Table of Contents Author Guidelines Submit a Manuscript
Clinical and Developmental Immunology
Volume 2012, Article ID 504215, 12 pages
http://dx.doi.org/10.1155/2012/504215
Review Article

Hamster and Murine Models of Severe Destructive Lyme Arthritis

1Wheaton Franciscan Laboratory, 11020 West Plank Court, Suite 100, Wauwatosa, WI 53226, USA
2College of Health Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI 53201, USA
3Dako North America, Inc., Carpinteria, CA 93013, USA
4Section of Infectious Diseases, Gundersen Lutheran Medical Center, La Crosse, WI 54601, USA
5Wisconsin State Laboratory of Hygiene, Madison, WI 53706, USA
6Department of Microbiology, University of Wisconsin-Madison, Madison, WI 53706, USA
7Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI 53706, USA

Received 20 July 2011; Revised 2 October 2011; Accepted 3 October 2011

Academic Editor: Franc Strle

Copyright © 2012 Erik Munson et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Centers for Disease Control and Prevention, “Lyme disease—connecticut,” Morbidity and Mortality Weekly Report, vol. 37, no. 1, pp. 1–3, 1988. View at Google Scholar
  2. A. C. Steere, N. H. Bartenhagen, J. E. Craft et al., “The early clinical manifestations of Lyme disease,” Annals of Internal Medicine, vol. 99, no. 1, pp. 76–82, 1983. View at Google Scholar · View at Scopus
  3. A. C. Steere, “Lyme disease,” New England Journal of Medicine, vol. 321, no. 9, pp. 586–596, 1989. View at Google Scholar · View at Scopus
  4. A. C. Steere, W. P. Batsford, and M. Weinberg, “Lyme carditis: cardiac abnormalities of Lyme disease,” Annals of Internal Medicine, vol. 93, no. 1 I, pp. 8–16, 1980. View at Google Scholar · View at Scopus
  5. E. L. Logigian, R. F. Kaplan, and A. C. Steere, “Chronic neurologic manifestations of Lyme disease,” New England Journal of Medicine, vol. 323, no. 21, pp. 1438–1144, 1990. View at Google Scholar · View at Scopus
  6. L. Reik Jr., “Neurologic aspects of North American Lyme disease,” in Lyme Disease, P. R. Coyle, Ed., pp. 101–112, Mosby, St. Louis, Mo, USA, 1993. View at Google Scholar
  7. A. C. Steere, R. T. Schoen, and E. Taylor, “The clinical evolution of Lyme arthritis,” Annals of Internal Medicine, vol. 107, no. 5, pp. 725–731, 1987. View at Google Scholar · View at Scopus
  8. I. S. Szer, E. Taylor, and A. C. Steere, “The long-term course of Lyme arthritis in children,” New England Journal of Medicine, vol. 325, no. 3, pp. 159–163, 1991. View at Google Scholar · View at Scopus
  9. Y. E. Johnston, P. H. Duray, A. C. Steere et al., “Lyme arthritis. Spirochetes found in synovial microangiopathic lesions,” American Journal of Pathology, vol. 118, no. 1, pp. 26–34, 1985. View at Google Scholar · View at Scopus
  10. M. T. Philipp and B. J. B. Johnson, “Animal models of Lyme disease: pathogenesis and immunoprophylaxis,” Trends in Microbiology, vol. 2, no. 11, pp. 431–437, 1994. View at Publisher · View at Google Scholar · View at Scopus
  11. A. C. Steere, C. E. Brinckerhoff, D. J. Miller et al., “Elevated levels of collagenase and prostaglandin E2 from synovium associated with erosion of cartilage and bone in a patient with chronic Lyme arthritis,” Arthritis and Rheumatism, vol. 238, no. 5, pp. 591–599, 1980. View at Google Scholar
  12. A. C. Steere, E. Dwyer, and R. Winchester, “Association of chronic Lyme arthritis with HLA-DR4 and HLA-DR2 alleles,” New England Journal of Medicine, vol. 323, no. 4, pp. 219–223, 1990. View at Google Scholar · View at Scopus
  13. A. C. Steere, A. Gibofsky, M. E. Patarroyo et al., “Chronic Lyme arthritis: clinical and immunogenetic differentiation from rheumatoid arthritis,” Annals of Internal Medicine, vol. 90, no. 6, pp. 896–901, 1979. View at Google Scholar
  14. R. A. Kalish, J. M. Leong, and A. C. Steere, “Association of treatment-resistant chronic Lyme arthritis with HLA-DR4 and antibody reactivity to OspA and OspB of Borrelia burgdorferi,” Infection and Immunity, vol. 61, no. 7, pp. 2774–2779, 1993. View at Google Scholar · View at Scopus
  15. D. M. Gross, T. Forsthuber, M. Tary-Lehmann et al., “Identification of LFA-1 as a candidate autoantigen in treatment- resistant Lyme arthritis,” Science, vol. 281, no. 5377, pp. 703–706, 1998. View at Google Scholar · View at Scopus
  16. A. C. Steere, W. Klitz, E. E. Drouin et al., “Antibiotic-refractory Lyme arthritis is associated with HLA-DR molecules that bind a Borrelia burgdorferi peptide,” Journal of Experimental Medicine, vol. 203, no. 4, pp. 961–971, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. E. E. Drouin, L. Glickstein, W. W. Kwok, G. T. Nepom, and A. C. Steere, “Searching for borrelial T cell epitopes associated with antibiotic-refractory Lyme arthritis,” Molecular Immunology, vol. 45, no. 8, pp. 2323–2332, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. J. L. Schmitz, R. F. Schell, A. Hejka, D. M. England, and L. Konick, “Induction of Lyme arthritis in LSH hamsters,” Infection and Immunity, vol. 56, no. 9, pp. 2336–2342, 1988. View at Google Scholar · View at Scopus
  19. S. W. Barthold, D. S. Beck, G. M. Hansen, G. A. Terwilliger, and K. D. Moody, “Lyme borreliosis in selected strains and ages of laboratory mice,” Journal of Infectious Diseases, vol. 162, no. 1, pp. 133–138, 1990. View at Google Scholar · View at Scopus
  20. Y. Ma, K. P. Seiler, E. J. Eichwald, J. H. Weis, C. Teuscher, and J. J. Weis, “Distinct characteristics of resistance to Borrelia burgdorferi induced arthritis in C57BL/6N mice,” Infection and Immunity, vol. 66, no. 1, pp. 161–168, 1998. View at Google Scholar · View at Scopus
  21. U. E. Schaible, M. D. Kramer, R. Wallich, T. Tran, and M. M. Simon, “Experimental Borrelia burgdorferi infection in inbred mouse strains: antibody response and association of H-2 genes with resistance and susceptibility to development of arthritis,” European Journal of Immunology, vol. 21, no. 10, pp. 2397–2405, 1991. View at Google Scholar · View at Scopus
  22. E. L. Munson, B. K. Du Chateau, D. A. Jobe et al., “Hamster model of Lyme borreliosis,” Journal of Spirochetal and Tick-borne Diseases, vol. 3, no. 1, pp. 15–21, 1996. View at Google Scholar
  23. D. T. Nardelli, J. O. Luedtke, E. L. Munson, T. F. Warner, S. M. Callister, and R. F. Schell, “Significant differences between the Borrelia-infection and Borrelia-vaccination and -infection models of Lyme arthritis in C3H/HeN mice,” FEMS Immunology and Medical Microbiology, vol. 60, no. 1, pp. 78–89, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Hejka, J. L. Schmitz, D. M. England, S. M. Callister, and R. F. Schell, “Histopathology of Lyme arthritis is LSH hamsters,” American Journal of Pathology, vol. 134, no. 5, pp. 1113–1123, 1989. View at Google Scholar · View at Scopus
  25. U. E. Schaible, M. D. Kramer, C. Museteanu, G. Zimmer, H. Mossmann, and M. M. Simon, “The severe combined immunodeficiency (scid) mouse: a laboratory model for the analysis of Lyme arthritis and carditis,” Journal of Experimental Medicine, vol. 170, no. 4, pp. 1427–1432, 1989. View at Google Scholar · View at Scopus
  26. U. E. Schaible, S. Gay, C. Museteanu et al., “Lyme borreliosis in the severe combined immunodeficiency (scid) mouse manifests predominantly in the joints, heart, and liver,” American Journal of Pathology, vol. 137, no. 4, pp. 811–820, 1990. View at Google Scholar · View at Scopus
  27. S. W. Barthold, C. L. Sidman, and A. L. Smith, “Lyme borreliosis in genetically resistant and susceptible mice with severe combined immunodeficiency,” American Journal of Tropical Medicine and Hygiene, vol. 47, no. 5, pp. 605–613, 1992. View at Google Scholar · View at Scopus
  28. L. C. L. Lim, D. M. England, B. K. Du Chateau et al., “Development of destructive arthritis in vaccinated hamsters challenged with Borrelia burgdorferi,” Infection and Immunity, vol. 62, no. 7, pp. 2825–2833, 1994. View at Google Scholar · View at Scopus
  29. B. K. Du Chateau, D. M. England, S. M. Callister, L. C. L. Lim, S. D. Lovrich, and R. F. Schell, “Macrophages exposed to Borrelia burgdorferi induce Lyme arthritis in hamsters,” Infection and Immunity, vol. 64, no. 7, pp. 2540–2547, 1996. View at Google Scholar · View at Scopus
  30. L. C. L. Lim, D. M. England, B. K. DuChateau, N. J. Glowacki, and R. F. Schell, “Borrelia burgdorferi-specific T lymphocytes induce severe destructive Lyme arthritis,” Infection and Immunity, vol. 63, no. 4, pp. 1400–1408, 1995. View at Google Scholar · View at Scopus
  31. L. C. L. Lim, D. M. England, N. J. Glowacki, B. K. Duchateau, and R. F. Schell, “Involvement of CD4+ T lymphocytes in induction of severe destructive Lyme arthritis in inbred LSH hamsters,” Infection and Immunity, vol. 63, no. 12, pp. 4818–4825, 1995. View at Google Scholar · View at Scopus
  32. B. K. Du Chateau, J. R. Jensen, D. M. England, S. M. Callister, S. D. Lovrich, and R. F. Schell, “Macrophages and enriched populations of T lymphocytes interact synergistically for the induction of severe, destructive Lyme arthritis,” Infection and Immunity, vol. 65, no. 7, pp. 2829–2836, 1997. View at Google Scholar · View at Scopus
  33. B. K. DuChateau, E. L. Munson, D. M. England et al., “Macrophages interact with enriched populations of distinct T lymphocyte subsets for the induction of severe destructive Lyme arthritis,” Journal of Leukocyte Biology, vol. 65, no. 2, pp. 162–170, 1999. View at Google Scholar · View at Scopus
  34. J. Kuo, D. T. Nardelli, T. F. Warner, S. M. Callister, and R. F. Schell, “Interleukin-35 enhances Lyme arthritis in Borrelia-vaccinated and -infected mice,” Clinical and Vaccine Immunology, vol. 18, no. 7, pp. 1125–1132, 2011. View at Publisher · View at Google Scholar
  35. E. L. Munson, D. J. DeCoster, D. T. Nardelli, D. M. England, S. M. Callister, and R. F. Schell, “Neutralization of gamma interferon augments borreliacidal antibody production and severe destructive Lyme arthritis in C3H/HeJ mice,” Clinical and Diagnostic Laboratory Immunology, vol. 11, no. 1, pp. 35–41, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. J. A. Christopherson, E. L. Munson, D. M. England et al., “Destructive arthritis in vaccinated interferon gamma-deficient mice challenged with Borrelia burgdorferi: modulation by tumor necrosis factor alpha,” Clinical and Diagnostic Laboratory Immunology, vol. 10, no. 1, pp. 44–52, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Burchill, D. T. Nardelli, D. M. England et al., “Inhibition of interleukin-17 prevents the development of arthritis in vaccinated mice challenged with Borrelia burgdorferi,” Infection and Immunity, vol. 71, no. 6, pp. 3437–3442, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. D. T. Nardelli, M. A. Burchill, D. M. England, J. Torrealba, S. M. Callister, and R. F. Schell, “Association of CD4+ CD25+ T cells with prevention of severe destructive arthritis in Borrelia burgdorferi-vaccinated and challenged gamma interferon-deficient mice treated with anti-interleukin-17 antibody,” Clinical and Diagnostic Laboratory Immunology, vol. 11, no. 6, pp. 1075–1084, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. S. D. Lovrich, S. M. Callister, L. C. L. Lim, and R. F. Schell, “Seroprotective groups among isolates of Borrelia burgdorferi,” Infection and Immunity, vol. 61, no. 10, pp. 4367–4374, 1993. View at Google Scholar · View at Scopus
  40. S. D. Lovrich, S. M. Callister, L. C. L. Lim, B. K. DuChateau, and R. F. Schell, “Seroprotective groups of Lyme borreliosis spirochetes from North America and Europe,” Journal of Infectious Diseases, vol. 170, no. 1, pp. 115–121, 1994. View at Google Scholar · View at Scopus
  41. S. D. Lovrich, S. M. Callister, B. K. DuChateau et al., “Abilities of OspA proteins from different seroprotective groups of Borrelia burgdorferi to protect hamsters from infection,” Infection and Immunity, vol. 63, no. 6, pp. 2113–2119, 1995. View at Google Scholar · View at Scopus
  42. J. L. Schmitz, R. F. Schell, S. D. Lovrich, S. M. Callister, and J. E. Coe, “Characterization of the protective antibody response to Borrelia burgdorferi in experimentally infected LSH hamsters,” Infection and Immunity, vol. 59, no. 6, pp. 1916–1921, 1991. View at Google Scholar · View at Scopus
  43. S. M. Callister, R. F. Schell, K. L. Case, S. D. Lovrich, and S. P. Day, “Characterization of the borreliacidal antibody response to Borrelia burgdorferi in humans: a serodiagnostic test,” Journal of Infectious Diseases, vol. 167, no. 1, pp. 158–164, 1993. View at Google Scholar · View at Scopus
  44. D. A. Jobe, S. M. Callister, L. C. L. Lim, S. D. Lovrich, and R. F. Schell, “Ability of canine Lyme disease vaccine to protect hamsters against infection with several isolates of Borrelia burgdorferi,” Journal of Clinical Microbiology, vol. 32, no. 3, pp. 618–622, 1994. View at Google Scholar · View at Scopus
  45. E. L. Munson, unpublished data.
  46. C. L. Croke, E. L. Munson, S. D. Lovrich et al., “Occurrence of severe destructive Lyme arthritis in hamsters vaccinated with outer surface protein A and challenged with Borrelia burgdorferi,” Infection and Immunity, vol. 68, no. 2, pp. 658–663, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. S. M. Callister, R. F. Schell, E. Fikrig et al., “Importance of protective borreliacidal antibodies in Lyme disease immunity and serodiagnosis,” Journal of Infectious Diseases, vol. 170, no. 2, pp. 499–500, 1994. View at Google Scholar · View at Scopus
  48. M. L. Padilla, S. M. Callister, R. F. Schell et al., “Characterization of the protective borreliacidal antibody response in humans and hamsters after vaccination with a Borrelia burgdorferi outer surface protein a vaccine,” Journal of Infectious Diseases, vol. 174, no. 4, pp. 739–746, 1996. View at Google Scholar · View at Scopus
  49. A. C. Steere, V. K. Sikand, F. Meurice et al., “Vaccination against Lyme disease with recombinant Borrelia burgdorferi outer-surface lipoprotein A with adjuvant,” New England Journal of Medicine, vol. 339, no. 4, pp. 209–215, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. L. H. Sigal, J. M. Zahradnik, P. Lavin et al., “A vaccine consisting of recombinant Borrelia burgdorferi outer-surface protein A to prevent Lyme disease,” New England Journal of Medicine, vol. 339, no. 4, pp. 216–222, 1998. View at Publisher · View at Google Scholar · View at Scopus
  51. C. R. Brown and S. L. Reiner, “Genetic control of experimental Lyme arthritis in the absence of specific immunity,” Infection and Immunity, vol. 67, no. 4, pp. 1967–1973, 1999. View at Google Scholar · View at Scopus
  52. A. G. Barbour, “Isolation and cultivation of Lyme disease spirochetes,” Yale Journal of Biology and Medicine, vol. 57, no. 4, pp. 521–525, 1984. View at Google Scholar · View at Scopus
  53. S. M. Callister, K. L. Case, W. A. Agger, R. F. Schell, R. C. Johnson, and J. L. E. Ellingson, “Effects of bovine serum albumin on the ability of Barbour-Stoenner-Kelly medium to detect Borrelia burgdorferi,” Journal of Clinical Microbiology, vol. 28, no. 2, pp. 363–365, 1990. View at Google Scholar · View at Scopus
  54. J. Oksi, J. Savolainen, J. Pène, J. Bousquet, P. Laippala, and M. K. Viljanen, “Decreased interleukin-4 and increased gamma interferon production by peripheral blood mononuclear cells of patients with Lyme borreliosis,” Infection and Immunity, vol. 64, no. 9, pp. 3620–3623, 1996. View at Google Scholar · View at Scopus
  55. L. Yang, J. H. Weis, E. Eichwald, C. P. Kolbert, D. H. Persing, and J. J. Weis, “Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues,” Infection and Immunity, vol. 62, no. 2, pp. 492–500, 1994. View at Google Scholar · View at Scopus
  56. A. Keane-Myers and S. P. Nickell, “Role of IL-4 and IFN-γ in modulation of immunity to Borrelia burgdorferi in mice,” Journal of Immunology, vol. 155, no. 4, pp. 2020–2028, 1995. View at Google Scholar · View at Scopus
  57. J. Matyniak and S. L. Reiner, “T helper phenotype and genetic susceptibility in experimental Lyme disease,” Journal of Experimental Medicine, vol. 181, no. 3, pp. 1251–1254, 1995. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Keane-Myers, C. R. Maliszewski, F. D. Finkelman, and S. P. Nickell, “Recombinant IL-4 treatment augments resistance to Borrelia burgdorferi infections in both normal susceptible and antibody-deficient susceptible mice,” Journal of Immunology, vol. 156, no. 7, pp. 2488–2494, 1996. View at Google Scholar · View at Scopus
  59. M.-C. Shanafelt, I. Kang, S. W. Barthold, and L. K. Bockenstedt, “Modulation of murine Lyme borreliosis by interruption of the B7/CD28 T- cell costimulatory pathway,” Infection and Immunity, vol. 66, no. 1, pp. 266–271, 1998. View at Google Scholar · View at Scopus
  60. C. R. Brown and S. L. Reiner, “Activation of natural killer cells in arthritis-susceptible but not arthritis-resistant mouse strains following Borrelia burgdorferi infection,” Infection and Immunity, vol. 66, no. 11, pp. 5208–5214, 1998. View at Google Scholar · View at Scopus
  61. C. R. Brown and S. L. Reiner, “Experimental Lyme arthritis in the absence of interleukin-4 or gamma interferon,” Infection and Immunity, vol. 67, no. 7, pp. 3329–3333, 1999. View at Google Scholar · View at Scopus
  62. D. T. Nardelli, T. F. Warner, S. M. Callister, and R. F. Schell, “Anti-CD25 antibody treatment of mice vaccinated and challenged with Borrelia spp. does not exacerbate arthritis but inhibits borreliacidal antibody production,” Clinical and Vaccine Immunology, vol. 13, no. 8, pp. 884–891, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. D. T. Nardelli, J. P. Cloute, K. H. Luk et al., “CD4+ CD25+ T cells prevent arthritis associated with Borrelia vaccination and infection,” Clinical and Diagnostic Laboratory Immunology, vol. 12, no. 6, pp. 786–792, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. G. Codolo, A. Amedei, A. C. Steere et al., “Borrelia burgdorferi NapA-driven Th17 cell inflammation in Lyme arthritis,” Arthritis and Rheumatism, vol. 58, no. 11, pp. 3609–3617, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Shen, J. J. Shin, K. Strle et al., “Treg cell numbers and function in patients with antibiotic-refractory or antibiotic-responsive Lyme arthritis,” Arthritis and Rheumatism, vol. 62, no. 7, pp. 2127–2137, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. E. Bettelli, Y. Carrier, W. Gao et al., “Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells,” Nature, vol. 441, no. 7090, pp. 235–238, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. K. E. Kisand, T. Prükk, K. V. Kisand, S.-M. Lüüs, I. Kalbe, and R. Uibo, “Propensity to excessive proinflammatory response in chronic Lyme borreliosis,” Acta Pathologica, Microbiologica et Immunologica Scandinavica, vol. 115, no. 2, pp. 134–141, 2007. View at Publisher · View at Google Scholar
  68. D. T. Nardelli, S. M. Callister, and R. F. Schell, “Lyme arthritis: current concepts and a change in paradigm,” Clinical and Vaccine Immunology, vol. 15, no. 1, pp. 21–34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Yssel, M.-C. Shanafelt, C. Soderberg, P. V. Schneider, J. Anzola, and G. Peltz, “Borrelia burgdorferi activates a T helper type 1-like T cell subset in Lyme arthritis,” Journal of Experimental Medicine, vol. 174, no. 3, pp. 593–601, 1991. View at Google Scholar · View at Scopus
  70. Y. Gao, F. Grassi, M. R. Ryan et al., “IFN-γ stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation,” Journal of Clinical Investigation, vol. 117, no. 1, pp. 122–132, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Kotake, N. Udagawa, N. Takahashi et al., “IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis,” Journal of Clinical Investigation, vol. 103, no. 9, pp. 1345–1352, 1999. View at Google Scholar · View at Scopus
  72. A. K. Shen, P. S. Mead, and C. B. Beard, “The Lyme disease vaccine—a public health perspective,” Clinical Infectious Diseases, vol. 52, supplement 3, pp. S247–S252, 2011. View at Publisher · View at Google Scholar
  73. S. A. Plotkin, “Correcting a public health fiasco: the need for a new vaccine against Lyme disease,” Clinical Infectious Diseases, vol. 52, supplement 3, pp. S271–S275, 2011. View at Publisher · View at Google Scholar
  74. I. Livey, M. O'Rourke, A. Traweger et al., “A new approach to a Lyme disease vaccine,” Clinical Infectious Diseases, vol. 52, supplement 3, pp. S266–S270, 2011. View at Publisher · View at Google Scholar
  75. E. L. Munson, B. K. Du Chateau, D. A. Jobe, S. D. Lovrich, S. M. Callister, and R. F. Schell, “Production of borreliacidal antibody to outer surface protein A in vitro and modulation by interleukin-4,” Infection and Immunity, vol. 68, no. 10, pp. 5496–5501, 2000. View at Publisher · View at Google Scholar · View at Scopus
  76. E. L. Munson, B. K. Du Chateau, J. R. Jensen, S. M. Callister, D. J. DeCoster, and R. F. Schell, “Gamma interferon inhibits production of anti-OspA borreliacidal antibody in vitro,” Clinical and Diagnostic Laboratory Immunology, vol. 9, no. 5, pp. 1095–1101, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. E. L. Munson, D. T. Nardelli, K. H. K. Luk, M. C. Remington, S. M. Callister, and R. F. Schell, “Interleukin-6 promotes anti-OspA borreliacidal antibody production in vitro,” Clinical and Vaccine Immunology, vol. 13, no. 1, pp. 19–25, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. M. C. Remington, E. L. Munson, S. M. Callister et al., “Interleukin-6 enhances production of anti-OspC immunoglobulin G2b borreliacidal antibody,” Infection and Immunity, vol. 69, no. 7, pp. 4268–4275, 2001. View at Google Scholar