Gut Flora Induces and Maintains Resistance Against Streptococcal Cell Wall-induced Arthritis in F344 Rats

Overview

Journal Clin Exp Immunol

Publisher Oxford University Press

Specialty Allergy & Immunology

Date 1992 May 1

PMID 1572097

Citations 16

Authors

M F van den Broek

M C van Bruggen

J P Koopman

M P Hazenberg

W B van den Berg

Affiliations

Soon will be listed here.

Abstract

Streptococcal cell wall (SCW)-induced arthritis is a chronic, erosive polyarthritis that can be induced in susceptible Lewis rats by one i.p. injection of an aqueous, sterile suspension of SCW. F344 rats are resistant to chronic joint inflammation. Our previous studies showed a correlation between susceptibility to SCW-induced arthritis and the ability to mount SCW-specific T cell responses, suggesting tolerance to SCW as a putative mechanism. Here we prevented the induction of tolerance to bacterial epitopes in F344 rats by using them germ-free and analysed susceptibility to arthritis subsequently. In addition, we conventionalized germ-free F344 rats at different times before induction of arthritis. Our results show that germ-free F344 rats are susceptible to SCW-induced arthritis with a similar severity, chronicity, incidence and onset as Lewis rats. Moreover, T cells isolated from germ-free F344 rats were able to respond to SCW. Conventionalization dramatically moderates arthritis and makes T cells unresponsive to SCW again. Thus, in normal rats (F344) a state of tolerance to arthritogenic epitopes is induced (neonatally) and maintained through life by the bacterial flora, resulting in resistance to bacterium-induced arthritides. In arthritis-prone (Lewis) rats, this tolerance is deficient and/or easily broken.

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References

WOOD F, Pearson C . Protection of rats against adjuvant arthritis by bacterial lipoplysaccharides. Science. 1962; 137(3529):544-5. DOI: 10.1126/science.137.3529.544. View

Kotani S, Watanabe Y, Shimono T, Harada K, Shiba T . Correlation between the immunoadjuvant activities and pyrogenicities of synthetic N-acetylmuramyl-peptides or -amino acids. Biken J. 1976; 19(1):9-13. View

van den Broek M, Van de Langerijt L, van Bruggen M, Billingham M, van den Berg W . Treatment of rats with monoclonal anti-CD4 induces long-term resistance to streptococcal cell wall-induced arthritis. Eur J Immunol. 1992; 22(1):57-61. DOI: 10.1002/eji.1830220110. View

Yocum D, Allen J, Wahl S, Calandra G, Wilder R . Inhibition by cyclosporin A of streptococcal cell wall-induced arthritis and hepatic granulomas in rats. Arthritis Rheum. 1986; 29(2):262-73. DOI: 10.1002/art.1780290215. View

Benjamin R, Qin S, Wise M, Cobbold S, Waldmann H . Mechanisms of monoclonal antibody-facilitated tolerance induction: a possible role for the CD4 (L3T4) and CD11a (LFA-1) molecules in self-non-self discrimination. Eur J Immunol. 1988; 18(7):1079-88. DOI: 10.1002/eji.1830180717. View

DeJoy S, Ferguson K, SAPP T, Zabriskie J, Oronsky A, Kerwar S . Streptococcal cell wall arthritis. Passive transfer of disease with a T cell line and crossreactivity of streptococcal cell wall antigens with Mycobacterium tuberculosis. J Exp Med. 1989; 170(2):369-82. PMC: 2189401. DOI: 10.1084/jem.170.2.369. View

van den Broek M . Streptococcal cell wall-induced polyarthritis in the rat. Mechanisms for chronicity and regulation of susceptibility. APMIS. 1989; 97(10):861-78. DOI: 10.1111/j.1699-0463.1989.tb00491.x. View

van den Broek M, Hogervorst E, van Bruggen M, van Eden W, van der Zee R, van den Berg W . Protection against streptococcal cell wall-induced arthritis by pretreatment with the 65-kD mycobacterial heat shock protein. J Exp Med. 1989; 170(2):449-66. PMC: 2189406. DOI: 10.1084/jem.170.2.449. View

van den Broek M, van Bruggen M, van de Putte L, van den Berg W . T cell responses to streptococcal antigens in rats: relation to susceptibility to streptococcal cell wall-induced arthritis. Cell Immunol. 1988; 116(1):216-29. DOI: 10.1016/0008-8749(88)90222-5. View

10.

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. 1986; 29(4):547-53. DOI: 10.1002/art.1780290413. View

11.

Wilder R, Allen J, Hansen C . Thymus-dependent and -independent regulation of Ia antigen expression in situ by cells in the synovium of rats with streptococcal cell wall-induced arthritis. Differences in site and intensity of expression in euthymic, athymic, and cyclosporin.... J Clin Invest. 1987; 79(4):1160-71. PMC: 424298. DOI: 10.1172/JCI112933. View

12.

Allen J, Malone D, Wahl S, Calandra G, Wilder R . Role of the thymus in streptococcal cell wall-induced arthritis and hepatic granuloma formation. Comparative studies of pathology and cell wall distribution in athymic and euthymic rats. J Clin Invest. 1985; 76(3):1042-56. PMC: 423980. DOI: 10.1172/JCI112057. View

13.

van den Broek M, van Bruggen M, Stimpson S, Severijnen A, van de Putte L, van den Berg W . Flare-up reaction of streptococcal cell wall induced arthritis in Lewis and F344 rats: the role of T lymphocytes. Clin Exp Immunol. 1990; 79(2):297-306. PMC: 1534749. DOI: 10.1111/j.1365-2249.1990.tb05194.x. View

14.

Wilder R, Allen J, Wahl L, Calandra G, Wahl S . The pathogenesis of group A streptococcal cell wall-induced polyarthritis in the rat. Comparative studies in arthritis resistant and susceptible inbred rat strains. Arthritis Rheum. 1983; 26(12):1442-51. DOI: 10.1002/art.1780261205. View

15.

Koopman J, Prins R, Mullink J, Welling G, Kennis H, Hectors M . Association of germfree mice with bacteria isolated from the intestinal tract of "normal" mice. Z Versuchstierkd. 1983; 25(2):57-62. View

16.

van den Berg W, van Beusekom H, van de Putte L, Zwarts W, van der Sluis M . Antigen handling in antigen-induced arthritis in mice: an autoradiographic and immunofluorescence study using whole joint sections. Am J Pathol. 1982; 108(1):9-16. PMC: 1916019. View

17.

Fox A, Brown R, ANDERLE S, Chetty C, CROMARTIE W, GOODER H . Arthropathic properties related to the molecular weight of peptidoglycan-polysaccharide polymers of streptococcal cell walls. Infect Immun. 1982; 35(3):1003-10. PMC: 351147. DOI: 10.1128/iai.35.3.1003-1010.1982. View

18.

Morrison D, Ryan J . Bacterial endotoxins and host immune responses. Adv Immunol. 1979; 28:293-450. DOI: 10.1016/s0065-2776(08)60802-0. View

19.

CROMARTIE W, CRADDOCK J, Schwab J, ANDERLE S, Yang C . Arthritis in rats after systemic injection of streptococcal cells or cell walls. J Exp Med. 1977; 146(6):1585-602. PMC: 2181919. DOI: 10.1084/jem.146.6.1585. View

20.

Bretscher P, Cohn M . A theory of self-nonself discrimination. Science. 1970; 169(3950):1042-9. DOI: 10.1126/science.169.3950.1042. View