Review: Animal models as a tool to dissect pivotal pathways driving spondyloarthritis

Arthritis and Rheumatology

Volumn 67, Issue 11, 2015, Pages 2813-2827

  Vieira Sousa, Elsa ^a   Van Duivenvoorde, Leonie M ^b   Fonseca, João E ^a   Lories, Rik J ^c   Baeten, Dominique L ^b  

^a UNIVERSITY OF LISBON   (Portugal)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; CURDLAN; HLA B27 ANTIGEN; INTERLEUKIN 23; MINICIRCLE DNA; TUMOR NECROSIS FACTOR;

ANIMAL MODEL; ANKYLOSING ENTHESITIS; ANKYLOSING SPONDYLITIS; ANTIGEN EXPRESSION; ENDOPLASMIC RETICULUM; ENTHESITIS; FISCHER 344 RAT; GIANT CELL; HUMAN; LEWIS RAT; MECHANICAL STRESS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; REVIEW; SPONDYLARTHRITIS; TRANSGENIC MOUSE; TRANSGENIC RAT; ANIMAL; DISEASE MODEL; PATHOPHYSIOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; SPONDYLARTHRITIS;

EID: 84946044362     PISSN: 23265191     EISSN: 23265205     Source Type: Journal    
DOI: 10.1002/art.39282     Document Type: Review

References (80)

1. Baeten DL, Kuchroo VK., How cytokine networks fuel inflammation: interleukin-17 and a tale of two autoimmune diseases. Nat Med 2013; 19: 824-5.
2. Coppin HL, McDevitt HO., Absence of polymorphism between HLA-B27 genomic exon sequences isolated from normal donors and ankylosing spondylitis patients. J Immunol 1986; 137: 2168-72.
3. 2-microglobulin) chains of HLA class I antigens. EMBO J 1987; 6: 1673-6.
4. 2-microglobulin. J Immunol 1988; 141: 4020-3.
5. Nickerson CL, Luthra HS, Savarirayan S, David CS., Susceptibility of HLA-B27 transgenic mice to Yersinia enterocolitica infection. Hum Immunol 1990; 28: 382-96.
6. Kalinke U, Arnold B, Hammerling GJ., Strong xenogeneic HLA response in transgenic mice after introducing an α3 domain into HLA B27. Nature 1990; 348: 642-4.
7. Weiss EH, Schliesser G, Botteron C, McMichael A, Riethmuller G, Kievits F, et al., HLA class-I-transgenic mice as model system to study MHC-restricted antigen recognition in man. Scand J Rheumatol Suppl 1990; 87: 91-6.
8. 2-microglobulin: a model of human spondyloarthropathies. J Exp Med 1995; 182: 1153-8.
9. 2m: an animal model of HLA-B27-associated human disorders. Cell 1990; 63: 1099-112.
10. 2-microglobulin curbs HLA-B27 misfolding and promotes arthritis and spondylitis without colitis in male HLA-B27-transgenic rats. Arthritis Rheum 2006; 54: 1317-27.
11. Kriegsmann J, Franklin BN, Gay RE, Taurog JD, Hammer RE, Gay S., Fusion of vertebral bodies and the sacroiliac joint by cartilaginous tissue in HLA-B27 transgenic rats [abstract]. Arthritis Rheum 1995; 38 Suppl: S202.
12. Taurog JD, Maika SD, Simmons WA, Breban M, Hammer RE., Susceptibility to inflammatory disease in HLA-B27 transgenic rat lines correlates with the level of B27 expression. J Immunol 1993; 150: 4168-78.
13. Hammer RE, Richardson JA, Simmons WA, White AL, Breban M, Taurog JD., High prevalence of colorectal cancer in HLA-B27 transgenic F344 rats with chronic inflammatory bowel disease. J Investig Med 1995; 43: 262-8.
14. McLean L, Hammer RE, Taurog JD., Contrasting cytokine profiles in colitis and synovitis of HLA-B27 transgenic rats [abstract]. Arthritis Rheum 1995; 38 Suppl: S315.
15. Taurog JD, Rival C, van Duivenvoorde LM, Satumtira N, Dorris ML, Sun M, et al., Autoimmune epididymoorchitis is essential to the pathogenesis of male-specific spondylarthritis in HLA-B27-transgenic rats. Arthritis Rheum 2012; 64: 2518-28.
16. 2-microglobulin-transgenic rat model of spondylarthritis. Arthritis Rheum 2012; 64: 3210-9.
17. Holmdahl R, Lorentzen JC, Lu S, Olofsson P, Wester L, Holmberg J, et al., Arthritis induced in rats with nonimmunogenic adjuvants as models for rheumatoid arthritis. Immunol Rev 2001; 184: 184-202.
18. 2m. J Clin Invest 1996; 98: 2746-55.
19. 2-microglobulin-deficient mice without expression of HLA-B27: association with deficiency of endogenous major histocompatibility complex class I expression. Arthritis Rheum 2000; 43: 2290-6.
20. Braun J, Brandt J, Listing J, Zink A, Alten R, Golder W, et al., Treatment of active ankylosing spondylitis with infliximab: a randomised controlled multicentre trial. Lancet 2002; 359: 1187-93.
21. Van den Bosch F, Kruithof E, Baeten D, Herssens A, de Keyser F, Mielants H, et al., Randomized double-blind comparison of chimeric monoclonal antibody to tumor necrosis factor α (infliximab) versus placebo in active spondylarthropathy. Arthritis Rheum 2002; 46: 755-65.
22. Bradley JR., TNF-mediated inflammatory disease. J Pathol 2008; 214: 149-60.
23. Schett G, Saag KG, Bijlsma JW., From bone biology to clinical outcome: state of the art and future perspectives. Ann Rheum Dis 2010; 69: 1415-9.
24. Keffer J, Probert L, Cazlaris H, Georgopoulos S, Kaslaris E, Kioussis D, et al., Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J 1991; 10: 4025-31.
25. Aloe L, Probert L, Kollias G, Bracci-Laudiero L, Spillantini MG, Levi-Montalcini R., The synovium of transgenic arthritic mice expressing human tumor necrosis factor contains a high level of nerve growth factor. Growth Factors 1993; 9: 149-55.
26. Kontoyiannis D, Pasparakis M, Pizarro TT, Cominelli F, Kollias G., Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 1999; 10: 387-98.
27. Redlich K, Gortz B, Hayer S, Zwerina J, Kollias G, Steiner G, et al., Overexpression of tumor necrosis factor causes bilateral sacroiliitis. Arthritis Rheum 2004; 50: 1001-5.
28. Diarra D, Stolina M, Polzer K, Zwerina J, Ominsky MS, Dwyer D, et al., Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007; 13: 156-63.
29. Uderhardt S, Diarra D, Katzenbeisser J, David JP, Zwerina J, Richards W, et al., Blockade of Dickkopf (DKK)-1 induces fusion of sacroiliac joints. Ann Rheum Dis 2010; 69: 592-7.
30. Armaka M, Apostolaki M, Jacques P, Kontoyiannis DL, Elewaut D, Kollias G., Mesenchymal cell targeting by TNF as a common pathogenic principle in chronic inflammatory joint and intestinal diseases. J Exp Med 2008; 205: 331-7.
31. Jacques P, Lambrecht S, Verheugen E, Pauwels E, Kollias G, Armaka M, et al., Proof of concept: enthesitis and new bone formation in spondyloarthritis are driven by mechanical strain and stromal cells. Ann Rheum Dis 2014; 73: 437-45.
32. Black RA., Tumor necrosis factor-α converting enzyme. Int J Biochem Cell Biol 2002; 34: 1-5.
33. Alexopoulou L, Pasparakis M, Kollias G., A murine transmembrane tumor necrosis factor (TNF) transgene induces arthritis by cooperative p55/p75 TNF receptor signaling. Eur J Immunol 1997; 27: 2588-92.
34. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, et al., Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003; 198: 1951-7.
35. Cortes A, Hadler J, Pointon JP, Robinson PC, Karaderi T, Leo P, et al., Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci. Nat Genet 2013; 45: 730-8.
36. Reveille JD, Sims AM, Danoy P, Evans DM, Leo P, Pointon JJ, et al., Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat Genet 2010; 42: 123-7.
37. Baeten D, Baraliakos X, Braun J, Sieper J, Emery P, van der Heijde D, et al., Anti-interleukin-17A monoclonal antibody secukinumab in treatment of ankylosing spondylitis: a randomised, double-blind, placebo-controlled trial [published erratum appears in Lancet 2014;383:1548]. Lancet 2013; 382: 1705-13.
38. McInnes IB, Sieper J, Braun J, Emery P, van der Heijde D, Isaacs JD, et al., Efficacy and safety of secukinumab, a fully human anti-interleukin-17A monoclonal antibody, in patients with moderate-to-severe psoriatic arthritis: a 24-week, randomised, double-blind, placebo-controlled, phase II proof-of-concept trial. Ann Rheum Dis 2014; 73: 349-56.
39. McInnes IB, Kavanaugh A, Gottlieb AB, Puig L, Rahman P, Ritchlin C, et al, on behalf of the PSUMMIT 1 Study Group. Efficacy and safety of ustekinumab in patients with active psoriatic arthritis: 1 year results of the phase 3, multicentre, double-blind, placebo-controlled PSUMMIT 1 trial. Lancet 2013; 382: 780-9.
40. Ritchlin C, Rahman P, Kavanaugh A, McInnes IB, Puig L, Li S, et al, on behalf of the PSUMMIT 2 Study Group. Efficacy and safety of the anti-IL-12/23 p40 monoclonal antibody, ustekinumab, in patients with active psoriatic arthritis despite conventional non-biological and biological anti-tumour necrosis factor therapy: 6-month and 1-year results of the phase 3, multicentre, double-blind, placebo-controlled, randomised PSUMMIT 2 trial. Ann Rheum Dis 2014; 73: 990-9.
41. Mease PJ, Genovese MC, Greenwald MW, Ritchlin CT, Beaulieu AD, Deodhar A, et al., Brodalumab, an anti-IL17RA monoclonal antibody, in psoriatic arthritis. N Engl J Med 2014; 370: 2295-306.
42. Adamopoulos IE, Tessmer M, Chao CC, Adda S, Gorman D, Petro M, et al., IL-23 is critical for induction of arthritis, osteoclast formation, and maintenance of bone mass. J Immunol 2011; 187: 951-9.
43. - entheseal resident T cells. Nat Med 2012; 18: 1069-76.
44. Souza D II,. IL23 overexpression demonstrates gut-joint inflammation link and increased expression of spondyloarthopathy associated genes in vivo [abstract]. Arthritis Rheumatol 2014; 66 Suppl: S844.
45. Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, et al., Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 2003; 426: 454-60.
46. Yoshitomi H, Sakaguchi N, Kobayashi K, Brown GD, Tagami T, Sakihama T, et al., 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: 949-60.
47. Ruutu M, Thomas G, Steck R, Degli-Esposti MA, Zinkernagel MS, Alexander K, et al., β- glucan triggers spondylarthritis and Crohn's disease-like ileitis in SKG mice. Arthritis Rheum 2012; 64: 2211-22.
48. Benham H, Rehaume LM, Hasnain SZ, Velasco J, Baillet AC, Ruutu M, et al., Interleukin-23 mediates the intestinal response to microbial β-1,3-glucan and the development of spondyloarthritis pathology in SKG mice. Arthritis Rheumatol 2014; 66: 1755-67.
49. Capkova J, Ivanyi P., H-2 influence on ankylosing enthesopathy of the ankle (ANKENT). Folia Biol (Praha) 1992; 38: 258-62.
50. Weinreich S, Eulderink F, Capkova J, Pla M, Gaede K, Heesemann J, et al., HLA-B27 as a relative risk factor in ankylosing enthesopathy in transgenic mice. Hum Immunol 1995; 42: 103-15.
51. Holmdahl R, Jansson L, Andersson M, Jonsson R., Genetic, hormonal and behavioural influence on spontaneously developing arthritis in normal mice. Clin Exp Immunol 1992; 88: 467-72.
52. Nordling C, Karlsson-Parra A, Jansson L, Holmdahl R, Klareskog L., Characterization of a spontaneously occurring arthritis in male DBA/1 mice. Arthritis Rheum 1992; 35: 717-22.
53. Lories RJ, Matthys P, de Vlam K, Derese I, Luyten FP., Ankylosing enthesitis, dactylitis, and onychoperiostitis in male DBA/1 mice: a model of psoriatic arthritis. Ann Rheum Dis 2004; 63: 595-8.
54. Corthay A, Hansson AS, Holmdahl R., T lymphocytes are not required for the spontaneous development of entheseal ossification leading to marginal ankylosis in the DBA/1 mouse. Arthritis Rheum 2000; 43: 844-51.
55. Braem K, Carter S, Lories RJ., Spontaneous arthritis and ankylosis in male DBA/1 mice: further evidence for a role of behavioral factors in "stress-induced arthritis". Biol Proced Online 2012; 14: 10.
56. Dougados M, Baeten D., Spondyloarthritis. Lancet 2011; 377: 2127-37.
57. Colbert RA, Tran TM, Layh-Schmitt G., HLA-B27 misfolding and ankylosing spondylitis. Mol Immunol 2014; 57: 44-51.
58. + and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol 2011; 186: 2672-80.
59. May E, Dorris ML, Satumtira N, Iqbal I, Rehman MI, Lightfoot E, et al., CD8αβ T cells are not essential to the pathogenesis of arthritis or colitis in HLA-B27 transgenic rats. J Immunol 2003; 170: 1099-105.
60. 2-microglobulin-transgenic rats is not prevented by lack of CD8. Arthritis Rheum 2009; 60: 1977-84.
61. Turner MJ, Sowders DP, DeLay ML, Mohapatra R, Bai S, Smith JA, et al., HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response. J Immunol 2005; 175: 2438-48.
62. Turner MJ, DeLay ML, Bai S, Klenk E, Colbert RA., HLA-B27 up-regulation causes accumulation of misfolded heavy chains and correlates with the magnitude of the unfolded protein response in transgenic rats: implications for the pathogenesis of spondylarthritis-like disease. Arthritis Rheum 2007; 56: 215-23.
63. DeLay ML, Turner MJ, Klenk EI, Smith JA, Sowders DP, Colbert RA., HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum 2009; 60: 2633-43.
64. Ciccia F, Accardo-Palumbo A, Rizzo A, Guggino G, Raimondo S, Giardina A, et al., Evidence that autophagy, but not the unfolded protein response, regulates the expression of IL-23 in the gut of patients with ankylosing spondylitis and subclinical gut inflammation. Ann Rheum Dis 2014; 73: 1566-74.
65. Taurog JD, Richardson JA, Croft JT, Simmons WA, Zhou M, Fernandez-Sueiro JL, et al., The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med 1994; 180: 2359-64.
66. Rehaume LM, Mondot S, Aguirre de Carcer D, Velasco J, Benham H, Hasnain SZ, et al., ZAP-70 genotype disrupts the relationship between microbiota and host, leading to spondyloarthritis and ileitis in SKG mice. Arthritis Rheumatol 2014; 66: 2780-92.
67. Rehakova Z, Capkova J, Stepankova R, Sinkora J, Louzecka A, Ivanyi P, et al., Germ-free mice do not develop ankylosing enthesopathy, a spontaneous joint disease. Hum Immunol 2000; 61: 555-8.
68. 2 microglobulin transgenic rats. J Clin Invest 1996; 98: 945-53.
69. Rath HC, Wilson KH, Sartor RB., Differential induction of colitis and gastritis in HLA-B27 transgenic rats selectively colonized with Bacteroides vulgatus or Escherichia coli. Infect Immun 1999; 67: 2969-74.
70. 2-microglobulin affect the gut microbiota of transgenic rats. PLoS One 2014; 9: e105684.
71. McGonagle D, Gibbon W, Emery P., Classification of inflammatory arthritis by enthesitis. Lancet 1998; 352: 1137-40.
72. Paramarta JE, van der Leij C, Gofita I, Yeremenko N, van de Sande MG, de Hair MJ, et al., Peripheral joint inflammation in early onset spondyloarthritis is not specifically related to enthesitis. Ann Rheum Dis 2014; 73: 735-40.
73. Van Duivenvoorde L, Baeten D., Comment on: 'Spondyloarthritis: may the force be with you?', the editorial by McGonagle et al. Ann Rheum Dis 2014; 73: e38.
74. 2m transgenic rats treated with a monoclonal antibody against TNF-α. J Cell Mol Med 2011; 15: 270-9.
75. Breban M, Hammer RE, Richardson JA, Taurog JD., Transfer of the inflammatory disease of HLA-B27 transgenic rats by bone marrow engraftment. J Exp Med 1993; 178: 1607-16.
76. Lories RJ, Derese I, De Bari C, Luyten FP., Evidence for uncoupling of inflammation and joint remodeling in a mouse model of spondylarthritis. Arthritis Rheum 2007; 56: 489-97.
77. Appel H, Maier R, Loddenkemper C, Kayser R, Meier O, Hempfing A, et al., Immunohistochemical analysis of osteoblasts in zygapophyseal joints of patients with ankylosing spondylitis reveal repair mechanisms similar to osteoarthritis. J Rheumatol 2010; 37: 823-8.
78. Lories RJ, Derese I, Luyten FP., Inhibition of osteoclasts does not prevent joint ankylosis in a mouse model of spondyloarthritis. Rheumatology (Oxford) 2008; 47: 605-8.
79. Lories RJ, Derese I, Luyten FP., Modulation of bone morphogenetic protein signaling inhibits the onset and progression of ankylosing enthesitis. J Clin Invest 2005; 115: 1571-9.
80. Lories RJ, Daans M, Derese I, Matthys P, Kasran A, Tylzanowski P, et al., Noggin haploinsufficiency differentially affects tissue responses in destructive and remodeling arthritis. Arthritis Rheum 2006; 54: 1736-46.