Advertisement

Angiogenesis in the inflammation of arthritis

  • David A. Walsh
  • Eirlys Williams
Part of the Progress in Inflammation Research book series (PIR)

Abstract

Arthritis is a major source of pain, distress, disability and lost productivity to many members of society. People may be afflicted by various forms of arthritis. Osteo-arthritis (OA) is almost universal in older people, with one joint or more being affected in almost everyone by the age of seventy. A process similar to OA can affect the spine (spondylosis) and is associated with back or neck pain. Rheumatoid arthritis (RA) affects 2–3% of western populations. Other forms of arthritis include the seronegative spondarthropathies associated with psoriasis, inflammatory bowel disease, anklosing spondylitis and reactive to infections. These each occur in smaller proportions of the population, but have major consequences for those who are affected. Currently available treatments help to control symptoms and may even limit the progression of joint damage, but none has so far been proven to cure joint disease. As with other chronic, incurable diseases, the burden of arthritis increases in ageing populations.

Keywords

Rheumatoid Arthritis Articular Surface Fibrovascular Tissue Cell Brown MAGNI FICATION 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Hamilton E, Pattrick M, Hornby J, Derrick G, Doherty M (1990) Synovial fluid calcium pyrophosphate dihydrate crystals and alizarin red positivity: Analysis of 3000 samples. Br J Rheumatol 29: 101–104PubMedCrossRefGoogle Scholar
  2. 2.
    Spector TD, Hart DJ, Nandra D, Doyle DV, Mackillop N, Gallimore JR, Pepys MB (1997) Low-level increases in serum C-reactive protein are present in early osteoarthritis of the knee and predict progressive disease. Arthritis Rheum 40: 723–727PubMedCrossRefGoogle Scholar
  3. 3.
    Conrozier T, Carlier MC, Mathieu P, Colson F, Debard AL, Richard, S, Favret H, Bienvenu J, Vignon E (2000) Serum levels of YKL-40 and Creactive protein in patients with hip osteoarthritis and healthy subjects: A cross sectional study. Ann Rheum Dis 59: 828–831PubMedCrossRefGoogle Scholar
  4. 4.
    Geba GP, Weaver AL, Polis AB, Dixon ME, Schnitzer TJ, Vioxx A, Celecoxib Trial, (VACT) Group (2002) Efficacy of rofecoxib, celecoxib, and acetaminophen in osteoarthritis of the knee: A randomized trial. JAMA 287: 64–71PubMedCrossRefGoogle Scholar
  5. 5.
    Liew M, Carson Dick W (1981) The anatomy and physiology of blood flow in a diarthrodial joint. Clin Rheum Dis 7: 131–149Google Scholar
  6. 6.
    Wojtys EM, Beaman DN, Glover RA, Janda D (1990) Innervation of the human knee joint by substance-P fibers. Arthroscopy 6: 254–63PubMedCrossRefGoogle Scholar
  7. 7.
    Suri S, Gill SE, Massena de Camin S, Wilson D, McWilliams DF, Walsh DA (2007) Neurovascular invasion at the osteochondral junction and in osteophytes in ostearthritis. Ann Rheum Dis 66: 1423–1428.PubMedCrossRefGoogle Scholar
  8. 8.
    Lane LB, Villacin A, Bullough PG (1977) The vascularity and remodelling of subchondrial bone and calcified cartilage in adult human femoral and humeral heads. An age-and stress-related phenomenon. J Bone Joint Surg Br 59: 272–278PubMedGoogle Scholar
  9. 9.
    Graf J, Neusel E, Freese U, Simank HG, Niethard FU (1992) Subchondral vascularisation and osteoarthritis. Int Orthop 16: 113–117PubMedCrossRefGoogle Scholar
  10. 10.
    Walsh DA, Bonnet CS, Turner EL, Wilson D, Situ M, McWilliams DF (2007) Angiogenesis in the synovium and at the osteochondral junction in osteoarthritis. Osteoarthritis Cartilage 15: 743–751PubMedCrossRefGoogle Scholar
  11. 11.
    McDougall JJ, Bray RC (1998) Vascular volume determination of articular tissues in normal and anterior cruciate ligament-deficient rabbit knees. Anat Rec 251: 207–213PubMedCrossRefGoogle Scholar
  12. 12.
    Bray RC, Smith JA, Eng MK, Leonard CA, Sutherland CA, Salo PT (2001) Vascular response of the meniscus to injury: Effects of immobilization. J Orthop Res 19: 384–390PubMedCrossRefGoogle Scholar
  13. 13.
    Isacsson G, Isberg A, Johansson AS, Larson O (1986) Internal derangement of the temporomandibular joint: Radiographic and histologie changes associated with severe pain. J Oral Maxillofac Surg 44: 771–778PubMedCrossRefGoogle Scholar
  14. 14.
    Smith MD, Triantafillou S, Parker A, Youssef PP, Coleman M (1997) Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J Rheumatol 24: 365–371PubMedGoogle Scholar
  15. 15.
    Nakamura H, Yoshino S, Kato T, Tsuruha J, Nishioka K (1999) T-cell mediated inflammatory pathway in osteoarthritis. Osteoarthritis Cartilage 7: 401–402PubMedCrossRefGoogle Scholar
  16. 16.
    Lindblad S, Hedfors E (1987) Arthroscopic and immunohistologic characterization of knee joint synovitis in osteoarthritis. Arthritis Rheum 30: 1081–1088PubMedCrossRefGoogle Scholar
  17. 17.
    Uson J, Balsa A, Pascual-Salcedo D, Cabezas JA, Gonzalez-Tarrio JM, Martin-Mola E, Fontan G (1997) Soluble interleukin 6 (IL-6) receptor and IL-6 levels in serum and synovial fluid of patients with different arthropathies. J Rheumatol 24: 2069–2075PubMedGoogle Scholar
  18. 18.
    Rhodes LA, Conaghan PG, Radjenovic A, Grainger AJ, Emery P, McGonagle D (2005) Further evidence that a cartilage-pannus junction synovitis predilection is not a specific feature of rheumatoid arthritis. Ann Rheum Dis 64: 1347–1349PubMedCrossRefGoogle Scholar
  19. 19.
    Tan AL, Grainger AJ, Tanner SF, Emery P, McGonagle D (2006) A high-resolution magnetic resonance imaging study of distal interphalangeal joint arthropathy in psoriatic arthritis and osteoarthritis: Are they the same?, Arthritis Rheum 54: 1328–1333PubMedCrossRefGoogle Scholar
  20. 20.
    Tolboom TCA, Pieterman E, van der Laan WH, Toes REM, Huidekoper AL, Nelissen RGHH, Breedveld FC, Huizinga TWJ (2002) Invasive properties of fibroblast-like synoviocytes: Correlation with growth characteristics and expression of MMP-1, MMP-3, and MMP-10. Ann Rheum Dis 61: 975–980PubMedCrossRefGoogle Scholar
  21. 21.
    Pataki A, Lothe K, Spycher MA, Ruttner JR, Cserhati MD (1983) Occurrence of pannus in arthrosis. Z. Rheumatol 42: 351–354PubMedGoogle Scholar
  22. 22.
    Shibakawa A, Aoki H, Masuko-Hongo K, Kato T, Tanaka M, Nishioka K, Nakamura H (2003) Presence of pannus-like tissue on osteoarthritic cartilage and its histological character. Osteoarthritis Cartilage 11: 133–140PubMedCrossRefGoogle Scholar
  23. 23.
    Yuan GH, Tanaka M, Masuko-Hongo K, Shibakawa A, Kato T, Nishioka K, Nakamura H (2004) Characterization of cells from pannus-like tissue over articular cartilage of advanced osteoarthritis. Osteoarthritis Cartilage 12: 38–45PubMedCrossRefGoogle Scholar
  24. 24.
    Wilhelmi G, Schneider-Faust R (1984) Proliferative and metaplastic reactions as tentative reparatory processes in spontaneous arthritis in the mouse. Z Rheumatol 43: 241–248PubMedGoogle Scholar
  25. 25.
    Lefkoe TP, Trafton PG, Ehrlich MG, Walsh WR, Dennehy DT, Barrach HJ, Akelman E (1993) An experimental model of femoral condylar defect leading to osteoarthrosis. J Orthop Trauma 7: 458–467PubMedCrossRefGoogle Scholar
  26. 26.
    Bromley M, Bertfield H, Evanson JM, Woolley DE (1985) Bidirectional erosion of cartilage in the rheumatoid knee joint. Ann Rheum Dis 44: 676–681PubMedCrossRefGoogle Scholar
  27. 27.
    O—Connell JX, Nielen GP, Rosenberg AE (1999) Subchondral acute inflammation in severe arthritis: A sterile osteomyelitis?. Am J Surg Pathol 23: 192–197CrossRefGoogle Scholar
  28. 28.
    Bugatti S, Caporali R, Manzo A, Vitolo B, Pitzalis C, Montecucco C (2005) Involvement of subchondral bone marrow in rheumatoid arthritis: Lymphoid neogenesis and in situ relationship to subchondral bone marrow osteoclast recruitment. Arthritis Rheum 52: 3448–3459PubMedCrossRefGoogle Scholar
  29. 29.
    Appel H, Kuhne M, Spiekermann S, Kohler D, Zacher J, Stein H, Sieper J Loddenkemper C (2006) Immunohistochemical analysis of hip arthritis in ankylosing spondylitis: Evaluation of the bone-cartilage interface and subchondral bone marrow. Arthritis Rheum 54: 1805–1813PubMedCrossRefGoogle Scholar
  30. 30.
    Walsh DA, Wade M, Mapp PI, Blake DR (1998) Focally regulated endothelial proliferation and cell death in human synovium. Am J Pathol 152: 691–702PubMedGoogle Scholar
  31. 31.
    Haywood L, McWilliams DF, Pearson CI, Gill SE, Ganesan A, Wilson D, Walsh DA (2003) Inflammation and angiogenesis in osteoarthritis. Arthritis Rheum 48: 2173–2177PubMedCrossRefGoogle Scholar
  32. 32.
    Reece RJ, Canete JD, Parsons WJ Emery P, Veale DJ (1999) Distinct vascular patterns of early synovitis in psoriatic, reactive, and rheumatoid arthritis. Arthritis Rheum 42: 1481–1484PubMedCrossRefGoogle Scholar
  33. 33.
    Fearon U, Griosios K, Fraser A, Reece R, Emery P, Jones PF, Veale DJ (2003) Angiopoietins, growth factors, and vascular morphology in early arthritis. J Rheumatol 30: 260–268PubMedGoogle Scholar
  34. 34.
    Schumacher HR Jr, Bautista BB, Krauser RE, Mathur AK, Gall EP (1994) Histological appearance of the synovium in early rheumatoid arthritis. Semin Arthritis Rheum 23(6 Suppl 2): 3–10PubMedCrossRefGoogle Scholar
  35. 35.
    Benito MJ, Veale DJ, FitzGerald O, van den Berg WB, Bresnihan B (2005) Synovial tissue inflammation in early and late osteoarthritis. Ann Rheum Dis 64: 1263–1267PubMedCrossRefGoogle Scholar
  36. 36.
    Bonnet CS, Walsh DA (2005) Osteoarthritis, angiogenesis and inflammation. Rheumatology 44: 7–16PubMedCrossRefGoogle Scholar
  37. 37.
    Seegers HC, Hood VC, Kidd BL, Cruwys SC, Walsh DA (2003) Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J Pharmacol Exp Ther 306: 8–12PubMedCrossRefGoogle Scholar
  38. 38.
    Seegers HC, Avery PS, McWilliams DF, Haywood L, Walsh DA (2004) Combined effect of bradykinin B2 and neurokinin-1 receptor activation on endothelial cell proliferation in acute synovitis. FASEB J 18: 762–764PubMedGoogle Scholar
  39. 39.
    Peacock DJ, Banquerigo ML, Brahn E (1992) Angiogenesis inhibition suppresses collagen arthritis. J Exp Med, 175: 1135–1138PubMedCrossRefGoogle Scholar
  40. 40.
    Peacock DJ, Banquerigo ML, Brahn E (1995) A novel angiogenesis inhibitor suppresses rat adjuvant arthritis. Cell Immunol 160: 178–184PubMedCrossRefGoogle Scholar
  41. 41.
    Mapp PI, Turley MJ, McWilliams DF, Walsh DA (2007) Calcitonin gene-related peptide causes endothelial cell proliferation in vivo. Rheumatology 46S1: i43Google Scholar
  42. 42.
    Storgard CM, Stupack DG, Jonczyk A, Goodman SL, Fox RI, Cheresh DA (1999) Decreased angiogenesis and arthritic disease in rabbits treated with an alphavbeta3 antagonist. J Clin Invest 103: 47–54PubMedCrossRefGoogle Scholar
  43. 43.
    Wernert N, Justen HP, Rothe M, Behrens P, Dreschers S, Neuhaus T, Florin A, Sachinidis A, Vetter H, Ko Y (2002) The Ets 1 transcription factor is upregulated during inflammatory angiogenesis in rheumatoid arthritis. J Mol Med 80: 258–266PubMedCrossRefGoogle Scholar
  44. 44.
    Canete JD, Pablos JL, Sanmarti R, Mallofre C, Marsal S, Maymo J, Gratacos J, Mezquita J, Mezquita C, Cid MC (2004) Antiangiogenic effects of anti-tumor necrosis factor alpha therapy with infliximab in psoriatic arthritis. Arthritis Rheum 50: 1636–1641PubMedCrossRefGoogle Scholar
  45. 45.
    Paleolog EM, Young S, Stark AC, McCloskey RV, Feldmann M, Maimi RN (1998) Modulation of angiogenic vascular endothelial growth factor by tumor necrosis factor alpha and interleukin-1 in rheumatoid arthritis. Arthritis Rheum 41: 1258–1265PubMedCrossRefGoogle Scholar
  46. 46.
    Nagashima M, Wauke K, Hirano D, Ishigami S, Aono H, Takai M, Sasano M, Yoshino S (2000) Effects of combinations of anti-rheumatic drugs on the production of vascular endothelial growth factor and basic fibroblast growth factor in cultured synoviocytes and patients with rheumatoid arthritis. Rheumatology (Oxford) 39: 1255–1262CrossRefGoogle Scholar
  47. 47.
    Walsh DA (2004) Angiogenesis in osteoarthritis and spondylosis: Successful repair with undesirable outcomes. Curr Opin Rheumatol 16: 609–615PubMedCrossRefGoogle Scholar
  48. 48.
    Meng ZH, Hudson AP, Schumacher HRJ, Baker JF Baker DG (1997) Monosodium urate, hydroxyapatite, and calcium pyrophosphate crystals induce tumor necrosis factor-alpha expression in a mononuclear cell line. J Rheumatol 24: 2385–2388PubMedGoogle Scholar
  49. 49.
    Liu R, O—Connell M, Johnson K, Pritzker K, Mackman N, Terkeltaub R (2000) Extracellular signal-regulated kinase 1/extracellular signal-regulated kinase 2 mitogen-activated protein kinase signaling and activation of activator protein 1 and nuclear factor kappaB transcription factors play central roles in interleukin-8 expression stimulated by monosodium urate monohydrate and calcium pyrophosphate crystals in monocytic cells. Arthritis Rheum 43: 1145–1155PubMedCrossRefGoogle Scholar
  50. 50.
    Guerne PA, Terkeltaub R, Zuraw B, Lotz M (1989) Inflammatory microcrystals stimulate interleukin-6 production and secretion by human monocytes and synoviocytes. Arthritis Rheum 32: 1443–1452PubMedCrossRefGoogle Scholar
  51. 51.
    Jackson JR, Minton JA, Ho ML, Wei N, Winkler JD (1997) Expression of vascular endothelial growth factor in synovial fibroblasts is induced by hypoxia and interleukin 1 beta. J Rheumatol 24: 1253–1259PubMedGoogle Scholar
  52. 52.
    Cho ML, Jung YO, Moon YM, Min SY, Yoon CH, Lee SH, Park SH, Cho CS, Jue DM, Kim HY (2006) Interleukin-18 induces the production of vascular endothelial growth factor (VEGF) in rheumatoid arthritis synovial fibroblasts via AP-1-dependent pathways. Immunol Lett 103: 159–166PubMedCrossRefGoogle Scholar
  53. 53.
    Inoue H, Takamori M, Nagata N, Nishikawa T, Oda H, Yamamoto S, Koshihara Y (2001) An investigation of cell proliferation and soluble mediators induced by interleukin 1beta in human synovial fibroblasts: Comparative response in osteoarthritis and rheumatoid arthritis. Inflamm Res 50: 65–72PubMedCrossRefGoogle Scholar
  54. 54.
    Levick JR (1990) Hypoxia and acidosis in chronic inflammatory arthritis; relation to vascular supply and dynamic effusion pressure. J Rheumatol 17: 579–582PubMedGoogle Scholar
  55. 55.
    Hollander AP, Corke KP, Freemont AJ, Lewis CE (2001) Expression of hypoxia-inducible factor 1alpha by macrophages in the rheumatoid synovium: Implications for targeting of therapeutic genes to the inflamed joint. Arthritis Rheum 44: 1540–1544PubMedCrossRefGoogle Scholar
  56. 56.
    Giatromanolaki A, Sivridis E, Maltezos E, Athanassou N, Papazoglou D, Gatter KC, Harris AL, Koukourakis MI (2003) Upregulated hypoxia inducible factor-1alpha and-2alpha pathway in rheumatoid arthritis and osteoarthritis. Arthritis Res Ther 5: R193–201PubMedCrossRefGoogle Scholar
  57. 57.
    Peters CL, Morris CJ, Mapp PI, Blake DR, Lewis CE, Winrow VR (2004) The transcription factors hypoxia-inducible factor 1alpha and Ers-1 colocalize in the hypoxic synovium of inflamed joints in adjuvant-induced arthritis. Arthritis Rheum 50: 291–296PubMedCrossRefGoogle Scholar
  58. 58.
    Pollman MJ, Naumovski L, Gibbons GH (1999) Endothelial cell apoptosis in capillary network remodeling. J Cell Physiol 178: 359–370PubMedCrossRefGoogle Scholar
  59. 59.
    Spyridopoulos I, Brogi E, Kearney M, Sullivan AB, Cetrulo C, Isner JM, Losordo DW (1997) Vascular endothelial growth factor inhibits endothelial cell apoptosis induced by tumor necrosis factor-alpha: Balance between growth and death signals. J Mol Cell Cardiol 29: 1321–1330PubMedCrossRefGoogle Scholar
  60. 60.
    Oliver SJ, Cheng TP, Banquerigo ML, Brahn E (1995) Suppression of collagen-induced arthritis by an angiogenesis inhibitor, AGM-1470, in combination with cyclosporin: Reduction of vascular endothelial growth factor (VEGF). Cell Immunol 166: 196–206PubMedCrossRefGoogle Scholar
  61. 61.
    Badger AM, Blake S, Kapadia R, Sarkar S, Levin J, Swift BA, Hoffman SJ, Stroup GB, Miller WH, Gowen M et al (2001) Disease-modifying activity of SB 273005, an orally active, nonpeptide alpha-v beta-3 (vitronectin receptor) antagonist, in rat adjuvant-induced arthritis. Arthritis Rheum 44: 128–137PubMedCrossRefGoogle Scholar
  62. 62.
    Oliver SJ, Banquerigo ML, Brahn E (1994) Suppression of collagen-induced arthritis using an angiogenesis inhibitor AGM-1470, and a microtubule stabilizer, taxol. Cell Immunol 157: 291–299PubMedCrossRefGoogle Scholar
  63. 63.
    de Bandt M, Grossin M, Weber AJ, Chopin M, Elbim C, Pla M, Gougerot-Pocidalo MA, Gaudry M (2000) Suppression of arthritis and protection from bone destruction by treatment with TNP-470/AGM-1470 in a transgenic mouse model of rheumatoid arthritis. Arthritis Rheum 43: 2056–2063PubMedCrossRefGoogle Scholar
  64. 64.
    Hannig G, Bernier SG, Hoyt JG, Doyle B, Clark E, Karp RM, Lorusso J, Westlin WF (2007) Suppression of inflammation and structural damage in experimental arthritis through molecular targeted therapy with PPI-2458. Arthritis Rheum 56: 850–860PubMedCrossRefGoogle Scholar
  65. 65.
    Bernier SG, Lazarus DD, Clark E, Doyle B, Labenski MT, Thompson CD, Westlin WF, Hannig G (2004) A methionine aminopeptidase-2 inhibitor, PPI-2458, for the treatment of rheumatoid arthritis. Proc Natl Acad Sci USA 101: 10768–10773PubMedCrossRefGoogle Scholar
  66. 66.
    Takahashi H, Kato K, Miyake K, Hirai Y, Yoshino S, Shimada T (2005) Adeno-associated virus vector-mediated anti-angiogenic gene therapy for collagen-induced arthritis in mice. Clin Exp Rheumatol 23: 455–461PubMedGoogle Scholar
  67. 67.
    Kim JM, Ho SH, Park EJ, Hahn W, Cho H, Jeong JG, Lee YW, Kim S (2002) Angiostatin gene transfer as an effective treatment strategy in murine collagen-induced arthritis. Arthritis Rheum 46: 793–801PubMedCrossRefGoogle Scholar
  68. 68.
    Kato K, Miyake K, Igarashi T, Yoshino S, Shimada T (2005) Human immunodeficiency virus vector-mediated intra-articular expression of angiostatin inhibits progression of collagen-induced arthritis in mice. Rheumatol Int 25: 522–529PubMedCrossRefGoogle Scholar
  69. 69.
    Yin G, Liu W, An P, Li P, Ding I, Planelles V, Schwarz EM, Min W (2002) Endostatin gene transfer inhibits joint angiogenesis and pannus formation in inflammatory arthritis. Mol Ther 5: 547–554PubMedCrossRefGoogle Scholar
  70. 70.
    Haas CS, Amin MA, Allen BB, Ruth JH, Haines GK 3rd, Woods JM, Koch AE (2006) Inhibition of angiogenesis by interleukin-4 gene therapy in rat adjuvant-induced arthritis. Arthritis Rheum 54: 2402–2414PubMedCrossRefGoogle Scholar
  71. 71.
    Woods JM, Amin MA, Katschke KJ Jr, Volin MV, Ruth JH, Connors MA, Woodruff DC, Kurata H, Arai K-I, Haines GK 3rd et al (2002) Interleukin-13 gene therapy reduces inflammation, vascularization, and bony destruction in rat adjuvant-induced arthritis. Hum Gene Ther 13: 381–393PubMedCrossRefGoogle Scholar
  72. 72.
    Wang C-R, Chen S-Y, Wu C-L, Liu M-F, Jin Y-T, Chao L, Chao J (2005) Prophylactic adenovirus-mediated human kallistatin gene therapy suppresses rat arthritis by inhibiting angiogenesis and inflammation. Arthritis Rheum 52: 1319–1324PubMedCrossRefGoogle Scholar
  73. 73.
    Jou IM, Shiau A-L, Chen S-Y, Wang C-R, Shieh D-B, Tsai C-S, Wu C-L (2005) Thrombospondin 1 as an effective gene therapeutic strategy in collagen-induced arthritis. Arthritis Rheum 52:339–344PubMedCrossRefGoogle Scholar
  74. 74.
    Grosios K, Wood J, Esser R, Raychaudhuri A, Dawson J (2004) Angiogenesis inhibition by the novel VEGF receptor tyrosine kinase inhibitor, PTK787/ZK222584, causes significant anti-arthritic effects in models of rheumatoid arthritis. Inflamm Res 53: 133–142PubMedCrossRefGoogle Scholar
  75. 75.
    Miotla J, Maciewicz R, Kendrew J, Feldmann M, Paleolog E (2000) Treatment with soluble VEGF receptor reduces disease severity in murine collagen-induced arthritis. Lab Invest 80: 1195–1205PubMedCrossRefGoogle Scholar
  76. 76.
    Chen Y, Donnelly E, Kobayashi H, Debusk LM, Lin PC (2005) Gene therapy targeting the Tie2 function ameliorates collagen-induced arthritis and protects against bone destruction. Arthritis Rheum 52: 1585–1594PubMedCrossRefGoogle Scholar
  77. 77.
    Apparailly F, Bouquet C, Miller V, Noel D, Jacquet C, Opolon P, Perricaudet M, Sany J, Yeh P, Jorgensen C (2002) Adenovirus-mediated gene transfer of urokinase plasminogen inhibitor inhibits angiogenesis in experimental arthritis. Gene Ther 9: 192–200PubMedCrossRefGoogle Scholar
  78. 78.
    Stevens CR, Blake DR, Merry P, Revell PA, Levick JR (1991) A comparative study by morphometry of the microvasculature in normal and rheumatoid synovium. Arthritis Rheum 34: 1508–1513PubMedGoogle Scholar
  79. 79.
    Ceponis A, Konttinen YT, MacKevicius Z, Solovieva SA Hukkanen M, Tamulaitiene M, Matulis A, Santavirta S (1996) Aberrant vascularity and von Willebrand factor distribution in inflamed synovial membrane. J Rheumatol 23: 1880–1886PubMedGoogle Scholar
  80. 80.
    Ostergaard M, Stoltenberg M, Lovgreen-Nielsen P, Volck B, Sonne-Holm S, Lorenzen I (1998) Quantification of synovitis by MRI: Correlation between dynamic and static gadolinium-enhanced magnetic resonance imaging and microscopic and macroscopic signs of synovial inflammation. Magn Reson Imaging 16: 743–754PubMedCrossRefGoogle Scholar
  81. 81.
    Taylor P (2002) VEGF and imaging of vessels in rheumatoid arthritis. Arthritis Res 4 Suppl 3: S99–107PubMedCrossRefGoogle Scholar
  82. 82.
    Veihelmann A, Krombach F, Refior HJ, Messmer K (1999) Effects of NO synthase inhibitors on the synovial microcirculation in the mouse knee joint. J Vasc Res 36: 379–384PubMedCrossRefGoogle Scholar
  83. 83.
    Walsh DA, Hu DE, Mapp PI, Polak JM, Blake, DR, Fan TP (1996) Innervation and neurokinin receptors during angiogenesis in the rat sponge granuloma. Histochem J 28: 759–769PubMedCrossRefGoogle Scholar
  84. 84.
    Kangesu T, Manek S, Terenghi G, Gu XH, Navsaria HA, Polak JM, Green CJ, Leigh IM (1998) Nerve and blood vessel growth in response to grafted dermis and cultured keratinocytes. Plast Reconstr Surg 101: 1029–1038PubMedCrossRefGoogle Scholar
  85. 85.
    Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1: 27–31PubMedCrossRefGoogle Scholar
  86. 86.
    Schmidt WA, Volker L, Zacher J, Schlafke M, Ruhnke M, Gromnica-Ihle E (2000) Colour Doppler ultrasonography to detect pannus in knee joint, synovitis. Clin Exp Rheumatol 18: 439–444PubMedGoogle Scholar
  87. 87.
    Fenwick SA, Gregg PJ, Rooney P (1999) Osteoarthritic cartilage loses its ability to remain avascular. Osteoarthritis Cartilage 7: 441–452PubMedCrossRefGoogle Scholar
  88. 88.
    Duncan H, Jundt J, Riddle JM, Pitchford W, Christopherson T (1987) The tibial subchondral plate. A scanning electron microscopic study. J Bone Joint Surg Am 69: 1212–1220PubMedGoogle Scholar
  89. 89.
    Clark JM (1990) The structure of vascular channels in the subchondral plate. J Anat 171: 105–115PubMedGoogle Scholar
  90. 90.
    Shibakawa A, Yudoh K, Masuko-Hongo K, Kato T, Nishioka K, Nakamura H (2005) The role of subchondral bone resorption pits in osteoarthritis: MMP production by cells derived from bone marrow. Osteoarthritis Cartilage 13: 679–687PubMedCrossRefGoogle Scholar
  91. 91.
    Boyde A, Firth EC (2004) Articular calcified cartilage canals in the third metacarpal bone of 2-year-old thoroughbred racehorses. J Anat 205: 491–500PubMedCrossRefGoogle Scholar
  92. 92.
    Saied A, Cherin E, Gaucher H, Laugier P, Gillet P, Floquet J, Netter P, Berger G (1997) Assessment of articular cartilage and subchondral bone: Subtle and progressive changes in experimental osteoarthritis using 50 MHz echography in vitro. J Bone Miner Res 12: 1378–1386PubMedCrossRefGoogle Scholar
  93. 93.
    Kangarlu A, Gahunia HK (2006) Magnetic resonance imaging characterization of osteochondral defect repair in a goat model at 8 T. Osteoarthritis Cartilage 14: 52–62PubMedCrossRefGoogle Scholar
  94. 94.
    Shikhman AR, Brinson DC, Lotz M (2000) Profile of glycosaminoglycan-degrading glycosidases and glycoside sulfatases secreted by human articular chondrocytes in homeostasis and inflammation. Arthritis Rheum 43: 1307–1314PubMedCrossRefGoogle Scholar
  95. 95.
    Jacques C, Gosset M, Berenbaum F, Gabay C (2006) The role of IL-1 and IL-1Ra in joint inflammation and cartilage degradation. Vitam Horm 74: 371–403PubMedCrossRefGoogle Scholar
  96. 96.
    Pelletier JP, Martel-Pelletier J, Ghandur-Mnaymneh L, Howell DS, Woessner JF Jr (1985) Role of synovial membrane inflammation in cartilage matrix breakdown in the Pond-Nuki dog model of osteoarthritis. Arthritis Rheum 28: 554–561PubMedCrossRefGoogle Scholar
  97. 97.
    Fuzzalari NL, Darrecott J, Vernon-Roberts B (1983) A quantitative description of selected stress regions of cancellous bone in the head of the femur using automatic image analysis. Metab Bone Dis Relat Res 5: 119–125CrossRefGoogle Scholar
  98. 98.
    Maksymowych WP, Jhangri GS, Leclercq S, Skeith K, Yan A, Russell AS (1998) An open study of pamidronate in the treatment of refractory ankylosing spondylitis. J Rheumatol 25: 714–717PubMedGoogle Scholar
  99. 99.
    Mazzantini M, Di Munno O, Metelli MR, Bulleri M, Giordani R (2002) Single infusion of neridronate (6-amino-1-hydroxyhexylidene-1,1-bisphosphonate) in patients with active rheumatoid arthritis: Effects on disease activity and bone resorption markers. Aging Clin Exp Res 14: 197–201PubMedGoogle Scholar
  100. 100.
    Santini D, Fratto ME, Vincenzi B, La Cesa A, Dianzani C, Tonini G (2004) Bisphosphonate effects in cancer and inflammatory diseases: In vitro and in vivo modulation of cytokine activities. Biodrugs 18: 269–278PubMedCrossRefGoogle Scholar
  101. 101.
    Colnot C (2005) Cellular and molecular interactions regulating skeletogenesis. J Cell Biochem 95: 688–697PubMedCrossRefGoogle Scholar
  102. 102.
    Collett GDM, Canfield AE (2005) Angiogenesis and pericytes in the initiation of ectopic calcification. Circ Res 96: 930–938PubMedCrossRefGoogle Scholar
  103. 103.
    Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE (2004) Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 110: 2226–2232PubMedCrossRefGoogle Scholar
  104. 104.
    Fortier LA, Nixon AJ (1997) Distributional changes in substance P nociceptive fiber patterns in naturally osteoarthritic articulations. J Rheumatol 24: 524–530PubMedGoogle Scholar
  105. 105.
    Hashimoto S, Creighton-Achermann L, Takahashi K, Amiel D, Coutts RD, Lotz M (2002) Development and regulation of osteophyte formation during experimental osteoarthritis. Osteoarthritis Cartilage 10: 180–187PubMedCrossRefGoogle Scholar
  106. 106.
    Moskowitz RW, Goldberg VM (1987) Studies of osteophyte pathogenesis in experimentally induced osteoarthritis. J Rheumatol 14: 311–320PubMedGoogle Scholar
  107. 107.
    Valdes AM, Hassett G, Hart DJ, Spector TD (2005) Radiographic progression of lumbar spine disc degeneration is influenced by variation at inflammatory genes: Acandidate SNP association study in the Chingford cohort. Spine 30: 2445–2451PubMedCrossRefGoogle Scholar
  108. 108.
    van Beuningen HM, van der Kraan PM, Arntz OJ, van den Berg WB (1994) Transforming growth factor-beta 1 stimulates articular chondrocyte proteoglycan synthesis and induces osteophyte formation in the murine knee joint. Lab Invest 71: 279–290PubMedGoogle Scholar
  109. 109.
    Pelletier JP, Jovanovic D, Fernandes JC, Manning P, Connor JR, Currie MG, Di Battista JA, Martel-Pelletier J (1998) Reduced progression of experimental osteoarthritis in vivo by selective inhibition of inducible nitric oxide synthase. Arthritis Rheum 41: 1275–1286PubMedCrossRefGoogle Scholar
  110. 110.
    Ledingham J, Regan M, Jones A, Doherty M (1995) Factors affecting radiographic progression of knee osteoarthritis. Ann Rheum Dis 54: 53–58PubMedCrossRefGoogle Scholar
  111. 111.
    Conrozier T, Chappuis-Cellier C, Richard M, Mathieu P, Richard S, Vignon E (1998) Increased serum C-reactive protein levels by immunonephelometry in patients with rapidly destructive hip osteoarthritis. Rev. Rhum Engl Ed 65: 759–765PubMedGoogle Scholar
  112. 112.
    Fam AG, Morava-Protzner I, Purcell C, Young BD, Bunting PS, Lewis AJ (1995) Acceleration of experimental lapine osteoarthritis by calcium pyrophosphate microcrystalline synovitis. Arthritis Rheum 38: 201–210PubMedCrossRefGoogle Scholar
  113. 113.
    Myers SL, Brandt KD, O—Connor BL (1991) Low dose prednisone treatment does not reduce the severity of osteoarthritis in dogs after anterior cruciate ligament transection. J Rheumatol 18: 1856–1862PubMedGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 2008

Authors and Affiliations

  • David A. Walsh
    • 1
  • Eirlys Williams
    • 1
  1. 1.Academic Rheumatology, University of Nottingham Clinical Sciences BuildingNottingham City HospitalNottinghamUK

Personalised recommendations