Protective role of female gender in programmed accelerated renal aging in the rat

Physiological Reports

Volumn 3, Issue 4, 2015, Pages

  Pijacka, Wioletta ^a,b   Clifford, Bethan ^b   Tilburgs, Chantal ^c   Joles, Jaap A ^c   Langley Evans, Simon ^b   McMullen, Sarah ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Age; Angiotensin II; Angiotensin II receptor; Estrogen; Sex steroids

Indexed keywords

ANGIOTENSIN 2 RECEPTOR; CARBONYL DERIVATIVE; ESTROGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

AGING; ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BLOOD SAMPLING; BODY WEIGHT; CONTROLLED STUDY; CREATININE CLEARANCE; EXPOSURE; FEMALE; FETAL EXPOSURE; FLUID INTAKE; GENDER; GLOMERULUS FILTRATION RATE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KIDNEY CORTEX; KIDNEY FUNCTION; LIPID STORAGE; NONHUMAN; ORGAN WEIGHT; OVARIECTOMY; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN RESTRICTION; PROTEIN URINE LEVEL; PROTEINURIA; RAT; REMOTE SENSING; UREA BLOOD LEVEL; URINE VOLUME; WESTERN BLOTTING;

EID: 85003582772     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12342     Document Type: Article

References (59)

1. Antus, B., P. Hamar, G. Kokeny, Z. Szollosi, I. Mucsi, Z. Nemes, et al. 2003. Estradiol is nephroprotective in the rat remnant kidney. Nephrol. Dial. Transplant. 18:54–61.
2. Attia, D. M., Z. N. Ni, P. Boer, M. A. Attia, R. Goldschmeding, H. A. Koomans, et al. 2002. Proteinuria is preceded by decreased nitric oxide synthesis and prevented by a NO donor in cholesterol-fed rats. Kidney Int. 61:1776–1787.
3. August, P., and S. Oparil. 1999. Hypertension in women. J. Clin. Endocrinol. Metab. 84:1862–1866.
4. Baiardi, G., M. Macova, I. Armando, H. Ando, D. Tyurmin, and J. M. Saavedra. 2005. Estrogen upregulates renal angiotensin II AT1 and AT2 receptors in the rat. Regul. Pept. 124:7–17.
5. Baylis, C. 2005. Changes in renal hemodynamics and structure in the aging kidney; sexual dimorphism and the nitric oxide system. Exp. Gerontol. 40:271–278.
6. Baylis, C. 2009. Sexual dimorphism, the aging kidney, and involvement of nitric oxide deficiency. Semin. Nephrol. 29:569–578.
7. Baylis, C. 2012. Sexual dimorphism: the aging kidney, involvement of nitric oxide deficiency, and angiotensin II overactivity. J. Gerontol. A Biol. Sci. Med. Sci. 67:1365–1372.
8. Baylis, C., M. Fredericks, J. Leypoldt, R. Frigon, C. Wilson, and L. Henderson. 1988. The mechanisms of proteinuria in aging rats. Mech. Ageing Dev. 45:111–126.
9. Birn, H., and E. I. Christensen. 2006. Renal albumin absorption in physiology and pathology. Kidney Int. 69:440–449.
10. Bongartz, L. G., B. Braam, M. C. Verhaar, M. J. Cramer, R. Goldschmeding, C. A. Gaillard, et al. 2010. Transient nitric oxide reduction induces permanent cardiac systolic dysfunction and worsens kidney damage in rats with chronic kidney disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298:R815–R823.
11. Bongartz, L. G., J. A. Joles, M. C. Verhaar, M. J. Cramer, R. Goldschmeding, C. Tilburgs, et al. 2012. Subtotal nephrectomy plus coronary ligation leads to more pronounced damage in both organs than either nephrectomy or coronary ligation. Am. J. Physiol. Heart Circ. Physiol. 302:H845–H854.
12. Botev, R., J. P. Mallie, C. Couchoud, O. Schuck, J. P. Fauvel, J. F. Wetzels, et al. 2009. Estimating glomerular filtration rate: Cockcroft-Gault and Modification of Diet in Renal Disease formulas compared to renal inulin clearance. Clin. J. Am. Soc. Nephrol. 4:899–906.
13. Colen, R. R., and F. A. Jolesz. 2010. Future potential of MRI- guided focused ultrasound brain surgery. Neuroimaging Clin. N. Am. 20:355–366.
14. Corman, B., and J. B. Michel. 1986. Renin-angiotensin system, converting-enzyme inhibition and kidney function in aging female rats. Am. J. Physiol. 251:R450–R455.
15. Cornock, R., S. C. Langley-Evans, A. Mobasheri, and S. McMullen. 2010. The impact of maternal protein restriction during rat pregnancy upon renal expression of angiotensin receptors and vasopressin-related aquaporins. Reprod. Biol. Endocrinol. 8:105.
16. Crofton, J. T., M. Ota, and L. Share. 1993. Role of vasopressin, the renin-angiotensin system and sex in Dahl salt-sensitive hypertension. J. Hypertens. 11:1031–1038.
17. Dendooven, A., D. A. Jr Ishola, T. Q. Nguyen, D. M. Van der Giezen, R. J. Kok, R. Goldschmeding, et al. 2011. Oxidative stress in obstructive nephropathy. Int. J. Exp. Pathol. 92:202–210.
18. Elliot, S. J., M. Karl, M. Berho, M. Potier, F. Zheng, B. Leclercq, et al. 2003. Estrogen deficiency accelerates progression of glomerulosclerosis in susceptible mice. Am. J. Pathol. 162:1441–1448.
19. Everitt, A. V., J. R. Wyndham, and D. L. Barnard. 1983. The anti-aging action of hypophysectomy in hypothalamic obese rats: effects on collagen aging, age-associated proteinuria development and renal histopathology. Mech. Ageing Dev. 22:233–251.
20. Gerondakis, S., T. S. Fulford, N. L. Messina, and R. J. Grumont. 2014. NF-kappaB control of T cell development. Nat. Immunol. 15:15–25.
21. Gerritsen, K. G., H. P. Peters, T. Q. Nguyen, M. P. Koeners, J. F. Wetzels, J. A. Joles, et al. 2010. Renal proximal tubular dysfunction is a major determinant of urinary connective tissue growth factor excretion. Am. J. Physiol. Renal. Physiol. 298:F1457–F1464.
22. Gorriz, J. L., and A. Martinez-Castelao. 2012. Proteinuria: detection and role in native renal disease progression. Transplant. Rev. (Orlando) 26:3–13.
23. Hinton, H. J., and M. J. Welham. 1999. Cytokine-induced protein kinase B activation and Bad phosphorylation do not correlate with cell survival of hemopoietic cells. J. Immunol. 162:7002–7009.
24. Joles, J. A., and L. Poston. 2010. Can exercise prevent preeclampsia? J. Hypertens. 28:2384–2385.
25. Joles, J. A., D. V. Sculley, and S. C. Langley-Evans. 2010a. Proteinuria in aging rats due to low-protein diet during mid-gestation. J. Dev. Orig. Health Dis. 1:75–83.
26. Joles, J. A., S. Wesseling, and B. Braam. 2010b. Renal glutathione S-transferase mu type 1 expression is already reduced in new-born spontaneously hypertensive rats. J. Hypertens. 28:633–634; author reply 634.
27. Jung, D., H. Biggs, J. Erikson, and P. U. Ledyard. 1975. New Colorimetric reaction for end-point, continuous-flow, and kinetic measurement of urea. Clin. Chem. 21:1136–1140.
28. Koeners, M. P., B. Braam, D. M. van der Giezen, R. Goldschmeding, and J. A. Joles. 2010. Perinatal micronutrient supplements ameliorate hypertension and proteinuria in adult fawn-hooded hypertensive rats. Am. J. Hypertens. 23:802–808.
29. Langley, S. C., and A. A. Jackson. 1994. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin. Sci. (Lond.) 86:217–222; discussion 121.
30. Langley-Evans, S. C., and D. V. Sculley. 2005. Programming of hepatic antioxidant capacity and oxidative injury in the ageing rat. Mech. Ageing Dev. 126:804–812.
31. Langley-Evans, S. C., G. J. Phillips, and A. A. Jackson. 1994. In utero exposure to maternal low protein diets induces hypertension in weanling rats, independently of maternal blood pressure changes. Clin. Nutr. 13:319–324.
32. Langley-Evans, S. C., S. J. Welham, and A. A. Jackson. 1999. Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 64:965–974.
33. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.
34. Macova, M., I. Armando, J. Zhou, G. Baiardi, D. Tyurmin, I. M. Larrayoz-Roldan, et al. 2008. Estrogen reduces aldosterone, upregulates adrenal angiotensin II AT2 receptors and normalizes adrenomedullary Fra-2 in ovariectomized rats. Neuroendocrinology 88:276–286.
35. Mazairac, A. H., and J. A. Joles. 2010. Renal sinus adiposity and hypertension. Hypertension 56:814–815.
36. McGrath, J. J., and J. L. Welham. 1999. Season of birth and schizophrenia: a systematic review and meta-analysis of data from the Southern Hemisphere. Schizophr. Res. 35:237–242.
37. McMullen, S., and S. C. Langley-Evans. 2005a. Maternal low- protein diet in rat pregnancy programs blood pressure through sex-specific mechanisms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:R85–R90.
38. McMullen, S., and S. C. Langley-Evans. 2005b. Sex-specific effects of prenatal low-protein and carbenoxolone exposure on renal angiotensin receptor expression in rats. Hypertension 46:1374–1380.
39. McMullen, S., D. S. Gardner, and S. C. Langley-Evans. 2004. Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br. J. Nutr. 91:133–140.
40. Miyata, N., F. Park, X. F. Li, and A. W. Jr Cowley. 1999. Distribution of angiotensin AT1 and AT2 receptor subtypes in the rat kidney. Am. J. Physiol. 277:F437–F446.
41. Poggio, E. D., A. D. Rule, R. Tanchanco, S. Arrigain, R. S. Butler, T. Srinivas, et al. 2009. Demographic and clinical characteristics associated with glomerular filtration rates in living kidney donors. Kidney Int. 75:1079–1087.
42. Potier, M., S. J. Elliot, I. Tack, O. Lenz, G. E. Striker, L. J. Striker, et al. 2001. Expression and regulation of estrogen receptors in mesangial cells: influence on matrix metalloproteinase-9. J. Am. Soc. Nephrol. 12:241–251.
43. Roesch, D. M. 2006. Effects of selective estrogen receptor agonists on food intake and body weight gain in rats. Physiol. Behav. 87:39–44.
44. Rule, A. D., H. Amer, L. D. Cornell, S. J. Taler, F. G. Cosio, W. K. Kremers, et al. 2010. The association between age and nephrosclerosis on renal biopsy among healthy adults. Ann. Intern. Med. 152:561–567.
45. Sahajpal, V., and N. Ashton. 2003. Renal function and angiotensin AT1 receptor expression in young rats following intrauterine exposure to a maternal low-protein diet. Clin. Sci. (Lond.) 104:607–614.
46. Sahajpal, V., and N. Ashton. 2005. Increased glomerular angiotensin II binding in rats exposed to a maternal low protein diet in utero. J. Physiol. 563:193–201.
47. Sasser, J. M., O. Akinsiku, N. C. Moningka, K. Jerzewski, C. Baylis, A. J. LeBlanc, et al. 2012. Sexual dimorphism in development of kidney damage in aging Fischer-344 rats. Gend. Med. 9:219–231.
48. Schreuder, M. F., and J. Nauta. 2007. Prenatal programming of nephron number and blood pressure. Kidney Int. 72:265–268.
49. Sherman, R. C., and S. C. Langley-Evans. 1998. Early administration of angiotensin-converting enzyme inhibitor captopril, prevents the development of hypertension programmed by intrauterine exposure to a maternal low- protein diet in the rat. Clin. Sci. (Lond.) 94:373–381.
50. Sherman, R. C., and S. C. Langley-Evans. 2000. Antihypertensive treatment in early postnatal life modulates prenatal dietary influences upon blood pressure in the rat. Clin. Sci. (Lond.) 98:269–275.
51. Swali, A., S. McMullen, H. Hayes, L. Gambling, H. J. McArdle, and S. C. Langley-Evans. 2011. Cell cycle regulation and cytoskeletal remodelling are critical processes in the nutritional programming of embryonic development. PLoS ONE 6:e23189
52. Vanhaesebroeck, B., K. Higashi, C. Raven, M. Welham, S. Anderson, P. Brennan, et al. 1999. Autophosphorylation of p110delta phosphoinositide 3-kinase: a new paradigm for the regulation of lipid kinases in vitro and in vivo. EMBO J. 18:1292–1302.
53. Vazquez, E., I. Coronel, R. Bautista, E. Romo, C. M. Villalon, M. C. Avila-Casado, et al. 2005. Angiotensin II-dependent induction of AT(2) receptor expression after renal ablation. Am. J. Physiol. Renal. Physiol. 288:F207–F213.
54. Wegorzewska, I. N., K. Walters, M. J. Weiser, D. F. Cruthirds, E. Ewell, D. O. Larco, et al. 2008. Postovariectomy weight gain in female rats is reversed by estrogen receptor alpha agonist, propylpyrazoletriol. Am. J. Obstet. Gynecol. 199:67 e61-65.
55. Wiggins, J. E., S. R. Patel, K. A. Shedden, M. Goyal, B. L. Wharram, S. Martini, et al. 2010. NFkappaB promotes inflammation, coagulation, and fibrosis in the aging glomerulus. J. Am. Soc. Nephrol. 21:587–597.
56. Woods, L. L., J. R. Ingelfinger, J. R. Nyengaard, and R. Rasch. 2001. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr. Res. 49:460–467.
57. Wyndham, J. R., A. V. Everitt, A. Eyland, and J. Major. 1987. Inhibitory effect of hypophysectomy and food restriction on glomerular basement membrane thickening, proteinuria and renal enlargement in aging male Wistar rats. Arch. Gerontol. Geriatr. 6:323–337.
58. Yin, Q., G. H. Kelsall, D. J. Vaughan, and N. J. Welham. 1999. Rotating Ring (Pt)-Disc (FeS2) Electrode Behavior in Hydrochloric Solutions. J. Colloid Interface Sci. 210:375–383.
59. Zheng, F., Q. L. Cheng, A. R. Plati, S. Q. Ye, M. Berho, A. Banerjee, et al. 2004. The glomerulosclerosis of aging in females: contribution of the proinflammatory mesangial cell phenotype to macrophage infiltration. Am. J. Pathol. 165:1789–1798.