Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase

Circulation

Volumn 110, Issue 14, 2004, Pages 1933-1939

  Landmesser, Ulf ^a   Engberding, Niels ^a   Bahlmann, Ferdinand H ^a   Schaefer, Arnd ^a   Wiencke, Antje ^a   Heineke, Andre ^a   Spiekermann, Stephan ^a   Hilfiker Kleiner, Denise ^a   Templin, Christian ^a   Kotlarz, Daniel ^a   Mueller, Maja ^a   Fuchs, Martin ^a   Hornig, Burkhard ^a   Haller, Hermann ^a   Drexler, Helmut ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Endothelium; Heart failure; Myocardial infarction; Nitric oxide synthase; Statins

Indexed keywords

ATORVASTATIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME ACTIVITY; FIBROSING ALVEOLITIS; HEART FIBRILLATION; HEART INFARCTION; HEART LEFT VENTRICLE FAILURE; HEART VENTRICLE FUNCTION; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; RANDOMIZATION; STEM CELL MOBILIZATION; SURVIVAL RATE; VASODILATATION;

ANIMALS; BIOLOGICAL AVAILABILITY; CAPILLARIES; CELLS, CULTURED; COLLATERAL CIRCULATION; DRUG RESISTANCE; ENDOTHELIAL CELLS; FIBROSIS; HEART FAILURE, CONGESTIVE; HEPTANOIC ACIDS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCARDIUM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PYRROLES; RANDOM ALLOCATION; VASODILATION; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 20844431696     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000143232.67642.7A     Document Type: Article

References (56)

1. Bauersachs J, Galuppo P, Fraccarollo D, et al. Improvement of left ventricular remodeling and function by hydroxymethylglutaryl coenzyme A reductase inhibition with cerivastatin in rats with heart failure after myocardial infarction. Circulation. 2001;104:982-985.
2. Hayashidani S, Tsutsui H, Shiomi T, et al. Fluvastatin, a 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitor, attenuates left ventricular remodeling and failure after experimental myocardial infarction. Circulation. 2002;105:868-873.
3. Krum H, McMurray JJ. Statins and chronic heart failure: do we need a large-scale outcome trial? J Am Coll Cardiol. 2002;39:1567-1573.
4. Node K, Fujita M, Kitakaze M, et al. Short-term statin therapy improves cardiac function and symptoms in patients with idiopathic dilated cardiomyopathy. Circulation. 2003;108:839-843.
5. Horwich TB, MacLellan WR, Fonarow GC. Statin therapy is associated with improved survival in ischemic and non-ischemic heart failure. J Am Coll Cardiol. 2004;43:642-648.
6. Laufs U, La Fata V, Plutzky J, et al. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation. 1998;97:1129-1135.
7. : Kureishi Y, Luo Z, Shiojima I, et al. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med. 2000;6:1004-1010.
8. Feron O, Dessy C, Desager JP, et al. Hydroxy-methylglutaryl-coenzyme A reductase inhibition promotes endothelial nitric oxide synthase activation through a decrease in caveolin abundance. Circulation. 2001;103:113-118.
9. Kalinowski L, Dobrucki LW, Brovkovych V, et al. Increased nitric oxide bioavailability in endothelial cells contributes to the pleiotropic effect of cerivastatin. Circulation. 2002;105:933-938.
10. Wassmann S, Laufs U, Baumer AT, et al. Inhibition of geranylgeranylation reduces angiotensin II-mediated free radical production in vascular smooth muscle cells: involvement of angiotensin AT1 receptor expression and Rac1 GTPase. Mol Pharmacol. 2001;59:646-54.
11. Qi XL, Stewart DJ, Gosselin H, et al. Improvement of endocardial and vascular endothelial function on myocardial performance by captopril treatment in postinfarct rat hearts. Circulation. 1999;100:1338-1345.
12. Bauersachs J, Bouloumie A, Fraccarollo D, et al. Endothelial dysfunction in chronic myocardial infarction despite increased vascular endothelial nitric oxide synthase and soluble guanylate cyclase expression: role of enhanced vascular Superoxide production. Circulation. 1999;100:292-298.
13. Wiemer G, Iiter G, Malinski T, et al. Decreased nitric oxide availability in normotensive and hypertensive rats with failing hearts after myocardial infarction. Hypertension. 2001;38:1367-1371.
14. Treasure CB, Vita JA, Cox DA, et al. Endothelium-dependent dilation of the coronary microvasculature is impaired in dilated cardiomyopathy. Circulation. 1990;81:772-779.
15. Hornig B, Maier V, Drexler H. Physical training improves endothelial function in patients with chronic heart failure. Circulation. 1996;93:210-214.
16. Mohri M, Egashira K, Tagawa T, et al. Basal release of nitric oxide is decreased in the coronary circulation in patients with heart failure. Hypertension. 1997;30:50-56.
17. Drexler H. Endothelium as a therapeutic target in heart failure. Circulation. 1998;98:2652-2655.
18. Matsunaga T, Weihrauch DW, Moniz MC, et al. Angiostatin inhibits coronary angiogenesis during impaired production of nitric oxide. Circulation. 2002;105:2185-2191.
19. Aicher A, Heeschen C, Mildner-Rihm C, et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9:1370-1376.
20. Scherrer-Crosbie M, Ullrich R, Bloch KD, et al. Endothelial nitric oxide synthase limits left ventricular remodeling after myocardial infarction in mice. Circulation. 2001;104:1286-1291.
21. Jones SP, Greer JJ, van Haperen R, et al. Endothelial nitric oxide synthase overexpression attenuates congestive heart failure in mice. Proc Natl Acad Sci USA. 2003;100:4891-4896.
22. Shesely EG, Maeda N, Kim HS, et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci U S A. 1996;93:13176-13181.
23. Fuchs M, Hilfiker A, Kaminski K, et al. Role of interleukin-6 for left ventricular remodeling and survival after experimental myocardial infarction. FASEB J. 2003;17:2118-2120.
24. Black AE, Sinz MW, Hayes RN, et al. Metabolism and excretion studies in mouse after single and multiple oral doses of the 3-hydroxy-3-methylglutaryl-CoA reductase inhibitor atorvastatin. Drug Metab Dispos. 1998;26:755-763.
25. Landmesser U, Dikalov S, Price SR, et al. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest. 2003;111:1201-1209.
26. Kojda G, Laursen JB, Ramasamy S, et al. Protein expression, vascular reactivity and soluble guanylate cyclase activity in mice lacking the endothelial cell nitric oxide synthase: contributions of NOS isoforms to blood pressure and heart rate control. Cardiovasc Res. 1999;42:206-213.
27. Huang PL, Huang Z, Mashimo H, et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature. 1995;377:239-242.
28. Schaefer A, Klein G, Brand B, et al. Evaluation of left ventricular diastolic function by pulsed Doppler tissue imaging in mice. J Am Soc Echocardiogr. 2003;16:1144-1149.
29. Wollert KC, Studer R, Doerfer K, et al. Differential effects of kinins on cardiomyocyte hypertrophy and interstitial collagen matrix in the surviving myocardium after myocardial infarction in the rat. Circulation. 1997;95:1910-1917.
30. Asahara T, Murohara T, Sullivan A, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967.
31. Bahlmann FH, De Groot K, Spandau JM, et al. Erythropoietin regulates endothelial progenitor cells. Blood. 2004;103:921-926.
32. Woessner JFJ. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys. 1961;93:440-447.
33. Ichinose F, Bloch KD, Wu JC, et al. Pressure overload-induced LV hypertrophy and dysfunction in mice are exacerbated by congenital NOS3 deficiency. Am J Physiol. 2004;286:H1070-H1075.
34. Kim NN, Villegas S, Summerour SR, et al. Regulation of cardiac fibroblast extracellular matrix production by bradykinin and nitric oxide. J Mol Cell Cardiol. 1999;31:457-466.
35. Asahara T, Masuda H, Takahashi T, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221-228.
36. Dimmeler S, Aicher A, Vasa M, et al. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI3-kinase/Akt pathway. J Clin Invest. 2001;108:391-397.
37. Llevadot J, Murasawa S, Kureishi Y, et al. HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J Clin Invest. 2001;108:399-405.
38. Neglia D, Parodi O, Gallopin M, et al. Myocardial blood flow response to pacing tachycardia and to dipyridamole infusion in patients with dilated cardiomyopathy without overt heart failure. Circulation. 1995;92:796-804.
39. Neglia D, Michelassi C, Trivieri MG, et al. Prognostic role of myocardial blood flow impairment in idiopathic left ventricular dysfunction. Circulation. 2002;105:186-193.
40. Xie YW, Shen W, Zhao G, et al. Role of endothelium-derived nitric oxide in the modulation of canine myocardial mitochondrial respiration in vitro: implications for the development of heart failure. Circ Res. 1996;79:381-387.
41. Trochu JN, Bouhour JB, Kaley G, et al. Role of endothelium-derived nitric oxide in the regulation of cardiac oxygen metabolism: implications in health and disease. Circ Res. 2000;87:1108-1117.
42. Kawamoto A, Gwon HC, Iwaguro H, et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation. 2001;103:634-637.
43. Kocher AA, Schuster MD, Szabolcs MJ, et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med. 2001;7:430-436.
44. Walter DH, Rittig K, Bahlmann FH, et al. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation. 2002;105:3017-3024.
45. Assmus B, Urbich C, Aicher A, et al. HMG-CoA reductase inhibitors reduce senescence and increase proliferation of endothelial progenitor cells via regulation of cell cycle regulatory genes. Circ Res. 2003;92:1049-1055.
46. Namba T, Koike H, Murakami K, et al. Angiogenesis induced by endothelial nitric oxide synthase gene through vascular endothelial growth factor expression in a rat hindlimb ischemia model. Circulation. 2003;108:2250-2257.
47. Fiedler B, Lohmann SM, Smolenski A, et al. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc Natl Acad Sci USA. 2002;99:11363-11368.
48. Wollen KC, Fiedler B, Gambaryan S, et al. Gene transfer of cGMP-dependent protein kinase I enhances the antihypertrophic effects of nitric oxide in cardiomyocytes. Hypertension. 2002;39:87-92.
49. Takemoto M, Node K, Nakagami H, et al. Statins as antioxidant therapy for preventing cardiac myocyte hypertrophy. J Clin Invest. 2001;108;1429-1437.
50. Kanno S, Lee PC, Zhang Y, et al. Attenuation of myocardial ischemia/ reperfusion injury by superinduction of inducible nitric oxide synthase. Circulation. 2000;101:2742-2748.
51. Quyyumi AA, Dakak N, Andrews NP, et al. Nitric oxide activity in the human coronary circulation: impact of risk factors for coronary atherosclerosis. J Clin Invest. 1995;95:1747-1755.
52. Buus NH, Bottcher M, Hermansen F, et al. Influence of nitric oxide synthase and adrenergic inhibition on adenosine-induced myocardial hyperemia. Circulation. 2001;104:2305-2310.
53. Heymes C, Vanderheyden M, Bronzwaer JG, et al. Endomyocardial nitric oxide synthase and left ventricular preload reserve in dilated cardiomyopathy. Circulation. 1999;99:3009-3016.
54. Drexler H. Nitric oxide synthases in the failing human heart: a doubled-edged sword? Circulation. 1999;99:2972-2975.
55. Massion PB, Feron O, Dessy C, et al. Nitric oxide and cardiac function: ten years after, and continuing. Circ Res. 2003;93:388-398.
56. Endo A, Tsujita Y, Kuroda M, et al. Effects of ML-236B on cholesterol metabolism in mice and rats: lack of hypocholesterolemic activity in normal animals. Biochim Biophys Acta. 1979;575:266-276.