The parasitic helminth product ES-62 suppresses pathogenesis in collagen-induced arthritis by targeting the interleukin-17-producing cellular network at multiple sites

Arthritis and Rheumatism

Volumn 64, Issue 10, 2012, Pages 3168-3178

  Pineda, Miguel A ^a   McGrath, Mairi A ^a   Smith, Pauline C ^a   Al Riyami, Lamyaa ^b   Rzepecka, Justyna ^b   Gracie, J Alastair ^a   Harnett, William ^b   Harnett, Margaret M ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRHEUMATIC AGENT; ES 62; HERMES ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 17; PROTECTIVE AGENT; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ARTHRITIS; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; IMMUNIZATION; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; ARTHRITIS, EXPERIMENTAL; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HELMINTH PROTEINS; INTERLEUKIN-17; JOINTS; MALE; MICE; UP-REGULATION;

EID: 84869047053     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.34581     Document Type: Article

References (48)

1. Cooke A, Zaccone P, Raine T, Phillips JM, Dunne DW. Infection and autoimmunity: are we winning the war, only to lose the peace? Trends Parasitol 2004; 20: 316-21. (Pubitemid 38749074)
2. McInnes IB, Leung BP, Harnett M, Gracie JA, Liew FY, Harnett W. A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. J Immunol 2003; 171: 2127-33. (Pubitemid 36966497)
3. Harnett MM, Kean DE, Boitelle A, McGuiness S, Thalhamer T, Steiger CN, et al. The phosphorycholine moiety of the filarial nematode immunomodulator ES-62 is responsible for its antiinflammatory action in arthritis. Ann Rheum Dis 2008; 67: 518-23. (Pubitemid 351498434)
4. Nakae S, Nambu A, Sudo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol 2003; 171: 6173-7. (Pubitemid 37467240)
5. Koenders MI, Lubberts E, Oppers-Walgreen B, Van Den Bersselaar L, Helsen MM, Kolls JK, et al. Induction of cartilage damage by overexpression of T cell interleukin-17A in experimental arthritis in mice deficient in interleukin-1. Arthritis Rheum 2005;52: 975-83. (Pubitemid 40365122)
6. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 2006; 203: 2673-82. (Pubitemid 44833343)
7. Benderdour M, Tardif G, Pelletier JP, Di Battista JA, Reboul P, Ranger P, et al. Interleukin 17 (IL-17) induces collagenase-3 production in human osteoarthritic chondrocytes via AP-1 dependent activation: differential activation of AP-1 members by IL-17 and IL-1-. J Rheumatol 2002; 29: 1262-72. (Pubitemid 34601964)
8. Koshy PJ, Henderson N, Logan C, Life PF, Cawston TE, Rowan AD. Interleukin 17 induces cartilage collagen breakdown: novel synergistic effects in combination with proinflammatory cytokines. Ann Rheum Dis 2002; 61: 704-13. (Pubitemid 34787708)
9. Shahrara S, Huang Q, Mandelin AM II, Pope RM. TH-17 cells in rheumatoid arthritis. Arthritis Res Ther 2008;10:R93.
10. Vermeire K, Heremans H, Vandeputte M, Huang S, Billiau A, Matthys P. Accelerated collagen-induced arthritis in IFN-receptor-deficient mice. J Immunol 1997; 158: 5507-13. (Pubitemid 127681260)
11. Chu CQ, Swart D, Alcorn D, Tocker J, Elkon KB. Interferon-regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum 2007; 56: 1145-51. (Pubitemid 46608639)
12. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-. Nature 2000; 408: 600-5.
13. Yago T, Nanke Y, Kawamoto M, Furuya T, Kobashigawa T, Kamatani N, et al. IL-23 induces human osteoclastogenesis via IL-17 in vitro, and anti-IL-23 antibody attenuates collageninduced arthritis in rats. Arthritis Res Ther 2007;9:R96.
14. Roark CL, French JD, Taylor MA, Bendele AM, Born WK, O'Brien RL. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing -T cells. J Immunol 2007; 179: 5576-83.
15. Marshall FA, Grierson AM, Garside P, Harnett W, Harnett MM. ES-62, an immunomodulator secreted by filarial nematodes, suppresses clonal expansion and modifies effector function of heterologous antigen-specific T cells in vivo. J Immunol 2005;175: 5817-26. (Pubitemid 41508066)
16. Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol 2000; 164: 6453-60. (Pubitemid 30408828)
17. Goodridge HS, Marshall FA, Wilson EH, Houston KM, Liew FY, Harnett MM, et al. In vivo exposure of murine dendritic cell and macrophage bone marrow progenitors to the phosphorylcholinecontaining filarial nematode glycoprotein ES-62 polarizes their differentiation to an anti-inflammatory phenotype. Immunology 2004; 113: 491-8. (Pubitemid 39593368)
18. Goodridge HS, McGuiness S, Houston KM, Egan CA, Al-Riyami L, Alcocer MJ, et al. Phosphorylcholine mimics the effects of ES-62 on macrophages and dendritic cells. Parasite Immunol 2007; 29: 127-37. (Pubitemid 46239262)
19. Goodridge HS, Marshall FA, Else KJ, Houston KM, Egan C, Al-Riyami L, et al. Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. J Immunol 2005; 174: 284-93. (Pubitemid 40007415)
20. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from -T cells, amplifying Th17 responses and autoimmunity. Immunity 2009; 31: 331-41.
21. Feng T, Qin H, Wang L, Benveniste EN, Elson CO, Cong Y. Th17 cells induce colitis and promote Th1 cell responses through IL-17 induction of innate IL-12 and IL-23 production. J Immunol 2011; 186:6313-8.
22. Murugaiyan G, Mittal A, Lopez-Diego R, Maier LM, Anderson DE, Weiner HL. IL-27 is a key regulator of IL-10 and IL-17 production by human CD4-T cells. J Immunol 2009; 183: 2435-43.
23. Ito Y, Usui T, Kobayashi S, Iguchi-Hashimoto M, Ito H, Yoshitomi H, et al. Gamma/delta T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum 2009; 60: 2294-303.
24. Harrington LE, Mangan PR, Weaver CT. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr Opin Immunol 2006; 18: 349-56.
25. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005;201: 233-40. (Pubitemid 40189432)
26. Al-Riyami L, Harnett W. Immunomodulatory properties of ES-62, a phosphorylcholine-containing glycoprotein secreted by acanthocheilonema viteae. Endocr Metab Immune Disord Drug Targets 2012; 12: 45-52.
27. Kulkarni R, Behboudi S, Sharif S. Insights into the role of Toll-like receptors in modulation of T cell responses. Cell Tissue Res 2011; 343: 141-52.
28. Reynolds JM, Pappu BP, Peng J, Martinez GJ, Zhang Y, Chung Y, et al. Toll-like receptor 2 signaling in CD4-T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease. Immunity 2010; 32: 692-702.
29. Ivanov II, Zhou L, Littman DR. Transcriptional regulation of Th17 cell differentiation. Semin Immunol 2007; 19: 409-17. (Pubitemid 351274050)
30. Kenny EF, O'Neill LA. Signalling adaptors used by Toll-like receptors: an update. Cytokine 2008; 43: 342-9.
31. Gulen MF, Kang Z, Bulek K, Youzhong W, Kim TW, Chen Y, et al. The receptor SIGIRR suppresses Th17 cell proliferation via inhibition of the interleukin-1 receptor pathway and mTOR kinase activation. Immunity 2010; 32: 54-66.
32. Staschke KA, Dong S, Saha J, Zhao J, Brooks NA, Hepburn DL, et al. IRAK4 kinase activity is required for Th17 differentiation and Th17-mediated disease. J Immunol 2009; 183: 568-77.
33. Shibata K, Yamada H, Hara H, Kishihara K, Yoshikai Y. Resident V-1-T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J Immunol 2007; 178:4466-72.
34. Conti L, Casetti R, Cardone M, Varano B, Martino A, Belardelli F, et al. Reciprocal activating interaction between dendritic cells and pamidronate-stimulated -T cells: role of CD86 and inflammatory cytokines. J Immunol 2005; 174: 252-60. (Pubitemid 40007411)
35. Tanaka Y, Brenner MB, Bloom BR, Morita CT. Recognition of nonpeptide antigens by T cells. J Mol Med (Berl) 1996; 74: 223-31. (Pubitemid 26175417)
36. Petermann F, Rothhammer V, Claussen MC, Haas JD, Blanco LR, Heink S, et al. -T cells enhance autoimmunity by restraining regulatory T cell responses via an interleukin-23-dependent mechanism. Immunity 2010; 33: 351-63.
37. Collins C, Shi C, Russell JQ, Fortner KA, Budd RC. Activation of -T cells by Borrelia burgdorferi is indirect via a TLR- and caspase-dependent pathway. J Immunol 2008; 181: 2392-8.
38. Fang H, Welte T, Zheng X, Chang GJ, Holbrook MR, Soong L, et al. -T cells promote the maturation of dendritic cells during West Nile virus infection. FEMS Immunol Med Microbiol 2010; 59:71-80.
39. Xu S, Han Y, Xu X, Bao Y, Zhang M, Cao X. IL-17A-producing -cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation. J Immunol 2010; 185: 5879-87.
40. Price SJ, Hope JC. Enhanced secretion of interferon-by bovine -T cells induced by coculture with Mycobacterium bovis-infected dendritic cells: evidence for reciprocal activating signals. Immunology 2009; 126: 201-8.
41. Xu R, Wang R, Han G, Wang J, Chen G, Wang L, et al. Complement C5a regulates IL-17 by affecting the crosstalk between DC and -T cells in CLP-induced sepsis. Eur J Immunol 2010; 40: 1079-88.
42. Niedbala W, Cai B, Wei X, Patakas A, Leung BP, McInnes IB, et al. Interleukin 27 attenuates collagen-induced arthritis. Ann Rheum Dis 2008; 67: 1474-9.
43. Pickens SR, Chamberlain ND, Volin MV, Mandelin AM II, Agrawal H, Matsui M, et al. Local expression of interleukin-27 ameliorates collagen-induced arthritis. Arthritis Rheum 2011;63: 2289-98.
44. Naor D, Nedvetzki S, Walmsley M, Yayon A, Turley EA, Golan I, et al. CD44 involvement in autoimmune inflammations: the lesson to be learned from CD44-targeting by antibody or from knockout mice. Ann N Y Acad Sci 2007; 1110: 233-47. (Pubitemid 350043012)
45. Szanto S, Gal I, Gonda A, Glant TT, Mikecz K. Expression of L-selectin, but not CD44, is required for early neutrophil extravasation in antigen-induced arthritis. J Immunol 2004; 172: 6723-34. (Pubitemid 38669109)
46. Lubberts E, Van Den Bersselaar L, Oppers-Walgreen B, Schwarzenberger P, Coenen-de Roo CJ, Kolls JK, et al. IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-B ligand/osteoprotegerin balance. J Immunol 2003; 170: 2655-62. (Pubitemid 36245658)
47. Kelchtermans H, Schurgers E, Geboes L, Mitera T, Van Damme J, Van Snick J, et al. Effector mechanisms of interleukin-17 in collagen-induced arthritis in the absence of interferon-and counteraction by interferon-. Arthritis Res Ther 2009;11:R122.
48. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M. Interleukin-17-producing -T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009; 31:321-30.