IFN-γ alters the response of Borrelia burgdorferi-activated endothelium to favor chronic inflammation

Journal of Immunology

Volumn 178, Issue 2, 2007, Pages 1172-1179

  Dame, Tarah M ^a   Orenzoff, Barbara L ^a   Palmer, Lance E ^a   Furie, Martha B ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE CCL8; CHEMOKINE CXCL2; CXCL1 CHEMOKINE; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MONOCYTE CHEMOTACTIC PROTEIN 3; UNCLASSIFIED DRUG;

ARTICLE; BORRELIA BURGDORFERI; CELL MIGRATION; CHRONIC INFLAMMATION; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENDOTHELIUM; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; LYME DISEASE; MONOLAYER CULTURE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; VASCULAR ENDOTHELIUM;

EID: 33846231052     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.2.1172     Document Type: Article

References (54)

1. Benach, J. L., E. M. Bosler, J. P. Hanrahan, J. L. Coleman, G. S. Habicht, T., F. Bast, D. J. Cameron, J. L. Ziegler, A. G. Barbour, W. Burgdorfer, et al. 1983. Spirochetes isolated from the blood of two patients with Lyme disease. N. Engl. J. Med. 308: 740-742.
2. Duray, P. H. 1987. The surgical pathology of human Lyme disease: an enlarging picture. Am. J. Surg. Pathol. 11(Suppl. 1): 47-60.
3. Ebnet, K., M. M. Simon, and S. Shaw. 1996. Regulation of chemokine gene expression in human endothelial cells by proinflammatory cytokines and Borrelia burgdorferi. Ann. NY Acad. Sci. 797: 107-117.
4. Burns, M. J., T. J. Sellati, E. I. Teng, and M. B. Furie. 1997. Production of interleukin-8 (IL-8) by cultured endothelial cells in response to Borrelia burgdorferi occurs independently of secreted IL-1: and tumor necrosis factor α and is required for subsequent transendothelial migration of neutrophils. Infect. Immun. 65: 1217-1222.
5. Sellati, T. J., M. J. Burns, M. A. Ficazzola, and M. B. Furie. 1995. Borrelia burgdorferi upregulates expression of adhesion molecules on endothelial cells and promotes transendothelial migration of neutrophils in vitro. Infect. Immun. 63: 4439-4447.
6. Gergel, E. I., and M. B. Furie. 2001. Activation of endothelium by Borrelia burgdorferi in vitro enhances transmigration of specific subsets of T lymphocytes. Infect. Immun. 69: 2190-2197.
7. Burns, M. J., and M. B. Furie. 1998. Borrelia burgdorferi and interleukin-1 promote the transendothelial migration of monocytes in vitro by different mechanisms. Infect. Immun. 66: 4875-4883.
8. Sellati, T. J., L. D. Abrescia, J. D. Radolf, and M. B. Furie. 1996. Outer surface lipoproteins of Borrelia burgdorferi activate vascular endothelium in vitro. Infect. Immun. 64: 3180-3187.
9. Gergel, E. I., and M. B. Furie. 2004. Populations of human T lymphocytes that traverse the vascular endothelium stimulated by Borrelia burgdorferi are enriched with cells that secrete α interferon. Infect. Immun. 72: 1530-1536.
10. Brown, C. R., V. A. Blaho, and C. M. Loiacono. 2003. Susceptibility to experimental Lyme arthritis correlates with KC and monocyte chemoattractant protein-1 production in joints and requires neutrophil recruitment via CXCR2. J. Immunol. 171: 893-901.
11. Duray, P. H., and A. C. Steere. 1988. Clinical pathologic correlations of Lyme disease by stage. Ann. NY Acad. Sci. 539: 65-79.
12. Gross, D. M., A. C. Steere, and B. T. Huber. 1998. T helper 1 response is dominant and localized to the synovial fluid in patients with Lyme arthritis. J. Immunol 160: 1022-1028.
13. Salazar, J. C., C. D. Pope, T. J. Sellati, H. M. Feder, Jr., T. G. Kiely, K. R. Dardick, R. L. Buckman, M. W. Moore, M. J. Caimano, J. G. Pope, et al. 2003. Coevolution of markers of innate and adaptive immunity in skin and peripheral blood of patients with erythema migrans. J. Immunol. 171: 2660-2670.
14. Colvin, R. A., G. S. Campanella, J. Sun, and A. D. Luster. 2004. Intracellular domains of CXCR3 that mediate CXCL9, CXCL10, and CXCL11 function. J. Biol. Chem. 279: 30219-30227.
15. Huang, A. J., M. B. Furie, S. C. Nicholson, J. Fischbarg, L. S. Liebovitch, and S. C. Silverstein. 1988. Effects of human neutrophil chemotaxis across human endothelial cell monolayers on the permeability of these monolayers to ions and macromolecules. J. Cell. Physiol. 135: 355-366.
16. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
17. Gautier, L., L. Cope, B. M. Bolstad, and R. A. Irizarry. 2004. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
18. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
19. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, et al. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25: 25-29.
20. Anderson, D. C., M. L. Mace, B. R. Brinkley, R. R. Martin, and C. W. Smith. 1981. Recurrent infection in glycogenosis type Ib: abnormal neutrophil motility related to impaired redistribution of adhesion sites. J. Infect. Dis. 143: 447-459.
21. Furie, M. B., E. B. Cramer, B. L. Naprstek, and S. C. Silverstein. 1984. Cultured endothelial cell monolayers that restrict the transendothelial passage of macromolecules and electrical current. J. Cell Biol. 98: 1033-1041.
22. Randolph, G. J., and M. B. Furie. 1995. A soluble gradient of endogenous monocyte chemoattractant protein-1 promotes the transendothelial migration of monocytes in vitro. J. Immunol. 155: 3610-3618.
23. 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.
24. Habicht, G. S., L. I. Katona, and J. L. Benach. 1991. Cytokines and the pathogenesis of neuroborreliosis: Borrelia burgdorferi induces glioma cells to secrete interleukin-6. J. Infect. Dis. 164: 568-574.
25. Grygorczuk, S., S. Pancewicz, J. Zajkowska, M. Kondrusik, R. Rwierzbinska, and T. Hermanowska-Szpakowicz. 2004. Concentrations of macrophage inflammatory proteins MIP-1α and MIP-1β and interleukin 8 (IL-8) in Lyme borreliosis. Infection 32: 350-355.
26. Reith, W., S. LeibundGut-Landmann, and J. M. Waldburger. 2005. Regulation of MHC class II gene expression by the class II transactivator. Nat. Rev. Immunol. 5: 793-806.
27. Albelda, S. M., C. W. Smith, and P. A. Ward. 1994. Adhesion molecules and inflammatory injury. FASEB J. 8: 504-512.
28. + T lymphocytes. FASEB J. 8: 1055-1060.
29. Liao, F., R. L. Rabin, J. R. Yannelli, L. G. Koniaris, P. Vanguri, and J. M. Farber. 1995. Human Mig chemokine: biochemical and functional characterization. J. Exp. Med. 182: 1301-1314.
30. Taub, D. D., A. R. Lloyd, K. Conlon, J. M. Wang, J. R. Ortaldo, A. Harada, K. Matsushima, D. J. Kelvin, and J. J. Oppenheim. 1993. Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J. Exp. Med. 177: 1809-1814.
31. Cole, K. E., C. A. Strick, T. J. Paradis, K. T. Ogborne, M. Loetscher, R. P. Gladue, W. Lin, J. G. Boyd, B. Moser, D. E. Wood, et al. 1998. Interferon-inducible T cell α chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J. Exp. Med. 187: 2009-2021.
32. Bazan, J. F., K. B. Bacon, G. Hardiman, W. Wang, K. Soo, D. Rossi, D. R. Greaves, A. Zlotnik, and T. J. Schall. 1997. A new class of membrane-bound chemokine with a CX3C motif. Nature 385: 640-644.
33. 2 terminal amino acid sequence identity with melanoma growth stimulatory activity. J. Exp. Med. 171: 1091-1100.
34. + T-cells migrating into the cerebiospinal fluid of patients with neuroborreliosis: the role of CXCL10 and CXCL11. J. Neuroimmunol. 163: 128-134.
35. Giunti, D., G. Borsellino, R. Benelli, M. Marchese, E. Capello, M. T. Valle, E. Pedemonte, D. Noonan, A. Albini, G. Bernardi, et al. 2003. Phenotypic and functional analysis of T cells homing into the CSF of subjects with inflammatory diseases of the CNS. J. Leukocyte Biol. 73: 584-590.
36. Duray, P. H. 1989. Histopathology of clinical phases of human Lyme disease. Rheum. Dis. Clin. North Am. 15: 691-710.
37. Rupprecht, T. A., U. Koedel, B. Muhlberger, B. Wilske, A. Fontana, and H. W. Pfister. 2005. CXCL11 is involved in leucocyte recruitment to the central nervous system in neuroborreliosis. J. Neurol. 252: 820-823.
38. Taub, D. D., P. Proost, W. J. Murphy, M. Anver, D. L. Longo, J. Van Damme, and J. J. Oppenheim. 1995. Monocyte chemotactic protein-1 (MCP-I), -2, and -3 are chemotactic for human T lymphocytes. J. Clin. Invest. 95: 1370-1376.
39. Locati, M., Y. M. Torre, E. Galliera, R. Bonecchi, H. Bodduluri, G. Vago, A. Vecchi, and A. Mantovani. 2005. Silent chemoattractant receptors: D6 as a decoy and scavenger receptor for inflammatory CC chemokines. Cytokine Growth Factor Rev. 16: 679-686.
40. Widhe, M., S. Jarefors, C. Ekerfelt, M. Vrethem, S. Bergstrom, P. Forsberg, and J. Ernerudh. 2004. Borrella-specific interferon-γ and interleukin-4 secretion in cerebrospinal fluid and blood during Lyme borreliosis in humans: association with clinical outcome. J. Infect. Dis. 189: 1881-1891.
41. Forsberg, P., J. Ernerudh, C. Ekerfelt, M. Roberg, M. Vrethem, and S. Bergstrom. 1995. The outer surface proteins of Lyme disease Borrelia spirochetes stimulate T cells to secrete interferon-γ (IFN-γ): diagnostic and pathogenic implications. Clin. Exp. Immunol. 101: 453-460.
42. Brown, C. R., and S. L. Reiner. 1999. Experimental Lyme arthritis in the absence of interleukin-4 or γ interferon. Infect. Immun. 67: 3329-3333.
43. Glickstein, L., M. Edelstein, and J. Z. Dong. 2001. γ Interferon is not required for arthritis resistance in the murine Lyme disease model. Infect. Immun. 69: 3737-3743.
44. Barthold, S. W., D. H. Persing, A. L. Armstrong, and R. A. Peeples. 1991. Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Am. J. Pathol. 139: 263-273.
45. Barthold, S. W., D. S. Beck, G. M. Hansen, G. A. Terwilliger, and K. D. Moody. 1990. Lyme borreliosis in selected strains and ages of laboratory mice. J. Infect. Dis. 162: 133-138.
46. Mohan, K., Z. Ding, J. Hanly, and T. B. Issekutz. 2002. IFN-γ-inducible T cell a chemoattractant is a potent stimulator of normal human blood T lymphocyte transendothelial migration: differential regulation by IFN-γ and TNF-α. J. Immunol. 168: 6420-6428.
47. Fraticelli, P., M. Sironi, G. Bianchi, D. D'Ambrosio, C. Albanesi, A. Stoppacciaro, M. Chieppa, P. Allavena, L. Ruco, G. Girolomoni, et al. 2001. Fractalkine (CX3CL1) as an amplification circuit of polarized Th1 responses. J. Clin. Invest. 107: 1173-1181.
48. Proost, P., A. K. Vynckier, F. Mahieu, W. Put, B. Grillet, S. Struyf, A. Wuyts, G. Opdenakker, and J. V. Damme. 2003. Microbial Toll-like receptor ligands differentially regulate CXCL10/IP-10 expression in fibroblasts and mononuclear leukocytes in synergy with IFN-γ and provide a mechanism for enhanced synovial chemokine levels in septic arthritis. Eur. J. Immunol. 33: 3146-3153.
49. Proost, P., S. Verpoest, B. K. Van de, E. Schutyser, S. Struyf, W. Put, I. Ronsse, B. Grillet, G. Opdenakker, and J. Van Damme. 2004. Synergistic induction of CXCL9 and CXCL11 by Toll-like receptor ligands and interferon-γ in fibroblasts correlates with elevated levels of CXCR3 ligands in septic arthritis synovial fluids. J. Leukocyte Biol. 75: 777-784.
50. Radolf, J. D., L. L. Arndt, D. R. Akins, L. L. Curetty, M. E. Levi, Y. Shen, L. S. Davis, and M. V. Norgard. 1995. Treponema pallidum and Borrelia burgdofferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol. 154: 2866-2877.
51. Haringman, I. J., T. J. Smeets, P. Reinders-Blankert, and P. P. Tak. 2006. Chemokine and chemokine receptor expression in paired peripheral blood mononuclear cells and synovial tissue of patients with rheumatoid arthritis, osteoarthritis, and reactive arthritis. Ann. Rheum. Dis. 65: 294-300.
52. Ruth, J. H., M. V. Volin, G. K. Haines III, D. C. Woodruff, K. J. Katschke, Jr., J. M. Woods, C. C. Park, J. C. Morel, and A. E. Koch. 2001. Fractalkine, a novel chemokine in rheumatoid arthritis and in rat adjuvant-induced arthritis. Arthritis Rheum. 44: 1568-1581.
53. Ueno, A., M. Yamamura, M. Iwahashi, A. Okamoto, T. Aita, N. Ogawa, and H. Makino. 2005. The production of CXCR3-agonistic chemokines by synovial fibroblasts from patients with rheumatoid arthritis. Rheumatol. Int. 25: 361-367.
54. Nanki, T., T. Imai, K. Nagasaka, Y. Urasaki, Y. Nonomura, K. Taniguchi, K. Hayashida, J. Hasegawa, O. Yoshie, and N. Miyasaka. 2002. Migration of CX3CR1-positive T cells producing type 1 cytokines and cytotoxic molecules into the synovium of patients with rheumatoid arthritis. Arthritis Rheum. 46: 2878-2883.