The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47

Matrix Biology

Volumn 31, Issue 3, 2012, Pages 162-169

  Roberts, David D ^a   Miller, Thomas W ^a   Rogers, Natasha M ^c   Yao, Mingyi ^c   Isenberg, Jeffrey S ^b,c  

^a NATIONAL CANCER INSTITUTE   (United States)

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

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

Blood pressure; CD47; CGMP; Ischemia; Nitric oxide; Thrombospondin 1

Indexed keywords

ACETYLCHOLINE; CD47 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; THROMBOSPONDIN 1; VASCULOTROPIN;

AGING; ALZHEIMER DISEASE; ANGIOGENESIS; ARTERY DILATATION; ATHEROSCLEROSIS; AUTONOMIC INNERVATION; BLOOD FLOW; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR RESPONSE; CELL PROLIFERATION; CHRONIC DISEASE; DIASTOLIC BLOOD PRESSURE; ENDOTHELIUM CELL; HEMOSTASIS; HOMEOSTASIS; HUMAN; HYPERTENSION; IMMUNITY; INJURY; MITOCHONDRION; NEOPLASM; NONHUMAN; PATHOGENESIS; PERIPHERAL VASCULAR DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION; REVIEW; SICKLE CELL ANEMIA; SIGNAL TRANSDUCTION; SKIN FLAP SURVIVAL; STRESS; SYSTOLIC BLOOD PRESSURE; THROMBOCYTE ACTIVATION; TISSUE PERFUSION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD47; CARDIOVASCULAR PHYSIOLOGICAL PROCESSES; CARDIOVASCULAR SYSTEM; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; THROMBOSPONDIN 1;

MUS;

EID: 84857787530     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2012.01.005     Document Type: Review

References (94)

1. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylate cyclase and increases guanosine 3':5'-cyclic monophosphate levels in various tissue preparations. Proc. Natl. Acad. Sci. U. S. A. 1977, 74:3203-3207.
2. Bamberger M.E., Harris M.E., McDonald D.R., Husemann J., Landreth G.E. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J. Neurosci. 2003, 23:2665-2674.
3. 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.
4. Bornstein P. Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J. Cell Biol. 1995, 130:503-506.
5. Bras M., Yuste V.J., Roue G., Barbier S., Sancho P., Virely C., Rubio M., Baudet S., Esquerda J.E., Merle-Beral H., Sarfati M., Susin S.A. Drp1 mediates caspase-independent type III cell death in normal and leukemic cells. Mol. Cell. Biol. 2007, 27:7073-7088.
6. Broere A., Van Den Meiracker A.H., Boomsma F., Derkx F.H., Veld A.J., Schalekamp M.A. Human renal and systemic hemodynamic, natriuretic, and neurohumoral responses to different doses of L-NAME. Am. J. Physiol. 1998, 275:F870-F877.
7. 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.
8. Calzada M.J., Zhou L., Sipes J.M., Zhang J., Krutzsch H.C., Iruela-Arispe M.L., Annis D.S., Mosher D.F., Roberts D.D. α4β1 integrin mediates selective endothelial cell responses to thrombospondins in vitro and modulates angiogenesis in vivo. Circ. Res. 2004, 94:462-470.
9. Carlson C.B., Lawler J., Mosher D.F. Structures of thrombospondins. Cell. Mol. Life Sci. 2008, 65:672-686.
10. Chen D., Asahara T., Krasinski K., Witzenbichler B., Yang J., Magner M., Kearney M., Frazier W.A., Isner J.M., Andres V. Antibody blockade of thrombospondin accelerates reendothelialization and reduces neointima formation in balloon-injured rat carotid artery. Circulation 1999, 100:849-854.
11. 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.
12. Cook S., Hugli O., Egli M., Menard B., Thalmann S., Sartori C., Perrin C., Nicod P., Thorens B., Vollenweider P., Scherrer U., Burcelin R. Partial gene deletion of endothelial nitric oxide synthase predisposes to exaggerated high-fat diet-induced insulin resistance and arterial hypertension. Diabetes 2004, 53:2067-2072.
13. Curwen J.O., Musgrove H.L., Kendrew J., Richmond G.H., Ogilvie D.J., Wedge S.R. Inhibition of vascular endothelial growth factor-a signaling induces hypertension: examining the effect of cediranib (recentin; AZD2171) treatment on blood pressure in rat and the use of concomitant antihypertensive therapy. Clin. Cancer Res. 2008, 14:3124-3131.
14. Danielewski O., Schultess J., Smolenski A. The NO/cGMP pathway inhibits Rap 1 activation in human platelets via cGMP-dependent protein kinase I. Thromb. Haemost. 2005, 93:319-325.
15. Dimmeler S., Dernbach E., Zeiher A.M. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett. 2000, 477:258-262.
16. Dudzinski D.M., Michel T. Life history of eNOS: partners and pathways. Cardiovasc. Res. 2007, 75:247-260.
17. Duval M., Le Boeuf F., Huot J., Gratton J.P. Src-mediated phosphorylation of Hsp90 in response to vascular endothelial growth factor (VEGF) is required for VEGF receptor-2 signaling to endothelial NO synthase. Mol. Biol. Cell 2007, 18:4659-4668.
18. Elzie C.A., Murphy-Ullrich J.E. The N-terminus of thrombospondin: the domain stands apart. Int. J. Biochem. Cell Biol. 2004, 36:1090-1101.
19. Fraisse A., Wessel D.L. Acute pulmonary hypertension in infants and children: cGMP-related drugs. Pediatr. Crit. Care Med. 2010, 11:S37-S40.
20. Frazier W.A., Gao A.-G., Dimitry J., Chung J., Brown E.J., Lindberg F.P., Linder M.E. The thrombospondin receptor integrin-associated protein (CD47) functionally couples to heterotrimeric Gi. J. Biol. Chem. 1999, 274:8554-8560.
21. Frazier W.A., Isenberg J.S., Kaur S., Roberts D.D. CD47., Nature Signaling Gateway 2010.
22. 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.
23. Gao A.-G., Lindberg F.P., Finn M.B., Blystone S.D., Brown E.J., Frazier W.A. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J. Biol. Chem. 1996, 271:21-24.
24. Garcia-Dorado D., Agullo L., Sartorio C.L., Ruiz-Meana M. Myocardial protection against reperfusion injury: the cGMP pathway. Thromb. Haemost. 2009, 101:635-642.
25. Gelinas D.S., Bernatchez P.N., Rollin S., Bazan N.G., Sirois M.G. Immediate and delayed VEGF-mediated NO synthesis in endothelial cells: role of PI3K, PKC and PLC pathways. Br. J. Pharmacol. 2002, 137:1021-1030.
26. Gonzalez D.R., Fernandez I.C., Ordenes P.P., Treuer A.V., Eller G., Boric M.P. Differential role of S-nitrosylation and the NO-cGMP-PKG pathway in cardiac contractility. Nitric Oxide 2008, 18:157-167.
27. 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.
28. 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.
29. Haas B., Mayer P., Jennissen K., Scholz D., Diaz M.B., Bloch W., Herzig S., Fassler R., Pfeifer A. Protein kinase G controls brown fat cell differentiation and mitochondrial biogenesis. Sci. Signal. 2009, 2:ra78.
30. Ignarro L.J. Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J. Physiol. Pharmacol. 2002, 53:503-514.
31. Isenberg J., Calzada M., Zhou L., Guo N., Lawler J., Wang X., Frazier W., Roberts 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.
32. 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.
33. 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.
34. 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.
35. Isenberg J.S., Hyodo F., Matsumoto K., Romeo M.J., Abu-Asab M., Tsokos M., Kuppusamy P., Wink D.A., Krishna M.C., Roberts D.D. Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 2007, 109:1945-1952.
36. 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.
37. Isenberg J.S., Frazier W.A., Krishna M.C., Wink D.A., Roberts D.D. Enhancing cardiovascular dynamics by inhibition of thrombospondin-1/CD47 signaling. Curr. Drug Targets 2008, 9:833-841.
38. Isenberg J.S., Maxhimer J.B., Powers P., Tsokos M., Frazier W.A., Roberts D.D. Treatment of ischemia/reperfusion injury by limiting thrombospondin-1/CD47 signaling. Surgery 2008, 144:752-761.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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, 9:182-194.
44. 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.
45. Isenberg J.S., Shiva S., Gladwin M. Thrombospondin-1-CD47 blockade and exogenous nitrite enhance ischemic tissue survival, blood flow and angiogenesis via coupled NO-cGMP pathway activation. Nitric Oxide 2009, 21:52-62.
46. Kaiser R.H., Frantz C., Bals R., Böhm M., Wilkens H. Thrombospondin-1 as a biomarker in pulmonary hypertension. Chest 2010, 138:893A.
47. Kaur S., Roberts D.D. CD47 applies the brakes to angiogenesis via vascular endothelial growth factor receptor-2. Cell Cycle 2011, 10:10-12.
48. Kaur S., Martin-Manso G., Pendrak M.L., Garfield S.H., Isenberg J.S., Roberts D.D. Thrombospondin-1 inhibits vascular endothelial growth factor receptor-2 signaling by disrupting its association with CD47. J. Biol. Chem. 2010, 285:38923-38932.
49. Kaur S., Kuznetsova S.A., Pendrak M.L., Sipes J.M., Romeo M.J., Li Z., Zhang L., Roberts D.D. Identification of CD47 and amyloid precursor-like protein-2 as the major heparan sulfate proteoglycans on T lymphocytes and this isoform of CD47 as the signaling receptor for thrombospondin-1. J. Biol. Chem. 2011, 286:14991-15002.
50. Kung C.F., Moreau P., Takase H., Luscher T.F. L-NAME hypertension alters endothelial and smooth muscle function in rat aorta. Prevention by trandolapril and verapamil. Hypertension 1995, 26:744-751.
51. 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.
52. Lamy L., Ticchioni M., Rouquette-Jazdanian A.K., Samson M., Deckert M., Greenberg A.H., Bernard A. CD47 and the 19 kDa interacting protein-3 (BNIP3) in T cell apoptosis. J. Biol. Chem. 2003, 278:23915-23921.
53. Lamy L., Foussat A., Brown E.J., Bornstein P., Ticchioni M., Bernard A. Interactions between CD47 and thrombospondin reduce inflammation. J. Immunol. 2007, 178:5930-5939.
54. Li Z., Zhang G., Feil R., Han J., Du X. Sequential activation of p38 and ERK pathways by cGMP-dependent protein kinase leading to activation of the platelet integrin alphaIIb beta3. Blood 2006, 107:965-972.
55. Li S.S., Liu Z., Uzunel M., Sundqvist K.G. Endogenous thrombospondin-1 is a cell surface ligand for regulation of integrin dependent T lymphocyte adhesion. Blood 2006, 108:3112-3120.
56. 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.
57. 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.
58. 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.
59. Manna P.P., Dimitry J., Oldenborg P.A., Frazier W.A. CD47 augments Fas/CD95-mediated apoptosis. J. Biol. Chem. 2005, 280:29637-29644.
60. 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.
61. 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.
62. 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.
63. Miller T.W., Isenberg J.S., Shih H.B., Wang Y., Roberts D.D. Amyloid-beta Inhibits No-cGMP Signaling in a CD36- and CD47-Dependent Manner. PLoS One 2010, 5:e15686.
64. Mosher, D.F., Adams, J.C., in press. Adhesion-modulating/matricellular ECM protein families: a structural, functional and evolutionary appraisal. Matrix Biol.
65. Murphy-Ullrich, J.E., Iozzo, R.V., in press. Thematic Mini-Review Series: Thrombospondins in physiology and disease, new tricks for an old dog. Matrix Biol.
66. Myers S.A., DeVries W.H., Andres K.R., Gruenthal M.J., Benton R.L., Hoying J.B., Hagg T., Whittemore S.R. CD47 knockout mice exhibit improved recovery from spinal cord injury. Neurobiol. Dis. 2011, 42:21-34.
67. Nisoli E., Carruba M.O. Nitric oxide and mitochondrial biogenesis. J. Cell Sci. 2006, 119:2855-2862.
68. Nossaman V.E., Nossaman B.D., Kadowitz P.J. Nitrates and nitrites in the treatment of ischemic cardiac disease. Cardiol. Rev. 2010, 18:190-197.
69. Ochoa C.D., Yu L., Al-Ansari E., Hales C.A., Quinn D.A. Thrombospondin-1 null mice are resistant to hypoxia-induced pulmonary hypertension. J. Cardiothorac. Surg. 2010, 5:32.
70. Ochoa C.D., Fouty B.W., Hales C.A. Thrombospondin-1, endothelium and systemic vascular tone. Future Cardiol. 2011, 7:169-172.
71. 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.
72. Papapetropoulos A., Garcia-Cardena G., Madri J.A., Sessa W.C. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 1997, 100:3131-3139.
73. Radomski M.W., Palmer R.M., Moncada S. An L-arginine/nitric oxide pathway present in human platelets regulates aggregation. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:5193-5197.
74. 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, 50:7787-7799.
75. Rebres R.A., Vaz L.E., Green J.M., Brown E.J. Normal ligand binding and signaling by CD47 (integrin-associated protein) requires a long range disulfide bond between the extracellular and membrane spanning domains. J. Biol. Chem. 2001, 13:13.
76. Rico M.C., Rough J.J., Del Carpio-Cano F.E., Kunapuli S.P., DeLa Cadena R.A. The axis of thrombospondin-1, transforming growth factor beta and connective tissue growth factor: an emerging therapeutic target in rheumatoid arthritis. Curr. Vasc. Pharmacol. 2010, 8:338-343.
77. 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.
78. Risher, W.C., Eroglu, C., in press. Thrombospondins as key regulators of synaptogenesis in the central nervous system. Matrix Biol.
79. Roberts D.D., Lau L.F. Matricellular proteins. The extracellular matrix: an overview 2011, 369-413. Springer-Verlag, Berlin Heidelberg. R.P. Mecham (Ed.).
80. Roth J.J., Gahtan V., Brown J.L., Gerhard C., Swami V.K., Rothman V.L., Tulenko T.N., Tuszynski G.P. Thrombospondin-1 is elevated with both intimal hyperplasia and hypercholesterolemia. J. Surg. Res. 1998, 74:11-16.
81. Schade D., Kotthaus J., Clement B. Modulating the NO generating system from a medicinal chemistry perspective: current trends and therapeutic options in cardiovascular disease. Pharmacol. Ther. 2010, 126:279-300.
82. Schellings M.W., van Almen G.C., Sage E.H., Heymans S. Thrombospondins in the heart: potential functions in cardiac remodeling. J. Cell Commun. Signal. 2009, 3:201-213.
83. Schmidt H.H., Schmidt P.M., Stasch J.P. NO- and haem-independent soluble guanylate cyclase activators. Handb. Exp. Pharmacol. 2009, 191:309-339.
84. 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.
85. Stauss H.M., Godecke A., Mrowka R., Schrader J., Persson P.B. Enhanced blood pressure variability in eNOS knockout mice. Hypertension 1999, 33:1359-1363.
86. Stenina O.I., Plow E.F. Counterbalancing forces: what is thrombospondin-1 doing in atherosclerotic lesions?. Circ. Res. 2008, 103:1053-1055.
87. Stone J.R., Marletta M.A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 1994, 33:5636-5640.
88. Sun J., Hopkins B.D., Tsujikawa K., Perruzzi C., Adini I., Swerlick R., Bornstein P., Lawler J., Benjamin L.E. Thrombospondin-1 modulates VEGF-A-mediated Akt signaling and capillary survival in the developing retina. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H1344-H1351.
89. Sweetwyne, M.T., Murphy-Ullrich, J.E., in press. Thrombospondin1 in tissue repair and fibrosis: TGF-β-dependent and independent mechanisms. Matrix Biol.
90. Tan K., Lawler J. The interaction of Thrombospondins with extracellular matrix proteins. J. Cell Commun. Signal. 2009, 3:177-187.
91. Watanabe N., Image I., Takagi S., Image I., Tominaga A., Image Image I., Tomita T., Image I., Iwatsubo T., Image Image I. Functional analysis of the transmembrane domains of presenilin 1: participation of transmembrane domains 2 and 6 in the formation of initial substrate-binding site of gamma-secretase. J. Biol. Chem. 2010, 285:19738-19746.
92. 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. 2010, 63:13-22.
93. Zaccolo M. cAMP signal transduction in the heart: understanding spatial control for the development of novel therapeutic strategies. Br. J. Pharmacol. 2009, 158:50-60.
94. Zhang X., Kazerounian S., Duquette M., Perruzzi C., Nagy J.A., Dvorak H.F., Parangi S., Lawler J. Thrombospondin-1 modulates vascular endothelial growth factor activity at the receptor level. FASEB J. 2009, 23:3368-3376.