Extracellular calreticulin is present in the joints of patients with rheumatoid arthritis and inhibits FasL (CD95L)-mediated apoptosis of T cells

Arthritis and Rheumatism

Volumn 62, Issue 10, 2010, Pages 2919-2929

  Tarr, Joanna M ^a   Winyard, Paul G ^a   Ryan, Brent ^a   Harries, Lorna W ^a   Haigh, Richard ^a   Viner, Nick ^a   Eggleton, Paul ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; FAS ANTIGEN; FAS LIGAND; LACTATE DEHYDROGENASE; NITRATE; NITRITE;

ADULT; AGED; APOPTOSIS; ARTICLE; CHEMOLUMINESCENCE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY SCORE 28; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME RELEASE; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PSORIATIC ARTHRITIS; QUANTITATIVE ANALYSIS; RHEUMATOID ARTHRITIS; SCORING SYSTEM; SYNOVIAL FLUID; T LYMPHOCYTE;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; ARTHRITIS, RHEUMATOID; CALRETICULIN; CASE-CONTROL STUDIES; FAS LIGAND PROTEIN; FEMALE; HUMANS; JURKAT CELLS; MALE; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; SYNOVIAL FLUID; T-LYMPHOCYTES;

EID: 77957682653     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.27602     Document Type: Article

References (51)

1. Salmon M, Scheel-Toellner D, Huissoon AP, Pilling D, Shamsadeen N, Hyde H, et al. Inhibition of T cell apoptosis in the rheumatoid synovium. J Clin Invest 1997;99:439-46. (Pubitemid 27414801)
2. Eguchi K. Apoptosis in autoimmune diseases. Intern Med 2001;40:275-84.
3. - T cells from rheumatoid arthritis patients. J Immunol 1998;161:1018-25.
4. Du F, Wang L, Zhang Y, Jiang W, Sheng H, Cao Q, et al. Role of GADD45β in the regulation of synovial fluid T cell apoptosis in rheumatoid arthritis. Clin Immunol 2008;128:238-47.
5. Sumida T, Hoa TT, Asahara H, Hasunuma T, Nishioka K. T cell receptor of Fas-sensitive T cells in rheumatoid synovium. J Immunol 1997;158:1965-70. (Pubitemid 127469557)
6. Zhang J, Bardos T, Mikecz K, Finnegan A, Glant TT. Impaired Fas signaling pathway is involved in defective T cell apoptosis in autoimmune murine arthritis. J Immunol 2001;166:4981-6. (Pubitemid 32280709)
7. Kawakami A, Eguchi K, Matsuoka N, Tsuboi M, Kawabe Y, Aoyagi T, et al. Inhibition of Fas antigen-mediated apoptosis of rheumatoid synovial cells in vitro by transforming growth factor β1. Arthritis Rheum 1996;39:1267-76. (Pubitemid 26270084)
8. Pundt N, Peters MA, Wunrau C, Strietholt S, Fehrmann C, Neugebauer K, et al. Susceptibility of rheumatoid arthritis synovial fibroblasts to FasL- and TRAIL-induced apoptosis is cell cycle-dependent. Arthritis Res Ther 2009;11:R16.
9. Johnson S, Michalak M, Opas M, Eggleton P. The ins and outs of calreticulin: from the ER lumen to the extracellular space. Trends Cell Biol 2001;11:122-9. (Pubitemid 32289442)
10. Duus K, Pagh RT, Holmskov U, Hojrup P, Skov S, Houen G. Interaction of calreticulin with CD40 ligand, TRAIL and Fas ligand. Scand J Immunol 2007;66:501-7.
11. Watanabe K, Ohira H, Orikasa H, Saito K, Kanno K, Shioya Y, et al. Anti-calreticulin antibodies in patients with inflammatory bowel disease. Fukushima J Med Sci 2006;52:1-11.
12. Eggleton P, Ward FJ, Johnson S, Khamashta MA, Hughes GR, Hajela VA, et al. Fine specificity of autoantibodies to calreticulin: epitope mapping and characterization. Clin Exp Immunol 2000;120:384-91.
13. Eggleton P, Llewellyn DH. Pathophysiological roles of calreticulin in autoimmune disease. Scand J Immunol 1999;49:466-73.
14. Goeb V, Thomas-L'Otellier M, Daveau R, Charlionet R, Fardellone P, Le Loet X, et al. Candidate autoantigens identified by mass spectrometry in early rheumatoid arthritis are chaperones and citrullinated glycolytic enzymes. Arthritis Res Ther 2009;11:R38.
15. Eggleton P, Lieu TS, Zappi EG, Sastry K, Coburn J, Zaner KS, et al. Calreticulin is released from activated neutrophils and binds to C1q and mannan-binding protein. Clin Immunol Immunopathol 1994;72:405-9.
16. Kovacs H, Campbell ID, Strong P, Johnson S, Ward FJ, Reid KB, et al. Evidence that C1q binds specifically to CH2-like immunoglobulin γ motifs present in the autoantigen calreticulin and interferes with complement activation. Biochemistry 1998;37:17865-74.
17. Ling S, Lai A, Borschukova O, Pumpens P, Holoshitz J. Activation of nitric oxide signaling by the rheumatoid arthritis shared epitope. Arthritis Rheum 2006;54:3423-32.
18. Ling S, Pi X, Holoshitz J. The rheumatoid arthritis shared epitope triggers innate immune signaling via cell surface calreticulin. J Immunol 2007;179:6359-67.
19. Patel JM, Li YD, Zhang J, Gelband CH, Raizada MK, Block ER. Increased expression of calreticulin is linked to ANG IV-mediated activation of lung endothelial NOS. Am J Physiol 1999;277:L794-801.
20. Tarr JM, Eggleton P, Winyard PG. Nitric oxide and the regulation of apoptosis in tumour cells. Curr Pharm Des 2006;12:4445-68.
21. Goicoechea S, Pallero MA, Eggleton P, Michalak M, Murphy-Ullrich JE. The anti-adhesive activity of thrombospondin is mediated by the N-terminal domain of cell surface calreticulin. J Biol Chem 2002;277:37219-28.
22. Honore C, Hummelshoj T, Hansen BE, Madsen HO, Eggleton P, Garred P. The innate immune component ficolin 3 (Hakata antigen) mediates the clearance of late apoptotic cells. Arthritis Rheum 2007;56:1598-607.
23. Young P, Szestakowska D, Morse R, Winyard PG, Whatmore J, Reid KB, et al. Purification, isolation and characterization of native and recombinant calreticulin. Calcium Binding Proteins 2006;1:160-9.
24. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988;31:315-24.
25. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7.
26. Moll JM, Wright V. Psoriatic arthritis. Semin Arthritis Rheum 1973;3:55-78.
27. Aguilar-Lemarroy A, Romero-Ramos JE, Olimon-Andalon V, Hernandez-Flores G, Lerma-Diaz JM, Ortiz-Lazareno PC, et al. Apoptosis induction in Jurkat cells and sCD95 levels in women's sera are related with the risk of developing cervical cancer. BMC Cancer 2008;8:99.
28. Knipp S, Feyen O, Ndagijimana J, Niehues T. Ex vivo apoptosis, CD95 and CD28 expression in T cells of children with juvenile idiopathic arthritis. Rheumatol Int 2003;23:112-5.
29. Kitani A, Nakashima N, Izumihara T, Inagaki M, Baoui X, Yu S, et al. Soluble VCAM-1 induces chemotaxis of Jurkat and synovial fluid T cells bearing high affinity very late antigen-4. J Immunol 1998;161:4931-8.
30. Peng SL. Fas (CD95)-related apoptosis and rheumatoid arthritis. Rheumatology (Oxford) 2006;45:26-30.
31. Higuchi K, Motomizu S. Flow-injection spectrophotometric determination of nitrite and nitrate in biological samples. Anal Sci 1999;15:129-34.
32. Bateman RM, Ellis CG, Freeman DJ. Optimization of nitric oxide chemiluminescence operating conditions for measurement of plasma nitrite and nitrate. Clin Chem 2002;48:570-3.
33. Prevoo ML, van 't Hof MA, Kuper HH, van Leeuwen MA, van de Putte LB, van Riel PL. Modified disease activity scores that include twenty-eight-joint counts: development and validation in a prospective longitudinal study of patients with rheumatoid arthritis. Arthritis Rheum 1995;38:44-8.
34. Rothman KJ. No adjustments are needed for multiple comparisons. Epidemiology 1990;1:43-6.
35. Kitas GD, Salmon M, Allan IM, Bacon PA. The T cell system in rheumatoid arthritis: activated or defective? Scand J Rheumatol Suppl 1988;76:161-73.
36. Peck A, Mellins ED. Breaking old paradigms: Th17 cells in autoimmune arthritis. Clin Immunol 2009;132:295-304.
37. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC, et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009;28:578-90.
38. Keller M, Ruegg A, Werner S, Beer HD. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008;132:818-31.
39. Tarr J, Young P, Morse R, Shaw D, Haigh R, Petrov P, et al. A mechanism of release of calreticulin from cells during oxidative stress and apoptosis. J Mol Biol 2010;401:799-812.
40. Visser K, van der Heijde DM. Risk and management of liver toxicity during methotrexate treatment in rheumatoid and psoriatic arthritis: a systematic review of the literature. Clin Exp Rheumatol 2009;27:1017-25.
41. Holoshitz J, Ling S. Nitric oxide signaling triggered by the rheumatoid arthritis shared epitope: a new paradigm for MHC disease association? Ann N Y Acad Sci 2007;1110:73-83.
42. Rocks SA, Davies CA, Hicks SL, Webb AJ, Klocke R, Timmins GS, et al. Measurement of S-nitrosothiols in extracellular fluids from healthy human volunteers and rheumatoid arthritis patients, using electron paramagnetic resonance spectrometry. Free Radic Biol Med 2005;39:937-48.
43. Ueki Y, Miyake S, Tominaga Y, Eguchi K. Increased nitric oxide levels in patients with rheumatoid arthritis. J Rheumatol 1996;23:230-6.
44. Choi JW. Nitric oxide production is increased in patients with rheumatoid arthritis but does not correlate with laboratory parameters of disease activity. Clin Chim Acta 2003;336:83-7.
45. Ersoy Y, Ozerol E, Baysal O, Temel I, MacWalter RS, Meral U, et al. Serum nitrate and nitrite levels in patients with rheumatoid arthritis, ankylosing spondylitis, and osteoarthritis. Ann Rheum Dis 2002;61:76-8.
46. Bryan NS, Grisham MB. Methods to detect nitric oxide and its metabolites in biological samples. Free Radic Biol Med 2007;43:645-57.
47. Ogden CA, deCathelineau A, Hoffmann PR, Bratton D, Ghebrehiwet B, Fadok VA, et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001;194:781-95.
48. Donnelly S, Roake W, Brown S, Young P, Naik H, Wordsworth P, et al. Impaired recognition of apoptotic neutrophils by the C1q/calreticulin and CD91 pathway in systemic lupus erythematosus. Arthritis Rheum 2006;54:1543-56.
49. Mountz JD, Hsu HC, Matsuki Y, Zhang HG. Apoptosis and rheumatoid arthritis: past, present, and future directions. Curr Rheumatol Rep 2001;3:70-8.
50. Pi X, Tan SY, Hayes M, Xiao L, Shayman JA, Ling S, et al. Sphingosine kinase 1-mediated inhibition of Fas death signaling in rheumatoid arthritis B lymphoblastoid cells. Arthritis Rheum 2006;54:754-64.
51. Firestein GS, Yeo M, Zvaifler NJ. Apoptosis in rheumatoid arthritis synovium. J Clin Invest 1995;96:1631-8.