Enalapril decreases cardiac mass and fetal gene expression without affecting the expression of endothelin-1, transforming growth factor β-1, or cardiotrophin-1 in the healthy normotensive rat

Canadian Journal of Physiology and Pharmacology

Volumn 89, Issue 3, 2011, Pages 197-205

  Mackovicova, Katarina ^a   Gazova, Andrea ^b   Kucerova, Dana ^a   Gajdacova, Beata ^a   Klimas, Jan ^a   Ochodnicky, Peter ^a   Goncalvesova, Eva ^c   Kyselovic, Jan ^a   Krenek, Peter ^a  

^a Physics and Informatics   (Slovakia)

^b Faculty of Medicine of Comenius University and University Hospital Bratislava   (Slovakia)

^c NATIONAL INSTITUTE OF CARDIOVASCULAR DISEASES   (Slovakia)

Author keywords

myosin heavy chain; Ace inhibitors; Atrial natriuretic peptide; Cardiotrophin 1; Enalapril; Endothelial nitric oxide synthase; Endothelin 1; Left ventricular mass; Normotensive rat; Transforming growth factor 1

Indexed keywords

ATRIAL NATRIURETIC FACTOR; CARDIOTROPHIN 1; CAVEOLIN 1; ENALAPRIL; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; RENIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOSE RESPONSE; DRUG ACTIVITY; DRUG EFFECT; GENE EXPRESSION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE; HEART RATE; HEART SIZE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SYSTOLIC BLOOD PRESSURE;

ANIMALS; BLOOD PRESSURE; CYTOKINES; ENALAPRIL; ENDOTHELIN-1; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART VENTRICLES; MALE; MYOCARDIUM; ORGAN SIZE; RATS; RATS, WISTAR; TRANSFORMING GROWTH FACTOR BETA1;

EID: 79952940507     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/Y11-014     Document Type: Article

References (49)

1. Aristizabal, D., Messerli, F.H., and Frohlich, E.D. 1994. Disparate structural effects on left and right ventricles by angiotensin-converting enzyme inhibitors and calcium antagonists in essential hypertension. Am. J. Cardiol. 73(7): 483-487. doi:10.1016/0002-9149(94)90679-3. PMID:8141090.
2. Bachetti, T., Comini, L., Pasini, E., Cargnoni, A., Curello, S., and Ferrari, R. 2001. Ace-inhibition with quinapril modulates the nitric oxide pathway in normotensive rats. J. Mol. Cell. Cardiol. 33(3): 395-403. doi:10.1006/jmcc.2000.1311. PMID:11181009.
3. Cadnapaphornchai, M.A., McFann, K., Strain, J.D., Masoumi, A., and Schrier, R.W. 2009. Prospective change in renal volume and function in children with ADPKD. Clin. J. Am. Soc. Nephrol. 4(4): 820-829. doi:10.2215/CJN.02810608. PMID:19346430.
4. Childs, T.J., Adams, M.A., and Mak, A.S. 1990. Regression of cardiac hypertrophy in spontaneously hypertensive rats by enalapril and the expression of contractile proteins. Hypertension, 16(6): 662-668. PMID:2147174.
5. Comini, L., Bachetti, T., Cargnoni, A., Bastianon, D., Gitti, G.L., Ceconi, C., and Ferrari, R. 2007. Therapeutic modulation of the nitric oxide: all ace inhibitors are not equivalent. Pharmacol. Res. 56(1): 42-48.doi:10.1016/j.phrs.2007.03.004. PMID:17475504.
6. Der Sarkissian, S., Marchand, E.L., Duguay, D., Hamet, P., and de-Blois, D. 2003. Reversal of interstitial fibroblast hyperplasia via apoptosis in hypertensive rat heart with valsartan or enalapril. Cardiovasc. Res. 57(3): 775-783. doi:10.1016/S0008-6363(02)00789-7. PMID:12618239.
7. Dillmann, W.H. 1980. Diabetes mellitus induces changes in cardiac myosin of the rat. Diabetes, 29(7): 579-582. PMID:6445843.
8. Donnini, S., Solito, R., Giachetti, A., Granger, H.J., Ziche, M., and Morbidelli, L. 2006. Fibroblast growth factor-2 mediates Angiotensin- converting enzyme inhibitor-induced angiogenesis in coronary endothelium. J. Pharmacol. Exp. Ther. 319(2): 515-522. doi:10.1124/jpet.106.108803. PMID:16868034.
9. Donnini, S., Terzuoli, E., Ziche, M., and Morbidelli, L. 2010. Sulfhydryl angiotensin-converting enzyme inhibitor promotes endothelial cell survival through nitric-oxide synthase, fibroblast growth factor-2, and telomerase cross-talk. J. Pharmacol. Exp. Ther. 332(3): 776-784. doi:10.1124/jpet.109.159178. PMID:19959747.
10. Fontaine, D., Fontaine, J., Dupont, I., Dessy, C., Piech, A., Carpentier, Y., and Berkenboom, G. 2002. Chronic hydroxymethylglutaryl coenzyme a reductase inhibition and endothelial function of the normocholesterolemic rat: comparison with angiotensin-converting enzyme inhibition. J. Cardiovasc. Pharmacol. 40(2): 172-180. doi:10.1097/00005344-200208000-00002. PMID:12131546.
11. Freed, D.H., Moon, M.C., Borowiec, A.M., Jones, S.C., Zahradka, P., and Dixon, I.M. 2003. Cardiotrophin-1: expression in experimental myocardial infarction and potential role in post-MI wound healing. Mol. Cell. Biochem. 254(1-2): 247-256.doi:10.1023/A:1027332504861. PMID:14674704.
12. Gray, M.O., Long, C.S., Kalinyak, J.E., Li, H.T., and Karliner, J.S. 1998. Angiotensin II stimulates cardiac myocyte hypertrophy via paracrine release of TGF-β 1 and endothelin-1 from fibroblasts. Cardiovasc. Res. 40(2): 352-363.doi:10.1016/S0008-6363(98)00121-7. PMID:9893729.
13. Hara, K., Kobayashi, N., Watanabe, S., Tsubokou, Y., and Matsuoka, H. 2001. Effects of quinapril on expression of eNOS, ACE, and AT1 receptor in deoxycorticosterone acetate-salt hypertensive rats. Am. J. Hypertens. 14(4): 321-330.doi:10.1016/S0895-7061(00)01283-8. PMID:11336177.
14. Harada, M., Itoh, H., Nakagawa, O., Ogawa, Y., Miyamoto, Y., Kuwahara, K., et al. 1997. Significance of ventricular myocytes and nonmyocytes interaction during cardiocyte hypertrophy: evidence for endothelin-1 as a paracrine hypertrophic factor from cardiac nonmyocytes. Circulation, 96(10): 3737-3744.PMID:9396478.
15. Ito, H., Hirata, Y., Adachi, S., Tanaka, M., Tsujino, M., Koike, A., et al. 1993. Endothelin-1 is an autocrine/paracrine factor in the mechanism of angiotensin II-induced hypertrophy in cultured rat cardiomyocytes. J. Clin. Invest. 92(1): 398-403. doi:10.1172/JCI116579. PMID:8326007.
16. Ji, Y., Huang, Y., Han, Y., Xu, Y., and Ferro, A. 2003. Cardiac effects of amiloride and of enalapril in the spontaneously hypertensive rat. J. Hypertens. 21(8): 1583-1589. doi:10.1097/00004872-200308000-00024. PMID:12872054.
17. Jougasaki, M., Tachibana, I., Luchner, A., Leskinen, H., Redfield, M.M., and Burnett, J.C., Jr. 2000. Augmented cardiac cardiotrophin-1 in experimental congestive heart failure. Circulation, 101(1): 14-17. PMID:10618298.
18. Kanno, S., Wu, Y.J., Lee, P.C., Billiar, T.R., and Ho, C. 2001. Angiotensin-converting enzyme inhibitor preserves p21 and endothelial nitric oxide synthase expression in monocrotalineinduced pulmonary arterial hypertension in rats. Circulation, 104(8): 945-950. doi:10.1161/hc3401.093155. PMID:11514384.
19. Kim, S., Ohta, K., Hamaguchi, A., Omura, T., Yukimura, T., Miura, K., et al. 1995. Angiotensin II type I receptor antagonist inhibits the gene expression of transforming growth factor-β 1 and extracellular matrix in cardiac and vascular tissues of hypertensive rats. J. Pharmacol. Exp. Ther. 273(1): 509-515. PMID:7714806.
20. Kim, S., Ohta, K., Hamaguchi, A., Yukimura, T., Miura, K., and Iwao, H. 1996. Effects of an AT1 receptor antagonist, an ACE inhibitor and a calcium channel antagonist on cardiac gene expressions in hypertensive rats. Br. J. Pharmacol. 118(3): 549-556. PMID:8762077.
21. Kim, S., Yoshiyama, M., Izumi, Y., Kawano, H., Kimoto, M., Zhan, Y., and Iwao, H. 2001. Effects of combination of ACE inhibitor and angiotensin receptor blocker on cardiac remodeling, cardiac function, and survival in rat heart failure. Circulation, 103(1): 148-154. PMID:11136700.
22. Kobayashi, N., Higashi, T., Hara, K., Shirataki, H., and Matsuoka, H. 1999. Effects of imidapril on NOS expression and myocardial remodelling in failing heart of Dahl salt-sensitive hypertensive rats. Cardiovasc. Res. 44(3): 518-526. doi:10.1016/S0008-6363(99)00237-0. PMID:10690283.
23. Krenek, P., Morel, N., Kyselovic, J., and Wibo, M. 2004. Amlodipine at high dose increases preproendothelin-1 expression in the ventricles and aorta of normotensive rats. J. Hypertens. 22(4): 827-835.doi:10.1097/00004872-200404000-00027. PMID:15126926.
24. Krenek, P., Klimas, J., Kroslakova, M., Gazova, A., Plandorova, J., Kucerova, D., et al. 2006. Increased expression of endothelial nitric oxide synthase and caveolin-1 in the aorta of rats with isoproterenol-induced cardiac hypertrophy. Can. J. Physiol. Pharmacol. 84(12): 1245-1250. doi:10.1139/Y06-073. PMID:17487232.
25. Linz, W., and Scholkens, B.A. 1992. A specific B2-bradykinin receptor antagonist HOE 140 abolishes the antihypertrophic effect of ramipril. Br. J. Pharmacol. 105(4): 771-772. PMID:1324047.
26. Linz, W., Wohlfart, P., Schoelkens, B.A., Becker, R.H., Malinski, T., and Wiemer, G. 1999. Late treatment with ramipril increases survival in old spontaneously hypertensive rats. Hypertension, 34(2): 291-295. PMID:10454456.
27. Liu, X., Sentex, E., Golfman, L., Takeda, S., Osada, M., and Dhalla, N.S. 1999. Modification of cardiac subcellular remodeling due to pressure overload by captopril and losartan. Clin. Exp. Hypertens. 21(1-2): 145-156. doi:10.3109/10641969909068657. PMID:10052650.
28. Livak, K.J., and Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCt. Methods, 25(4): 402-408. doi:10.1006/meth.2001.1262. PMID: 11846609.
29. Machackova, J., Liu, X., Lukas, A., and Dhalla, N.S. 2004. Reninangiotensin blockade attenuates cardiac myofibrillar remodelling in chronic diabetes. Mol. Cell. Biochem. 261(1): 271-278. doi:10.1023/B:MCBI.0000028765.89855.73. PMID:15362513.
30. Magga, J., Kalliovalkama, J., Romppanen, H., Vuolteenaho, O., Pörsti, I., Kähönen, M., et al. 1999. Differential regulation of cardiac adrenomedullin and natriuretic peptide gene expression by AT1 receptor antagonism and ACE inhibition in normotensive and hypertensive rats. J. Hypertens. 17(11): 1543-1552. doi:10.1097/00004872-199917110-00006. PMID:10608466.
31. Mercadier, J.J., Lompré, A.M., Wisnewsky, C., Samuel, J.L., Bercovici, J., Swynghedauw, B., and Schwartz, K. 1981. Myosin isoenzyme changes in several models of rat cardiac hypertrophy. Circ. Res. 49(2): 525-532. PMID:6454511.
32. Michel, J.B., Salzmann, J.L., Cerol, M.L., Dussaule, J.C., Azizi, M., Corman, B., et al. 1988. Myocardial effect of converting enzyme inhibition in hypertensive and normotensive rats. Am. J. Med. 84(3 Suppl 1): 12-21. doi:10.1016/0002-9343(88)90200-8. PMID:2975459.
33. Mooser, V., Casley, D., Trinder, D., Paxton, D.L., and Johnston, C.I. 1991. Reduction in left ventricular mass in normotensive and spontaneously hypertensive rats given enalapril. Clin. Exp. Pharmacol. Physiol. 18(5): 341-344. doi:10.1111/j.1440-1681. 1991.tb01459.x. PMID:1829664.
34. Paul, M., and Ganten, D. 1992. The molecular basis of cardiovascular hypertrophy: the role of the renin-angiotensin system. J. Cardiovasc. Pharmacol. 19(Suppl 5): S51-S58. PMID:1381795.
35. Pelouch, V., Kolar, F., Ost'adal, B., Milerova, M., Cihak, R., and Widimsky, J. 1997. Regression of chronic hypoxia-induced pulmonary hypertension, right ventricular hypertrophy, and fibrosis: effect of enalapril. Cardiovasc. Drugs Ther. 11(2): 177-185. doi:10.1023/A:1007788915732. PMID:9140694.
36. Pennica, D., King, K.L., Shaw, K.J., Luis, E., Rullamas, J., Luoh, S.M., et al. 1995. Expression cloning of cardiotrophin 1, a cytokine that induces cardiac myocyte hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 92(4): 1142-1146. doi:10.1073/pnas.92.4. 1142. PMID:7862649.
37. Pierce, G.N., and Dhalla, N.S. 1981. Cardiac myofibrillar ATPase activity in diabetic rats. J. Mol. Cell. Cardiol. 13(12): 1063-1069. doi:10.1016/0022-2828(81)90296-0. PMID:6120242.
38. Ritchie, R.H., Schiebinger, R.J., LaPointe, M.C., and Marsh, J.D. 1998. Angiotensin II-induced hypertrophy of adult rat cardiomyocytes is blocked by nitric oxide. Am. J. Physiol. 275(4 Pt 2): H1370-H1374. PMID:9746487.
39. Sadoshima, J., and Izumo, S. 1993. Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ. Res. 73(3): 413-423. PMID:8348686.
40. Sadoshima, J., Xu, Y., Slayter, H.S., and Izumo, S. 1993. Autocrine release of angiotensin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell, 75(5): 977-984. doi:10.1016/0092-8674(93)90541-W. PMID:8252633.
41. Sano, M., Fukuda, K., Kodama, H., Pan, J., Saito, M., Matsuzaki, J., et al. 2000. Interleukin-6 family of cytokines mediate angiotensin II-induced cardiac hypertrophy in rodent cardiomyocytes. J. Biol. Chem. 275(38): 29717-29723. doi:10.1074/jbc.M003128200. PMID:10843995.
42. Schmieder, R.E., and Messerli, F.H. 2000. Hypertension and the heart. J. Hum. Hypertens. 14(10-11): 597-604. doi:10.1038/sj.jhh.1001044. PMID:11095153.
43. Schweda, F., Friis, U., Wagner, C., Skott, O., and Kurtz, A. 2007. Renin release. Physiology (Bethesda), 22: 310-319. PMID:17928544.
44. Takai, S., Jin, D., Sakaguchi, M., and Miyazaki, M. 2004. Significant target organs for hypertension and cardiac hypertrophy by angiotensin-converting enzyme inhibitors. Hypertens. Res. 27(3): 213-219. doi:10.1291/hypres.27.213. PMID:15080380.
45. Takuwa, N., Takuwa, Y., Yanagisawa, M., Yamashita, K., and Masaki, T. 1989. A novel vasoactive peptide endothelin stimulates mitogenesis through inositol lipid turnover in Swiss 3T3 fibroblasts. J. Biol. Chem. 264(14): 7856-7861. PMID:2542249.
46. Wang, J., Liu, X., Ren, B., Rupp, H., Takeda, N., and Dhalla, N.S. 2002. Modification of myosin gene expression by imidapril in failing heart due to myocardial infarction. J. Mol. Cell. Cardiol. 34(7): 847-857. doi:10.1006/jmcc.2002.2023. PMID:12099723.
47. Wang, J., Guo, X., and Dhalla, N.S. 2004. Modification of myosin protein and gene expression in failing hearts due to myocardial infarction by enalapril or losartan. Biochim. Biophys. Acta, 1690(2): 177-184. PMID:15469907.
48. Yanagisawa, M., Kurihara, H., Kimura, S., Tomobe, Y., Kobayashi, M., Mitsui, Y., et al. 1988. A novel potent vasoconstrictor pep-tide produced by vascular endothelial cells. Nature, 332(6163): 411-415. doi:10.1038/332411a0. PMID:2451132.
49. Yu, W.C., Lin, Y.P., Lin, I.F., Chuang, S.Y., and Chen, C.H. 2006. Effect of ramipril on left ventricular mass in normotensive hemodialysis patients. Am. J. Kidney Dis. 47(3): 478-484. doi:10.1053/j.ajkd.2005.11.024. PMID:16490627.