K/BxN serum-transfer arthritis as a model for human inflammatory arthritis

Frontiers in Immunology

Volumn 7, Issue JUN, 2016, Pages

  Christensen, Anne D ^a,b   Haase, Claus ^b   Cook, Andrew D ^a   Hamilton, John A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b NOVO NORDISK A S   (Denmark)

Author keywords

Animal model; Autoantibodies; Immune complex driven arthritis; K BxN serum transfer arthritis model; Rheumatoid arthritis

Indexed keywords

AUTOANTIBODY; CHEMOKINE; COMPLEMENT FACTOR; FC RECEPTOR; GLUCOSE 6 PHOSPHATE ISOMERASE; INTEGRIN; TOLL LIKE RECEPTOR;

ANTIGEN ANTIBODY COMPLEX; BONE EROSION; CARTILAGE DEGENERATION; COLLAGEN ANTIBODY-INDUCED ARTHRITIS; DNA FLANKING REGION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; INFLAMMATION; MACROPHAGE; MAST CELL; NATURAL KILLER T CELL; NEUTROPHIL; NONHUMAN; PAIN; REVIEW; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION;

EID: 84977496990     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00213     Document Type: Review

References (142)

1. KouskoffVR, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell (1996) 87(5):811-22. doi:10.1016/S0092-8674(00)81989-3
2. Matsumoto I, Staub A, Benoist C, Mathis D. Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme. Science (1999) 286(5445):1732-5. doi:10.1126/science.286.5445.1732
3. Ditzel HJ. The K/BxN mouse: a model of human inflammatory arthritis. Trends Mol Med (2004) 10(1):40-5. doi:10.1016/j.molmed.2003.11.004
4. Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, et al. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity (1999) 10(4):451-61. doi:10.1016/S1074-7613(00)80045-X
5. Mangialaio S, Ji H, Korganow AS, KouskoffVR, Benoist C, Mathis D. The arthritogenic T cell receptor and its ligand in a model of spontaneous arthritis. Arthritis Rheum (1999) 42(12):2517-23. doi:10.1002/1529-0131(199912)42:12<2517::AID-ANR3>3.0.CO;2-W
6. Ji H, Gauguier D, Ohmura K, Gonzalez A, Duchatelle V, Danoy P, et al. Genetic influences on the end-stage effector phase of arthritis. J Exp Med (2001) 194(3):321-30. doi:10.1084/jem.194.3.321
7. Choi J, Kim ST, Craft J. The pathogenesis of systemic lupus erythematosus-an update. Curr Opin Immunol (2012) 24(6):651-7. doi:10.1016/j.coi.2012.10.004
8. Wright C, Sibani S, Trudgian D, Fischer R, Kessler B, LaBaer J, et al. Detection of multiple autoantibodies in patients with ankylosing spondylitis using nucleic acid programmable protein arrays. Mol Cell Proteomics (2012) 11(2):M9.00384. doi:10.1074/mcp. M9.00384
9. Matsumoto I, Maccioni M, Lee DM, Maurice M, Simmons B, Brenner M, et al. How antibodies to a ubiquitous cytoplasmic enzyme may provoke joint-specific autoimmune disease. Nat Immunol (2002) 3(4):360-5. doi:10.1038/ni772
10. Wipke BT, Wang Z, Kim J, McCarthy TJ, Allen PM. Dynamic visualization of a joint-specific autoimmune response through positron emission tomography. Nat Immunol (2002) 3(4):366-72. doi:10.1038/ni775
11. Maccioni M, Zeder-Lutz G, Huang H, Ebel C, Gerber P, Hergueux J, et al. Arthritogenic monoclonal antibodies from K/BxN mice. J Exp Med (2002) 195(8):1071-7. doi:10.1084/jem.20011941
12. Wipke BT, Wang Z, Nagengast W, Reichert DE, Allen PM. Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J Immunol (2004) 172(12):7694-702. doi:10.4049/jimmunol.172.12.7694
13. Corr M, Crain B. The role of FcyR signaling in the K/BxN serum transfer model of arthritis. J Immunol (2002) 169(11):6604-9. doi:10.4049/jimmunol.169.11.6604
14. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM, Mahmood U, et al. Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol (2006) 7(3):284-92. doi:10.1038/ni1306
15. Nimmerjahn F, Ravetch JV. Fc-receptors as regulators of immunity. Adv Immunol (2007) 96:179-204. doi:10.1016/S0065-2776(07)96005-8
16. Ji H, Ohmura K, Mahmood U, Lee DM, Hofhuis FM, Boackle SA, et al. Arthritis critically dependent on innate immune system players. Immunity (2002) 16(2):157-68. doi:10.1016/S1074-7613(02)00275-3
17. Boross P, van Lent PL, Martin-Ramirez J, van der Kaa J, Mulder MHCM, Claassens JWC, et al. Destructive arthritis in the absence of both FcyRI and FcyRIII. J Immunol (2008) 180(7):5083-91. doi:10.4049/jimmunol.180.7.5083
18. Mancardi DA, Jonsson F, Iannascoli B, Khun H, Van Rooijen N, Huerre M, et al. Cutting edge: the murine high-affinity IgG receptor FcyRIV is sufficient for autoantibody-induced arthritis. J Immunol (2011) 186(4):1899-903. doi:10.4049/jimmunol.1003642
19. Seeling M, HillenhoffU, David JP, Schett G, Tuckermann J, Lux A, et al. Inflammatory monocytes and Fcgamma receptor IV on osteoclasts are critical for bone destruction during inflammatory arthritis in mice. Proc Natl Acad Sci U S A (2013) 110(26):10729-34. doi:10.1073/pnas.1301001110
20. Bruhns P, Samuelsson A, Pollard JW, Ravetch JV. Colony-stimulating factor-1-dependent macrophages are responsible for IVIG protection in antibody-induced autoimmune disease. Immunity (2003) 18(4):573-81. doi:10.1016/S1074-7613(03)00080-3
21. Campbell IK, Miescher S, Branch DR, Mott PJ, Lazarus AH, Han D, et al. Therapeutic effect of IVIG on inflammatory arthritis in mice is dependent on the Fc portion and independent of sialylation or basophils. J Immunol (2014) 192(11):5031-8. doi:10.4049/jimmunol.1301611
22. Fiebiger BM, Maamary J, Pincetic A, Ravetch JV. Protection in antibody-and T cell-mediated autoimmune diseases by antiinflammatory IgG Fcs requires type II FcRs. Proc Natl Acad Sci U S A (2015) 112(18):E2385-94. doi:10.1073/pnas.1505292112
23. Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature (2011) 475(7354):110-3. doi:10.1038/nature10134
24. Samuelsson A, Towers TL, Ravetch JV. Anti-inflammatory activity of IVIG mediated through the inhibitory Fc receptor. Science (2001) 291(5503):484-6. doi:10.1126/science.291.5503.484
25. Wipke BT, Allen PM. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol (2001) 167(3):1601-8. doi:10.4049/jimmunol.167.3.1601
26. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol (2008) 83(1):64-70. doi:10.1189/jlb.0407247
27. Wang JX, Bair AM, King SL, Shnayder R, Huang YF, Shieh CC, et al. Ly6G ligation blocks recruitment of neutrophils via a beta2-integrin-dependent mechanism. Blood (2012) 120(7):1489-98. doi:10.1182/blood-2012-01-404046
28. Monach PA, Nigrovic PA, Chen M, Hock H, Lee DM, Benoist C, et al. Neutrophils in a mouse model of autoantibody-mediated arthritis: critical producers of Fc receptor gamma, the receptor for C5a, and lymphocyte function-associated antigen 1. Arthritis Rheum (2010) 62(3):753-64. doi:10.1002/art.27238
29. Tager AM, Dufour JH, Goodarzi K, Bercury SD, von Andrian UH, Luster AD. BLTR mediates leukotriene B(4)-induced chemotaxis and adhesion and plays a dominant role in eosinophil accumulation in a murine model of peritonitis. J Exp Med (2000) 192(3):439-46. doi:10.1084/jem.192.3.439
30. Haribabu B, Verghese MW, Steeber DA, Sellars DD, Bock CB, Snyderman R. Targeted disruption of the leukotriene B(4) receptor in mice reveals its role in inflammation and platelet-activating factor-induced anaphylaxis. J Exp Med (2000) 192(3):433-8. doi:10.1084/jem.192.3.433
31. Chen M, Lam BK, Kanaoka Y, Nigrovic PA, Audoly LP, Austen KF, et al. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis. J Exp Med (2006) 203(4):837-42. doi:10.1084/jem.20052371
32. Kim ND, Chou RC, Seung E, Tager AM, Luster AD. A unique requirement for the leukotriene B4 receptor BLT1 for neutrophil recruitment in inflammatory arthritis. J Exp Med (2006) 203(4):829-35. doi:10.1084/jem.20052349
33. Chou RC, Kim ND, Sadik CD, Seung E, Lan Y, Byrne MH, et al. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity (2010) 33(2):266-78. doi:10.1016/j.immuni.2010.07.018
34. Jacobs JP, Ortiz-Lopez A, Campbell JJ, Gerard CJ, Mathis D, Benoist C. Deficiency of CXCR2, but not other chemokine receptors, attenuates autoantibody-mediated arthritis in a murine model. Arthritis Rheum (2010) 62(7):1921-32. doi:10.1002/art.27470
35. Sadik CD, Kim ND, Iwakura Y, Luster AD. Neutrophils orchestrate their own recruitment in murine arthritis through C5aR and FcgammaR signaling. Proc Natl Acad Sci U S A (2012) 109(46):E3177-85. doi:10.1073/pnas.1213797109
36. Shushakova N, Skokowa J, Schulman J, Baumann U, Zwirner J, Schmidt RE, et al. C5a anaphylatoxin is a major regulator of activating versus inhibitory FcgammaRs in immune complex-induced lung disease. J Clin Invest (2002) 110(12):1823-30. doi:10.1172/JCI16577
37. Jakus ZN, Simon E, Balazs B, Mocsai A. Genetic deficiency of Syk protects mice from autoantibody-induced arthritis. Arthritis Rheum (2010) 62(7):1899-910. doi:10.1002/art.27438
38. Elliott ER, Van Ziffle JA, Scapini P, Sullivan BM, Locksley RM, Lowell CA. Deletion of Syk in neutrophils prevents immune complex arthritis. J Immunol (2011) 187(8):4319-30. doi:10.4049/jimmunol.1100341
39. Christensen AD, Haase C, Cook AD, Hamilton JA. Granulocyte colony-stimulating factor (G-CSF) plays an important role in immune complex-mediated arthritis. Eur J Immunol (2016) 46:1235-45. doi:10.1002/eji.201546185
40. Blom AB, van Lent PL, van VH, Holthuysen AE, Jacobs C, van de Putte LB, et al. Fc gamma R expression on macrophages is related to severity and chronicity of synovial inflammation and cartilage destruction during experimental immune-complex-mediated arthritis (ICA). Arthritis Res (2000) 2(6):489-503. doi:10.1186/ar131
41. Solomon S, Rajasekaran N, Jeisy-Walder E, Snapper SB, Illges H. A crucial role for macrophages in the pathology of K/BxN serum-induced arthritis. Eur J Immunol (2005) 35(10):3064-73. doi:10.1002/eji.200526167
42. Misharin AV, Cuda CM, Saber R, Turner JD, Gierut AK, Haines GK III, et al. Nonclassical Ly6C(-) monocytes drive the development of inflammatory arthritis in mice. Cell Rep (2014) 9(2):591-604. doi:10.1016/j.celrep.2014.09.032
43. Cook AD, Turner AL, Braine EL, Pobjoy J, Lenzo JC, Hamilton JA. Regulation of systemic and local myeloid cell subpopulations by bone marrow cell-derived granulocyte-macrophage colony-stimulating factor in experimental inflammatory arthritis. Arthritis Rheum (2011) 63(8):2340-51. doi:10.1002/art.30354
44. Hamilton JA. GM-CSF as a target in inflammatory/autoimmune disease: current evidence and future therapeutic potential. Expert Rev Clin Immunol (2015) 11(4):457-65. doi:10.1586/1744666X.2015.1024110
45. Feyerabend T-B, Weiser A, Tietz A, Stassen M, Harris N, Kopf M, et al. Cre-mediated cell ablation contests mast cell contribution in models of antibody-and T cell-mediated autoimmunity. Immunity (2011) 35(5):832-44. doi:10.1016/j.immuni.2011.09.015
46. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB. Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science (2002) 297(5587):1689-92. doi:10.1126/science.1073176
47. Nigrovic PA, Binstadt BA, Monach PA, Johnsen A, Gurish M, Iwakura Y, et al. Mast cells contribute to initiation of autoantibody-mediated arthritis via IL-1. Proc Natl Acad Sci U S A (2007) 104(7):2325-30. doi:10.1073/pnas.0610852103
48. Kneilling M, Hueltner L, Pichler BJ, Mailhammer R, Morawietz L, Solomon S, et al. Targeted mast cell silencing protects against joint destruction and angiogenesis in experimental arthritis in mice. Arthritis Rheum (2007) 56(6):1806-16. doi:10.1002/art.22602
49. Shin K, Nigrovic PA, Crish J, Boilard E, McNeil HP, Larabee KS, et al. Mast cells contribute to autoimmune inflammatory arthritis via their tryptase/heparin complexes. J Immunol (2009) 182(1):647-56. doi:10.4049/jimmunol.182.1.647
50. Kim HY, Kim S, Chung DH. FcyRIII engagement provides activating signals to NKT cells in antibody-induced joint inflammation. J Clin Invest (2006) 116(9):2484-92. doi:10.1172/JCI27219
51. Kim HY, Kim HJ, Min HS, Kim S, Park WS, Park SH, et al. NKT cells promote antibody-induced joint inflammation by suppressing transforming growth factor B1 production. J Exp Med (2005) 201(1):41-7. doi:10.1084/jem.20041400
52. Solomon S, Kolb C, Mohanty S, Jeisy-Walder E, Preyer R, Schollhorn V, et al. Transmission of antibody-induced arthritis is independent of complement component 4 (C4) and the complement receptors 1 and 2 (CD21/35). Eur J Immunol (2002) 32(3):644-51. doi:10.1002/1521-4141(200203)32:3<644::AID-IMMU644>3.0.CO;2-5
53. Monach PA, Verschoor A, Jacobs JP, Carroll MC, Wagers AJ, Benoist C, et al. Circulating C3 is necessary and sufficient for induction of autoantibody-mediated arthritis in a mouse model. Arthritis Rheum (2007) 56(9):2968-74. doi:10.1002/art.22859
54. Klaus GG, Pepys MB, Kitajima K, Askonas BA. Activation of mouse complement by different classes of mouse antibody. Immunology (1979) 38(4):687-95.
55. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med (2011) 365(23):2205-19. doi:10.1056/NEJMra1004965
56. van den Berg WB. Lessons from animal models of arthritis over the past decade. Arthritis Res Ther (2009) 11(5):250. doi:10.1186/ar2803
57. Ji H, Pettit A, Ohmura K, Ortiz-Lopez A, Duchatelle V, Degott C, et al. Critical roles for interleukin 1 and tumor necrosis factor a in antibody-induced arthritis. J Exp Med (2002) 196(1):77-85. doi:10.1084/jem.20020439
58. Kyburz D, Carson DA, Corr M. The role of CD40 ligand and tumor necrosis factor a signaling in the transgenic K/BxN mouse model of rheumatoid arthritis. Arthritis Rheum (2000) 43(11):2571-7. doi:10.1002/1529-0131(200011)43:11<2571::AID-ANR26>3.0.CO;2-4
59. Lamacchia C, Rodriguez E, Palmer G, Vigne S, Martin P, Talabot-Ayer D, et al. Articular inflammation is controlled by myeloid cell-derived interleukin 1 receptor antagonist during the acute phase of arthritis in mice. Ann Rheum Dis (2012) 71(2):281-7. doi:10.1136/annrheumdis-2011-200429
60. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity (2008) 28(4):454-67. doi:10.1016/j.immuni.2008.03.004
61. Patel DD, Lee DM, Kolbinger F, Antoni C. Effect of IL-17A blockade with secukinumab in autoimmune diseases. Ann Rheum Dis (2013) 72(Suppl 2):ii116-23. doi:10.1136/annrheumdis-2012-202371
62. Jacobs JP, Wu HJ, Benoist C, Mathis D. IL-17-producing T cells can augment autoantibody-induced arthritis. Proc Natl Acad Sci U S A (2009) 106(51):21789-94. doi:10.1073/pnas.0912152106
63. Katayama M, Ohmura K, Yukawa N, Terao C, Hashimoto M, Yoshifuji H, et al. Neutrophils are essential as a source of IL-17 in the effector phase of arthritis. PLoS One (2013) 8(5):e62231. doi:10.1371/journal.pone.0062231
64. Koenders MI, Lubberts E, van de Loo FA, Oppers-Walgreen B, van den Bersselaar L, Helsen MM, et al. Interleukin-17 acts independently of TNF-alpha under arthritic conditions. J Immunol (2006) 176(10):6262-9. doi:10.4049/jimmunol.176.10.6262
65. Chen M, Boilard E, Nigrovic PA, Clark P, Xu D, Fitzgerald GA, et al. Predominance of cyclooxygenase 1 over cyclooxygenase 2 in the generation of proinflammatory prostaglandins in autoantibody-driven K/BxN serum-transfer arthritis. Arthritis Rheum (2008) 58(5):1354-65. doi:10.1002/art.23453
66. Koenders MI, van den Berg WB. Novel therapeutic targets in rheumatoid arthritis. Trends Pharmacol Sci (2015) 36(4):189-95. doi:10.1016/j.tips.2015.02.001
67. Brightbill HD, Libraty DH, Krutzik SR, Yang RB, Belisle JT, Bleharski JR, et al. Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science (1999) 285(5428):732-6. doi:10.1126/science.285.5428.732
68. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, et al. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity (1998) 9(1):143-50. doi:10.1016/S1074-7613(00)80596-8
69. Choe JY, Crain B, Wu SR, Corr M. Interleukin 1 receptor dependence of serum transferred arthritis can be circumvented by toll-like receptor 4 signaling. J Exp Med (2003) 197(4):537-42. doi:10.1084/jem.20021850
70. Christianson CA, Dumlao DS, Stokes JA, Dennis EA, Svensson CI, Corr M, et al. Spinal TLR4 mediates the transition to a persistent mechanical hypersensitivity after the resolution of inflammation in serum-transferred arthritis. Pain (2011) 152(12):2881-91. doi:10.1016/j.pain.2011.09.020
71. Abdollahi-Roodsaz S, Koenders MI, Walgreen B, Bolscher J, Helsen MM, van den Bersselaar LA, et al. Toll-like receptor 2 controls acute immune complex-driven arthritis in mice by regulating the inhibitory Fcgamma receptor IIB. Arthritis Rheum (2013) 65(10):2583-93. doi:10.1002/art.38087
72. Kim HS, Chung DH. TLR4-mediated IL-12 production enhances IFN-gamma and IL-1beta production, which inhibits TGF-beta production and promotes antibody-induced joint inflammation. Arthritis Res Ther (2012) 14(5):R210. doi:10.1186/ar4048
73. Wu HJ, Sawaya H, Binstadt B, Brickelmaier M, Blasius A, Gorelik L, et al. Inflammatory arthritis can be reined in by CpG-induced DC-NK cell cross talk. J Exp Med (2007) 204(8):1911-22. doi:10.1084/jem.20070285
74. Duffau P, Menn-Josephy H, Cuda CM, Dominguez S, Aprahamian TR, Watkins AA, et al. Promotion of inflammatory arthritis by interferon regulatory factor 5 in a mouse model. Arthritis Rheumatol (2015) 67(12):3146-57. doi:10.1002/art.39321
75. Hogg N, Laschinger M, Giles K, McDowall A. T-cell integrins: more than just sticking points. J Cell Sci (2003) 116(23):4695-705. doi:10.1242/jcs.00876
76. Ueda T, Rieu P, Brayer J, Arnaout MA. Identification of the complement iC3b binding site in the beta 2 integrin CR3 (CD11b/CD18). Proc Natl Acad Sci U S A (1994) 91(22):10680-4. doi:10.1073/pnas.91.22.10680
77. Watts GM, Beurskens FJM, Martin-Padura I, Ballantyne CM, Klickstein LB, Brenner MB, et al. Manifestations of inflammatory arthritis are critically dependent on LFA-1. J Immunolog (2005) 174(6):3668-75. doi:10.4049/jimmunol.174.6.3668
78. Henderson RB, Hobbs JA, Mathies M, Hogg N. Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood (2003) 102(1):328-35. doi:10.1182/blood-2002-10-3228
79. Garcia S, Forteza J, Lopez-Otin C, Gomez-Reino JJ, Gonzalez A, Conde C. Matrix metalloproteinase-8 deficiency increases joint inflammation and bone erosion in the K/BxN serum-transfer arthritis model. Arthritis Res Ther (2010) 12(6):R224. doi:10.1186/ar3211
80. Joosten LA, Helsen MM, Saxne T, van De Loo FA, Heinegard D, van Den Berg WB. IL-1 alpha beta blockade prevents cartilage and bone destruction in murine type II collagen-induced arthritis, whereas TNF-alpha blockade only ameliorates joint inflammation. J Immunol (1999) 163(9):5049-55.
81. Pettit AR, Ji H, von Stechow D, Muller R, Goldring SR, Choi Y, et al. TRANCE/RANKL knockout mice are protected from bone erosion in a serum transfer model of arthritis. Am J Pathol (2001) 159(5):1689-99. doi:10.1016/S0002-9440(10)63016-7
82. Chen Z, Ma T, Huang C, Zhang L, Hu T, Li J. MIF, a potential therapeutic target for rheumatoid arthritis? Rheumatol Int (2014) 34(10):1481-2. doi:10.1007/s00296-013-2877-y
83. Singh A, Leng L, Fan J, Gajda M, Brauer R, Fingerle-Rowson G, et al. Macrophage-derived, macrophage migration inhibitory factor (MIF) is necessary to induce disease in the K/BxN serum-induced model of arthritis. Rheumatol Int (2013) 33(9):2301-8. doi:10.1007/s00296-013-2713-4
84. Gu R, Santos LL, Ngo D, Fan H, Singh PP, Fingerle-Rowson G, et al. Macrophage migration inhibitory factor is essential for osteoclastogenic mechanisms in vitro and in vivo mouse model of arthritis. Cytokine (2015) 72(2):135-45. doi:10.1016/j.cyto.2014.11.015
85. Walsh DA, McWilliams DF. Mechanisms, impact and management of pain in rheumatoid arthritis. Nat Rev Rheumatol (2014) 10(10):581-92. doi:10.1038/nrrheum.2014.64
86. Christianson CA, Corr M, Firestein GS, Mobargha A, Yaksh TL, Svensson CI. Characterization of the acute and persistent pain state present in K/BxN serum transfer arthritis. Pain (2010) 151(2):394-403. doi:10.1016/j.pain.2010.07.030
87. Christianson CA, Corr M, Yaksh TL, Svensson CI. K/BxN serum transfer arthritis as a model of inflammatory joint pain. Methods Mol Biol (2012) 851:249-60. doi:10.1007/978-1-61779-561-9_19
88. Borbely E, Botz B, Bolcskei K, Kenyer T, Kereskai L, Kiss T, et al. Capsaicin-sensitive sensory nerves exert complex regulatory functions in the serum-transfer mouse model of autoimmune arthritis. Brain Behav Immunol (2015) 45:50-9. doi:10.1016/j.bbi.2014.12.012
89. Rao SM, Auger JL, Gaillard P, Weissleder R, Wada E, Torres R, et al. The neuropeptide neuromedin U promotes autoantibody-mediated arthritis. Arthritis Res Ther (2012) 14(1):R29. doi:10.1186/ar3732
90. Stangenberg L, Burzyn D, Binstadt BA, Weissleder R, Mahmood U, Benoist C, et al. Denervation protects limbs from inflammatory arthritis via an impact on the microvasculature. Proc Natl Acad Sci U S A (2014) 111(31):11419-24. doi:10.1073/pnas.1410854111
91. Nandakumar K, Holmdahl R. Antibody-induced arthritis: disease mechanisms and genes involved at the effector phase of arthritis. Arthritis Res Ther (2006) 8(6):223. doi:10.1186/ar2089
92. Kagari T, Doi H, Shimozato T. The importance of IL-1-beta and TNF-alpha, and the noninvolvement of IL-6, in the development of monoclonal antibody-induced arthritis. J Immunol (2002) 169(3):1459-66. doi:10.4049/jimmunol.169.3.1459
93. Nandakumar K, Backlund J, Vestberg M, Holmdahl R. Collagen type II (CII)-specific antibodies induce arthritis in the absence of T or B cells but the arthritis progression is enhanced by CII-reactive T cells. Arthritis Res Ther (2004) 6(6):R544-50. doi:10.1186/ar1217
94. Kagari T, Tanaka D, Doi H, Shimozato T. Essential role of Fcy receptors in anti-type II collagen antibody-induced arthritis. J Immunol (2003) 170(8):4318-24. doi:10.4049/jimmunol.170.8.4318
95. Banda NK, Hyatt S, Antonioli AH, White JT, Glogowska M, Takahashi K, et al. Role of C3a receptors, C5a receptors, and complement protein C6 deficiency in collagen antibody-induced arthritis in mice. J Immunol (2012) 188(3):1469-78. doi:10.4049/jimmunol.1102310
96. Tanaka D, Kagari T, Doi H, Shimozato T. Essential role of neutrophils in anti-type II collagen antibody and lipopolysaccharide-induced arthritis. Immunology (2006) 119(2):195-202. doi:10.1111/j.1365-2567.2006.02424.x
97. Banda NK, Thurman JM, Kraus D, Wood A, Carroll MC, Arend WP, et al. Alternative complement pathway activation is essential for inflammation and joint destruction in the passive transfer model of collagen-induced arthritis. J Immunol (2006) 177(3):1904-12. doi:10.4049/jimmunol.177.3.1904
98. Hietala MA, Nandakumar KS, Persson L, Fahlen S, Holmdahl R, Pekna M. Complement activation by both classical and alternative pathways is critical for the effector phase of arthritis. Eur J Immunol (2004) 34(4):1208-16. doi:10.1002/eji.200424895
99. Banda NK, Takahashi K, Wood AK, Holers VM, Arend WP. Pathogenic complement activation in collagen antibody-induced arthritis in mice requires amplification by the alternative pathway. J Immunol (2007) 179(6):4101-9. doi:10.4049/jimmunol.179.6.4101
100. Khachigian LM. Collagen antibody-induced arthritis. Nat Protocols (2006) 1(5):2512-6. doi:10.1038/nprot.2006.393
101. Rosloniec EF, Cremer M, Kang AH, Myers LK, Brand DD. Collagen-induced arthritis. Curr Protoc Immunol (2010) Chapter 15:Unit-25. doi:10.1002/0471142735.im1505s89
102. Monach PA, Mathis D, Benoist C. The K/BxN arthritis model. Curr Protoc Immunol (2008) Chapter 15:Unit 15 22. doi:10.1002/0471142735.im1522s81
103. Kannan K, Ortmann RA, Kimpel D. Animal models of rheumatoid arthritis and their relevance to human disease. Pathophysiology (2005) 12(3):167-81. doi:10.1016/j.pathophys.2005.07.011
104. Watson WC, Townes AS. Genetic susceptibility to murine collagen II autoimmune arthritis. Proposed relationship to the IgG2 autoantibody subclass response, complement C5, major histocompatibility complex (MHC) and non-MHC loci. J Exp Med (1985) 162(6):1878-91. doi:10.1084/jem.162.6.1878
105. Kleinau S, Martinsson P, Heyman B. Induction and suppression of collagen-induced arthritis is dependent on distinct fcgamma receptors. J Exp Med (2000) 191(9):1611-6. doi:10.1084/jem.191.9.1611
106. Ståhl TD, Andrén M, Martinsson P, Verbeek JS, Kleinau S. Expression of FcγRIII is required for development of collagen-induced arthritis. Eur J Immunol (2002) 32(10):2915-22. doi:10.1002/1521-4141(2002010)32:10<2915:AID-IMMU2915>3.0.CO;2-4
107. Andersson C, Wenander CS, Usher PA, Hebsgaard JB, Sondergaard BC, Rono B, et al. Rapid-onset clinical and mechanistic effects of anti-C5aR treatment in the mouse collagen-induced arthritis model. Clin Exp Immunol (2014) 177(1):219-33. doi:10.1111/cei.12338
108. Hietala MA, Jonsson IM, Tarkowski A, Kleinau S, Pekna M. Complement deficiency ameliorates collagen-induced arthritis in mice. J Immunol (2002) 169(1):454-9. doi:10.4049/jimmunol.169.1.454
109. Eyles JL, Hickey MJ, Norman MU, Croker BA, Roberts AW, Drake SF, et al. A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood (2008) 112(13):5193-201. doi:10.1182/blood-2008-02-139535
110. Van Lent PL, Holthuysen AE, Van Rooijen N, Van De Putte LB, Van Den Berg WB. Local removal of phagocytic synovial lining cells by clodronate-liposomes decreases cartilage destruction during collagen type II arthritis. Ann Rheum Dis (1998) 57(7):408-13. doi:10.1136/ard.57.7.408
111. Nandakumar KS, Holmdahl R. Arthritis induced with cartilage-specific antibodies is IL-4-dependent. Eur J Immunol (2006) 36(6):1608-18. doi:10.1002/eji.200535633
112. Campbell IK, Rich MJ, Bischof RJ, Dunn AR, Grail D, Hamilton JA. Protection from collagen-induced arthritis in granulocyte-macrophage colony-stimulating factor-deficient mice. J Immunol (1998) 161(7):3639-44.
113. Fujimoto M, Serada S, Mihara M, Uchiyama Y, Yoshida H, Koike N, et al. Interleukin-6 blockade suppresses autoimmune arthritis in mice by the inhibition of inflammatory Th17 responses. Arthritis Rheum (2008) 58(12):3710-9. doi:10.1002/art.24126
114. Lubberts E, Joosten LA, Oppers B, van den Bersselaar L, Coenen-de Roo CJ, Kolls JK, et al. IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J Immunol (2001) 167(2):1004-13. doi:10.4049/jimmunol.167.2.1004
115. Ohmura K, Nguyen LT, Locksley RM, Mathis D, Benoist C. Interleukin-4 can be a key positive regulator of inflammatory arthritis. Arthritis Rheum (2005) 52(6):1866-75. doi:10.1002/art.21104
116. Holmdahl R, Mo JA, Jonsson R, Karlstrom K, Scheynius A. Multiple epitopes on cartilage type II collagen are accessible for antibody binding in vivo. Autoimmunity (1991) 10(1):27-34. doi:10.3109/08916939108997144
117. Crombie DE, Turer M, Zuasti BB, Wood B, McNaughton D, Nandakumar KS, et al. Destructive effects of murine arthritogenic antibodies to type II collagen on cartilage explants in vitro. Arthritis Res Ther (2005) 7(5):R927-37. doi:10.1186/ar1766
118. Hegen M, Keith JC Jr, Collins M, Nickerson-Nutter CL. Utility of animal models for identification of potential therapeutics for rheumatoid arthritis. Ann Rheum Dis (2008) 67(11):1505-15. doi:10.1136/ard.2007.076430
119. Asquith DL, Miller AM, McInnes IB, Liew FY. Animal models of rheumatoid arthritis. Eur J Immunol (2009) 39(8):2040-4. doi:10.1002/eji.200939578
120. Horsfall AC, Butler DM, Marinova L, Warden PJ, Williams RO, Maini RN, et al. Suppression of collagen-induced arthritis by continuous administration of IL-4. J Immunol (1997) 159(11):5687-96.
121. Yazici Y, Paget SA. Elderly-onset rheumatoid arthritis. Rheum Dis Clin North Am (2000) 26(3):517-26. doi:10.1016/S0889-857X(05)70154-X
122. Firestein GS. Evolving concepts of rheumatoid arthritis. Nature (2003) 423(6937):356-61. doi:10.1038/nature01661
123. van Boekel MA, Vossenaar ER, van den Hoogen FH, van Venrooij WJ. Autoantibody systems in rheumatoid arthritis: specificity, sensitivity and diagnostic value. Arthritis Res (2002) 4(2):87-93. doi:10.1186/ar533
124. Berglin E, Padyukov L, Sundin U, Hallmans G, Stenlund H, van Venrooij WJ, et al. A combination of autoantibodies to cyclic citrullinated peptide (CCP) and HLA-DRB1 locus antigens is strongly associated with future onset of rheumatoid arthritis. Arthritis Res Ther (2004) 6(4):R303-8. doi:10.1186/ar1187
125. Ytterberg AJ, Malmstrom V. Ways forward to identify new ACPA targets in RA. Arthritis Res Ther (2012) 14(5):124. doi:10.1186/ar4031
126. Monach PA, Benoist C, Mathis D. The role of antibodies in mouse models of rheumatoid arthritis, and relevance to human disease. Adv Immunol (2004) 82:217-48. doi:10.1016/S0065-2776(04)82005-4
127. Firestein GS. Immunologic mechanisms in the pathogenesis of rheumatoid arthritis. J Clin Rheumatol (2005) 11(3 Suppl):S39-44. doi:10.1097/01.rhu.0000166673.34461.33
128. Patel HB, Kornerup KN, Sampaio AL, D'Acquisto F, Seed MP, Girol AP, et al. The impact of endogenous annexin A1 on glucocorticoid control of inflammatory arthritis. Ann Rheum Dis (2012) 71(11):1872-80. doi:10.1136/annrheumdis-2011-201180
129. Ryan SM, McMorrow J, Umerska A, Patel HB, Kornerup KN, Tajber L, et al. An intra-articular salmon calcitonin-based nanocomplex reduces experimental inflammatory arthritis. J Control Release (2013) 167(2):120-9. doi:10.1016/j.jconrel.2013.01.027
130. Zhou HF, Hu G, Wickline SA, Lanza GM, Pham CT. Synergistic effect of antiangiogenic nanotherapy combined with methotrexate in the treatment of experimental inflammatory arthritis. Nanomedicine (Lond) (2010) 5(7):1065-74. doi:10.2217/nnm.10.78
131. Choe JY, Park KY, Park SH, Lee SI, Kim SK. Regulatory effect of calcineurin inhibitor, tacrolimus, on IL-6/sIL-6R-mediated RANKL expression through JAK2-STAT3-SOCS3 signaling pathway in fibroblast-like synoviocytes. Arthritis Res Ther (2013) 15(1):R26. doi:10.1186/ar4162
132. Schaller M, Burton DR, Ditzel HJ. Autoantibodies to GPI in rheumatoid arthritis: linkage between an animal model and human disease. Nat Immunol (2001) 2(8):746-53. doi:10.1038/90696
133. Matsumoto I, Lee DM, Goldbach-Mansky R, Sumida T, Hitchon CA, Schur PH, et al. Low prevalence of antibodies to glucose-6-phosphate isomerase in patients with rheumatoid arthritis and a spectrum of other chronic autoimmune disorders. Arthritis Rheum (2003) 48(4):944-54. doi:10.1002/art.10898
134. Schubert D, Schmidt M, Zaiss D, Jungblut PR, Kamradt T. Autoantibodies to GPI and creatine kinase in RA. Nat Immunol (2002) 3(5):411-3. doi:10.1038/ni0502-411a
135. Kassahn D, Kolb C, Solomon S, Bochtler P, Illges H. Few human autoimmune sera detect GPI. Nat Immunol (2002) 3(5):411-2. doi:10.1038/ni0502-411b
136. Herve CA, Wait R, Venables PJ. Glucose-6-phosphate isomerase is not a specific autoantigen in rheumatoid arthritis. Rheumatology (Oxford) (2003) 42(8):986-8. doi:10.1093/rheumatology/keg271
137. van Gaalen FA, Toes RE, Ditzel HJ, Schaller M, Breedveld FC, Verweij CL, et al. Association of autoantibodies to glucose-6-phosphate isomerase with extraarticular complications in rheumatoid arthritis. Arthritis Rheum (2004) 50(2):395-9. doi:10.1002/art.20028
138. Schaller M, Stohl W, Tan SM, Benoit VM, Hilbert DM, Ditzel HJ. Raised levels of anti-glucose-6-phosphate isomerase IgG in serum and synovial fluid from patients with inflammatory arthritis. Ann Rheum Dis (2005) 64(5):743-9. doi:10.1136/ard.2004.025502
139. Zong M, Lu T, Fan S, Zhang H, Gong R, Sun L, et al. Glucose-6-phosphate isomerase promotes the proliferation and inhibits the apoptosis in fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Res Ther (2015) 17(1):100. doi:10.1186/s13075-015-0619-0
140. van den Berg WB. Anti-cytokine therapy in chronic destructive arthritis. Arthritis Res (2001) 3(1):18-26. doi:10.1186/ar303
141. Kollias G, Papadaki P, Apparailly F, Vervoordeldonk MJ, Holmdahl R, Baumans V, et al. Animal models for arthritis: innovative tools for prevention and treatment. Ann Rheum Dis (2011) 70(8):1357-62. doi:10.1136/ard.2010.148551
142. Vincent TL, Williams RO, Maciewicz R, Silman A, Garside P. Arthritis Research UKamwg. Mapping pathogenesis of arthritis through small animal models. Rheumatology (Oxford) (2012) 51(11):1931-41. doi:10.1093/rheumatology/kes035