Advertisement

In Vivo Models for Inflammatory Arthritis

  • Gareth W. JonesEmail author
  • David G. Hill
  • Katie Sime
  • Anwen S. Williams
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1725)

Abstract

In vivo mouse models of inflammatory arthritis are extensively used to investigate pathogenic mechanisms governing inflammation-driven joint damage. Two commonly utilized models include collagen-induced arthritis (CIA) and methylated bovine serum albumin (mBSA) antigen-induced arthritis (AIA). These offer unique advantages for modeling different aspects of human disease. CIA involves breach of immunological tolerance resulting in systemic autoantibody-driven arthritis, while AIA results in local resolving inflammatory flares and articular T cell-mediated damage. Despite limitations that apply to all animal models of human disease, CIA and AIA have been instrumental in identifying pathogenic mediators, immune cell subsets and stromal cell responses that determine disease onset, progression, and severity. Moreover, these models have enabled investigation of disease phases not easily studied in patients and have served as testing beds for novel biological therapies, including cytokine blockers and small molecule inhibitors of intracellular signaling that have revolutionized rheumatoid arthritis treatment.

Key words

Inflammatory arthritis Rheumatoid arthritis Collagen-induced arthritis Antigen-induced arthritis Histopathology 

Notes

Acknowledgments

G.J. is supported by an Arthritis Research UK Career Development Fellowship (20305). D.H. is supported by a Medical Research Council PhD studentship and Life Science Research Network Wales, an initiative funded through the Welsh Government’s Ser Cymru program. K.S. is supported by a PhD studentship funded through a generous donation from The Elizabeth Owens Bequest at Cardiff University.

References

  1. 1.
    Smolen JS, Aletaha D, McInnes IB (2016) Rheumatoid arthritis. Lancet S0140-6736:30173–30178Google Scholar
  2. 2.
    Asquith DL, Miller AM, McInnes IB, Liew FY (2009) Animal models of rheumatoid arthritis. Eur J Immunol 39:2040–2044CrossRefPubMedGoogle Scholar
  3. 3.
    Brand DD (2005) Rodent models of rheumatoid arthritis. Comp Med 55:114–122PubMedGoogle Scholar
  4. 4.
    Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B (1980) Immunisation against heterologous type II collagen induces arthritis in mice. Nature 283:666–668CrossRefPubMedGoogle Scholar
  5. 5.
    Luross JA, Williams NA (2001) The genetic and immunopathological processes underlying collagen-induced arthritis. Immunology 103:407–416CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Inglis JJ, Criado G, Medghalchi M, Andrews M, Sandison A, Feldmann M, Williams RO (2007) Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res Ther 9:R113CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Campbell IK, Hamilton JA, Wicks IP (2000) Collagen-induced arthritis in C57BL/6 (H-2b) mice: new insights into an important disease model of rheumatoid arthritis. Eur J Immunol 30:1568–1575CrossRefPubMedGoogle Scholar
  8. 8.
    Brand DD, Latham KA, Rosloniec EF (2007) Collagen-induced arthritis. Nat Protoc 2:1269–1275CrossRefPubMedGoogle Scholar
  9. 9.
    Boissier MC, Feng XZ, Carlioz A, Roudier R, Fournier C (1987) Experimental autoimmune arthritis in mice. I. Homologous type II collagen is responsible for self-perpetuating chronic polyarthritis. Ann Rheum Dis 46:691–700CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Holmdahl R, Jansson L, Larsson E, Rubin K, Klareskog L (1986) Homologous type II collagen induces chronic and progressive arthritis in mice. Arthritis Rheum 29:106–113CrossRefPubMedGoogle Scholar
  11. 11.
    Malfait AM, Williams RO, Malik AS, Maini RN, Feldmann M (2001) Chronic relapsing homologous collagen-induced arthritis in DBA/1 mice as a model for testing disease-modifying and remission-inducing therapies. Arthritis Rheum 44:1215–1224CrossRefPubMedGoogle Scholar
  12. 12.
    Brackertz D, Mitchell GF, Mackay IR (1977) Antigen-induced arthritis in mice. I. Induction of arthritis in various strains of mice. Arthritis Rheum 20:841–850CrossRefPubMedGoogle Scholar
  13. 13.
    Brackertz D, Mitchell GF, Vadas MA, Mackay IR, Miller JF (1977) Studies on antigen-induced arthritis in mice. II. Immunologic correlates of arthritis susceptibility in mice. J Immunol 118:1639–1644PubMedGoogle Scholar
  14. 14.
    Wong PK, Quinn JM, Sims NA, van Nieuwenhuijze A, Campbell IK, Wicks IP (2006) Interleukin-6 modulates production of T lymphocyte-derived cytokines in antigen-induced arthritis and drives inflammation-induced osteoclastogenesis. Arthritis Rheum 54:158–168CrossRefPubMedGoogle Scholar
  15. 15.
    van den Berg WB, van de Putte LB (1985) Electrical charge of the antigen determines its localization in the mouse knee joint. Deep penetration of cationic BSA in hyaline articular cartilage. Am J Pathol 121:224–234PubMedPubMedCentralGoogle Scholar
  16. 16.
    van den Berg WB, van de Putte LB, Zwarts WA, Joosten LA (1984) Electrical charge of the antigen determines intraarticular antigen handling and chronicity of arthritis in mice. J Clin Invest 74:1850–1859CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Maffia P, Brewer JM, Gracie JA, Ianaro A, Leung BP, Mitchell PJ, Smith KM, McInnes IB, Garside P (2004) Inducing experimental arthritis and breaking self-tolerance to joint-specific antigens with trackable, ovalbumin-specific T cells. J Immunol 173:151–156CrossRefPubMedGoogle Scholar
  18. 18.
    Nickdel MB, Conigliaro P, Valesini G, Hutchison S, Benson R, Bundick RV, Leishman AJ, McInnes IB, Brewer JM, Garside P (2009) Dissecting the contribution of innate and antigen-specific pathways to the breach of self-tolerance observed in a murine model of arthritis. Ann Rheum Dis 68:1059–1066CrossRefPubMedGoogle Scholar
  19. 19.
    Nowell MA, Williams AS, Carty SA, Scheller J, Hayes AJ, Jones GW, Richards PJ, Slinn S, Ernst M, Jenkins BJ, Topley N, Rose-John S, Jones SA (2009) Therapeutic targeting of IL-6 trans signaling counteracts STAT3 control of experimental inflammatory arthritis. J Immunol 182:613–622CrossRefPubMedGoogle Scholar
  20. 20.
    Wengner AM, Hopken UE, Petrow PK, Hartmann S, Schurigt U, Brauer R, Lipp M (2007) CXCR5- and CCR7-dependent lymphoid neogenesis in a murine model of chronic antigen-induced arthritis. Arthritis Rheum 56:3271–3283CrossRefPubMedGoogle Scholar
  21. 21.
    Jones GW, Bombardieri M, Greenhill CJ, McLeod L, Nerviani A, Rocher-Ros V, Cardus A, Williams AS, Pitzalis C, Jenkins BJ, Jones SA (2015) Interleukin-27 inhibits ectopic lymphoid-like structure development in early inflammatory arthritis. J Exp Med 212:1793–1802CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hawkins P, Armstrong R, Boden T, Garside P, Knight K, Lilley E, Seed M, Wilkinson M, Williams RO (2015) Applying refinement to the use of mice and rats in rheumatoid arthritis research. Inflammopharmacology 23:131–150CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 39:175–191CrossRefPubMedGoogle Scholar
  24. 24.
    Charan J, Kantharia ND (2013) How to calculate sample size in animal studies? J Pharmacol Pharmacother 4:303–306CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    van den Berg WB, Joosten LA, van Lent PL (2007) Murine antigen-induced arthritis. Methods Mol Med 136:243–253CrossRefPubMedGoogle Scholar
  26. 26.
    Lens JW, van den Berg WB, van de Putte LB (1984) Flare-up of antigen-induced arthritis in mice after challenge with intravenous antigen: studies on the characteristics of and mechanisms involved in the reaction. Clin Exp Immunol 55:287–294PubMedPubMedCentralGoogle Scholar
  27. 27.
    Vingsbo C, Sahlstrand P, Brun JG, Jonsson R, Saxne T, Holmdahl R (1996) Pristane-induced arthritis in rats: a new model for rheumatoid arthritis with a chronic disease course influenced by both major histocompatibility complex and non-major histocompatibility complex genes. Am J Pathol 149:1675–1683PubMedPubMedCentralGoogle Scholar
  28. 28.
    Holmdahl R, Goldschmidt TJ, Kleinau S, Kvick C, Jonsson R (1992) Arthritis induced in rats with adjuvant oil is a genetically restricted, alpha beta T-cell dependent autoimmune disease. Immunology 76:197–202PubMedPubMedCentralGoogle Scholar
  29. 29.
    Katz L, Piliero SJ (1969) A study of adjuvant-induced polyarthritis in the rat with special reference to associated immunological phenomena. Ann N Y Acad Sci 147:517–536CrossRefPubMedGoogle Scholar
  30. 30.
    Zidek Z, Perlik F (1971) Genetic control of adjuvant-induced arthritis in rats. J Pharm Pharmacol 23:389–390CrossRefPubMedGoogle Scholar
  31. 31.
    Cromartie WJ, Craddock JG, Schwab JH, Anderle SK, Yang CH (1977) Arthritis in rats after systemic injection of streptococcal cells or cell walls. J Exp Med 146:1585–1602CrossRefPubMedGoogle Scholar
  32. 32.
    Carlsen S, Hansson AS, Olsson H, Heinegard D, Holmdahl R (1998) Cartilage oligomeric matrix protein (COMP)-induced arthritis in rats. Clin Exp Immunol 114:477–484CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hanyecz A, Berlo SE, Szanto S, Broeren CP, Mikecz K, Glant TT (2004) Achievement of a synergistic adjuvant effect on arthritis induction by activation of innate immunity and forcing the immune response toward the Th1 phenotype. Arthritis Rheum 50:1665–1676CrossRefPubMedGoogle Scholar
  34. 34.
    Carlsen S, Nandakumar KS, Backlund J, Holmberg J, Hultqvist M, Vestberg M, Holmdahl R (2008) Cartilage oligomeric matrix protein induction of chronic arthritis in mice. Arthritis Rheum 58:2000–2011CrossRefPubMedGoogle Scholar
  35. 35.
    Lu S, Carlsen S, Hansson AS, Holmdahl R (2002) Immunization of rats with homologous type XI collagen leads to chronic and relapsing arthritis with different genetics and joint pathology than arthritis induced with homologous type II collagen. J Autoimmun 18:199–211CrossRefPubMedGoogle Scholar
  36. 36.
    Trentham DE, Townes AS, Kang AH (1977) Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med 146:857–868CrossRefPubMedGoogle Scholar
  37. 37.
    Griffiths RJ (1992) Characterisation and pharmacological sensitivity of antigen arthritis induced by methylated bovine serum albumin in the rat. Agents Actions 35:88–95CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2018

Authors and Affiliations

  • Gareth W. Jones
    • 1
    Email author
  • David G. Hill
    • 1
  • Katie Sime
    • 1
  • Anwen S. Williams
    • 1
  1. 1.Division of Infection and Immunity, Systems Immunity University Research Institute, School of MedicineCardiff UniversityCardiffUK

Personalised recommendations