Skip to main content
Top
Published in: Arthritis Research & Therapy 2/2012

Open Access 01-04-2012 | Research article

Characterization of synovial angiogenesis in osteoarthritis patients and its modulation by chondroitin sulfate

Authors: Cécile Lambert, Marianne Mathy-Hartert, Jean-Emile Dubuc, Eulàlia Montell, Josep Vergés, Carine Munaut, Agnès Noël, Yves Henrotin

Published in: Arthritis Research & Therapy | Issue 2/2012

Login to get access

Abstract

Introduction

This work aimed at comparing the production of inflammatory and pro- and anti-angiogenic factors by normal/reactive (N/R) or inflammatory (I) areas of the osteoarthritic synovial membrane. The effects of interleukin (IL)-1β and chondroitin sulfate (CS) on the expression of pro- and anti-angiogenic factors by synovial fibroblasts cells (SFC) were also studied.

Methods

Biopsies from N/R or from I areas of osteoarthritic synovial membrane were collected at the time of surgery. The inflammatory status of the synovial membrane was characterized by the surgeon according to macroscopic criteria, including the synovial vascularization, the villi formation and the hypertrophic aspect of the tissue. We assessed the expression of CD45, von Willebrand factor and vascular endothelial growth factor (VEGF) antigen by immunohistochemistry in both N/R and I biopsies. The production of IL-6, -8, VEGF and thrombospondin (TSP)-1 by N/R or I synovial cells was quantified by ELISA. SFC were cultured in the absence or in the presence of IL-1β (1 ng/ml) and with or without CS (10, 50, 200 μg/ml). Gene expression of pro-angiogenic factors (VEGF, basic fibroblast growth factor (bFGF), nerve growth factor (NGF), matrix metalloproteinase (MMP)-2 and angiopoietin (ang)-1) and anti-angiogenic factors (vascular endothelial growth inhibitor (VEGI), TSP-1 and -2) were determined by real time RT-PCR. Production of VEGI and TSP-1 was also estimated by ELISA.

Results

Immunohistochemistry showed the increase of lymphocyte infiltration, vascular density and VEGF expression in I compared to N/R synovial biopsies. Synovial cells from I areas produced more IL-6, IL-8 and VEGF but less TSP-1 than cells isolated from N/R synovial biopsies. The expression of pro-angiogenic factors by SFC was stimulated by IL-1β. A time dependent regulation of the expression of anti-angiogenic factor genes was observed. IL-1β stimulated the expression of anti-angiogenic factor genes but inhibited it after 24 h. CS reversed the inhibitory effect of IL-1β on anti-angiogenic factors, VEGI and TSP-1.

Conclusions

We demonstrated that synovial biopsies from I areas expressed a pro-angiogenic phenotype. IL-1β induced an imbalance between pro- and anti-angiogenic factors in SFC and CS tended to normalize this IL-1β-induced imbalance, providing a new possible mechanism of action of this drug.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Haywood L, McWilliams DF, Pearson CI, Gill SE, Ganesan A, Wilson D, Walsh DA: Inflammation and angiogenesis in osteoarthritis. Arthritis Rheum. 2003, 48: 2173-2177. 10.1002/art.11094.CrossRefPubMed Haywood L, McWilliams DF, Pearson CI, Gill SE, Ganesan A, Wilson D, Walsh DA: Inflammation and angiogenesis in osteoarthritis. Arthritis Rheum. 2003, 48: 2173-2177. 10.1002/art.11094.CrossRefPubMed
3.
go back to reference Walsh DA, Bonnet CS, Turner EL, Wilson D, Situ M, McWilliams DF: Angiogenesis in the synovium and at the osteochondral junction in osteoarthritis. Osteoarthritis Cartilage. 2007, 15: 743-751. 10.1016/j.joca.2007.01.020.CrossRefPubMed Walsh DA, Bonnet CS, Turner EL, Wilson D, Situ M, McWilliams DF: Angiogenesis in the synovium and at the osteochondral junction in osteoarthritis. Osteoarthritis Cartilage. 2007, 15: 743-751. 10.1016/j.joca.2007.01.020.CrossRefPubMed
4.
go back to reference Papetti M, Herman IM: Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol. 2002, 282: C947-970.CrossRefPubMed Papetti M, Herman IM: Mechanisms of normal and tumor-derived angiogenesis. Am J Physiol Cell Physiol. 2002, 282: C947-970.CrossRefPubMed
5.
go back to reference Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D: Nerve growth factor as an angiogenic factor. Microvasc Res. 2008, 75: 135-141. 10.1016/j.mvr.2007.07.004.CrossRefPubMed Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D: Nerve growth factor as an angiogenic factor. Microvasc Res. 2008, 75: 135-141. 10.1016/j.mvr.2007.07.004.CrossRefPubMed
6.
go back to reference Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD: Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996, 87: 1171-1180. 10.1016/S0092-8674(00)81813-9.CrossRefPubMed Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD: Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996, 87: 1171-1180. 10.1016/S0092-8674(00)81813-9.CrossRefPubMed
7.
go back to reference Pepper MS: Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol. 2001, 21: 1104-1117. 10.1161/hq0701.093685.CrossRefPubMed Pepper MS: Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol. 2001, 21: 1104-1117. 10.1161/hq0701.093685.CrossRefPubMed
9.
go back to reference Yu J, Tian S, Metheny-Barlow L, Chew LJ, Hayes AJ, Pan H, Yu GL, Li LY: Modulation of endothelial cell growth arrest and apoptosis by vascular endothelial growth inhibitor. Circ Res. 2001, 89: 1161-1167. 10.1161/hh2401.101909.CrossRefPubMed Yu J, Tian S, Metheny-Barlow L, Chew LJ, Hayes AJ, Pan H, Yu GL, Li LY: Modulation of endothelial cell growth arrest and apoptosis by vascular endothelial growth inhibitor. Circ Res. 2001, 89: 1161-1167. 10.1161/hh2401.101909.CrossRefPubMed
10.
go back to reference Koch AE, Harlow LA, Haines GK, Amento EP, Unemori EN, Wong WL, Pope RM, Ferrara N: Vascular endothelial growth factor. A cytokine modulating endothelial function in rheumatoid arthritis. J Immunol. 1994, 152: 4149-4156.PubMed Koch AE, Harlow LA, Haines GK, Amento EP, Unemori EN, Wong WL, Pope RM, Ferrara N: Vascular endothelial growth factor. A cytokine modulating endothelial function in rheumatoid arthritis. J Immunol. 1994, 152: 4149-4156.PubMed
11.
go back to reference Nakashima M, Eguchi K, Aoyagi T, Yamashita I, Ida H, Sakai M, Shimada H, Kawabe Y, Nagataki S, Koji T: Expression of basic fibroblast growth factor in synovial tissues from patients with rheumatoid arthritis: detection by immunohistological staining and in situ hybridisation. Ann Rheum Dis. 1994, 53: 45-50. 10.1136/ard.53.1.45.PubMedCentralCrossRefPubMed Nakashima M, Eguchi K, Aoyagi T, Yamashita I, Ida H, Sakai M, Shimada H, Kawabe Y, Nagataki S, Koji T: Expression of basic fibroblast growth factor in synovial tissues from patients with rheumatoid arthritis: detection by immunohistological staining and in situ hybridisation. Ann Rheum Dis. 1994, 53: 45-50. 10.1136/ard.53.1.45.PubMedCentralCrossRefPubMed
12.
go back to reference Barthel C, Yeremenko N, Jacobs R, Schmidt RE, Bernateck M, Zeidler H, Tak PP, Baeten D, Rihl M: Nerve growth factor and receptor expression in rheumatoid arthritis and spondyloarthritis. Arthritis Res Ther. 2009, 11: R82-10.1186/ar2716.PubMedCentralCrossRefPubMed Barthel C, Yeremenko N, Jacobs R, Schmidt RE, Bernateck M, Zeidler H, Tak PP, Baeten D, Rihl M: Nerve growth factor and receptor expression in rheumatoid arthritis and spondyloarthritis. Arthritis Res Ther. 2009, 11: R82-10.1186/ar2716.PubMedCentralCrossRefPubMed
13.
go back to reference 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. 10.1186/ar407.PubMedCentralCrossRefPubMed 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. 10.1186/ar407.PubMedCentralCrossRefPubMed
14.
go back to reference Goldbach-Mansky R, Lee JM, Hoxworth JM, Smith D, Duray P, Schumacher RH, Yarboro CH, Klippel J, Kleiner D, El-Gabalawy HS: Active synovial matrix metalloproteinase-2 is associated with radiographic erosions in patients with early synovitis. Arthritis Res. 2000, 2: 145-153. 10.1186/ar79.PubMedCentralCrossRefPubMed Goldbach-Mansky R, Lee JM, Hoxworth JM, Smith D, Duray P, Schumacher RH, Yarboro CH, Klippel J, Kleiner D, El-Gabalawy HS: Active synovial matrix metalloproteinase-2 is associated with radiographic erosions in patients with early synovitis. Arthritis Res. 2000, 2: 145-153. 10.1186/ar79.PubMedCentralCrossRefPubMed
15.
go back to reference Gotis-Graham I, Hogg PJ, McNeil HP: Significant correlation between thrombospondin 1 and serine proteinase expression in rheumatoid synovium. Arthritis Rheum. 1997, 40: 1780-1787. 10.1002/art.1780401009.CrossRefPubMed Gotis-Graham I, Hogg PJ, McNeil HP: Significant correlation between thrombospondin 1 and serine proteinase expression in rheumatoid synovium. Arthritis Rheum. 1997, 40: 1780-1787. 10.1002/art.1780401009.CrossRefPubMed
16.
go back to reference Park YW, Kang YM, Butterfield J, Detmar M, Goronzy JJ, Weyand CM: Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in rheumatoid arthritis. Am J Pathol. 2004, 165: 2087-2098. 10.1016/S0002-9440(10)63259-2.PubMedCentralCrossRefPubMed Park YW, Kang YM, Butterfield J, Detmar M, Goronzy JJ, Weyand CM: Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in rheumatoid arthritis. Am J Pathol. 2004, 165: 2087-2098. 10.1016/S0002-9440(10)63259-2.PubMedCentralCrossRefPubMed
17.
go back to reference Cassatella MA, Pereira-da-Silva G, Tinazzi I, Facchetti F, Scapini P, Calzetti F, Tamassia N, Wei P, Nardelli B, Roschke V, Vecchi A, Mantovani A, Bambara LM, Edwards SW, Carletto A: Soluble TNF-like cytokine (TL1A) production by immune complexes stimulated monocytes in rheumatoid arthritis. J Immunol. 2007, 178: 7325-7333. Erratum in J Immunol 2007, 179:1390. da Silva, Gabriela Pereira (corrected to Pereira da-Silva, Gabriela)CrossRefPubMed Cassatella MA, Pereira-da-Silva G, Tinazzi I, Facchetti F, Scapini P, Calzetti F, Tamassia N, Wei P, Nardelli B, Roschke V, Vecchi A, Mantovani A, Bambara LM, Edwards SW, Carletto A: Soluble TNF-like cytokine (TL1A) production by immune complexes stimulated monocytes in rheumatoid arthritis. J Immunol. 2007, 178: 7325-7333. Erratum in J Immunol 2007, 179:1390. da Silva, Gabriela Pereira (corrected to Pereira da-Silva, Gabriela)CrossRefPubMed
18.
go back to reference Leeb BF, Schweitzer H, Montag K, Smolen JS: A metaanalysis of chondroitin sulfate in the treatment of osteoarthritis. J Rheumatol. 2000, 27: 205-211.PubMed Leeb BF, Schweitzer H, Montag K, Smolen JS: A metaanalysis of chondroitin sulfate in the treatment of osteoarthritis. J Rheumatol. 2000, 27: 205-211.PubMed
19.
go back to reference McAlindon TE, LaValley MP, Gulin JP, Felson DT: Glucosamine and chondroitin for treatment of osteoarthritis: a systematic quality assessment and meta-analysis. JAMA. 2000, 283: 1469-1475. 10.1001/jama.283.11.1469.CrossRefPubMed McAlindon TE, LaValley MP, Gulin JP, Felson DT: Glucosamine and chondroitin for treatment of osteoarthritis: a systematic quality assessment and meta-analysis. JAMA. 2000, 283: 1469-1475. 10.1001/jama.283.11.1469.CrossRefPubMed
20.
go back to reference Richy F, Bruyere O, Ethgen O, Cucherat M, Henrotin Y, Reginster JY: Structural and symptomatic efficacy of glucosamine and chondroitin in knee osteoarthritis: a comprehensive meta-analysis. Arch Intern Med. 2003, 163: 1514-1522. 10.1001/archinte.163.13.1514.CrossRefPubMed Richy F, Bruyere O, Ethgen O, Cucherat M, Henrotin Y, Reginster JY: Structural and symptomatic efficacy of glucosamine and chondroitin in knee osteoarthritis: a comprehensive meta-analysis. Arch Intern Med. 2003, 163: 1514-1522. 10.1001/archinte.163.13.1514.CrossRefPubMed
21.
go back to reference Hochberg MC: Structure-modifying effects of chondroitin sulfate in knee osteoarthritis: an updated meta-analysis of randomized placebo-controlled trials of 2-year duration. Osteoarthritis Cartilage. 2010, 18 (Suppl 1): S28-31.CrossRefPubMed Hochberg MC: Structure-modifying effects of chondroitin sulfate in knee osteoarthritis: an updated meta-analysis of randomized placebo-controlled trials of 2-year duration. Osteoarthritis Cartilage. 2010, 18 (Suppl 1): S28-31.CrossRefPubMed
22.
go back to reference Hochberg MC, Zhan M, Langenberg P: The rate of decline of joint space width in patients with osteoarthritis of the knee: a systematic review and meta-analysis of randomized placebo-controlled trials of chondroitin sulfate. Curr Med Res Opin. 2008, 24: 3029-3035. 10.1185/03007990802434932.CrossRefPubMed Hochberg MC, Zhan M, Langenberg P: The rate of decline of joint space width in patients with osteoarthritis of the knee: a systematic review and meta-analysis of randomized placebo-controlled trials of chondroitin sulfate. Curr Med Res Opin. 2008, 24: 3029-3035. 10.1185/03007990802434932.CrossRefPubMed
23.
go back to reference Monfort J, Pelletier JP, Garcia-Giralt N, Martel-Pelletier J: Biochemical basis of the effect of chondroitin sulphate on osteoarthritis articular tissues. Ann Rheum Dis. 2008, 67: 735-740. 10.1136/ard.2006.068882.CrossRefPubMed Monfort J, Pelletier JP, Garcia-Giralt N, Martel-Pelletier J: Biochemical basis of the effect of chondroitin sulphate on osteoarthritis articular tissues. Ann Rheum Dis. 2008, 67: 735-740. 10.1136/ard.2006.068882.CrossRefPubMed
24.
go back to reference Martel-Pelletier J, Kwan Tat S, Pelletier JP: Effects of chondroitin sulfate in the pathophysiology of the osteoarthritic joint: a narrative review. Osteoarthritis Cartilage. 2010, 18 (Suppl 1): S7-11.CrossRefPubMed Martel-Pelletier J, Kwan Tat S, Pelletier JP: Effects of chondroitin sulfate in the pathophysiology of the osteoarthritic joint: a narrative review. Osteoarthritis Cartilage. 2010, 18 (Suppl 1): S7-11.CrossRefPubMed
25.
go back to reference Lauder RM: Chondroitin sulphate: a complex molecule with potential impacts on a wide range of biological systems. Complement Ther Med. 2009, 17: 56-62. 10.1016/j.ctim.2008.08.004.CrossRefPubMed Lauder RM: Chondroitin sulphate: a complex molecule with potential impacts on a wide range of biological systems. Complement Ther Med. 2009, 17: 56-62. 10.1016/j.ctim.2008.08.004.CrossRefPubMed
26.
go back to reference Clegg DO, Reda DJ, Harris CL, Klein MA, O'Dell JR, Hooper MM, Bradley JD, Bingham CO, Weisman MH, Jackson CG, Lane NE, Cush JJ, Moreland LW, Schumacher HR, Oddis CV, Wolfe F, Molitor JA, Yocum DE, Schnitzer TJ, Furst DE, Sawitzke AD, Shi H, Brandt KD, Moskowitz RW, Williams HJ: Glucosamine, chondroitin sulfate, and the two in combination for painful knee osteoarthritis. N Engl J Med. 2006, 354: 795-808. 10.1056/NEJMoa052771.CrossRefPubMed Clegg DO, Reda DJ, Harris CL, Klein MA, O'Dell JR, Hooper MM, Bradley JD, Bingham CO, Weisman MH, Jackson CG, Lane NE, Cush JJ, Moreland LW, Schumacher HR, Oddis CV, Wolfe F, Molitor JA, Yocum DE, Schnitzer TJ, Furst DE, Sawitzke AD, Shi H, Brandt KD, Moskowitz RW, Williams HJ: Glucosamine, chondroitin sulfate, and the two in combination for painful knee osteoarthritis. N Engl J Med. 2006, 354: 795-808. 10.1056/NEJMoa052771.CrossRefPubMed
27.
go back to reference Ayral X: Diagnostic and quantitative arthroscopy: quantitative arthroscopy. Baillieres Clin Rheumatol. 1996, 10: 477-494. 10.1016/S0950-3579(96)80045-8.CrossRefPubMed Ayral X: Diagnostic and quantitative arthroscopy: quantitative arthroscopy. Baillieres Clin Rheumatol. 1996, 10: 477-494. 10.1016/S0950-3579(96)80045-8.CrossRefPubMed
28.
go back to reference Sellam J, Berenbaum F: The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis. Nat Rev Rheumatol. 2010, 6: 625-635. 10.1038/nrrheum.2010.159.CrossRefPubMed Sellam J, Berenbaum F: The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis. Nat Rev Rheumatol. 2010, 6: 625-635. 10.1038/nrrheum.2010.159.CrossRefPubMed
29.
go back to reference Labarca C, Paigen K: A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980, 102: 344-352. 10.1016/0003-2697(80)90165-7.CrossRefPubMed Labarca C, Paigen K: A simple, rapid, and sensitive DNA assay procedure. Anal Biochem. 1980, 102: 344-352. 10.1016/0003-2697(80)90165-7.CrossRefPubMed
30.
go back to reference Bonnet CS, Walsh DA: Osteoarthritis, angiogenesis and inflammation. Rheumatology (Oxford). 2005, 44: 7-16. 10.1093/rheumatology/keh344.CrossRef Bonnet CS, Walsh DA: Osteoarthritis, angiogenesis and inflammation. Rheumatology (Oxford). 2005, 44: 7-16. 10.1093/rheumatology/keh344.CrossRef
31.
go back to reference Pearle AD, Scanzello CR, George S, Mandl LA, DiCarlo EF, Peterson M, Sculco TP, Crow MK: Elevated high-sensitivity C-reactive protein levels are associated with local inflammatory findings in patients with osteoarthritis. Osteoarthritis Cartilage. 2007, 15: 516-523. 10.1016/j.joca.2006.10.010.CrossRefPubMed Pearle AD, Scanzello CR, George S, Mandl LA, DiCarlo EF, Peterson M, Sculco TP, Crow MK: Elevated high-sensitivity C-reactive protein levels are associated with local inflammatory findings in patients with osteoarthritis. Osteoarthritis Cartilage. 2007, 15: 516-523. 10.1016/j.joca.2006.10.010.CrossRefPubMed
32.
go back to reference Hsieh JL, Shen PC, Shiau AL, Jou IM, Lee CH, Wang CR, Teo ML, Wu CL: Intraarticular gene transfer of thrombospondin-1 suppresses the disease progression of experimental osteoarthritis. J Orthop Res. 2010, 28: 1300-1306. 10.1002/jor.21134.CrossRefPubMed Hsieh JL, Shen PC, Shiau AL, Jou IM, Lee CH, Wang CR, Teo ML, Wu CL: Intraarticular gene transfer of thrombospondin-1 suppresses the disease progression of experimental osteoarthritis. J Orthop Res. 2010, 28: 1300-1306. 10.1002/jor.21134.CrossRefPubMed
33.
go back to reference Jackson JR, Minton JA, Ho ML, Wei N, Winkler JD: Expression of vascular endothelial growth factor in synovial fibroblasts is induced by hypoxia and interleukin 1beta. J Rheumatol. 1997, 24: 1253-1259.PubMed Jackson JR, Minton JA, Ho ML, Wei N, Winkler JD: Expression of vascular endothelial growth factor in synovial fibroblasts is induced by hypoxia and interleukin 1beta. J Rheumatol. 1997, 24: 1253-1259.PubMed
34.
go back to reference Manni L, Lundeberg T, Fiorito S, Bonini S, Vigneti E, Aloe L: Nerve growth factor release by human synovial fibroblasts prior to and following exposure to tumor necrosis factor-alpha, interleukin-1 beta and cholecystokinin-8: the possible role of NGF in the inflammatory response. Clin Exp Rheumatol. 2003, 21: 617-624.PubMed Manni L, Lundeberg T, Fiorito S, Bonini S, Vigneti E, Aloe L: Nerve growth factor release by human synovial fibroblasts prior to and following exposure to tumor necrosis factor-alpha, interleukin-1 beta and cholecystokinin-8: the possible role of NGF in the inflammatory response. Clin Exp Rheumatol. 2003, 21: 617-624.PubMed
35.
go back to reference Gravallese EM, Pettit AR, Lee R, Madore R, Manning C, Tsay A, Gaspar J, Goldring MB, Goldring SR, Oettgen P: Angiopoietin-1 is expressed in the synovium of patients with rheumatoid arthritis and is induced by tumour necrosis factor alpha. Ann Rheum Dis. 2003, 62: 100-107. 10.1136/ard.62.2.100.PubMedCentralCrossRefPubMed Gravallese EM, Pettit AR, Lee R, Madore R, Manning C, Tsay A, Gaspar J, Goldring MB, Goldring SR, Oettgen P: Angiopoietin-1 is expressed in the synovium of patients with rheumatoid arthritis and is induced by tumour necrosis factor alpha. Ann Rheum Dis. 2003, 62: 100-107. 10.1136/ard.62.2.100.PubMedCentralCrossRefPubMed
36.
go back to reference Lyons-Giordano B, Kefalides NA, Brinker JM, Pratta MA, Arner EC: The effects of interleukin-1 on the expression of thrombospondin and fibronectin by rabbit articular chondrocytes. Exp Cell Res. 1991, 195: 462-467. 10.1016/0014-4827(91)90397-D.CrossRefPubMed Lyons-Giordano B, Kefalides NA, Brinker JM, Pratta MA, Arner EC: The effects of interleukin-1 on the expression of thrombospondin and fibronectin by rabbit articular chondrocytes. Exp Cell Res. 1991, 195: 462-467. 10.1016/0014-4827(91)90397-D.CrossRefPubMed
37.
go back to reference Morandi V, Cherradi SE, Lambert S, Fauvel-Lafeve F, Legrand YJ, Legrand C: Proinflammatory cytokines (interleukin-1 beta and tumor necrosis factor-alpha) down regulate synthesis and secretion of thrombospondin by human endothelial cells. J Cell Physiol. 1994, 160: 367-377. 10.1002/jcp.1041600218.CrossRefPubMed Morandi V, Cherradi SE, Lambert S, Fauvel-Lafeve F, Legrand YJ, Legrand C: Proinflammatory cytokines (interleukin-1 beta and tumor necrosis factor-alpha) down regulate synthesis and secretion of thrombospondin by human endothelial cells. J Cell Physiol. 1994, 160: 367-377. 10.1002/jcp.1041600218.CrossRefPubMed
38.
go back to reference Migone TS, Zhang J, Luo X, Zhuang L, Chen C, Hu B, Hong JS, Perry JW, Chen SF, Zhou JX, Cho YH, Ullrich S, Kanakaraj P, Carrell J, Boyd E, Olsen HS, Hu G, Pukac L, Liu D, Ni J, Kim S, Gentz R, Feng P, Moore PA, Ruben SM, Wei P: TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator. Immunity. 2002, 16: 479-492. 10.1016/S1074-7613(02)00283-2.CrossRefPubMed Migone TS, Zhang J, Luo X, Zhuang L, Chen C, Hu B, Hong JS, Perry JW, Chen SF, Zhou JX, Cho YH, Ullrich S, Kanakaraj P, Carrell J, Boyd E, Olsen HS, Hu G, Pukac L, Liu D, Ni J, Kim S, Gentz R, Feng P, Moore PA, Ruben SM, Wei P: TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator. Immunity. 2002, 16: 479-492. 10.1016/S1074-7613(02)00283-2.CrossRefPubMed
39.
go back to reference Iovu M, Dumais G, du Souich P: Anti-inflammatory activity of chondroitin sulfate. Osteoarthritis Cartilage. 2008, 16 (Suppl 3): S14-18.CrossRefPubMed Iovu M, Dumais G, du Souich P: Anti-inflammatory activity of chondroitin sulfate. Osteoarthritis Cartilage. 2008, 16 (Suppl 3): S14-18.CrossRefPubMed
41.
go back to reference Liu Y, Yang H, Otaka K, Takatsuki H, Sakanishi A: Effects of vascular endothelial growth factor (VEGF) and chondroitin sulfate A on human monocytic THP-1 cell migration. Colloids Surf B Biointerfaces. 2005, 43: 216-220. 10.1016/j.colsurfb.2005.04.011.CrossRefPubMed Liu Y, Yang H, Otaka K, Takatsuki H, Sakanishi A: Effects of vascular endothelial growth factor (VEGF) and chondroitin sulfate A on human monocytic THP-1 cell migration. Colloids Surf B Biointerfaces. 2005, 43: 216-220. 10.1016/j.colsurfb.2005.04.011.CrossRefPubMed
Metadata
Title
Characterization of synovial angiogenesis in osteoarthritis patients and its modulation by chondroitin sulfate
Authors
Cécile Lambert
Marianne Mathy-Hartert
Jean-Emile Dubuc
Eulàlia Montell
Josep Vergés
Carine Munaut
Agnès Noël
Yves Henrotin
Publication date
01-04-2012
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 2/2012
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar3771

Other articles of this Issue 2/2012

Arthritis Research & Therapy 2/2012 Go to the issue