Sex-Specific Changes in Renal Angiotensin-Converting Enzyme and Angiotensin-Converting Enzyme 2 Gene Expression and Enzyme Activity at Birth and over the First Year of Life

Reproductive Sciences

Volumn 23, Issue 2, 2016, Pages 200-210

  Chen, K A I ^a   Bi, Jianli ^a   Su, Y I X I N ^a   Chappell, Mark C ^a   Rose, James C ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

angiotensin converting enzyme; angiotensin converting enzyme 2; kidney; renin angiotensin system; sex

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; DIPEPTIDYL CARBOXYPEPTIDASE; MESSENGER RNA;

ADULT; ARTICLE; BIRTH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; FEMALE; FETUS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; KIDNEY FUNCTION; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SEX DIFFERENCE; SHEEP; ANIMAL; BLOOD PRESSURE; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; BLOOD PRESSURE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KIDNEY; MALE; PEPTIDYL-DIPEPTIDASE A; RENIN-ANGIOTENSIN SYSTEM; SEX CHARACTERISTICS; SHEEP;

EID: 84954182968     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719115597760     Document Type: Article

References (68)

1. Givertz MM,. Manipulation of the renin-angiotensin system. Circulation. 2001; 104 (5): E14-E18.
2. Timmermans PB, Wong PC, Chiu AT, et al. Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacol Rev. 1993; 45 (2): 205-251.
3. Peach MJ,. Molecular actions of angiotensin. Biochem Pharmacol. 1981; 30 (20): 2745-2751.
4. Csikos T, Gallinat S, Unger T,. Extrarenal aspects of angiotensin II function. Eur J Endocrinol. 1997; 136 (4): 349-358.
5. Bottari SP, De GM, Steckelings UM, Levens NR,. Angiotensin II receptor subtypes: characterization, signalling mechanisms, and possible physiological implications. Front Neuroendocrinol. 1993; 14 (2): 123-171.
6. Carey RM,. Cardiovascular and renal regulation by the angiotensin type 2 receptor: the AT2 receptor comes of age. Hypertension. 2005; 45 (5): 840-844.
7. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ,. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem. 2000; 275 (43): 33238-33243.
8. Vickers C, Hales P, Kaushik V, et al. Hydrolysis of biological peptides by human angiotensin-converting enzyme-related carboxypeptidase. J Biol Chem. 2002; 277 (17): 14838-14843.
9. Santos RA, Haibara AS, Campagnole-Santos MJ, et al. Characterization of a new selective antagonist for angiotensin-(1-7), D-pro7-angiotensin-(1-7). Hypertension. 2003; 41 (3 pt 2): 737-743.
10. Ferrario CM, Trask AJ, Jessup JA,. Advances in biochemical and functional roles of angiotensin-converting enzyme 2 and angiotensin-(1-7) in regulation of cardiovascular function. Am J Physiol Heart Circ Physiol. 2005; 289 (6): H2281-H2290.
11. Brosnihan KB, Li P, Ferrario CM,. Angiotensin-(1-7) dilates canine coronary arteries through kinins and nitric oxide. Hypertension. 1996; 27 (3 pt 2): 523-528.
12. Santos RA, Campagnole-Santos MJ, Andrade SP,. Angiotensin-(1-7): an update. Regul Pept. 2000; 91 (1-3): 45-62.
13. Wakahara S, Konoshita T, Mizuno S, et al. Synergistic expression of angiotensin-converting enzyme (ACE) and ACE2 in human renal tissue and confounding effects of hypertension on the ACE to ACE2 ratio. Endocrinology. 2007; 148 (5): 2453-2457.
14. Forhead AJ, Gillespie CE, Fowden AL,. Role of cortisol in the ontogenic control of pulmonary and renal angiotensin-converting enzyme in fetal sheep near term. J Physiol. 2000; 526 (pt 2): 409-416.
15. Song R, Preston G, Yosypiv IV,. Ontogeny of angiotensin-converting enzyme 2. Pediatr Res. 2012; 71 (1): 13-19.
16. Tikellis C, Cooper ME, Bialkowski K, et al. Developmental expression of ACE2 in the SHR kidney: a role in hypertension? Kidney Int. 2006; 70 (1): 34-41.
17. Baumbach GL, Chillon JM,. Effects of angiotensin-converting enzyme inhibitors on cerebral vascular structure in chronic hypertension. J Hypertens Suppl. 2000; 18 (1): S7-S11.
18. Salvetti A, Pedrinelli R, Arzilli F, et al. Angiotensin-converting enzyme inhibitors in hypertension: a review. Int J Clin Pharmacol Res. 1985; 5 (6): 429-438.
19. Su Z, Zimpelmann J, Burns KD,. Angiotensin-(1-7) inhibits angiotensin II-stimulated phosphorylation of MAP kinases in proximal tubular cells. Kidney Int. 2006; 69 (12): 2212-2218.
20. Ye M, Wysocki J, Naaz P, Salabat MR, LaPointe MS, Batlle D,. Increased ACE 2 and decreased ACE protein in renal tubules from diabetic mice: a renoprotective combination? Hypertension. 2004; 43 (5): 1120-1125.
21. Landazuri P, Granobles C, Loango N,. Gender differences in serum angiotensin-converting enzyme activity and blood pressure in children: an observational study. Arq Bras Cardiol. 2008; 91 (6): 352-357.
22. Zapater P, Novalbos J, Gallego-Sandin S, Hernandez FT, bad-Santos F,. Gender differences in angiotensin-converting enzyme (ACE) activity and inhibition by enalaprilat in healthy volunteers. J Cardiovasc Pharmacol. 2004; 43 (5): 737-744.
23. Gandolfo MT, Verzola D, Salvatore F, et al. Gender and the progression of chronic renal diseases: does apoptosis make the difference? Minerva Urol Nefrol. 2004; 56 (1): 1-14.
24. Neugarten J, Acharya A, Silbiger SR,. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis. J Am Soc Nephrol. 2000; 11 (2): 319-329.
25. Silbiger S, Neugarten J,. Gender and human chronic renal disease. Gend Med. 2008; 5 (suppl A): S3-S10.
26. Silbiger SR, Neugarten J,. The impact of gender on the progression of chronic renal disease. Am J Kidney Dis. 1995; 25 (4): 515-533.
27. Silbiger SR, Neugarten J,. The role of gender in the progression of renal disease. Adv Ren Replace Ther. 2003; 10 (1): 3-14.
28. Tang L, Carey LC, Bi J, et al. Gender differences in the effects of antenatal betamethasone exposure on renal function in adult sheep. Am J Physiol Regul Integr Comp Physiol. 2009; 296 (2): R309-R317.
29. Wang DH, Elijovich F,. Modulation and function of extrarenal angiotensin receptors. Cell Biochem Biophys. 1999; 31 (1): 1-17.
30. Chen K, Carey LC, Liu J, Valego NK, Tatter SB, Rose JC,. The effect of hypothalamo-pituitary disconnection on the renin-angiotensin system in the late-gestation fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2005; 288 (5): R1279-R1287.
31. Ferrario CM, Jessup J, Chappell MC, et al. Effect of angiotensin-converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2. Circulation. 2005; 111 (20): 2605-2610.
32. Allred AJ, Diz DI, Ferrario CM, Chappell MC,. Pathways for angiotensin-(1 - -7) metabolism in pulmonary and renal tissues. Am J Physiol Renal Physiol. 2000; 279 (5): F841-F850.
33. Shaltout HA, Figueroa JP, Rose JC, Diz DI, Chappell MC,. Alterations in circulatory and renal angiotensin-converting enzyme and angiotensin-converting enzyme 2 in fetal programmed hypertension. Hypertension. 2009; 53 (2): 404-408.
34. Freshour JR, Chase SE, Vikstrom KL,. Gender differences in cardiac ACE expression are normalized in androgen-deprived male mice. Am J Physiol Heart Circ Physiol. 2002; 283 (5): H1997-H2003.
35. Brosnihan KB, Weddle D, Anthony MS, Heise C, Li P, Ferrario CM,. Effects of chronic hormone replacement on the renin-angiotensin system in cynomolgus monkeys. J Hypertens. 1997; 15 (7): 719-726.
36. Kulemina LV, Ostrov DA,. Prediction of off-target effects on angiotensin-converting enzyme 2. J Biomol Screen. 2011; 16 (8): 878-885.
37. Gallagher PE, Li P, Lenhart JR, Chappell MC, Brosnihan KB,. Estrogen regulation of angiotensin-converting enzyme mRNA. Hypertension. 1999; 33 (1 pt 2): 323-328.
38. Komukai K, Mochizuki S, Yoshimura M,. Gender and the renin-angiotensin-aldosterone system. Fundam Clin Pharmacol. 2010; 24 (6): 687-698.
39. Liu J, Ji H, Zheng W, et al. Sex differences in renal angiotensin converting enzyme 2 (ACE2) activity are 17beta-oestradiol-dependent and sex chromosome-independent. Biol Sex Differ. 2010; 1 (1): 6.
40. 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 (1): H10-H20.
41. Ji H, Menini S, Zheng W, Pesce C, Wu X, Sandberg K,. Role of angiotensin-converting enzyme 2 and angiotensin(1-7) in 17beta-oestradiol regulation of renal pathology in renal wrap hypertension in rats. Exp Physiol. 2008; 93 (5): 648-657.
42. Wysocki J, Ye M, Soler MJ, et al. ACE and ACE2 activity in diabetic mice. Diabetes. 2006; 55 (7): 2132-2139.
43. Wosten-van Asperen RM, Lutter R, et al. Acute respiratory distress syndrome leads to reduced ratio of ACE/ACE2 activities and is prevented by angiotensin-(1-7) or an angiotensin II receptor antagonist. J Pathol. 2011; 225 (4): 618-627.
44. Dai R, Phillips RA, Karpuzoglu E, Khan D, Ahmed SA,. Estrogen regulates transcription factors STAT-1 and NF-kappaB to promote inducible nitric oxide synthase and inflammatory responses. J Immunol. 2009; 183 (11): 6998-7005.
45. Hernandez Prada JA, Ferreira AJ, et al. Structure-based identification of small-molecule angiotensin-converting enzyme 2 activators as novel antihypertensive agents. Hypertension. 2008; 51 (5): 1312-1317.
46. Qi Y, Zhang J, Cole-Jeffrey CT, et al. Diminazene aceturate enhances angiotensin-converting enzyme 2 activity and attenuates ischemia-induced cardiac pathophysiology. Hypertension. 2013; 62 (4): 746-752.
47. Lloyd LJ, Foster T, Rhodes P, Rhind SM, Gardner DS,. Protein-energy malnutrition during early gestation in sheep blunts fetal renal vascular and nephron development and compromises adult renal function. J Physiol. 2012; 590 (2): 377-393.
48. Esther CR Jr, Howard TE, Marino EM, Goddard JM, Capecchi MR, Bernstein KE,. Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. Lab Invest. 1996; 74 (5): 953-965.
49. Gonzalez-Villalobos RA, Janjoulia T, Fletcher NK, et al. The absence of intrarenal ACE protects against hypertension. J Clin Invest. 2013; 123 (5): 2011-2023.
50. Sandnberg ME, Smith LJ, Correa-Rotter R, Hostetter TH,. The paradox of the renin-angiotensin system in chronic renal disease. Kidney Int. 1994; 45 (2): 403-410.
51. Zhong JC, Huang DY, Yang YM, et al. Upregulation of angiotensin-converting enzyme 2 by all-trans retinoic acid in spontaneously hypertensive rats. Hypertension. 2004; 44 (6): 907-912.
52. Hilliard LM, Sampson AK, Brown RD, Denton KM,. The "his and hers" of the renin-angiotensin system. Curr Hypertens Rep. 2013; 15 (1): 71-79.
53. Sandberg K,. Mechanisms underlying sex differences in progressive renal disease. Gend Med. 2008; 5 (1): 10-23.
54. Lankadeva YR, Singh RR, Tare M, Moritz KM, Denton KM,. Loss of a kidney during fetal life: long-term consequences and lessons learned. Am J Physiol Renal Physiol. 2014; 306 (8): F791-F800.
55. Gilbert RE, Wu LL, Kelly DJ, et al. Pathological expression of renin and angiotensin II in the renal tubule after subtotal nephrectomy. Implications for the pathogenesis of tubulointerstitial fibrosis. Am J Pathol. 1999; 155 (2): 429-440.
56. Harris RC, Cheng HF,. The intrarenal renin-angiotensin system: a paracrine system for the local control of renal function separate from the systemic axis. Exp Nephrol. 1996; 4 (suppl 1): 2-7.
57. Schulman IH, Zhou MS, Treuer AV, Chadipiralla K, Hare JM, Raij L,. Altered renal expression of angiotensin II receptors, renin receptor, and ACE-2 precede the development of renal fibrosis in aging rats. Am J Nephrol. 2010; 32 (3): 249-261.
58. Vio CP, Jeanneret VA,. Local induction of angiotensin-converting enzyme in the kidney as a mechanism of progressive renal diseases. Kidney Int Suppl. 2003;(86): S57-S63.
59. Anderson S, Rennke HG, Brenner BM,. Therapeutic advantage of converting enzyme inhibitors in arresting progressive renal disease associated with systemic hypertension in the rat. J Clin Invest. 1986; 77 (6): 1993-2000.
60. Lafayette RA, Mayer G, Park SK, Meyer TW,. Angiotensin II receptor blockade limits glomerular injury in rats with reduced renal mass. J Clin Invest. 1992; 90 (3): 766-771.
61. Lewis EJ, Hunsicker LG, Bain RP, Rohde RD,. The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. N Engl J Med. 1993; 329 (20): 1456-1462.
62. Rose e M, Wysocki J, William J, Soler MJ, Cokic I, Batlle D,. Glomerular localization and expression of angiotensin-converting enzyme 2 and angiotensin-converting enzyme: implications for albuminuria in diabetes. J Am Soc Nephrol. 2006; 17 (11): 3067-3075.
63. Oudit GY, Herzenberg AM, Kassiri Z, et al. Loss of angiotensin-converting enzyme-2 leads to the late development of angiotensin II-dependent glomerulosclerosis. Am J Pathol. 2006; 168 (6): 1808-1820.
64. Chappell MC,. Emerging evidence for a functional angiotensin-converting enzyme 2-angiotensin-(1-7)-MAS receptor axis: more than regulation of blood pressure? Hypertension. 2007; 50 (4): 596-599.
65. Liu CX, Hu Q, Wang Y, et al. Angiotensin-converting enzyme (ACE) 2 overexpression ameliorates glomerular injury in a rat model of diabetic nephropathy: a comparison with ACE inhibition. Mol Med. 2011; 17 (1-2): 59-69.
66. Gwathmey TM, Pendergrass KD, Reid SD, Rose JC, Diz DI, Chappell MC,. Angiotensin-(1-7)-angiotensin-converting enzyme 2 attenuates reactive oxygen species formation to angiotensin II within the cell nucleus. Hypertension. 2010; 55 (1): 166-171.
67. Koka V, Huang XR, Chung AC, Wang W, Truong LD, Lan HY,. Angiotensin II up-regulates angiotensin I-converting enzyme (ACE), but down-regulates ACE2 via the AT1-ERK/p38 MAP kinase pathway. Am J Pathol. 2008; 172 (5): 1174-1183.
68. Tikellis C, Johnston CI, Forbes JM, et al. Characterization of renal angiotensin-converting enzyme 2 in diabetic nephropathy. Hypertension. 2003; 41 (3): 392-397.