. Beutler, B. 2004. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430:257.
31. Beutler, B. 2005. The Toll-like receptors: Analysis by forward genetic methods. Immunogenetics 57:385.
32. Akira, S. and Hemmi, H. 2003. Recognition of pathogenassociated molecular patterns by TLR family. Immunol. Lett. 85:85.
33. Henneke, P., Takeuchi, O., van Strijp, J. A. et al. 2001. Novel engagement of CD14 and multiple Toll-like receptors by Group B Streptococci. J. Immunol. 167:7069.
34. Manukyan, M., Triantafilou, K., Triantafilou, M. et al. 2005. Binding of lipopeptide to CD14 induces physical proximity of CD14, TLR2 and TLR1. Eur. J. Immunol. 35:911.
35. Hattar, K., Grandel, U., Moeller, A. et al. 2006. Lipoteichoic acid (LTA) from Staphylococcus aureus stimulates human neutrophil cytokine release by a CD14-dependent, Toll-like-receptor-independent mechanism: autocrine role of tumor necrosis factor-[alpha] in mediating LTA-induced interleukin-8 generation. Crit. Care Med. 34:835.
36. Henneke, P., Takeuchi, O., Malley, R. et al. 2002. Cellular activation, phagocytosis, and bacterial activity against Group B Streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways. J. Immunol. 169:3970.
37. Flo, T. H., Halaas, O., Lien, E. et al. 2000. Human toll-like receptor 2 mediates monocyte activation by Listeria monocytogenes, but not by group B Streptococci or lipopolysaccharide. J. Immunol. 164:2064.
38. Um, S. H., Rhee, D. K. and Pyo, S. 2002. Involvement of protein kinase C and tyrosin kinase in tumoricidal activation of macrophage induced by Streptococcus pneumoniae type II capsular polysaccharide. Int. Immunopharmacol. 2:129.
39. Raffatellu, M., Chessa, D., Wilson, R. P., Dusold, R., Rubino, S. and Baumler, A. J. 2005. The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect. Immun. 73:3367.
40. Kobisch, M., Gottschalk, M., Morvan, P., Cariolet, R., Bénévent, G. and Joly, J. P. 1995. Experimental infection of SPF piglets with Streptococcus suis serotype 2. J. Rech. Porcine Fr. 27:97.
41. del Campo Sepulveda, E. M., 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. Vet. Microbiol. 52:113.
42. Tuomanen, E., Tomasz, A., Hengstler, B. and Zak, O. 1985. The relative role of bacterial cell wall and capsule in the induction of inflammation in pneumococcal meningitis. J. Infect. Dis. 151:535.
43. Heumann, D., Barras, C., Severin, A., Glauser, M. P. and Tomasz, A. 1994. Gram-positive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes. Infect. Immun. 62:2715.
44. Blasi, E., Mathieson, B. J., Varesio, L., Cleveland, J. L., Borchert, P. A. and Rapp, U. R. 1986. Selective immortalization of murine macrophages from fresh bone marrow by a raf/myc recombinant murine retrovirus. Nature 318:667.
45. Blasi, E., Mucci, A., Neglia, R. et al. 2005. Biological importance of the two Toll-like receptors, TLR2 and TLR4, in macrophage response to infection with Candida albicans. FEMS Immunol. Med. Microbiol. 44:69.
46. Takeuchi, O., Hoshino, K., Kawai, T. et al. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Grampositive bacterial cell wall components. Immunity 11:443.
47. Adachi, O., Kawai, T., Takeda, K. et al. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9:143.
48. Cox, G., Mathieson, B. J., Gandino, L., Blasi, E., Radzioch, D. and Varesio, L. 1989. Heterogeneity of hemopoietic cells immortalized by v-raf/v-myc recombinant retrovirus infection of bone marrow or fetal liver. J. Natl Cancer Inst. 81:1492.
49. Zhang, F. X., Kirschning, C. J., Mancinelli, R. et al. 1999. Bacterial lipopolysaccharide activates nuclear factor-jB through interleukin-1 signalling mediators in cultured human endothelial cells and mononuclear phagocytes. J. Biol. Chem. 274:7611.
50. Kaufmann, A., Muhlradt, P. F., Gemsa, D. and Sprenger, H. 1999. Induction of cytokines and chemokines in human monocytes by Mycoplasma fermentans-derived lipoprotein MALP-2. Infect. Immun. 67:6303.
51. Poltorak, A., He, X., Smirnova, I. et al. 1998. Defective LPS signalling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282:2085.
52. Tamai, R., Sugawara, S., Takeuchi, O., Akira, S. and Takada, H. 2003. Synergistic effects of lipopolysaccharide and interferongamma in inducing interleukin-8 production in human monocytic THP-1 cells is accompanied by up-regulation of CD14, Toll-like receptor 4, MD-2 and MyD88 expression. J. Endotoxin Res. 9:145.
53. Hajishengallis, G., Tapping, R. I., Martin, M. H. et al. 2005. Toll-like receptor 2 mediates cellular activation by the B subunits of type II heat-labile enterotoxins. Infect. Immun. 73:1343.
54. Giambartolomei, G. H., Zwerdling, A., Cassataro, J., Bruno, L., Fossati, C. A. and Philipp, M. T. 2004. Lipoproteins, not lipopolysaccharide, are the key mediators of the proinflammatory response elicited by heat-killed Brucella abortus. J. Immunol. 173:4635.
55. Wang, J. H., Doyle, M., Manning, B. J., Di Wu, Q., Blankson, S. and Redmond, H. P. 2002. Induction of bacterial lipoprotein tolerance is associated with suppression of toll-like receptor 2 expression. J. Biol. Chem. 277:36068.
56. Nomura, F., Akashi, S., Sakao, Y. et al. 2000. Cutting edge: Endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface Toll-like receptor 4 expression. J. Immunol. 164:3476.
57. Medvedev, A. E., Kopydlowski, K. M. and Vogeland, S. N. 2000. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: Dysregulation of cytokine, chemokine, and Toll-like receptor 2 and 4 gene expression. J. Immunol. 164:5564.
58. Sato, S., Nomura, F., Kawai, T. et al. 2000. Synergy and cross-tolerance between Toll-like receptor (TLR) 2- and TLR4-mediated signaling pathways. J. Immunol. 165:7096.
59. Labeta, M. O., Durieux, J. J., Spagnoli, G., Fernandez, N., Wijdenes, J. and Herrmann, R. 1993. CD14 and tolerance to lipopolysaccharide: biochemical and functional analysis. Immunology 80:415.
60. Mambula, S. S., Sau, K., Henneke, P., Golenbock, D. T. and Levitz, S. M. 2002. Toll-like receptor (TLR) signaling in response to Aspergillus fumigatus. J. Biol. Chem. 277:39320.
61. Mancuso, G., Midiri, A., Beninati, C. et al. 2004. Dual role of TLR2 and myeloid differentiation factor 88 in a mouse model of invasive group B streptococcal disease. J. Immunol. 172:6324.
62. Khan, A. Q., Chen, Q., Wu, Z. Q., Paton, J. C. and Snapper, C. M. 2005. Both innate immunity and type 1 humoral immunity to Streptococcus pneumoniae are mediated by MyD88 but differ in their relative levels of dependence on toll-like receptor 2. Infect. Immun. 73:298.
63. Pridmore, A. C., Jarvis, G. A., John, C. M., Jack, D. L., Dower, S. K. and Read, R. C. 2003. Activation of toll-like receptor 2 (TLR2) and TLR4/ MD2 by Neisseria is independent of capsule and lipooligosaccharide (LOS) sialylation but varies widely among LOS from different strains. Infect. Immun. 71:3901.
64. Um, S. H., Son, E. W., Kim, B. O., Moon, E. Y., Rhee, D. K. and Pyo, S. 2000. Activation of murine peritoneal macrophages by Streptococcus pneumoniae type II capsular polysaccharide: Involvement of CD14-dependent pathway. Scand. J. Immunol. 52:39.
65. Schwarz, M., Wahl, M., Resch, K. and Radeke, H. H. 2002. IFNgamma induces functional chemokine receptor expression in human mesangial cells. Clin. Exp. Immunol. 128:285.
66. Liu, Y., Wang, Y., Yamakuchi, M. et al. 2001. Up-regulation of Tolllike receptor 2 gene expression in macrophage response to peptidoglycan and high concentration of lipopolysacharide is involved in NF-jB activation. Infect. Immun. 69:2788.
67. Musikacharoen, T., Matsuguchi, T., Kikuchi, T. and Yoshikai, Y. 2001. NF-kappa B and STAT5 play important roles in the regulation of mouse Toll-like receptor 2 gene expression. J. Immunol. 166:4516.
68. Wheeler, M. D. and Thurman, R. G. 2003. Up-regulation of CD14 in liver caused by acute ethanol involves oxidant-dependent AP-1 pathway. J. Biol. Chem. 278:8435.
69. Song, L. and Pachter, J. S. 2004. Monocyte chemoattractant protein-1 alters expression of tight junction-associated proteins in brain microvascular endothelial cells. Microvasc. Res. 67:78.
70. Charland, N., Nizet, V., Rubens, C., Kim, K. S., Lacouture, S. and Gottschalk, M. 2000. Streptococcus suis serotype 2 interactions with human brain microvascular endothelial cells. Infect. Immun. 68:637.
71. Dominguez, M., Plante, M., Segura, M., Lacouture, S., Rivest, S. and Gottschalk, M. 2006. Usefulness of a mouse experimental model of infection to study systemic and cerebral inflammation associated to Streptococcus suis. International Society for Infectious Diseases, p. S309. (abstract).