Thrombospondin-2 modulates extracellular matrix remodeling during physiological angiogenesis

American Journal of Pathology

Volumn 173, Issue 3, 2008, Pages 879-891

  Krady, Marie M ^a,c   Zeng, Jianmin ^a,c   Yu, Jun ^a,c   MacLauchlan, Susan ^a,c   Skokos, Eleni A ^a,c   Tian, Weiming ^a,c   Bornstein, Paul ^d   Sessa, William C ^a,c   Kyriakides, Themis R ^a,b,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Yale University   (United States)

^c YALE UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBRIL; GELATINASE B; THROMBOSPONDIN 2;

ANGIOGENESIS; ANIMAL CELL; ARTERY BLOOD FLOW; ARTICLE; ASSAY; CELL MIGRATION; CONTROLLED STUDY; DISEASE MODEL; ENDOTHELIUM CELL; EXCISION; EXTRACELLULAR MATRIX; FEMORAL ARTERY; FIBROBLAST; HINDLIMB; HUMAN; HUMAN CELL; LEG ISCHEMIA; MOUSE; MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 51349110872     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.080128     Document Type: Article

References (54)

1. Adams JC: Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol 2001, 17:25-51
2. Bornstein P: Thrombospondins as matricellular modulators of cell function. J Clin Invest 2001, 107:929-934
3. Iruela-Arispe ML, Luque A, Lee N: Thrombospondin modules and angiogenesis. Int J Biochem Cell Biol 2004, 36:1070-1078
4. Bornstein P, Devarayalu S, Li P, Disteche CM, Framson P: A second thrombospondin gene in the mouse is similar in organization to thrombospondin 1 but does not respond to serum. Proc Natl Acad Sci USA 1991, 88:8636-8640
5. Bornstein P, O'Rourke K, Wikstrom K, Wolf FW, Katz R, Li P, Dixit VM: A second, expressed thrombospondin gene (Thbs2) exists in the mouse genome. J Biol Chem 1991, 266:12821-12824
6. 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
7. 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
8. Adams JC, Lawler J: The thrombospondins. Int J Biochem Cell Biol 2004, 36:961-968
9. Oganesian A, Armstrong LC, Migliorini MM, Strickland DK, Bornstein P: Thrombospondins use the VLDL receptor and a non-apoptotic pathway to inhibit cell division in microvascular endothelial cells. Mol Biol Cell 2008, 19:563-571
10. Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, Bouck NP: A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci USA 1990, 87:6624-6628
11. Lawler J: Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J Cell Mol Med 2002, 6:1-12
12. Cursiefen C, Masli S, Ng TF, Dana MR, Bornstein P, Lawler J, Streilein JW: Roles of thrombospondin-1 and -2 in regulating corneal and iris angiogenesis. Invest Ophthalmol Vis Sci 2004, 45:1117-1124
13. Zhang X, Lawler J: Thrombospondin-based antiangiogenic therapy. Microvasc Res 2007, 74:90-99
14. Volpert OV, Stellmach V, Bouck N: The modulation of thrombospondin and other naturally occurring inhibitors of angiogenesis during tumor progression. Breast Cancer Res Treat 1995, 36:119-126
15. Panetti TS, Chen H, Misenheimer TM, Getzler SB, Mosher DF: Endothelial cell mitogenesis induced by LPA: inhibition by thrombospondin-1 and thrombospondin-2. J Lab Clin Med 1997, 129:208-216
16. Murphy-Ullrich JE, Gurusiddappa S, Frazier WA, Hook M: Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity. J Biol Chem 1993, 268:26784-26789
17. Murphy-Ullrich JE, Hook M: Thrombospondin modulates focal adhesions in endothelial cells. J Cell Biol 1989, 109:1309-1319
18. 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
19. Jiménez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N: Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000, 6:41-48
20. Simantov R, Febbraio M, Silverstein RL: The antiangiogenic effect of thrombospondin-2 is mediated by CD36 and modulated by histidine-rich glycoprotein. Matrix Biol 2005, 24:27-34
21. 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
22. 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
23. 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
24. Isenberg JS, Romeo MJ, Abu-Asab M, Tsokos M, Oldenborg A, Pappan L, Wink DA, Frazier WA, Roberts DD: Increasing survival of ischemic tissue by targeting CD47. Circ Res 2007, 100:602-613
25. Isenberg JS, Hyodo F, Matsumoto K, Romeo MJ, Abu-Asab M, Tsokos M, Kuppusamy P, Wink DA, Krishna MC, Roberts DD: Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 2007, 109:1945-1952
26. Kopp HG, Hooper AT, Broekman MJ, Avecilla ST, Petit I, Luo M, Milde T, Ramos CA, Zhang F, Kopp T, Bornstein P, Jin DK, Marcus AJ, Rafii S: Thrombospondins deployed by thrombopoietic cells determine angiogenic switch and extent of revascularization. J Clin Invest 2006, 116:3277-3291
27. Kyriakides TR, Rojnuckarin P, Reidy MA, Hankenson KD, Papayannopoulou T, Kaushansky K, Bornstein P: Megakaryocytes require thrombospondin-2 for normal platelet formation and function. Blood 2003, 101:3915-3923
28. 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
29. Yang Z, Kyriakides TR, Bornstein P: Matricellular proteins as modulators of cell-matrix interactions: adhesive defect in thrombospondin 2-null fibroblasts is a consequence of increased levels of matrix metalloproteinase-2. Mol Biol Cell 2000, 11:3353-3364
30. Schroen B, Heymans S, Sharma U, Blankesteijn WM, Pokharel S, Cleutjens JP, Porter JG, Evelo CT, Duisters R, van Leeuwen RE, Janssen BJ, Debets JJ, Smits JF, Daemen MJ, Crijns HJ, Bornstein P, Pinto YM: Thrombospondin-2 is essential for myocardial matrix integrity: increased expression identifies failure-prone cardiac hypertrophy. Circ Res 2004, 95:515-522
31. Yang Z, Strickland DK, Bornstein P: Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein-related scavenger receptor and thrombospondin 2. J Biol Chem 2001, 276:8403-8408
32. Waters RE, Terjung RL, Peters KG, Annex BH: Preclinical models of human peripheral arterial occlusive disease: implications for investigation of therapeutic agents. J Appl Physiol 2004, 97:773-780
33. Heil M, Schaper W: Cellular mechanisms of arteriogenesis. EXS 2005, 94:181-191
34. Heil M, Schaper W: Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ Res 2004, 95:449-458
35. Xu J, Rodriguez D, Kim JJ, Brooks PC: Generation of monoclonal antibodies to cryptic collagen sites by using subtractive immunization. Hybridoma 2000, 19:375-385
36. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, Shibata R, Ouchi N, Easton RM, Galasso G, Birnbaum MJ, Walsh K, Sessa WC: Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest 2005, 115:2119-2127
37. Yu J, deMuinck ED, Zhuang Z, Drinane M, Kauser K, Rubanyi GM, Qian HS, Murata T, Escalante B, Sessa WC: Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc Natl Acad Sci USA 2005, 102:10999-11004
38. Tritsaris K, Myren M, Ditlev SB, Hubschmann MV, van der Blom I, Hansen AJ, Olsen UB, Cao R, Zhang J, Jia T, Wahlberg E, Dissing S, Cao Y: IL-20 is an arteriogenic cytokine that remodels collateral networks and improves functions of ischemic hind limbs. Proc Natl Acad Sci USA 2007, 104:15364-15369
39. Agah A, Kyriakides TR, Bornstein P: Proteolysis of cell-surface tissue transglutaminase by matrix metalloproteinase-2 contributes to the adhesive defect and matrix abnormalities in thrombospondin-2-null fibroblasts and mice. Am J Pathol 2005, 167:81-88
40. 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
41. Agah A, Kyriakides TR, Letrondo N, Bjorkblom B, Bornstein P: Thrombospondin 2 levels are increased in aged mice: consequences for cutaneous wound healing and angiogenesis. Matrix Biol 2004, 22:539-547
42. Gagne PJ, Tihonov N, Li X, Glaser J, Qiao J, Silberstein M, Yee H, Gagne E, Brooks P: Temporal exposure of cryptic collagen epitopes within ischemic muscle during hindlimb reperfusion. Am J Pathol 2005, 167:1349-1359
43. Johnson C, Sung HJ, Lessner SM, Fini ME, Galis ZS: Matrix metalloproteinase-9 is required for adequate angiogenic revascularization of ischemic tissues: potential role in capillary branching. Circ Res 2004, 94:262-268
44. Cheng XW, Kuzuya M, Nakamura K, Maeda K, Tsuzuki M, Kim W, Sasaki T, Liu Z, Inoue N, Kondo T, Jin H, Numaguchi Y, Okumura K, Yokota M, Iguchi A, Murohara T: Mechanisms underlying the impairment of ischemia-induced neovascularization in matrix metalloproteinase 2-deficient mice. Circ Res 2007, 100:904-913
45. Cheng XW, Kuzuya M, Nakamura K, Maeda K, Tsuzuki M, Kim W, Sasaki T, Liu Z, Inoue N, Kondo T, Jin H, Numaguchi Y, Okumura K, Yokota M, Iguchi A, Murohara T: Mechanisms underlying the impairment of ischemia-induced neovascularization in matrix metalloproteinase 2-deficient mice. Circ Res 2007, 100:904-913
46. Simons M: Angiogenesis: where do we stand now? Circulation 2005, 111:1556-1566
47. Helisch A, Schaper W: Arteriogenesis: the development and growth of collateral arteries. Microcirculation 2003, 10:83-97
48. 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
49. Fears CY, Grammer JR, Stewart Jr JE, Annis DS, Mosher DF, Bornstein P, Gladson CL: Low-density lipoprotein receptor-related protein contributes to the antiangiogenic activity of thrombospondin-2 in a murine glioma model. Cancer Res 2005, 65:9338-9346
50. Bein K, Simons M: Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity. J Biol Chem 2000, 275:32167-32173
51. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D: Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000, 2:737-744
52. Lee S, Jilani SM, Nikolova GV, Carpizo D, Iruela-Arispe ML: Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 2005, 169:681-691
53. Rodriguez-Manzaneque JC, Lane TF, Ortega MA, Hynes RO, Lawler J, Iruela-Arispe ML: Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc Natl Acad Sci USA 2001, 98:12485-12490
54. Isenberg JS, Romeo MJ, Yu C, Yu CK, Nghiem K, Monsale J, Rick ME, Wink DA, Frazier WA, Roberts DD: Thrombospondin-1 stimulates platelet aggregation by blocking the anti-thrombotic activity of nitric oxide/cGMP signaling. Blood 2008, 111:613-623