Thrombospondin-1 inhibition of vascular smooth muscle cell responses occurs via modulation of both cAMP and cGMP

Pharmacological Research

Volumn 63, Issue 1, 2011, Pages 13-22

  Yao, Mingyi ^a   Roberts, David D ^c   Isenberg, Jeff S ^a,b  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

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

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

cAMP; cGMP; Thrombospondin 1; Vascular smooth muscle cells

Indexed keywords

ADENYLATE CYCLASE; CD47 ANTIGEN; CYCLIC AMP; CYCLIC GMP; FORSKOLIN; ISOPRENALINE; MYOSIN LIGHT CHAIN 2; NITRIC OXIDE; PHOSPHODIESTERASE III; THROMBOSPONDIN 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL LEVEL; CELL STIMULATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; MALE; MOUSE; MUSCLE LEVEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASODILATATION; WILD TYPE;

ACTINS; ANIMALS; ANTIGENS, CD47; CELLS, CULTURED; CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 3; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; ENDOTHELIAL CELLS; GUANYLATE CYCLASE; HUMANS; HYDROLYSIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SKELETAL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NITRIC OXIDE; PHOSPHODIESTERASE INHIBITORS; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; THROMBOSPONDIN 1; VASODILATION; VASODILATOR AGENTS;

EID: 79151470115     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2010.10.014     Document Type: Article

References (56)

1. L.J. Ignarro Nitric oxide as a unique signaling molecule in the vascular system: a historical overview J Physiol Pharmacol 53 2002 503 514
2. J.S. Isenberg, D.A. Wink, and D.D. Roberts Thrombospondin-1 antagonizes nitric oxide-stimulated vascular smooth muscle cell responses Cardiovasc Res 71 2006 785 793
3. J.S. Isenberg, F. Hyodo, K. Matsumoto, M.J. Romeo, M. Abu-Asab, and M. Tsokos Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation Blood 109 2007 1945 1952
4. J.S. Isenberg, F. Hyodo, L.K. Pappan, M. Abu-Asab, M. Tsokos, and M.C. Krishna Blocking thrombospondin-1/CD47 signaling alleviates deleterious effects of aging on tissue responses to ischemia Arterioscler Thromb Vasc Biol 27 2007 2582 2588
5. J.S. Isenberg, M.J. Romeo, J.B. Maxhimer, J. Smedley, W.A. Frazier, and D.D. Roberts Gene silencing of CD47 and antibody ligation of thrombospondin-1 enhance ischemic tissue survival in a porcine model: implications for human disease Ann Surg 247 2008 860 868
6. J.S. Isenberg, Y. Qin, J.B. Maxhimer, J.M. Sipes, D. Despres, and J. Schnermann Thrombospondin-1 and CD47 regulate blood pressure and cardiac responses to vasoactive stress Matrix Biol 28 2009 110 119
7. Bauer EM, Qin Y, Miller TW, Bandle RW, Csanyi G, Pagano PJ, et al. Thrombospondin-1 supports blood pressure by limiting enos activation and endothelial-dependent vasorelaxation. Cardiovasc Res 2010 Aug 4. [Epub ahead of print].
8. L.J. Ignarro Nitric oxide. A novel signal transduction mechanism for transcellular communication Hypertension 16 1990 477 483
9. J.S. Isenberg, L.A. Ridnour, J. Dimitry, W.A. Frazier, D.A. Wink, and D.D. Roberts CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1 J Biol Chem 281 2006 26069 26080
10. J.S. Isenberg, M.J. Romeo, C. Yu, C.K. Yu, K. Nghiem, and J. Monsale Thrombospondin-1 stimulates platelet aggregation by blocking the antithrombotic activity of nitric oxide/cGMP signaling Blood 111 2008 613 623
11. Kaur S, Martin-Manso G, Pendrak ML, Garfield SH, Isenberg JS, Roberts DD. Thrombospondin-1 inhibits vascular endothelial growth factor receptor-2 signaling by disrupting its association with CD47. J Biol Chem 2010 Oct 5. [Epub ahead of print].
12. J.S. Isenberg, L.A. Ridnour, E.M. Perruccio, M.G. Espey, D.A. Wink, and D.D. Roberts Thrombospondin-1 inhibits endothelial cell responses to nitric oxide in a cGMP-dependent manner Proc Natl Acad Sci USA 102 2005 13141 13146
13. i-dependent inhibition of protein kinase A J Immunol 170 2003 3544 3553
14. G.M. Rath, C. Schneider, S. Dedieu, H. Sartelet, H. Morjani, and L. Martiny Thrombospondin-1 C-terminal-derived peptide protects thyroid cells from ceramide-induced apoptosis through the adenylyl cyclase pathway Int J Biochem Cell Biol 38 2006 2219 2228
15. i-mediated inhibition of adenylate cyclase and extracellular-regulated kinases J Cell Biol 147 1999 389 400
16. i J Biol Chem 274 1999 8554 8560
17. J.E. Brittain, J. Han, K.I. Ataga, E.P. Orringer, and L.V. Parise Mechanism of CD47-induced alpha4beta1 integrin activation and adhesion in sickle reticulocytes J Biol Chem 279 2004 42393 42402
18. Y.J. Rao, and L. Xi Pivotal effects of phosphodiesterase inhibitors on myocyte contractility and viability in normal and ischemic hearts Acta Pharmacol Sin 30 2009 1 24
19. T. Matsumoto, T. Kobayashi, and K. Kamata Phosphodiesterases in the vascular system J Smooth Muscle Res 39 2003 67 86
20. D.D. Roberts, J. Cashel, and N. Guo Purification of thrombospondin from human platelets J Tissue Cult Methods 16 1994 217 222
21. K. Nakamura, Y. Koga, H. Sakai, K. Homma, and M. Ikebe cGMP-dependent relaxation of smooth muscle is coupled with the change in the phosphorylation of myosin phosphatase Circ Res 101 2007 712 722
22. S. Pelletier, C. Julien, M.R. Popoff, N. Lamarche-Vane, and S. Meloche Cyclic AMP induces morphological changes of vascular smooth muscle cells by inhibiting a Rac-dependent signaling pathway J Cell Physiol 204 2005 412 422
23. L.L. Wu, C. Tang, and M.S. Liu Altered phosphorylation and calcium sensitivity of cardiac myofibrillar proteins during sepsis Am J Physiol Regul Integr Comp Physiol 281 2001 R408 416
24. G. Pfitzer Signal transduction in smooth muscle: invited review: regulation of myosin phosphorylation in smooth muscle J Appl Physiol 91 2001 497 503
25. T.P. Woodsome, A. Polzin, K. Kitazawa, M. Eto, and T. Kitazawa Agonist- and depolarization-induced signals for myosin light chain phosphorylation and force generation of cultured vascular smooth muscle cells J Cell Sci 119 2006 1769 1780
26. 2+/calmodulin of an exogenous myosin light chain kinase (MLCK) in mouse arteries J Physiol 2009
27. G. Rabbani, V. Vijay, M.R. Sarabu, and S.A. Gupte Regulation of human internal mammary and radial artery contraction by extracellular and intracellular calcium channels and cyclic adenosine 3′, 5′ monophosphate Ann Thorac Surg 83 2007 510 515
28. J.M. Enserink, L.S. Price, T. Methi, M. Mahic, A. Sonnenberg, and J.L. Bos The cAMP-Epac-Rap1 pathway regulates cell spreading and cell adhesion to laminin-5 through the alpha3beta1 integrin but not the alpha6beta4 integrin J Biol Chem 279 2004 44889 44896
29. T. Aizawa, H. Wei, J.M. Miano, J. Abe, B.C. Berk, and C. Yan Role of phosphodiesterase 3 in NO/cGMP-mediated antiinflammatory effects in vascular smooth muscle cells Circ Res 93 2003 406 413
30. E. Delpy, H. Coste, and A.C. Gouville Effects of cyclic GMP elevation on isoprenaline-induced increase in cyclic AMP and relaxation in rat aortic smooth muscle: role of phosphodiesterase 3 Br J Pharmacol 119 1996 471 478
31. S.D. Rybalkin, C. Yan, K.E. Bornfeldt, and J.A. Beavo Cyclic GMP phosphodiesterases and regulation of smooth muscle function Circ Res 93 2003 280 291
32. X. Pan, E. Arauz, J.J. Krzanowski, D.F. Fitzpatrick, and J.B. Polson Synergistic interactions between selective pharmacological inhibitors of phosphodiesterase isozyme families PDE iii and PDE iv to attenuate proliferation of rat vascular smooth muscle cells Biochem Pharmacol 48 1994 827 835
33. D.H. Maurice Cyclic nucleotide phosphodiesterase-mediated integration of cGMP and cAMP signaling in cells of the cardiovascular system Front Biosci 10 2005 1221 1228
34. C. Boulanger, V.B. Schini, H. Hendrickson, and P.M. Vanhoutte Chronic exposure of cultured endothelial cells to eicosapentaenoic acid potentiates the release of endothelium-derived relaxing factor(s) Br J Pharmacol 99 1990 176 180
35. J.S. Isenberg, J.B. Maxhimer, P. Powers, M. Tsokos, W.A. Frazier, and D.D. Roberts Treatment of liver ischemia-reperfusion injury by limiting thrombospondin-1/CD47 signaling Surgery 144 2008 752 761
36. I.K. Lillestll, K.B. Helle, and S. Aardal Relaxing effects of cyclic GMP and cyclic AMP-enhancing agents on the long-lasting contraction to endothelin-1 in the porcine coronary artery Scand J Clin Lab Invest 58 1998 625 634
37. V.J. Watts, and K.A. Neve Sensitization of adenylate cyclase by Galpha i/o-coupled receptors Pharmacol Ther 106 2005 405 421
38. M. Zaccolo, and M.A. Movsesian cAMP and cGMP signaling cross-talk: role of phosphodiesterases and implications for cardiac pathophysiology Circ Res 100 2007 1569 1578
39. D.H. Maurice, D. Palmer, D.G. Tilley, H.A. Dunkerley, S.J. Netherton, and D.R. Raymond Cyclic nucleotide phosphodiesterase activity, expression, and targeting in cells of the cardiovascular system Mol Pharmacol 64 2003 533 546
40. D.H. Maurice Dynamic regulation of cAMP signaling by cGMP in the cardiovascular system: roles of phosphodiesterase 2 and phosphodiesterase 3 enzymes Proc West Pharmacol Soc 46 2003 32 36
41. G.S. Baillie, and M.D. Houslay Arrestin times for compartmentalised cAMP signalling and phosphodiesterase-4 enzymes Curr Opin Cell Biol 17 2005 129 134
42. B. Jimenez, O.V. Volpert, S.E. Crawford, M. Febbraio, R.L. Silverstein, and N. Bouck Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1 Nat Med 6 2000 41 48
43. J.S. Isenberg, Y. Jia, J. Fukuyama, C.H. Switzer, D.A. Wink, and D.D. Roberts Thrombospondin-1 inhibits nitric oxide signaling via CD36 by inhibiting myristic acid uptake J Biol Chem 282 2007 15404 15415
44. I. McPhee, S.J. Yarwood, G. Scotland, E. Huston, M.B. Beard, and A.H. Ross Association with the SRC family tyrosyl kinase LYN triggers a conformational change in the catalytic region of human cAMP-specific phosphodiesterase HSPDE4A4B. Consequences for rolipram inhibition J Biol Chem 274 1999 11796 11810
45. M.A. Movsesian cAMP-mediated signal transduction and sarcoplasmic reticulum function in heart failure Ann N Y Acad Sci 853 1998 231 239
46. A. Carlucci, L. Lignitto, and A. Feliciello Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome Trends Cell Biol 18 2008 604 613
47. J.S. Lymn, M.K. Patel, G.F. Clunn, S.J. Rao, K.L. Gallagher, and A.D. Hughes Thrombospondin-1 differentially induces chemotaxis and DNA synthesis of human venous smooth muscle cells at the receptor-binding level J Cell Sci 115 2002 4353 4360
48. J.S. Isenberg, M.J. Calzada, L. Zhou, N. Guo, J. Lawler, and X.Q. Wang Endogenous thrombospondin-1 is not necessary for proliferation but is permissive for vascular smooth muscle cell responses to platelet-derived growth factor Matrix Biol 24 2005 110 123
49. S.M. Nesselroth, A.I. Willis, S. Fuse, E.T. Olson, J. Lawler, and B.E. Sumpio The C-terminal domain of thrombospondin-1 induces vascular smooth muscle cell chemotaxis J Vasc Surg 33 2001 595 600
50. T. Lee, S.M. Nesselroth, E.T. Olson, N. Esemuede, J. Lawler, and B.E. Sumpio Thrombospondin-1-induced vascular smooth muscle cell chemotaxis: the role of the type 3 repeat and carboxyl terminal domains J Cell Biochem 89 2003 500 506
51. W.T. Gerthoffer, M.A. Trevethick, and R.A. Murphy Myosin phosphorylation and cyclic adenosine 3′,5′-monophosphate in relaxation of arterial smooth muscle by vasodilators Circ Res 54 1984 83 89
52. I. Martin-Padura, F. de Nigris, E. Migliaccio, G. Mansueto, S. Minardi, and M. Rienzo p66Shc deletion confers vascular protection in advanced atherosclerosis in hypercholesterolemic apolipoprotein E knockout mice Endothelium 15 2008 276 287
53. R. Riessen, M. Kearney, J. Lawler, and J.M. Isner Immunolocalization of thrombospondin-1 in human atherosclerotic and restenotic arteries Am Heart J 135 1998 357 364
54. J.J. Roth, V. Gahtan, J.L. Brown, C. Gerhard, V.K. Swami, and V.L. Rothman Thrombospondin-1 is elevated with both intimal hyperplasia and hypercholesterolemia J Surg Res 74 1998 11 16
55. A.E. Canfield, C. Farrington, M.D. Dziobon, R.P. Boot-Handford, A.M. Heagerty, and S.N. Kumar The involvement of matrix glycoproteins in vascular calcification and fibrosis: an immunohistochemical study J Pathol 196 2002 228 234
56. C.S. Lin, X. Liu, R. Tu, S. Chow, and T.F. Lue Age-related decrease of protein kinase G activation in vascular smooth muscle cells Biochem Biophys Res Commun 287 2001 244 248