Maternal High Sodium Diet Yields Kidney Alterations in Mice Offspring
DOI:
https://doi.org/10.12970/2310-984X.2014.02.02.4Keywords:
Wilms’ tumor suppressor gene, Podocin, Renal function, Offspring, Mice.Abstract
Background-Aims: We aimed to examine the effects of a maternal high-sodium diet in the kidney and blood pressure (BP) of the offspring. Materials and Methods: Beginning eight weeks before pregnancy, female mice received a diet containing either 0.25% sodium chloride (NaCl) - (standard chow, SC) or 4.0% NaCl (high-sodium, HS). Females were mated with male mice fed a SC diet. Their offspring were analyzed at three different ages: at birth, at day 10, and at three months. Results: Before mating, HS dams exhibited higher corticosterone levels and higher BP than the SC dams. At birth, neonatal mortality was higher in the offspring of HS dams than in those from SC dams. At three months of age, HS offspring compared to SC offspring, showed higher proteinuria and BP, greater glomerular sclerosis, and lower creatinine clearance, blood urea nitrogen clearance, and glomerular filtration rate. The fractional excretions of sodium, potassium, urea, and the protein expressions of the renin-angiotensin system (RAS) were higher in HS than in SC offspring, but AT2R, Wilms’ tumor suppressor gene (WT)1 and podocin were lower in HS than in SC offspring. Conclusion: The offspring exposed to a maternal diet with high sodium content shows glomerular sclerosis with consequent high blood pressure and a shift in the renal expression of proteins (WT1, podocin, and RAS) at maturity. Consequently, the renal function of the offspring deteriorates more quickly than offspring from mothers fed a standard sodium diet.References
[1] Almeida JR, Passos MA, Souza ER, Mandarim-De-Lacerda CA. Glomerular developmental chronology in human fetuses. J Cell Mol Med 2003; 7: 492-3. http://dx.doi.org/10.1111/j.1582-4934.2003.tb00253.x
[2] Garcia-Villalba P, Denkers ND, Wittwer CT, Hoff C, Nelson RD, Mauch TJ. Real-time PCR quantification of AT1 and AT2 angiotensin receptor mRNA expression in the developing rat kidney. Nephron Exp Nephrol 2003; 94: e154-9. http://dx.doi.org/10.1159/000072499
[3] Burrow CR. Regulatory molecules in kidney development. Pediatr Nephrol 2000; 14: 240-53. http://dx.doi.org/10.1007/s004670050049
[4] Barker DJ. In utero programming of chronic disease. Clin Sci (Lond) 1998; 95: 115-28. http://dx.doi.org/10.1042/CS19980019
[5] de Gusmao Correia ML, Volpato AM, Aguila MB, Mandarimde-Lacerda CA. Developmental origins of health and disease: experimental and human evidence of fetal programming for metabolic syndrome. J Hum Hypertens 2012; 26: 405-19. http://dx.doi.org/10.1038/jhh.2011.61
[6] Ferreira DN, Katayama IA, Oliveira IB, et al. Salt-induced cardiac hypertrophy and interstitial fibrosis are due to a blood pressure-independent mechanism in Wistar rats. J Nutr 2010; 140: 1742-51. http://dx.doi.org/10.3945/jn.109.117473
[7] Ogihara T, Asano T, Ando K, et al. High-salt diet enhances insulin signaling and induces insulin resistance in Dahl saltsensitive rats. Hypertension 2002; 40: 83-9. http://dx.doi.org/10.1161/01.HYP.0000022880.45113.C9
[8] Koleganova N, Piecha G, Ritz E, et al. Both high and low maternal salt intake in pregnancy alter kidney development in the offspring. Am J Physiol Renal Physiol 2011; 301: F344- 54. http://dx.doi.org/10.1152/ajprenal.00626.2010
[9] Ramos DR, Costa NL, Jang KL, et al. Maternal high-sodium intake alters the responsiveness of the renin-angiotensin system in adult offspring. Life Sci 2012; 90: 785-92. http://dx.doi.org/10.1016/j.lfs.2012.04.011
[10] Reeves PG, Nielsen FH, Fahey GC, Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993; 123: 1939-51.
[11] Hotchkiss AK, Vandenbergh JG. The anogenital distance index of mice (Mus musculus domesticus): an analysis. Contemp Top Lab Anim Sci 2005; 44: 46-8.
[12] Frantz ED, Penna-de-Carvalho A, Batista Tde M, Aguila MB, Mandarim-de-Lacerda CA. Comparative effects of the reninangiotensin system blockers on nonalcoholic fatty liver disease and insulin resistance in C57BL/6 mice. Metab Syndr Relat Disord 2014; 12: 191-201. http://dx.doi.org/10.1089/met.2013.0129
[13] Almeida JR, Mandarim-de-Lacerda CA. Maternal gestational protein-calorie restriction decreases the number of glomeruli and causes glomerular hypertrophy in adult hypertensive rats. Am J Obstet Gynecol 2005; 192: 945-51. http://dx.doi.org/10.1016/j.ajog.2004.09.010
[14] Nascimento FA, Ceciliano TC, Aguila MB, Mandarim-deLacerda CA. Maternal vitamin D deficiency delays glomerular maturity in F1 and F2 offspring. PLoS One 2012; 7: e41740. http://dx.doi.org/10.1371/journal.pone.0041740
[15] Chong E, Yosypiv IV. Developmental programming of hypertension and kidney disease. Int J Nephrol 2012; 2012: 760580. http://dx.doi.org/10.1155/2012/760580
[16] Gray C, Al-Dujaili EA, Sparrow AJ, et al. Excess maternal salt intake produces sex-specific hypertension in offspring: putative roles for kidney and gastrointestinal sodium handling. PLoS One 2013; 8: e72682. http://dx.doi.org/10.1371/journal.pone.0072682
[17] Mao C, Liu R, Bo L, et al. High-salt diets during pregnancy affected fetal and offspring renal renin-angiotensin system. J Endocrinol 2013; 218: 61-73. http://dx.doi.org/10.1530/JOE-13-0139
[18] Cao Z, Kelly DJ, Cox A, et al. Angiotensin type 2 receptor is expressed in the adult rat kidney and promotes cellular proliferation and apoptosis. Kidney Int 2000; 58: 2437-51. http://dx.doi.org/10.1046/j.1523-1755.2000.00427.x
[19] Jin K, Vaziri ND. Salt-sensitive hypertension in mitochondrial superoxide dismutase deficiency is associated with intrarenal oxidative stress and inflammation. Clin Exp Nephrol 2014; 18: 445-52. http://dx.doi.org/10.1007/s10157-013-0851-3
[20] Kett MM, Denton KM. Renal programming: cause for concern? Am J Physiol Regul Integr Comp Physiol 2011; 300: R791-803. http://dx.doi.org/10.1152/ajpregu.00791.2010
[21] Almond K, Bikker P, Lomax M, Symonds ME, Mostyn A. The influence of maternal protein nutrition on offspring development and metabolism: the role of glucocorticoids. Proc Nutr Soc 2012; 71: 198-203. http://dx.doi.org/10.1017/S0029665111003363
[22] Benigni A, Cassis P, Remuzzi G. Angiotensin II revisited: new roles in inflammation, immunology and aging. EMBO Mol Med 2010; 2: 247-57. http://dx.doi.org/10.1002/emmm.201000080
[23] Hayashi K, Sasamura H, Ishiguro K, Sakamaki Y, Azegami T, Itoh H. Regression of glomerulosclerosis in response to transient treatment with angiotensin II blockers is attenuated by blockade of matrix metalloproteinase-2. Kidney Int 2010; 78: 69-78. http://dx.doi.org/10.1038/ki.2010.81
[24] Alt JM, Hackbarth H, Deerberg F, Stolte H. Proteinuria in rats in relation to age-dependent renal changes. Lab Anim 1980; 14: 95-101. http://dx.doi.org/10.1258/002367780780942809
[25] Bhargava S, Jain A, Gupta V. Fractional excretion of sodium- -a simple test for the differential diagnosis of acute renal failure. Clin Nephrol 2002; 58: 79-80. http://dx.doi.org/10.5414/CNP58079
[26] Wyrwoll CS, Mark PJ, Waddell BJ. Developmental programming of renal glucocorticoid sensitivity and the reninangiotensin system. Hypertension 2007; 50: 579-84. http://dx.doi.org/10.1161/HYPERTENSIONAHA.107.091603
[27] Contreras RJ, Wong DL, Henderson R, Curtis KS, Smith JC. High dietary NaCl early in development enhances mean arterial pressure of adult rats. Physiol Behav 2000; 71: 173-81. http://dx.doi.org/10.1016/S0031-9384(00)00331-0
[28] Moritz KM, Wintour EM, Black MJ, Bertram JF, Caruana G. Factors influencing mammalian kidney development: implications for health in adult life. Adv Anat Embryol Cell Biol 2008; 196: 1-78.
[29] Lin L, Phillips WE, Manning RD. Intrarenal Angiotensin ii is associated with inflammation, renal damage and dysfunction in dahl salt-sensitive hypertension. J Amer Soc Hypert 2009; 3: 306-14. http://dx.doi.org/10.1016/j.jash.2009.08.002
[30] Li J, Zhao D, Ding J, et al. WT1 mutation and podocyte molecular expression in a Chinese Frasier syndrome patient. Pediatr Nephrol 2007; 22: 2133-6. http://dx.doi.org/10.1007/s00467-007-0579-y
[31] Ho J, Ng KH, Rosen S, Dostal A, Gregory RI, Kreidberg JA. Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J Am Soc Nephrol 2008; 19: 2069-75. http://dx.doi.org/10.1681/ASN.2008020162