HLA-DR alleles determine responsiveness to Borrelia burgdorferi antigens in a mouse model of self-perpetuating arthritis

Arthritis Rheum. 2009 Dec;60(12):3831-40. doi: 10.1002/art.25005.

Abstract

Objective: Arthritis is a prominent manifestation of Lyme disease, which is caused by infection with Borrelia burgdorferi (Bb). Chronic Lyme arthritis persisting even after antibiotic treatment is linked to HLA-DRB1*0401 (DR4) and related alleles. In contrast, patients whose Lyme arthritis resolves within 3 months postinfection show an increased frequency of HLA-DRB1*1101 (DR11). The aim of this study was to analyze the underlying mechanism by which HLA-DR alleles confer genetic susceptibility or resistance to antibiotic-refractory Lyme arthritis.

Methods: We generated DR11-transgenic (DR11-Tg) mice on a murine MHCII-/- background and compared their immune response to Bb antigens with the response of DR4-Tg mice after immunization with Bb outer surface protein A (OspA) or infection with live Bb.

Results: T cells from OspA-immunized and Bb-infected DR11-Tg mice had defective production of interferon-gamma as compared with those from DR4-Tg mice. In contrast, DR11-Tg mice developed higher titers of anti-OspA and anti-Bb antibodies, respectively, than did DR4-Tg mice. Consistent with this observation, we found that the Bb-infected DR11-Tg mice had a decreased spirochetal burden as compared with the DR4-Tg mice, as measured by quantitative polymerase chain reaction.

Conclusion: This study provides direct evidence that in the presence of HLA-DR11, the immune response against Bb antigens is directed toward a protective antibody response. In contrast, an inflammatory Th1 response is induced in the presence of DR4. These observations offer an explanation for the differential genetic susceptibility of DR4+ and DR11+ individuals to the development of chronic Lyme arthritis and, eventually, the progression to antibiotic-refractory Lyme arthritis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibodies, Bacterial / immunology
  • Antigens, Surface / immunology
  • Arthritis, Infectious / immunology
  • Arthritis, Infectious / microbiology*
  • Bacterial Outer Membrane Proteins / immunology
  • Bacterial Vaccines / immunology
  • Borrelia burgdorferi / immunology*
  • Disease Models, Animal
  • Genetic Predisposition to Disease*
  • HLA-DR Antigens / genetics*
  • HLA-DR Antigens / immunology
  • HLA-DR Serological Subtypes
  • Humans
  • Interferon-gamma / metabolism
  • Lipoproteins / immunology
  • Lyme Disease / complications*
  • Lyme Disease / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • T-Lymphocytes / immunology

Substances

  • Antibodies, Bacterial
  • Antigens, Surface
  • Bacterial Outer Membrane Proteins
  • Bacterial Vaccines
  • HLA-DR Antigens
  • HLA-DR Serological Subtypes
  • HLA-DR11 antigen
  • Lipoproteins
  • OspA protein
  • Interferon-gamma