Thrombospondin 2 functions as an endogenous regulator of angiogenesis and inflammation in rheumatoid arthritis

American Journal of Pathology

Volumn 165, Issue 6, 2004, Pages 2087-2098

  Yong, Wook Park ^a   Young, Mo Kang ^a   Butterfield, Joe ^a   Detmar, Michael ^b   Goronzy, Jörg J ^a   Weyand, Cornelia M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; MATRIX PROTEIN; THROMBOSPONDIN 2; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL AGGREGATION; CELL BASED GENE THERAPY; CHRONIC INFLAMMATION; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOARCHITECTURE; EMBRYO; ENDOTHELIUM CELL; FIBROBLAST; GENETIC TRANSFECTION; GERMINAL CENTER; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; NONHUMAN; ORGANOGENESIS; PERITONEUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RHEUMATOID ARTHRITIS; SYNOVIUM; T LYMPHOCYTE; VASCULARIZATION;

EID: 9644264253     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0002-9440(10)63259-2     Document Type: Article

References (56)

1. Marrack P, Kappler J, Kotzin BL: Autoimmune disease: why and where it occurs. Nat Med 2001, 7:899-905
2. McInnes IB: Rheumatoid arthritis. From bench to bedside. Rheum Dis Clin North Am 2001, 27:373-387
3. Schroder AE, Greiner A, Seyfert C, Berek C: Differentiation of B cells in the nonlymphoid tissue of the synovial membrane of patients with rheumatoid arthritis. Proc Natl Acad Sci USA 1996, 93:221-225
4. Weyand CM, Kang YM, Kurtin PJ, Goronzy JJ: The power of the third dimension: tissue architecture and autoimmunity in rheumatoid arthritis. Curr Opin Rheumatol 2003, 15:259-266
5. Klimiuk PA, Goronzy JJ, Bjornsson J, Beckenbaugh RD, Weyand CM: Tissue cytokine patterns distinguish variants of rheumatoid synovitis. Am J Pathol 1997, 151:1311-1319
6. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH, O'Fallon WM, Goronzy JJ, Weyand CM: Lymphoid neogenesis in rheumatoid synovitis. J Immunol 2001, 167:1072-1080
7. Klimiuk PA, Sierakowski S, Latosiewicz R, Cylwik B, Skowronski J, Chwiecko J: Serum cytokines in different histological variants of rheumatoid arthritis. J Rheumatol 2001, 28:1211-1217
8. Page G, Lebecque S, Miossec P: Anatomic localization of immature and mature dendritic cells in an ectopic lymphoid organ: correlation with selective chemokine expression in rheumatoid synovium. J Immunol 2002, 168:5333-5341
9. Kang YM, Zhang X, Wagner UG, Yang H, Beckenbaugh RD, Kurtin PJ, Goronzy JJ, Weyand CM: CD8 T cells are required for the formation of ectopic germinal centers in rheumatoid synovitis. J Exp Med 2002, 195:1325-1336
10. Wagner UG, Kurtin PJ, Wahner A, Brackertz M, Berry DJ, Goronzy JJ, Weyand CM: The role of CD8+ CD40L+ T cells in the formation of germinal centers in rheumatoid synovitis. J Immunol 1998, 161:6390-6397
11. Newton JL, Harney SM, Wordsworth BP, Brown MA: A review of the MHC genetics of rheumatoid arthritis. Genes Immun 2004, 5:151-157
12. Weyand CM, Hicok KC, Conn DL, Goronzy JJ: The influence of HLA-DRB1 genes on disease severity in rheumatoid arthritis. Ann Intern Med 1992, 117:801-806
13. Yen JH, Moore BE, Nakajima T, Scholl D, Schaid DJ, Weyand CM, Goronzy JJ: Major histocompatibility complex class I-recognizing receptors are disease risk genes in rheumatoid arthritis. J Exp Med 2001, 193:1159-1167
14. Snyder MR, Lucas M, Vivier E, Weyand CM, Goronzy JJ: Selective activation of the c-Jun NH2-terminal protein kinase signaling pathway by stimulatory KIR in the absence of KARAP/DAP12 in CD4+ T cells. J Exp Med 2003, 197:437-449
15. Groh V, Bruhl A, El-Gabalawy H, Nelson JL, Spies T: Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc Natl Acad Sci USA 2003, 100:9452-9457
16. Ji H, Gauguier D, Ohmura K, Gonzalez A, Duchatelle V, Danoy P, Garchon HJ, Degott C, Lathrop M, Benoist C, Mathis D: Genetic influences on the end-stage effector phase of arthritis. J Exp Med 2001, 194:321-330
17. Grant EP, Picarella D, Burwell T, Delaney T, Croci A, Avitahl N, Humbles AA, Gutierrez-Ramos JC, Briskin M, Gerard C, Coyle AJ: Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J Exp Med 2002, 196:1461-1471
18. Weyand CM, Kurtin PJ, Goronzy JJ: Ectopic lymphoid organogenesis: a fast track for autoimmunity. Am J Pathol 2001, 159:787-793
19. 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
20. Koch AE: Angiogenesis as a target in rheumatoid arthritis. Ann Rheum Dis 2003, 62(Suppl 2):S60-S67
21. Paleolog EM, Fava RA: Angiogenesis in rheumatoid arthritis: implications for future therapeutic strategies. Springer Semin Immunopathol 1998, 20:73-94
22. Fearon U, Griosios K, Fraser A, Reece R, Emery P, Jones PF, Veale DJ: Angiopoietins, growth factors, and vascular morphology in early arthritis. J Rheumatol 2003, 30:260-268
23. Parangi S, O'Reilly M, Christofori G, Holmgren L, Grosfeld J, Folkman J, Hanahan D: Antiangiogenic therapy of transgenic mice impairs de novo tumor growth. Proc Natl Acad Sci USA 1996, 93:2002-2007
24. Fava RA, Olsen NJ, Spencer-Green G, Yeo KT, Yeo TK, Berse B, Jackman RW, Senger DR, Dvorak HF, Brown LF: Vascular permeability factor/endothelial growth factor (VPF/VEGF): accumulation and expression in human synovial fluids and rheumatoid synovial tissue. J Exp Med 1994, 180:341-346
25. 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
26. Uchida T, Nakashima M, Hirota Y, Miyazaki Y, Tsukazaki T, Shindo H: Immunohistochemical localisation of protein tyrosine kinase receptors Tie-1 and Tie-2 in synovial tissue of rheumatoid arthritis: correlation with angiogenesis and synovial proliferation. Ann Rheum Dis 2000, 59:607-614
27. Iruela-Arispe ML, Bornstein P, Sage H: Thrombospondin exerts an antiangiogenic effect on cord formation by endothelial cells in vitro. Proc Natl Acad Sci USA 1991, 88:5026-5030
28. Bornstein P, Armstrong LC, Hankenson KD, Kyriakides TR, Yang Z: Thrombospondin 2, a matricellular protein with diverse functions. Matrix Biol 2000, 19:557-568
29. O'Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J: Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 1994, 79:315-328
30. O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR, Folkman J: Endostatin: an endogenous in-hibitor of angiogenesis and tumor growth. Cell 1997, 88:277-285
31. Pike SE, Yao L, Jones KD, Cherney B, Appella E, Sakaguchi K, Nakhasi H, Teruya-Feldstein J, Wirth P, Gupta G, Tosato G: Vasostatin, a calreticulin fragment, inhibits angiogenesis and suppresses tumor growth. J Exp Med 1998, 188:2349-2356
32. Kyriakides TR, Zhu YH, Yang Z, Bornstein P: The distribution of the matricellular protein thrombospondin 2 in tissues of embryonic and adult mice. J Histochem Cytochem 1998, 46:1007-1015
33. Lawler J: The functions of thrombospondin-1 and -2. Curr Opin Cell Biol 2000, 12:634-640
34. Kyriakides TR, Bornstein P: Matricellular proteins as modulators of wound healing and the foreign body response. Thromb Haemost 2003, 90:986-992
35. Kyriakides TR, Zhu YH, Smith LT, Bain SD, Yang Z, Lin MT, Danielson KG, Iozzo RV, LaMarca M, McKinney CE, Ginns EI, Bornstein P: Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol 1998, 140:419-430
36. Kyriakides TR, Zhu YH, Yang Z, Huynh G, Bornstein P: Altered extracellular matrix remodeling and angiogenesis in sponge granulomas of thrombospondin 2-null mice. Am J Pathol 2001, 159:1255-1262
37. Agah A, Kyriakides TR, Lawler J, Bornstein P: The lack of thrombospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice. Am J Pathol 2002, 161:831-839
38. Hawighorst T, Velasco P, Streit M, Hong YK, Kyriakides TR, Brown LF, Bornstein P, Detmar M: Thrombospondin-2 plays a protective role in multistep carcinogenesis: a novel host anti-tumor defense mechanism. EMBO J 2001, 20:2631-2640
39. Lange-Asschenfeldt B, Weninger W, Velasco P, Kyriakides TR, von Andrian UH, Bornstein P, Detmar M: Increased and prolonged inflammation and angiogenesis in delayed-type hypersensitivity reactions elicited in the skin of thrombospondin-2-deficient mice. Blood 2002, 99:538-545
40. Streit M, Stephen AE, Hawighorst T, Matsuda K, Lange-Asschenfeldt B, Brown LF, Vacanti JP, Detmar M: Systemic inhibition of tumor growth and angiogenesis by thrombospondin-2 using cell-based antiangiogenic gene therapy. Cancer Res 2002, 62:2004-2012
41. Armstrong LC, Bjorkblom B, Hankenson KD, Siadak AW, Stiles CE, Bornstein P: Thrombospondin 2 inhibits microvascular endothelial cell proliferation by a caspase-independent mechanism. Mol Biol Cell 2002, 13:1893-1905
42. Kyriakides TR, Tam JW, Bornstein P: Accelerated wound healing in mice with a disruption of the thrombospondin 2 gene. J Invest Dermatol 1999, 113:782-787
43. Kyriakides TR, Leach KJ, Hoffman AS, Ratner BD, Bornstein P: Mice that lack the angiogenesis inhibitor, thrombospondin 2, mount an altered foreign body reaction characterized by increased vascularity. Proc Natl Acad Sci USA 1999, 96:4449-4454
44. Smeets TJ, Barg EC, Kraan MC, Smith MD, Breedveld FC, Tak PP: Analysis of the cell infiltrate and expression of proinflammatory cytokines and matrix metalloproteinases in arthroscopic synovial biopsies: comparison with synovial samples from patients with end stage, destructive rheumatoid arthritis. Ann Rheum Dis 2003, 62:635-638
45. Matsuno H, Yudoh K, Katayama R, Nakazawa F, Uzuki M, Sawai T, Yonezawa T, Saeki Y, Panayi GS, Pitzalis C, Kimura T: The role of TNF-alpha in the pathogenesis of inflammation and joint destruction in rheumatoid arthritis (RA): a study using a human RA/SCID mouse chimera. Rheumatology (Oxford) 2002, 41:329-337
46. Vallejo AN, Mugge LO, Klimiuk PA, Weyand CM, Goronzy JJ: Central role of thrombospondin-1 in the activation and clonal expansion of inflammatory T cells. J Immunol 2000, 164:2947-2954
47. Brown EJ, Frazier WA: Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 2001, 11:130-135
48. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP: CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 1997, 138:707-717
49. Chen H, Strickland DK, Mosher DF: Metabolism of thrombospondin 2. Binding and degradation by 3t3 cells and glycosaminoglycan-variant Chinese hamster ovary cells. J Biol Chem 1996, 271:15993-15999
50. Chen H, Sottile J, O'Rourke KM, Dixit VM, Mosher DF: Properties of recombinant mouse thrombospondin 2 expressed in Spodoptera cells. J Biol Chem 1994, 269:32226-32232
51. Li Z, Calzada MJ, Sipes JM, Cashel JA, Krutzsch HC, Annis DS, Mosher DF, Roberts DD: Interactions of thrombospondins with alpha4beta1 integrin and CD47 differentially modulate T cell behavior. J Cell Biol 2002, 157:509-519
52. Li Z, He L, Wilson K, Roberts D: Thrombospondin-1 inhibits TCR-mediated T lymphocyte early activation. J Immunol 2001, 166:2427-2436
53. Beppu R, Nakamura K, Miyajima-Uchida H, Kuroki M, Khare PD, Yamauchi Y, Yamashita Y, Shirakusa T: Soluble thrombospondin-1 suppresses T cell proliferation and enhances IL-10 secretion by antigen presenting cells stimulated with phytohemagglutinin. Immunol Invest 2001, 30:143-156
54. Doyen V, Rubio M, Braun D, Nakajima T, Abe J, Saito H, Delespesse G, Sarfati M: Thrombospondin 1 is an autocrine negative regulator of human dendritic cell activation. J Exp Med 2003, 198:1277-1283
55. Avice MN, Rubio M, Sergerie M, Delespesse G, Sarfati M: CD47 ligation selectively inhibits the development of human naive T cells into Th1 effectors. J Immunol 2000, 165:4624-4631
56. Vallejo AN, Yang H, Klimiuk PA, Weyand CM, Goronzy JJ: Synoviocyte-mediated expansion of inflammatory T cells in rheumatoid synovitis is dependent on CD47-thrombospondin 1 interaction. J Immunol 2003, 171:1732-1740