Inhibition of endothelial nitric oxide synthase induces and enhances myocardial fibrosis

Cardiovascular Research

Volumn 100, Issue 2, 2013, Pages 211-221

  Kazakov, Andrey ^a   Hall, Rabea ^b   Jagoda, Philippe ^a   Bachelier, Katrin ^a   Müller Best, Patrick ^a   Semenov, Alexander ^a   Lammert, Frank ^b   Böhm, Michael ^a   Laufs, Ulrich ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b Klinik fur Innere Medizin III   (Germany)

Author keywords

Cardiac fibrosis; eNOS inhibition; Fibrocytes; SDF 1

Indexed keywords

7 NITROINDAZOLE; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; COLLAGEN TYPE 1; COLLAGEN TYPE 1ALPHA 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GREEN FLUORESCENT PROTEIN; HYDRALAZINE; MESSENGER RNA; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; N(G) NITROARGININE METHYL ESTER; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; BONE MARROW TRANSPLANTATION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; FIBROBLAST; FIBROSING ALVEOLITIS; HEART CELL CULTURE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION;

CARDIAC FIBROSIS; ENOS INHIBITION; FIBROCYTES; SDF-1;

ANIMALS; ANIMALS, NEWBORN; BLOOD PRESSURE; CELLS, CULTURED; CHEMOKINE CXCL12; FIBROSIS; MALE; MICE; MICE, INBRED C57BL; MYOCARDIUM; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; VENTRICULAR FUNCTION, LEFT;

EID: 84886056529     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt181     Document Type: Article

References (28)

1. Förstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 2012;33:829-837.
2. Umar S, van der Laarse A. Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart. Mol Cell Biochem 2010;333:191-201.
3. Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B et al. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 2005;115:1221-1231.
4. Moens AL, Takimoto E, Tocchetti CG, Chakir K, Bedja D, Cormaci G et al. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation 2008;117: 2626-2636.
5. Ichinose F, Bloch KD, Wu JC, Hataishi R, Aretz HT, Picard MH et al. Pressure overload-induced LV hypertrophy and dysfunction in mice are exacerbated by congenital NOS3 deficiency. Am J Physiol Heart Circ Physiol 2004;286:H1070-H1075.
6. Ruetten H, Dimmeler S, Gehring D, Ihling C, Zeiher AM. Concentric left ventricular remodeling in endothelial nitric oxide synthase knockout mice by chronic pressure overload. Cardiovasc Res 2005;66:444-453.
7. Buys ES, Raher MJ, Blake SL, Neilan TG, Graveline AR, Passeri JJ et al. Cardiomyocyterestricted restoration of nitric oxide synthase 3 attenuates left ventricular remodeling after chronic pressure overload. Am J Physiol Heart Circ Physiol 2007;293:H620-H627.
8. Kazakov A, Müller P, Jagoda P, Semenov A, Böhm M, Laufs U. Endothelial nitric oxide synthase of the bone marrow regulates myocardial hypertrophy, fibrosis, and angiogenesis. Cardiovasc Res 2012;93:397-405.
9. Kim NN, Villegas S, Summerour SR, Villarreal FJ. Regulation of cardiac fibroblast extracellular matrix production by bradykinin and nitric oxide. J Mol Cell Cardiol 1999;31: 457-466.
10. Liou JY, Hong HJ, Sung LC, Chao HH, Chen PY, Cheng TH et al. Nicorandil inhibits angiotensin-II-induced proliferation of cultured rat cardiac fibroblasts. Pharmacology 2011;87:144-151.
11. Wang K, Hu X, Du C, Tu S, Zhang F, Xie X. Angiotensin-(1-7) suppresses the number and function of the circulating fibrocytes by upregulating endothelial nitric oxide synthase expression. Mol Cell Biochem 2012;365:19-27.
12. Krenning G, Zeisberg EM, Kalluri R. The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol 2010;225:631-637.
13. Haudek SB, Xia Y, Huebener P, Lee JM, Carlson S, Crawford JR et al. Bone marrowderived fibroblast precursors mediate ischemic cardiomyopathy in mice. Proc Natl Acad Sci USA 2006;103:18284-18289.
14. Zeisberg EM, Tarnavski O, Zeisberg M, Dorfman AL, McMullen JR, Gustafsson E et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 2007; 13:952-961.
15. Chu PY, Mariani J, Finch S, McMullen JR, Sadoshima J, Marshall T et al. Bone marrowderived cells contribute to fibrosis in the chronically failing heart. Am J Pathol 2010; 176:1735-1742.
16. Sopel MJ, Rosin NL, Lee TDG, Legare JF. Myocardial fibrosis in response to angiotensin II is preceded by the recruitment of mesenchymal progenitor cells. Lab Invest 2011;91: 565-578.
17. Phillips RJ, Burdick MD, Hong K, Lutz MA, Murray LA, Xue YY et al. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest 2004;114: 438-446.
18. Wang CH, Huang CD, Lin HC, Lee KY, Lin SM, Liu CY et al. Increased circulating fibrocytes in asthma with chronic airflow obstruction. Am J Respir Crit Care Med 2008;178: 583-591.
19. Moeller A, Gilpin SE, Ask K, Cox G, Cook D, Gauldie J et al. Circulating fibrocytes are an indicator of poor prognosis in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2009;179:588-594.
20. Mehrad B, Burdick MD, Strieter RM. Fibrocyte CXCR4 regulation as a therapeutic target in pulmonary fibrosis. Int J Biochem Cell Biol 2009;41:1708-1718.
21. Chu PY, Zatta A, Kiriazis H, Chin-Dusting J, Du XJ, Marshall T et al. CXCR4 Antagonism attenuates the cardiorenal consequences of mineralocorticoid excess. Circ Heart Fail 2011;4:651-658.
22. Southan GJ, Szabó C. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem Pharm 1996;51:383-394.
23. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ et al. 1400WIs a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 1997;272:4959-4963.
24. Proulx C, El-Helou V, Gosselin H, Clement R, Gillis MA, Villeneuve L et al. Antagonism of stromal cell-derived factor-1a reduces infarct size and improves ventricular function after myocardial infarction. Pflugers Arch-Eur J Physiol 2007;455: 241-250.
25. Zhang P, Xu X, Hu X, van Deel ED, Zhu G, Chen Y. Inducible nitric oxide synthase deficiency protects the heart from systolic overload-induced ventricular hypertrophy and congestive heart failure. Circ Res 2007;100:1089-1098.
26. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S et al. Cell. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 2006; 124:175-189.
27. Müller P, Kazakov A, Semenov A, Böhm M, Laufs U. Pressure-induced cardiac overload induces upregulation of endothelial and myocardial progenitor cells. Cardiovasc Res 2008; 77:151-159.
28. Meirelles Pereira LM, Mandarim-de-Lacerda CA. Effect of antihypertensive drugs on the myocardial microvessels in rats with nitric oxide blockade. Pathol Res Pract 2000;196: 305-311.