Abstract
T-helper responses following Borrelia burgdorferi infection in mice determine susceptibility to Lyme arthritis. The ratio of interleukin 4-positive, CD4+ to gamma interferon (IFN-gamma)-positive, CD4+ T cells was significantly greater in infected BALB/cJ mice than in infected C3H/HeJ mice. Increased numbers of IFN-gamma-producing cells predicted greater arthritis severity, and CD8+ T cells were the main source of IFN-gamma in both strains.
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- Barthold S. W., Beck D. S., Hansen G. M., Terwilliger G. A., Moody K. D. Lyme borreliosis in selected strains and ages of laboratory mice. J Infect Dis. 1990 Jul;162(1):133–138. doi: 10.1093/infdis/162.1.133. [DOI] [PubMed] [Google Scholar]
- Barthold S. W., Fikrig E., Bockenstedt L. K., Persing D. H. Circumvention of outer surface protein A immunity by host-adapted Borrelia burgdorferi. Infect Immun. 1995 Jun;63(6):2255–2261. doi: 10.1128/iai.63.6.2255-2261.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barthold S. W. Infectivity of Borrelia burgdorferi relative to route of inoculation and genotype in laboratory mice. J Infect Dis. 1991 Feb;163(2):419–420. doi: 10.1093/infdis/163.2.419. [DOI] [PubMed] [Google Scholar]
- Blanas E., Carbone F. R., Allison J., Miller J. F., Heath W. R. Induction of autoimmune diabetes by oral administration of autoantigen. Science. 1996 Dec 6;274(5293):1707–1709. doi: 10.1126/science.274.5293.1707. [DOI] [PubMed] [Google Scholar]
- Busch D. H., Jassoy C., Brinckmann U., Girschick H., Huppertz H. I. Detection of Borrelia burgdorferi-specific CD8+ cytotoxic T cells in patients with Lyme arthritis. J Immunol. 1996 Oct 15;157(8):3534–3541. [PubMed] [Google Scholar]
- Coburn J., Barthold S. W., Leong J. M. Diverse Lyme disease spirochetes bind integrin alpha IIb beta 3 on human platelets. Infect Immun. 1994 Dec;62(12):5559–5567. doi: 10.1128/iai.62.12.5559-5567.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finlay B. B., Cossart P. Exploitation of mammalian host cell functions by bacterial pathogens. Science. 1997 May 2;276(5313):718–725. doi: 10.1126/science.276.5313.718. [DOI] [PubMed] [Google Scholar]
- Flores Villanueva P. O., Harris T. S., Ricklan D. E., Stadecker M. J. Macrophages from schistosomal egg granulomas induce unresponsiveness in specific cloned Th-1 lymphocytes in vitro and down-regulate schistosomal granulomatous disease in vivo. J Immunol. 1994 Feb 15;152(4):1847–1855. [PubMed] [Google Scholar]
- Heinzel F. P., Sadick M. D., Mutha S. S., Locksley R. M. Production of interferon gamma, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7011–7015. doi: 10.1073/pnas.88.16.7011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keane-Myers A., Nickell S. P. Role of IL-4 and IFN-gamma in modulation of immunity to Borrelia burgdorferi in mice. J Immunol. 1995 Aug 15;155(4):2020–2028. [PubMed] [Google Scholar]
- Keane-Myers A., Nickell S. P. T cell subset-dependent modulation of immunity to Borrelia burgdorferi in mice. J Immunol. 1995 Feb 15;154(4):1770–1776. [PubMed] [Google Scholar]
- Liblau R. S., Singer S. M., McDevitt H. O. Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases. Immunol Today. 1995 Jan;16(1):34–38. doi: 10.1016/0167-5699(95)80068-9. [DOI] [PubMed] [Google Scholar]
- Lim L. C., England D. M., DuChateau B. K., Glowacki N. J., Creson J. R., Lovrich S. D., Callister S. M., Jobe D. A., Schell R. F. Development of destructive arthritis in vaccinated hamsters challenged with Borrelia burgdorferi. Infect Immun. 1994 Jul;62(7):2825–2833. doi: 10.1128/iai.62.7.2825-2833.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matsuzaki G., Song F., Nomoto K. Suppression of T-helper type-1 immune response against Listeria monocytogenes by treatment of mice with goat antibodies to mouse IgD. Immunology. 1996 Jan;87(1):15–20. [PMC free article] [PubMed] [Google Scholar]
- Matyniak J. E., Reiner S. L. T helper phenotype and genetic susceptibility in experimental Lyme disease. J Exp Med. 1995 Mar 1;181(3):1251–1254. doi: 10.1084/jem.181.3.1251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McFarland H. F. Complexities in the treatment of autoimmune disease. Science. 1996 Dec 20;274(5295):2037–2038. doi: 10.1126/science.274.5295.2037. [DOI] [PubMed] [Google Scholar]
- Normark S., Wolf-Watz H. Common themes amid diversity. Science. 1997 May 2;276(5313):659–659. doi: 10.1126/science.276.5313.659. [DOI] [PubMed] [Google Scholar]
- Norris S. J., Howell J. K., Garza S. A., Ferdows M. S., Barbour A. G. High- and low-infectivity phenotypes of clonal populations of in vitro-cultured Borrelia burgdorferi. Infect Immun. 1995 Jun;63(6):2206–2212. doi: 10.1128/iai.63.6.2206-2212.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Openshaw P., Murphy E. E., Hosken N. A., Maino V., Davis K., Murphy K., O'Garra A. Heterogeneity of intracellular cytokine synthesis at the single-cell level in polarized T helper 1 and T helper 2 populations. J Exp Med. 1995 Nov 1;182(5):1357–1367. doi: 10.1084/jem.182.5.1357. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Panitch H. S., Hirsch R. L., Schindler J., Johnson K. P. Treatment of multiple sclerosis with gamma interferon: exacerbations associated with activation of the immune system. Neurology. 1987 Jul;37(7):1097–1102. doi: 10.1212/wnl.37.7.1097. [DOI] [PubMed] [Google Scholar]
- Reiner S. L., Zheng S., Wang Z. E., Stowring L., Locksley R. M. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection. J Exp Med. 1994 Feb 1;179(2):447–456. doi: 10.1084/jem.179.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Romani L., Mencacci A., Cenci E., Spaccapelo R., Mosci P., Puccetti P., Bistoni F. CD4+ subset expression in murine candidiasis. Th responses correlate directly with genetically determined susceptibility or vaccine-induced resistance. J Immunol. 1993 Feb 1;150(3):925–931. [PubMed] [Google Scholar]
- Schaible U. E., Kramer M. D., Eichmann K., Modolell M., Museteanu C., Simon M. M. Monoclonal antibodies specific for the outer surface protein A (OspA) of Borrelia burgdorferi prevent Lyme borreliosis in severe combined immunodeficiency (scid) mice. Proc Natl Acad Sci U S A. 1990 May;87(10):3768–3772. doi: 10.1073/pnas.87.10.3768. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaible U. E., Kramer M. D., Justus C. W., Museteanu C., Simon M. M. Demonstration of antigen-specific T cells and histopathological alterations in mice experimentally inoculated with Borrelia burgdorferi. Infect Immun. 1989 Jan;57(1):41–47. doi: 10.1128/iai.57.1.41-47.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaible U. E., Kramer M. D., Wallich R., Tran T., Simon M. M. Experimental Borrelia burgdorferi infection in inbred mouse strains: antibody response and association of H-2 genes with resistance and susceptibility to development of arthritis. Eur J Immunol. 1991 Oct;21(10):2397–2405. doi: 10.1002/eji.1830211016. [DOI] [PubMed] [Google Scholar]
- Simon A. K., Seipelt E., Sieper J. Divergent T-cell cytokine patterns in inflammatory arthritis. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8562–8566. doi: 10.1073/pnas.91.18.8562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Starnbach M. N., Bevan M. J., Lampe M. F. Protective cytotoxic T lymphocytes are induced during murine infection with Chlamydia trachomatis. J Immunol. 1994 Dec 1;153(11):5183–5189. [PubMed] [Google Scholar]
- Steere A. C. Lyme disease. N Engl J Med. 1989 Aug 31;321(9):586–596. doi: 10.1056/NEJM198908313210906. [DOI] [PubMed] [Google Scholar]
- Telford S. R., 3rd, Fikrig E., Barthold S. W., Brunet L. R., Spielman A., Flavell R. A. Protection against antigenically variable Borrelia burgdorferi conferred by recombinant vaccines. J Exp Med. 1993 Aug 1;178(2):755–758. doi: 10.1084/jem.178.2.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Telford S. R., 3rd, Kantor F. S., Lobet Y., Barthold S. W., Spielman A., Flavell R. A., Fikrig E. Efficacy of human Lyme disease vaccine formulations in a mouse model. J Infect Dis. 1995 May;171(5):1368–1370. doi: 10.1093/infdis/171.5.1368. [DOI] [PubMed] [Google Scholar]
- Tsuchida T., Parker K. C., Turner R. V., McFarland H. F., Coligan J. E., Biddison W. E. Autoreactive CD8+ T-cell responses to human myelin protein-derived peptides. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10859–10863. doi: 10.1073/pnas.91.23.10859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang L., Ma Y., Schoenfeld R., Griffiths M., Eichwald E., Araneo B., Weis J. J. Evidence for B-lymphocyte mitogen activity in Borrelia burgdorferi-infected mice. Infect Immun. 1992 Aug;60(8):3033–3041. doi: 10.1128/iai.60.8.3033-3041.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang L., Weis J. H., Eichwald E., Kolbert C. P., Persing D. H., Weis J. J. Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues. Infect Immun. 1994 Feb;62(2):492–500. doi: 10.1128/iai.62.2.492-500.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yssel H., Shanafelt M. C., Soderberg C., Schneider P. V., Anzola J., Peltz G. Borrelia burgdorferi activates a T helper type 1-like T cell subset in Lyme arthritis. J Exp Med. 1991 Sep 1;174(3):593–601. doi: 10.1084/jem.174.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]