Identification of a TLR-independent pathway for Borrelia burgdorferi-induced expression of matrix metalloproteinases and inflammatory mediators through binding to integrin α3β1

Journal of Immunology

Volumn 177, Issue 1, 2006, Pages 657-664

  Behera, Aruna K ^a   Hildebrand, Ethan ^a   Uematsu, Satoshi ^b   Akira, Shizuo ^b   Coburn, Jenifer ^a   Hu, Linden T ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; CELL SURFACE RECEPTOR; CHEMOKINE; CYTOKINE; ENTACTIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTEGRIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; LIPOPROTEIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 19; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; RANTES; STRESS ACTIVATED PROTEIN KINASE; STROMELYSIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTICULAR CARTILAGE; BORRELIA BURGDORFERI; CARTILAGE CELL; CELL COMMUNICATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; IMMUNOSTIMULATION; INFECTION CONTROL; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 33745320471     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.1.657     Document Type: Article

References (54)

1. Steere, A. 1989. Lyme disease. N. Engl. J. Med. 321: 586-596.
2. Grygorczuk, S., S. Pancewicz, J. Zajkowska, M. Kondrusik, R. Rwierzbinska, and T. Hermanowska-Szpakowicz. 2004. Concentrations of macrophage inflammatory proteins MTP-1α and MIP-1β and interleukin 8 (IL-8) in Lyme borreliosis. Infection 32: 350-355.
3. Glickstein, L., B. Moore, T. Bledsoe, N. Damle, V. Sikand, and A. C. Steere. 2003. Inflammatory cytokine production predominates in early Lyme disease in patients with erythema migrans. Infect. Immun. 71: 6051-6053.
4. 2 integrins control the severity of murine Lyme carditis. Infect. Immun. 73: 3242-3250.
5. Sprenger, H., A. Krause, A. Kaufmann, S. Priem, D. Fabian, G. R. Burmester, D. Gemsa, and M. G. Rittig. 1997. Borrelia burgdorferi induces chemokines in human monocytes. Infect. Immun. 65: 4384-4388.
6. Hirschfeld, M., C. J. Kirschning, R. Schwandner, H. Wesche, J. H. Weis, R. M. Wooten, and J. J. Weis. 1999. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by Toll-like receptor 2. J. Immunol. 163: 2382-2386.
7. Alexopoulou, L., V. Thomas, M. Schnare, Y. Lobet, J. Anguita, R. T. Schoen, R. Medzhitov, E. Fikrig, and R. A. Flavell. 2002. Hyporesponsiveness to vaccination with Borrelia burgdorferi OspA in humans and in TLR1- and TLR2-deficient mice. Nat. Med. 8: 878-884.
8. Bolz, D. D., R. S. Sundsbak, Y. Ma, S. Akira, C. J. Kirschning, J. F. Zachary, J. H. Weis, and J. J. Weis. 2004. MyD88 plays a unique role in host defense but not arthritis development in Lyme disease. J. Immunol. 173: 2003-2010.
9. Liu, N., R. R. Montgomery, S. W. Barthold, and L. K. Bockenstedt. 2004. Myeloid differentiation antigen 88 deficiency impairs pathogen clearance but does not alter inflammation in Borrelia burgdorferi-infected mice. Infect. Immun. 72: 3195-3203.
10. Lin, B., J. M. Kidder, R. Noring, A. C. Steere, M. S. Klempner, and L. T. Hu. 2001. Differences in synovial fluid levels of matrix metalloproteinases suggest separate mechanisms of pathogenesis in Lyme arthritis before and after antibiotic treatment. J. Infect. Dis. 184: 174-180.
11. Hu, L. T., M. A. Eskildsen, C. Masgala, A. C. Steere, E. C. Arner, M. A. Pratta, A. J. Grodzinsky, A. Loening, and G. Perides. 2001. Host metalloproteinases in Lyme arthritis. Arthritis Rheum. 44: 1401-1410.
12. Behera, A. K., E. Hildebrand, J. Scagliotti, A. C. Steere, and L. T. Hu. 2005. Induction of host matrix metalloproteinases by Borrelia burgdorferi differs in human and murine Lyme arthritis. Infect. Immun. 73: 126-134.
13. Behera, A. K., C. M. Thorpe, J. M. Kidder, W. Smith, E. Hildebrand, and L. T. Hu. 2004. Borrelia burgdorferi-induced expression of matrix metalloproteinases from human chondrocytes requires mitogen-activated protein kinase and Janus kinase/signal transducer and activator of transcription signaling pathways. Infect. Immun. 72: 2864-2871.
14. Gebbia, J. A., J. L. Coleman, and J. L. Benach. 2004. Selective induction of matrix metalloproteinases by Borrelia burgdorferi via Toll-like receptor 2 in monocytes. J. Infect. Dis. 189: 113-119.
15. 3 mediates binding of the Lyme disease agent Borrelia burgdorferi to human platelets. Proc. Natl. Acad. Sci. USA 90: 7059-7063.
16. 1 mediate attachment of Lyme disease spirochetes to human cells. Infect. Immun. 66: 1946-1952.
17. 3 on human platelets. Infect. Immun. 62: 5559-5567.
18. 3. Proc. Natl. Acad. Sci. USA 100: 7301-7306.
19. Ingalls, R. R., M. A. Arnaout, and D. T. Golenbock. 1997. Outside-in signaling by lipopolysaccharide through a tailless integrin. J. Immunol. 159: 433-438.
20. Perera, P. Y., T. N. Mayadas, O. Takeuchi, S. Akira, M. Zaks-Zilberman, S. M. Goyert, and S. N. Vogel. 2001. CD11b/CD18 acts in concert with CD14 and Toll-like receptor (TLR) 4 to elicit full lipopolysaccharide and taxol-inducible gene expression. J. Immunol. 166: 574-581.
21. Vogel, S., M. J. Hirschfeld, and P. Y. Perera. 2001. Signal integration in lipopolysaccharide (LPS)-stimulated murine macrophages. J. Endotoxin Res. 7: 237-241.
22. Troelstra, A., L. A. de Graaf-Miltenburg, T. van Bommel, J. Verhoef, K. P. Van Kessel, and J. A. Van Strijp. 1999. Lipopolysaccharide-coated erythrocytes activate human neutrophils via CD14 while subsequent binding is through CD11b/CD18. J. Immunol. 162: 4220-4225.
23. Barbour, A. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57: 521-525.
24. Hu, L. T., G. Perides, R. Noring, and M. S. Klempner. 1995. Binding of human plasminogen to Borrelia burgdorferi. Infect. Immun. 63: 3491-3496.
25. Flo, T. H., L. Ryan, E. Latz, O. Takeuchi, B. G. Monks, E. Lien, O. Halaas, S. Akira, G. Skjak-Braek, D. T. Golenbock, and T. Espevik. 2002. Involvement of Toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J. Biol. Chem. 277: 35489-35495.
26. Sigal, L. H., J. M. Zahradnik, P. Lavin, S. J. Patella, G. Bryant, R. Haselby, E. Hilton, M. Kunkel, D. Adler-Klein, T. Doherty, et al. 1998. A vaccine consisting of recombinant Borrelia burgdorferi outer-surface protein A to prevent Lyme disease: recombinant outer-surface protein A Lyme disease vaccine study consortium. N. Engl. J. Med. 339: 216-222.
27. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
28. 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.
29. 1 integrin-mediated adhesion and neurite-like outgrowth and inhibits proliferation of small cell lung carcinoma cells. Cancer Res. 60: 457-466.
30. Goral, J., and E. J. Kovacs. 2005. In vivo ethanol exposure down-regulates TLR2-, TLR4-, and TLR9-mediated macrophage inflammatory response by limiting p38 and ERK1/2 activation. J. Immunol. 174: 456-463.
31. Aleman, M., P. Schierloh, S. S. de la Barrera, R. M. Musella, M. A. Saab, M. Baldini, E. Abbate, M. C. Sasiain, O. Bachar, M. Adner, et al. 2004. Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving Toll-like receptor 2 and p38 mitogen protein kinase in tuberculosis patients, Infect. Immun. 72: 5150-5158.
32. Bachar, O., M. Adner, R. Uddman, and L. O. Cardell. 2004. Toll-like receptor stimulation induces airway hyper-responsiveness to bradykinin, an effect mediated by JNK and NF-κB signaling pathways. Eur. J. Immunol. 34: 1196-1207.
33. Ropert, C., M. Closel, A. C. Chaves, and R. T. Gazzinelli. 2003. Inhibition of a p38/stress-activated protein kinase-2-dependent phosphatase restores function of IL-1 receptor-associate kinase-1 and reverses Toll-like receptor 2- and 4-dependent tolerance of macrophages. J. Immunol. 171: 1456-1465.
34. Juliano, R. L., P. Reddig, S. Alahari, M. Edin, A. Howe, and A. Aplin. 2004. Integrin regulation of cell signalling and motility. Biochem. Soc. Trans. 32: 443-446.
35. Kettritz, R., M. Choi, S. Rolle, M. Wellner, and F. C. Luft. 2004. Integrins and cytokines activate nuclear transcription factor-κB in human neutrophils. J. Biol. Chem. 279: 2657-2665.
36. Schlaepfer, D. D., and S. K. Mitra. 2004. Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14: 92-101.
37. Coburn, J. 2001. Adhesion mechanisms of the Lyme disease spirochete, Borrelia burgdorferi. Curr. Drug Targets Infect. Disord. 1: 171-179.
38. Tavella, S., G. Bellese, P. Castagnola, I. Martin, D. Piccini, R. Doliana, A. Colombatti, R. Cancedda, and C. Tacchetti. 1997. Regulated expression of fibronectin, laminin and related integrin receptors during the early chondrocyte differentiation. J. Cell Sci. 110: 2261-2270.
39. 1) in the integrin family. Cell Differ. Dev. 32: 229-238.
40. Elices, M. J., L. A. Urry, and M. E. Hemler. 1991. Receptor functions for the integrin VLA-3: fibronectin, collagen, and laminin binding are differentially influenced by Arg-Gly-Asp peptide and by divalent cations. J. Cell Biol. 112: 169-181.
41. Weitzman, J. B., R. Pasqualini, Y. Takada, and M. E. Hemler. 1993. The function and distinctive regulation of the integrin VLA-3 in cell adhesion, spreading, and homotypic cell aggregation. J. Biol. Chem. 268: 8651-8657.
42. 1 integrins in extracellular matrix assembly. J. Cell Sci. 108: 2511-2523.
43. 1. J. Biol. Chem. 267: 18908-18914.
44. 1. J. Biol. Chem. 273: 15854-15859.
45. 1 in epithelial basement membranes. Cell 65: 599-610.
46. 1 integrins: recognition of laminin isoforms. Mol. Biol. Cell 5: 203-215.
47. 3 integrins are up-regulated after vascular injury and modulate thrombospondin- and thrombin-induced proliferation of cultured smooth muscle cells. Circulation 97: 907-915.
48. 3 integrin controls ligand binding strength. J. Biol. Chem. 277: 3943-3949.
49. 1 is an alternative cellular receptor for adenovirus serotype 5. J. Virol. 77: 13448-13454.
50. 1 integrin has a crucial role in kidney and lung organogenesis. Development 122: 3537-3547.
51. 1 antagonist prevents development of murine Lyme arthritis without affecting protective immunity. J. Immunol. 175: 4724-4734.
52. Moore, K. J., L. P. Andersson, R. R. Ingalls, B. G. Monks, R. Li, M. A. Arnaout, D. T. Golenbock, and M. W. Freeman. 2000. Divergent response to LPS and bacteria in CD14-deficient murine macrophages. J. Immunol. 165: 4272-4280.
53. Behera, A. K., E. Hildebrand, R. T. Bronson, G. Perides, and L. T. Hu. 2006. MyD88 deficiency results in tissue specific changes in cytokine induction and inflammation in B. burgdorferi infected mice that are IL-18 independent. Infect. Immun. 74: 1462-1470.
54. Jung, H. C., L. Eckmann, S. K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95: 55-65.