Endothelial nitric oxide synthase promotes neonatal cardiomyocyte proliferation by inhibiting tissue inhibitor of metalloproteinase-3 expression

Cardiovascular Research

Volumn 75, Issue 2, 2007, Pages 359-368

  Hammoud, Lamis ^a,b   Xiang, Fuli ^a,b   Lu, Xiangru ^b   Brunner, Friedrich ^c   Leco, Kevin ^a   Feng, Qingping ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF GRAZ   (Austria)

Author keywords

AP 1; Cardiomyocyte; Endothelial nitric oxide synthase; Nitric oxide; Tissue inhibitor of metalloproteinase 3

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; KI 67 ANTIGEN; TISSUE INHIBITOR OF METALLOPROTEINASE 3;

ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; HEART MUSCLE CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; TRANSGENIC MOUSE; WILD TYPE;

ADENOVIRIDAE; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, MONOCLONAL; CELL PROLIFERATION; CELLS, CULTURED; GENETIC VECTORS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCYTES, CARDIAC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITROSATION; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASE-3; TRANSCRIPTION FACTOR AP-1; TRANSDUCTION, GENETIC;

EID: 34250726643     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2007.05.006     Document Type: Article

References (34)

1. Balligand J.L., and Cannon P.J. Nitric oxide synthases and cardiac muscle. Autocrine and paracrine influences. Arterioscler Thromb Vasc Biol 17 (1997) 1846-1858
2. Bloch W., Fleischmann B.K., Lorke D.E., Andressen C., Hops B., Hescheler J., et al. Nitric oxide synthase expression and role during cardiomyogenesis. Cardiovasc Res 43 (1999) 675-684
3. Duda D.G., Fukumura D., and Jain R.K. Role of eNOS in neovascularization: NO for endothelial progenitor cells. Trends Mol Med 10 (2004) 143-145
4. Razavi H.M., Hamilton J.A., and Feng Q. Modulation of apoptosis by nitric oxide: implications in myocardial ischemia and heart failure. Pharmacol Ther 106 (2005) 147-162
5. Zhao X., Lu X., and Feng Q. Deficiency in endothelial nitric oxide synthase impairs myocardial angiogenesis. Am J Physiol Heart Circ Physiol 283 (2002) H2371-H2378
6. Feng Q., Song W., Lu X., Hamilton J.A., Lei M., Peng T., et al. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase. Circulation 106 (2002) 873-879
7. Lepic E., Burger D., Lu X., Song W., and Feng Q. Lack of endothelial nitric oxide synthase decreases cardiomyocyte proliferation and delays cardiac maturation. Am J Physiol Cell Physiol 291 (2006) C1240-C1246
8. Cluzeaut F., and Maurer-Schultze B. Proliferation of cardiomyocytes and interstitial cells in the cardiac muscle of the mouse during pre- and postnatal development. Cell Tissue Kinet 19 (1986) 267-274
9. Soonpaa M.H., Kim K.K., Pajak L., Franklin M., and Field L.J. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol 271 (1996) H2183-H2189
10. Li F., Wang X., Capasso J.M., and Gerdes A.M. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol 28 (1996) 1737-1746
11. Baker A.H., Edwards D.R., and Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 115 (2002) 3719-3727
12. Kim H., Pennie W.D., Sun Y., and Colburn N.H. Differential functional significance of AP-1 binding sites in the promoter of the gene encoding mouse tissue inhibitor of metalloproteinases-3. Biochem J 324 Pt 2 (1997) 547-553
13. Fedak P.W., Verma S., Weisel R.D., and Li R.K. Cardiac remodeling and failure from molecules to man (Part II). Cardiovasc Pathol 14 (2005) 49-60
14. Satoh M., Nakamura M., Saitoh H., Satoh H., Maesawa C., Segawa I., et al. Tumor necrosis factor-alpha-converting enzyme and tumor necrosis factor-alpha in human dilated cardiomyopathy. Circulation 99 (1999) 3260-3265
15. Fedak P.W., Smookler D.S., Kassiri Z., Ohno N., Leco K.J., Verma S., et al. TIMP-3 deficiency leads to dilated cardiomyopathy. Circulation 110 (2004) 2401-2409
16. Baker A.H., Zaltsman A.B., George S.J., and Newby A.C. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. TIMP-3 promotes apoptosis. J Clin Invest 101 (1998) 1478-1487
17. Hess D.T., Matsumoto A., Kim S.O., Marshall H.E., and Stamler J.S. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6 (2005) 150-166
18. Marshall H.E., Merchant K., and Stamler J.S. Nitrosation and oxidation in the regulation of gene expression. FASEB J 14 (2000) 1889-1900
19. Brunner F., Andrew P., Wolkart G., Zechner R., and Mayer B. Myocardial contractile function and heart rate in mice with myocyte-specific overexpression of endothelial nitric oxide synthase. Circulation 104 (2001) 3097-3102
20. Leco K.J., Waterhouse P., Sanchez O.H., Gowing K.L., Poole A.R., Wakeham A., et al. Spontaneous air space enlargement in the lungs of mice lacking tissue inhibitor of metalloproteinases-3 (TIMP-3). J Clin Invest 108 (2001) 817-829
21. Song W., Lu X., and Feng Q. Tumor necrosis factor-alpha induces apoptosis via inducible nitric oxide synthase in neonatal mouse cardiomyocytes. Cardiovasc Res 45 (2000) 595-602
22. Burger D., Lei M., Geoghegan-Morphet N., Lu X., Xenocostas A., and Feng Q. Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase. Cardiovasc Res 72 (2006) 51-59
23. Peng T., Lu X., and Feng Q. Pivotal role of gp91phox-containing NADH oxidase in lipopolysaccharide-induced tumor necrosis factor-alpha expression and myocardial depression. Circulation 111 (2005) 1637-1644
24. Peng T., Lu X., Lei M., and Feng Q. Endothelial nitric-oxide synthase enhances lipopolysaccharide-stimulated tumor necrosis factor-alpha expression via cAMP-mediated p38 MAPK pathway in cardiomyocytes. J Biol Chem 278 (2003) 8099-8105
25. Kwon Y.H., Jovanovic A., Serfas M.S., and Tyner A.L. The Cdk inhibitor p21 is required for necrosis, but it inhibits apoptosis following toxin-induced liver injury. J Biol Chem 278 (2003) 30348-30355
26. Zhang X., Wang H.M., Lin H.Y., Liu G.Y., Li Q.L., and Zhu C. Regulation of matrix metalloproteinases (MMPS) and their inhibitors (TIMPS) during mouse peri-implantation: role of nitric oxide. Placenta 25 (2004) 243-252
27. Orucevic A., Bechberger J., Green A.M., Shapiro R.A., Billiar T.R., and Lala P.K. Nitric-oxide production by murine mammary adenocarcinoma cells promotes tumor-cell invasiveness. Int J Cancer 81 (1999) 889-896
28. Schroeder R.A., Cai C., and Kuo P.C. Endotoxin-mediated nitric oxide synthesis inhibits IL-1beta gene transcription in ANA-1 murine macrophages. Am J Physiol Cell Physiol 277 (1999) C523-C530
29. Qi J.H., Ebrahem Q., Moore N., Murphy G., Claesson-Welsh L., Bond M., et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 9 (2003) 407-415
30. Yang T.T., and Hawkes S.P. Role of the 21-kDa protein TIMP-3 in oncogenic transformation of cultured chicken embryo fibroblasts. Proc Natl Acad Sci U S A 89 (1992) 10676-10680
31. Gill S.E., Pape M.C., and Leco K.J. Tissue inhibitor of metalloproteinases 3 regulates extracellular matrix-cell signaling during bronchiole branching morphogenesis. Dev Biol 298 (2006) 540-554
32. Kang M.J., Kim J.S., Chae S.W., Koh K.N., and Koh G.Y. Cyclins and cyclin dependent kinases during cardiac development. Mol Cells 7 (1997) 360-366
33. Yoshizumi M., Lee W.S., Hsieh C.M., Tsai J.C., Li J., Perrella M.A., et al. Disappearance of cyclin A correlates with permanent withdrawal of cardiomyocytes from the cell cycle in human and rat hearts. J Clin Invest 95 (1995) 2275-2280
34. Bond M., Murphy G., Bennett M.R., Newby A.C., and Baker A.H. Tissue inhibitor of metalloproteinase-3 induces a fas-associated death domain-dependent type II apoptotic pathway. J Biol Chem 277 (2002) 13787-13795