Thymic Hassall's corpuscles, regulatory T-cells, and rheumatoid arthritis

Seminars in Arthritis and Rheumatism

Volumn 39, Issue 5, 2010, Pages 347-355

  Berthelot, Jean Marie ^a   le Goff, Benoît ^a   Maugars, Yves ^a  

^a NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Anti CCP; Hassall's; Regulatory T cells; Rheumatoid arthritis; Thymic B cells; Thymus

Indexed keywords

AUTOANTIGEN; CD4 ANTIGEN; CD59 ANTIGEN; DECAY ACCELERATING FACTOR; FILAGGRIN; GLYCOPROTEIN GP 39; IMMUNOGLOBULIN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7;

ANTIGEN EXPRESSION; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL AGING; CELL CLONING; CYTOPLASM; EPITHELIUM CELL; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; THIRD TRIMESTER PREGNANCY; THYMUS;

ARTHRITIS, RHEUMATOID; AUTOANTIGENS; EPITHELIAL CELLS; HUMANS; IMMUNOMODULATION; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 77949567845     PISSN: 00490172     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semarthrit.2008.08.010     Document Type: Review

References (94)

1. Watanabe N., Wang Y.H., Lee H.K., Ito T., Wang Y.H., Cao W., et al. Hassall's corpuscles instruct dendritic cells to induce CD4+CD25+ regulatory T cells in human thymus. Nature 2005, 436:1181-1185.
2. Bodey B., Kaiser H.E. Development of Hassall's bodies of the thymus in humans and other vertebrates (especially mammals) under physiological and pathologic conditions: immunocytochemical, electronmicrocopic and in vitro observations. In Vivo 1997, 11:61-85.
3. Bodey B., Bodey B., Siegel S.E., Kaiser H.E. Novel insights into the function of the thymic Hassall's bodies. In Vivo 2000, 14:407-418.
4. Hale L.P., Markert M.L. Corticosteroids regulate epithelial cell differentiation and hassall body formation in the human thymus. J Immunol 2004, 172:617-624.
5. Wong J., Obst R., Correia-Neves M., Lsyev G., Mathis D., Benoist C. Adaptation of TCR repertoires to self-peptides in regulatory and non-regulatory CD4+ T cells. J Immunol 2007, 178:7032-7041.
6. Rochman I., Watanabe N., Arima K., Liu Y.J., Leonard W.J. Cutting edge: direct action of thymic stromal lymphopoietin on activated human CD4+ T cells. J Immunol 2007, 178:6720-6724.
7. Aschenbrenner K., D'Cruz L.M., Vollmann E.H., Hinterberger M., Emmerich J., Swee L.K., et al. Selection of FoxP3 regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat Immunol 2007, 8:351-358.
8. Cope A.P., Schulze-Koops H., Aringer M. The central role of T cells in rheumatoid arthritis. Clin Exp Rheumatol 2007, 25(5 Suppl 46):S4-S11.
9. Fournier C. Where do T cells stand in rheumatoid arthritis?. Joint Bone Spine 2005, 72:527-532.
10. Mandik-Nayak L., Allen P.M. Initiation of an autoimmune response: insights from a transgenic model of rheumatoid arthritis. Immunol Res 2005, 32:5-13.
11. 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, 426:454-460.
12. Leipe J., Skapenko A., Lipsky P.E., Schulze-Koops H. Regulatory T cells in rheumatoid arthritis. Arthritis Res Ther 2005, 7:93-99.
13. Sakaguchi S., Ono M., Setoguchi R., Yagi H., Hori S., Fehervari Z., et al. Foxp3 CD25+CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006, 212:8-27.
14. Coutinho A., Caramalho I., Seixas E., Demengeot J. Thymic commitment of regulatory T cells is a pathway of TCR-dependent selection that isolates repertoires undergoing positive or negative selection. Curr Top Microbiol Immunol 2005, 293:43-71.
15. Pakravan N., Hassan A.T., Hassan Z.M. Naturally occurring self reactive CD4+CD25+ regulatory T cells: universal immune code. Cell Mol Immunol 2007, 4:197-201.
16. D'Cruz L.M., Klein L. Development and function of agonist-induced CD25+FoxP3+ regulatory T cells in the absence of interleukin 2 signaling. Nat Immunol 2005, 6:1152-1159.
17. Gavanescu I., Kessler B., Ploegh H., Benoist C., Mathis D. Loss of Aire-dependent thymic expression of a peripheral tissue antigen renders it a target of autoimmunity. Proc Natl Acad Sci USA 2007, 104:4583-4587.
18. Tuovinen H., Salminen J.T., Arstila T.P. Most human thymic and peripheral-blood CD4+CD25+ regulatory T cells express 2 T cell receptors. Blood 2006, 108:4063-4070.
19. Taub D.D., Longo D.L. Insights into thymic aging and regeneration. Immunol Rev 2005, 205:72-93.
20. Vukimanovic-Stejic M., Zhang Y., Cook J.E., Fletcher J.M., McQuaid A., Masters J.E., et al. Human CD4+CD25+hiHoxp3 regulatory T cells are derived by rapid turnover of memory populations in vivo. J Clin Invest 2006, 116:2423-2433.
21. Valmori D., Merlo A., Souleimanian N.E., Hesdorffer C.S., Ayyoub M. A peripheral circulating compartment of natural naive CD4+ Tregs. J Clin Invest 2005, 115:1953-1962.
22. Haas J., Fritzsching B., Trubswetter P., Korporal M., Milkova L., Fritz B., et al. Prevalence of newly generated naïve regulatory T cells (Treg) is critical for Treg suppressive function and determines Treg dysfunction in multiple sclerosis. J Immunol 2007, 179:1322-1330.
23. Cao D., van Vollenhoven R., Klareskog L., Trollmo C., Malmström V. CD25brightCD4+ regulatory T cells are enriched in inflamed joints of patients with chronic rheumatic disease. Arthritis Res Ther 2004, 6:R335-R346.
24. Van Amelsfort J.M., Noordegraaf M., Bijlsma J.W.J., Taams L.S., Lafeber F.P.J.G. Influence of the inflammatory milieu on the suppressive function of CD4+CD25+ T cells in rheumatoid arthritis. Arthritis Rheum 2004, 50:S526.
25. Ehrenstein M.R., Evans J.G., Singh A., Moore S., Warnes G., Isenberg D.A., et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med 2004, 200:277-285.
26. Nadkarni S., Mauri C., Ehrenstein M.R. Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med 2007, 204:33-39.
27. Wei S., Kryczek I., Zou W. Regulatory T-cell compartmentalization and trafficking. Blood 2006, 108:426-431.
28. Van Bilsen J.H., van Dongen H., Lard L.R., van der Voort E.L., Elferink D.G., Bakker A.M., et al. Functional regulatory immune responses against human cartilage glycoprotein-39 in health Vs proinflammatory responses in rheumatoid arthritis. Proc Natl Acad Sci USA 2004, 101:17180-17185.
29. Waase I., Kayser C., Carlson P.J., Goronzy J.J., Weyand C.M. Oligoclonal T cell proliferation in patients with rheumatoid arthritis and their unaffected siblings. Arthritis Rheum 1996, 39:904-913.
30. Forger F, Marcoli N, Gaodla S, Möller B, Villiger PM, Ostensen M. Pregnancy induces numerical and functional changes of CD4+CD25+high regulatory T cells in patients with rheumatoid arthritis. Ann Rheum Dis 2007; E pub ahead of aprint.
31. Kendall M.D., Clarke A.G. The thymus in the mouse changes its activity during pregnancy: a study of the microenvironment. J Anat 2000, 197(Pt. 3):393-411.
32. Kumar N., Marshall N.J., Hammal D.M., Pearce M.S., Parker L., Furniss S.S., et al. Causes of death in patients with rheumatoid arthritis: comparison with siblings and matched osteoarthritis controls. J Rheumatol 2007, 34:1695-1698.
33. Beauparlant P., Papp K., Haraoui B. The incidence of cancer associated with the treatment of rheumatoid arthritis. Semin Arthritis Rheum 1999, 29:148-158.
34. Hemminki K., Li X., Sundquist K., Sundquist J. Cancer risk in hospitalized rheumatoid arthritis patients. Rheumatology (Oxford) 2008, 47:698-701.
35. Stolfi C., Fina D., Caruso R., Caprioli F., Sarra M., Fantini M.C., et al. Cyclooxygenase-2-dependent and -independent inhibition of proliferation of colon cancer cells by 5-aminosalicylic acid. Biochem Pharmacol 2008, 75:668-676.
36. Lev-Ari S., Kazanov D., Liberman E., Ben-Yosef R., Arber N. Down-regulation of PGE2 by physiologic levels of celecoxib is not sufficient to induce apoptosis or inhibit cell proliferation in human colon carcinoma cell lines. Dig Dis Sci 2007, 52(4):1128-1133.
37. Mahic M., Yaqub S., Johansson C.C., Taskén K., Aandahl E.M. FoxP3+CD4+CD25+ adaptative regulatory T cells express cyclooxygenase-2 and suppress effector T cells by a prostaglandin E-2 dependent mechanism. J Immunol 2006, 177:246-254.
38. Baratelli F., Lin Y., Zhu L., Yang S.C., Heuzé-Vourc'h N., Zheng G., et al. Prostaglandin E2 induces FoxP3 gene expression and T regulatory cell function in human CD4+ T cells. J Immunol 2005, 175:1483-1490.
39. Thewissen M., Linsen L., Somers V., Geusens P., Raus J., Stinissen P. Premature immunosenescence in rheumatoid arthritis and multiple sclerosis patients. Ann NY Acad Sci 2005, 1051:255-262.
40. Weyand C.M., Fulbright J.W., Goronzy J.J. Immunosenescence, autoimmunity, and rheumatoid arthritis. Exp Gerontol 2003, 38:833-841.
41. Goronzy J.J., Weyand C.M. Aging, autoimmunity and arthritis: T-cell senescence and contraction of T-cell repertoire diversity-catalysts of autoimmunity and chronic inflammation. Arthritis Res Ther 2003, 5(5):225-234.
42. Vang T., Congia M., Macis M.D., Musumeci L., Orru V., Zavattari P., et al. Autoimmune-associated lymphoid tyrosine phosphatase is a gain-of-function variant. Nat Genet 2005, 37:1317-1319.
43. Anderson M.S., Venanzi E.S., Klein L., Chen Z., Berzins S.P., Turley S.J., et al. Projection of an immunological self shadow within the thymus by the aire protein. Science 2002, 298:1395-1401.
44. Derbinski J., Gäbler J., Brors B., Tierling S., Joannkuty S., Hergenhahn M., et al. Promiscuous gene expression in thymic epithelial cells is regulated at multiple levels. J Exp Med 2005, 202:33-45.
45. Kyewski B., Klein L. A central role for central tolerance. Annu Rev Immunol 2006, 24:571-606.
46. Gray D., Abramson J., Benoist C., Mathis D. Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire. J Exp Med 2007, 204:2521-2528.
47. Gotter J., Brors B., Hergenhahn M., Kyewski B. Medullary epithelial cells of the human thymus express a highly diverse selection of tissue-specific genes colocalized in chromosomal clusters. J Exp Med 2004, 199:155-166.
48. Gillard G.O., Farr A.G. Features of medullary thymic epithelium implicate postnatal development in maintaining epithelial heterogeneity and tissue-restricted antigen expression. J Immunol 2006, 176:5815-5824.
49. Gray D.H., Gavanescu I., Benoist C., Mathis D. Danger-free autoimmune disease in Aire-deficient mice. Proc Natl Acad Sci USA 2007, 104:18193-18198.
50. Kuroda N., Mitani T., Takeda N., Ishimaru N., Arakaki R., Hayashi Y., et al. Development of autoimmunity against transcriptionally unrepressed target antigen in the thymus of Aire-deficient mice. J Immunol 2005, 174:1862-1870.
51. Kekalainen E., Tuovinen H., Joensuu J., Gulling M., Franssila R., Pontynen N., et al. A defect of regulatory T cells in patients with autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy. J Immunol 2007, 178:1208-1215.
52. Venanzi E.S., Gray D.H., Benoist C., Mathis D. Lymphotoxin pathway and Aire influences on thymic medullary epithelial cells are unconnected. J Immunol 2007, 179:5693-5700.
53. Taubert R., Schwendemann J., Kyewski B. Highly variable expression of tissue-restricted self-antigens in human thymus: implications for self-tolerance and autoimmunity. Eur J Immunol 2007, 37:838-848.
54. Chentoufi A.A., Palumbo M., Polychronakos C. Proinsulin expression by Hassall's corpuscles in the mouse thymus. Diabetes 2004, 53:354-359.
55. Girbal-Neuhauser E., Durieux J.J., Arnaud M., Dalbon P., Sebbag M., Vincent C., et al. The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. J Immunol 1999, 162:585-594.
56. Masson-Bessière C., Sebbag M., Girbal-Neuhauser E., Nogueira L., Vincent C., Senshu T., et al. The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. J Immunol 2001, 166:4177-4184.
57. Renaudineau Y., Jamin C., Saraux A., Youinou P. Rheumatoid factor on a daily basis. Autoimmunity 2005, 38:11-16.
58. Favre A. Filaggrin in Hassall's corpuscle by histochemical and immunohistochemical methods. Acta Anat (Basel) 1989, 135:71-76.
59. Guerrin M., Ishigami A., Mechin M.C., Nachat R., Valramy S., Sebbag M., et al. cDNA cloning, gene organization and expression analysis of human peptidylarginine deiminase type I. Biochem J 2003, 370(Pt. 1):167-174.
60. Moscarello M.A., Mastronardi F.G., Wood D.D. The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res 2007, 32:251-256.
61. Henry L., Anderson G. Immunoglobulins in Hassall's corpuscles of the human thymus. J Anat 1990, 168:185-197.
62. Chaudhury C., Brooks C.L., Carter D.C., Robinson J.M., Anderson C.L. Albumin binding to FcRn: distinct from the FcRn-IgG interaction. Biochemistry 2006, 45:4983-4990.
63. Dzidic A., Mohr A., Meyer K., Bauer J., Meyer H.H., Pfaffi M.W. Effects of mycophenolic acid (MPA) treatment on expression of Fc recptor (FcRn) and polymeric immunoglobulin receptor (pIgR) mRNA in adult sheep tissues. Croat Med J 2004, 45:130-135.
64. Yoshida M., Claypool S.M., Wagner J.S., Mizoguchi E., Mizoguchi A., Roopenian D.C., et al. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 2004, 20:769-783.
65. Spiekermann G.M., Finn P.W., Ward E.S., Dumont J., Dickison B.L., Blumberg R.S., et al. Receptor-mediated immunoglobulin G transport across mucosal barriers in adult life: functional expression of FcRn in the mammalian lung. J Exp Med 2002, 196:303-310.
66. Sladowski D., Wasiutynski A., Wilczynski G., Grabska-Liberek I., Coecke S., Kinsner A., et al. Expression of the membrane complement regulatory proteins (CD55 and CD59) in human thymus. Folia Histochem Cytobiol 2006, 44:263-267.
67. Kennedy M.K., Willis C.R., Armitage R.J. Deciphering CD30 ligand biology and its role in humoral immunity. Immunology 2006, 118:143-152.
68. Edwards J.C., Leigh R.D., Cambridge G. Expression of molecules involved in B lymphocyte survival and differentiation by synovial fibroblasts. Clin Exp Immunol 1997, 108:407-414.
69. Spencer J., Choy M., Hussell T., Papadaki L., Kington J.P., Isaacson P.G. Properties of human thymic B cells. Immunology 1992, 75:596-600.
70. Mori S., Inaba M., Sugihara A., Taketani S., Doi H., Fukuba Y., et al. Presence of B cell progenitors in the thymus. J Immunol 1997, 158:4193-4199.
71. Yoshitake T., Takahama T., Kanai F., Ohnishi K., Suzuki T., Kametani Y., et al. B cell population and its autoimmune activity in the thymus of patients associated with myasthenia gravis. Kyobu Geka 1993, 46:1083-1087.
72. Fend F., Kirchner T., Marx A., Müller-Hermelink H.K. B-cells in thymic epithelial tumours. An immunohistochemical analysis of intra- and extraepithelial B cell compartments. Virchows Arch B Cell Pathol Incl Mol Pathol 1993, 63:241-247.
73. McAleer J., Weber P., Sun J., Butler J.E. Antibody repertoire development in fetal and neonatal piglets. XI. The thymic B-cell repertoire develops independently from that in blood and mesenteric lymph nodes. Immunology 2005, 114:171-183.
74. Guarnotta G., Burgio V.L., Triolo G. Do immune complexes formed with autoantibodies have a role in the maintenance of immune homeostasis through interaction with Fc receptors. Autoimmunity 2000, 32:153-160.
75. Zhong X., Gao W., Degauqe N., Bai C., Lu Y., Kenny J., et al. Reciprocal generation of Th1/Th17 and Tregs cells by B1 and B2 cells. Eur J Imnunol 2007, 37:2400-2404.
76. Lemke H., Lange H. Is there a maternally induced immunological imprinting phase à la Konrad Lorenz?. Scand J Immunol 1999, 50:348-354.
77. Johansson M., Arlestig L., Hallmans G., Rantapaa-Dahlqvist S. PTPN22 polymorphism and anti-cyclic citrullinated peptide antibodies in combination strongly predicts future onset of rheumatoid arthritis and has a specificity of 100% for the disease. Arthritis Res Ther 2006, 8(1):R19.
78. Chapuy-Regaud S., Sebbag M., Baeten D., Clavel C., Foulquier C., De Keyser F., et al. Fibrin deimination in synovial tissue is not specific for rheumatoid arthritis but commonly occurs during synovitides. J Immunol 2005, 174:5057-5064.
79. Duplan V., Foulquier C., Clavel C., Al Badine R., Serre G., Saoudi A., et al. In the rat, citrullinated autologous fibrinogen is immunogenic but the induced autoimmune response is not arthritogenic. Clin Exp Immunol 2006, 145:502-512.
80. Mandik-Nayak L., Wipke B.T., Shih F.F., Unanue R., Allen P.M. Despite ubiquitous autoantigen expression, arthritogenic autoantibody response initiates in the local lymph node. Proc Natl Acad Sci USA 2002, 99:14368-14373.
81. Vani J., Justin J., Nagasuma R.C., Nayak R., Shaila M.S. Peptidomimics of antigen are present in variable region of heavy and light chains of anti-idiotypic antibody and function as surrogate antigen for perpetuation of immunological memory. Mol Immunol 2007, 44:3345-3354.
82. Munthe L.A., Corthay A., Os A., Zangani M., Bogen B. Systemic autoimmune disease caused by autoreactive B cells that receive chronic help from Ig V region-specific T cells. J Immunol 2005, 175:2391-2400.
83. Phillips W.J., Smith D.J., Bona C.A., Bot A., Zaghouani H. Recombinant immunoglobulin-based epitope delivery: a novel class of autoimmune regulators. Int Rev Immunol 2005, 24:501-517.
84. Sebbag M., Moinard N., Auger I., Clavel C., Arnaud J., Nogueira L., et al. Epitopes of human fibrin recognized by the rheumatoid arthritis-specific autoantibodies to citrullinated proteins. Eur J Immunol 2006, 36:2250-2263.
85. Nishihara R.M., Skare T.L., Silva M.B., Messias-Reason I.T., Oliveira N.P., Fiedler P.T., et al. High positivity of anti-CCP antibodies in patients with Down syndrome. Clin Rheumatol 2007, 26:2031-2035.
86. Padmakumar B., Evans Jones L.G., Sills J.A. Is arthritis more common in children with Down syndrome?. Rheumatology (Oxford) 2002, 41:1191-1193.
87. Levin S., Schlesinger M., Handzel Z., Hahn T., Altman Y., Czernobilsky B., et al. Thymic deficiency in Down's syndrome. Pediatrics 1979, 63:80-87.
88. Berthelot J.M. Could rheumatoid arthritis result from an abnormal T cell response towards lubricin/superficial zone protein?. Med Hypotheses 2004, 62:894-897.
89. Sun Y., Berger E.J., Zhao C., An K.N., Amadio P.C., Jay G. Mapping lubricin in canine musculoskeletal tissues. Connect Tissue Res 2006, 47:215-221.
90. Volin M.V., Shahrara S., Haines K., Woods J.M., Koch A.E. Expression of mucin 3 and mucin 5AC in arthritis synovial tissue. Arthritis Rheum 2008, 58:46-52.
91. Setoguchi K., Misaki Y., Kawahata K., Shimada K., Juji T., Tanaka S., et al. Suppression of T cell responses by chondromodulin I, a cartilage derived angiogenesis inhibitory factor: therapeutic potential in rheumatoid arthritis. Arthritis Rheum 2004, 50:828-839.
92. Brandau O., Meindl A., Fassler R., Aszodi A. A novel gene, tendin, is strongly expressed in tendons and ligaments and shows high homology with chondromodulin-1. Dev Dyn 2001, 221:72-80.
93. Chin R.K., Zhu M., Christiansen P.A., Liu W., Ware C., Peltonen L., et al. Lymphotoxin pathway-directed, autoimmune regulator-independent central tolerance to arthritogenic collagen. J Immunol 2006, 177:290-297.
94. Roord S.T.A., Zonneveld-Huijssoon E., Le T., Yung G.P., Koffeman E., Ronaghy A., et al. Modulation of T cell function by combination of epitope specific and low dose anticytokine therapy controls autoimmune arthritis. PLoS ONE1 2006, (1):e87.