View More View Less
  • 1 Vaccines and Sera “Torlak” Immunology Research Center, Institute of Virology Belgrade Serbia
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $784.00

We have investigated the humoral immune response to antigens of predominant gut aerobic bacterial strains (i.e. Escherichia coli) over the course of adjuvant arthritis and oil-induced arthritis in two inbred rat strains: Dark Agouti (DA) and Albino Oxford (AO). We report the presence of antibodies specific to proteins of E. coli in molecular weight range between 20–30 kDa in sera of diseased DA rats, and the absence of these antibodies in the sera of AO rats. In DA rats, CFA and IFA provoked a stronger antibody response to E. coli, especially of the IgG2b antibody class. Intramuscular administration of E. coli preceding the adjuvant arthritis induction had no effect on the development and course of disease, as well as on the activation of T cells in the draining inguinal lymph nodes. Higher serum levels of natural and induced IgA antibodies, combined with a higher CD3+CD26+ cell percentage were found in AO rats. The observed correlation between the serologic response to commensal flora and rats’ genetic background as a defining factor for arthritis susceptibility may contribute to the process of creating a favorable (or less favorable) milieu for arthritis development.

  • Lanchbury, J.S.: The HLA association with rheumatoid arthritis. Clin Exp Rheumatol 10, 301–304 (1992).

    Lanchbury J.S. , 'The HLA association with rheumatoid arthritis ' (1992 ) 10 Clin Exp Rheumatol : 301 -304.

    • Search Google Scholar
  • Bridges, S.L. Jr.: The genetics of rheumatoid arthritis: influences on susceptibility, severity, and treatment response. Curr Rheumatol Rep 1, 164–171 (1999).

    Bridges S.L. , 'The genetics of rheumatoid arthritis: influences on susceptibility, severity, and treatment response ' (1999 ) 1 Curr Rheumatol Rep : 164 -171.

    • Search Google Scholar
  • Corrigall, V.M., Bodman-Smith, M.D., Fife, M.S., Canas, B., Myers L.K., Wooley, P., Soh, C., Staines, N.A., Pappin, D.J., Berlo, S.E., van Eden, W., van Der Zee, R., Lanchbury, J.S., Panayi, G.S.: The human endoplasmic reticulum molecular chaperone BiP is an autoantigen for rheumatoid arthritis and prevents the induction of experimental arthritis. J Immunol 166, 1492–1498 (2001).

    Panayi G.S. , 'The human endoplasmic reticulum molecular chaperone BiP is an autoantigen for rheumatoid arthritis and prevents the induction of experimental arthritis ' (2001 ) 166 J Immunol : 1492 -1498.

    • Search Google Scholar
  • Jawaheer, D., Gregersen, P.K.: Rheumatoid arthritis. The genetic components. Rheum Dis Clin North Am 28, 1–15 (2002).

    Gregersen P.K. , 'Rheumatoid arthritis. The genetic components ' (2002 ) 28 Rheum Dis Clin North Am : 1 -15.

    • Search Google Scholar
  • Christen, U., von Herrath, M.G.: Infections and autoimmunity–good or bad? J Immunol 174, 7481–7486 (2005).

    Herrath M.G. , 'Infections and autoimmunity–good or bad ' (2005 ) 174 J Immunol : 7481 -7486.

    • Search Google Scholar
  • Tlaskalova-Hogenova, H., Tučkova, L., Lodinova-Žadnikova, R., Štepankova, R., Cukrowska, B., Funda, D.P., Striž, I., Kozakova, H., Trebichavsky, I., Sokol, D., Rehakova, Z., Šinkora, J., Fundova, P., Horakova, D., Jelinkova, L., Sanchez, D.: Mucosal immunity: Its role in defense and allergy. Int Arch Allergy Immunol 128, 77–89 (2002).

    Sanchez D. , 'Mucosal immunity: Its role in defense and allergy ' (2002 ) 128 Int Arch Allergy Immunol : 77 -89.

    • Search Google Scholar
  • Kverka, M., Tlaskalova-Hogenova, H.: Two faces of microbiota in inflammatory and autoimmune diseases: triggers and drugs. APMIS 121, 403–421 (2013).

    Tlaskalova-Hogenova H. , 'Two faces of microbiota in inflammatory and autoimmune diseases: triggers and drugs ' (2013 ) 121 APMIS : 403 -421.

    • Search Google Scholar
  • Scher, J.U., Abramson, S.B.: The microbiome and rheumatoid arthritis. Nat Rev Rheumatol 7, 569–578 (2011).

    Abramson S.B. , 'The microbiome and rheumatoid arthritis ' (2011 ) 7 Nat Rev Rheumatol : 569 -578.

    • Search Google Scholar
  • Tlaskalova-Hogenova, H., Štepankova, R., Hudcovic, T., Tučkova, L., Cukrowska, B., Lodinova-Žadnikova, R., Kozakova, H., Rossman, P., Bartova, J., Sokol, D., Funda, D.P., Borovska, D., Rehakova, Z., Šinkora, J., Hofman, J., Drastich, P., Kokešova, A.: Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunology Lett 93, 97–108 (2004).

    Kokešova A. , 'Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases ' (2004 ) 93 Immunology Lett : 97 -108.

    • Search Google Scholar
  • Dimitrijević, M., Laban, O., Djurić, V.J., Stanojević, S., Miletić, T., Kovacevič-Jovanović, V., Todorović, Č., Radulović, J.: Behavior and severity of adjuvant arthritis in four rat strains. Brain Behav Immun 15, 255–265 (2001).

    Radulović J. , 'Behavior and severity of adjuvant arthritis in four rat strains ' (2001 ) 15 Brain Behav Immun : 255 -265.

    • Search Google Scholar
  • Kovačevic-Jovanović, V., Mitić, K., Stanojević, S., Miletic, T., Vujić, V., Dimitrijević, M.: Production of H2O2 and NO by rat peritoneal macrophages in response to gut commensal bacteria. Acta Veterinaria 59, 111–122 (2009).

    Dimitrijević M. , 'Production of H2O2 and NO by rat peritoneal macrophages in response to gut commensal bacteria ' (2009 ) 59 Acta Veterinaria : 111 -122.

    • Search Google Scholar
  • Kovačević-Jovanović, V., Miletić, T., Stanojević, S., Mitić, K., Dimitrijević, M.: Strain differences in the humoral immune response to commensal bacterial antigens in rats. Acta Microbiol Immunol Hung 60, 271–288 (2013).

    Dimitrijević M. , 'Strain differences in the humoral immune response to commensal bacterial antigens in rats ' (2013 ) 60 Acta Microbiol Immunol Hung : 271 -288.

    • Search Google Scholar
  • Holmdahl, R., Goldschmidt, T.J., Kleinau, S., Kvick, C., Jonsson, R.: Arthritis induced in rats with adjuvant oil is a genetically restricted, T-cell dependent autoimmune disease. Immunology 76, 197–202 (1992).

    Jonsson R. , 'Arthritis induced in rats with adjuvant oil is a genetically restricted, T-cell dependent autoimmune disease ' (1992 ) 76 Immunology : 197 -202.

    • Search Google Scholar
  • Griffiths, M.M., DeWitt, C.W.: Immunogenetic control of experimental collagen-induced arthritis in rats. II. ECIA susceptibility and immune response to type II collagen (CALF) are linked to RT1. J Immunogenet 8, 463–470 (1981).

    DeWitt C.W. , 'Immunogenetic control of experimental collagen-induced arthritis in rats. II. ECIA susceptibility and immune response to type II collagen (CALF) are linked to RT1 ' (1981 ) 8 J Immunogenet : 463 -470.

    • Search Google Scholar
  • Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685 (1970).

    Laemmli U.K. , 'Cleavage of structural proteins during the assembly of the head of bacteriophage T4 ' (1970 ) 227 Nature : 680 -685.

    • Search Google Scholar
  • Towbin, H., Stachlin, T., Gordon, J.: Electrophoretic transfer of proteins from polyacrylamide gels to nitro-cellulose sheets: procedures and some applications. Proc Natl Acad Sci U S A 76, 4350–4354 (1979).

    Gordon J. , 'Electrophoretic transfer of proteins from polyacrylamide gels to nitro-cellulose sheets: procedures and some applications ' (1979 ) 76 Proc Natl Acad Sci U S A : 4350 -4354.

    • Search Google Scholar
  • Albani, S., Tuckwell, J., Esparza, D., Carson, D., Roudier, J.: The susceptibility sequence to rheumatoid arthritis is a cross-reactive B-cell epitope shared by Escherichia coli heat shock protein dnaJ and the histocompatibility leucocyte antigen DRB10401 molecule. J Clin Investig 89, 327–331 (1992).

    Roudier J. , 'The susceptibility sequence to rheumatoid arthritis is a cross-reactive B-cell epitope shared by Escherichia coli heat shock protein dnaJ and the histocompatibility leucocyte antigen DRB10401 molecule ' (1992 ) 89 J Clin Investig : 327 -331.

    • Search Google Scholar
  • Newkirk, M.M., Goldbach-Mansky, R., Senior, B.W., Klippel, J., Schumacher, H.R, Jr, El-Gabalawy, H.S.: Elevated levels of IgM and IgA antibodies to Proteus mirabilis and IgM antibodies to Escherichia coli are associated with early rheumatoid factor (RF)-positive rheumatoid arthritis. Rheumatology 44, 1433–1441 (2005).

    El-Gabalawy H.S. , 'Elevated levels of IgM and IgA antibodies to Proteus mirabilis and IgM antibodies to Escherichia coli are associated with early rheumatoid factor (RF)-positive rheumatoid arthritis ' (2005 ) 44 Rheumatology : 1433 -1441.

    • Search Google Scholar
  • Wallin, R.P., Lundqvist, A., More, S.H., von Bonin, A., Kiessling, R., Ljunggren, H.G.: Heat-shock proteins as activators of the innate immune system. Trends Immunol 23, 130–135 (2002).

    Ljunggren H.G. , 'Heat-shock proteins as activators of the innate immune system ' (2002 ) 23 Trends Immunol : 130 -135.

    • Search Google Scholar
  • Zugel, U., Kaufmann, S.H.: Role of heat shock proteins in protection from and pathogenesis of infectious diseases. Clin Microbiol Rev 12, 19–39 (1999).

    Kaufmann S.H. , 'Role of heat shock proteins in protection from and pathogenesis of infectious diseases ' (1999 ) 12 Clin Microbiol Rev : 19 -39.

    • Search Google Scholar
  • Desai, N.S., Agarwal, A.A., Uplap, S.S.: HSP: evolved and conserved proteins, structure and sequence studies. Int J of Bioi Res 2, 67–87 (2010).

    Uplap S.S. , 'HSP: evolved and conserved proteins, structure and sequence studies ' (2010 ) 2 Int J of Bioi Res : 67 -87.

    • Search Google Scholar
  • Huang, M.N., Yu, H., Moudgil, K.D.: The involvement of heat-shock proteins in the pathogenesis of autoimmune arthritis: a critical appraisal. Semin Arthritis Rheum 40, 164–175 (2010).

    Moudgil K.D. , 'The involvement of heat-shock proteins in the pathogenesis of autoimmune arthritis: a critical appraisal ' (2010 ) 40 Semin Arthritis Rheum : 164 -175.

    • Search Google Scholar
  • Kohashi, O., Kohashi, Y., Takahashi, T., Ozawa, A., Shigematsu, N.: Suppressive effect of Escherichia coli on adjuvant-induced arthritis in germ-free rats. Arthritis Rheum 29, 547–553 (1986).

    Shigematsu N. , 'Suppressive effect of Escherichia coli on adjuvant-induced arthritis in germ-free rats ' (1986 ) 29 Arthritis Rheum : 547 -553.

    • Search Google Scholar
  • Ulmansky, R., Cohen, C.J., Szafer, F., Moallem, E., Fridlender, Z.G., Kashi, Y., Naparstek, Y.: Resistance to adjuvant arthritis is due to protective antibodies against heat shock protein surface epitopes and the induction of IL-10 secretion. J Immunol 168, 6463–6469 (2002).

    Naparstek Y. , 'Resistance to adjuvant arthritis is due to protective antibodies against heat shock protein surface epitopes and the induction of IL-10 secretion ' (2002 ) 168 J Immunol : 6463 -6469.

    • Search Google Scholar
  • van Eden, W., Wendling, U., Paul, L., Prakken, B., van Kooten, P., van der Zee, R.: Arthritis protective regulatory potential of self-heat shock protein cross-reactive T cells. Cell Stress & Chaperones 5, 452–457 (2000).

    Zee R. , 'Arthritis protective regulatory potential of self-heat shock protein cross-reactive T cells ' (2000 ) 5 Cell Stress & Chaperones : 452 -457.

    • Search Google Scholar
  • Cobelens, P.M., Heijnen, C.J., Nieuwenhuis, E.E., Kramer, P.P., van der Zee, R., van Eden, W., Kavelaars, A.: Treatment of adjuvant-induced arthritis by oral administration of mycobacterial Hsp65 during disease. Arthritis Rheum 43, 2694–2702 (2000).

    Kavelaars A. , 'Treatment of adjuvant-induced arthritis by oral administration of mycobacterial Hsp65 during disease ' (2000 ) 43 Arthritis Rheum : 2694 -2702.

    • Search Google Scholar
  • Bowman, L.M., Holt, P.G.: Selective enhancement of systemic Th1 immunity in immunologically immature rats with an orally administered bacterial extract. Infect Immun 69, 3719–3727 (2001).

    Holt P.G. , 'Selective enhancement of systemic Th1 immunity in immunologically immature rats with an orally administered bacterial extract ' (2001 ) 69 Infect Immun : 3719 -3727.

    • Search Google Scholar
  • Saoudi, A., Kuhn, J., Huygen, K., de Kozak, Y., Velu, T., Goldman, M., Druet, P., Bellon, B.: TH2 activated cells prevent experimental autoimmune uveoretinitis, a TH1-dependent autoimmune disease. Eur J Immunol 23, 3096–3103 (1993).

    Bellon B. , 'TH2 activated cells prevent experimental autoimmune uveoretinitis, a TH1-dependent autoimmune disease ' (1993 ) 23 Eur J Immunol : 3096 -3103.

    • Search Google Scholar
  • Wykes, M., Pombo, A., Jenkins, C., MacPherson, G.G.: Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J Immunol 161, 1313–1319 (1998).

    MacPherson G.G. , 'Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response ' (1998 ) 161 J Immunol : 1313 -1319.

    • Search Google Scholar
  • Shibaki, A., Katz, S.I.: Induction of skewed Th1/Th2 T-cell differentiation via subcutaneous immunization with Freund’s adjuvant. Exp Dermatol 11, 126–134 (2002).

    Katz S.I. , 'Induction of skewed Th1/Th2 T-cell differentiation via subcutaneous immunization with Freund’s adjuvant ' (2002 ) 11 Exp Dermatol : 126 -134.

    • Search Google Scholar
  • Billiau, A., Matthys, P.: Modes of action of Freund’s adjuvants in experimental models of autoimmune diseases. J Leukoc Biol 70, 849–860 (2001).

    Matthys P. , 'Modes of action of Freund’s adjuvants in experimental models of autoimmune diseases ' (2001 ) 70 J Leukoc Biol : 849 -860.

    • Search Google Scholar
  • Busso, N., Wagtmann, N., Herling, C., Chobaz-Péclat, V., Bischof-Delaloye, A., So, A., Grouzmann, E.: Circulating CD26 is negatively associated with inflammation in human and experimental arthritis. Am J Pathol 66, 433–442 (2005).

    Grouzmann E. , 'Circulating CD26 is negatively associated with inflammation in human and experimental arthritis ' (2005 ) 66 Am J Pathol : 433 -442.

    • Search Google Scholar
  • Preller, V., Gerber, A., Wrenger, S., Togni, M., Marguet, D., Tadje, J., Lendeckel, U., Röcken, C., Faust, J., Neubert, K., Schraven, B., Martin, R., Ansorge, S., Brocke, S., Reinhold, D.: TGF-beta1-mediated control of central nervous system inflammation and autoimmunity through the inhibitory receptor CD26. J Immunol 178, 4632–4640 (2007).

    Reinhold D. , 'TGF-beta1-mediated control of central nervous system inflammation and autoimmunity through the inhibitory receptor CD26 ' (2007 ) 178 J Immunol : 4632 -4640.

    • Search Google Scholar
  • Reinhold, D., Kähne, T., Steinbrecher, A., Wrenger, S., Neubert, K., Ansorge, S., Brocke, S.: The role of dipeptidyl peptidase IV (DP IV) enzymatic activity in T cell activation and autoimmunity. Biol chem 383, 1133–1138 (2002).

    Brocke S. , 'The role of dipeptidyl peptidase IV (DP IV) enzymatic activity in T cell activation and autoimmunity ' (2002 ) 383 Biol chem : 1133 -1138.

    • Search Google Scholar
  • Sedo, A., Duke-Cohan, J.S., Balaziova, E., Sedova, L.R.: Dipeptidyl peptidase IV activity and/or structure homologs: contributing factors in the pathogenesis of rheumatoid arthritis? Arthritis Res Ther 7, 253–269 (2005).

    Sedova L.R. , 'Dipeptidyl peptidase IV activity and/or structure homologs: contributing factors in the pathogenesis of rheumatoid arthritis ' (2005 ) 7 Arthritis Res Ther : 253 -269.

    • Search Google Scholar
  • De Meester, I., Korom, S., Van Damme, J., Scharpé, S.: CD26, let it cut or cut it down. Immunol Today 20, 367–375 (1999).

    Scharpé S. , 'CD26, let it cut or cut it down ' (1999 ) 20 Immunol Today : 367 -375.

  • Bush, K.A., Walker, J.S., Lee, C.S., Kirkham, B.W.: Cytokine expression and synovial pathology in the initiation and spontaneous resolution phases of adjuvant arthritis: interleukin-17 expression is upregulated in early disease. Clin Exp Immunol 123, 487–495 (2001).

    Kirkham B.W. , 'Cytokine expression and synovial pathology in the initiation and spontaneous resolution phases of adjuvant arthritis: interleukin-17 expression is upregulated in early disease ' (2001 ) 123 Clin Exp Immunol : 487 -495.

    • Search Google Scholar
  • Ohnuma, K., Yamochi, T., Uchiyama, M., Nishibashi, K., Iwata, S., Hosono, O., Kawasaki, H., Tanaka, H., Dang, N.H., Morimoto, C.: CD26 mediates dissociation of tollip and IRAK-1 from caveolin-1 and induces upregulation of CD86 on antigen-presenting cells. Mol Cell Biol 25, 7743–7757 (2005).

    Morimoto C. , 'CD26 mediates dissociation of tollip and IRAK-1 from caveolin-1 and induces upregulation of CD86 on antigen-presenting cells ' (2005 ) 25 Mol Cell Biol : 7743 -7757.

    • Search Google Scholar

Monthly Content Usage

Abstract Views Full Text Views PDF Downloads
Oct 2020 6 0 0
Nov 2020 6 2 0
Dec 2020 3 0 0
Jan 2021 0 0 0
Feb 2021 8 1 2
Mar 2021 5 0 0
Apr 2021 3 0 0