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Applicability and implementation of the collagen‑induced arthritis mouse model, including protocols (Review)
- Authors:
- Jing Luan
- Zhifang Hu
- Jianghong Cheng
- Ruisan Zhang
- Peng Yang
- Huifang Guo
- Gang Nan
- Na Guo
- Xingchun Gou
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Affiliations: Shaanxi Key Laboratory of Brain Disorders and Department of Immunology, Xi'an Medical University, Xi'an, Shaanxi 710021, P.R. China, Intensive Care Unit, Gansu Provincial People's Hospital, Lanzhou, Gansu 730000, P.R. China, National Translational Science Center for Molecular Medicine and Department of Cell Biology, Fourth Military Medical University, Xi'an, Shaanxi 710032, P.R. China - Published online on: July 1, 2021 https://doi.org/10.3892/etm.2021.10371
- Article Number: 939
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Copyright: © Luan et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
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Bird P, Kirkham B, Portek I, Shnier R, Joshua F, Edmonds J and Lassere M: Documenting damage progression in a two-year longitudinal study of rheumatoid arthritis patients with established disease (the DAMAGE study cohort): Is there an advantage in the use of magnetic resonance imaging as compared with plain radiography? Arthritis Rheum. 50:1383–1389. 2004.PubMed/NCBI View Article : Google Scholar | |
Døhn UM, Ejbjerg BJ, Hasselquist M, Narvestad E, Møller J, Thomsen HS and Østergaard M: Detection of bone erosions in rheumatoid arthritis wrist joints with magnetic resonance imaging, computed tomography and radiography. Arthritis Res Ther. 10(R25)2008.PubMed/NCBI View Article : Google Scholar | |
van der Woude D and van der Helm-van Mil AHM: Update on the epidemiology, risk factors, and disease outcomes of rheumatoid arthritis. Best Pract Res Clin Rheumatol. 32:174–187. 2018.PubMed/NCBI View Article : Google Scholar | |
Ejbjerg BJ, Vestergaard A, Jacobsen S, Thomsen HS and Østergaard M: The smallest detectable difference and sensitivity to change of magnetic resonance imaging and radiographic scoring of structural joint damage in rheumatoid arthritis finger, wrist, and toe joints: A comparison of the OMERACT rheumatoid arthritis magnetic resonance imaging score applied to different joint combinations and the Sharp/van der Heijde radiographic score. Arthritis Rheum. 52:2300–2306. 2005.PubMed/NCBI View Article : Google Scholar | |
Bendstrup E, Møller J, Kronborg-White S, Prior TS and Hyldgaard C: Interstitial Lung Disease in Rheumatoid Arthritis Remains a Challenge for Clinicians. J Clin Med. 8(E2038)2019.PubMed/NCBI View Article : Google Scholar | |
Bandyopadhyay D, Banerjee U, Hajra A, Chakraborty S, Amgai B, Ghosh RK, Haddadin FI, Modi VA, Sinha K, Aronow WS, et al: Trends of Cardiac Complications in Patients With Rheumatoid Arthritis: Analysis of the United States National Inpatient Sample; 2005-2014. Curr Probl Cardiol. 46(100455)2021.PubMed/NCBI View Article : Google Scholar | |
Zulfiqar AA, Niazi R, Pennaforte JL and Andres E: Rheumatoid arthritis and cardiovascular risk factor: Literature review. Rev Med Liege. 73:634–639. 2018.PubMed/NCBI(In French). | |
Atzeni F, Talotta R, Masala IF, Gerardi MC, Casale R and Sarzi-Puttini P: Central nervous system involvement in rheumatoid arthritis patients and the potential implications of using biological agents. Best Pract Res Clin Rheumatol. 32:500–510. 2018.PubMed/NCBI View Article : Google Scholar | |
Nakao E, Mitsunaga A, Hamano T, Shirato M, Shirato I and Nishino T: Case report of rheumatoid arthritis associated with type A gastritis and Hashimoto thyroiditis. Nihon Shokakibyo Gakkai Zasshi. 107:1927–1932. 2010.PubMed/NCBI(In Japanese). | |
Lora V, Cerroni L and Cota C: Skin manifestations of rheumatoid arthritis. G Ital Dermatol Venereol. 153:243–255. 2018.PubMed/NCBI View Article : Google Scholar | |
Kurmann RD and Mankad R: Atherosclerotic Heart Disease in Women With Autoimmune Rheumatologic Inflammatory Conditions. Can J Cardiol. 34:381–389. 2018.PubMed/NCBI View Article : Google Scholar | |
Favalli EG, Biggioggero M, Crotti C, Becciolini A, Raimondo MG and Meroni PL: Sex and Management of Rheumatoid Arthritis. Clin Rev Allergy Immunol. 56:333–345. 2019.PubMed/NCBI View Article : Google Scholar | |
Law ST and Taylor PC: Role of biological agents in treatment of rheumatoid arthritis. Pharmacol Res. 150(104497)2019.PubMed/NCBI View Article : Google Scholar | |
Bolon B, Stolina M, King C, Middleton S, Gasser J, Zack D and Feige U: Rodent preclinical models for developing novel antiarthritic molecules: Comparative biology and preferred methods for evaluating efficacy. J Biomed Biotechnol. 2011(569068)2011.PubMed/NCBI View Article : Google Scholar | |
Hirose J and Tanaka S: Animal models for bone and joint disease. CIA, CAIA model. Clin Calcium. 21:253–259. 2011.PubMed/NCBI(In Japanese). | |
Hanyecz A, Olasz K, Tarjanyi O, Nemeth P, Mikecz K, Glant TT and Boldizsar F: Proteoglycan aggrecan conducting T cell activation and apoptosis in a murine model of rheumatoid arthritis. BioMed Res Int. 2014(942148)2014.PubMed/NCBI View Article : Google Scholar | |
Corrado A, Donato P, Maccari S, Cecchi R, Spadafina T, Arcidiacono L, Tavarini S, Sammicheli C, Laera D, Manetti AG, et al: Staphylococcus aureus-dependent septic arthritis in murine knee joints: Local immune response and beneficial effects of vaccination. Sci Rep. 6(38043)2016.PubMed/NCBI View Article : Google Scholar | |
Choudhary N, Bhatt LK and Prabhavalkar KS: Experimental animal models for rheumatoid arthritis. Immunopharmacol Immunotoxicol. 40:193–200. 2018.PubMed/NCBI View Article : Google Scholar | |
Christensen AD, Haase C, Cook AD and Hamilton JA: K/BxN Serum-Transfer Arthritis as a Model for Human Inflammatory Arthritis. Front Immunol. 7(213)2016.PubMed/NCBI View Article : Google Scholar | |
Sønderstrup G: Development of humanized mice as a model of inflammatory arthritis. Springer Semin Immunopathol. 25:35–45. 2003.PubMed/NCBI View Article : Google Scholar | |
Nakano K, Yamaoka K, Hanami K, Saito K, Sasaguri Y, Yanagihara N, Tanaka S, Katsuki I, Matsushita S and Tanaka Y: Dopamine induces IL-6-dependent IL-17 production via D1-like receptor on CD4 naive T cells and D1-like receptor antagonist SCH-23390 inhibits cartilage destruction in a human rheumatoid arthritis/SCID mouse chimera model. J Immunol. 186:3745–3752. 2011.PubMed/NCBI View Article : Google Scholar | |
Liu S, Hasegawa H, Takemasa E, Suzuki Y, Oka K, Kiyoi T, Takeda H, Ogasawara T, Sawasaki T, Yasukawa M, et al: Efficiency and Safety of CRAC Inhibitors in Human Rheumatoid Arthritis Xenograft Models. J Immunol. 199:1584–1595. 2017.PubMed/NCBI View Article : Google Scholar | |
Williams RO: Collagen-induced arthritis in mice. Methods Mol Med. 136:191–199. 2007.PubMed/NCBI View Article : Google Scholar | |
Caplazi P, Baca M, Barck K, Carano RA, DeVoss J, Lee WP, Bolon B and Diehl L: Mouse Models of Rheumatoid Arthritis. Vet Pathol. 52:819–826. 2015.PubMed/NCBI View Article : Google Scholar | |
Cho YG, Cho ML, Min SY and Kim HY: Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun Rev. 7:65–70. 2007.PubMed/NCBI View Article : Google Scholar | |
Schurgers E, Billiau A and Matthys P: Collagen-induced arthritis as an animal model for rheumatoid arthritis: Focus on interferon-γ. J Interferon Cytokine Res. 31:917–926. 2011.PubMed/NCBI View Article : Google Scholar | |
Trentham DE, Townes AS and Kang AH: Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med. 146:857–868. 1977.PubMed/NCBI View Article : Google Scholar | |
Cathcart ES, Hayes KC, Gonnerman WA, Lazzari AA and Franzblau C: Experimental arthritis in a nonhuman primate. I. Induction by bovine type II collagen. Lab Invest. 54:26–31. 1986.PubMed/NCBI | |
Courtenay JS, Dallman MJ, dayan AD, Martin A and Mosedale B: Immunisation against heterologous type II collagen induces arthritis in mice. Nature. 283:666–668. 1980.PubMed/NCBI View Article : Google Scholar | |
Nandakumar KS: Pathogenic antibody recognition of cartilage. Cell Tissue Res. 339:213–220. 2010.PubMed/NCBI View Article : Google Scholar | |
Wooley PH, Luthra HS, Stuart JM and David CS: Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J Exp Med. 154:688–700. 1981.PubMed/NCBI View Article : Google Scholar | |
Tarkowski A, Holmdahl R and Klareskog L: Rheumatoid factors in mice. Monogr Allergy. 26:214–229. 1989.PubMed/NCBI | |
Benson RA, McInnes IB, Garside P and Brewer JM: Model answers: Rational application of murine models in arthritis research. Eur J Immunol. 48:32–38. 2018.PubMed/NCBI View Article : Google Scholar | |
Myers LK, Tang B, Rosloniec EF, Stuart JM, Chiang TM and Kang AH: Characterization of a peptide analog of a determinant of type II collagen that suppresses collagen-induced arthritis. J Immunol. 161:3589–3595. 1998.PubMed/NCBI | |
Brand DD, Kang AH and Rosloniec EF: Immunopathogenesis of collagen arthritis. Springer Semin Immunopathol. 25:3–18. 2003.PubMed/NCBI View Article : Google Scholar | |
Inglis JJ, Simelyte E, McCann FE, Criado G and Williams RO: Protocol for the induction of arthritis in C57BL/6 mice. Nat Protoc. 3:612–618. 2008.PubMed/NCBI View Article : Google Scholar | |
Stuart JM, Townes AS and Kang AH: Collagen autoimmune arthritis. Annu Rev Immunol. 2:199–218. 1984.PubMed/NCBI View Article : Google Scholar | |
Joe B and Wilder RL: Animal models of rheumatoid arthritis. Mol Med Today. 5:367–369. 1999.PubMed/NCBI View Article : Google Scholar | |
Kannan K, Ortmann RA and Kimpel D: Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology. 12:167–181. 2005.PubMed/NCBI View Article : Google Scholar | |
Hegen M, Keith JC Jr, Collins M and Nickerson-Nutter CL: Utility of animal models for identification of potential therapeutics for rheumatoid arthritis. Ann Rheum Dis. 67:1505–1515. 2008.PubMed/NCBI View Article : Google Scholar | |
Petersen F and Yu X: A novel preclinical model for rheumatoid arthritis research. Arthritis Res Ther. 12(148)2010.PubMed/NCBI View Article : Google Scholar | |
Brand DD, Latham KA and Rosloniec EF: Collagen-induced arthritis. Nat Protoc. 2:1269–1275. 2007.PubMed/NCBI View Article : Google Scholar | |
Huang JC, Vestberg M, Minguela A, Holmdahl R and Ward ES: Analysis of autoreactive T cells associated with murine collagen-induced arthritis using peptide-MHC multimers. Int Immunol. 16:283–293. 2004.PubMed/NCBI View Article : Google Scholar | |
Buglak NE and Bahnson ESM: A Rat Carotid Artery Pressure-Controlled Segmental Balloon Injury with Periadventitial Therapeutic Application. J Vis Exp 161: 10.3791/60473, 2020. | |
Holmdahl R, Jansson L, Larsson E, Rubin K and Klareskog L: Homologous type II collagen induces chronic and progressive arthritis in mice. Arthritis Rheum. 29:106–113. 1986.PubMed/NCBI View Article : Google Scholar | |
Boissier MC, Feng XZ, Carlioz A, Roudier R and Fournier C: Experimental autoimmune arthritis in mice. I. Homologous type II collagen is responsible for self-perpetuating chronic polyarthritis. Ann Rheum Dis. 46:691–700. 1987.PubMed/NCBI View Article : Google Scholar | |
Wilder RL: Hormones and autoimmunity: Animal models of arthritis. Baillieres Clin Rheumatol. 10:259–271. 1996.PubMed/NCBI View Article : Google Scholar | |
Vandenbroucke JP, Valkenburg HA, Boersma JW, Cats A, Festen JJ, Huber-Bruning O and Rasker JJ: Oral contraceptives and rheumatoid arthritis: Further evidence for a preventive effect. Lancet. 2:839–842. 1982.PubMed/NCBI View Article : Google Scholar | |
Lee YK, Choi KH, Kwak HS and Chang YH: The preventive effects of nanopowdered red ginseng on collagen-induced arthritic mice. Int J Food Sci Nutr. 69:308–317. 2018.PubMed/NCBI View Article : Google Scholar | |
Holmdahl R, Jansson L, Gullberg D, Rubin K, Forsberg PO and 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. 62:639–646. 1985.PubMed/NCBI | |
Stewart-Tull DE: Freund's complete and incomplete adjuvants, preparation, and quality control standards for experimental laboratory animals use. Methods Mol Biol. 626:59–72. 2010.PubMed/NCBI View Article : Google Scholar | |
Wooley PH, Luthra HS, Griffiths MM, Stuart JM, Huse A and David CS: Type II collagen-induced arthritis in mice. IV. Variations in immunogenetic regulation provide evidence for multiple arthritogenic epitopes on the collagen molecule. J Immunol. 135:2443–2451. 1985.PubMed/NCBI | |
Chen HH, Chen DY, Chao YH, Chen YM, Wu CL, Lai KL, Lin CH and Lin CC: Acarbose Decreases the Rheumatoid Arthritis Risk of Diabetic Patients and Attenuates the Incidence and Severity of Collagen-induced Arthritis in Mice. Sci Rep. 5(18288)2015.PubMed/NCBI View Article : Google Scholar | |
Inglis JJ, Criado G, Medghalchi M, Andrews M, Sandison A, Feldmann M and Williams RO: 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(R113)2007.PubMed/NCBI View Article : Google Scholar | |
Liu L, Yang J, Zu B, Wang J, Sheng K, Zhao L and Xu W: Acacetin regulated the reciprocal differentiation of Th17 cells and Treg cells and mitigated the symptoms of collagen-induced arthritis in mice. Scand J Immunol. 88(e12712)2018.PubMed/NCBI View Article : Google Scholar | |
Deng Y, Luo H, Shu J, Shu H, Lu C, Zhao N, Geng Y, He X and Lu A: Pien Tze Huang alleviate the joint inflammation in collagen-induced arthritis mice. Chin Med. 15(30)2020.PubMed/NCBI View Article : Google Scholar | |
Luan J, Zhang K, Yang P, Zhang Y, Feng F, Zhu YM, Zhu P and Chen ZN: The combination of FK506 and an anti-CD147 mAb exerts potential therapeutic effects on a mouse model of collagen-induced arthritis. Mol Immunol. 101:1–9. 2018.PubMed/NCBI View Article : Google Scholar | |
Fu J, Zhang L, Song S, Sheng K, Li Y, Li P, Song S, Wang Q, Chu J and Wei W: Effect of bone marrow-derived CD11b(+)F4/80 (+) immature dendritic cells on the balance between pro-inflammatory and anti-inflammatory cytokines in DBA/1 mice with collagen-induced arthritis. Inflamm Res. 63:357–367. 2014.PubMed/NCBI View Article : Google Scholar | |
Zhou X, Zhao X, Tang L, Zhang Y, Ruan H, Pi H, Qiu J and Wu J: Immunomodulatory activity of the rhizomes of Impatiens pritzellii var. hupehensis on collagen-induced arthritis mice. J Ethnopharmacol. 109:505–509. 2007.PubMed/NCBI View Article : Google Scholar | |
Wang Z, Zhuo F, Chu P, Yang X and Zhao G: Germacrone alleviates collagen-induced arthritis via regulating Th1/Th2 balance and NF-κB activation. Biochem Biophys Res Commun. 518:560–564. 2019.PubMed/NCBI View Article : Google Scholar | |
Jia Q, Wang T, Wang X, Xu H, Liu Y, Wang Y, Shi Q and Liang Q: Astragalin Suppresses Inflammatory Responses and Bone Destruction in Mice With Collagen-Induced Arthritis and in Human Fibroblast-Like Synoviocytes. Front Pharmacol. 10(94)2019.PubMed/NCBI View Article : Google Scholar | |
Svetlicky N, Kivity S, Odeh Q, Shovman O, Gertel S, Amital H, Gendelman O, Volkov A, Barshack I, Bar-Meir E, et al: Anti-citrullinated-protein-antibody-specific intravenous immunoglobulin attenuates collagen-induced arthritis in mice. Clin Exp Immunol. 182:241–250. 2015.PubMed/NCBI View Article : Google Scholar | |
Yang P, Qian F, Zhang M, Xu AL, Wang X, Jiang B, Zhou L and Zhou X: Zishen Tongluo formula ameliorates collagen-induced arthritis in mice by modulation of Th17/Treg balance. J Ethnopharmacol. 250(112428)2020.PubMed/NCBI View Article : Google Scholar | |
Feng ZT, Yang T, Hou XQ, Wu HY, Feng JT, Ou BJ, Cai SJ, Li J and Mei ZG: Sinomenine mitigates collagen-induced arthritis mice by inhibiting angiogenesis. Biomed Pharmacother. 113(108759)2019.PubMed/NCBI View Article : Google Scholar | |
Fan J, Luo J, Yan C, Hao R, Zhao X, Jia R, He J, Xu D, Miao M and Li X: Methotrexate, combined with cyclophosphamide attenuates murine collagen induced arthritis by modulating the expression level of Breg and DCs. Mol Immunol. 90:106–117. 2017.PubMed/NCBI View Article : Google Scholar | |
Wu S, Li Y, Li Y, Yao L, Lin T, Jiang S, Shen H, Xia L and Lu J: Interleukin-35 attenuates collagen-induced arthritis through suppression of vascular endothelial growth factor and its receptors. Int Immunopharmacol. 34:71–77. 2016.PubMed/NCBI View Article : Google Scholar | |
Gui H, Liu X, Liu LR, Su DF and Dai SM: Activation of cannabinoid receptor 2 attenuates synovitis and joint distruction in collagen-induced arthritis. Immunobiology. 220:817–822. 2015.PubMed/NCBI View Article : Google Scholar | |
Xuzhu G, Komai-Koma M, Leung BP, Howe HS, McSharry C, McInnes IB and Xu D: Resveratrol modulates murine collagen-induced arthritis by inhibiting Th17 and B-cell function. Ann Rheum Dis. 71:129–135. 2012.PubMed/NCBI View Article : Google Scholar | |
Guo Y, Xing E, Song H, Feng G, Liang X, An G, Zhao X and Wang M: Therapeutic effect of dioscin on collagen-induced arthritis through reduction of Th1/Th2. Int Immunopharmacol. 39:79–83. 2016.PubMed/NCBI View Article : Google Scholar | |
Suszko A and Obmińska-Mrukowicz B: Influence of polysaccharide fractions isolated from Caltha palustris L. on the cellular immune response in collagen-induced arthritis (CIA) in mice. A comparison with methotrexate. J Ethnopharmacol. 145:109–117. 2013.PubMed/NCBI View Article : Google Scholar | |
Bessis N, Decker P, Assier E, Semerano L and Boissier MC: Arthritis models: Usefulness and interpretation. Semin Immunopathol. 39:469–486. 2017.PubMed/NCBI View Article : Google Scholar | |
Zhong C, Wang J, Li B, Xiang H, Ultsch M, Coons M, Wong T, Chiang NY, Clark S, Clark R, et al: Development and preclinical characterization of a humanized antibody targeting CXCL12. Clin Cancer Res. 19:4433–4445. 2013.PubMed/NCBI View Article : Google Scholar | |
Huang X, He Y, Han J, Zhuang J, He J and Sun E: Not only anti-inflammation, etanercept abrogates collagen-induced arthritis by inhibiting dendritic cell migration and maturation. Cent Eur J Immunol. 44:237–245. 2019.PubMed/NCBI View Article : Google Scholar | |
Alabarse PVG, Lora PS, Silva JMS, Santo RCE, Freitas EC, de Oliveira MS, Almeida AS, Immig M, Teixeira VON, Filippin LI, et al: Collagen-induced arthritis as an animal model of rheumatoid cachexia. J Cachexia Sarcopenia Muscle. 9:603–612. 2018.PubMed/NCBI View Article : Google Scholar | |
Evans WJ, Morley JE, Argilés J, Bales C, Baracos V, Guttridge D, Jatoi A, Kalantar-Zadeh K, Lochs H, Mantovani G, et al: Cachexia: A new definition. Clin Nutr. 27:793–799. 2008.PubMed/NCBI View Article : Google Scholar | |
Vincent TL, Williams RO, Maciewicz R, Silman A and Garside P: Arthritis Research UK animal models working group. Mapping pathogenesis of arthritis through small animal models. Rheumatology (Oxford). 51:1931–1941. 2012.PubMed/NCBI View Article : Google Scholar | |
Marazziti D, Ambrogi F, Abelli M, Di Nasso E, Catena M, Massimetti G, Carlini M and Dell'Osso L: Lymphocyte subsets, cardiovascular measures and anxiety state before and after a professional examination. Stress. 10:93–99. 2007.PubMed/NCBI View Article : Google Scholar | |
Melkus MW, Estes JD, Padgett-Thomas A, Gatlin J, Denton PW, Othieno FA, Wege AK, Haase AT and Garcia JV: Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat Med. 12:1316–1322. 2006.PubMed/NCBI View Article : Google Scholar | |
Akkina R: Humanized Mice for Studying Human Immune Responses and Generating Human Monoclonal Antibodies. Microbiol Spectr. 2:2014.PubMed/NCBI View Article : Google Scholar | |
Vatakis DN, Bristol GC, Kim SG, Levin B, Liu W, Radu CG, Kitchen SG and Zack JA: Using the BLT humanized mouse as a stem cell based gene therapy tumor model. J Vis Exp. 70(e4181)2012.PubMed/NCBI View Article : Google Scholar |