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Maternal low-protein diet suppresses vascular and renal endothelial nitric oxide synthase phosphorylation in rat offspring independent of a postnatal fructose diet

Published online by Cambridge University Press:  16 March 2011

S. Sato ,
Y. Mukai  and
T. Norikura
S. Sato*
Affiliation:
Department of Nutrition, Aomori University of Health and Welfare, Aomori, Japan
Y. Mukai
Affiliation:
Department of Nutrition, Aomori University of Health and Welfare, Aomori, Japan
T. Norikura
Affiliation:
Department of Nutrition, Aomori University of Health and Welfare, Aomori, Japan
*
*Address for correspondence: Dr S. Sato, Department of Nutrition, Aomori University of Health and Welfare, Mase 58-1, Hamadate, Aomori 030-8505, Japan. (Email s_sato3@auhw.ac.jp)
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Abstract

We investigated the effects of a postnatal fructose diet on the programmed hypertension and vascular and renal dysfunction in offspring from dams exposed to protein restriction. Pregnant Wistar rats were fed control and low-protein diets during the gestation and suckling periods. From the end of lactation, male offspring received standard chow or a 60% fructose diet: a control diet in the gestation and suckling periods and a control diet from the end of lactation, control-on-control (CC), 60% fructose diet-on-control (CF), control-on-low-protein diet (LPC) and 60% fructose diet-on-low-protein diet (LPF). The systolic blood pressure (SBP) was measured during treatment. At postnatal days 94–101, urinary 24 h nitrate/nitrite (NOx) content, protein levels of endothelial nitric oxide synthase (eNOS) and mRNA levels of endothelin-1 (ET-1), and NAD(P)H oxidase subunits in the aorta and kidney were examined. The SBP at postnatal days 97–101 increased in CF (137 ± 2 mmHg, P < 0.05), LPC (135 ± 1 mmHg, P < 0.05) and LPF (141 ± 2 mmHg, P < 0.05), compared with CC (124 ± 1 mmHg). The urinary NOx contents and eNOS phosphorylation in the aorta and kidney of CF, LPC and LPF decreased when compared with CC. In the aorta, the mRNA levels of NAD(P)H oxidase subunits p47phox in LPC and ET-1 in LPC and LPF increased. These results indicate that maternal protein restriction elevated the blood pressure, the downregulated nitric oxide production and eNOS phosphorylation, whereas the postnatal fructose diet made no significant difference to these alterations.

Keywords

blood pressureendothelial nitric oxide synthasefructosematernal protein restrictionrat
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 2 , Issue 3 , June 2011 , pp. 168 - 175
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

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References

1. Barker, DJ, Bagby, SP, Hanson, MA. Mechanisms of disease: in utero programming in the pathogenesis of hypertension. Nat Clin Pract Nephrol. 2006; 2, 700–707.CrossRefGoogle ScholarPubMed
2. Lamireau, D, Nuyt, AM, Hou, X, et al. Altered vascular function in fetal programming of hypertension. Stroke. 2002; 33, 2992–2998.CrossRefGoogle ScholarPubMed
3. Tulassay, T, Vásárhelyi, B. Birth weight and renal function. Curr Opin Nephrol Hypertens. 2002; 11, 347–352.CrossRefGoogle ScholarPubMed
4. Curhan, GC, Willett, WC, Rimm, EB, et al. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation. 1996; 94, 3246–3250.CrossRefGoogle ScholarPubMed
5. Langley, SC, Jackson, AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond). 1994; 86, 217–222.CrossRefGoogle ScholarPubMed
6. Alexander, BT. Fetal programming of hypertension. Am J Physiol Regul Integr Comp Physiol. 2006; 290, R1–R10.CrossRefGoogle ScholarPubMed
7. Cambonie, G, Comte, B, Yzydorczyk, C, et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1236–R1245.CrossRefGoogle ScholarPubMed
8. Kawamura, M, Itoh, H, Yura, S, et al. Undernutrition in utero augments systolic blood pressure and cardiac remodeling in adult mouse offspring: possible involvement of local cardiac angiotensin system in developmental origins of cardiovascular disease. Endocrinology. 2007; 148, 1218–1225.CrossRefGoogle ScholarPubMed
9. Rocha, SO, Gomes, GN, Forti, AL, et al. Long-term effects of maternal diabetes on vascular reactivity and renal function in rat male offspring. Pediatr Res. 2005; 58, 1274–1279.CrossRefGoogle ScholarPubMed
10. McIntyre, M, Bohr, DF, Dominiczak, AF. Endothelial function in hypertension: the role of superoxide anion. Hypertension. 1999; 34, 539–545.CrossRefGoogle ScholarPubMed
11. Taniyama, Y, Griendling, KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension. 2003; 42, 1075–1081.CrossRefGoogle ScholarPubMed
12. Thorburn, AW, Storlien, LH, Jenkins, AB, et al. Fructose-induced in vivo insulin resistance and elevated plasma triglyceride levels in rats. Am J Clin Nutr. 1989; 49, 1155–1163.CrossRefGoogle ScholarPubMed
13. Sanchez-Lozada, LG, Tapia, E, Jimenez, A, et al. Fructose-induced metabolic syndrome is associated with glomerular hypertension and renal microvascular damage in rats. Am J Physiol Renal Physiol. 2007; 292, F423–F429.CrossRefGoogle ScholarPubMed
14. Brown, CM, Dulloo, AG, Yepuri, G, et al. Fructose ingestion acutely elevates blood pressure in healthy young humans. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R730–R737.CrossRefGoogle ScholarPubMed
15. Hwang, IS, Ho, H, Hoffman, BB, et al. Fructose-induced insulin resistance and hypertension in rats. Hypertension. 1987; 10, 512–516.CrossRefGoogle ScholarPubMed
16. Takagawa, Y, Berger, ME, Hori, MT, et al. Long-term fructose feeding impairs vascular relaxation in rat mesenteric arteries. Am J Hypertens. 2001; 14, 811–817.CrossRefGoogle ScholarPubMed
17. Johnson, RJ, Segal, MS, Sautin, Y, et al. Potential role of sugar (fructose) in the epidemic of hypertension, obesity and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am J Clin Nutr. 2007; 86, 899–906.Google ScholarPubMed
18. Wlodek, ME, Mibus, A, Tan, A, et al. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J Am Soc Nephrol. 2007; 18, 1688–1696.CrossRefGoogle ScholarPubMed
19. Kerr, S, Brosnan, MJ, McIntyre, M, et al. Superoxide anion production is increased in a model of genetic hypertension: role of the endothelium. Hypertension. 1999; 33, 1353–1358.CrossRefGoogle Scholar
20. Miatello, R, Risler, N, Castro, C, et al. Aortic smooth muscle cell proliferation and endothelial nitric oxide synthase activity in fructose-fed rats. Am J Hypertens. 2001; 14, 1135–1141.CrossRefGoogle ScholarPubMed
21. Zhao, CX, Xu, X, Cui, Y, et al. Increased endothelial nitric-oxide synthase expression reduces hypertension and hyperinsulinemia in fructose-treated rats. J Pharmacol Exp Ther. 2009; 328, 610–620.CrossRefGoogle ScholarPubMed
22. Rodford, JL, Torrens, C, Siow, RC, et al. Endothelial dysfunction and reduced antioxidant protection in an animal model of the developmental origins of cardiovascular disease. J Physiol. 2008; 586, 4709–4720.CrossRefGoogle Scholar
23. Torrens, C, Hanson, MA, Gluckman, PD, et al. Maternal undernutrition leads to endothelial dysfunction in adult male rat offspring independent of postnatal diet. Br J Nutr. 2009; 101, 27–33.CrossRefGoogle ScholarPubMed
24. Franco Mdo, C, Arruda, RM, Dantas, AP, et al. Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring. Cardiovasc Res. 2002; 56, 145–153.CrossRefGoogle ScholarPubMed
25. Nishimoto, Y, Tomida, T, Matsui, H, et al. Decrease in renal medullary endothelial nitric oxide synthase of fructose-fed, salt-sensitive hypertensive rats. Hypertension. 2002; 40, 190–194.CrossRefGoogle ScholarPubMed
26. Merezak, S, Reusens, B, Renard, A, et al. Effect of maternal low-protein diet and taurine on the vulnerability of adult Wistar rat islets to cytokines. Diabetologia. 2004; 47, 669–675.Google ScholarPubMed
27. Goosse, K, Bouckenooghe, T, Balteau, M, et al. Implication of nitric oxide in the increased islet-cells vulnerability of adult progeny from protein-restricted mothers and its prevention by taurine. J Endocrinol. 2009; 200, 177–187.CrossRefGoogle ScholarPubMed
28. Theys, N, Clippe, A, Bouckenooghe, T, et al. Early low protein diet aggravates unbalance between antioxidant enzymes leading to islet dysfunction. PLoS One. 2009; 4, e6110.CrossRefGoogle ScholarPubMed
29. Fleming, I, Busse, R. Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol. 2003; 284, R1–R12.CrossRefGoogle ScholarPubMed
30. Schulman, IH, Zhou, MS, Jaimes, EA, et al. Dissociation between metabolic and vascular insulin resistance in aging. Am J Physiol Heart Circ Physiol. 2007; 293, H853–H859.CrossRefGoogle ScholarPubMed
31. Motley, ED, Eguchi, K, Patterson, MM, et al. Mechanism of endothelial nitric oxide synthase phosphorylation and activation by thrombin. Hypertension. 2007; 49, 577–583.CrossRefGoogle ScholarPubMed
32. Franco, MC, Akamine, EH, Reboucas, N, et al. Long-term effects of intrauterine malnutrition on vascular function in female offspring: implications of oxidative stress. Life Sci. 2007; 80, 709–715.CrossRefGoogle ScholarPubMed
33. Roghair, RD, Segar, JL, Volk, KA, et al. Vascular nitric oxide and superoxide anion contribute to sex-specific programmed cardiovascular physiology in mice. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R651–R662.CrossRefGoogle ScholarPubMed