Effects of 17β-estradiol on cardiac Na+/K+-ATPase in high fat diet fed rats

Molecular and Cellular Endocrinology

Volumn 416, Issue , 2015, Pages 46-56

  Obradovic, Milan ^a   Zafirovic, Sonja ^a   Jovanovic, Aleksandra ^a   Milovanovic, Emina Sudar ^a   Mousa, Shaker A ^b   Labudovic Borovic, Milica ^c   Isenovic, Esma R ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b ALBANY COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

^c UNIVERSITY OF BELGRADE   (Serbia)

Author keywords

Estradiol; High fat diet; Insulin resistance; Obesity; Sodium potassium adenosine triphosphatase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANGIOTENSIN II RECEPTOR TYPE 1; ANGIOTENSIN RECEPTOR; ESTRADIOL; INSULIN RECEPTOR SUBSTRATE 1; LEPTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE SUBUNIT P85; PROTEIN KINASE B; RHO KINASE; SODIUM; SODIUM POTASSIUM ADENOSINE TRIPHOSPHATASE ALPHA 1; SODIUM POTASSIUM ADENOSINE TRIPHOSPHATASE ALPHA 2; UNCLASSIFIED DRUG; ANGIOTENSIN 1 RECEPTOR; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HEART FAILURE; IN VIVO STUDY; INTRACELLULAR SIGNALING; LIPID DIET; MALE; NONHUMAN; OBESITY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SODIUM BLOOD LEVEL; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; BLOOD; CARDIAC MUSCLE; CARDIOMEGALY; DRUG EFFECTS; ENZYMOLOGY; INSULIN RESISTANCE; METABOLISM; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; CARDIOMEGALY; DIET, HIGH-FAT; ESTRADIOL; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MALE; MYOCARDIUM; OBESITY; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECEPTOR, ANGIOTENSIN, TYPE 1; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84943625339     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.08.020     Document Type: Article

References (96)

1. Aikawa R., Komuro I., Nagai R., Yazaki Y. Rho plays an important role in angiotensin II-induced hypertrophic responses in cardiac myocytes. Mol. Cell Biochem. 2000, 212(1-2):177-182.
2. Ainslie D.A., Morris M.J., Wittert G., Turnbull H., Proietto J., Thorburn A.W. Estrogen deficiency causes central leptin insensitivity and increased hypothalamic neuropeptide Y. Int. J. Obes. Relat. Metab. Disord. 2001, 25(11):1680-1688.
3. Al-Khalili L., Kotova O., Tsuchida H., Ehren I., Feraille E., Krook A., Chibalin A.V. ERK1/2 mediates insulin stimulation of Na(+),K(+)-ATPase by phosphorylation of the alpha-subunit in human skeletal muscle cells. J. Biol. Chem. 2004, 279(24):25211-25218.
4. +-ATPase trafficking in skeletal muscle: insulin stimulates translocation of both alpha 1- and alpha 2-subunit isoforms. FEBS Lett. 2003, 536(1-3):198-202.
5. Antolovic R., Bauer N., Mohadjerani M., Kost H., Neu H., Kirch U., Grunbaum E.G., Schoner W. Endogenous ouabain and its binding globulin: effects of physical exercise and study on the globulin's tissue distribution. Hypertens. Res. 2000, 23(Suppl. l):S93-S98.
6. Aoki H., Izumo S., Sadoshima J. Angiotensin II activates RhoA in cardiac myocytes: a critical role of RhoA in angiotensin II-induced premyofibril formation. Circ. Res. 1998, 82(6):666-676.
7. Araujo I.G., Elias L.L., Antunes-Rodrigues J., Reis L.C., Mecawi A.S. Effects of acute and subchronic AT receptor blockade on cardiovascular, hydromineral and neuroendocrine responses in female rats. Physiol. Behav. 2013, 122:C104-C112.
8. Artham S.M., Lavie C.J., Patel H.M., Ventura H.O. Impact of obesity on the risk of heart failure and its prognosis. J. Cardiometab. Syndr. 2008, 3(3):155-161.
9. Bagrov A.Y., Shapiro J.I., Fedorova O.V. Endogenous cardiotonic steroids: physiology, pharmacology, and novel therapeutic targets. Pharmacol. Rev. 2009, 61(1):9-38.
10. Barnard R.J., Roberts C.K., Varon S.M., Berger J.J. Diet-induced insulin resistance precedes other aspects of the metabolic syndrome. J. Appl. Physiol. (1985) 1998, 84(4):1311-1315.
11. Bennett P.A., Lindell K., Wilson C., Carlsson L.M., Carlsson B., Robinson I.C. Cyclical variations in the abundance of leptin receptors, but not in circulating leptin, correlate with NPY expression during the oestrous cycle. Neuroendocrinology 1999, 69(6):417-423.
12. +-ATPase alpha1 and alpha2 subunits in T-tubule and surface sarcolemmal membranes. Cardiovasc. Res. 2007, 73(1):92-100.
13. Bray G.A., Yukimura Y. Activity of (Na+ + K+)-ATPase in the liver of animals with experimental obesity. Life Sci. 1978, 22(18):1637-1642.
14. Bryzgalova G., Lundholm L., Portwood N., Gustafsson J.A., Khan A., Efendic S., Dahlman-Wright K. Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. Am. J. Physiol. Endocrinol. Metab. 2008, 295(4):E904-E912.
15. Buettner R., Scholmerich J., Bollheimer L.C. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 2007, 15(4):798-808.
16. Burnette W.N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 1981, 112(2):195-203.
17. Cassis L.A., Fettinger M.J., Roe A.L., Shenoy U.R., Howard G. Characterization and regulation of angiotensin II receptors in rat adipose tissue. Angiotensin receptors in adipose tissue. Adv. Exp. Med. Biol. 1996, 39639-39647.
18. Chiang S.H., Baumann C.A., Kanzaki M., Thurmond D.C., Watson R.T., Neudauer C.L., Macara I.G., Pessin J.E., Saltiel A.R. Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature 2001, 410(6831):944-948.
19. +-ATPase is initiated by phosphorylation of Ser-18 in the rat alpha subunit and is responsible for the decreased activity in epithelial cells. J. Biol. Chem. 1999, 274(4):1920-1927.
20. +-ATPase endocytosis. J. Biol. Chem. 1998, 273(15):8814-8819.
21. Clegg D.J., Brown L.M., Woods S.C., Benoit S.C. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 2006, 55(4):978-987.
22. Clegg D.J., Riedy C.A., Smith K.A., Benoit S.C., Woods S.C. Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 2003, 52(3):682-687.
23. Dean S.A., Tan J., O'Brien E.R., Leenen F.H. 17beta-estradiol downregulates tissue angiotensin-converting enzyme and ANG II type 1 receptor in female rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288(3):R759-R766.
24. Devarajan P., Benz E.J. Translational regulation of Na-K-ATPase subunit mRNAs by glucocorticoids. Am. J. Physiol. Ren. Physiol. 2000, 279(6):F1132-F1138.
25. Dzurba A., Ziegelhoffer A., Vrbjar N. Influence of estradiol on sarcolemmal (Na,K)-ATPase of the myocardium. Proceedings of the International Symposium on Hormones and Cardiovascular System 1983, Czechoslovak Medical Society, Prague. J.E.E. Purkyne (Ed.).
26. Dzurba A., Ziegelhoffer A., Vrbjar N., Styk J., Slezak J. Estradiol modulates the sodium pump in the heart sarcolemma. Mol. Cell Biochem. 1997, 176(1-2):113-118.
27. Ewart H.S., Klip A. Hormonal regulation of the Na(+)-K(+)-ATPase: mechanisms underlying rapid and sustained changes in pump activity. Am. J. Physiol. 1995, 269(2 Pt 1):C295-C311.
28. Fabris B., Candido R., Bortoletto M., Toffoli B., Bernardi S., Stebel M., Bardelli M., Zentilin L., Giacca M., Carretta R. Stimulation of cardiac apoptosis in ovariectomized hypertensive rats: potential role of the renin-angiotensin system. J. Hypertens. 2011, 29(2):273-281.
29. Fischer M., Baessler A., Schunkert H. Renin angiotensin system and gender differences in the cardiovascular system. Cardiovasc. Res. 2002, 53(3):672-677.
30. Fuller W., Tulloch L.B., Shattock M.J., Calaghan S.C., Howie J., Wypijewski K.J. Regulation of the cardiac sodium pump. Cell Mol. Life Sci. 2013, 70(8):1357-1380.
31. Garty H., Karlish S.J. Role of FXYD proteins in ion transport. Annu. Rev. Physiol. 2006, 68431-68459.
32. Gayard M., Guilluy C., Rousselle A., Viollet B., Henrion D., Pacaud P., Loirand G., Rolli-Derkinderen M. AMPK alpha 1-induced RhoA phosphorylation mediates vasoprotective effect of estradiol. Arterioscler. Thromb. Vasc. Biol. 2011, 31(11):2634-2642.
33. +-ATPase alpha-subunit gene expression in hypertension. Science 1988, 241(4862):221-223.
34. Higashi M., Shimokawa H., Hattori T., Hiroki J., Mukai Y., Morikawa K., Ichiki T., Takahashi S., Takeshita A. Long-term inhibition of Rho-kinase suppresses angiotensin II-induced cardiovascular hypertrophy in rats in vivo: effect on endothelial NAD(P)H oxidase system. Circ. Res. 2003, 93(8):767-775.
35. Hundal H.S., Marette A., Mitsumoto Y., Ramlal T., Blostein R., Klip A. Insulin induces translocation of the alpha 2 and beta 1 subunits of the Na+/K(+)-ATPase from intracellular compartments to the plasma membrane in mammalian skeletal muscle. J. Biol. Chem. 1992, 267(8):5040-5043.
36. Iacobellis G., Ribaudo M.C., Zappaterreno A., Iannucci C.V., Di Mario U., Leonetti F. Adapted changes in left ventricular structure and function in severe uncomplicated obesity. Obes. Res. 2004, 12(10):1616-1621.
37. Iannello S., Milazzo P., Belfiore F. Animal and human tissue Na,K-ATPase in normal and insulin-resistant states: regulation, behaviour and interpretative hypothesis on NEFA effects. Obes. Rev. 2007, 8(3):231-251.
38. + pump involves the phosphatidylinositol-3 kinase and p42/44 mitogen-activated protein kinase signaling pathways in vascular smooth muscle cells. Endocrinology 2004, 145(3):1151-1160.
39. Isenovic E.R., Meng Y., Jamali N., Milivojevic N., Sowers J.R. Ang II attenuates IGF-1-stimulated Na+, K(+)-ATPase activity via PI3K/Akt pathway in vascular smooth muscle cells. Int. J. Mol. Med. 2004, 13(6):915-922.
40. Isenovic E.R., Sha Q., Milivojevic N.M., Sowers J.R. Ang II inhibits E2-induced nitric oxide production and gene expression of the catalytic subunit of the sodium pump in VSMC. Proceedings of 62nd Scientific Sessions. Diabetes, Moscone Center, San Francisco, Supplement 2 2002, Diabetes, San Francisco.
41. James P.F., Grupp I.L., Grupp G., Woo A.L., Askew G.R., Croyle M.L., Walsh R.A., Lingrel J.B. Identification of a specific role for the Na,K-ATPase α2 isoform as a regulator of calcium in the heart. Mol. Cell. 1999, 3(5):555-563.
42. Javeshghani D., Touyz R.M., Sairam M.R., Virdis A., Neves M.F., Schiffrin E.L. Attenuated responses to angiotensin II in follitropin receptor knockout mice, a model of menopause-associated hypertension. Hypertension 2003, 42(4):761-767.
43. Jewell E.A., Shamraj O.I., Lingrel J.B. Isoforms of the alpha subunit of Na,K-ATPase and their significance. Acta Physiol. Scand. Suppl. 1992, 607161-607169.
44. Kaplan J.H. Biochemistry of Na,K-ATPase. Annu. Rev. Biochem. 2002, 71511-71535.
45. Kaschina E., Unger T. Angiotensin AT1/AT2 receptors: regulation, signalling and function. Blood Press 2003, 12(2):70-88.
46. Katz A.I., Epstein F.H. The role of sodium-potassium-activated adenosine triphosphatase in the reabsorption of sodium by the kidney. J. Clin. Invest. 1967, 46(12):1999-2011.
47. Kim S., Iwao H. Molecular and cellular mechanisms of angiotensin II-mediated cardiovascular and renal diseases. Pharmacol. Rev. 2000, 52(1):11-34.
48. Knowlton A.A., Lee A.R. Estrogen and the cardiovascular system. Pharmacol. Ther. 2012, 135(1):54-70.
49. Kshatriya S., Liu K., Salah A., Szombathy T., Freeman R.H., Reams G.P., Spear R.M., Villarreal D. Obesity hypertension: the regulatory role of leptin. Int. J. Hypertens. 2011, 2011. 270624.
50. Kumar V., Bhandari U., Tripathi C.D., Khanna G. Evaluation of antiobesity and cardioprotective effect of Gymnema sylvestre extract in murine model. Indian J. Pharmacol. 2012, 44(5):607-613.
51. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
52. Lavie C.J., Messerli F.H. Cardiovascular adaptation to obesity and hypertension. Chest 1986, 90(2):275-279.
53. Lee M.J., Fried S.K. Multilevel regulation of leptin storage, turnover, and secretion by feeding and insulin in rat adipose tissue. J. Lipid Res. 2006, 47(9):1984-1993.
54. +-ATPase. J. Biol. Chem. 2011, 286(37):32289-32299.
55. +-ATPase enzyme units in skeletal muscle from lean and obese mice. Biochem. Biophys. Res. Commun. 1978, 80(2):398-404.
56. Liu C., Bai Y., Chen Y., Wang Y., Sottejeau Y., Liu L., Li X., Lingrel J.B., Malhotra D., Cooper C.J., et al. Reduction of Na/K-ATPase potentiates marinobufagenin-induced cardiac dysfunction and myocyte apoptosis. J. Biol. Chem. 2012, 287(20):16390-16398.
57. 2+-ATPase and carbonic anhydrase iv in H9C2 cells. Clin. Exp. Pharmacol. Physiol. 2007, 34(10):998-1004.
58. Liu Y.F., Herschkovitz A., Boura-Halfon S., Ronen D., Paz K., Leroith D., Zick Y. Serine phosphorylation proximal to its phosphotyrosine binding domain inhibits insulin receptor substrate 1 function and promotes insulin resistance. Mol. Cell Biol. 2004, 24(21):9668-9681.
59. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193(1):265-275.
60. Luiken J.J., Koonen D.P., Willems J., Zorzano A., Becker C., Fischer Y., Tandon N.N., Van Der Vusse G.J., Bonen A., Glatz J.F. Insulin stimulates long-chain fatty acid utilization by rat cardiac myocytes through cellular redistribution of FAT/CD36. Diabetes 2002, 51(10):3113-3119.
61. Martin S.S., Qasim A., Reilly M.P. Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease. J. Am. Coll. Cardiol. 2008, 52(15):1201-1210.
62. Masek J., Fabry P. High-fat diet and the development of obesity in albino rats. Experientia 1959, 15444-15445.
63. Mauro L., Salerno M., Panno M.L., Bellizzi D., Sisci D., Miglietta A., Surmacz E., Ando S. Estradiol increases IRS-1 gene expression and insulin signaling in breast cancer cells. Biochem. Biophys. Res. Commun. 2001, 288(3):685-689.
64. McDonough A.A., Zhang Y., Shin V., Frank J.S. Subcellular distribution of sodium pump isoform subunits in mammalian cardiac myocytes. Am. J. Physiol. 1996, 270(4 Pt 1):C1221-C1227.
65. Mirza F.S., Ong P., Collins P., Okamura K., Gerhard-Herman M., Williams G.H., Seely E.W. Effects of estradiol and the angiotensin II receptor blocker irbesartan on vascular function in postmenopausal women. Menopause 2008, 15(1):44-50.
66. Murphy E. Estrogen signaling and cardiovascular disease. Circ. Res. 2011, 109(6):687-696.
67. Nickenig G., Baumer A.T., Grohe C., Kahlert S., Strehlow K., Rosenkranz S., Stablein A., Beckers F., Smits J.F., Daemen M.J., et al. Estrogen modulates AT1 receptor gene expression in vitro and in vivo. Circulation 1998, 97(22):2197-2201.
68. Nishimatsu H., Suzuki E., Satonaka H., Takeda R., Omata M., Fujita T., Nagai R., Kitamura T., Hirata Y. Endothelial dysfunction and hypercontractility of vascular myocytes are ameliorated by fluvastatin in obese Zucker rats. Am. J. Physiol. Heart Circ. Physiol. 2005, 288(4):H1770-H1776.
69. Oakes N.D., Cooney G.J., Camilleri S., Chisholm D.J., Kraegen E.W. Mechanisms of liver and muscle insulin resistance induced by chronic high-fat feeding. Diabetes 1997, 46(11):1768-1774.
70. Obradovic M., Bjelogrlic P., Rizzo M., Katsiki N., Haidara M., Stewart A.J., Jovanovic A., Isenovic E.R. Effects of obesity and estradiol on Na+/K+-ATPase and their relevance to cardiovascular diseases. J. Endocrinol. 2013, 218(3):R13-R23.
71. Obradovic M., Stewart A.J., Pitt S.J., Labudovic-Borovic M., Sudar E., Petrovic V., Zafirovic S., Maravic-Stojkovic V., Vasic V., Isenovic E.R. In vivo effects of 17beta-estradiol on cardiac Na(+)/K(+)-ATPase expression and activity in rat heart. Mol. Cell Endocrinol. 2014, 388(1-2):58-68.
72. Obradovic M., Sudar E., Zafirovic S., Stanimirovic J., Labudovic-Borovic M., Isenovic E.R. Estradiol in vivo induces changes in cardiomyocytes size in obese rats. Angiology 2015, 66(1):25-35.
73. Ouwens D.M., Boer C., Fodor M., de Galan P., Heine R.J., Maassen J.A., Diamant M. Cardiac dysfunction induced by high-fat diet is associated with altered myocardial insulin signalling in rats. Diabetologia 2005, 48(6):1229-1237.
74. Palacios J., Marusic E.T., Lopez N.C., Gonzalez M., Michea L. Estradiol-induced expression of N(+)-K(+)-ATPase catalytic isoforms in rat arteries: gender differences in activity mediated by nitric oxide donors. Am. J. Physiol. Heart Circ. Physiol. 2004, 286(5):H1793-H1800.
75. Saltiel A.R., Kahn C.R. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001, 414(6865):799-806.
76. Schwinger R.H., Bundgaard H., Muller-Ehmsen J., Kjeldsen K. The Na, K-ATPase in the failing human heart. Cardiovasc. Res. 2003, 57(4):913-920.
77. 2+ exchanger protein levels in human heart failure. Circulation 1999, 99(16):2105-2112.
78. Shimizu H., Shimomura Y., Nakanishi Y., Futawatari T., Ohtani K., Sato N., Mori M. Estrogen increases in vivo leptin production in rats and human subjects. J. Endocrinol. 1997, 154(2):285-292.
79. Sudar E., Velebit J., Gluvic Z., Zakula Z., Lazic E., Vuksanovic-Topic L., Putnikovic B., Neskovic A., Isenovic E.R. Hypothetical mechanism of sodium pump regulation by estradiol under primary hypertension. J. Theor. Biol. 2008, 251(4):584-592.
80. Sun X.J., Goldberg J.L., Qiao L.Y., Mitchell J.J. Insulin-induced insulin receptor substrate-1 degradation is mediated by the proteasome degradation pathway. Diabetes 1999, 48(7):1359-1364.
81. Sykiotis G.P., Papavassiliou A.G. Serine phosphorylation of insulin receptor substrate-1: a novel target for the reversal of insulin resistance. Mol. Endocrinol. 2001, 15(11):1864-1869.
82. Taras M.J., Greenberg A.E., Hoak R.D., Rand M.C. Standard Methods for the Examination of Water and Wastewater 1971, DC American Public Health Association, Washington.
83. Therien A.G., Blostein R. Mechanisms of sodium pump regulation. Am. J. Physiol. Cell Physiol. 2000, 279(3):C541-C566.
84. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 1979, 76(9):4350-4354.
85. Treasure J.L., Ploth D.W., Treasure T. Measurement of potassium concentration on-line with an ion-specific electrode during hemodialysis. Miner. Electrolyte Metab. 1986, 12(3):161-164.
86. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T., Tamakawa H., Yamagami K., Inui J., Maekawa M., et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 1997, 389(6654):990-994.
87. van Son J.A., Smedts F., de Wilde P.C., Pijls N.H., Wong-Alcala L., Kubat K., Tavilla G., Lacquet L.K. Histological study of the internal mammary artery with emphasis on its suitability as a coronary artery bypass graft. Ann. Thorac. Surg. 1993, 55(1):106-113.
88. Vrbjar N., Bernatova I., Pechanova O. Functional alterations of cardiac (Na,K)-ATPase in L-NAME induced hypertension. Gen. Physiol. Biophys. 1999, 18(Suppl. l):110-112.
89. Vrbjar N., Wachalova K., Sipola M., Vapaatalo H. Sodium and ATP affinities of the cardiac Na(+),K(+)-ATPase in spontaneously hypertensive rats. Gen. Physiol. Biophys. 2002, 21(3):303-313.
90. Worth H.G. A comparison of the measurement of sodium and potassium by flame photometry and ion-selective electrode. Ann. Clin. Biochem. 1985, 22(Pt 4):343-350.
91. Xu R.Y., Wan Y.P., Tang Q.Y., Wu J., Cai W. The effects of high fat on central appetite genes in Wistar rats: a microarray analysis. Clin. Chim. Acta 2008, 397(1-2):96-100.
92. Yamamoto S., Akera T., Brody T.M. Positive inotropic action of digoxigenin and sodium pump inhibition: effects of enhanced sodium influx. J. Pharmacol. Exp. Ther. 1980, 213(1):105-109.
93. Ye Y., Hu S.J., Li L. Inhibition of farnesylpyrophosphate synthase prevents angiotensin II-induced hypertrophic responses in rat neonatal cardiomyocytes: involvement of the RhoA/Rho kinase pathway. FEBS Lett. 2009, 583(18):2997-3003.
94. Zacharieva S., Kirilov G., Kalinov K., Shigarminova R., Nachev E., Orbetzova M., Atanassova I. Effect of different hormone replacement therapy regimens on circadian blood pressure profile and active renin in postmenopausal women. Gynecol. Endocrinol. 2002, 16(6):461-467.
95. Zhang L., Song H., Ge Y., Ji G., Yao Z. Temporal relationship between diet-induced steatosis and onset of insulin/leptin resistance in male Wistar rats. PLoS One 2015, 10(2):1-15.
96. Zhou M.S., Schulman I.H., Zeng Q. Link between the renin-angiotensin system and insulin resistance: implications for cardiovascular disease. Vasc. Med. 2012, 17(5):330-341.