Toll-like receptor 2 deficiency results in impaired antibody responses and septic shock during Borrelia hermsii infection

Infection and Immunity

Volumn 78, Issue 11, 2010, Pages 4579-4588

  Dickinson, Gregory S ^a   Piccone, Heather ^a   Sun, Guizhi ^a   Lien, Egil ^b   Gatto, Louis ^c,d   Alugupalli, Kishore R ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

^d STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; CASPASE RECRUITMENT DOMAIN PROTEIN 15; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTEREMIA; BORRELIA HERMSII; BORRELIA HERMSII INFECTION; BORRELIA INFECTION; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOKINE RESPONSE; DEATH; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; INFLAMMATION; MACROPHAGE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTIC SHOCK; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODY FORMATION; BACTEREMIA; BORRELIA; CELL LINE; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NOD2 SIGNALING ADAPTOR PROTEIN; RELAPSING FEVER; SHOCK, SEPTIC; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2;

EID: 78049448242     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00438-10     Document Type: Article

References (65)

1. Abraham, E., and M. Singer. 2007. Mechanisms of sepsis-induced organ dysfunction. Crit. Care Med. 35:2408-2416.
2. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
3. Alugupalli, K. R. 2008. A distinct role for B1b lymphocytes in T-cell-independent immunity. Curr. Top. Microbiol. Immunol. 319:105-130.
4. Alugupalli, K. R., S. Akira, E. Lien, and J. M. Leong. 2007. MyD88- and Bruton's tyrosine kinase-mediated signals are essential for T-cell-independent pathogen-specific IgM responses. J. Immunol. 178:3740-3749.
5. Alugupalli, K. R., R. M. Gerstein, J. Chen, E. Szomolanyi-Tsuda, R. T. Woodland, and J. M. Leong. 2003. The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J. Immunol. 170:3819-3827.
6. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T-cell-independent long-lasting immunity. Immunity 21:379-390.
7. Alugupalli, K. R., A. D. Michelson, M. R. Barnard, D. Robbins, J. Coburn, E. K. Baker, M. H. Ginsberg, T. G. Schwan, and J. M. Leong. 2001. Platelet activation by a relapsing fever spirochete results in enhanced bacteriumplatelet interaction via integrin αIIbβ3 activation. Mol. Microbiol. 39:330-340.
8. Alugupalli, K. R., A. D. Michelson, I. Joris, T. G. Schwan, K. Hodivala-Dilke, R. O. Hynes, and J. M. Leong. 2003. Spirochete-platelet attachment and thrombocytopenia in murine relapsing fever borreliosis. Blood 102:2843-2850.
9. Angus, D. C., W. T. Linde-Zwirble, J. Lidicker, G. Clermont, J. Carcillo, and M. R. Pinsky. 2001. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29:1303-1310.
10. Ansel, K. M., R. B. Harris, and J. G. Cyster. 2002. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16:67-76.
11. Bagshaw, S. M., S. Lapinsky, S. Dial, Y. Arabi, P. Dodek, G. Wood, P. Ellis, J. Guzman, J. Marshall, J. E. Parrillo, Y. Skrobik, and A. Kumar. 2009. Acute kidney injury in septic shock: clinical outcomes and impact of duration of hypotension prior to initiation of antimicrobial therapy. Intensive Care Med. 35:871-881.
12. Balasz, M., F. Martin, T. Zhou, and J. F. Kearney. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17:341-352.
13. Barbour, A. G. 1990. Antigenic variation of a relapsing fever Borrelia species. Annu. Rev. Microbiol. 44:155-171.
14. Barbour, A. G., and V. Bundoc. 2001. In vitro and in vivo neutralization of the relapsing fever agent Borrelia hermsii with serotype-specific immunoglobulin M antibodies. Infect. Immun. 69:1009-1015.
15. Bernasconi, N. L., N. Onai, and A. Lanzavecchia. 2003. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101:4500-4504.
16. Bolz, D. D., R. S. Sundsbak, Y. Ma, S. Akira, J. H. Weis, T. G. Schwan, and J. J. Weis. 2006. Dual role of MyD88 in rapid clearance of relapsing fever Borrelia spp. Infect. Immun. 74:6750-6760.
17. Cadavid, D., and A. G. Barbour. 1998. Neuroborreliosis during relapsing fever: review of the clinical manifestations, pathology, and treatment of infections in humans and experimental animals. Clin. Infect. Dis. 26:151-164.
18. Colombo, M. J., and K. R. Alugupalli. 2008. Complement factor H-binding protein, a putative virulence determinant of Borrelia hermsii, is an antigenic target for protective B1b lymphocytes. J. Immunol. 180:4858-4864.
19. Connolly, S. E., and J. L. Benach. 2005. The versatile roles of antibodies in Borrelia infections. Nat. Rev. Microbiol. 3:411-420.
20. Dear, J. W., H. Yasuda, X. Hu, S. Hieny, P. S. Yuen, S. M. Hewitt, A. Sher, and R. A. Star. 2006. Sepsis-induced organ failure is mediated by different pathways in the kidney and liver: acute renal failure is dependent on MyD88 but not renal cell apoptosis. Kidney Int. 69:832-836.
21. Efron, P. A., K. Tinsley, D. J. Minnich, V. Monterroso, J. Wagner, P. Lainee, K. Lorre, P. E. Swanson, R. Hotchkiss, and L. L. Moldawer. 2004. Increased lymphoid tissue apoptosis in baboons with bacteremic shock. Shock 21:566-571.
22. Fisher, C. J., Jr., J. F. Dhainaut, S. M. Opal, J. P. Pribble, R. A. Balk, G. J. Slotman, T. J. Iberti, E. C. Rackow, M. J. Shapiro, R. L. Greenman, et al. 1994. Recombinant human interleukin 1 receptor antagonist in the treatment of patients with sepsis syndrome: results from a randomized, doubleblind, placebo-controlled trial. JAMA 271:1836-1843.
23. Franchi, L., J. H. Park, M. H. Shaw, N. Marina-Garcia, G. Chen, Y. G. Kim, and G. Nuñez. 2008. Intracellular NOD-like receptors in innate immunity, infection, and disease. Cell Microbiol. 10:1-8. (Pubitemid 350239051)
24. Fritz, J. H., R. L. Ferrero, D. J. Philpott, and S. E. Girardin. 2006. Nod-like proteins in immunity, inflammation, and disease. Nat. Immunol. 7:1250-1257.
25. Gebbia, J. A., J. C. Monco, J. L. Degen, T. H. Bugge, and J. L. Benach. 1999. The plasminogen activation system enhances brain and heart invasion in murine relapsing fever borreliosis. J. Clin. Invest. 103:81-87.
26. Gelderblom, H., D. Londono, Y. Bai, E. S. Cabral, J. Quandt, R. Hornung, R. Martin, A. Marques, and D. Cadavid. 2007. High production of CXCL13 in blood and brain during persistent infection with the relapsing fever spirochete Borrelia turicatae. J. Neuropathol Exp. Neurol. 66:208-217.
27. Girardin, S. E., I. G. Boneca, L. A. Carneiro, A. Antignac, M. Jehanno, J. Viala, K. Tedin, M. K. Taha, A. Labigne, U. Zahringer, A. J. Coyle, P. S. DiStefano, J. Bertin, P. J. Sansonetti, and D. J. Philpott. 2003. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300:1584-1587.
28. Girardin, S. E., L. H. Travassos, M. Herve, D. Blanot, I. G. Boneca, D. J. Philpott, P. J. Sansonetti, and D. Mengin-Lecreulx. 2003. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278:41702-41708.
29. Gururajan, M., J. Jacob, and B. Pulendran. 2007. Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets. PLoS One 2:e863.
30. Ha, S. A., M. Tsuji, K. Suzuki, B. Meek, N. Yasuda, T. Kaisho, and S. Fagarasan. 2006. Regulation of B1 cell migration by signals through Toll-like receptors. J. Exp. Med. 203:2541-2550.
31. Hiramatsu, M., R. S. Hotchkiss, I. E. Karl, and T. G. Buchman. 1997. Cecal ligation and puncture (CLP) induces apoptosis in thymus, spleen, lung, and gut by an endotoxin and TNF-independent pathway. Shock 7:247-253.
32. Hotchkiss, R. S., P. E. Swanson, J. P. Cobb, A. Jacobson, T. G. Buchman, and I. E. Karl. 1997. Apoptosis in lymphoid and parenchymal cells during sepsis: findings in normal and T- and B-cell-deficient mice. Crit. Care Med. 25:1298-1307.
33. Hotchkiss, R. S., P. E. Swanson, B. D. Freeman, K. W. Tinsley, J. P. Cobb, G. M. Matuschak, T. G. Buchman, and I. E. Karl. 1999. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 27:1230-1251.
34. + T lymphocytes in humans. J. Immunol. 166:6952-6963.
35. Inohara, N., M. Chamaillard, C. McDonald, and G. Nuñez. 2005. NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74:355-383.
36. Kawai, T., and S. Akira. 2009. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 21:317-337.
37. Kim, Y. G., J. H. Park, M. H. Shaw, L. Franchi, N. Inohara, and G. Nuñez. 2008. The cytosolic sensors Nod1 and Nod2 are critical for bacterial recognition and host defense after exposure to Toll-like receptor ligands. Immunity 28:246-257.
38. Klaviter, E. C., and R. C. Johnson. 1979. Isolation of the outer envelope, chemical components, and ultrastructure of Borrelia hermsii grown in vitro. Acta Trop. 36:123-131.
39. Kumar, A., D. Roberts, K. E. Wood, B. Light, J. E. Parrillo, S. Sharma, R. Suppes, D. Feinstein, S. Zanotti, L. Taiberg, D. Gurka, A. Kumar, and M. Cheang. 2006. Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit. Care Med. 34:1589-1596.
40. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401.
41. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416:603-607.
42. Lopez, A., J. A. Lorente, J. Steingrub, J. Bakker, A. McLuckie, S. Willatts, M. Brockway, A. Anzueto, L. Holzapfel, D. Breen, M. S. Silverman, J. Takala, J. Donaldson, C. Arneson, G. Grove, S. Grossman, and R. Grover. 2004. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit. Care Med. 32:21-30.
43. Malley, R., P. Henneke, S. C. Morse, M. J. Cieslewicz, M. Lipsitch, C. M. Thompson, E. Kurt-Jones, J. C. Paton, M. R. Wessels, and D. T. Golenbock. 2003. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc. Natl. Acad. Sci. U. S. A. 100:1966-1971.
44. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14:617-629.
45. Meylan, E., J. Tschopp, and M. Karin. 2006. Intracellular pattern recognition receptors in the host response. Nature 442:39-44.
46. Mikkelsen, M. E., A. N. Miltiades, D. F. Gaieski, M. Goyal, B. D. Fuchs, C. V. Shah, S. L. Bellamy, and J. D. Christie. 2009. Serum lactate is associated with mortality in severe sepsis independent of organ failure and shock. Crit. Care Med. 37:1670-1677.
47. Miyaji, T., X. Hu, P. S. Yuen, Y. Muramatsu, S. Iyer, S. M. Hewitt, and R. A. Star. 2003. Ethyl pyruvate decreases sepsis-induced acute renal failure and multiple organ damage in aged mice. Kidney Int. 64:1620-1631.
48. Nilsen, N., U. Nonstad, N. Khan, C. F. Knetter, S. Akira, A. Sundan, T. Espevik, and E. Lien. 2004. Lipopolysaccharide and double-stranded RNA up-regulate Toll-like receptor two independently of myeloid differentiation factor 88. J. Biol. Chem. 279:39727-39735.
49. Okada, T., and J. G. Cyster. 2006. B-cell migration and interactions in the early phase of antibody responses. Curr. Opin. Immunol. 18:278-285.
50. Opal, S. M., C. J. Fisher, Jr., J. F. Dhainaut, J. L. Vincent, R. Brase, S. F. Lowry, J. C. Sadoff, G. J. Slotman, H. Levy, R. A. Balk, M. P. Shelly, J. P. Pribble, J. F. LaBrecque, J. Lookabaugh, H. Donovan, H. Dubin, R. Baughman, J. Norman, E. DeMaria, K. Matzel, E. Abraham, and M. Seneff. 1997. Confirmatory interleukin-1 receptor antagonist trial in severe sepsis: a phase III, randomized, double-blind, placebo-controlled, multicenter trial. Crit. Care Med. 25:1115-1124.
51. Osuchowski, M. F., K. Welch, J. Siddiqui, and D. G. Remick. 2006. Circulating cytokine/inhibitor profiles reshape the understanding of the SIRS/CARS continuum in sepsis and predict mortality. J. Immunol. 177:1967-1974.
52. Plitas, G., B. M. Burt, H. M. Nguyen, Z. M. Bamboat, and R. P. DeMatteo. 2008. Toll-like receptor 9 inhibition reduces mortality in polymicrobial sepsis. J. Exp. Med. 205:1277-1283.
53. Reinhart, K., and W. Karzai. 2001. Anti-tumor necrosis factor therapy in sepsis: update on clinical trials and lessons learned. Crit. Care Med. 29:S121-125.
54. Riedemann, N. C., R. F. Guo, and P. A. Ward. 2003. The enigma of sepsis. J. Clin. Invest. 112:460-467.
55. Rivers, E., B. Nguyen, S. Havstad, J. Ressler, A. Muzzin, B. Knoblich, E. Peterson, and M. Tomlanovich. 2001. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N. Engl. J. Med. 345:1368-1377.
56. Rupprecht, T. A., C. J. Kirschning, B. Popp, S. Kastenbauer, V. Fingerle, H. W. Pfister, and U. Koedel. 2007. Borrelia garinii induces CXCL13 production in human monocytes through Toll-like receptor 2. Infect. Immun. 75:4351-4356.
57. Schroder, K., and J. Tschopp. The inflammasomes. Cell 140:821-832.
58. Schwan, T. G., and B. J. Hinnebusch. 1998. Bloodstream- versus tick-associated variants of a relapsing fever bacterium. Science 280:1938-1940.
59. Southern, P. M., Jr., and J. P. Sanford. 1969. Relapsing fever: a clinical and microbiological review. Medicine 48:129-149.
60. Strober, W., P. J. Murray, A. Kitani, and T. Watanabe. 2006. Signaling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6:9-20.
61. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17:1-14.
62. Watanabe, T., A. Kitani, P. J. Murray, and W. Strober. 2004. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat. Immunol. 5:800-808.
63. Watanabe, T., A. Kitani, P. J. Murray, Y. Wakatsuki, I. J. Fuss, and W. Strober. 2006. Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis. Immunity 25:473-485.
64. Yasuda, H., P. S. Yuen, X. Hu, H. Zhou, and R. A. Star. 2006. Simvastatin improves sepsis-induced mortality and acute kidney injury via renal vascular effects. Kidney Int. 69:1535-1542.
65. Zhang, D., G. Zhang, M. S. Hayden, M. B. Greenblatt, C. Bussey, R. A. Flavell, and S. Ghosh. 2004. A Toll-like receptor that prevents infection by uropathogenic bacteria. Science 303:1522-1526.