Thrombospondin-1 and CD47 regulation of cardiac, pulmonary and vascular responses in health and disease

Matrix Biology

Volumn 37, Issue , 2014, Pages 92-101

  Rogers, Natasha M ^a,b   Sharifi Sanjani, Maryam ^a   Csányi, Gábor ^a   Pagano, Patrick J ^a   Isenberg, Jeffrey S ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Blood flow; Cardiovascular disease; CD47; Nitric oxide; ROS; Thrombospondin 1

Indexed keywords

CD47 ANTIGEN; CELL SURFACE RECEPTOR; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; THROMBOSPONDIN 1; CD47 PROTEIN, HUMAN; CYCLIC AMP; CYCLIC GMP; VASCULOTROPIN A;

ARTICLE; BLOOD FLOW; BLOOD PRESSURE; BLOOD VESSEL; BLOOD VESSEL TONE; CARDIOPULMONARY HEMODYNAMICS; CARDIOVASCULAR DISEASE; HUMAN; IN VIVO STUDY; NONHUMAN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR SMOOTH MUSCLE; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; THROMBOSIS;

ANTIGENS, CD47; CARDIOVASCULAR DISEASES; CYCLIC AMP; CYCLIC GMP; GENE EXPRESSION REGULATION; HUMANS; MODELS, BIOLOGICAL; NITRIC OXIDE; REGIONAL BLOOD FLOW; SIGNAL TRANSDUCTION; THROMBOSIS; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84908329397     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.01.002     Document Type: Review

References (144)

1. Adams J.C., Lawler J. The thrombospondins. Cold Spring Harb. Perspect. Biol. 2011, 3:a009712.
2. Allwood M.J. Blood flow in the foot and calf in the elderly; a comparison with that in young adults. Clin. Sci. (Lond.) 1958, 17:331-338.
3. Andraweera P.H., Dekker G.A., Thompson S.D., North R.A., McCowan L.M., Roberts C.T., Scope C. A functional variant in the thrombospondin-1 gene and the risk of small for gestational age infants. J. Thromb. Haemost. 2011, 9:2221-2228.
4. Audet G.N., Fulks D., Stricker J.C., Olfert I.M. Chronic delivery of a thrombospondin-1 mimetic decreases skeletal muscle capillarity in mice. PLoS One 2013, 8:e55953.
5. Baenziger N.L., Brodie G.N., Majerus P.W. A thrombin-sensitive protein of human platelet membranes. Proc. Natl. Acad. Sci. U. S. A. 1971, 68:240-243.
6. Bath P.M. The effect of nitric oxide-donating vasodilators on monocyte chemotaxis and intracellular cGMP concentrations in vitro. Eur. J. Clin. Pharmacol. 1993, 45:53-58.
7. Batlle M., Perez-Villa F., Lazaro A., Garcia-Pras E., Vallejos I., Sionis A., Castel M.A., Roig E. Decreased expression of thrombospondin-1 in failing hearts may favor ventricular remodeling. Transplant. Proc. 2009, 41:2231-2233.
8. Bauer E.M., Qin Y., Miller T.W., Bandle R.W., Csanyi G., Pagano P.J., Bauer P.M., Schnermann J., Roberts D.D., Isenberg J.S. Thrombospondin-1 supports blood pressure by limiting eNOS activation and endothelial-dependent vasorelaxation. Cardiovasc. Res. 2010, 88:471-481.
9. Bauer P.M., Bauer E.M., Rogers N.M., Yao M., Feijoo-Cuaresma M., Pilewski J.M., Champion H.C., Zuckerbraun B.S., Calzada M.J., Isenberg J.S. Activated CD47 promotes pulmonary arterial hypertension through targeting caveolin-1. Cardiovasc. Res. 2012, 93:682-693.
10. Bergseth G., Lappegard K.T., Videm V., Mollnes T.E. A novel enzyme immunoassay for plasma thrombospondin. Comparison with beta-thromboglobulin as platelet activation marker in vitro and in vivo. Thromb. Res. 2000, 99:41-50.
11. Blecher K., Martinez L.R., Tuckman-Vernon C., Nacharaju P., Schairer D., Chouake J., Friedman J.M., Alfieri A., Guha C., Nosanchuk J.D., Friedman A.J. Nitric oxide-releasing nanoparticles accelerate wound healing in NOD-SCID mice. Nanomedicine 2012, 8:1364-1371.
12. Bredt D.S., Snyder S.H. Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 1994, 63:175-195.
13. Butt E., Abel K., Krieger M., Palm D., Hoppe V., Hoppe J., Walter U. cAMP- and cGMP-dependent protein kinase phosphorylation sites of the focal adhesion vasodilator-stimulated phosphoprotein (VASP) in vitro and in intact human platelets. J. Biol. Chem. 1994, 269:14509-14517.
14. Canfield A.E., Farrington C., Dziobon M.D., Boot-Handford R.P., Heagerty A.M., Kumar S.N., Roberts I.S. The involvement of matrix glycoproteins in vascular calcification and fibrosis: an immunohistochemical study. J. Pathol. 2002, 196:228-234.
15. Carlson C.B., Lawler J., Mosher D.F. Structures of thrombospondins. Cell. Mol. Life Sci. 2008, 65:672-686.
16. Centers for Disease, C.Prevention Prevalence of coronary heart disease - United States, 2006-2010. MMWR Morb. Mortal. Wkly Rep. 2011, 60:1377-1381.
17. Centers for Disease, C.Prevention Vital signs: avoidable deaths from heart disease, stroke, and hypertensive disease - United States, 2001-2010. MMWR Morb. Mortal. Wkly Rep. 2013, 62:721-727.
18. Chin M.S., Freniere B.B., Bonney C.F., Lancerotto L., Saleeby J.H., Lo Y.C., Orgill D.P., Fitzgerald T.J., Lalikos J.F. Skin perfusion and oxygenation changes in radiation fibrosis. Plast. Reconstr. Surg. 2013, 131:707-716.
19. Chirkov Y.Y., Horowitz J.D. Impaired tissue responsiveness to organic nitrates and nitric oxide: a new therapeutic frontier?. Pharmacol. Ther. 2007, 116:287-305.
20. Csanyi G., Yao M., Rodriguez A.I., Al Ghouleh I., Sharifi-Sanjani M., Frazziano G., Huang X., Kelley E.E., Isenberg J.S., Pagano P.J. Thrombospondin-1 regulates blood flow via CD47 receptor-mediated activation of NADPH oxidase 1. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2966-2973.
21. Dameron K.M., Volpert O.V., Tainsky M.A., Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 1994, 265:1582-1584.
22. Derakhshan B., Hao G., Gross S.S. Balancing reactivity against selectivity: the evolution of protein S-nitrosylation as an effector of cell signaling by nitric oxide. Cardiovasc. Res. 2007, 75:210-219.
23. Derakhshan B., Wille P.C., Gross S.S. Unbiased identification of cysteine S-nitrosylation sites on proteins. Nat. Protoc. 2007, 2:1685-1691.
24. Devaux Y., Azuaje F., Vausort M., Yvorra C., Wagner D.R. Integrated protein network and microarray analysis to identify potential biomarkers after myocardial infarction. Funct. Integr. Genomics 2010, 10:329-337.
25. Dinerman J.L., Lowenstein C.J., Snyder S.H. Molecular mechanisms of nitric oxide regulation. Potential relevance to cardiovascular disease. Circ. Res. 1993, 73:217-222.
26. DiPietro L.A., Polverini P.J. Angiogenic macrophages produce the angiogenic inhibitor thrombospondin 1. Am. J. Pathol. 1993, 143:678-684.
27. Eid A.H. cAMP induces adhesion of microvascular smooth muscle cells to fibronectin via an Epac-mediated but PKA-independent mechanism. Cell. Physiol. Biochem. 2012, 30:247-258.
28. Faulcon L.M., Fu Z., Dulloor P., Barron-Casella E., Savage W., Jennings J.M., Van Eyk J.E., Debaun M., Casella J.F., Everett A. Thrombospondin-1 and L-selectin are associated with silent cerebral infarct in children with sickle cell anaemia. Br. J. Haematol. 2013, 162:421-424.
29. Fleming I., Busse R. Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003, 284:R1-R12.
30. Floquet N., Dedieu S., Martiny L., Dauchez M., Perahia D. Human thrombospondin's (TSP-1) C-terminal domain opens to interact with the CD-47 receptor: a molecular modeling study. Arch. Biochem. Biophys. 2008, 478:103-109.
31. Frangogiannis N.G., Ren G., Dewald O., Zymek P., Haudek S., Koerting A., Winkelmann K., Michael L.H., Lawler J., Entman M.L. Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation 2005, 111:2935-2942.
32. Frazier E.P., Isenberg J.S., Shiva S., Zhao L., Schlesinger P., Dimitry J., Abu-Asab M.S., Tsokos M., Roberts D.D., Frazier W.A. Age-dependent regulation of skeletal muscle mitochondria by the thrombospondin-1 receptor CD47. Matrix Biol. 2011, 30:154-161.
33. Freyberg M.A., Kaiser D., Graf R., Vischer P., Friedl P. Integrin-associated protein and thrombospondin-1 as endothelial mechanosensitive death mediators. Biochem. Biophys. Res. Commun. 2000, 271:584-588.
34. Freyberg M.A., Kaiser D., Graf R., Buttenbender J., Friedl P. Proatherogenic flow conditions initiate endothelial apoptosis via thrombospondin-1 and the integrin-associated protein. Biochem. Biophys. Res. Commun. 2001, 286:141-149.
35. Frieda S., Pearce A., Wu J., Silverstein R.L. Recombinant GST/CD36 fusion proteins define a thrombospondin binding domain. Evidence for a single calcium-dependent binding site on CD36. J. Biol. Chem. 1995, 270:2981-2986.
36. Go A.S., Mozaffarian D., Roger V.L., Benjamin E.J., Berry J.D., Borden W.B., Bravata D.M., Dai S., Ford E.S., Fox C.S., Franco S., Fullerton H.J., Gillespie C., Hailpern S.M., Heit J.A., Howard V.J., Huffman M.D., Kissela B.M., Kittner S.J., Lackland D.T., Lichtman J.H., Lisabeth L.D., Magid D., Marcus G.M., Marelli A., Matchar D.B., McGuire D.K., Mohler E.R., Moy C.S., Mussolino M.E., Nichol G., Paynter N.P., Schreiner P.J., Sorlie P.D., Stein J., Turan T.N., Virani S.S., Wong N.D., Woo D., Turner M.B., American Heart Association Statistics, C.Stroke Statistics, S. Heart disease and stroke statistics - 2013 update: a report from the American Heart Association. Circulation 2013, 127:e6-e245.
37. Godyna S., Liau G., Popa I., Stefansson S., Argraves W.S. Identification of the low density lipoprotein receptor-related protein (LRP) as an endocytic receptor for thrombospondin-1. J. Cell Biol. 1995, 129:1403-1410.
38. Golledge J., Clancy P., Hankey G.J., Norman P.E. Relation between serum thrombospondin-2 and cardiovascular mortality in older men screened for abdominal aortic aneurysm. Am. J. Cardiol. 2013, 111:1800-1804.
39. Greenaway J., Lawler J., Moorehead R., Bornstein P., Lamarre J., Petrik J. Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1). J. Cell. Physiol. 2007, 210:807-818.
40. Gupta K., Gupta P., Wild R., Ramakrishnan S., Hebbel R.P. Binding and displacement of vascular endothelial growth factor (VEGF) by thrombospondin: effect on human microvascular endothelial cell proliferation and angiogenesis. Angiogenesis 1999, 3:147-158.
41. Hamamdzic D., Wilensky R.L. Porcine models of accelerated coronary atherosclerosis: role of diabetes mellitus and hypercholesterolemia. J. Diabetes Res. 2013, 2013:761415.
42. Harrison D.G., Gongora M.C., Guzik T.J., Widder J. Oxidative stress and hypertension. J. Am. Soc. Hypertens. 2007, 1:30-44.
43. Heinrich T.A., da Silva R.S., Miranda K.M., Switzer C.H., Wink D.A., Fukuto J.M. Biological nitric oxide signalling: chemistry and terminology. Br. J. Pharmacol. 2013, 169:1417-1429.
44. Hogg P.J., Hotchkiss K.A., Jimenez B.M., Stathakis P., Chesterman C.N. Interaction of platelet-derived growth factor with thrombospondin 1. Biochem. J. 1997, 326(Pt 3):709-716.
45. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:9265-9269.
46. Iruela-Arispe M.L., Lombardo M., Krutzsch H.C., Lawler J., Roberts D.D. Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation 1999, 100:1423-1431.
47. Isenberg J.S., Calzada M.J., Zhou L., Guo N., Lawler J., Wang X.Q., Frazier W.A., Roberts D.D. Endogenous thrombospondin-1 is not necessary for proliferation but is permissive for vascular smooth muscle cell responses to platelet-derived growth factor. Matrix Biol. 2005, 24:110-123.
48. Isenberg J.S., Ridnour L.A., Perruccio E.M., Espey M.G., Wink D.A., Roberts D.D. Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13141-13146.
49. Isenberg J.S., Ridnour L.A., Dimitry J., Frazier W.A., Wink D.A., Roberts D.D. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J. Biol. Chem. 2006, 281:26069-26080.
50. Isenberg J.S., Ridnour L.A., Thomas D.D., Wink D.A., Roberts D.D., Espey M.G. Guanylyl cyclase-dependent chemotaxis of endothelial cells in response to nitric oxide gradients. Free Radic. Biol. Med. 2006, 40:1028-1033.
51. Isenberg J.S., Wink D.A., Roberts D.D. Thrombospondin-1 antagonizes nitric oxide-stimulated vascular smooth muscle cell responses. Cardiovasc. Res. 2006, 71:785-793.
52. Isenberg J.S., Hyodo F., Pappan L.K., Abu-Asab M., Tsokos M., Krishna M.C., Frazier W.A., Roberts D.D. Blocking thrombospondin-1/CD47 signaling alleviates deleterious effects of aging on tissue responses to ischemia. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2582-2588.
53. Isenberg J.S., Romeo M.J., Abu-Asab M., Tsokos M., Oldenborg A., Pappan L., Wink D.A., Frazier W.A., Roberts D.D. Increasing survival of ischemic tissue by targeting CD47. Circ. Res. 2007, 100:712-720.
54. Isenberg J.S., Maxhimer J.B., Powers P., Tsokos M., Frazier W.A., Roberts D.D. Treatment of liver ischemia-reperfusion injury by limiting thrombospondin-1/CD47 signaling. Surgery 2008, 144:752-761.
55. Isenberg J.S., Pappan L.K., Romeo M.J., Abu-Asab M., Tsokos M., Wink D.A., Frazier W.A., Roberts D.D. Blockade of thrombospondin-1-CD47 interactions prevents necrosis of full thickness skin grafts. Ann. Surg. 2008, 247:180-190.
56. Isenberg J.S., Romeo M.J., Maxhimer J.B., Smedley J., Frazier W.A., Roberts D.D. Gene silencing of CD47 and antibody ligation of thrombospondin-1 enhance ischemic tissue survival in a porcine model: implications for human disease. Ann. Surg. 2008, 247:860-868.
57. Isenberg J.S., Romeo M.J., Yu C., Yu C.K., Nghiem K., Monsale J., Rick M.E., Wink D.A., Frazier W.A., Roberts D.D. Thrombospondin-1 stimulates platelet aggregation by blocking the antithrombotic activity of nitric oxide/cGMP signaling. Blood 2008, 111:613-623.
58. Isenberg J.S., Yu C., Roberts D.D. Differential effects of ABT-510 and a CD36-binding peptide derived from the type 1 repeats of thrombospondin-1 on fatty acid uptake, nitric oxide signaling, and caspase activation in vascular cells. Biochem. Pharmacol. 2008, 75:875-882.
59. Isenberg J.S., Annis D.S., Pendrak M.L., Ptaszynska M., Frazier W.A., Mosher D.F., Roberts D.D. Differential interactions of thrombospondin-1, -2, and-4 with CD47 and effects on cGMP signaling and ischemic injury responses. J. Biol. Chem. 2009, 284:1116-1125.
60. Isenberg J.S., Qin Y., Maxhimer J.B., Sipes J.M., Despres D., Schnermann J., Frazier W.A., Roberts D.D. Thrombospondin-1 and CD47 regulate blood pressure and cardiac responses to vasoactive stress. Matrix Biol. 2009, 28:110-119.
61. Isenberg J.S., Martin-Manso G., Maxhimer J.B., Roberts D.D. Regulation of nitric oxide signalling by thrombospondin 1: implications for anti-angiogenic therapies. Nat. Rev. Cancer 2009, 9(3):182-194. http://dx.doi.org/10.1038/nrc2561. (Electronic publication ahead of print 2009 Feb 5). Review. PMID:19194382.
62. Jearawiriyapaisarn N., Moulton H.M., Sazani P., Kole R., Willis M.S. Long-term improvement in mdx cardiomyopathy after therapy with peptide-conjugated morpholino oligomers. Cardiovasc. Res. 2010, 85:444-453.
63. Jin G., Tsuji K., Xing C., Yang Y.G., Wang X., Lo E.H. CD47 gene knockout protects against transient focal cerebral ischemia in mice. Exp. Neurol. 2009, 217:165-170.
64. Jurk K., Ritter M.A., Schriek C., Van Aken H., Droste D.W., Ringelstein E.B., Kehrel B.E. Activated monocytes capture platelets for heterotypic association in patients with severe carotid artery stenosis. Thromb. Haemost. 2010, 103:1193-1202.
65. Kataoka Y., Shao M., Wolski K., Uno K., Puri R., Tuzcu E.M., Nissen S.E., Nicholls S.J. Multiple risk factor intervention and progression of coronary atherosclerosis in patients with type 2 diabetes mellitus. Eur. J. Prev. Cardiol. 2013, 20:209-217.
66. Kaur S., Martin-Manso G., Pendrak M.L., Garfield S.H., Isenberg J.S., Roberts D.D. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J. Biol. Chem. 2010, 285:38923-38932.
67. Kaur S., Kuznetsova S.A., Pendrak M.L., Sipes J.M., Romeo M.J., Li Z., Zhang L., Roberts D.D. Heparan sulfate modification of the transmembrane receptor CD47 is necessary for inhibition of T cell receptor signaling by thrombospondin-1. J. Biol. Chem. 2011, 286:14991-15002.
68. Koltsova E.K., Hedrick C.C., Ley K. Myeloid cells in atherosclerosis: a delicate balance of anti-inflammatory and proinflammatory mechanisms. Curr. Opin. Lipidol. 2013, 24:371-380.
69. Kvansakul M., Adams J.C., Hohenester E. Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO J. 2004, 23:1223-1233.
70. Laklai H., Laval S., Dumartin L., Rochaix P., Hagedorn M., Bikfalvi A., Le Guellec S., Delisle M.B., Schally A.V., Susini C., Pyronnet S., Bousquet C. Thrombospondin-1 is a critical effector of oncosuppressive activity of sst2 somatostatin receptor on pancreatic cancer. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17769-17774.
71. Lawler J. The functions of thrombospondin-1 and -2. Curr. Opin. Cell Biol. 2000, 12:634-640.
72. Lawler P.R., Lawler J. Molecular basis for the regulation of angiogenesis by thrombospondin-1 and-2. Cold Spring Harb. Perspect. Med. 2012, 2:a006627.
73. Lee T., Esemuede N., Sumpio B.E., Gahtan V. Thrombospondin-1 induces matrix metalloproteinase-2 activation in vascular smooth muscle cells. J. Vasc. Surg. 2003, 38:147-154.
74. Li S.S., Ivanoff A., Bergstrom S.E., Sandstrom A., Christensson B., van Nerven J., Holgersson J., Hauzenberger D., Arencibia I., Sundqvist K.G. T lymphocyte expression of thrombospondin-1 and adhesion to extracellular matrix components. Eur. J. Immunol. 2002, 32:1069-1079.
75. Ligi I., Simoncini S., Tellier E., Vassallo P.F., Sabatier F., Guillet B., Lamy E., Sarlon G., Quemener C., Bikfalvi A., Marcelli M., Pascal A., Dizier B., Simeoni U., Dignat-George F., Anfosso F. A switch toward angiostatic gene expression impairs the angiogenic properties of endothelial progenitor cells in low birth weight preterm infants. Blood 2011, 118:1699-1709.
76. Lin T.N., Kim G.M., Chen J.J., Cheung W.M., He Y.Y., Hsu C.Y. Differential regulation of thrombospondin-1 and thrombospondin-2 after focal cerebral ischemia/reperfusion. Stroke 2003, 34:177-186.
77. Lincoln T.M., Dey N., Sellak H. Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J. Appl. Physiol. 2001, 91:1421-1430. ((1985)).
78. Liu Z., Zhao Q., Han Q., Gao M., Zhang N. Serum thrombospondin-1 is altered in patients with hemorrhagic fever with renal syndrome. J. Med. Virol. 2008, 80:1799-1803.
79. Malek M.H., Olfert I.M. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp. Physiol. 2009, 94:749-760.
80. Maloney J.P., Stearman R.S., Bull T.M., Calabrese D.W., Tripp-Addison M.L., Wick M.J., Broeckel U., Robbins I.M., Wheeler L.A., Cogan J.D., Loyd J.E. Loss-of-function thrombospondin-1 mutations in familial pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 302:L541-L554.
81. Martin-Manso G., Galli S., Ridnour L.A., Tsokos M., Wink D.A., Roberts D.D. Thrombospondin 1 promotes tumor macrophage recruitment and enhances tumor cell cytotoxicity of differentiated U937 cells. Cancer Res. 2008, 68:7090-7099.
82. Maxhimer J.B., Shih H.B., Isenberg J.S., Miller T.W., Roberts D.D. Thrombospondin-1/CD47 blockade following ischemia-reperfusion injury is tissue protective. Plast. Reconstr. Surg. 2009, 124:1880-1889.
83. Maxhimer J.B., Soto-Pantoja D.R., Ridnour L.A., Shih H.B., Degraff W.G., Tsokos M., Wink D.A., Isenberg J.S., Roberts D.D. Radioprotection in normal tissue and delayed tumor growth by blockade of CD47 signaling. Sci. Transl. Med. 2009, 1. (3ra7).
84. McCready R.A., Hyde G.L., Bivins B.A., Mattingly S.S., Griffen W.O. Radiation-induced arterial injuries. Surgery 1983, 93:306-312.
85. McCrohan M.B., Huang S.W., Sleasman J.W., Klein P.A., Kao K.J. Plasma thrombospondin as an indicator of intravascular platelet activation in patients with vasculitis. Thromb. Haemost. 1987, 58:850-852.
86. Mikhailenko I., Krylov D., Argraves K.M., Roberts D.D., Liau G., Strickland D.K. Cellular internalization and degradation of thrombospondin-1 is mediated by the amino-terminal heparin binding domain (HBD). High affinity interaction of dimeric HBD with the low density lipoprotein receptor-related protein. J. Biol. Chem. 1997, 272:6784-6791.
87. Miller T.W., Isenberg J.S., Roberts D.D. Thrombospondin-1 is an inhibitor of pharmacological activation of soluble guanylate cyclase. Br. J. Pharmacol. 2010, 159:1542-1547.
88. Moncada S., Higgs A. The L-arginine-nitric oxide pathway. N. Engl. J. Med. 1993, 329:2002-2012.
89. Moulton H.M., Moulton J.D. Morpholinos and their peptide conjugates: therapeutic promise and challenge for Duchenne muscular dystrophy. Biochim. Biophys. Acta 2010, 1798:2296-2303.
90. Moura R., Tjwa M., Vandervoort P., Cludts K., Hoylaerts M.F. Thrombospondin-1 activates medial smooth muscle cells and triggers neointima formation upon mouse carotid artery ligation. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2163-2169.
91. Murphy-Ullrich J.E., Iozzo R.V. Thrombospondins in physiology and disease: new tricks for old dogs. Matrix Biol. 2012, 31:152-154.
92. Napoli C., Ignarro L.J. Nitric oxide and pathogenic mechanisms involved in the development of vascular diseases. Arch. Pharm. Res. 2009, 32:1103-1108.
93. Narizhneva N.V., Byers-Ward V.J., Quinn M.J., Zidar F.J., Plow E.F., Topol E.J., Byzova T.V. Molecular and functional differences induced in thrombospondin-1 by the single nucleotide polymorphism associated with the risk of premature, familial myocardial infarction. J. Biol. Chem. 2004, 279:21651-21657.
94. Narizhneva N.V., Razorenova O.V., Podrez E.A., Chen J., Chandrasekharan U.M., DiCorleto P.E., Plow E.F., Topol E.J., Byzova T.V. Thrombospondin-1 up-regulates expression of cell adhesion molecules and promotes monocyte binding to endothelium. FASEB J. 2005, 19:1158-1160.
95. Nor J.E., Mitra R.S., Sutorik M.M., Mooney D.J., Castle V.P., Polverini P.J. Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J. Vasc. Res. 2000, 37:209-218.
96. Novelli E.M., Kato G.J., Ragni M.V., Zhang Y., Hildesheim M.E., Nouraie M., Barge S., Meyer M.P., Hassett A.C., Gordeuk V.R., Gladwin M.T., Isenberg J.S. Plasma thrombospondin-1 is increased during acute sickle cell vaso-occlusive events and associated with acute chest syndrome, hydroxyurea therapy, and lower hemolytic rates. Am. J. Hematol. 2012, 87:326-330.
97. Ochoa C.D., Fouty B.W., Hales C.A. Thrombospondin-1, endothelium and systemic vascular tone. Future Cardiol. 2011, 7:169-172.
98. Odievre M.H., Bony V., Benkerrou M., Lapoumeroulie C., Alberti C., Ducrocq R., Jacqz-Aigrain E., Elion J., Cartron J.P. Modulation of erythroid adhesion receptor expression by hydroxyurea in children with sickle cell disease. Haematologica 2008, 93:502-510.
99. Olsson M., Oldenborg P.A. CD47 on experimentally senescent murine RBCs inhibits phagocytosis following Fcgamma receptor-mediated but not scavenger receptor-mediated recognition by macrophages. Blood 2008, 112:4259-4267.
100. Panchatcharam M., Miriyala S., Yang F., Leitges M., Chrzanowska-Wodnicka M., Quilliam L.A., Anaya P., Morris A.J., Smyth S.S. Enhanced proliferation and migration of vascular smooth muscle cells in response to vascular injury under hyperglycemic conditions is controlled by beta3 integrin signaling. Int. J. Biochem. Cell Biol. 2010, 42:965-974.
101. Patel M.K., Lymn J.S., Clunn G.F., Hughes A.D. Thrombospondin-1 is a potent mitogen and chemoattractant for human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 1997, 17:2107-2114.
102. Phelan M.W., Forman L.W., Perrine S.P., Faller D.V. Hypoxia increases thrombospondin-1 transcript and protein in cultured endothelial cells. J. Lab. Clin. Med. 1998, 132:519-529.
103. Qian X., Wang T.N., Rothman V.L., Nicosia R.F., Tuszynski G.P. Thrombospondin-1 modulates angiogenesis in vitro by up-regulation of matrix metalloproteinase-9 in endothelial cells. Exp. Cell Res. 1997, 235:403-412.
104. Rabinovitch M. Molecular pathogenesis of pulmonary arterial hypertension. J. Clin. Invest. 2012, 122:4306-4313.
105. Radomski M.W., Palmer R.M., Moncada S. Modulation of platelet aggregation by an L-arginine-nitric oxide pathway. Trends Pharmacol. Sci. 1991, 12:87-88.
106. Raman P., Krukovets I., Marinic T.E., Bornstein P., Stenina O.I. Glycosylation mediates up-regulation of a potent antiangiogenic and proatherogenic protein, thrombospondin-1, by glucose in vascular smooth muscle cells. J. Biol. Chem. 2007, 282:5704-5714.
107. Ramanathan S., Mazzalupo S., Boitano S., Montfort W.R. Thrombospondin-1 and angiotensin II inhibit soluble guanylyl cyclase through an increase in intracellular calcium concentration. Biochemistry 2011, 50(36):7787-7799. [Electronic publication ahead of print 2011 Aug 16]. PMID:21823650. 10.1021/bi201060c.
108. Rath G.M., Schneider C., Dedieu S., Sartelet H., Morjani H., Martiny L.El, Btaouri H. Thrombospondin-1C-terminal-derived peptide protects thyroid cells from ceramide-induced apoptosis through the adenylyl cyclase pathway. Int. J. Biochem. Cell Biol. 2006, 38:2219-2228.
109. Riessen R., Kearney M., Lawler J., Isner J.M. Immunolocalization of thrombospondin-1 in human atherosclerotic and restenotic arteries. Am. Heart J. 1998, 135:357-364.
110. Roberts D.D., Miller T.W., Rogers N.M., Yao M., Isenberg J.S. The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47. Matrix Biol. 2012, 31:162-169.
111. Rogers N.M., Thomson A.W., Isenberg J.S. Activation of parenchymal CD47 promotes renal ischemia-reperfusion injury. J. Am. Soc. Nephrol. 2012, 23:1538-1550.
112. Rogers N.M., Roberts D.D., Isenberg J.S. Age-associated induction of cell membrane CD47 limits basal and temperature-induced changes in cutaneous blood flow. Ann. Surg. 2013, 258:184-191.
113. Roue G., Bitton N., Yuste V.J., Montange T., Rubio M., Dessauge F., Delettre C., Merle-Beral H., Sarfati M., Susin S.A. Mitochondrial dysfunction in CD47-mediated caspase-independent cell death: ROS production in the absence of cytochrome c and AIF release. Biochimie 2003, 85:741-746.
114. Sarfati M., Fortin G., Raymond M., Susin S. CD47 in the immune response: role of thrombospondin and SIRP-alpha reverse signaling. Curr. Drug Targets 2008, 9:842-850.
115. Saumet A., Slimane M.B., Lanotte M., Lawler J., Dubernard V. Type 3 repeat/C-terminal domain of thrombospondin-1 triggers caspase-independent cell death through CD47/alphavbeta3 in promyelocytic leukemia NB4 cells. Blood 2005, 106:658-667.
116. Scarborough J.E., Daggett C.W., Lodge A.J., Chai P.J., Williamson J.A., Jaggers J., George S.E., Ungerleider R.M. The role of endothelial nitric oxide synthase expression in the development of pulmonary hypertension in chronically hypoxic infant swine. J. Thorac. Cardiovasc. Surg. 1998, 115:343-348. (discussion 348-350).
117. Schaffer M., Bongartz M., Fischer S., Proksch B., Viebahn R. Nitric oxide restores impaired healing in normoglycaemic diabetic rats. J. Wound Care 2007, 16:311-316.
118. Schultz-Cherry S., Lawler J., Murphy-Ullrich J.E. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 1994, 269:26783-26788.
119. Schultz-Cherry S., Ribeiro S., Gentry L., Murphy-Ullrich J.E. Thrombospondin binds and activates the small and large forms of latent transforming growth factor-beta in a chemically defined system. J. Biol. Chem. 1994, 269:26775-26782.
120. Sedeek M., Hebert R.L., Kennedy C.R., Burns K.D., Touyz R.M. Molecular mechanisms of hypertension: role of Nox family NADPH oxidases. Curr. Opin. Nephrol. Hypertens. 2009, 18:122-127.
121. Sezaki S., Hirohata S., Iwabu A., Nakamura K., Toeda K., Miyoshi T., Yamawaki H., Demircan K., Kusachi S., Shiratori Y., Ninomiya Y. Thrombospondin-1 is induced in rat myocardial infarction and its induction is accelerated by ischemia/reperfusion. Exp. Biol. Med. (Maywood) 2005, 230:621-630.
122. Shabani M., Pulfer S.K., Bulgrin J.P., Smith D.J. Enhancement of wound repair with a topically applied nitric oxide-releasing polymer. Wound Repair Regen. 1996, 4:353-362.
123. Shih B., Sultan M.J., Chaudhry I.H., Tan K.T., Johal K.S., Marstan A., Tsai M., Baguneid M., Bayat A. Identification of biomarkers in sequential biopsies of patients with chronic wounds receiving simultaneous acute wounds: a genetic, histological, and noninvasive imaging study. Wound Repair Regen. 2012, 20:757-769.
124. Short S.M., Derrien A., Narsimhan R.P., Lawler J., Ingber D.E., Zetter B.R. Inhibition of endothelial cell migration by thrombospondin-1 type-1 repeats is mediated by beta1 integrins. J. Cell Biol. 2005, 168:643-653.
125. Simantov R., Febbraio M., Crombie R., Asch A.S., Nachman R.L., Silverstein R.L. Histidine-rich glycoprotein inhibits the antiangiogenic effect of thrombospondin-1. J. Clin. Invest. 2001, 107:45-52.
126. Smadja D.M., d'Audigier C., Bieche I., Evrard S., Mauge L., Dias J.V., Labreuche J., Laurendeau I., Marsac B., Dizier B., Wagner-Ballon O., Boisson-Vidal C., Morandi V., Duong-Van-Huyen J.P., Bruneval P., Dignat-George F., Emmerich J., Gaussem P. Thrombospondin-1 is a plasmatic marker of peripheral arterial disease that modulates endothelial progenitor cell angiogenic properties. Arterioscler. Thromb. Vasc. Biol. 2011, 31:551-559.
127. Soto Pantoja D.R., Kaur S., Miller T.W., Isenberg J.S., Roberts D.D. Leukocyte surface antigen CD47. UCSD Molecule Pages Published online: 19 2013, (Apr 2013). 10.6072/H0.MP.A005186.01.
128. Stenina O.I., Krukovets I., Wang K., Zhou Z., Forudi F., Penn M.S., Topol E.J., Plow E.F. Increased expression of thrombospondin-1 in vessel wall of diabetic Zucker rat. Circulation 2003, 107:3209-3215.
129. Thakar C.V., Zahedi K., Revelo M.P., Wang Z., Burnham C.E., Barone S., Bevans S., Lentsch A.B., Rabb H., Soleimani M. Identification of thrombospondin 1 (TSP-1) as a novel mediator of cell injury in kidney ischemia. J. Clin. Invest. 2005, 115:3451-3459.
130. Tooney P.A., Sakai T., Sakai K., Aeschlimann D., Mosher D.F. Restricted localization of thrombospondin-2 protein during mouse embryogenesis: a comparison to thrombospondin-1. Matrix Biol. 1998, 17:131-143.
131. Topol E.J., McCarthy J., Gabriel S., Moliterno D.J., Rogers W.J., Newby L.K., Freedman M., Metivier J., Cannata R., O'Donnell C.J., Kottke-Marchant K., Murugesan G., Plow E.F., Stenina O., Daley G.Q. Single nucleotide polymorphisms in multiple novel thrombospondin genes may be associated with familial premature myocardial infarction. Circulation 2001, 104:2641-2644.
132. Tucker A.N., Lillich T.T. Internally generated reduced nicotinamide adenine dinucleotide as a substrate for glycine transport by membrane vesicles of Paracoccus denitrificans. J. Bacteriol. 1977, 129:559-561.
133. Tulasne D., Judd B.A., Johansen M., Asazuma N., Best D., Brown E.J., Kahn M., Koretzky G.A., Watson S.P. C-terminal peptide of thrombospondin-1 induces platelet aggregation through the Fc receptor gamma-chain-associated signaling pathway and by agglutination. Blood 2001, 98:3346-3352.
134. van den Berg T.K., van der Schoot C.E. Innate immune 'self' recognition: a role for CD47-SIRPalpha interactions in hematopoietic stem cell transplantation. Trends Immunol. 2008, 29:203-206.
135. Wang X.Q., Lindberg F.P., Frazier W.A. Integrin-associated protein stimulates alpha2beta1-dependent chemotaxis via Gi-mediated inhibition of adenylate cyclase and extracellular-regulated kinases. J. Cell Biol. 1999, 147:389-400.
136. Wang S., Lincoln T.M., Murphy-Ullrich J.E. Glucose downregulation of PKG-I protein mediates increased thrombospondin1-dependent TGF-{beta} activity in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 2010, 298:C1188-C1197.
137. Weller R., Finnen M.J. The effects of topical treatment with acidified nitrite on wound healing in normal and diabetic mice. Nitric Oxide 2006, 15:395-399.
138. Wikner N.E., Dixit V.M., Frazier W.A., Clark R.A. Human keratinocytes synthesize and secrete the extracellular matrix protein, thrombospondin. J. Invest. Dermatol. 1987, 88:207-211.
139. Xing C., Lee S., Kim W.J., Jin G., Yang Y.G., Ji X., Wang X., Lo E.H. Role of oxidative stress and caspase 3 in CD47-mediated neuronal cell death. J. Neurochem. 2009, 108:430-436.
140. Xu W., Kaneko F.T., Zheng S., Comhair S.A., Janocha A.J., Goggans T., Thunnissen F.B., Farver C., Hazen S.L., Jennings C., Dweik R.A., Arroliga A.C., Erzurum S.C. Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J. 2004, 18:1746-1748.
141. Yang S.N., Burch M.L., Tannock L.R., Evanko S., Osman N., Little P.J. Transforming growth factor-beta regulation of proteoglycan synthesis in vascular smooth muscle: contribution to lipid binding and accelerated atherosclerosis in diabetes. J. Diabetes 2010, 2:233-242.
142. Yao M., Roberts D.D., Isenberg J.S. Thrombospondin-1 inhibition of vascular smooth muscle cell responses occurs via modulation of both cAMP and cGMP. Pharmacol. Res. 2011, 63:13-22.
143. Zhao X.M., Hu Y., Miller G.G., Mitchell R.N., Libby P. Association of thrombospondin-1 and cardiac allograft vasculopathy in human cardiac allografts. Circulation 2001, 103:525-531.
144. Zhu W., Smart E.J. Myristic acid stimulates endothelial nitric-oxide synthase in a CD36- and an AMP kinase-dependent manner. J. Biol. Chem. 2005, 280:29543-29550.