Sexual dimorphism of the aging kidney: Role of nitric oxide deficiency

Physiology

Volumn 23, Issue 3, 2008, Pages 142-150

  Baylis, Chris ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; SEX HORMONE;

AGING; ANIMAL; CARDIOVASCULAR DISEASE; COMPARATIVE STUDY; FEMALE; HUMAN; KIDNEY; KIDNEY DISEASE; MALE; METABOLISM; RAT; REVIEW; SEXUAL DEVELOPMENT;

AGING; ANIMALS; CARDIOVASCULAR DISEASES; FEMALE; GONADAL STEROID HORMONES; HUMANS; KIDNEY; KIDNEY DISEASES; MALE; NITRIC OXIDE; RATS; SEX CHARACTERISTICS;

EID: 49049105360     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00001.2008     Document Type: Review

References (117)

1. Anderson S, Rennke HG, Zatz R. Glomerular adaptations with normal aging and with long-term converting enzyme inhibition in rats. Am J Physiol Renal Physiol 267: F35-F43, 1994.
2. Attia DM, Goldschmeding R, Attia MA, Boer P, Koomans HA, Joles JA. Male gender increases sensitivity to renal injury in response to cholesterol loading. Am J Physiol Renal Physiol 284: F718-F726, 2003.
3. Baylis C. Age-dependent glomerular damage in the rat: dissociation between glomerular injury and both glomerular hypertension and hypertrophy. Male gender as a primary risk factor. J Clin Invest 94: 1823-1829, 1994.
4. Baylis C. Nitric oxide deficiency: both consequence and cause of chronic renal disease (CKD). Hypertens Nephrol 5: 193-201, 2001.
5. 4a. Baylis C. Changes in renal hemodynamics and structure in the aging kidney: sexual dimorphism and the nitric oxide system. Exp Gerontol 40: 271-278, 2005.
6. Baylis C. Arginine, arginine analogs and nitric oxide production in chronic kidney disease (CKD). Nature Clin Practice Nephrol 2: 209-220, 2006.
7. Baylis C, Corman B. The aging kidney: insights from experimental studies. J Am Soc Nephrol 9: 699-709, 1998.
8. Berg UB. Differences in decline in GFR with age between males and females. Reference data on clearances of inulin and PAH in potential kidney donors. Nephrol Dial Transplant 21: 2577-2582, 2006.
9. Bleyer AJ, Shemanski LR, Burke GL, Hansen KJ, Appel RG. Tobacco, hypertension and vascular disease: risk factors for renal functional decline in an older population. Kidney Int 57: 2072-2079, 2000.
10. Blush J, Lei J, Ju W, Silbiger S, Pullman J, Neugarten J. Estradiol reverses renal injury in Alb/TGF-beta1 transgenic mice. Kidney Int 66: 2148-2154, 2004.
11. Bode-Boger SM, Muke J, Surdacki A, Brabant G, Boger RH, Frolich JC. Oral L-arginine improves endothelial function in healthy individuals older than 70 years. Vasc Med 8: 77-81, 2003.
12. Böger RH, Sydow K, Borlak J, Thum T, Lenzen H, Schubert B, Tsikas D, Bode-Böger SM. LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S- adenosylmethionine-dependent methyltransferases. Circ Res 87: 99-105, 2000.
13. Braunstein G.D.. Safety of testosterone treatment in postmenopausal women. Fertil Steril 88: 1-17, 2007.
14. Brinkworth GD, Noakes M, Moran LJ, Norman R, Clifton PM. Flow-mediated dilatation in overweight and obese women with polycystic ovary syndrome. BJOG 113: 1308-1314, 2006.
15. Ceccatelli S, Grandison L, Scott RE, Pfaff DW, Kow LM. Estradiol regulation of nitric oxide synthase mRNAs in rat hypothalamus. Neuroendocrinology 64: 357-363, 1996.
16. Celermajer DS, Sorensen KE, Spiegelhalter DJ, Georgakopoulos D, Robinson J, Deanfield JE. Aging is associated with endothelial dysfunction in healthy men years before the age-related decline in women. J Am Coll Cardiol 24: 471-476, 1994.
17. Cernadas MR, Sanchez de Miguel L, Garcia-Duran M, Gonzalez-Fernandez F, Millas I, Monton M, Rodrigo J, Rico L, Fernandez P, de Frutos T, Rodruigez-Feo JA, Guerra J, Carmelo C, Casado S, Lopez-Farre A. Expression of constitutive and inducible NOS in the vascular wall of young and aging rats. Circ Res 83: 279-286, 1998.
18. Cerrutti JA, Quaglia NB, Torres AM. Characterization of the mechanisms involved in the gender differences in p-aminohippurate renal elimination in rats. Can J Physiol Pharmacol 79: 805-813, 2001.
19. Cho JJ, Cadet P, Salamon E, Mantione KJ, Stefano GB. The nongenomic protective effects of estrogen on the male cardiovascular system: clinical and therapeutic implications in aging men. Med Sci Monit 9: RA63-RS68, 2003.
20. Dubey RK, Gillespie DG, Keller PJ, Imthurn B, Zacharia LC, Jackson EK. Role of methoxyestradiols in the growth inhibitory effects of estradiol on human glomerular mesangial cells. Hypertension 39: 418-424, 2002.
21. Dubey RK, Imthurn B, Barton M, Jackson EK. Vascular consequences of menopause and hormone therapy: importance of timing of treatment and type of estrogen. Cardiovasc Res 66: 295-306, 2005.
22. Dubey RK, Jackson EK. Estrogen-induced cardiorenal protection: potential cellular, biochemical and molecular mechanisms. Am J Physiol Renal Physiol 280: F365-F388, 2001.
23. Elliot SJ, Berho M, Korach K, Doublier S, Lupia E, Striker GE, Karl M. Gender-specific effects of endogenous testosterone: female alpha-estrogen receptor-deficient C57Bl/6J mice develop glomerulosclerosis. Kidney Int 72:464-472, 2007.
24. Elliot SJ, Karl M, Berho M, Potier M, Zheng F, Leclercq B, Striker GE, Striker LJ. Estrogen deficiency accelerates progression of glomerulosclerosis in susceptible mice. Am J Pathol 162: 1441-1448, 2003.
25. Erdely A, Greenfeld Z, Wagner L, Baylis C. Sexual dimorphism in the aging kidney; inverse relationship between injury and nitric oxide system. Kidney Int 63: 1021-1026, 2003.
26. Esqueda D, Craig T, Hinojosa-Laborde C. Effect of ovariectomy on renal estrogen receptor-alpha and renal estrogen receptor-beta in young salt-sensitive and resistant rats. Hypertension 50: 768-772, 2007.
27. Fadel PJ, Zhao W, Thomas GD. Impaired vasomodulation is associated with reduced neuronal nitric oxide synthase in skeletal muscle of ovariectomized rats. J Physiol 549: 243-253, 2003
28. Feinfeld DA, Guzik H, Carvounis CP, Lynn RI, Somer B, Aronson MK, Frishman WH. Sequential changes in renal function tests in the old old: results from the Bronx Longitudinal Aging Study. J Am Geriatr Soc 43: 412-414, 1995.
29. Fliser D, Franek E, Joest M, Block S, Mutschler E, Ritz E. Renal function in the elderly: impact of hypertension and cardiac function. Kidney Int 51: 1196-1204, 1997.
30. Forte P, Kneale BJ, Milne E, Chowienczyk PJ, Johnston A, Benjamin N, Ritter JM. Evidence for a difference in nitric oxide biosynthesis between healthy women and men. Hypertension 32: 730-734, 1998.
31. Fujihara CK, Limongi DMZP, DeOliveira HCF, Zatz R. Absence of focal glomerulosclerosis in aging analbuminemic rats. Am J Physiol 262: R947-R954, 1992.
32. Gabel SA, Walker VR, London RE, Steenbergen C, Korach KS, Murphy E. Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 38: 289-297, 2005.
33. Gades MD, Stern JS, van Goor H, Nguyen D, Johnson PR, Kaysen GA. Estrogen accelerates the development of renal disease in female obese Zucker rats. Kidney Int 53:130-135, 1998.
34. Gooren LJ, Giltay EJ. Review of studies of androgen treatment of female-to-male transsexuals: effects and risks of administration of androgens to females. J Sex Med 5: 765-776, 2008.
35. Guccione M, Silbiger S, Lei J, Neugarten J. Estradiol upregulates mesangial cell MMP-2 activity via the transcription factor AP-2. Am J Physiol Renal Physiol 282: F164-F169, 2002.
36. Harris H. Estrogen receptor β: recent lessons from in vivo studies. Mol Endocrinol 21: 1-13, 2007.
37. Hayashi T, Yamada K, Esaki T, Mutoh E, Iguchi A. Effect of estrogen on isoforms of nitric oxide synthase: possible mechanism of anti-atherosclerotic effect of estrogen. Gerontology 43, Suppl 1: 24-34, 1997.
38. Hemmelgarn BR, Zhang J, Manns BJ, Tonelli M, Larsen E, Ghali WA, Southern DA, McLaughlin K, Mortis G, Culleton BF. Progression of kidney dysfunction in the community-dwelling elderly. Kidney Int 69: 2155-2261, 2006.
39. Hill C, Lateef AM, Engels K, Samsell L, Baylis C. Basal and stimulated nitric oxide in control of kidney function in the aging rat. Am J Physiol Regul Integr Comp Physiol 272: R1747-R1753, 1997.
40. Holden DP, Cartwright JE, Nussey SS, Whitley GS. Estrogen stimulates dimethylarginine dimethylaminohydrolase activity and the metabolism of asymmetric dimethylarginine. Circulation 108: 1575-1580, 2003.
41. Hulley S, Grady D, Bush T, Furberg C, Herrington D, Riggs B, Vittinghoff E. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. JAMA 280: 605-613, 1998.
42. Jelinsky SA, Harris HA, Brown EL, Flanagan K, Zhang X, Tunkey C, Lai K, Lane MV, Simcoe DK, Evans MJ. Global transcription profiling of estrogen activity: estrogen receptor regulates gene expression in the kidney. Endocrinology 144: 701-710, 2003.
43. Joles JA, van Goor H, Koomans HA Estrogen induces glomerulosclerosis in analbuminemic rats. Kidney Int 53: 862-868, 1998.
44. Kapoor D, Malkin CJ, Channer KS, Jones TH. Androgens, insulin resistance and vascular disease in men. Clin Endocrinol (Oxf) 63: 239-250, 2005.
45. Karl M, Potier M, Schulman IH, Rivera A, Werner H, Fornoni A, Elliot SJ. Autocrine activation of the local insulin-like growth factor I system is up-regulated by estrogen receptor (ER)-independent estrogen actions and accounts for decreased ER expression in Type 2 diabetic mesangial cells. Endocrinology 146: 889-900, 2005.
46. Kasiske BL. Relationship between vascular disease and age-associated changes in the human kidney. Kidney Int 31: 1153-1159, 1987.
47. Kielstein JT, Bode-Boger SM, Frolich JC, Ritz E, Haller H, Fliser D. Asymmetric dimethylarginine, blood pressure, and renal perfusion in elderly subjects. Circulation 107: 1891-1895, 2003.
48. Kone BC, Baylis C. Biosynthesis and homeostatic roles of nitric oxide in the kidney. Editorial review. Am J Physiol Renal Physiol 272: F561-F578, 1997.
49. Krepinsky J, Ingram AJ, James L, Ly H, Thai K, Cattran DC, Miller JA, Scholey JW. 17Beta-estradiol modulates mechanical strain-induced MAPK activation in mesangial cells. J Biol Chem 277: 9387-9394, 2002.
50. Kwan G, Neugarten J, Sherman M, Ding Q, Fotadar U, Lei J, Silbiger S. Effects of sex hormones on mesangial cell proliferation and collagen synthesis. Kidney Int 50: 1173-1179, 1996.
51. Laughlin GA, Barrett-Connor E, May S. Sex-specific association of the androgen to oestrogen ratio with adipocytokine levels in older adults: the Rancho Bernardo Study. Clin Endocrinol (Oxf) 65: 506-513, 2006.
52. Levi M, Rowe JW. Renal function and dysfunction in aging. In: The Kidney: Physiology and Pathophysiology, edited by Seldin DW, Giebisch G. New York: Raven, 1992, p. 3433-3456.
53. Lindeman RD, Tobin J, Shock NW. Longitudinal studies on the rate of decline in renal function with age. J Am Geriatr Soc 33: 278-285, 1985.
54. Littleton-Kearney M, Hurn PD. Testosterone as a modulator of vascular behavior. Biol Res Nurs 5: 276-285, 2004.
55. Lombet JR, Adler SG, Anderson PS, Nast CC, Olsen DR, Glassock RJ. Sex vulnerability in the subtotal nephrectomy model of glomerulosclerosis in the rat. J Lab Clin Med 114: 66-74, 1989.
56. Lovegrove AS, Sun J,Gould KA, Lubahn DB, Korach KS, Lane PH. Estrogen receptor-mediated events promote sex-specific diabetic glomerular hypertrophy. Am J Physiol Renal Physiol 287: F586-F591, 2004.
57. Lu H, Lei X, Klaassen C. Gender differences in renal nuclear receptors and aryl hydrocarbon receptor in 5/6 nephrectomized rats. Kidney Int 70: 1920-1928, 2006.
58. Lu R, Hu CP, Wu XP, Liao EY, Li YJ. Effect of age on bone mineral density and the serum concentration of endogenous nitric oxide synthase inhibitors in rats. Comp Med 52: 224-228, 2002.
59. Lyons D, Roy S, Patel M, Benjamin N, Swift CG. Impaired nitric oxide-mediated vasodilatation and total body nitric oxide production in healthy old age. Clin Sci (Colch) 93: 519-525, 1997.
60. McLachlan MS, Guthrie JC, Anderson CK, Fulker MJ. Vascular and glomerular changes in the ageing kidney. J Pathol 121: 65-78, 1977.
61. Mershon JL, Baker RS, Clark KE. Estrogen increases iNOS expression in the ovine coronary artery. Am J Physiol Heart Circ Physiol 283: H1169-H1180, 2002.
62. Meyer MR, Haas E, Barton M. Gender differences of cardiovascular disease new perspectives for estrogen receptor signaling. Hypertension 47: 1019-1026, 2006.
63. Miller KK, Biller BM, Schaub A, Pulaski-Liebert K, Bradwin G, Rifai N, Klibanski A. Effects of testosterone therapy on cardiovascular risk markers in androgen-deficient women with hypopituitarism. J Clin Endocrinol Metab 92: 2474-9479, 2007.
64. Mistry S, Greenfeld Z, Morris S, Baylis C. The "intestinal- renal" arginine biosynthetic axis in the aging rat. Mech Ageing Dev 123: 1159-1165, 2002.
65. Mukherjee TK, Dinh H, Chaudhuri G, Nathan L. Testosterone attenuates expressiom of vascular cell adhesion molecule 1 by conversion to estradiol in endothelial cells: implications in atherosclerosis. PNAS 99: 4055-4060, 2002.
66. Munger K, Baylis C. Sex differences in renal hemodynamics in rats. Am J Physiol 254: F223-F231, 1988.
67. Nathan L, Shi W, Dinh H, Mukherjee TK, Wang X, Lusis AJ, Chaudhuri G. Testosterone inhibits early atherogenesis by conversion to estradiol: critical role of aromatase. PNAS 98: 3589-3593, 2001.
68. Neugarten J, Acharya A, Lei J, Silbiger S. Selective estrogen receptor modulators suppress mesangial cell collagen synthesis. Am J Physiol Renal Physiol 279: F309-F318, 2000.
69. Neugarten J, Acharya A, Silbiger SR. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis. J Am Soc Nephrol 11: 319-329, 2000.
70. Neugarten J, Ding Q, Friedman A, Le J, Silbiger S. Sex hormones and renal nitric oxide synthases. J Am Soc Nephrol 8: 1240-1246, 1997.
71. Neugarten J, Gallo G, Silbiger S, Kasiske B. Glomerulosclerosis in aging humans is not influenced by gender. Am J Kidney Dis 34: 884-888, 1999.
72. Neugarten J, Medve I, Lei J, Silbiger SR. Estradiol suppresses mesangial cell type I collagen synthesis via activation of the MAP kinase cascade. Am J Physiol 277: F875-F881, 1999.
73. Nijveldt RJ, Teerlink T, van Guldener C, Prins HA, van Lambalgen AA, Stehouwer CD, Rauwerda JA, van Leeuwen PA. Handling of asymmetrical dimethylarginine and symmetrical dimethylarginine by the rat kidney under basal conditions and during endotoxaemia. Nephrol Dial Transplant 18: 2542-2550, 2003.
74. Nijveldt RJ, Van Leeuwen PA, Van Guldener C, Stehouwer CD, Rauwerda JA, Teerlink T. Net renal extraction of asymmetrical (ADMA) and symmetrical (SDMA) dimethylarginine in fasting humans. Nephrol Dial Transplant 17: 1999-2002, 2002.
75. Noris M, Todeschini M, Zappella S, Bonazzola S, Zoja C, Corna D, Gaspari F, Marchetti G, Aiello S, Remuzzi G. 17beta-estradiol corrects hemostasis in uremic rats by limiting vascular expression of nitric oxide synthases. Am J Physiol Renal Physiol 279: F626-F635, 2000.
76. Oestreicher EM, Guo C, Seely EW, Kikuchi T, Martinez-Vasquez D, Jonasson L, Yao T, Burr D, Mayoral S, Roubsanthisuk W, Ricchiuti V, Adler GK. Estradiol increases proteinuria and angiotensin II type 1 receptor in kidneys of rats receiving L-NAME and angiotensin II. Kidney Int 70: 1759-1768, 2006.
77. Orshal JM, Khalil RA. Gender, sex hormones, and vascular tone. Am J Physiol Regul Integr Comp Physiol 286: R233-R249, 2004.
78. Potier M, Karl M, Zheng F, Elliot SJ, Striker GE, Striker LJ. Estrogen-related abnormalities in glomerulosclerosis-prone mice reduced mesangial cell estrogen receptor expression and prosclerotic response to estrogens. Am J Pathol 160: 1877-1885, 2002.
79. Rahman F, Christian HC. Non-classical actions of testosterone: an update. Trends Endocrinol Metab 18: 371-378, 2007.
80. Reckelhoff JF. Gender differences in the regulation of blood pressure. Hypertension 27: 1199-1208, 2001.
81. Reckelhoff JF, Baylis C. Glomerular metalloprotease activity is suppressed by androgens in the ageing kidney. J Am Soc Nephrol 3: 1835-1838, 1993.
82. Reckelhoff JF, Hennington BS, Moore AG, Blanchard EJ, Cameron J. Gender differences in the renal nitric oxide (NO) system: dissociation between expression of endothelial NO synthase and renal hemodynamic response to NO synthase inhibition. Am J Hypertens 11: 97-104, 1998.
83. Reckelhoff JF, Kellum JA, Blanchard EJ, Bacon EE, Wesley EJ, Kruckeberger WC. Changes in nitric oxide precursor, L-arginine and metabolites, nitrate and nitrite, with aging. Life Sci 55: 1895-1902, 1994.
84. Reckelhoff JF, Manning RD Jr. Role of endothelium-derived nitric oxide in control of renal microvasculature in aging male rats. Am J Physiol Regul Integr Comp Physiol 265: R1126-R1131, 1993.
85. Remuzzi A, Puntorieri S, Mazzoleni A, Remuzzi G. Sex related differences in glomerular ultrafiltration and proteinuria in Munich Wistar rats. Kidney Int 34: 481-486, 1988.
86. Rizzo M, Rini GB, Carmina E. Androgen excess and cardiovascular risk. Minerva Endocrinol 32: 67-71, 2007.
87. Rogers JL, Adam R, Mitchell AR, Maric C, Sandberg K, Myers A, Mulroney SE. Effect of sex hormones on renal estrogen and angiotensin type 1 receptors in female and male rats. Am J Physiol Regul Integr Comp Physiol 292: R794-R799, 2007.
88. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J; Writing Group for the Women's Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288: 321-333, 2002.
89. Schleich F, Legros JJ. Effects of androgen substitution on lipid profile in the adult and aging hypogonadal male. Eur J Endocrinol 151: 415-424, 2004.
90. Schmidt RJ, Beierwaltes WH, Baylis C. Aging and alterations in dietary sodium intake on total nitric oxide production in normal man. Am J Kidney Dis 37: 900-908, 2001.
91. Schmieder RE, Schachinger H, Messerli FH. Accelerated decline in renal perfusion with aging in essential hypertension. Hypertension 23: 351-357, 1994.
92. G-dimethyl-L-arginine in 500 subjects. Eur J Clin Invest 35: 622-626, 2005.
93. Seliger SL, Davis C, Stehman-Breen C. Gender and the progression of renal disease. Curr Opin Nephrol Hypertens 10: 219-225, 2001.
94. Sharma PK, Thakur MK. Estrogen receptor a expression in mice kidney shows sex differences during aging. Biogerontology 5: 375-381, 2004.
95. Shaw LJ, Merz CN, Azziz R, Stanczyk FZ, Sopko G, Braunstein GD, Kelsey SF, Kip KE, Cooper-Dehoff RM, Johnson BD, Vaccarino V, Reis SE, Bittner V, Hodgson TK, Rogers W, Pepine CJ. Postmenopausal women with a history of irregular menses and elevated androgen measurements at high risk for worsening cardiovascular event-free survival: results from the National Institutes of Health - National Heart, Lung, and Blood Institute sponsored Women's Ischemia Syndrome Evaluation (WISE). J Clin Endocrinol Metab 93: 1276-1284, 2008.
96. Silbiger S, Lei J, Ziyadeh FN, Neugarten J. Estradiol reverses TGF-beta1-stimulated type IV collagen gene transcription in murine mesangial cells. Am J Physiol Renal Physiol 274: F1113-F1118, 1998.
97. Simons JL, Provoost AP, Anderson S, Troy JL, Rennke HG, Sandstrom DJ, Brenner BM. Pathogenesis of glomerular injury in the fawn-hooded rat: early glomerular capillary hypertension predicts glomerular sclerosis. J Am Soc Nephrol 3: 1775-1782, 1993.
98. Sonaka I, Futami Y, Maki T. L-Arginine-nitric oxide pathway and chronic nephropathy in aged rats. J Gerontol Biol Sci 49: B157-B161, 1990.
99. Stier CT Jr, Chander PN Rosenfeld L, Powers CA. Estrogen promotes microvascular pathology in female stroke-prone spontaneously hypertensive rats. Am J Physiol Endocrinol Metab 285: E232-E239, 2003.
100. Sun J, Langer WJ, Devish K, Lane PH. Compensatory kidney growth in estrogen receptor-alpha null mice. Am J Physiol Renal Physiol 290: F319-F323, 2006.
101. Uribarri J, Cai W, Peppa M, Goodman S, Ferrucci L, Striker G, Vlassara H. Circulating glycotoxins and dietary advanced glycation endproducts: two links to inflammatory response, oxidative stress, and aging. J Gerontol A Biol Sci Med Sci 62: 427-433, 2007.
102. Van Dijk SJ, Specht PA, Lazar J, Jacob HJ, Provoost AP. Renal damage susceptibility and autoregulation in RF-1 and RF-5 congenic rats. Nephron Exp Nephrol 101: e59-e66, 2005.
103. Vasudevan H, Nagareddy PR, McNeill JH. Gonadectomy prevents endothelial dysfunction in fructose-fed male rats, a factor contributing to the development of hypertension. Am J Physiol Heart Circ Physiol 291: H3058-H3064, 2006.
104. Verhagen AM, Attia DM, Koomans HA, Joles JA. Male gender increases sensitivity to proteinuria induced by mild NOS inhibition in rats: role of sex hormones. Am J Physiol Renal Physiol 279: F664-F670, 2000.
105. Wells CC, Riazi S, Mankhey RW, Bhatti F, Ecelbarger C, Maric C. Diabetic nephropathy is associated with decreased circulating estradiol levels and imbalance in the expression of renal estrogen receptors. Gend Med 2: 227-237, 2005.
106. Wesson LG Jr. Renal hemodynamics in physiological states. In: Physiology of the Human Kidney. New York: Grune and Stratton, 1969, p. 96-108.
107. Williams MR, Dawood T, Ling S, Dai A, Lew R, Myles K, Funder JW, Sudhir K, Komesaroff PA. Dehydroepiandrosterone increases endothelial cell proliferation in vitro and improves endothelial function in vivo by mechanisms independent of androgen and estrogen receptors. J Clin Endocrinol Metab 89: 4708-4715, 2004.
108. Wynne FL, Payne JA, Cain AE, Reckelhoff JF, Khalil RA. Age-related reduction in estrogen receptor-mediated mechanisms of vascular relaxation in female spontaneously hypertensive rats. Hypertension 43: 405-412, 2004.
109. Xiao S, Gillespie DG, Baylis C, Jackson EK, Dubey RK. Effects of estradiol and its metabolites on glomerular endothelial NO synthesis and mesangial cell growth. Hypertension 37: 645-650, 2001.
110. Xiong Y, Yuan LW, Deng HW, Li YJ, Chen BM. Elevated serum endogenous inhibitor of nitric oxide synthase and endothelial dysfunction in aged rats. Clin Exp Pharmacol Physiol 28: 842-847, 2001.
111. Xue JL, Eggers PW, Agodoa LY, Foley RN, Collins AJ. Longitudinal study of racial and ethnic differences in developing end-stage renal disease among aged medicare beneficiaries. J Am Soc Nephrol 18: 1299-1306, 2007.
112. Yamagata K, Ishida K, Sairenchi T, Takahashi H, Ohba S, Shiigai T, Narita M, Koyama A. Risk factors for chronic kidney disease in a community-based population: a 10-year follow-up study. Kidney Int 71: 159-166, 2007.
113. Yildiz O. Vascular smooth muscle and endothelial functions in aging. Ann NY Acad Sci 1100: 353-360, 2007.
114. You HJ, Kim JY, Jeong HG. 17 Beta-estradiol increases inducible nitric oxide synthase expression in macrophages. Biochem Biophys Res Commun 303: 1129-1134, 2003.
115. Yu J, Eto M, Akishita M, Kaneko A, Ouchi Y, Okabe T. Signaling pathway of nitric oxide production induced by ginsenoside Rb1 in human aortic endothelial cells: a possible involvement of androgen receptor. Biochem Biophys Res Commun 353: 764-769, 2007.
116. Zheng F, Plati AR, Potier M, Schulman Y, Berho M, Banerjee A, Leclercq B, Zisman A, Striker LJ, Striker GE. Resistance to glomerulosclerosis in B6 mice disappears after menopause. Am J Pathol 162: 1339-1348, 2003.
117. Zhu Y, Bian Z, Lu P, Karas RH, Bao L, Cox D, Hodgin J, Shaul PW, Thoren P, Smithies O, Gustafsson JA, Mendelsohn ME. Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science 295: 505-508, 2002.