Sex hormones promote opposite effects on ACE and ACE2 activity, hypertrophy and cardiac contractility in spontaneously hypertensive rats

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Dalpiaz, P L M ^a   Lamas, A Z ^a   Caliman, I F ^a   Ribeiro, R F ^a   Abreu, G R ^a   Moyses, M R ^a   Andrade, T U ^b   Gouvea, S A ^a   Alves, M F ^c   Carmona, A K ^c   Bissoli, N S ^a  

^a FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^b UNIVERSIDADE VILA VELHA   (Brazil)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; SEX HORMONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HEART FUNCTION; HEART HYPERTROPHY; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CONTRACTILITY; MALE; NONHUMAN; ORCHIECTOMY; OVARIECTOMY; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; SPONTANEOUSLY HYPERTENSIVE RAT; WESTERN BLOTTING; ANIMAL; BLOOD PRESSURE; BODY WEIGHT; CARDIOMEGALY; COMPLICATION; DENSITOMETRY; DRUG EFFECTS; ENZYMOLOGY; GONAD; HEART CONTRACTION; HEART VENTRICLE; HEMODYNAMICS; HYPERTENSION; METABOLISM; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; SURGERY; SYSTOLE;

ANIMALS; BLOOD PRESSURE; BLOTTING, WESTERN; BODY WEIGHT; CARDIOMEGALY; DENSITOMETRY; FEMALE; GONADAL STEROID HORMONES; GONADS; HEART VENTRICLES; HEMODYNAMICS; HYPERTENSION; MALE; MYOCARDIAL CONTRACTION; ORGAN SIZE; PEPTIDYL-DIPEPTIDASE A; RATS, INBRED SHR; SYSTOLE;

EID: 84960125372     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127515     Document Type: Article

References (65)

1. Vallotton MB. The renin-Angiotensin system. Trends Pharmacol Sci. 1987; 8: 69-74.
2. Pendergrass KD, Pirro NT, Westwood BM, Ferrario CM, Brosnihan KB, Chappell MC. Sex differences in circulating and renal angiotensins of hypertensive mRen(2). Lewis but not normotensive Lewis rats. Am J Physiol Heart Circ Physiol. 2008; 295: H10-20. doi: 10.1152/ajpheart.01277.2007 PMID: 18456730
3. Zimmerman MA, Sullivan JC. What's sex got to do with it? Hypertension. 2013; 28: 234-244. doi: 10. 1152/physiol.00013.2013 PMID: 23817798
4. Sarkissian S Der, Tea B, Touyz RM. Role of angiotensin II type 2 receptor during regression of cardiac hypertrophy in spontaneously hypertensive rats. J Am Soc Hypertens. Elsevier Ltd; 2013; 7: 118-127.
5. Crowley SD, Coffman TM. Recent advances involving the renin-Angiotensin system. Exp Cell Res. Elsevier Inc.; 2012; 318: 1049-1056. doi: 10.1016/j.yexcr.2012.02.023 PMID: 22410251
6. Ferreira AJ, Santos RAS, Bradford CN, Mecca AP, Sumners C, Katovich MJ, et al. Therapeutic Implications of the Vasoprotective Axis of the Renin-Angiotensin System in Cardiovascular Diseases. Hypertension. 2010; 55: 207-213. doi: 10.1161/HYPERTENSIONAHA.109.140145 PMID: 20038757
7. Os I, Franco V, Kjeldsen SE, Manhem K, Devereux RB, Gerdts E, et al. Effects of losartan in women with hypertension and left ventricular hypertrophy: Results from the losartan intervention for endpoint reduction in hypertension study. Hypertension. 2008; 51: 1103-8. doi: 10.1161/HYPERTENSIONAHA. 107.105296 PMID: 18259029
8. Reckelhoff JF, Zhang H, Srivastava K. Gender differences in Development of hypertension in spontaneously hypertensive rats: Role of the renin-Angiotensin system. Hypertension. 2000; 35: 480-483. PMID: 10642345
9. Komukai K, Mochizuki S, Yoshimura M. Gender and the renin-Angiotensin-Aldosterone system. Fundam Clin Pharmacol. 2010; 24: 687-698. doi: 10.1111/j.1472-8206.2010.00854.x PMID: 20608988
10. Sullivan JC, Bhatia K, Yamamoto T, Elmarakby AA. Ang (1-7) Receptor Antagonism Equalizes Angiotensin II-Induced Hypertension In Male And Female Spontaneously Hypertensive Rats. Hypertension. 2010; 56: 658-66. doi: 10.1161/HYPERTENSIONAHA.110.153668 PMID: 20713916
11. Dalpiaz PLM, Lamas AZ, Caliman IF, Medeiros ARS, Abreu GR, Moysés MR, et al. The chronic blockade of angiotensin I-converting enzyme eliminates the sex differences of serum cytokine levels of spontaneously hypertensive rats. Brazilian J Med Biol Res. 2013; 46: 171-177. PMID: 23369979
12. Sullivan JC. Sex and the renin-Angiotensin system: inequality between the sexes in response to RAS stimulation and inhibition. Am J Physiol Regul Integr Comp Physiol. 2008; 294: R1220-6. doi: 10.1152/ajpregu.00864.2007 PMID: 18287217
13. Maric-Bilkan C, Manigrasso MB. Sex differences in hypertension: contribution of the renin-Angiotensin system. Gend Med. Excerpta Medica, Inc.; 2012; 9: 287-91.
14. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, et al. Strategies and methods for research on sex differences in brain and behavior. Endocrinology. 2005; 146: 1650-73. PMID: 15618360
15. Yin FC, Spurgeon HA, Rakusan K, Weisfeldt ML, Lakatta EG. Use of tibial length to quantify cardiac hypertrophy: application in the aging rat. Am J Physiol. 1982; 243: H941-7. PMID: 6216817
16. Alves MF, Araujo MC, Juliano MA, Oliveira EM, Krieger JE, Casarini DE, et al. A continuous fluorescent assay for the determination of plasma and tissue angiotensin I-converting enzyme activity. Braz J Med Biol Res. 2005; 38: 861-8. PMID: 15933779
17. Vickers C, Hales P, Kaushik V, Dick L, Gavin J, Tang J, et al. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase. J Biol Chem. 2002; 277: 14838-43. PMID: 11815627
18. Wang X, Ren B, Liu S, Sentex E, Tappia PS, Dhalla NS. Characterization of cardiac hypertrophy and heart failure due to volume overload in the rat. J Appl Physiol. 2003; 94: 752-63. PMID: 12531914
19. R RF Jr., Fernandes AA, Meira EF, Batista PR, Siman FDM, Vassallo DV, et al. Soybean oil increases SERCA2a expression and left ventricular contractility in rats without change in arterial blood pressure. Lipids Health Dis. 2010; 9: 1-6. doi: 10.1186/1476-511X-9-1 PMID: 20053284
20. Pelzer T, Jazbutyte V, Hu K, Segerer S, Nahrendorf M, Nordbeck P, et al. The estrogen receptor-Agonist 16 ?-LE2 inhibits cardiac hypertrophy and improves hemodynamic function in estrogen-deficient spontaneously hypertensive rats. Cardiovasc Res. 2005; 67: 604-12. PMID: 15950203
21. Reckelhoff JF, Zhang H, Granger JP. Testosterone exacerbates hypertension and reduces pressurenatriuresis in male spontaneously hypertensive rats. Hypertension. 1998; 31: 435-439. PMID: 9453341
22. Tatchum-Talom A, Eyster KM, K CK Jr., Martin DS. Blood pressure and mesenteric vascular reactivity in SHR seven months after gonadectomy. J Cardiovasc pharmacol. 2012; 57: 357-364.
23. Reckelhoff JF, Zhang H, Srivastava K, Granger JP. Gender differences in hypertension in spontaneously hypertensive Rats: Role of androgens and androgen receptor. Hypertension. 1999; 34: 920-923. PMID: 10523385
24. Hudson M, Rahme E, Behlouli H, Sheppard R, Pilote L. Sex differences in the effectiveness of angiotensin receptor blockers and angiotensin converting enzyme inhibitors in patients with congestive heart failure-A population study. Eur J Heart Fail. 2007; 9: 602-609. PMID: 17383932
25. Bubb KJ, Khambata RS, Ahluwalia A. Sexual dimorphism in rodent models of hypertension and atherosclerosis. Br J Pharmacol. 2012; 167: 298-312. doi: 10.1111/j.1476-5381.2012.02036.x PMID: 22582712
26. Hilliard LM, Sampson AK, Brown RD, Denton KM. The "his and hers" of the renin-Angiotensin system. Curr Hypertens Rep. 2013; 15: 71-9. doi: 10.1007/s11906-012-0319-y PMID: 23180053
27. Khalil RA. Sex hormones as potential modulators of vascular function in hypertension. Hypertension. 2005; 46: 249-254. PMID: 15983238
28. Yanes LL, Reckelhoff JF. A new piece in the hypertension puzzle: central blood pressure regulation by sex steroids. Am J Physiol Heart Circ Physiol. 2009; 297: H1583-4. doi: 10.1152/ajpheart.00901.2009 PMID: 19801489
29. Bhatia K, Zimmerman MA, Sullivan JC. Sex differences in angiotensin-converting enzyme modulation of Ang (1-7) levels in normotensive WKY rats. Am J Hypertens. 2013; 26: 591-8. doi: 10.1093/ajh/hps088 PMID: 23547034
30. Burrell LM, Risvanis J, Kubota E, Dean RG, MacDonald PS, Lu S, et al. Myocardial infarction increases ACE2 expression in rat and humans. Eur Heart J. 2005; 26: 369-75; discussion 322-4. PMID: 15671045
31. Burchill L, Velkoska E, Dean RG, Lew RA, Smith AI, Levidiotis V, et al. Acute kidney injury in the rat causes cardiac remodelling and increases angiotensin-converting enzyme 2 expression. Exp Physiol. 2008; 93: 622-30. doi: 10.1113/expphysiol.2007.040386 PMID: 18223026
32. Kassiri Z, Zhong J, Guo D, Basu R, Wang X, Liu PP, et al. Loss of angiotensin-converting enzyme 2 accelerates maladaptive left ventricular remodeling in response to myocardial infarction. Circ Heart Fail. 2009; 2: 446-55. doi: 10.1161/CIRCHEARTFAILURE.108.840124 PMID: 19808375
33. Der Sarkissian S, Grobe JL, Yuan L, Narielwala DR, Walter GA, Katovich MJ, et al. Cardiac overexpression of angiotensin converting enzyme 2 protects the heart from ischemia-induced pathophysiology. Hypertension. 2008; 51: 712-8. doi: 10.1161/HYPERTENSIONAHA.107.100693 PMID: 18250366
34. Li L, Yi-Ming W, Li Z-Z, Zhao L, Yu Y-S, Li D-J, et al. Local RAS and inflammatory factors are involved in cardiovascular hypertrophy in spontaneously hypertensive rats. Pharmacol Res. 2008; 58: 196-201. doi: 10.1016/j.phrs.2008.06.009 PMID: 18639638
35. Zhao YX, Yin HQ, Yu QT, Qiao Y, Dai HY, Zhang MX, et al. ACE2 overexpression ameliorates left ventricular remodeling and dysfunction in a rat model of myocardial infarction. Hum Gene Ther. 2010; 21: 1545-54. doi: 10.1089/hum.2009.160 PMID: 20507236
36. Burrell LM, Johnston CI, Tikellis C, Cooper ME. ACE2, a new regulator of the renin-Angiotensin system. Trends Endocrinol Metab. 2004; 15: 166-9. PMID: 15109615
37. Lim YK, Retnam L, Bhagavath B, Sethi SK, Ali A Bin, Lim S-K. Gonadal effects on plasma ACE activity in mice. Atherosclerosis. 2002; 160: 311-316. PMID: 11849653
38. Riviére G, Michaud A, Breton C, VanCamp G, Laborie C, Enache M, et al. Angiotensin-converting enzyme 2 (ACE2) and ACE activities display tissue-specific sensitivity to undernutrition-programmed hypertension in the adult rat. Hypertension. 2005; 46: 1169-74. PMID: 16203874
39. Campbell DJ, Alexiou T, Xiao HD, Fuchs S, McKinley MJ, Corvol P, et al. Effect of reduced angiotensin-converting enzyme gene expression and angiotensin-converting enzyme inhibition on angiotensin and bradykinin peptide levels in mice. Hypertension. 2004; 43: 854-9. PMID: 14769811
40. Campbell DJ. Vasopeptidase inhibition: A double-edged sword? Hypertension. 2003; 41: 383-389. PMID: 12623931
41. Lindsey SH, Cohen JA, Brosnihan KB, Gallagher PE, Chappell MC. Chronic treatment with the G protein-coupled receptor 30 agonist G-1 decreases blood pressure in ovariectomized mRen2.Lewis rats. Endocrinology. 2009; 150: 3753-3758. doi: 10.1210/en.2008-1664 PMID: 19372194
42. Chappell MC, Gallagher PE, Averill DB, Ferrario CM, Bridget Brosnihan K. Estrogen or the AT1 antagonist olmesartan reverses the development of profound hypertension in the congenic mRen2.Lewis Rat. Hypertension. 2003; 42: 781-786. PMID: 12874087
43. Gallagher PE, Chappell MC, Errario CM, Tallant EA, Patricia E. Distinct roles for ANG II and ANG-(1-7) in the regulation of angiotensin-converting enzyme 2 in rat astrocytes. Am J Physiol Cell Physiol. 2006; 1032: 420-426.
44. Dong B, Yu QT, Dai HY, Gao YY, Zhou ZL, Zhang L, et al. Angiotensin-converting enzyme-2 overexpression improves left ventricular remodeling and function in a rat model of diabetic cardiomyopathy. J Am Coll Cardiol. 2012; 59: 739-47. doi: 10.1016/j.jacc.2011.09.071 PMID: 22340266
45. Fabris B, Candido R, Bortoletto M, Toffoli B, Bernardi S, Stebel M, et al. Stimulation of cardiac apoptosis in ovariectomized hypertensive rats: potential role of the renin-Angiotensin system. J Hypertens. 2011; 29: 273-281. doi: 10.1097/HJH.0b013e328340d0d3 PMID: 21107282
46. Dias DPM, Oliveira M, Salgado HC, F R Jr. Ovariectomy does not affect the cardiac sympathovagal balance of female SHR but estradiol does. Brazilian J Med Biol Res. 2010; 43: 969-975. PMID: 20945035
47. Reckelhoff JF. Gender differences in the regulation of blood pressure. Hypertension. 2001; 37: 1199-208. PMID: 11358929
48. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, et al. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature. 2002; 417: 822-8. PMID: 12075344
49. Falcón BL, Stewart JM, Bourassa E, Katovich MJ, Walter G, Speth RC, et al. Angiotensin II type 2 receptor gene transfer elicits cardioprotective effects in an angiotensin II infusion rat model of hypertension. Physiol Genomics. 2004; 19: 255-61. PMID: 15383639
50. Shenoy V, Grobe JL, Qi Y, Ferreira AJ, Fraga-Silva RA, Collamat G, et al. 17beta-Estradiol modulates local cardiac renin-Angiotensin system to prevent cardiac remodeling in the DOCA-salt model of hypertension in rats. Peptides. 2009; 30: 2309-15. doi: 10.1016/j.peptides.2009.09.005 PMID: 19747516
51. Hayasaki-kajiwara Y, Kitano Y, Iwasaki T, Naya N, Iwaki K, Nakajima M. Na+ Influx via Na+/H + Exchange Activates Protein Kinase C Isozymes and ? in Cultured Neonatal Rat Cardiac Myocytes. J Mol Cell Cardiol. 1999; 31: 1559-1572. PMID: 10423353
52. Brosnihan KB, Li P, Ganten D, Ferrario CM. Estrogen protects transgenic hypertensive rats by shifting the vasoconstrictor-vasodilator balance of RAS. Am J Physiol. 1997; 273: R1908-15. PMID: 9435644
53. Bachmann J, Wagner J, Haufe C, Wystrychowski A, Ciechanowicz A, Ganten D. Modulation of blood pressure and the renin-Angiotensin system in transgenic and spontaneously hypertensive rats afer ovariectomy. J Hypertens. 1993; 11: S226-7. PMID: 8158357
54. Xue B, Pamidimukkala J, Hay M. Sex differences in the development of angiotensin II-induced hypertension in conscious mice. Am J Physiol Heart Circ Physiol. 2005; 288: H2177-84. PMID: 15626687
55. Ferreira Filho C, Abreu LC De, Valenti VE, Ferreira M, Meneghini A, Silveira JA, et al. Anti-hypertensive drugs have different effects on ventricular hypertrophy regression. Clinics (Sao Paulo). 2010; 65: 723-8. doi: 10.1590/S1807-59322010000700012 PMID: 20668631
56. Duarte DR, Minicucci MF, Azevedo PS, Matsubara BB, Matsubara LS, Novelli EL, et al. The role of oxidative stress and lipid peroxidation in ventricular remodeling induced by tobacco smoke exposure after myocardial infarction. Clinics (Sao Paulo). 2009; 64: 691-7. doi: 10.1590/S1807-59322009000700014 PMID: 19606247
57. Piro M, Della Bona R, Abbate A, Biasucci LM, Crea F. Sex-related differences in myocardial remodeling. J Am Coll Cardiol. Elsevier Inc.; 2010; 55: 1057-65. doi: 10.1016/j.jacc.2009.09.065 PMID: 20223363
58. Remme WJ. Pharmacological modulation of cardiovascular remodeling: a guide to heart failure therapy. Cardiovasc Drugs Ther. 2003; 17: 349-60. PMID: 14618097
59. Chu SH, Sutherland K, Beck J, Kowalski J, Goldspink P, Schwertz D. Sex differences in expression of calcium-handling proteins and beta-Adrenergic receptors in rat heart ventricle. Life Sci. 2005; 76: 2735-49. PMID: 15792839
60. Chen J, Petranka J, Yamamura K, London RE, Steenbergen C, Murphy E. Gender differences in sarcoplasmic reticulum calcium loading after isoproterenol. Am J Physiol Hear Circ Physiol. 2003; 27709: 2657-2662.
61. Koss K, Grupp I, Kranias E. The relative phospholamban and SERCA2 ratio: a critical determinant of myocardial contractility. Basic Res Cardiol. 1997; 92: 17-24. PMID: 9062648
62. Simmerman HK, Jones LR. Phospholamban: protein structure, mechanism of action, and role in cardiac function. Physiol Rev. 1998; 78: 921-947. PMID: 9790566
63. Kadambi VJ, Ponniah S, Harrer JM, Hoit BD, Dorn GW, Walsh R a., et al. Cardiac-specific overexpression of phospholamban alters calcium kinetics and resultant cardiomyocyte mechanics in transgenic mice. J Clin Invest. 1996; 97: 533-539. PMID: 8567978
64. Chen YF, Naftilan AJ, Oparil S. Androgen-dependent angiotensinogen and renin messenger RNA expression in hypertensive rats. Hypertension. 1992; 19: 456-463. PMID: 1568764
65. Ellison KE, Ingelfinger JR, Pivor M, Dzau VJ. Androgen regulation of rat renal angiotensinogen messenger RNA expression. J Clin Invest. 1989; 83: 1941-1945. PMID: 2723066