Experimental African Trypanosome Infection by Needle Passage or Natural Tsetse Fly Challenge Thwarts the Development of Collagen-Induced Arthritis in DBA/1 Prone Mice via an Impairment of Antigen Specific B Cell Autoantibody Titer
De Trez, Carl; Katsandegwaza, Brunette; Caljon, Guyet al.
[en] Collagen-induced arthritis is a B cell-mediated autoimmune disease. Recently published studies have demonstrated that in some rare cases pathogens can confer protection from autoimmunity. Trypanosoma brucei parasites are tsetse fly transmitted extracellular protozoans causing sleeping sickness disease in humans and Nagana in livestock in sub-Saharan endemic areas. In the past, we demonstrated that trypanosome infections impair B cell homeostasis and abolish vaccine-induced protection against unrelated antigens. Hence, here we hypothesized that trypanosome infection can affect the onset of CIA by specifically dampening specific B-cell responses and type II collagen antibody titers in DBA/1 prone mice. We observed a substantial delay in the onset of collagen-induced arthritis in T. brucei-infected DBA/1 mice that correlates with a drastic decrease of type II collagen titers of the different IgG isotypes in the serum. Treatment of infected mice with Berenil, a trypanocidal drug, restored the development of CIA-associated clinical symptoms. Interestingly, these data were confirmed by the challenge of immunized DBA/1 prone mice with T. brucei-infected tsetse flies. Together, these results demonstrate that T. brucei infection is impairing the maintenance of the antigen specific plasma B cell pool driving the development of CIA in DBA/1 prone mice.
Research Center/Unit :
Vrije Universiteit Brussels
Disciplines :
Microbiology Veterinary medicine & animal health
Author, co-author :
De Trez, Carl ✱
Katsandegwaza, Brunette ✱; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Immunologie vétérinaire
Caljon, Guy
Magez, Stefan
✱ These authors have contributed equally to this work.
Language :
English
Title :
Experimental African Trypanosome Infection by Needle Passage or Natural Tsetse Fly Challenge Thwarts the Development of Collagen-Induced Arthritis in DBA/1 Prone Mice via an Impairment of Antigen Specific B Cell Autoantibody Titer
This work was supported by Fonds voor Wetenschappelijk Onderzoek (FWO) via a “Krediet aan Navorsers” grant # 1517313N/KN251 and Belgian Federal Science Policy Office via “Interuniversity Attraction Poles” grant # 7–41.
Okada H, Kuhn C, Feillet H, Bach JF. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin Exp Immunol. 2010 Apr; 160(1):1-9. doi: 10.1111/j.1365-2249.2010.04139.x PMID: 20415844
Martinez FD. The coming-of-age of the hygiene hypothesis. Respir Res. 2001; 2(3):129-32. PMID: 11686875
Feldmann M, Brennan FM, Maini RN. Rheumatoid arthritis. Cell. 1996 May 3; 85(3):307-10. PMID: 8616886
Holmdahl R, Jansson L, Gullberg D, Rubin K, Forsberg PO, Klareskog L. Incidence of arthritis and autoreactivity of anti-collagen antibodies after immunization of DBA/1 mice with heterologous and autologous collagen II. Clin Exp Immunol. 1985 Dec; 62(3):639-46. PMID: 4085150
Janossy G, Panayi G, Duke O, Bofill M, Poulter LW, Goldstein G. Rheumatoid arthritis: a disease of T-lymphocyte/macrophage immunoregulation. Lancet. 1981 Oct 17; 2(8251):839-42. PMID: 6116956
Panayi GS. B cells: a fundamental role in the pathogenesis of rheumatoid arthritis? Rheumatology (Oxford). 2005 May; 44 Suppl 2:ii3-ii7.
Svensson L, Jirholt J, Holmdahl R, Jansson L. B cell-deficient mice do not develop type II collagen-induced arthritis (CIA). Clin Exp Immunol. 1998 Mar; 111(3):521-6. PMID: 9528892
Yanaba K, Hamaguchi Y, Venturi GM, Steeber DA, St Clair EW, Tedder TF. B cell depletion delays collagen-induced arthritis in mice: arthritis induction requires synergy between humoral and cell-mediated immunity. J Immunol. 2007 Jul 15; 179(2):1369-80. PMID: 17617630
Corthay A, Johansson A, Vestberg M, Holmdahl R. Collagen-induced arthritis development requires alpha beta T cells but not gamma delta T cells: studies with T cell-deficient (TCR mutant) mice. Int Immunol. 1999 Jul; 11(7):1065-73. PMID: 10383939
Brand DD, Marion TN, Myers LK, Rosloniec EF, Watson WC, Stuart JM, et al. Autoantibodies to murine type II collagen in collagen-induced arthritis: a comparison of susceptible and nonsusceptible strains. J Immunol. 1996 Dec 1; 157(11):5178-84. PMID: 8943430
Magez S, Radwanska M. African trypanosomiasis and antibodies: implications for vaccination, therapy and diagnosis. Future Microbiol. 2009 Oct; 4(8):1075-87.
Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, Cazzulo JJ, et al. The trypanosomiases. Lancet. 2003 Nov 1; 362(9394):1469-80. PMID: 14602444
Radwanska M, Guirnalda P, De Trez C, Ryffel B, Black S, Magez S. Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog. 2008 May; 4(5):e1000078. doi: 10.1371/journal.ppat.1000078 PMID: 18516300
Bhattacharya P, Fan J, Haddad C, Essani A, Gopisetty A, Elshabrawy HA, et al. A novel pancreatic beta-cell targeting bispecific-antibody (BsAb) can prevent the development of type 1 diabetes in NOD mice. Clin Immunol. Jul; 153(1):187-98. doi: 10.1016/j.clim.2014.04.014 PMID: 24792135
Elshabrawy HA, Coughlin MM, Baker SC, Prabhakar BS. Human monoclonal antibodies against highly conserved HR1 and HR2 domains of the SARS-CoV spike protein are more broadly neutralizing. PLoS One. 7(11):e50366. doi: 10.1371/journal.pone.0050366 PMID: 23185609
Bockstal V, Guirnalda P, Caljon G, Goenka R, Telfer JC, Frenkel D, et al. T. brucei infection reduces B lymphopoiesis in bone marrow and truncates compensatory splenic lymphopoiesis through transitional B-cell apoptosis. PLoS Pathog. 2011 Jun; 7(6):e1002089. doi: 10.1371/journal.ppat.1002089 PMID: 21738467
Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med. 2002 Sep 19; 347(12):911-20. PMID: 12239261
Wilson MS, Maizels RM. Regulation of allergy and autoimmunity in helminth infection. Clin Rev Allergy Immunol. 2004 Feb; 26(1):35-50. PMID: 14755074
Drennan MB, Stijlemans B, Van den Abbeele J, Quesniaux VJ, Barkhuizen M, Brombacher F, et al. The induction of a type 1 immune response following a Trypanosoma brucei infection is MyD88 dependent. J Immunol. 2005 Aug 15; 175(4):2501-9. PMID: 16081822
Chu CQ, Swart D, Alcorn D, Tocker J, Elkon KB. Interferon-gamma regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum. 2007 Apr; 56(4):1145-51. PMID: 17393396
Rurangirwa FR, Tabel H, Losos GJ, Tizard IR. Suppression of antibody response to Leptospira biflexa and Brucella abortus and recovery from immunosuppression after Berenil treatment. Infect Immun. 1979 Dec; 26(3):822-6. PMID: 118933
Mattsson L, Larsson P, Erlandsson-Harris H, Klareskog L, Harris RA. Parasite-mediated down-regulation of collagen-induced arthritis (CIA) in DA rats. Clin Exp Immunol. 2000 Dec; 122(3):477-83. PMID: 11122258
Farooq SM, Ashour HM. Type II collagen induces peripheral tolerance in BALB/c mice via the generation of CD8+ T regulatory cells. PLoS One. 2012; 7(11):e48635. doi: 10.1371/journal.pone.0048635 PMID: 23133648
Farooq SM, Kumar A, Ashour HM. Eye-mediated immune tolerance to Type II collagen in arthritisprone strains of mice. J Cell Mol Med. 2014 Dec; 18(12):2512-8. doi: 10.1111/jcmm.12376 PMID: 25211510
Greenwood BM. Autoimmune disease and parasitic infections in Nigerians. Lancet. 1968 Aug 17; 2 (7564):380-2. PMID: 4174413