The role and clinical implications of G6PI in experimental models of rheumatoid arthritis

Arthritis Research and Therapy

Volumn 7, Issue 1, 2005, Pages 20-28

  Kamradt, Thomas ^a,b   Schubert, David ^b  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

Author keywords

Arthritis; CD4+ lymphocytes; DBA l mice; FC receptors; Glucose 6 phosphate isomerase

Indexed keywords

AUTOANTIBODY; AUTOANTIBODY JO 1; AUTOANTIGEN; CD4 ANTIGEN; COLLAGEN TYPE 11; COLLAGEN TYPE 2; GLUCOSE 6 PHOSPHATE ISOMERASE; GLYCOLYTIC ENZYME; HLA DR ANTIGEN; IMMUNOGLOBULIN G1 ANTIBODY; INTERLEUKIN 1; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOCHONDRION ANTIBODY; MONOCYTE CHEMOTACTIC PROTEIN; MYELOBLASTIN; OKT 4; PROTEIN KINASE ZAP 70; PROTEIN SH2; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; BACTERIAL CELL WALL; CELLULAR IMMUNITY; EXPERIMENTAL MODEL; HELPER CELL; HISTOPATHOLOGY; IMMUNOREACTIVITY; MAST CELL; MOUSE; MOUSE STRAIN; NEURITIS; NEUTROPHIL; NONHUMAN; POLYARTHRITIS; PROTEIN EXPRESSION; REVIEW; RHEUMATOID ARTHRITIS; STREPTOCOCCUS; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; ANTIBODY SPECIFICITY; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; AUTOANTIBODIES; AUTOANTIGENS; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CELL WALL; COLLAGEN TYPE II; COMPLEMENT SYSTEM PROTEINS; CROSSES, GENETIC; GLUCOSE-6-PHOSPHATE ISOMERASE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNIZATION; IMMUNIZATION, PASSIVE; IMMUNOGLOBULIN G; INTERLEUKIN-1; MAST CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, INBRED NOD; MICE, TRANSGENIC; NERVOUS SYSTEM AUTOIMMUNE DISEASE, EXPERIMENTAL; NEUTROPHILS; RECEPTORS, ANTIGEN, T-CELL;

EID: 13444252643     PISSN: 14786354     EISSN: None     Source Type: Journal    
DOI: 10.1186/ar1476     Document Type: Review

References (106)

1. Zvaifler NJ: The immunopathology of joint inflammation in rheumatoid arthritis. Adv Immunol 1973, 16:265-336.
2. Van Boxel JA, Paget SA: Predominantly T cell infiltrate in rheumatoid synovial membranes. N Engl J Med 1975, 293: 517-520.
3. Firestein GS, Zvaifler NJ: How important are T cells in chronic rheumatoid synovitis. Arthritis Rheum 1990, 33: 68-773.
4. Smolen JS, Steiner G: Rheumatoid arthritis is more than cytokines: autoimmunity and rheumatoid arthritis. Arthritis Rheum 2001, 44:2218-2220.
5. Steiner G, Smolen J: Autoantibodies in rheumatoid arthritis and their clinical significance. Arthritis Res 2002, Suppl 2:S1-S5.
6. Firestein GS, Zvaifler NJ: How important are T cells in chronic rheumatoid synovitis?: II. T cell-independent mechanisms from beginning to end. Arthritis Rheum 2002, 46:298-308.
7. Feldmann M: Development of anti-TNF therapy for rheumatoid arthritis. Nat Rev Immunol 2002, 2:364-371.
8. Dorner T, Egerer K, Feist E, Burmester GR: Rheumatoid factor revisited. Curr Opin Rheumatol 2004, 16:246-253.
9. Gregersen PK, Silver J, Winchester RJ: The shared epitope hypothesis: an approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum 1987, 30:1205-1213.
10. Winchester R: The molecular basis of susceptibility to rheumatoid arthritis. Adv Immunol 1994, 56:389-466.
11. Hammer J, Gallazi F, Bono E, Karr RW, Guenot J, Valsasnini P, Nagy ZA, Sinigaglia F: Peptide binding specificity of HLA-DR4 molecules: correlation with rheumatoid arthritis association. J Exp Med 1995, 181:1847-1855.
12. Buckner JH, Nepom GT: Genetics of rheumatoid arthritis: is there a scientific explanation for the human leukocyte antigen association? Curr Opin Rheumatol 2002, 14:254-259.
13. Nepom GT: Major histocompatibility complex-directed susceptibility to rheumatoid arthritis. Adv Immunol 1998, 68: 15-332.
14. Berg L, Ronnelid J, Sanjeevi CB, Lampa J, Klareskog L: Interferon-gamma production in response to in vitro stimulation with collagen type II in rheumatoid arthritis is associated with HLA-DRB1(*)0401 and HLA-DQ8. Arthritis Res 2000, 2:75-84.
15. Kotzin BL, Falta MT, Crawford F, Rosloniec EF, Bill J, Marrack P, Kappler J: Use of soluble peptide-DR4 tetramers to detect synovial T cells specific for cartilage antigens in patients with rheumatoid arthritis. Proc Natl Acad Sci USA 2000, 97: 91-296.
16. Bennett SR, Falta MT, Bill J, Kotzin BL: Antigen-specific T cells in rheumatoid arthritis. Curr Rheumatol Rep 2003, 5: 55-263.
17. Horneff G, Burmester GR, Emmrich F, Kalden JR: Treatment of rheumatoid arthritis with an anti-CD4 monoclonal antibody. Arthritis Rheum 1991, 34:129-140.
18. Trentham DE, Dynesius-Trentham RA, Orav EJ, Combitchi D, Lorenzo C, Sewell KL, Hafler DA, Weiner HL: Effects of oral administration of type II collagen on rheumatoid arthritis. Science 1993, 261:1727-1730.
19. Sieper J, Kary S, Sorensen H, Alten R, Eggens U, Huge W, Hiepe F, Kuhne A, Listing J, Ulbrich N, et al.: Oral type II collagen treatment in early rheumatoid arthritis. A double-blind, placebo-controlled, randomized trial. Arthritis Rheum 1996, 39:41-51.
20. Kalden JR, Sieper J: Oral collagen in the treatment of rheumatoid arthritis. Arthritis Rheum 1998, 41:191-194.
21. Kalden JR, Breedveld FC, Burkhardt H, Burmester GR: Immunological treatment of autoimmune diseases. Adv Immunol 1998, 68:333-361.
22. Kamradt T, Mitchison NA: Tolerance and autoimmunity. N Engl J Med 2001, 344:655-664.
23. Elliott MJ, Maini RN, Feldmann M, Kalden JR, Antoni C, Smolen JS, Leeb B, Breedveld FC, Macfarlane JD, Bijl H, et ai.: Randomised double-blind comparison of chimeric monoclonal antibody to tumour necrosis factor alpha (cA2) versus placebo in rheumatoid arthritis. Lancet 1994, 344:1105-1110.
24. Kremer JM, Westhovens R, Leon M, Di Giorgio E, Alten R, Steinfeld S, Russell A, Dougados M, Emery P, Nuamah IF, et al.: Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med 2003, 349:1907-1915.
25. Sakaguchi N, Takahashi T, Hata H, Nomura T, Tagami T, Yamazaki S, Sakihama T, Matsutani T, Negishi I, Nakatsuru 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: 54-460.
26. Arce S, Cassese G, Hauser A, Dorner T, Odendahl M, Manz R, Radbruch A, Hiepe F: The role of long-lived plasma cells in autoimmunity. Immunobiology 2002, 206:558-562.
27. Dorner T, Burmester GR: The role of B cells in rheumatoid arthritis: mechanisms and therapeutic targets. Curr Opin Rheumatol 2003, 15:246-252.
28. Edwards JC, Szczepanski L, Szechinski J, Filipowicz-Sosnowska A, Emery P, Close DR, Stevens RM, Shaw T: Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004, 350:2572-2581.
29. 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: 7-93.
30. van Gaalen FA, Linn-Rasker SP, van Venrooij WJ, de Jong BA, Breedveld FC, Verweij CL, Toes RE, Huizinga TW: Autoantibodies to cyclic citrullinated peptides predict progression to rheumatoid arthritis in patients with undifferentiated arthritis: a prospective cohort study. Arthritis Rheum 2004, 50:709-715.
31. Goldbach-Mansky R, Lee J, McCoy A, Hoxworth J, Yarboro C, Smolen JS, Steiner G, Rosen A, Zhang C, Menard HA, et al.: Rheumatoid arthritis associated autoantibodies in patients with synovitis of recent onset. Arthritis Res 2000, 2:236-243.
32. Corrigall VM, Panayi GS: Autoantigens and immune pathways in rheumatoid arthritis. Crit Rev Immunol 2002, 22: 81-293.
33. Wooley PH, Luthra HS, O'Duffy JD, Bunch TW, Moore SB, Stuart JM: Anti-type II collagen antibodies in rheumatoid arthritis. The influence of HLA phenotype. Tissue Antigens 1984, 23: 263-269.
34. Ronnelid J, Lysholm J, Engstrom-Laurent A, Klareskog L, Heyman B: Local anti-type II collagen antibody production in rheumatoid arthritis synovial fluid. Evidence for an HLA-DR4-restricted IgG response. Arthritis Rheum 1994, 37:1023-1029.
35. Backlund J, Carlsen S, Hoger T, Holm B, Fugger L, Kihlberg J, Burkhardt H, Holmdahl R: Predominant selection of T cells specific for the glycosylated collagen type II epitope (263-270) in humanized transgenic mice and in rheumatoid arthritis. Proc Natl Acad Sci USA 2002, 99:9960-9965.
36. Holmdahl R, Andersson M, Goldschmidt TJ, Gustafsson K, Jansson L, Mo JA: Type II collagen autoimmunity in animals and provocations leading to arthritis. Immunol Rev 1990, 118: 193-232.
37. Jirholt J, Lindqvist AB, Holmdahl R: The genetics of rheumatoid arthritis and the need for animal models to find and understand the underlying genes. Arthritis Res 2001, 3: 7-97.
38. Stuart JM, Dixon FJ: Serum transfer of collagen-induced arthritis in mice. J Exp Med 1983, 158:378-392.
39. Watson WC, Brown PS, Pitcock JA, Townes AS: Passive transfer studies with type II collagen antibody in B10.D2/old and new line and C57BI/6 normal and beige (Chediak-Higashi) strains: evidence of important roles for C5 and multiple inflammatory cell types in the development of erosive arthritis. Arthritis Rheum 1987, 30: 60-465.
40. Holmdahl R, Jansson L, Larsson A, Jonsson R: Arthritis in DBA/1 mice induced with passively transferred collagen type II immune serum. Immunohistopathology and serum levels of anti-type II collagen autoantibodies. Scand J Immunol 1990, 31:147-157.
41. Terato K, Hasty KA, Reife RA, Cremer MA, Kang AH, Stuart JM: Induction of arthritis with monoclonal antibodies to collagen. J Immunol 1992, 148:2103-2108.
42. Nandakumar KS, Svensson L, Holmdahl R: Collagen type II-specific monoclonal antibody-induced arthritis in mice: description of the disease and the influence of age, sex, and genes. Am J Pathol 2003, 163:1827-1837.
43. Tarkowski A, Klareskog L, Carlsten H, Herberts P, Koopman WJ: Secretion of antibodies to types I and II collagen by synovial tissue cells in patients with rheumatoid arthritis. Arthritis Rheum 1989, 32:1087-1092.
44. Cook AD, Rowley MJ, Mackay IR, Gough A, Emery P: Antibodies to type II collagen in early rheumatoid arthritis. Correlation with disease progression. Arthritis Rheum 1996, 39: 720-1727.
45. Svendsen P, Andersen CB, Willcox N, Coyle AJ, Holmdahl R, Kamradt T, Fugger L: Tracking of proinflammatory collagen-specific T cells in early and late collagen-induced arthritis in humanized mice. J Immunol 2004, 173:7037-7045.
46. Taurog JD, Kerwar SS, McReynolds RA, Sandberg GP, Leary SL, Mahowald ML: Synergy between adjuvant arthritis and collagen-induced arthritis in rats. J Exp Med 1985, 162:962-978.
47. + T cells play a role in initiation and regulate recovery phase of collagen-induced arthritis. J Immunol 1996, 156:4520-4526.
48. Plows D, Kontogeorgos G, Kollias G: Mice lacking mature T and B lymphocytes develop arthritic lesions after immunization with type II collagen. J Immunol 1999, 162:1018-1023.
49. Londei M, Savill CM, Verhoef A, Brennan F, Leech ZA, Duance V, Maini RN, Feldmann M: Persistence of collagen type II-specific T-cell clones in the synovial membrane of a patient with rheumatoid arthritis. Proc Natl Acad Sci USA 1989, 86:636-640.
50. Snowden N, Reynolds I, Morgan K, Holt L: T cell responses to human type II collagen in patients with rheumatoid arthritis and healthy controls. Arthritis Rheum 1997, 40:1210-1218.
51. Kim HY, Kim WU, Cho ML, Lee SK, Youn J, Kim SI, Yoo WH, Park JH, Min JK, Lee SH, et al.: Enhanced T cell proliferative response to type II collagen and synthetic peptide CII (255-274) in patients with rheumatoid arthritis. Arthritis Rheum 1999, 42: 085-2093.
52. McKown KM, Carbone LD, Kaplan SB, Aelion JA, Lohr KM, Cremer MA, Bustillo J, Gonzalez M, Kaeley G, Steere EL, et al.: Lack of efficacy of oral bovine type II collagen added to existing therapy in rheumatoid arthritis. Arthritis Rheum 1999, 42: 1204-1208.
53. Cremer MA, Ye XJ, Terato K, Owens SW, Seyer JM, Kang AH: Type XI collagen-induced arthritis in the Lewis rat. Characterization of cellular and humoral immune responses to native types XI, V, and II collagen and constituent alpha-chains. J Immunol 1994, 153: 24-832.
54. Cope AP, Patel SD, Hall F, Congia M, Hubers HA, Verheijden GF, Boots AM, Menon R, Trucco M, Rijnders AW, et al.: T cell responses to a human cartilage autoantigen in the context of rheumatoid arthritis-associated and nonassociated HLA-DR4 alleles. Arthritis Rheum 1999, 42:1497-1507.
55. Carlsen S, Hansson AS, Olsson H, Heinegard D, Holmdahl R: Cartilage oligomeric matrix protein (COMP)-induced arthritis in rats. Clin Exp Immunol 1998, 114:477-484.
56. Glant TT, Finnegan A, Mikecz K: Proteoglycan-induced arthritis: immune regulation, cellular mechanisms, and genetics. Crit Rev Immunol 2003, 23:199-250.
57. Pearson CM: Development of arthritis, periarthritis, and periostitis in rats given adjuvants. Proc Soc Exp Biol Med 1956, 91:95-101.
58. van Eden W, Thole JE, van der Zee R, Noordzij A, van Embden JD, Hensen EJ, Cohen IR: Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature 1988, 331:171-173.
59. 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.
60. Deng GM, Nilsson IM, Verdrengh M, Collins LV, Tarkowski A: Intra-articularly localized bacterial DNA containing CpG motifs induces arthritis. Nat Med 1999, 5:702-705.
61. Kimpel D, Dayton T, Kannan K, Wolf RE: Streptococcal cell wall arthritis: kinetics of immune cell activation in inflammatory arthritis. Clin Immunol 2002, 105:351-362.
62. van den Berg WB, van de Putte LB, Zwarts WA, Joosten LA: Electrical charge of the antigen determines intraarticular antigen handling and chronicity of arthritis in mice. J Clin Invest 1984, 74:1850-1859.
63. von Banchet GS, Petrow PK, Brauer R, Schaible HG: Monoarticular antigen-induced arthritis leads to pronounced bilateral upregulation of the expression of neurokinin 1 and bradykinin 2 receptors in dorsal root ganglion neurons of rats. Arthritis Res 2000, 2:424-427.
64. Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D: Organ-specific disease provoked by systemic autoimmunity. Cell 1996, 87:811-822.
65. Korganow AS, Ji H, Mangialaio S, Duchatelle V, Pelanda R, Martin T, Degott C, Kikutani H, Rajewsky K, Pasquali JL, et al.: From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity 1999, 10:451-461.
66. Matsumoto I, Staub A, Benoist C, Mathis D: Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme. Science 1999, 286:1732-1735.
67. Gracy RW, Tilley BE: Phosphoglucose isomerase of human erythrocytes and cardiac tissue. Methods Enzymol 1975, 41: 392-400.
68. West JD, Flockhart JH, Peters J, Ball ST: Death of mouse embryos that lack a functional gene for glucose phosphate isomerase. Genet Res 1990, 56:223-236.
69. Maccioni M, Zeder-Lutz G, Huang H, Ebel C, Gerber P, Hergueux J, Marchal P, Duchatelle V, Degott C, van Regenmortel M, et al.: Arthritogenic monoclonal antibodies from K/BxN mice. J Exp Med 2002, 195:1071-1077.
70. Ji H, Ohmura K, Mahmood U, Lee DM, Hofhuis FM, Boackle SA, Takahashi K, Holers VM, Walport M, Gerard C, et al.: Arthritis critically dependent on innate immune system players. Immunity 2002, 16:157-168.
71. Ji H, Gauguier D, Ohmura K, Gonzalez A, Duchatelle V, Danoy P, Garchon HJ, Degott C, Lathrop M, Benoist C, et al.: Genetic influences on the end-stage effector phase of arthritis. J Exp Med 2001, 194:321-330.
72. Corr M, Crain B: The role of FcgammaR signaling in the K/B x N serum transfer model of arthritis. J Immunol 2002, 169: 6604-6609.
73. Wipke BT, Allen PM: Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 2001, 167:1601-1608.
74. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB: Mast cells: a cellular link between autoantibodies and inflammatory arthritis. Science 2002, 297:1689-1692.
75. Kyburz D, Carson D, Corr M: The role of CD40 ligand and tumor necrosis factor alpha signaling in the transgenic K/BxN mouse model of rheumatoid arthritis. Arthritis Rheum 2000, 43: 571-2577.
76. Ji H, Pettit A, Ohmura K, Ortiz-Lopez A, Duchatelle V, Degott C, Gravallese E, Mathis D, Benoist C: Critical roles for interleukin 1 and tumor necrosis factor alpha in antibody-induced arthritis. J Exp Med 2002, 196:77-85.
77. Alonzi T, Fattori E, Lazzaro D, Costa P, Probert L, Kollias G, De Benedetti F, Poli V, Ciliberto G: Interleukin 6 is required for the development of collagen-induced arthritis. J Exp Med 1998, 187:461-468.
78. + T regulatory cells. J Exp Med 2004, 199: 23-335.
79. Schaller M, Burton DR, Ditzel HJ: Autoantibodies to GPI in rheumatoid arthritis: linkage between an animal model and human disease. Nat Immunol 2001, 2:746-753.
80. Kassahn D, Kolb C, Solomon S, Bochtler P, Illges H: Few human autoimmune sera detect GPI [letter]. Nat Immunol 2002, 3:411-412.
81. Schubert D, Schmidt M, Zaiss D, Jungblut PR, Kamradt T: Autoantibodies against GPI and creatine kinase in rheumatoid arthritis [letter]. Nat Immunol 2002, 3:411.
82. Herve CA, Wait R, Venables PJ: Glucose-6-phosphate isomerase is not a specific autoantigen in rheumatoid arthritis. Rheumatology (Oxford) 2003, 8:986-988.
83. Matsumoto I, Lee DM, Goldbach-Mansky R, Sumida T, Hitchon CA, Schur PH, Anderson RJ, Coblyn JS, Weinblatt ME, Brenner M, 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, 48:944-954.
84. Schmitt A, Schubert D, Sengler C, Kamradt T: Autoantibodies against glucose-6-phosphate-isomerase are not a diagnostic marker for juvenile idiopathic arthritis [letter]. Ann Rheum Dis 2004, 63:463.
85. van Gaalen FA, Toes REM, Ditzel HJ, Schaller M, Breedveld FC, Verweij CL, Huizinga TWJ: Association of autoantibodies to glucose-6-phosphate isomerase with extraarticular complications in rheumatoid arthritis. Arthritis Rheum 2004, 50:395-399.
86. Cha H-S, Kim TJ, Kim J-Y, Lee M-H, Jeon CH, Kim J, Bae E-K, Ahn K-S, Koh E-M: Autoantibodies to glucose-6-phosphate isomerase are elevated in the synovial fluid of rheumatoid arthritis patients. Scand J Rheumatol 2004, 33:179-184.
87. Oono T, Fukui Y, Masuko S, Hashimoto O, Ueno T, Sanui T, Inayoshi A, Noda M, Sata M, Sasazuki T: Organ-specific autoimmunity in mice whose T cell repertoire is shaped by a single antigenic peptide. J Clin Invest 2001, 108:1589-1596.
88. Mathews MB, Bernstein RM: Myositis autoantibody inhibits histidyl-tRNA synthetase: a model for autoimmunity. Nature 1983, 304:177-179.
89. Feist E, Dorner T, Kuckelkorn U, Schmidtke G, Micheel B, Hiepe F, Burmester GR, Kloetzel PM: Proteasome alpha-type subunit C9 is a primary target of autoantibodies in sera of patients with myositis and systemic lupus erythematosus. J Exp Med 1996, 184: 313-1318.
90. Plotz PH: The autoantibody repertoire: searching for order. Nat Rev Immunol 2003, 3:73-78.
91. Kaplan MM: Primary biliary cirrhosis. N Engl J Med 1996, 335: 1570-1580.
92. van der Geld YM, Limburg PC, Kallenberg CG: Proteinase 3, Wegener's autoantigen: from gene to antigen. J Leukoc Biol 2001, 69:177-190.
93. Schubert D, Maier B, Morawietz L, Krenn V, Kamradt T: Immunization with glucose-6-phosphate isomerase induces T-cell dependent peripheral polyarthritis in genetically unaltered mice. J Immunol 2004, 172:4503-4509.
94. Mandik-Nayak L, Wipke BT, Shih FF, Unanue ER, Allen PM: Despite ubiquitous autoantigen expression, arthritogenic autoantibody response initiates in the local lymph node. Proc Natl Acad Sci USA 2002, 99:14368-14373.
95. 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, 3:366-372.
96. 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, 172:7694-7702.
97. Gondolf KB, Mihatsch M, Curschellas M, Dunn JJ, Batsford SR: Induction of experimental allergic arthritis with outer surface proteins of Borrelia burgdorferi. Arthritis Rheum 1994, 37: 1070-1077.
98. Matsumoto I, Maccioni M, Lee DM, Maurice M, Simmons B, Brenner M, Mathis D, Benoist C: How antibodies to a ubiquitous cytoplasmic enzyme may provoke joint-specific autoimmune disease. Nat Immunol 2002, 3:360-365.
99. Jeffery CJ: Moonlighting proteins. Trends Biochem Sci 1999, 24:8-11.
100. Gurney ME, Heinrich SP, Lee MR, Yin HS: Molecular cloning and expression of neuroleukin, a neurotrophic factor for spinal and sensory neurons. Science 1986, 234:566-574.
101. Chaput M, Claes V, Portetelle D, Cludts I, Cravador A, Burny A, Gras H, Tartar A: The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 1988, 332: 54-455.
102. Liotta LA, Mandler R, Murano G, Katz DA, Gordon RK, Chiang PK, Schiffmann E: Tumor cell autocrine motility factor. Proc Natl Acad Sci USA 1986, 83:3302-3306.
103. Silletti S, Raz A: Regulation of autocrine motility factor receptor expression in tumor cell locomotion and metastasis. Curr Top Microbiol Immunol 1996, 213:137-169.
104. Xu W, Seiter K, Feldman E, Ahmed T, Chiao JW: The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood 1996, 87:4502-4506.
105. Nabi IR, Raz A: Cell shape modulation alters glycosylation of a metastatic melanoma cell-surface antigen. Int J Cancer 1987, 40:396-402.
106. Fang S, Ferrone M, Yang C, Jensen JP, Tiwari S, Weissman AM: The tumor autocrine motility factor receptor, gp78, is a ubiquitin protein ligase implicated in degradation from the endoplasmatic reticulum. Proc Natl Acad Sci USA 2001, 98: 14422-14427.