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High maternal sodium intake alters sex-specific renal renin–angiotensin system components in newborn Wistar offspring

Published online by Cambridge University Press:  28 January 2016

D. R. R. Maia ,
K. L. Lopes ,
J. C. Heimann  and
L. N. S. Furukawa
D. R. R. Maia
Affiliation:
Laboratory of Experimental Hypertension, Department of Internal Medicine, Nephrology Division, University of São Paulo School of Medicine, Sao Paulo, Brazil
K. L. Lopes
Affiliation:
Laboratory of Experimental Hypertension, Department of Internal Medicine, Nephrology Division, University of São Paulo School of Medicine, Sao Paulo, Brazil
J. C. Heimann
Affiliation:
Laboratory of Experimental Hypertension, Department of Internal Medicine, Nephrology Division, University of São Paulo School of Medicine, Sao Paulo, Brazil
L. N. S. Furukawa*
Affiliation:
Laboratory of Experimental Hypertension, Department of Internal Medicine, Nephrology Division, University of São Paulo School of Medicine, Sao Paulo, Brazil
*
*Address for correspondence: L. N. S. Furukawa, Laboratory of Experimental Hypertension, Department of Internal Medicine, Nephrology Division, University of São Paulo School of Medicine, Av. Dr. Arnaldo, 455, 3° andar, sala 3342 São Paulo, SP 01246-903, Brazil. (Email luzia@usp.br)
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Abstract

This study aimed to evaluate the systemic and renal renin–angiotensin–aldosterone system (RAAS) at birth in male and female offspring and in mothers fed a high sodium diet (HSD) before and during gestation. Female Wistar rats were fed a HSD (8.0% NaCl) or a normal sodium diet (1.3% NaCl) from 8 weeks of age until delivery of their first litter. Maternal body weight, tail blood pressure, and food and water intake were evaluated. The litter sizes were assessed, and the body and kidney weights of the offspring were measured. Both mothers and offspring were euthanized immediately following the birth of the pups to evaluate plasma renin activity (PRA), renal renin content (RRC), renal angiotensin-converting enzyme (ACE) activity, renal angiotensin (Ang) II content, serum aldosterone (ALDO) levels, and renal cortical and medullary renin messenger RNA expression. In mothers in the HSD group, water intake and kidney mass were higher, whereas renal ACE activity, Ang II, PRA, ALDO and RRC were decreased. In the offspring of HSD-fed dams, the body and kidney mass were lower in both genders, renal ACE activity was lower in females and renal Ang II was lower in males. PRA, RRC, renin gene expression and ALDO levels did not differ between the groups of offspring. The data presented herein showed that a maternal HSD during pregnancy induces low birth weight and a sex-specific response in the RAAS in offspring.

Keywords

high sodium dietnewbornoffspringrenin–angiotensin–aldosterone system
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 3: Themed Issue: Ibero-American DOHaD Society , June 2016 , pp. 282 - 289
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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References

1. Kagami, S, Border, WA, Miller, DE, et al. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-b expression in rat glomerular mesangial cells. J Clin Invest. 1994; 93, 2431–2437.Google Scholar
2. Chen, Y, Lasaitiene, D, Friberg, P. The renin–angiotensin system in kidney development. Acta Physiol Scand. 2004; 181, 529–535.Google Scholar
3. Roberts, AB, McCune, BK, Sporn, MB. TGF-b: regulation of extracellular matrix. Kidney Int. 1992; 41, 557–559.Google Scholar
4. Thiery, JP, Duband, JL, Dufour, S, et al. Role of fibronectin in embryogenesis. In Biology of Extracellular Matrix: Fibronectin ((ed. Mosher DF), 1989; pp. 181–212. Academic Press: San Diego, CA.Google Scholar
5. Damkjær, M, Isaksson, GL, Stubbe, J, et al. Renal renin secretion as regulator of body fluid homeostasis. Eur J Physiol. 2013; 465, 153–165.Google Scholar
6. Bie, P. Blood volume, blood pressure and total body sodium: internal signalling and output control. Acta Physiol. 2009; 195, 187–196.Google Scholar
7. Graudal, NA, Galløe, AM, Garred, P. Effects of sodium restriction on blood pressure, renin, aldosterone, catecholamines, cholesterols, and triglycerides meta-analysis. JAMA. 1998; 279, 1383–1391.Google Scholar
8. Drenjančević-Perić, I, Jelaković, B, Lombard, JH, et al. High-salt diet and hypertension: focus on the renin-angiotensin system. Kidney Blood Press Res. 2011; 34, 1–11.Google Scholar
9. Cholewa, BC, Meister, CJ, Mattson, DL. Importance of the renin–angiotensin system in the regulation of arterial blood pressure in conscious mice and rats. Acta Physiol Scand. 2005; 183, 309–320.Google Scholar
10. He, FJ, MacGregor, GA. Salt, blood pressure and the renin-angiotensin system. J Renin Angiotensin Aldosterone Syst. 2003; 4, 11–16.Google Scholar
11. Contreras, RJ, Wong, DL, Henderson, R, et al. High dietary NaCl early in development enhances mean arterial pressure of adult rats. Physiol Behav. 2000; 71, 173–181.Google Scholar
12. Contreras, RJ. Differences in perinatal NaCl exposure alters blood pressure levels of adult rats. Am J Physiol. 1989; 256(Pt 2), R70–R77.Google Scholar
13. da Silva, AA, Noronha, LL, Oliveira, LB, et al. Renin angiotensin system function and blood pressure in adult rats after perinatal salt overload. Nutr Metab Cardiovasc Dis. 2003; 13, 133–139.Google Scholar
14. Swenson, SJ, Speth, RC, Porter, JP. Effect of a perinatal high-salt diet on blood pressure control mechanisms in young Sprague-Dawley rats. Am J Physiol Regul Integr Comp Physiol. 2004; 286, R764–R770.Google Scholar
15. Porter, JP, King, SH, Honeycutt, AD. Prenatal high-salt diet in the Sprague-Dawley rat programs blood pressure and heart rate hyperresponsiveness to stress in adult female offspring. Am J Physiol Regul Integr Comp Physiol. 2007; 293, R334–R342.Google Scholar
16. Ramos, DR, Costa, NL, Jang, KLL, et al. Maternal high-sodium intake alters the responsiveness of the renin–angiotensin system in adult offspring. Life Sci. 2012; 90, 785–792.Google Scholar
17. Ding, Y, Lv, J, Mao, C, et al. High-salt diet during pregnancy and angiotensin-related cardiac changes. J Hypertens. 2010; 28, 1290–1297.Google Scholar
18. Leandro, SM, Furukawa, LN, Shimizu, MH, et al. Low birth weight in response to salt restriction during pregnancy is not due to alterations in uterine-placental blood flow or the placental and peripheral renin–angiotensin system. Physiol Behav. 2008; 95, 5–51.Google Scholar
19. Jiménez, W, Martínez-Pardo, A, Arroyo, V, et al. Effect of the method of blood extraction on plasma levels of renin in the Wistar rat. Rev Esp Fisiol. 1985; 41, 299–303.Google Scholar
20. Schenk, HD, Radke, J, Ensink, FB, et al. Interactions between renal and general hemodynamics in fentanyl, droperidol, ketamine, thiopental and in peridural anesthesia animal studies. Anaesthesiol Reanim. 1995; 20, 60–70.Google Scholar
21. Giammattei, CE, Jack, WS, James, CR. Regulation of in vitro renin secretion by ANG II feedback manipulation in vivo in the ovine fetus. Am J Physiol. 1999; 277, R1230–R1238.Google Scholar
22. Santos, RA, Krieger, EM, Greene, LJ. An improved fluorimetric assay of rat serum and plasma converting enzyme. Hypertension. 1985; 7, 244–252.Google Scholar
23. Woods, LL, Ingelfinger, JR, Nyengaard, JR, et al. Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res. 2001; 49, 460–467.Google Scholar
24. Vaccari, B, Mesquita, FF, Jose, AR, et al. Fetal kidney programming by severe food restriction: effects on structure, hormonal receptor expression and urinary sodium excretion in rats. J Renin Angiotensin Aldosterone Syst. 2015; 16, 33–46.Google Scholar
25. Tufro-McReddie, A, Johns, DW, Geary, KM, et al. Angiotensin II type 1 receptor: role in renal growth and gene expression during normal development. Am J Physiol. 1994; 266(Pt 2), F911–F918.Google Scholar
26. Yosipiv, IV, El-Dahr, SS. Activation of angiotensin-generating systems in the developing rat kidney. Hypertension. 1996; 27, 281–286.Google Scholar
27. Yosipiv, IV, Dipp, S, El-Dahr, SS. Ontogeny of somatic angiotensin-converting enzyme. Hypertension. 1994; 23, 369–374.Google Scholar
28. Balbi, APC, Costa, RS, Coimbra, TM. Postnatal renal development of rats from mothers that received increased sodium intake. Pediatr Nephrol. 2004; 19, 1212–1218.Google Scholar
29. Coelho, MS, Passadore, MD, Gasparetti, AL, et al. High- or low-salt diet from weaning to adulthood: effect on body weight, food intake and energy balance in rats. Nutr Metab Cardiovasc Dis. 2006; 16, 148–155.Google Scholar
30. Lima, NKC, Lima, FB, Dos Santos, EA, et al. Effect of lifelong high- or low-salt intake on blood pressure, left ventricular mass and plasma insulin in Wistar rats. Am J Med Sci. 2006; 331, 309–314.Google Scholar
31. Lumbers, ER. Functions of the renin-angiotensin system during development. Clin Exp Pharmacol Physiol. 1995; 22, 499–505.Google Scholar
32. Berger, S, Bleich, M, Schmid, W, et al. Mineralocorticoid receptor knockout mice: pathophysiology of Na metabolism. Proc Natl Acad Sci. 1998; 95, 9424–9429.Google Scholar
33. Chevalier, RL, Thornhill, BA, Belmonte, DC, et al. Endogenous angiotensin II inhibits natriuresis following acute expansion in the neonatal rat. Am J Physiol Regul Integr Comp Physiol. 1996; 270, R393–R397.Google Scholar
34. Tufro-McReddie, A, Johns, DW, Geary, KM, et al. Angiotensin II type 1 receptor: role in renal growth and gene expression during normal development. Am J Physiol. 1994; 266, F911–F918.Google Scholar
35. Hazon, N, Henderson, IW. Effects of altered dietary sodium intake on hormonal profiles in salt-sensitive hypertensive rats. J Endocrinol. 1990; 127, 243–248.Google Scholar
36. Gray, CC, 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.Google Scholar
37. Kantorowicz, L, Valego, NK, Tang, L, et al. Plasma and renal renin concentrations in adult sheep after prenatal betamethasone exposure. Reprod Sci. 2008; 15, 831–838.Google Scholar
38. Woods, LL, Ingelfinger, JR, Rasch, R. Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol. 2005; 289, R1131–R1136.Google Scholar
39. Chandran, M, Phillips, S, Ciaraldi, T, et al. Adiponectin: more than just another fat cell? Diabetes Care. 2003; 26, 2442–2450.Google Scholar
40. Zhou, D, Pan, YX. Pathophysiological basis for compromised health beyond generations: role of maternal high fat diet and low grade chronic inflammation. J Nutr Biochem. 2015; 26, 1–8.Google Scholar
41. Drake, A, McPherson, R, Godfrey, K, et al. An unbalanced maternal diet in pregnancy associates with offspring epigenetic changes in genes controlling glucocorticoid action and foetal growth. Clin Endocrinol (Oxf). 2012; 77, 808–815.Google Scholar
42. Allard, C, Desgagn, V, Patenaude, J, et al. Mendelian randomization supports causality between maternal hyperglycemia and epigenetic regulation of leptin gene in newborns. Epigenetics. 2015; 10, 342–351.Google Scholar
43. Hiejmans, B, Tobi, E, Stein, A, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008; 105, 17046–17049.Google Scholar
44. Lopez, JP, Gomez, AD, Sotomayer, RA, Mantilla, GD, Lopez, LJ. Maternal undernutrition and cardiometabolic disease: a Latin American perspective. BMC Med. 2015; 13, 293.Google Scholar
45. Hales, CN, Barker, DJ, Clark, PMS, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303, 1019–1022.Google Scholar
46. Barker, DJ, Winter, PD, Osmond, C, et al. Weight in infancy and death from ischemic heart disease. Lancet. 1989; 2, 577–580.Google Scholar
47. Tarry-Adkins, JL, Ozanne, SE. Mechanisms of early life programming: current knowledge and future directions. Am J Clin Nutr. 2014; 94(Suppl.), 1765S–1771S.Google Scholar