BALB/c mice genetically susceptible to proteoglycan-induced arthritis and spondylitis show colony-dependent differences in disease penetrance

Arthritis Research and Therapy

Volumn 11, Issue 1, 2009, Pages

  Farkas, Balint ^a   Boldizsar, Ferenc ^a,b   Tarjanyi, Oktavia ^a   Laszlo, Anna ^a   Lin, Simon M ^c   Hutas, Gabor ^a   Tryniszewska, Beata ^a   Mangold, Aaron ^a   Nagyeri, Gyorgy ^a   Rosenzweig, Holly L ^d   Finnegan, Alison ^a   Mikecz, Katalin ^a   Glant, Tibor T ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF PÉCS   (Hungary)

^c NORTHWESTERN UNIVERSITY   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; COMPLEMENTARY DNA; CYTOKINE; PROTEOGLYCAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTHRITIS; ARTICLE; BAGG ALBINO MOUSE; CONTROLLED STUDY; DISEASE SEVERITY; DNA MICROARRAY; FEMALE; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; HISTOPATHOLOGY; IMMUNE RESPONSE; IN VITRO STUDY; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PENETRANCE; PHENOTYPIC VARIATION; PROTEIN BLOOD LEVEL; SINGLE NUCLEOTIDE POLYMORPHISM; SPLEEN CELL; SPONDYLITIS; STRAIN DIFFERENCE; T LYMPHOCYTE; ANIMAL; ANKYLOSING SPONDYLITIS; BLOOD; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC PREDISPOSITION; GENETICS; HUMAN; IMMUNOLOGY; IN SITU HYBRIDIZATION; PATHOLOGY; PHENOTYPE;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IN SITU HYBRIDIZATION; MICE; MICE, INBRED BALB C; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PENETRANCE; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEOGLYCANS; SPONDYLITIS, ANKYLOSING;

EID: 62149099615     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2613     Document Type: Article

References (92)

1. Gregersen PK Genetics of rheumatoid arthritis: Confronting complexity Arthritis Res 1999, 1:37-44 128868 11094412 10.1186/ar9
2. Pearson CM Development of arthritis, periarthritis and periostitis in rats given adjuvants Proc Soc Exp Biol Med 1956, 91:95-101 13297719
3. Holmdahl R Lorentzen JC Lu S Olofsson P Wester L Holmberg J Pettersson U Arthritis induced in rats with nonimmunogenic adjuvants as models for rheumatoid arthritis Immunol Rev 2001, 184:184-202 10.1034/ j.1600-065x.2001.1840117.x 12086312
4. Kannan K Ortmann RA Kimpel D Animal models of rheumatoid arthritis and their relevance to human disease Pathophysiology 2005, 12:167-181 10.1016/j.pathophys.2005.07.011 16171986
5. Trentham DE Townes AS Kang AH Autoimmunity to type II collagen: An experimental model of arthritis J Exp Med 1977, 146:857-868 2180804 894190 10.1084/jem.146.3.857
6. Courtenay JS Dallman MJ Dayan AD Martin A Mosedale B Immunization against heterologous type II collagen induces arthritis in mice Nature 1980, 283:666-668 6153460 10.1038/283666a0
7. Glant TT Mikecz K Arzoumanian A Poole AR Proteoglycan-induced arthritis in BALB/c mice. Clinical features and histopathology Arthritis Rheum 1987, 30:201-212 10.1002/art.1780300211 3827960
8. Glant TT Bardos T Vermes C Chandrasekaran R Valdéz JC Otto JM Gerard D Velins S Lovász G Zhang J Mikecz K Finnegan A Variations in susceptibility to proteoglycan-induced arthritis and spondylitis among C3H substrains of mice. Evidence of genetically acquired resistance to autoimmune disease Arthritis Rheum 2001, 44:682-692 10.1002/1529-0131(200103)44:3<682::AID-ANR118>3.0.CO;2-E 11263784
9. 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
10. Bardos T Szabo Z Czipri M Vermes C Tunyogi-Csapo M Urban RM Mikecz K Glant TT Longitudinal study on an autoimmune murine model of ankylosing spondylitis Ann Rheum Dis 2005, 64:981-987 1755557 15640265 10.1136/ ard.2004.029710
11. Szabo Z Szanto S Vegvari A Szekanecz Z Mikecz K Glant TT Genetic control of experimental spondyloarthropathy Arthritis Rheum 2005, 52:2452-2460 10.1002/art.21193 16059927
12. Adarichev VA Vegvari A Szabo Z Kis-Toth K Mikecz K Glant TT Congenic strains displaying similar clinical phenotype of arthritis represent different immunologic models of inflammation Genes Immun 2008, 9:591-601 10.1038/gene.2008.54 18650834
13. Zhang Y Guerassimov A Leroux JY Cartman A Webber C Lalic R de Miguel E Rosenberg LC Poole AR Induction of arthritis in BALB/c mice by cartilage link protein. Involvement of distinct regions recognized by T- and B lymphocytes Am J Pathol 1998, 153:1283-1291 1853050 9777960
14. Verheijden GFM Rijnders AWM Bos E De Roo CJJC van Staveren CJ Miltenburg AMM Meijerink JH Elewaut D de Keyser F Veys E Boots AM Human cartilage glycoprotein-39 as a candidate autoantigen in rheumatoid arthritis Arthritis Rheum 1997, 40:1115-1125 10.1002/art.1780400616 9182922
15. 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 2195765 10637275 10.1084/jem.191.2.313
16. 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
17. Mouse Genome Informatics homepage http://www.informatics.jax.org
18. Mikecz K Glant TT Poole AR Immunity to cartilage proteoglycans in BALB/c mice with progressive polyarthritis and ankylosing spondylitis induced by injection of human cartilage proteoglycan Arthritis Rheum 1987, 30:306-318 10.1002/art.1780300310 3566822
19. Glant TT Cs-Szabó G Nagase H Jacobs JJ Mikecz K Progressive polyarthritis induced in BALB/c mice by aggrecan from human osteoarthritic cartilage Arthritis Rheum 1998, 41:1007-1018 10.1002/ 1529-0131(199806)41:6<1007::AID-ART7>3.0.CO;2-6 9627010
20. Glant TT Mikecz K Proteoglycan aggrecan-induced arthritis. A murine autoimmune model of rheumatoid arthritis Methods Mol Med 2004, 102:313-338 15286393
21. Hanyecz A Berlo SE Szanto S Broeren CPM Mikecz K Glant TT 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 2004, 50:1665-1676 10.1002/art.20180 15146438
22. MacGregor AJ Snieder H Rigby AS Koskenvuo M Kaprio J Aho K Silman AJ Characterizing the quantitative genetic contribution to rheumatoid arthritis using data from twins Arthritis Rheum 2000, 43:30-37 10.1002/ 1529-0131(200001)43:1<30::AID-ANR5>3.0.CO;2-B 10643697
23. Otto JM Cs-Szabó G Gallagher J Velins S Mikecz K Buzas EI Enders JT Li Y Olsen BR Glant TT Identification of multiple loci linked to inflammation and autoantibody production by a genome scan of a murine model of rheumatoid arthritis Arthritis Rheum 1999, 42:2524-2531 10.1002/ 1529-0131(199912)42:12<2524::AID-ANR4>3.0.CO;2-0 10615997
24. Adarichev VA Valdez JC Bardos T Finnegan A Mikecz K Glant TT Combined autoimmune models of arthritis reveal shared and independent qualitative (binary) and quantitative trait loci J Immunol 2003, 170:2283-2292 12594249
25. Glant TT Mikecz K Poole AR Monoclonal antibodies to different protein-related epitopes of human articular cartilage proteoglycans Biochem J 1986, 234:31-41 1146523 2423072
26. Irizarry RA Hobbs B Collin F Beazer-Barclay YD Antonellis KJ Scherf U Speed TP Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 2003, 4:249-264 10.1093/biostatistics/4.2.249 12925520
27. Reiner A Yekutieli D Benjamini Y Identifying differentially expressed genes using false discovery rate controlling procedures Bioinformatics 2003, 19:368-375 10.1093/bioinformatics/btf877 12584122
28. Tunyogi-Csapo M Kis-Toth K Radacs M Farkas B Jacobs JJ Finnegan A Mikecz K Glant TT Cytokine-controlled RANKL and osteoprotegerin expression by human and mouse synovial fibroblasts: Fibroblast-mediated pathologic bone resorption Arthritis Rheum 2008, 58:2397-2408 10.1002/art.23653 18668542
29. Vegvari A Szabo Z Szanto S Nesterovitch AB Mikecz K Glant TT Adarichev VA Two major interacting chromosome loci control disease susceptibility in murine model of spondyloarthropathy J Immunol 2005, 175:2475-2483 16081819
30. Straub RH Rauch L Fassold A Lowin T Pongratz G Neuronally released sympathetic neurotransmitters stimulate splenic interferon-gamma secretion from T cells in early type II collagen-induced arthritis Arthritis Rheum 2008, 58:3450-3460 10.1002/art.24030 18975332
31. Coelho FM Pinho V Amaral FA Sachs D Costa VV Rodrigues DH Vieira AT Silva TA Souza DG Bertini R Teixeira AL Teixeira MM The chemokine receptors CXCR1/CXCR2 modulate antigen-induced arthritis by regulating adhesion of neutrophils to the synovial microvasculature Arthritis Rheum 2008, 58:2329-2337 10.1002/art.23622 18668539
32. Conte FP Barja-Fidalgo C Verri WA Jr Cunha FQ Rae GA Penido C Henriques MG Endothelins modulate inflammatory reaction in zymosan-induced arthritis: Participation of LTB4, TNF-alpha, and CXCL-1 J Leukoc Biol 2008, 84:652-660 10.1189/jlb.1207827 18515326
33. Adarichev VA Vermes C Hanyecz A Ludanyi K Tunyogi-Csapo M Finnegan A Mikecz K Glant TT Antigen-induced differential gene expression in lymphocytes and gene expression profile in synovium prior to the onset of arthritis Autoimmunity 2006, 39:663-673 10.1080/08916930601062643 17178563
34. Brown CR Blaho VA Loiacono CM Susceptibility to experimental Lyme arthritis correlates with KC and monocyte chemoattractant protein-1 production in joints and requires neutrophil recruitment via CXCR2 J Immunol 2003, 171:893-901 12847259
35. Wang Z Choi MK Ban T Yanai H Negishi H Lu Y Tamura T Takaoka A Nishikura K Taniguchi T Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules Proc Natl Acad Sci USA 2008, 105:5477-5482 2291118 18375758 10.1073/pnas.0801295105
36. Ishii KJ Kawagoe T Koyama S Matsui K Kumar H Kawai T Uematsu S Takeuchi O Takeshita F Coban C Akira S TANK-binding kinase-1 delineates innate and adaptive immune responses to DNA vaccines Nature 2008, 451:725-729 10.1038/nature06537 18256672
37. Takaoka A Wang Z Choi MK Yanai H Negishi H Ban T Lu Y Miyagishi M Kodama T Honda K Ohba Y Taniguchi T DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response Nature 2007, 448:501-505 10.1038/nature06013 17618271
38. Hsu HC Yang P Wang J Wu Q Myers R Chen J Yi J Guentert T Tousson A Stanus AL Le TV Lorenz RG Xu H Kolls JK Carter RH Chaplin DD Williams RW Mountz JD Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice Nat Immunol 2008, 9:166-175 10.1038/ni1552 18157131
39. Hsu HC Wu Y Yang P Wu Q Job G Chen J Wang J Accavitti-Loper MA Grizzle WE Carter RH Mountz JD Overexpression of activation-induced cytidine deaminase in B cells is associated with production of highly pathogenic autoantibodies J Immunol 2007, 178:5357-5365 17404321
40. Hsu HC Zhou T Kim H Barnes S Yang P Wu Q Zhou J Freeman BA Luo M Mountz JD Production of a novel class of polyreactive pathogenic autoantibodies in BXD2 mice causes glomerulonephritis and arthritis Arthritis Rheum 2006, 54:343-355 10.1002/art.21550 16385526
41. Wu Y Liu J Feng X Yang P Xu X Hsu HC Mountz JD Synovial fibroblasts promote osteoclast formation by RANKL in a novel model of spontaneous erosive arthritis Arthritis Rheum 2005, 52:3257-3268 10.1002/art.21354 16200600
42. Mountz JD Yang P Wu Q Zhou J Tousson A Fitzgerald A Allen J Wang X Cartner S Grizzle WE Yi N Lu L Williams RW Hsu HC Genetic segregation of spontaneous erosive arthritis and generalized autoimmune disease in the BXD2 recombinant inbred strain of mice Scand J Immunol 2005, 61:128-138 10.1111/j.0300-9475.2005.01548.x 15683449
43. Rivera J Proia RL Olivera A The alliance of sphingosine-1-phosphate and its receptors in immunity Nat Rev Immunol 2008, 8:753-763 10.1038/ nri2400 18787560
44. Yao Z Nakamura H Masuko-Hongo K Suzuki-Kurokawa M Nishioka K Kato T Characterisation of cartilage intermediate layer protein (CILP)-induced arthropathy in mice Ann Rheum Dis 2004, 63:252-258 1754905 14962958 10.1136/ard.2003.008045
45. Lorenzo P Bayliss MT Heinegard D A novel cartilage protein (CILP) present in the mid-zone of human articular cartilage increases with age J Biol Chem 1998, 273:23463-23468 10.1074/jbc.273.36.23463 9722583
46. Tsuruha J Masuko-Hongo K Kato T Sakata M Nakamura H Nishioka K Implication of cartilage intermediate layer protein in cartilage destruction in subsets of patients with osteoarthritis and rheumatoid arthritis Arthritis Rheum 2001, 44:838-845 10.1002/ 1529-0131(200104)44:4<838::AID-ANR140>3.0.CO;2-C 11315923
47. Kubagawa H Burrows PD Cooper MD A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells Proc Natl Acad Sci USA 1997, 94:5261-5266 24666 9144225 10.1073/pnas.94.10.5261
48. Puttick A Briggs D Welsh K Jacoby R Williamson E Jones V Extended haplotypes in rheumatoid arthritis and preliminary evidence for an interaction with immunoglobulin genes Dis Markers 1986, 4:139-144 3482986
49. Yu X Bauer K Wernhoff P Koczan D Moller S Thiesen HJ Ibrahim SM Fine mapping of collagen-induced arthritis quantitative trait loci in an advanced intercross line J Immunol 2006, 177:7042-7049 17082620
50. Brugmans L Kanaar R Essers J Analysis of DNA double-strand break repair pathways in mice Mutat Res 2007, 614:95-108 16797606
51. D'Avirro N Truong D Luong M Kanaar R Selsing E Gene conversion-like sequence transfers between transgenic antibody V genes are independent of RAD54 J Immunol 2002, 169:3069-3075 12218123
52. Arranz A Gutiérrez-Cañas I Carrión M Juarranz Y Pablos JL Martínez C Gomariz RP VIP reverses the expression profiling of TLR4-stimulated signaling pathway in rheumatoid arthritis synovial fibroblasts Mol Immunol 2008, 45:3065-3073 10.1016/ j.molimm.2008.03.011 18452992
53. Ahmad R Sylvester J Zafarullah M MyD88, IRAK1 and TRAF6 knockdown in human chondrocytes inhibits interleukin-1-induced matrix metalloproteinase-13 gene expression and promoter activity by impairing MAP kinase activation Cell Signal 2007, 19:2549-2557 10.1016/ j.cellsig.2007.08.013 17905570
54. Cho ML Ju JH Kim HR Oh HJ Kang CM Jhun JY Lee SY Park MK Min JK Park SH Lee SH Kim HY Toll-like receptor 2 ligand mediates the upregulation of angiogenic factor, vascular endothelial growth factor and interleukin-8/ CXCL8 in human rheumatoid synovial fibroblasts Immunol Lett 2007, 108:121-128 10.1016/j.imlet.2006.11.005 17182109
55. Tanaka Y Bi K Kitamura R Hong S Altman Y Matsumoto A Tabata H Lebedeva S Bushway PJ Altman A SWAP-70-like adapter of T cells, an adapter protein that regulates early TCR-initiated signaling in Th2 lineage cells Immunity 2003, 18:403-414 10.1016/S1074-7613(03)00054-2 12648457
56. Mavrakis KJ McKinlay KJ Jones P Sablitzky F DEF6, a novel PH-DH-like domain protein, is an upstream activator of the Rho GTPases Rac1, Cdc42, and RhoA Exp Cell Res 2004, 294:335-344 10.1016/j.yexcr.2003.12.004 15023524
57. Gupta S Fanzo JC Hu C Cox D Jang SY Lee AE Greenberg S Pernis AB T cell receptor engagement leads to the recruitment of IBP, a novel guanine nucleotide exchange factor, to the immunological synapse J Biol Chem 2003, 278:43541-43549 10.1074/jbc.M308960200 12923183
58. Gupta S Lee A Hu C Fanzo J Goldberg I Cattoretti G Pernis AB Molecular cloning of IBP, a SWAP-70 homologous GEF, which is highly expressed in the immune system Hum Immunol 2003, 64:389-401 10.1016/ S0198-8859(03)00024-7 12651066
59. Bo GP Zhou LN He WF Luo GX Jia XF Gan CJ Chen GX Fang YF Larsen PM Wu J Analyses of differential proteome of human synovial fibroblasts obtained from arthritis Clin Rheumatol 2009, 28:191-199 10.1007/s10067-008-1013-y 18807103
60. Ainola M Li TF Mandelin J Hukkanen M Choi SJ Salo J Konttinen YT Involvement of a disintegrin and a metalloproteinase 8 (ADAM8) in osteoclastogenesis and pathological bone destruction Ann Rheum Dis 2009, 68:427-434 10.1136/ard.2008.088260 18397961
61. Gómez-Gaviro M Domínguez-Luis M Canchado J Calafat J Janssen H Lara-Pezzi E Fourie A Tugores A Valenzuela-Fernández A Mollinedo F Sánchez-Madrid F Díaz-González F Expression and regulation of the metalloproteinase ADAM-8 during human neutrophil pathophysiological activation and its catalytic activity on L-selectin shedding J Immunol 2007, 178:8053-8063 17548643
62. Weskamp G Ford JW Sturgill J Martin S Docherty AJ Swendeman S Broadway N Hartmann D Saftig P Umland S Sehara-Fujisawa A Black RA Ludwig A Becherer JD Conrad DH Blobel CP ADAM10 is a principal 'sheddase' of the low-affinity immunoglobulin E receptor CD23 Nat Immunol 2006, 7:1293-1298 10.1038/ni1399 17072319
63. Mandelin J Li TF Hukkanen MV Liljestrom M Chen ZK Santavirta S Kitti U Konttinen YT Increased expression of a novel osteoclast-stimulating factor, ADAM8, in interface tissue around loosened hip prostheses J Rheumatol 2003, 30:2033-2038 12966612
64. Corn RA Hunter C Liou HC Siebenlist U Boothby MR Opposing roles for RelB and Bcl-3 in regulation of T-box expressed in T cells, GATA-3, and Th effector differentiation J Immunol 2005, 175:2102-2110 16081776
65. Oda T Kujovich J Reis M Newman B Druker BJ Identification and characterization of two novel SH2 domain-containing proteins from a yeast two hybrid screen with the ABL tyrosine kinase Oncogene 1997, 15:1255-1262 10.1038/sj.onc.1201299 9315092
66. Adarichev VA Bardos T Christodoulou S Phillips MT Mikecz K Glant TT Major histocompatibility complex controls susceptibility and dominant inheritance, but not the severity of the disease in mouse models of rheumatoid arthritis Immunogenetics 2002, 54:184-192 10.1007/ s00251-002-0462-8 12073147
67. Broek van den MF Berg van den WB Putte van de LBA Severijnen AJ Streptococcal cell wall-induced arthritis and flare-up reaction in mice induced by homologous or heterologous cell walls Am J Pathol 1988, 133:139-149 1880648 3052092
68. Potter M The BALB/c Mouse: Genetics and Immunology (Current Topics in Microbiology and Immunology) Berlin: Springer-Verlag 1985
69. Köhler G Milstein C Continuous cultures of fused cells secreting antibody of predefined specificity Nature 1975, 256:495-497 10.1038/ 256495a0 1172191
70. Adarichev VA Glant TT Experimental spondyloarthropathies: Animal models of ankylosing spondylitis Curr Rheumatol Rep 2006, 8:267-274 10.1007/ s11926-006-0007-5 16839505
71. Festing MF Inbred strains of mice Mouse Genome 1996, 94:523-677
72. Staats J The laboratory mouse Biology of the Laboratory Mouse New York: McGraw-Hill Green EL 1966:1-9
73. Braun J Bollow M Sieper J Radiologic diagnosis and pathology of the spondyloarthropathies Rheum Dis Clin North Am 1998, 24:697-735 10.1016/ S0889-857X(05)70038-7 9891707
74. Buzas E Vegvari A Murad YM Finnegan A Mikecz K Glant TT T-cell recognition of differentially tolerated epitopes of cartilage proteoglycan aggrecan in arthritis Cell Immunol 2005, 235:98-108 10.1016/ j.cellimm.2004.08.006 16185673
75. Glant TT Buzas EI Finnegan A Negroiu G Cs-Szabó G Mikecz K Critical role of glycosaminoglycan side chains of cartilage proteoglycan (aggrecan) in antigen recognition and presentation J Immunol 1998, 160:3812-3819 9558085
76. Hanyecz A Bardos T Berlo SE Buzas EI Nesterovitch AB Mikecz K Glant TT Induction of arthritis in SCID mice by T cells specific for the 'shared epitope' sequence in the G3 domain of human cartilage proteoglycan Arthritis Rheum 2003, 48:2959-2973 10.1002/art.11275 14558103
77. Szanto S Bárdos T Szabo Z David CS Buzás E Mikecz K Glant TT Induction of arthritis in HLA-DR4-humanized and HLA-DQ8-humanized mice by human cartilage proteoglycan aggrecan but only in the presence of an appropriate (non-MHC) genetic background Arthritis Rheum 2004, 50:1984-1995 10.1002/art.20285 15188376
78. Zhang Y Guerassimov A Leroux J-Y Cartman A Webber C Lalic R de Miguel E Rosenberg LC Poole AR Arthritis induced by proteoglycan aggrecan G1 domain in BALB/c mice. Evidence for T cell involvement and the immunosuppressive influence of keratan sulfate on recognition of T and B cell epitopes J Clin Invest 1998, 101:1678-1686 508749 9541498 10.1172/ JCI1666
79. Lipson SJ Muir H Vertebral osteophyte formation in experimental disc degeneration. Morphologic and proteoglycan changes over time Arthritis Rheum 1980, 23:319-324 10.1002/art.1780230309 7362683
80. Mahowald ML Krug H Taurog J Progressive ankylosis in mice. An animal model of spondylarthropathy. I. Clinical and radiographic findings Arthritis Rheum 1988, 31:1390-1399 10.1002/art.1780311108 3190783
81. Moskowitz RW Ziv I Denko CW Boja B Jones PK Adler JH Spondylosis in sand rats: A model of intervertebral disc degeneration and hyperostosis J Orthop Res 1990, 8:401-411 10.1002/jor.1100080312 2182801
82. Fry TR Eurell JC Johnson AL Brown MD Losonsky JM Schaeffer DJ Radiographic and histologic effects of chondroitinase ABC on normal canine lumbar intervertebral disc Spine 1991, 16:816-819 10.1097/ 00007632-199107000-00022 1925759
83. Hammer RE Maika SD Richardson JA Tang JP Taurog JD Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human b2m: An animal model of HLA-B27-associated human disorders Cell 1990, 63:1099-1112 10.1016/0092-8674(90)90512-D 2257626
84. Khare SD Luthra HS David CS Spontaneous inflammatory arthritis in HLA-B27 transgenic mice lacking b2-microglobulin: A model of human spondyloarthropathies J Exp Med 1995, 182:1153-1158 2192301 7561688 10.1084/jem.182.4.1153
85. Taurog JD Maika SD Satumtira N Dorris ML McLean IL Yanagisawa H Sayad A Stagg AJ Fox GM Lê O'Brien A Rehman M Zhou M Weiner AL Splawski JB Richardson JA Hammer RE Inflammatory disease in HLA-B27 transgenic rats Immunol Rev 1999, 169:209-223 10.1111/j.1600-065X.1999.tb01317.x 10450519
86. Weyand CM Goronzy JJ Takemura S Kurtin PJ Cell-cell interactions in synovitis. Interactions between T cells and B cells in rheumatoid arthritis Arthritis Res 2000, 2:457-463 128875 11094459 10.1186/ar128
87. Boldizsar F Tarjanyi O Farkas B Mikecz K Glant TT Th1 and Th17 cells dominate in the peritoneal cavity of BALB/c mice during the initiation phase of proteoglycan-induced arthritis (PGIA) Arthritis Rheum 2008, 58:S842-S843
88. Nilsson UR Muller-Eberhard HJ Deficiency of the fifth component of complement in mice with an inherited complement defect J Exp Med 1967, 125:1-16 2138349 4959665 10.1084/jem.125.1.1
89. Ooi YM Colten HR Genetic defect in secretion of complement C5 in mice Nature 1979, 282:207-208 10.1038/282207a0 492335
90. Moeller GR Terry L Snyderman R The inflammatory response and resistance to endotoxin in mice J Immunol 1978, 120:116-123 627714
91. Green MC Shultz LD Motheaten, an immunodeficient mutant of the mouse. I. Genetics and pathology J Hered 1975, 66:250-258 1184950
92. Shultz LD Schweitzer PA Rajan TV Yi T Ihle JN Matthews RJ Thomas ML Beier DR Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene Cell 1993, 73:1445-1454 10.1016/0092-8674(93)90369-2 8324828