Characterization of a novel and spontaneous mouse model of inflammatory arthritis

Arthritis Research and Therapy

Volumn 13, Issue 4, 2011, Pages

  Adipue, Iris A ^a   Wilcox, Joel T ^a   King, Cody ^a   Rice, Carolyn A Y ^a   Shaum, Katherine M ^a   Suard, Cory M ^a   Brink, Elri T ^a   Miller, Stephen D ^b   McMahon, Eileen J ^a  

^a WESTMONT COLLEGE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 2; CYTOKINE; IMMUNOGLOBULIN G1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRITIS; ARTICLE; BONE EROSION; CARTILAGE; CD3+ T LYMPHOCYTE; CD4 CD8 RATIO; CELL COMPARTMENTALIZATION; CELL INFILTRATION; CLINICAL EXAMINATION; CONTROLLED STUDY; DATA ANALYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC ANALYSIS; HISTOPATHOLOGIC SKIN REACTION; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL PARAMETERS; INHERITANCE; LYMPHOID ORGAN; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PROTEIN BLOOD LEVEL; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; ANIMAL; CELL SEPARATION; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CELL SEPARATION; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC;

EID: 79960164282     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3399     Document Type: Article

References (77)

1. Grassi W, De Angelis R, Lamanna G, Cervini C. The clinical features of rheumatoid arthritis. Eur J Radiol 1998, 27(Suppl 1):S18-S24.
2. Turesson C, O'Fallon WM, Crowson CS, Gabriel SE, Matteson EL. Extra-articular disease manifestations in rheumatoid arthritis: incidence trends and risk factors over 46 years. Ann Rheum Dis 2003, 62:722-727. 10.1136/ard.62.8.722, 1754626, 12860726.
3. Young A, Koduri G. Extra-articular manifestations and complications of rheumatoid arthritis. Best Pract Res Clin Rheumatol 2007, 21:907-927. 10.1016/j.berh.2007.05.007, 17870035.
4. Sangha O. Epidemiology of rheumatic diseases. Rheumatology (Oxford) 2000, 39(Suppl 2):3-12.
5. Woolf AD, Pfleger B. Burden of major musculoskeletal conditions. Bull World Health Organ 2003, 81:646-656. 2572542, 14710506.
6. Helmick CG, Felson DT, Lawrence RC, Gabriel S, Hirsch R, Kwoh CK, Liang MH, Kremers HM, Mayes MD, Merkel PA, Pillemer SR, Reveille JD, Stone JH, . National Arthritis Data Workgroup Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part I. Arthritis Rheum 2008, 58:15-25. 10.1002/art.23177, 18163481, National Arthritis Data Workgroup.
7. Manners PJ, Bower C. Worldwide prevalence of juvenile arthritis: why does it vary so much?. J Rheumatol 2002, 29:1520-1530.
8. Alamanos Y, Drosos AA. Epidemiology of adult rheumatoid arthritis. Autoimmun Rev 2005, 4:130-136. 10.1016/j.autrev.2004.09.002, 15823498.
9. Sokka T, Kautiainen H, Pincus T, Verstappen SM, Aggarwal A, Alten R, Andersone D, Badsha H, Baecklund E, Belmonte M, Craig-Müller J, da Mota LM, Dimic A, Fathi NA, Ferraccioli G, Fukuda W, Géher P, Gogus F, Hajjaj-Hassouni N, Hamoud H, Haugeberg G, Henrohn D, Horslev-Petersen K, Ionescu R, Karateew D, Kuuse R, Laurindo IM, Lazovskis J, et al. Work disability remains a major problem in rheumatoid arthritis in the 2000s: data from 32 countries in the QUEST-RA study. Arthritis Res Ther 2010, 12:R42. 2888189, 20226018.
10. Nandakumar KS, Holmdahl R. Antibody-induced arthritis: disease mechanisms and genes involved at the effector phase of arthritis. Arthritis Res Ther 2006, 8:223. 10.1186/ar2089, 1794524, 17254316.
11. Goronzy JJ, Weyand CM. Developments in the scientific understanding of rheumatoid arthritis. Arthritis Res Ther 2009, 11:249. 10.1186/ar2758, 2787299, 19835638.
12. van Vollenhoven RF. Treatment of rheumatoid arthritis: state of the art 2009. Nat Rev Rheumatol 2009, 5:531-541. 10.1038/nrrheum.2009.182, 19798027.
13. Edwards JC, Cambridge G. B-cell targeting in rheumatoid arthritis and other autoimmune diseases. Nat Rev Immunol 2006, 6:394-403. 10.1038/nri1838, 16622478.
14. Firestein GS. The T cell cometh: interplay between adaptive immunity and cytokine networks in rheumatoid arthritis. J Clin Invest 2004, 114:471-474. 503778, 15314683.
15. Skapenko A, Leipe J, Lipsky PE, Schulze-Koops H. The role of the T cell in autoimmune inflammation. Arthritis Res Ther 2005, 7(Suppl 2):S4-S14. 10.1186/ar1703, 2833981, 15833146.
16. Gutcher I, Becher B. APC-derived cytokines and T cell polarization in autoimmune inflammation. J Clin Invest 2007, 117:1119-1127. 10.1172/JCI31720, 1857272, 17476341.
17. Nistala K, Wedderburn LR. Th17 and regulatory T cells: rebalancing pro- and anti-inflammatory forces in autoimmune arthritis. Rheumatology (Oxford) 2009, 48:602-606.
18. Imboden JB. The immunopathogenesis of rheumatoid arthritis. Annu Rev Pathol 2009, 4:417-434. 10.1146/annurev.pathol.4.110807.092254, 18954286.
19. Toh ML, Miossec P. The role of T cells in rheumatoid arthritis: new subsets and new targets. Curr Opin Rheumatol 2007, 19:284-288. 10.1097/BOR.0b013e32805e87e0, 17414957.
20. Kunz M, Ibrahim SM. Cytokines and cytokine profiles in human autoimmune diseases and animal models of autoimmunity. Mediators Inflamm 2009, 2009:979258. 2768824, 19884985.
21. Brennan FM, McInnes IB. Evidence that cytokines play a role in rheumatoid arthritis. J Clin Invest 2008, 118:3537-3545. 10.1172/JCI36389, 2575731, 18982160.
22. Fonseca JE, Santos MJ, Canhao H, Choy E. Interleukin-6 as a key player in systemic inflammation and joint destruction. Autoimmun Rev 2009, 8:538-542. 10.1016/j.autrev.2009.01.012, 19189867.
23. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu Rev Immunol 2009, 27:485-517. 10.1146/annurev.immunol.021908.132710, 19132915.
24. Manel N, Unutmaz D, Littman DR. The differentiation of human TH-17 cells requires transforming growth factor-β and induction of the nuclear receptor RORγt. Nat Immunol 2008, 9:641-649. 10.1038/ni.1610, 2597394, 18454151.
25. Di Paola R, Cuzzocrea S. Predictivity and sensitivity of animal models of arthritis. Autoimmun Rev 2008, 8:73-75. 10.1016/j.autrev.2008.07.029, 18708167.
26. Asquith DL, Miller AM, McInnes IB, Liew FY. Animal models of rheumatoid arthritis. Eur J Immunol 2009, 39:2040-2044. 10.1002/eji.200939578, 19672892.
27. Ahlqvist E, Hultqvist M, Holmdahl R. The value of animal models in predicting genetic susceptibility to complex diseases such as rheumatoid arthritis. Arthritis Res Ther 2009, 11:226. 10.1186/ar2600, 2714094, 19490601.
28. Holmdahl R, Bockermann R, Backlund J, Yamada H. The molecular pathogenesis of collagen-induced arthritis in mice: a model for rheumatoid arthritis. Ageing Res Rev 2002, 1:135-147. 10.1016/S0047-6374(01)00371-2, 12039453.
29. Glant TT, Finnegan A, Mikecz K. Proteoglycan-induced arthritis: immune regulation, cellular mechanisms, and genetics. Crit Rev Immunol 2003, 23:199-250. 10.1615/CritRevImmunol.v23.i3.20, 14584879.
30. Hang L, Theofilopoulos AN, Dixon FJ. A spontaneous rheumatoid arthritis-like disease in MRL/l mice. J Exp Med 1982, 155:1690-1701. 10.1084/jem.155.6.1690, 2186697, 7077223.
31. Kamogawa J, Terada M, Mizuki S, Nishihara M, Yamamoto H, Mori S, Abe Y, Morimoto K, Nakatsuru S, Nakamura Y, Nose M. Arthritis in MRL/lpr mice is under the control of multiple gene loci with an allelic combination derived from the original inbred strains. Arthritis Rheum 2002, 46:1067-1074. 10.1002/art.10193, 11953986.
32. Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell 1996, 87:811-822. 10.1016/S0092-8674(00)81989-3, 8945509.
33. Keffer J, Probert L, Cazlaris H, Georgopoulos S, Kaslaris E, Kioussis D, Kollias G. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J 1991, 10:4025-4031. 453150, 1721867.
34. Horai R, Saijo S, Tanioka H, Nakae S, Sudo K, Okahara A, Ikuse T, Asano M, Iwakura Y. Development of chronic inflammatory arthropathy resembling rheumatoid arthritis in interleukin 1 receptor antagonist-deficient mice. J Exp Med 2000, 191:313-320. 10.1084/jem.191.2.313, 2195765, 10637275.
35. Atsumi T, Ishihara K, Kamimura D, Ikushima H, Ohtani T, Hirota S, Kobayashi H, Park SJ, Saeki Y, Kitamura Y, Hirano T. A point mutation of Tyr-759 in interleukin 6 family cytokine receptor subunit gp130 causes autoimmune arthritis. J Exp Med 2002, 196:979-990. 10.1084/jem.20020619, 2194024, 12370259.
36. Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, Sakihama T, Matsutani T, Negishi I, Nakatsuru S, Sakaguchi S. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 2003, 426:454-460. 10.1038/nature02119, 14647385.
37. Waldner H, Whitters MJ, Sobel RA, Collins M, Kuchroo VK. Fulminant spontaneous autoimmunity of the central nervous system in mice transgenic for the myelin proteolipid protein-specific T cell receptor. Proc Natl Acad Sci USA 2000, 97:3412-3417. 10.1073/pnas.97.7.3412, 16253, 10737797.
38. Sawa S, Kamimura D, Jin GH, Morikawa H, Kamon H, Nishihara M, Ishihara K, Murakami M, Hirano T. Autoimmune arthritis associated with mutated interleukin (IL)-6 receptor gp130 is driven by STAT3/IL-7-dependent homeostatic proliferation of CD4+ T cells. J Exp Med 2006, 203:1459-1470. 10.1084/jem.20052187, 2118324, 16717113.
39. Kaplan CD, O'Neill SK, Koreny T, Czipri M, Finnegan A. Development of inflammation in proteoglycan-induced arthritis is dependent on FcγR regulation of the cytokine/chemokine environment. J Immunol 2002, 169:5851-5859.
40. Tompkins SM, Padilla J, Dal Canto MC, Ting JP, Van Kaer L, Miller SD. De novo central nervous system processing of myelin antigen is required for the initiation of experimental autoimmune encephalomyelitis. J Immunol 2002, 168:4173-4183.
41. McMahon EJ, Bailey SL, Castenada CV, Waldner H, Miller SD. Epitope spreading initiates in the CNS in two mouse models of multiple sclerosis. Nat Med 2005, 11:335-339. 10.1038/nm1202, 15735651.
42. De Vos M. Joint involvement associated with inflammatory bowel disease. Dig Dis 2009, 27:511-515. 10.1159/000233290, 19897967.
43. Hazenberg MP, Klasen IS, Kool J, Ruseler-van Embden JG, Severijnen AJ. Are intestinal bacteria involved in the etiology of rheumatoid arthritis? Review article. APMIS 1992, 100:1-9. 10.1111/j.1699-0463.1992.tb00833.x, 1536716.
44. Shen Z, Fox JG, Dewhirst FE, Paster BJ, Foltz CJ, Yan L, Shames B, Perry L. Helicobacter rodentium sp. nov., a urease-negative Helicobacter species isolated from laboratory mice. Int J Syst Bacteriol 1997, 47:627-634. 10.1099/00207713-47-3-627, 9226892.
45. Chichlowski M, Sharp JM, Vanderford DA, Myles MH, Hale LP. Helicobacter typhlonius and Helicobacter rodentium differentially affect the severity of colon inflammation and inflammation-associated neoplasia in IL10-deficient mice. Comp Med 2008, 58:534-541. 2710754, 19149410.
46. Myles MH, Livingston RS, Franklin CL. Pathogenicity of Helicobacter rodentium in A/JCr and SCID mice. Comp Med 2004, 54:549-557.
47. Shomer NH, Dangler CA, Marini RP, Fox JG. Helicobacter bilis/Helicobacter rodentium co-infection associated with diarrhea in a colony of scid mice. Lab Anim Sci 1998, 48:455-459.
48. Edwards SW, Hallett MB. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol Today 1997, 18:320-324. 10.1016/S0167-5699(97)01087-6, 9238834.
49. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003, 423:356-361. 10.1038/nature01661, 12748655.
50. Ishigame H, Nakajima A, Saijo S, Komiyama Y, Nambu A, Matsuki T, Nakae S, Horai R, Kakuta S, Iwakura Y. The role of TNFα and IL-17 in the development of excess IL-1 signaling-induced inflammatory diseases in IL-1 receptor antagonist-deficient mice. Ernst Schering Res Found Workshop 2006, 56:129-153.
51. Gottenberg JE, Miceli-Richard C, Ducot B, Goupille P, Combe B, Mariette X. Markers of B-lymphocyte activation are elevated in patients with early rheumatoid arthritis and correlated with disease activity in the ESPOIR cohort. Arthritis Res Ther 2009, 11:R114. 10.1186/ar2773, 2745796, 19627580.
52. Lleo A, Battezzati PM, Selmi C, Gershwin ME, Podda M. Is autoimmunity a matter of sex?. Autoimmun Rev 2008, 7:626-630. 10.1016/j.autrev.2008.06.009, 18603021.
53. Taneja V, Behrens M, Mangalam A, Griffiths MM, Luthra HS, David CS. New humanized HLA-DR4-transgenic mice that mimic the sex bias of rheumatoid arthritis. Arthritis Rheum 2007, 56:69-78. 10.1002/art.22213, 17195209.
54. Behrens M, Trejo T, Luthra H, Griffiths M, David CS, Taneja V. Mechanism by which HLA-DR4 regulates sex-bias of arthritis in humanized mice. J Autoimmun 2010, 35:1-9. 10.1016/j.jaut.2009.12.007, 20061120.
55. Abe K, Fuchs H, Lisse T, Hans W, Hrabé de Angelis M. New ENU-induced semidominant mutation, Ali18, causes inflammatory arthritis, dermatitis, and osteoporosis in the mouse. Mamm Genome 2006, 17:915-926. 10.1007/s00335-006-0014-x, 16964445.
56. Yu P, Constien R, Dear N, Katan M, Hanke P, Bunney TD, Kunder S, Quintanilla-Martinez L, Huffstadt U, Schröder A, Jones NP, Peters T, Fuchs H, de Angelis MH, Nehls M, Grosse J, Wabnitz P, Meyer TP, Yasuda K, Schiemann M, Schneider-Fresenius C, Jagla W, Russ A, Popp A, Josephs M, Marquardt A, Laufs J, Schmittwolf C, Wagner H, Pfeffer K, Mudde GC. Autoimmunity and inflammation due to a gain-of-function mutation in phospholipase Cγ2 that specifically increases external Ca2+ entry. Immunity 2005, 22:451-465. 10.1016/j.immuni.2005.01.018, 15845450.
57. Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, Degott C, Kikutani H, Rajewsky K, Pasquali JL, Benoist C, Mathis D. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity 1999, 10:451-461. 10.1016/S1074-7613(00)80045-X, 10229188.
58. Crispin JC, Liossis SN, Kis-Toth K, Lieberman LA, Kyttaris VC, Juang YT, Tsokos GC. Pathogenesis of human systemic lupus erythematosus: recent advances. Trends Mol Med 2010, 16:47-57. 10.1016/j.molmed.2009.12.005, 2823952, 20138006.
59. Zhou T, Bluethmann H, Eldridge J, Berry K, Mountz JD. Origin of CD4-CD8-B220+ T cells in MRL-lpr/lpr mice: clues from a T cell receptor β transgenic mouse. J Immunol 1993, 150:3651-3667.
60. Lindwasser OW, Chaudhuri R, Bonifacino JS. Mechanisms of CD4 downregulation by the Nef and Vpu proteins of primate immunodeficiency viruses. Curr Mol Med 2007, 7:171-184. 10.2174/156652407780059177, 17346169.
61. Schonrich G, Kalinke U, Momburg F, Malissen M, Schmitt-Verhulst AM, Malissen B, Hammerling GJ, Arnold B. Down-regulation of T cell receptors on self-reactive T cells as a novel mechanism for extrathymic tolerance induction. Cell 1991, 65:293-304. 10.1016/0092-8674(91)90163-S, 1849799.
62. Zhang L, Fung-Leung W, Miller RG. Down-regulation of CD8 on mature antigen-reactive T cells as a mechanism of peripheral tolerance. J Immunol 1995, 155:3464-3471.
63. Nicholson LB, Anderson AC, Kuchroo VK. Tuning T cell activation threshold and effector function with cross-reactive peptide ligands. Int Immunol 2000, 12:205-213. 10.1093/intimm/12.2.205, 10653856.
64. Illes Z, Waldner H, Reddy J, Anderson AC, Sobel RA, Kuchroo VK. Modulation of CD4 co-receptor limits spontaneous autoimmunity when high-affinity transgenic TCR specific for self-antigen is expressed on a genetically resistant background. Int Immunol 2007, 19:1235-1248. 10.1093/intimm/dxm094, 17804690.
65. Thomson CW, Lee BP, Zhang L. Double-negative regulatory T cells: non-conventional regulators. Immunol Res 2006, 35:163-178. 10.1385/IR:35:1:163, 17003518.
66. Voelkl S, Gary R, Mackensen A. Characterization of the immunoregulatory function of human TCR-αβ+ CD4-CD8- double-negative T cells. Eur J Immunol 2011, 41:739-748. 10.1002/eji.201040982, 21287552.
67. Hamad AR, Mohamood AS, Trujillo CJ, Huang CT, Yuan E, Schneck JP. B220+ double-negative T cells suppress polyclonal T cell activation by a Fas-independent mechanism that involves inhibition of IL-2 production. J Immunol 2003, 171:2421-2426.
68. Yoshitomi H, Sakaguchi N, Kobayashi K, Brown GD, Tagami T, Sakihama T, Hirota K, Tanaka S, Nomura T, Miki I, Gordon S, Akira S, Nakamura T, Sakaguchi S. A role for fungal β-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005, 201:949-960. 10.1084/jem.20041758, 2213107, 15781585.
69. Fernando MM, Stevens CR, Walsh EC, De Jager PL, Goyette P, Plenge RM, Vyse TJ, Rioux JD. Defining the role of the MHC in autoimmunity: a review and pooled analysis. PLoS Genet 2008, 4:e1000024. 10.1371/journal.pgen.1000024, 2291482, 18437207.
70. Festen EA, Goyette P, Scott R, Annese V, Zhernakova A, Lian J, Lefebvre C, Brant SR, Cho JH, Silverberg MS, Taylor KD, de Jong DJ, Stokkers PC, McGovern D, Palmieri O, Achkar JP, Xavier RJ, Daly MJ, Duerr RH, Wijmenga C, Weersma RK, Rioux JD. Genetic variants in the region harbouring IL2/IL21 associated with ulcerative colitis. Gut 2009, 58:799-804. 10.1136/gut.2008.166918, 2757103, 19201773.
71. Kochi Y, Okada Y, Suzuki A, Ikari K, Terao C, Takahashi A, Yamazaki K, Hosono N, Myouzen K, Tsunoda T, Kamatani N, Furuichi T, Ikegawa S, Ohmura K, Mimori T, Matsuda F, Iwamoto T, Momohara S, Yamanaka H, Yamada R, Kubo M, Nakamura Y, Yamamoto K. A regulatory variant in CCR6 is associated with rheumatoid arthritis susceptibility. Nat Genet 2010, 42:515-519. 10.1038/ng.583, 20453841.
72. Lettre G, Rioux JD. Autoimmune diseases: insights from genome-wide association studies. Hum Mol Genet 2008, 17:R116-R121. 10.1093/hmg/ddn246, 2782355, 18852199.
73. Asada Y, Isomoto H, Shikuwa S, Wen CY, Fukuda E, Miyazato M, Okamoto K, Nakamura T, Nishiyama H, Mizuta Y, Migita K, Ito M, Kohno S. Development of ulcerative colitis during the course of rheumatoid arthritis: association with selective IgA deficiency. World J Gastroenterol 2006, 12:5240-5243.
74. Georgiadis AN, Tzambouras N, Ioachim E, Tsianos EV, Agnantis N, Drosos AA. Seropositive rheumatoid arthritis associated with Crohn's disease. Clin Exp Rheumatol 2003, 21:363-365.
75. Davis JC, Mease PJ. Insights into the pathology and treatment of spondyloarthritis: from the bench to the clinic. Semin Arthritis Rheum 2008, 38:83-100. 10.1016/j.semarthrit.2007.10.007, 18166219.
76. Papamichael K, Tsirogianni A, Papasteriades C, Mantzaris GJ. Low prevalence of antibodies to cyclic citrullinated peptide in patients with inflammatory bowel disease regardless of the presence of arthritis. Eur J Gastroenterol Hepatol 2010, 22:705-709.
77. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, Medsger TA, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988, 31:315-324. 10.1002/art.1780310302, 3358796.