Angiogenesis in rheumatoid arthritis is fostered directly by toll-like receptor 5 ligation and indirectly through interleukin-17 induction

Arthritis and Rheumatism

Volumn 65, Issue 8, 2013, Pages 2024-2036

  Kim, Seung Jae ^a   Chen, Zhenlong ^a   Chamberlain, Nathan D ^a   Volin, Michael V ^b   Swedler, William ^a   Volkov, Suncica ^a   Sweiss, Nadera ^a   Shahrara, Shiva ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b MIDWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; METHEMOGLOBIN; TOLL LIKE RECEPTOR 5; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANKLE; ARTICLE; BONE EROSION; BONE MARROW CELL; CELL INFILTRATION; CELL MIGRATION; CLINICAL ASSESSMENT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; HEMOGLOBIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; POLARIZATION; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SPLEEN CELL; SYNOVIAL FLUID; SYNOVIUM; TH17 CELL; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; FLAGELLIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERLEUKIN-17; JOINTS; LEUKOCYTES, MONONUCLEAR; MICE; NEOVASCULARIZATION, PATHOLOGIC; SPLEEN; SYNOVIAL FLUID; TH17 CELLS; TOLL-LIKE RECEPTOR 5;

EID: 84881322272     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.37992     Document Type: Article

References (50)

1. Brentano F, Kyburz D, Schorr O, Gay R, Gay S,. The role of Toll-like receptor signalling in the pathogenesis of arthritis. Cell Immunol 2005; 233: 90-6.
2. Drexler SK, Sacre SM, Foxwell BM,. Toll-like receptors: a new target in rheumatoid arthritis? Expert Rev Clin Immunol 2006; 2: 585-99.
3. Iwahashi M, Yamamura M, Aita T, Okamoto A, Ueno A, Ogawa N, et al. Expression of Toll-like receptor 2 on CD16+ blood monocytes and synovial tissue macrophages in rheumatoid arthritis. Arthritis Rheum 2004; 50: 1457-67.
4. Radstake TR, Roelofs MF, Jenniskens YM, Oppers-Walgreen B, van Riel PL, Barrera P, et al. Expression of Toll-like receptors 2 and 4 in rheumatoid synovial tissue and regulation by proinflammatory cytokines interleukin-12 and interleukin-18 via interferon-γ. Arthritis Rheum 2004; 50: 3856-65.
5. Seibl R, Birchler T, Loeliger S, Hossle JP, Gay RE, Saurenmann T, et al. Expression and regulation of Toll-like receptor 2 in rheumatoid arthritis synovium. Am J Pathol 2003; 162: 1221-7.
6. Drexler SK, Foxwell BM,. The role of toll-like receptors in chronic inflammation. Int J Biochem Cell Biol 2010; 42: 506-18.
7. Huang QQ, Pope RM,. The role of toll-like receptors in rheumatoid arthritis. Curr Rheumatol Rep 2009; 11: 357-64.
8. Kim KW, Cho ML, Lee SH, Oh HJ, Kang CM, Ju JH, et al. Human rheumatoid synovial fibroblasts promote osteoclastogenic activity by activating RANKL via TLR-2 and TLR-4 activation. Immunol Lett 2007; 110: 54-64.
9. Grote K, Schutt H, Schieffer B,. Toll-like receptors in angiogenesis. ScientificWorldJournal 2011; 11: 981-91.
10. Chamberlain ND, Vila OM, Volin MV, Volkov S, Pope RM, Swedler W, et al. TLR5, a novel and unidentified inflammatory mediator in rheumatoid arthritis that correlates with disease activity score and joint TNF-α levels. J Immunol 2012; 189: 475-83.
11. 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.
12. Koch AE,. Angiogenesis: implications for rheumatoid arthritis. Arthritis Rheum 1998; 41: 951-62.
13. Szekanecz Z, Koch AE,. Angiogenesis and its targeting in rheumatoid arthritis. Vascul Pharmacol 2009; 51: 1-7.
14. Szekanecz Z, Pakozdi A, Szentpetery A, Besenyei T, Koch AE,. Chemokines and angiogenesis in rheumatoid arthritis. Front Biosci (Elite Ed) 2009; 1: 44-51.
15. Cho ML, Ju JH, Kim HR, Oh HJ, Kang CM, Jhun JY, et al. Toll-like receptor 2 ligand mediates the upregulation of angiogenic factor, vascular endothelial growth factor and interleukin-8/CXCL8 in human rheumatoid synovial fibroblasts. Immunol Lett 2007; 108: 121-8.
16. Saber T, Veale DJ, Balogh E, McCormick J, NicAnUltaigh S, Connolly M, et al. Toll-like receptor 2 induced angiogenesis and invasion is mediated through the Tie2 signalling pathway in rheumatoid arthritis. PLoS ONE 2011; 6: e23540.
17. Ramanathan M, Pinhal-Enfield G, Hao I, Leibovich SJ,. Synergistic up-regulation of vascular endothelial growth factor (VEGF) expression in macrophages by adenosine A2A receptor agonists and endotoxin involves transcriptional regulation via the hypoxia response element in the VEGF promoter. Mol Biol Cell 2007; 18: 14-23.
18. Pickens SR, Volin MV, Mandelin AM II, Kolls JK, Pope RM, Shahrara S,. IL-17 contributes to angiogenesis in rheumatoid arthritis. J Immunol 2010; 184: 3233-41.
19. Pickens SR, Chamberlain ND, Volin MV, Pope RM, Talarico NE, Mandelin AM II, et al. Role of the CCL21 and CCR7 pathway in rheumatoid arthritis angiogenesis. Arthritis Rheum 2012; 64: 2471-81.
20. Park CC, Morel JC, Amin MA, Connors MA, Harlow LA, Koch AE,. Evidence of IL-18 as a novel angiogenic mediator. J Immunol 2001; 167: 1644-53.
21. Haas CS, Amin MA, Ruth JH, Allen BL, Ahmed S, Pakozdi A, et al. In vivo inhibition of angiogenesis by interleukin-13 gene therapy in a rat model of rheumatoid arthritis. Arthritis Rheum 2007; 56: 2535-48.
22. Shahrara S, Pickens SR, Mandelin AM II, Karpus WJ, Huang Q, Kolls JK, et al. IL-17-mediated monocyte migration occurs partially through CC chemokine ligand 2/monocyte chemoattractant protein-1 induction. J Immunol 2010; 184: 4479-87.
23. 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.
24. Pickens SR, Chamberlain ND, Volin MV, Pope RM, Mandelin AM II, Shahrara S,. Characterization of CCL19 and CCL21 in rheumatoid arthritis. Arthritis Rheum 2011; 63: 914-22.
25. Pickens SR, Chamberlain ND, Volin MV, Pope RM, Talarico NE, Mandelin AM II, et al. Characterization of interleukin-7 and interleukin-7 receptor in the pathogenesis of rheumatoid arthritis. Arthritis Rheum 2011; 63: 2884-93.
26. Roelofs MF, Joosten LA, Abdollahi-Roodsaz S, van Lieshout AW, Sprong T, van den Hoogen FH, et al. The expression of Toll-like receptors 3 and 7 in rheumatoid arthritis synovium is increased and costimulation of Toll-like receptors 3, 4, and 7/8 results in synergistic cytokine production by dendritic cells. Arthritis Rheum 2005; 52: 2313-22.
27. Chamberlain ND, Kim SJ, Vila OM, Volin MV, Volkov S, Pope RM, et al. Ligation of TLR7 by rheumatoid arthritis synovial fluid single strand RNA induces transcription of TNFα in monocytes. Ann Rheum Dis 2012; 72: 418-26.
28. Rhee SH, Im E, Pothoulakis C,. Toll-like receptor 5 engagement modulates tumor development and growth in a mouse xenograft model of human colon cancer. Gastroenterology 2008; 135: 518-28.
29. Kumar P, Amin MA, Harlow LA, Polverini PJ, Koch AE,. Src and phosphatidylinositol 3-kinase mediate soluble E-selectin-induced angiogenesis. Blood 2003; 101: 3960-8.
30. Amin MA, Haas CS, Zhu K, Mansfield PJ, Kim MJ, Lackowski NP, et al. Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFκB. Blood 2006; 107: 2252-61.
31. Rabquer BJ, Amin MA, Teegala N, Shaheen MK, Tsou PS, Ruth JH, et al. Junctional adhesion molecule-C is a soluble mediator of angiogenesis. J Immunol 2010; 185: 1777-85.
32. Ulici V, Hoenselaar KD, Agoston H, McErlain DD, Umoh J, Chakrabarti S, et al. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification. Bone 2009; 45: 1133-45.
33. Moran EM, Connolly M, Gao W, McCormick J, Fearon U, Veale DJ,. Interleukin-17A induction of angiogenesis, cell migration, and cytoskeletal rearrangement. Arthritis Rheum 2011; 63: 3263-73.
34. Chan A, Akhtar M, Brenner M, Zheng Y, Gulko PS, Symons M,. The GTPase Rac regulates the proliferation and invasion of fibroblast-like synoviocytes from rheumatoid arthritis patients. Mol Med 2007; 13: 297-304.
35. Abdollahi-Roodsaz S, Joosten LA, Roelofs MF, Radstake TR, Matera G, Popa C, et al. Inhibition of Toll-like receptor 4 breaks the inflammatory loop in autoimmune destructive arthritis. Arthritis Rheum 2007; 56: 2957-67.
36. Abdollahi-Roodsaz S, Joosten LA, Koenders MI, Devesa I, Roelofs MF, Radstake TR, et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J Clin Invest 2008; 118: 205-16.
37. Abdollahi-Roodsaz S, Joosten LA, Helsen MM, Walgreen B, van Lent PL, van den Bersselaar LA, et al. Shift from Toll-like receptor 2 (TLR-2) toward TLR-4 dependency in the erosive stage of chronic streptococcal cell wall arthritis coincident with TLR-4-mediated interleukin-17 production. Arthritis Rheum 2008; 58: 3753-64.
38. Yarilina A, DiCarlo E, Ivashkiv LB,. Suppression of the effector phase of inflammatory arthritis by double-stranded RNA is mediated by type I IFNs. J Immunol 2007; 178: 2204-11.
39. Alzabin S, Kong P, Medghalchi M, Palfreeman A, Williams R, Sacre S,. Investigation of the role of endosomal Toll-like receptors in murine collagen-induced arthritis reveals a potential role for TLR7 in disease maintenance. Arthritis Res Ther 2012; 14: R142.
40. Roses RE, Xu S, Xu M, Koldovsky U, Koski G, Czerniecki BJ,. Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists. J Immunol 2008; 181: 5120-7.
41. Benwell RK, Lee DR,. Essential and synergistic roles of IL1 and IL6 in human Th17 differentiation directed by TLR ligand-activated dendritic cells. Clin Immunol 2010; 134: 178-87.
42. Vijay-Kumar M, Wu H, Jones R, Grant G, Babbin B, King TP, et al. Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol 2006; 169: 1686-700.
43. Carvalho FA, Koren O, Goodrich JK, Johansson ME, Nalbantoglu I, Aitken JD, et al. Transient inability to manage proteobacteria promotes chronic gut inflammation in TLR5-deficient mice. Cell Host Microbe 2012; 12: 139-52.
44. Carvalho FA, Nalbantoglu I, Ortega-Fernandez S, Aitken JD, Su Y, Koren O, et al. Interleukin-1β (IL-1β) promotes susceptibility of Toll-like receptor 5 (TLR5) deficient mice to colitis. Gut 2012; 61: 373-84.
45. Pinhal-Enfield G, Ramanathan M, Hasko G, Vogel SN, Salzman AL, Boons GJ, et al. An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A(2A) receptors. Am J Pathol 2003; 163: 711-21.
46. Park JH, Yoon HE, Jeon DI, Ahn SG, Yoon JH,. Activation of TLR2 and TLR5 did not affect tumor progression of an oral squamous cell carcinoma, YD-10B cells. J Oral Pathol Med 2010; 39: 781-5.
47. Jiang BH, Zheng JZ, Aoki M, Vogt PK,. Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc Natl Acad Sci U S A 2000; 97: 1749-53.
48. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 1999; 98: 147-57.
49. Pickens SR, Chamberlain ND, Volin MV, Gonzalez M, Pope RM, Mandelin AM II, et al. Anti-CXCL5 therapy ameliorates IL-17-induced arthritis by decreasing joint vascularization. Angiogenesis 2011; 14: 443-55.
50. Starnes T, Robertson MJ, Sledge G, Kelich S, Nakshatri H, Broxmeyer HE, et al. Cutting edge: IL-17F, a novel cytokine selectively expressed in activated T cells and monocytes, regulates angiogenesis and endothelial cell cytokine production. J Immunol 2001; 167: 4137-40.