A polymorphism in the interleukin-4 receptor affects the ability of interleukin-4 to regulate Th17 cells: A possible immunoregulatory mechanism for genetic control of the severity of rheumatoid arthritis

Arthritis Research and Therapy

Volumn 13, Issue 1, 2011, Pages

  Wallis, Susan K ^a   Cooney, Laura A ^a   Endres, Judith L ^a   Lee, Min Jie ^a   Ryu, Jennifer ^a   Somers, Emily C ^a   Fox, David A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 4 RECEPTOR; INTERLEUKIN 4;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENETIC REGULATION; GENOTYPE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PROTEIN BLOOD LEVEL; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TH17 CELL; BIOSYNTHESIS; CELL CULTURE; CELL SEPARATION; CROSS-SECTIONAL STUDY; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY; PILOT STUDY;

ADULT; ARTHRITIS, RHEUMATOID; CELL SEPARATION; CELLS, CULTURED; CROSS-SECTIONAL STUDIES; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; INTERLEUKIN-17; INTERLEUKIN-4; MALE; MIDDLE AGED; PILOT PROJECTS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, INTERLEUKIN-4; SIGNAL TRANSDUCTION; TH17 CELLS; YOUNG ADULT;

EID: 79551595156     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3239     Document Type: Article

References (41)

1. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005, 6:1123-1132. 10.1038/ni1254, 16200070.
2. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005, 6:1133-1141. 10.1038/ni1261, 1618871, 16200068.
3. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005, 201:233-240. 10.1084/jem.20041257, 2212798, 15657292.
4. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748. 10.1038/nature01355, 12610626.
5. Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 2003, 198:1951-1957. 10.1084/jem.20030896, 2194162, 14662908.
6. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238. 10.1038/nature04753, 16648838.
7. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, Hatton RD, Wahl SM, Schoeb TR, Weaver CT. Transforming growth factor-β induces development of the TH17 lineage. Nature 2006, 441:231-234. 10.1038/nature04754, 16648837.
8. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-189. 10.1016/j.immuni.2006.01.001, 16473830.
9. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, Basham B, Smith K, Chen T, Morel F, Lecron JC, Kastelein RA, Cua DJ, McClanahan TK, Bowman EP, de Waal Malefyt R. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007, 8:950-957. 10.1038/ni1497, 17676044.
10. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007, 8:942-949. 10.1038/ni1496, 17676045.
11. Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev 2008, 223:87-113. 10.1111/j.1600-065X.2008.00628.x, 18613831.
12. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 2006, 24:677-688. 10.1016/j.immuni.2006.06.002, 16782025.
13. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009, 27:485-517. 10.1146/annurev.immunol.021908.132710, 19132915.
14. Myers LK, Tang B, Stuart JM, Kang AH. The role of IL-4 in regulation of murine collagen-induced arthritis. Clin Immunol 2002, 102:185-191. 10.1006/clim.2001.5162, 11846461.
15. Morita Y, Yang J, Gupta R, Shimizu K, Shelden EA, Endres J, Mule JJ, McDonagh KT, Fox DA. Dendritic cells genetically engineered to express IL-4 inhibit murine collagen-induced arthritis. J Clin Invest 2001, 107:1275-1284. 10.1172/JCI11490, 209294, 11375417.
16. Sarkar S, Tesmer LA, Hindnavis V, Endres JL, Fox DA. Interleukin-17 as a molecular target in immune-mediated arthritis: immunoregulatory properties of genetically modified murine dendritic cells that secrete interleukin-4. Arthritis Rheum 2007, 56:89-100. 10.1002/art.22311, 17195211.
17. Kim SH, Bianco NR, Shufesky WJ, Morelli AE, Robbins PD. Effective treatment of inflammatory disease models with exosomes derived from dendritic cells genetically modified to express IL-4. J Immunol 2007, 179:2242-2249.
18. Skapenko A, Wendler J, Lipsky PE, Kalden JR, Schulze-Koops H. Altered memory T cell differentiation in patients with early rheumatoid arthritis. J Immunol 1999, 163:491-499.
19. Kruse S, Japha T, Tedner M, Sparholt SH, Forster J, Kuehr J, Deichmann KA. The polymorphisms S503P and Q576R in the interleukin-4 receptor α gene are associated with atopy and influence the signal transduction. Immunology 1999, 96:365-371. 10.1046/j.1365-2567.1999.00705.x, 2326760, 10233717.
20. Risma KA, Wang N, Andrews RP, Cunningham CM, Ericksen MB, Bernstein JA, Chakraborty R, Hershey GK. V75R576 IL-4 receptor α is associated with allergic asthma and enhanced IL-4 receptor function. J Immunol 2002, 169:1604-1610.
21. Prots I, Skapenko A, Wendler J, Mattyasovszky S, Yone CL, Spriewald B, Burkhardt H, Rau R, Kalden JR, Lipsky PE, Schulze-Koops H. Association of the IL4R single-nucleotide polymorphism I50V with rapidly erosive rheumatoid arthritis. Arthritis Rheum 2006, 54:1491-1500. 10.1002/art.21832, 16646030.
22. Grigor C, Capell H, Stirling A, McMahon AD, Lock P, Vallance R, Kincaid W, Porter D. Effect of a treatment strategy of tight control for rheumatoid arthritis [the TICORA study]: a single-blind randomised controlled trial. Lancet 2004, 364:263-269. 10.1016/S0140-6736(04)16676-2, 15262104.
23. Goekoop-Ruiterman YP, de Vries-Bouwstra JK, Allaart CF, van Zeben D, Kerstens PJ, Hazes JM, Zwinderman AH, Ronday HK, Han KH, Westedt ML, Gerards AH, van Groenendael JH, Lems WF, van Krugten MV, Breedveld FC, Dijkmans BA. Clinical and radiographic outcomes of four different treatment strategies in patients with early rheumatoid arthritis [the BeSt study]: a randomized, controlled trial. Arthritis Rheum 2008, 58:S126-S135. 10.1002/art.23364, 18240203.
24. Leipe J, Grunke M, Dechant C, Reindl C, Kerzendorf U, Schulze-Koops H, Skapenko A. Role of Th17 cells in human autoimmune arthritis. Arthritis Rheum 2010, 62:2876-2885. 10.1002/art.27622, 20583102.
25. Sarkar S, Cooney LA, Fox DA. The role of T helper type 17 cells in inflammatory arthritis. Clin Exp Immunol 2010, 159:225-237. 10.1111/j.1365-2249.2009.04016.x, 19758374.
26. Marinou I, Till SH, Moore DJ, Wilson AG. Lack of association or interactions between the IL-4, IL-4α and IL-13 genes, and rheumatoid arthritis. Arthritis Res Ther 2008, 10:R80. 10.1186/ar2454, 2575626, 18625055.
27. Stephenson L, Johns MH, Woodward E, Mora AL, Boothby M. An IL-4Rα allelic variant, I50, acts as a gain-of-function variant relative to V50 for Stat6, but not Th2 differentiation. J Immunol 2004, 173:4523-4528.
28. Mitsuyasu H, Yanagihara Y, Mao XQ, Gao PS, Arinobu Y, Ihara K, Takabayashi A, Hara T, Enomoto T, Sasaki S, Kawai M, Hamasaki N, Shirakawa T, Hopkin JM, Izuhara K. Cutting edge: dominant effect of Ile50Val variant of the human IL-4 receptor α-chain in IgE synthesis. J Immunol 1999, 162:1227-1231.
29. Yabiku K, Hayashi M, Komiya I, Yamada T, Kinjo Y, Ohshiro Y, Kouki T, Takasu N. Polymorphisms of interleukin [IL]-4 receptor alpha and signal transducer and activator of transcription-6 [Stat6] are associated with increased IL-4Rα-Stat6 signalling in lymphocytes and elevated serum IgE in patients with Graves' disease. Clin Exp Immunol 2007, 148:425-431. 10.1111/j.1365-2249.2007.03366.x, 1941918, 17362266.
30. Szekanecz Z, Koch AE. Angiogenesis and its targeting in rheumatoid arthritis. Vascul Pharmacol 2009, 51:1-7. 10.1016/j.vph.2009.02.002, 2917972, 19217946.
31. Haas CS, Amin MA, Allen BB, Ruth JH, Haines GK, Woods JM, Koch AE. Inhibition of angiogenesis by interleukin-4 gene therapy in rat adjuvant-induced arthritis. Arthritis Rheum 2006, 54:2402-2414. 10.1002/art.22034, 16869003.
32. Lubberts E, Joosten LA, van Den Bersselaar L, Helsen MM, Bakker AC, van Meurs JB, Graham FL, Richards CD, van Den Berg WB. Adenoviral vector-mediated overexpression of IL-4 in the knee joint of mice with collagen-induced arthritis prevents cartilage destruction. J Immunol 1999, 163:4546-4556.
33. Hong KH, Cho ML, Min SY, Shin YJ, Yoo SA, Choi JJ, Kim WU, Song SW, Cho CS. Effect of interleukin-4 on vascular endothelial growth factor production in rheumatoid synovial fibroblasts. Clin Exp Immunol 2007, 147:573-579. 10.1111/j.1365-2249.2006.03295.x, 1810499, 17302909.
34. Chabaud M, Garnero P, Dayer JM, Guerne PA, Fossiez F, Miossec P. Contribution of interleukin 17 to synovium matrix destruction in rheumatoid arthritis. Cytokine 2000, 12:1092-1099. 10.1006/cyto.2000.0681, 10880256.
35. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 1999, 103:1345-1352. 10.1172/JCI5703, 408356, 10225978.
36. Yamada A, Takami M, Kawawa T, Yasuhara R, Zhao B, Mochizuki A, Miyamoto Y, Eto T, Yasuda H, Nakamichi Y, Kim N, Katagiri T, Suda T, Kamijo R. Interleukin-4 inhibition of osteoclast differentiation is stronger than that of interleukin-13 and they are equivalent for induction of osteoprotegerin production from osteoblasts. Immunology 2007, 120:573-579. 10.1111/j.1365-2567.2006.02538.x, 2265899, 17343616.
37. Koenders MI, Lubberts E, Oppers-Walgreen B, van den Bersselaar L, Helsen MM, Di Padova FE, Boots AM, Gram H, Joosten LA, van den Berg WB. Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. Am J Pathol 2005, 167:141-149. 10.1016/S0002-9440(10)62961-6, 1603454, 15972960.
38. Palmqvist P, Lundberg P, Persson E, Johansson A, Lundgren I, Lie A, Conaway HH, Lerner UH. Inhibition of hormone and cytokine-stimulated osteoclastogenesis and bone resorption by interleukin-4 and interleukin-13 is associated with increased osteoprotegerin and decreased RANKL and RANK in a STAT6-dependent pathway. J Biol Chem 2006, 281:2414-2429. 10.1074/jbc.M510160200, 16251181.
39. Yorimitsu M, Nishida K, Shimizu A, Doi H, Miyazawa S, Komiyama T, Nasu Y, Yoshida A, Watanabe S, Ozaki T. Intra-articular injection of interleukin-4 decreases nitric oxide production by chondrocytes and ameliorates subsequent destruction of cartilage in instability-induced osteoarthritis in rat knee joints. Osteoarthritis Cartilage 2008, 16:764-771. 10.1016/j.joca.2007.11.006, 18182309.
40. Arpa L, Valledor AF, Lloberas J, Celada A. IL-4 blocks M-CSF-dependent macrophage proliferation by inducing p21Waf1 in a STAT6-dependent way. Eur J Immunol 2009, 39:514-526. 10.1002/eji.200838283, 19130475.
41. Cao Y, Brombacher F, Tunyogi-Csapo M, Glant TT, Finnegan A. Interleukin-4 regulates proteoglycan-induced arthritis by specifically suppressing the innate immune response. Arthritis Rheum 2007, 56:861-870. 10.1002/art.22422, 17330244.