Chronic Exposure to Staphylococcal Superantigen Elicits a Systemic Inflammatory Disease Mimicking Lupus

Journal of Immunology

Volumn 189, Issue 4, 2012, Pages 2054-2062

  Chowdhary, Vaidehi R ^a   Tilahun, Ashenafi Y ^a   Clark, Chad R ^a   Grande, Joseph P ^a   Rajagopalan, Govindarajan ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINUCLEAR ANTIBODY; CD28 ANTIGEN; GAMMA INTERFERON; HLA DQ8 ANTIGEN; INTERLEUKIN 12; STAPHYLOCOCCUS ENTEROTOXIN B; STAT4 PROTEIN; SUPERANTIGEN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR V BETA 8; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; GLOMERULUS; INFLAMMATORY DISEASE; KIDNEY; LIVER; LUNG; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIGENS, CD28; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HLA-DQ ANTIGENS; HUMANS; INFUSIONS, SUBCUTANEOUS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, TRANSGENIC; STAPHYLOCOCCUS AUREUS; SUPERANTIGENS;

EID: 84864797526     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201097     Document Type: Article

References (61)

1. Sfriso, P., A. Ghirardello, C. Botsios, M. Tonon, M. Zen, N. Bassi, F. Bassetto, and A. Doria. 2010. Infections and autoimmunity: the multifaceted relationship. J. Leukoc. Biol. 87: 385-395.
2. Schiffenbauer, J., J. Soos, and H. Johnson. 1998. The possible role of bacterial superantigens in the pathogenesis of autoimmune disorders. Immunol. Today 19: 117-120. (Pubitemid 28194657)
3. Fraser, J. D., and T. Proft. 2008. The bacterial superantigen and superantigen-like proteins. Immunol. Rev. 225: 226-243.
4. Kissner, T. L., G. Ruthel, S. Alam, R. G. Ulrich, S. Fernandez, and K. U. Saikh. 2011. Activation of MyD88 signaling upon staphylococcal enterotoxin binding to MHC class II molecules. PLoS ONE 6: e15985.
5. Murray, R. J. 2005. Recognition and management of Staphylococcus aureus toxin-mediated disease. Intern. Med. J. 35(Suppl. 2): S106-S119. (Pubitemid 44933544)
6. Lappin, E., and A. J. Ferguson. 2009. Gram-positive toxic shock syndromes. Lancet Infect. Dis. 9: 281-290.
7. Graham, P. L., III, S. X. Lin, and E. L. Larson. 2006. A U.S. population-based survey of Staphylococcus aureus colonization. Ann. Intern. Med. 144: 318-325.
8. Sivaraman, K., N. Venkataraman, and A. M. Cole. 2009. Staphylococcus aureus nasal carriage and its contributing factors. Future Microbiol. 4: 999-1008.
9. Frank, D. N., L. M. Feazel, M. T. Bessesen, C. S. Price, E. N. Janoff, and N. R. Pace. 2010. The human nasal microbiota and Staphylococcus aureus carriage. PLoS ONE 5: e10598.
10. Kluytmans, J., A. van Belkum, and H. Verbrugh. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10: 505-520. (Pubitemid 27359263)
11. Thomas, D., S. Chou, O. Dauwalder, and G. Lina. 2007. Diversity in Staphylococcus aureus enterotoxins. Chem. Immunol. Allergy 93: 24-41. (Pubitemid 46924870)
12. Seiberling, K. A., D. B. Conley, A. Tripathi, L. C. Grammer, L. Shuh, G. K. Haines, III, R. Schleimer, and R. C. Kern. 2005. Superantigens and chronic rhinosinusitis: detection of staphylococcal exotoxins in nasal polyps. Laryngoscope 115: 1580-1585. (Pubitemid 41330665)
13. Van Zele, T., P. Gevaert, J. B. Watelet, G. Claeys, G. Holtappels, C. Claeys, P. van Cauwenberge, and C. Bachert. 2004. Staphylococcus aureus colonization and IgE antibody formation to enterotoxins is increased in nasal polyposis. J. Allergy Clin. Immunol. 114: 981-983. (Pubitemid 39330280)
14. Burian, M., D. Grumann, S. Holtfreter, C. Wolz, C. Goerke, and B. M. Bröker. 2012. Expression of staphylococcal superantigens during nasal colonization is not sufficient to induce a systemic neutralizing antibody response in humans. Eur. J. Clin. Microbiol. Infect. Dis. 31: 251-256.
15. Rajagopalan, G., M. M. Sen, M. Singh, N. S. Murali, K. A. Nath, K. Iijima, H. Kita, A. A. Leontovich, U. Gopinathan, R. Patel, and C. S. David. 2006. Intranasal exposure to staphylococcal enterotoxin B elicits an acute systemic inflammatory response. Shock 25: 647-656. (Pubitemid 44297027)
16. Rajagopalan, G., M. K. Smart, N. Murali, R. Patel, and C. S. David. 2007. Acute systemic immune activation following vaginal exposure to staphylococcal enterotoxin B - implications for menstrual shock. J. Reprod. Immunol. 73: 51-59. (Pubitemid 46161831)
17. Rajagopalan, G., M. K. Smart, R. Patel, and C. S. David. 2006. Acute systemic immune activation following conjunctival exposure to staphylococcal enterotoxin B. Infect. Immun. 74: 6016-6019. (Pubitemid 44484590)
18. Laouini, D., S. Kawamoto, A. Yalcindag, P. Bryce, E. Mizoguchi, H. Oettgen, and R. S. Geha. 2003. Epicutaneous sensitization with superantigen induces allergic skin inflammation. J. Allergy Clin. Immunol. 112: 981-987. (Pubitemid 37412069)
19. Schlievert, P. M., K. L. Strandberg, Y. C. Lin, M. L. Peterson, and D. Y. Leung. 2010. Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J. Allergy Clin. Immunol. 125: 39-49.
20. Iwatsuki, K., O. Yamasaki, S. Morizane, and T. Oono. 2006. Staphylococcal cutaneous infections: invasion, evasion and aggression. J. Dermatol. Sci. 42: 203-214.
21. Nishifuji, K., M. Sugai, and M. Amagai. 2008. Staphylococcal exfoliative toxins: "molecular scissors" of bacteria that attack the cutaneous defense barrier in mammals. J. Dermatol. Sci. 49: 21-31. (Pubitemid 350236706)
22. Stegeman, C. A., J. W. Tervaert, W. J. Sluiter, W. L. Manson, P. E. de Jong, and C. G. Kallenberg. 1994. Association of chronic nasal carriage of Staphylococcus aureus and higher relapse rates in Wegener granulomatosis. Ann. Intern. Med. 120: 12-17. (Pubitemid 24011495)
23. Popa, E. R., C. A. Stegeman, W. H. Abdulahad, B. van der Meer, J. Arends, W. M. Manson, N. A. Bos, C. G. M. Kallenberg, and J. W. Tervaert. 2007. Staphylococcal toxic-shock-syndrome-toxin-1 as a risk factor for disease relapse in Wegener's granulomatosis. Rheumatology (Oxford) 46: 1029-1033. (Pubitemid 47062516)
24. Mulvey, M. R., M. Doupe, M. Prout, C. Leong, R. Hizon, A. Grossberndt, M. Klowak, A. Gupta, M. Melanson, A. Gomori, et al. 2011. Staphylococcus aureus harbouring Enterotoxin A as a possible risk factor for multiple sclerosis exacerbations. Mult. Scler. 17: 397-403.
25. Jackson, M. S., J. Bagg, M. N. Gupta, and R. D. Sturrock. 1999. Oral carriage of staphylococci in patients with rheumatoid arthritis. Rheumatology (Oxford) 38: 572-575. (Pubitemid 29504846)
26. Tabarya, D., and W. L. Hoffman. 1996. Staphylococcus aureus nasal carriage in rheumatoid arthritis: antibody response to toxic shock syndrome toxin-1. Ann. Rheum. Dis. 55: 823-828. (Pubitemid 26392282)
27. DaSilva, L., B. C. Welcher, R. G. Ulrich, M. J. Aman, C. S. David, and S. Bavari. 2002. Humanlike immune response of human leukocyte antigen-DR3 transgenic mice to staphylococcal enterotoxins: a novel model for superantigen vaccines. J. Infect. Dis. 185: 1754-1760. (Pubitemid 34615469)
28. Tilahun, A. Y., M. Holz, T.-T. Wu, C. S. David, and G. Rajagopalan. 2011. Interferon gamma-dependent intestinal pathology contributes to the lethality in bacterial superantigen-induced toxic shock syndrome. PLoS ONE 6: e16764.
29. Tilahun, A. Y., E. V. Marietta, T.-T.Wu, R. Patel, C. S. David, and G. Rajagopalan. 2011. Human leukocyte antigen class II transgenic mouse model unmasks the significant extrahepatic pathology in toxic shock syndrome. Am. J. Pathol. 178: 2760-2773.
30. Rajagopalan, G., K. Iijima, M. Singh, H. Kita, R. Patel, and C. S. David. 2006. Intranasal exposure to bacterial superantigens induces airway inflammation in HLA class II transgenic mice. Infect. Immun. 74: 1284-1296. (Pubitemid 43185568)
31. Rajagopalan, G., G. Polich, M. M. Sen, M. Singh, B. E. Epstein, A. K. Lytle, M. S. Rouse, R. Patel, and C. S. David. 2008. Evaluating the role of HLA-DQ polymorphisms on immune response to bacterial superantigens using transgenic mice. Tissue Antigens 71: 135-145.
32. Rajagopalan, G., M. K. Smart, S. Cheng, C. J. Krco, K. L. Johnson, and C. S. David. 2003. Expression and function of HLA-DR3 and DQ8 in transgenic mice lacking functional H2-M. Tissue Antigens 62: 149-161. (Pubitemid 36986599)
33. Rajagopalan, G., M. K. Smart, C. J. Krco, and C. S. David. 2002. Expression and function of transgenic HLA-DQ molecules and lymphocyte development in mice lacking invariant chain. J. Immunol. 169: 1774-1783. (Pubitemid 34857637)
34. Sriskandan, S., M. Unnikrishnan, T. Krausz, H. Dewchand, S. Van Noorden, J. Cohen, and D. M. Altmann. 2001. Enhanced susceptibility to superantigen-associated streptococcal sepsis in human leukocyte antigen-DQ transgenic mice. J. Infect. Dis. 184: 166-173. (Pubitemid 32614045)
35. Chau, T. A., M. L. McCully, W. Brintnell, G. An, K. J. Kasper, E. D. Vinés, P. Kubes, S. M. Haeryfar, J. K. McCormick, E. Cairns, et al. 2009. Toll-like receptor 2 ligands on the staphylococcal cell wall downregulate superantigen-induced T cell activation and prevent toxic shock syndrome. Nat. Med. 15: 641-648.
36. Whary, M. T., T. J. Morgan, C. A. Dangler, K. J. Gaudes, N. S. Taylor, and J. G. Fox. 1998. Chronic active hepatitis induced by Helicobacter hepaticus in the A/JCr mouse is associated with a Th1 cell-mediated immune response. Infect. Immun. 66: 3142-3148. (Pubitemid 28303109)
37. Skerrett, S. J., H. D. Liggitt, A. M. Hajjar, R. K. Ernst, S. I. Miller, and C. B. Wilson. 2004. Respiratory epithelial cells regulate lung inflammation in response to inhaled endotoxin. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L143-L152. (Pubitemid 38787661)
38. Reilly, C. M., L. W. Farrelly, D. Viti, S. T. Redmond, F. Hutchison, P. Ruiz, P. Manning, J. Connor, and G. S. Gilkeson. 2002. Modulation of renal disease in MRL/lpr mice by pharmacologic inhibition of inducible nitric oxide synthase. Kidney Int. 61: 839-846. (Pubitemid 34175449)
39. Chowdhary, V. R., J. P. Grande, H. S. Luthra, and C. S. David. 2007. Characterization of haemorrhagic pulmonary capillaritis: another manifestation of Pristane-induced lupus. Rheumatology (Oxford) 46: 1405-1410. (Pubitemid 47333620)
40. Gebhardt, T., P. G. Whitney, A. Zaid, L. K. Mackay, A. G. Brooks, W. R. Heath, F. R. Carbone, and S. N. Mueller. 2011. Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477: 216-219.
41. Wurster, A. L., T. Tanaka, and M. J. Grusby. 2000. The biology of Stat4 and Stat6. Oncogene 19: 2577-2584. (Pubitemid 30339213)
42. Torres, B. A., and H. M. Johnson. 1998. Modulation of disease by superantigens. Curr. Opin. Immunol. 10: 465-470. (Pubitemid 28393831)
43. Paliard, X., S. G. West, J. A. Lafferty, J. R. Clements, J. W. Kappler, P. Marrack, and B. L. Kotzin. 1991. Evidence for the effects of a superantigen in rheumatoid arthritis. Science 253: 325-329. (Pubitemid 21917160)
44. Kallenberg, C. G. 2010. Pathophysiology of ANCA-associated small vessel vasculitis. Curr. Rheumatol. Rep. 12: 399-405.
45. Tumang, J. R., J. L. Zhou, D. Gietl, M. K. Crow, K. B. Elkon, and S. M. Friedman. 1996. T helper cell-dependent, microbial superantigen-mediated B cell activation in vivo. Autoimmunity 24: 247-255. (Pubitemid 27086934)
46. Stohl, W., J. E. Elliott, and P. S. Linsley. 1994. Human T cell-dependent B cell differentiation induced by staphylococcal superantigens. J. Immunol. 153: 117-127. (Pubitemid 24186524)
47. Berstein, G., and R. T. Abraham. 2008. Moving out: mobilizing activated T cells from lymphoid tissues. Nat. Immunol. 9: 455-457. (Pubitemid 351560509)
48. Bright, J. J., Z. Xin, and S. Sriram. 1999. Superantigens augment antigenspecific Th1 responses by inducing IL-12 production in macrophages. J. Leukoc. Biol. 65: 665-670. (Pubitemid 29227059)
49. Kato, M., Y. Nakamura, T. Suda, Y. Ozawa, N. Inui, N. Seo, T. Nagata, Y. Koide P. Kalinski, H. Nakamura, and K. Chida. 2011. Enhanced anti-tumor immunity by superantigen-pulsed dendritic cells. Cancer Immunol. Immunother. 60: 1029-1038.
50. Tucci, M., L. Lombardi, H. B. Richards, F. Dammacco, and F. Silvestris. 2008. Overexpression of interleukin-12 and T helper 1 predominance in lupus nephritis. Clin. Exp. Immunol. 154: 247-254.
51. Bueno, C., C. D. Lemke, G. Criado, M. L. Baroja, S. S. Ferguson, A. K. Rahman, C. D. Tsoukas, J. K. McCormick, and J. Madrenas. 2006. Bacterial superantigens bypass Lck-dependent T cell receptor signaling by activating a Galpha11-dependent, PLC-beta-mediated pathway. Immunity 25: 67-78. (Pubitemid 44066827)
52. Vinuesa, C. G., S. G. Tangye, B. Moser, and C. R. Mackay. 2005. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 5: 853-865. (Pubitemid 41581667)
53. Sun, J. C., and M. J. Bevan. 2003. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300: 339-342. (Pubitemid 36433727)
54. Singh, R. P., A. La Cava, M. Wong, F. Ebling, and B. H. Hahn. 2007. CD8+ T cell-mediated suppression of autoimmunity in a murine lupus model of peptide-induced immune tolerance depends on Foxp3 expression. J. Immunol. 178: 7649-7657. (Pubitemid 46898035)
55. Lu, J.-W., H.Wang, J. Yan-Li, C. Zhang, H. Ning, X.-Y. Li, H. Zhang, Z.-H. Duan, L. Zhao, W. Wei, and D.-X. Xu. 2008. Differential effects of pyrrolidine dithiocarbamate on TNF-alpha-mediated liver injury in two different models of fulminant hepatitis. J. Hepatol. 48: 442-452.
56. Lu, L., and H. Cantor. 2008. Generation and regulation of CD8(+) regulatory T cells. Cell. Mol. Immunol. 5: 401-406.
57. Kim, H.-J., B. Verbinnen, X. Tang, L. Lu, and H. Cantor. 2010. Inhibition of follicular T-helper cells by CD8(+) regulatory T cells is essential for self tolerance. Nature 467: 328-332.
58. Larinkari, U., M. Leirisalo, P. J. Pentikäinen, U. Turunen, P. Pikkarainen, M. Vuoristo, J. Lumio, T. Räsänen, and V. V. Valtonen. 1983. Occurrence of antibodies to teichoic acid in patients with diseases other than staphylococcal infection. J. Med. Microbiol. 16: 45-52. (Pubitemid 13178082)
59. Wu, Z. Q., D. Drayton, and D. S. Pisetsky. 1997. Specificity and immunochemical properties of antibodies to bacterial DNA in sera of normal human subjects and patients with systemic lupus erythematosus (SLE). Clin. Exp. Immunol. 109: 27-31. (Pubitemid 27293879)
60. Wada, Y., M. Tomikawa, M. Kubo, and Y. Etoh. 2001. [A boy diagnosed SLE after Staphylococcus aureus infection over a long period]. Nihon Rinsho Meneki Gakkai Kaishi 24: 48-56.
61. Furukawa, F., Y. Tokura, K. Matsushita, K. Iwasaki-Inuzuka, K. Onagi-Suzuki, H. Yagi, H. Wakita, and M. Takigawa. 1996. Selective expansions of T cells expressing V beta 8 and V beta 13 in skin lesions of patients with chronic cutaneous lupus erythematosus. J. Dermatol. 23: 670-676. (Pubitemid 26396726)