IL-35 Inhibits Angiogenesis through VEGF/Ang2/Tie2 Pathway in Rheumatoid Arthritis

Cellular Physiology and Biochemistry

Volumn 40, Issue 5, 2016, Pages 1105-1116

  Jiang, Shenyi ^a   Li, Yuxuan ^a   Lin, Tiantian ^a   Yuan, Lin ^a   Li, Yunxia ^a   Wu, Suqin ^a   Xia, Liping ^a   Shen, Hui ^a   Lu, Jing ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Ang2; Angiogenesis; IL 35; Rheumatoid arthritis; Tie2

Indexed keywords

ANGIOPOIETIN 2; ANGIOPOIETIN RECEPTOR; FIBRONECTIN; GELATINASE A; GELATINASE B; INTERLEUKIN 35; INTERLEUKIN 6; INTERLEUKIN 8; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; AUTACOID; CYTOKINE; INTERLEUKIN DERIVATIVE; MATRIX METALLOPROTEINASE; VASCULOTROPIN A;

ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; SYNOVIUM; UMBILICAL VEIN ENDOTHELIAL CELL; WOUND HEALING; ZYMOGRAPHY; ANGIOGENESIS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMOTAXIS; DRUG EFFECTS; METABOLISM; PATHOLOGY;

ANGIOPOIETIN-2; ANIMALS; ARTHRITIS, RHEUMATOID; CELL ADHESION; CHEMOTAXIS; CYTOKINES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; INFLAMMATION MEDIATORS; INTERLEUKINS; MATRIX METALLOPROTEINASES; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTOR, TIE-2; SIGNAL TRANSDUCTION; SYNOVIAL MEMBRANE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 85006340052     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000453165     Document Type: Article

References (40)

1. Elshabrawy HA, Chen Z, Volin MV, Ravella S, Virupannavar S, Shahrara S: The pathogenic role of angiogenesis in rheumatoid arthritis. Angiogenesis 2015;18:433-448.
2. Szekanecz Z, Besenyei T, Szentpetery A, Koch AE: Angiogenesis and vasculogenesis in rheumatoid arthritis. Curr Opin Rheumatol 2010;22:299-306.
3. Nagashima M, Yoshino S, Ishiwata T, Asano G: Role of vascular endothelial growth factor in angiogenesis of rheumatoid arthritis. J Rheumatol 1995;22:1624-1630.
4. Maruotti N, Cantatore FP, Crivellato E, Vacca A, Ribatti D: Angiogenesis in rheumatoid arthritis. Histol Histopathol 2006;21:557-566.
5. Kayakabe K, Kuroiwa T, Sakurai N, Ikeuchi H, Kadiombo AT, Sakairi T, Matsumoto T, Maeshima A, Hiromura K, Nojima Y: Interleukin-6 promotes destabilized angiogenesis by modulating angiopoietin expression in rheumatoid arthritis. Rheumatology (Oxford) 2012;51:1571-1579.
6. Clavel G, Bessis N, Boissier MC: Recent data on the role for angiogenesis in rheumatoid arthritis. Joint Bone Spine 2003;70:321-326.
7. Marrelli A, Cipriani P, Liakouli V, Carubbi F, Perricone C, Perricone R, Giacomelli R: Angiogenesis in rheumatoid arthritis: A disease specific process or a common response to chronic inflammation Autoimmun Rev 2011;10:595-598.
8. Morisada T, Kubota Y, Urano T, Suda T, Oike Y: Angiopoietins and angiopoietin-like proteins in angiogenesis. Endothelium 2006;13:71-79.
9. Kobayashi H, Lin PC: Angiopoietin/Tie2 signaling, tumor angiogenesis and inflammatory diseases. Front Biosci 2005;10:666-674.
10. Shahrara S, Volin MV, Connors MA, Haines GK, Koch AE: Differential expression of the angiogenic Tie receptor family in arthritic and normal synovial tissue. Arthritis Res 2002;4:201-208.
11. DeBusk LM, Chen Y, Nishishita T, Chen J, Thomas JW, Lin PC: Tie2 receptor tyrosine kinase, a major mediator of tumor necrosis factor alpha-induced angiogenesis in rheumatoid arthritis. Arthritis Rheum 2003;48:2461-2471.
12. Saber T, Veale DJ, Balogh E, McCormick J, NicAnUltaigh S, Connolly M, Fearon U: Toll-like receptor 2 induced angiogenesis and invasion is mediated through the Tie2 signalling pathway in rheumatoid arthritis. PLoS One 2011;6:e23540.
13. Krausz S, Garcia S, Ambarus CA, de Launay D, Foster M, Naiman B, Iverson W, Connor JR, Sleeman MA, Coyle AJ, Hamann J, Baeten D, Tak PP, Reedquist KA: Angiopoietin-2 promotes inflammatory activation of human macrophages and is essential for murine experimental arthritis. Ann Rheum Dis 2012;71:1402-1410.
14. van de Sande MG, de Launay D, de Hair MJ, Garcia S, van de Sande GP, Wijbrandts CA, Gerlag DM, Reedquist KA, Tak PP: Local synovial engagement of angiogenic TIE-2 is associated with the development of persistent erosive rheumatoid arthritis in patients with early arthritis. Arthritis Rheum 2013;65:3073-3083.
15. Chen Y, Donnelly E, Kobayashi H, Debusk LM, Lin PC: Gene therapy targeting the Tie2 function ameliorates collagen-induced arthritis and protects against bone destruction. Arthritis Rheum 2005;52:1585-1594.
16. Collison LW, Workman CJ, Kuo TT, Boyd K, Wang Y, Vignali KM, Cross R, Sehy D, Blumberg RS, Vignali DA: The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007;450:566-569.
17. Collison LW, Vignali DA: Interleukin-35: odd one out or part of the family Immunol Rev 2008;226:248-262.
18. Collison LW, Delgoffe GM, Guy CS, Vignali KM, Chaturvedi V, Fairweather D, Satoskar AR, Garcia KC, Hunter CA, Drake CG, Murray PJ, Vignali DA: The composition and signaling of the IL-35 receptor are unconventional. Nat Immunol 2012;13:290-299.
19. Chaturvedi V, Collison LW, Guy CS, Workman CJ, Vignali DA: Cutting edge: Human regulatory T cells require IL-35 to mediate suppression and infectious tolerance. J Immunol 2011;186:6661-6666.
20. Castellani ML, Anogeianaki A, Felaco P, Toniato E, De Lutiis MA, Shaik B, Fulcheri M, Vecchiet J, Tete S, Salini V, Theoharides TC, Caraffa A, Antinolfi P, Frydas I, Conti P, Cuccurullo C, Ciampoli C, Cerulli G, Kempuraj D: IL-35, an anti-inflammatory cytokine which expands CD4+CD25+ Treg Cells. J Biol Regul Homeost Agents 2010;24:131-135.
21. Li X, Mai J, Virtue A, Yin Y, Gong R, Sha X, Gutchigian S, Frisch A, Hodge I, Jiang X, Wang H, Yang XF: IL-35 is a novel responsive anti-inflammatory cytokine-a new system of categorizing anti-inflammatory cytokines. PLoS One 2012;7:e33628.
22. Niedbala W, Wei XQ, Cai B, Hueber AJ, Leung BP, McInnes IB, Liew FY: IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells. Eur J Immunol 2007;37:3021-3029.
23. Kochetkova I, Golden S, Holderness K, Callis G, Pascual DW: IL-35 stimulation of CD39+ regulatory T cells confers protection against collagen II-induced arthritis via the production of IL-10. J Immunol 2010;184:7144-7153.
24. Whitehead GS, Wilson RH, Nakano K, Burch LH, Nakano H, Cook DN: IL-35 production by inducible costimulator (ICOS)-positive regulatory T cells reverses established IL-17-dependent allergic airways disease. J Allergy Clin Immunol 2012;129:207-215 e201-205.
25. Sha X, Meng S, Li X, Xi H, Maddaloni M, Pascual DW, Shan H, Jiang X, Wang H, Yang XF: Interleukin-35 Inhibits Endothelial Cell Activation by Suppressing MAPK-AP-1 Pathway. J Biol Chem 2015;290:19307-19318.
26. Wang Z, Liu JQ, Liu Z, Shen R, Zhang G, Xu J, Basu S, Feng Y, Bai XF: Tumor-derived IL-35 promotes tumor growth by enhancing myeloid cell accumulation and angiogenesis. J Immunol 2013;190:2415-2423.
27. Liu C, Kong X, Li X, Guo W, Zhang C, Sun Y, Su X, Liu X, Lu A, Lin N: Wen Luo Yin inhibits angiogenesis in collagen-induced arthritis rat model and in vitro. J Ethnopharmacol 2013;149:478-489.
28. Fearon U, Mullan R, Markham T, Connolly M, Sullivan S, Poole AR, FitzGerald O, Bresnihan B, Veale DJ: Oncostatin M induces angiogenesis and cartilage degradation in rheumatoid arthritis synovial tissue and human cartilage cocultures. Arthritis Rheum 2006;54:3152-3162.
29. Xu D, Yan S, Wang H, Gu B, Sun K, Yang X, Sun B, Wang X: IL-29 Enhances LPS/TLR4-Mediated Inflammation in Rheumatoid Arthritis. Cell Physiol Biochem 2015;37:27-34.
30. Akhtar N, Dickerson EB, Auerbach R: The sponge/Matrigel angiogenesis assay. Angiogenesis 2002;5:75-80.
31. Zhang L, Yang N, Park JW, Katsaros D, Fracchioli S, Cao G, O'Brien-Jenkins A, Randall TC, Rubin SC, Coukos G: Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res 2003;63:3403-3412.
32. Firestein GS: Starving the synovium: Angiogenesis and inflammation in rheumatoid arthritis. J Clin Invest 1999;103:3-4.
33. Yan C, Kong D, Ge D, Zhang Y, Zhang X, Su C, Cao X: Mitomycin C induces apoptosis in rheumatoid arthritis fibroblast-like synoviocytes via a mitochondrial-mediated pathway. Cell Physiol Biochem 2015;35:1125-1136.
34. Maruotti N, Cantatore FP, Ribatti D: Putative effects of potentially anti-angiogenic drugs in rheumatic diseases. Eur J Clin Pharmacol 2014;70:135-140.
35. Carmeliet P, Jain RK: Angiogenesis in cancer and other diseases. Nature 2000;407:249-257.
36. Wu S, Li Y, Li Y, Yao L, Lin T, Jiang S, Shen H, Xia L, Lu J: Interleukin-35 attenuates collagen-induced arthritis through suppression of vascular endothelial growth factor and its receptors. Int Immunopharmacol 2016;34:71-77.
37. Lu J, Kasama T, Kobayashi K, Yoda Y, Shiozawa F, Hanyuda M, Negishi M, Ide H, Adachi M: Vascular endothelial growth factor expression and regulation of murine collagen-induced arthritis. J Immunol 2000;164:5922-5927.
38. Biniecka M, Connolly M, Gao W, Ng CT, Balogh E, Gogarty M, Santos L, Murphy E, Brayden D, Veale DJ, Fearon U: Redox-mediated angiogenesis in the hypoxic joint of inflammatory arthritis. Arthritis Rheumatol 2014;66:3300-3310.
39. Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y: Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem 1999;274:15732-15739.
40. Gao W, Sweeney C, Walsh C, Rooney P, McCormick J, Veale DJ, Fearon U: Notch signalling pathways mediate synovial angiogenesis in response to vascular endothelial growth factor and angiopoietin 2. Ann Rheum Dis 2013;72:1080-1088.