Dual role of interleukin-10 in murine lyme disease: Regulation of arthritis severity and host defense

Infection and Immunity

Volumn 67, Issue 10, 1999, Pages 5142-5150

  Brown, Jeanette P ^a   Zachary, James F ^b   Teuscher, Cory ^b   Weis, Janis J ^a   Wooten, R Mark ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 6; LIPOPROTEIN; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANKLE; ANTIBODY PRODUCTION; ARTHRITIS; ARTICLE; BORRELIA BURGDORFERI; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HOST RESISTANCE; INFLAMMATION; LYME DISEASE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

EID: 0032880314     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.10.5142-5150.1999     Document Type: Article

References (75)

1. Anguita, J., S. Samanta, S. W. Barthold, and E. Fikrig. 1997. Ablation of inlerleukin-12 exacerbates Lyme arthritis in SCID mice. Infect. Immun. 65:4334-4336.
2. Apparailly, F., C. Verwaerde, C. Jacquet, C. Auriault, J. Sany, and C. Jorgensen. 1998. Adenovirus-mediated transfer of viral IL-10 gene inhibits murine collagen-induced arthritis. J. Immunol. 160:5213-5220.
3. Barthold, S. W. 1991. Infectivity of Borrelia burgdorferi relative to route of inoculation and genotype in laboratory mice. J. Infect. Dis. 163:419-420.
4. Barthold, S. W. 1996. Lyme borreliosis in the laboratory mouse. J. Spirochetal Tick-Borne Dis. 3:22-44.
5. 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.
6. Barthold, S. W., C. L. Sidman, and A. L. Smith. 1992. Lyme borreliosis in genetically resistant and susceptible mice with severe combined immunodeficiency. Am. J. Trop. Med. Hyg. 47:605-613.
7. Bessis, N., G. Chiocchia, G. Kollias, A. Minty, C. Fournier, D. Fradelizi, and M. C. Boissier. 1998. Modulation of proinflammatory cytokine production in tumour necrosis factor-alpha (TNF-α)-transgenic mice by treatment with cells engineered to secrete IL-4, IL-10 or IL-13. Clin. Exp. Immunol. 111: 391-396.
8. Bogdan, C., Y. Vodovotz, and C. Nathan. 1991. Macrophage deactivation by interleukin 10. J. Exp. Med. 174:1549-1555.
9. Brown, C. R., and S. L. Reiner. 1999. Genetic control of experimental Lyme arthritis in the absence of specific immunity. Infect. Immun. 67:1967-1973.
10. Buchan, G., K. Barrett, M. Turner, D. Chantry, R. N. Maini, and M. Feldmann. 1988. Interleukin-1 and tumour necrosis factor mRNA expression in rheumatoid arthritis: prolonged production of IL-1 alpha. Clin. Exp. Immunol. 73:449-455.
11. Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, and J. P. Davis. 1982. Lyme disease: a tick-borne spirochetosis? Science 216: 1317-1319.
12. 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.
13. 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 secretion IL-1 and tumor necrosis factor alpha and is required for subsequent transendothelial migration of neutro-phils. Infect. Immun. 65:1217-1222.
14. Dai, W. J., G. Kohler, and F. Brombacher. 1997. Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice. J. Immunol. 158:2259-2267.
15. de Silva, A. M., and E. Fikrig. 1997. Arthropod- and host-specific gene expression by Borrelia burgdorferi. J. Clin. Investig. 99:377-379.
16. de Waal Malefyt, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220.
17. Ding, A. H., C. F. Nathan, and D. J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141:2407-2412.
18. Ebnet, K., K. D. Brown, U. K. Siebenlist, M. M. Simon, and S. Shaw. 1997. Borrelia burgdorferi activates nuclear factor-kappa B and is a potent inducer of chemokine and adhesion molecule gene expression in endothelial cells and fibroblasts. J. Immunol. 158:3285-3292.
19. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147:3815-3822.
20. Firestein, G. S., J. M. Alvaro-Gracia, R. Maki, and J. M. Alvaro-Garcia. 1990. Quantitative analysis of cytokine gene expression in rheumatoid arthritis. J. Immunol. 144:3347-3353.
21. Flesch, I. E., J. H. Hess, I. P. Oswald, and S. H. Kaufmann. 1994. Growth inhibition of Mycobacterium bovis by IFN-gamma stimulated macrophages: regulation by endogenous tumor necrosis factor-alpha and by IL-10. Int. Immunol. 6:693-700.
22. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. While, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, and J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
23. Giambartolomei, G. H., V. A. Dennis, B. L. Lasater, and M. T. Philipp. 1999. Induction of pro- and anti-inflammatory cytokines by Borrelia burgdorferi lipoproteins in monocytes is mediated by CD14. Infect. Immun. 67:140-147.
24. Giambartolomei, G. H., V. A. Dennis, and M. T. Philipp. 1998. Borrelia burgdorferi stimulates the production of inteileukin-10 in peripheral blood mononuclear cells from uninfected humans and rhesus monkeys. Infect. Immun. 66:2691-2697.
25. Gondolf, K. B., M. Mihatsch, E. Curschellas, J. J. Dunn, and S. R. Batsford. 1994. Induction of experimental allergic arthritis with outer surface proteins of Borrelia burgdorferi. Arthritis Rheum. 37:1070-1077.
26. Hom, J. T., A. M. Bendele, and D. G. Carlson. 1988. In vivo administration with IL-1 accelerates the development of collagen-induced arthritis in mice. J. Immunol. 141:834-841.
27. Isomaki, P., R. Luukkainen, R. Saario, P. Toivanen, and J. Punnonen. 1996. Interleukin-10 functions as an antiinflammatory cytokine in rheumatoid synovium. Arthritis Rheum. 39:386-395.
28. Johnson, R. C., G. P. Schmid, F. W. Hyde, A. G. Steigwalt, and D. J. Brenner. 1984. Borrelia burgdorferi sp. nov.: etiologic agent of Lyme Disease. Int. J. Syst. Bacteriol. 34:496-497.
29. Joosten, L. A., E. Lubberts, P. Durez, M. M. Helsen, M. J. Jacobs, M. Goldman, and W. B. van den Berg. 1997. Role of interleukin-4 and interleukin-10 in murine collagen-induced arthritis. Protective effect of interleukin-4 and interleukin-10 treatment on cartilage destruction. Arthritis Rheum. 40:249-260.
30. Jouvin-Marche, E., M. G. Morgado, C. Leguern, D. Voegtle, F. Bonhomme, and P. A. Cazenave. 1989. The mouse Igh-1a and Igh-1b H chain constant regions are derived from two distinct isotypic genes. Immunogenetics 29:92-97.
31. Kang, I., S. W. Barthold, D. H. Persing, and L. K. Bockenstedt. 1997. T-helper-cell cytokines in the early evolution of murine Lyme arthritis. Infect. Immun. 65:3107-3111.
32. Kasama, T., R. M. Strieter, N. W. Lukacs, P. M. Lincoln, M. D. Burdick, and S. L. Kunkel. 1995. Interleukin-10 expression and chemokine regulation during the evolution of murine type II collagen-induced arthritis. J. Clin. Investig. 95:2868-2876.
33. Keffer, J., L. Probert, H. Cazlaris, S. Georgopoulos, E. Kaslaris, D. Kioussis, and G. Kollias. 1991. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J. 10:4025-4031.
34. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274.
35. Lentsch, A. B., T. P. Shanley, V. Sarma, and P. A. Ward. 1997. In vivo suppression of NF-κB and preservation of IκBα by interleukin-10 and interleukin-13. J. Clin. Investig. 100:2443-2448.
36. Lubberts, E., L. A. Joosten, M. M. Helsen, and W. B. van den Berg. 1998. Regulatory role of interleukin 10 in joint inflammation and cartilage destruction in murine streptococcal cell wall (SCW) arthritis. More therapeutic benefit with IL-4/IL-10 combination therapy than with IL-10 treatment alone. Cytokine 10:361-369.
37. Ma, Y., K. P. Seiler, E. J. Eichwald, J. H. Weis, C. Teuscher, and J. J. Weis. 1998. Distinct characteristics of resistance to Borrelia burgdorferi-induced arthritis in C57BL/6N mice. Infect. Immun. 66:161-168.
38. Ma, Y., K. P. Seiler, K.-F. Tai, L. Yang, M. Woods, and J. J. Weis. 1994. Outer surface lipoproteins of Borrelia burgdorferi stimulate nitric oxide production by the cytokine-inducible pathway. Infect Immun. 62:3663-3671.
39. Ma, Y., S. Thornton, L. E. Duwel, G. P. Boivin, E. H. Giannini, J. M. Leiden, J. A. Bluestone, and R. Hirsch. 1998. Inhibition of collagen-induced arthritis in mice by viral IL-10 gene transfer. J. Immunol. 161:1516-1524.
40. Ma, Y., and J. J. Weis. 1993. Borrelia burgdorferi outer surface lipoproteins OspA and OspB possess B-cell mitogenic and cytokine-stimulatory properties. Infect. Immun. 61:3843-3853.
41. Martin, R. M., and A. M. Lew. 1998. Is IgG2a a good Th1 marker in mice? Immunol. Today 19:49.
42. Martin, R. M., A. Silva, and A. M. Lew. 1997. The Igh-1 sequence of the non-obese diabetic (NOD) mouse assigns it to the IgG2c isotype. Immuno-genetics 46:167-168.
43. Moore, K. W., A. O'Garra, R. de Waal Malefyt, P. Viera, and T. R. Mosmann. 1993. Interleukin-10. Annu. Rev. Immunol. 11:165-190.
44. Morrison, T. B., Y. Ma, J. H. Weis, and J. J. Weis. 1999. Rapid and sensitive quantification of Borrelia burgdorferi-infected mouse tissues by continuous fluorescent monitoring of PCR. J. Clin. Microbiol. 37:987-992.
45. Morrison, T. B., J. H. Weis, and J. J. Weis. 1997. Borrelia burgdorferi outer surface protein A (OspA) activates and primes human neutrophils. J. Immunol. 158:4838-4845.
46. Morrison, T. B., J. J. Weis, and C. T. Wittwer. 1998. Quantification of low copy transcripts by continuous SYBR Green I monitoring during amplification. BioTechniques 24:954-962.
47. Murray, P. J., L. Wang, C. Onufryk, R. I. Tepper, and R. A. Young. 1997. T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J. Immunol. 158:315-321.
48. Nocton, J. J., F. Dressler, B. J. Rutledge, P. N. Rys, D. H. Persing, and A. C. Steere. 1994. Detection of Borrelia burgdorferi DNA by polymerase chain reaction in synovial fluid from patients with Lyme arthritis. N. Engl. J. Med. 330:229-234.
49. Nocton, J. J., and A. C. Steere. 1995. Lyme disease. Adv. Intern. Med. 40:69-117.
50. Norgard, M. V., L. L. Arndt, D. R. Akins, L. L. Curetty, D. A. Harrich, and J. D. Radolf. 1996. Activation of human monocytic cells by Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides proceeds via a pathway distinct from that of lipopolysaccharide but involves transcriptional activator NF-κB. Infect. Immun. 64:3845-3852.
51. Norgard, M. V., B. S. Riley, J. A. Richardson, and J. D. Radolf. 1995. Dermal inflammation elicited by synthetic analogs of Treponema pallidum and Borrelia burgdorferi lipoproteins. Infect. Immun. 63:1507-1515.
52. Pachner, A. R., E. Delaney, and N. S. Ricalton, 1992. Murine Lyme borreliosis: route of inoculation determines immune response and infectivity. Reg. Immunol. 4:345-351.
53. Pennington, P. M., C. D. Allred, C. S. West, R. Alvarez, and A. G. Barbour. 1997. Arthritis severity and spirochete burden are determined by serotype in the Borrelia turicatae-mouse model of Lyme disease. Infect. Immun. 65:285-292.
54. Pettipher, E. R., G. A. Higgs, and B. Henderson. 1986. Interleukin 1 induces leukocyte infiltration and cartilage proteoglycan degradation in the synovial joint. Proc. Natl. Acad. Sci. USA 83:8749-8753.
55. 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 burgdorferi lipoproteins and synthetic lipopeptides activate monocytes/macrophages. J. Immunol. 154:2866-2877.
56. Radolf, J. D., M. V. Norgard, M. E. Brandt, R. D. Isaacs, P. A. Thompson, and B. Beutler. 1991. Lipoproteins of Borrelia burgdorferi and Treponema pallidum activate cachectin/tumor necrosis factor synthesis: analysis using a CAT reporter construct. J. Immunol. 147:1968-1974.
57. Schaible, U. E., S. Gay, C. Museteanu, M. D. Kramer, G. Zimmer, K. Eichmann, U. Museteanu, and M. M. Simon. 1990. Lyme borreliosis in the severe combined immunodeficiency (scid) mouse manifests predominantly in the joints, heart, and liver. Am. J. Pathol. 137:811-820.
58. Seiler, K. P., and J. J. Weis. 1996. Immunity to Lyme disease: protection, pathology and persistence. Curr. Opin. Immunol. 8:503-509.
59. 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.
60. Sellati, T. J., D. A. Bouis, R. L. Kitchens, R. P. Darveau, J. Pugin, R. J. Ulevitch, S. C. Gangloff, S. M. Goyert, M. V. Norgard, and J. D. Radolf. 1998. Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J. Immunol. 160:5455-5464.
61. 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.
62. Sigal, L. H. 1997. Lyme disease: a review of aspects of its immunology and immunopathogenesis. Annu. Rev. Immunol. 15:63-92.
63. Tai, K.-F., Y. Ma, and J. J. Weis. 1994. Normal human B lymphocytes and mononuclear cells respond to the mitogenic and cytokine-stimulatory activities of Borrelia burgdorferi and its lipoprotein OspA. Infect. Immun. 62:520-528.
64. Ulevitch, R. J., and P. S. Tobias. 1995. Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu. Rev. Immunol. 13:437-457.
65. Wagner, R. D., N. M. Maroushek, J. F. Brown, and C. J. Czuprynski. 1994. Treatment with anti-interleukin-10 monoclonal antibody enhances early resistance to but impairs complete clearance of Listeria monocytogenes infection in mice. Infect. Immun. 62:2345-2353.
66. Walmsley, M., P. D. Katsikis, E. Abney, S. Parry, R. O. Williams, R. N. Maini, and M. Feldmann. 1996. Interleukin-10 inhibition of the progression of established collagen-induced arthritis. Arthritis Rheum. 39:495-503.
67. Weis, J. J., Y. Ma, and L. F. Erdile. 1994. Biological activities of native and recombinant Borrelia burgdorferi outer surface protein A: dependence on lipid modification. Infect. Immun. 62:4632-4636.
68. Weis, J. J., B. A. McCracken, Y. Ma, D. Fairbairn, R. J. Roper, T. B. Morrison, J. H. Weis, J. F. Zachary, R. W. Doerge, and C. Teuscher. 1999. Identification of quantitative trait loci governing arthritis severity and humoral responses in the murine model of Lyme disease. J. Immunol. 162:948-956.
69. Williams, R. O., M. Feldmann, and R. N. Maini. 1992. Anti-tumor necrosis factor ameliorates joint disease in murine collagen-induced arthritis. Proc. Natl. Acad. Sci. USA 89:9784-9788.
70. Wooten, R. M., V. R. Modur, T. M. McIntyre, and J. J. Weis. 1996. Borrelia burgdorferi outer membrane protein A induces nuclear translocation of nuclear factor-kappa B and inflammatory activation in human endothelial cells. J. Immunol. 157:4584-4590.
71. Wooten, R. M., T. B. Morrison, J. H. Weis, S. D. Wright, R. Thieringer, and J. J. Weis. 1998. The role of CD14 in signaling mediated by outer membrane lipoproteins of Borrelia burgdorferi. J. Immunol. 160:5485-5492.
72. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, and J. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249:1431-1433.
73. Yang, L., Y. Ma, R. Schoenfeld, M. Griffiths, E. Eichwald, B. Araneo, and J. J. Weis. 1992. Evidence for B-lymphocyte mitogen activity in Borrelia burgdorferi-infected mice. Infect. Immun. 60:3033-3041.
74. Yang, L., J. H. Weis, E. Eichwald, C. P. Kolbert, D. H. Persing, and J. J. Weis. 1994. Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues. Infect. Immun. 62:492-500.
75. Yang, X., K. T. Hay-Glass, and R. C. Brunham. 1996. Genetically determined differences in IL-10 and IFN-gamma responses correlate with clearance of Chlamydia trachomatis mouse pneumonitis infection. J. Immunol. 156:4338-4344.