Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-21T14:20:09.689Z Has data issue: false hasContentIssue false

Branched-chain amino acid supplemented diet during maternal food restriction prevents developmental hypertension in adult rat offspring

Published online by Cambridge University Press:  28 January 2011

T. Fujii
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
S. Yura*
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency (JST), Saitama, Japan
K. Tatsumi
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
E. Kondoh
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
H. Mogami
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
K. Fujita
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
K. Kakui
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
S. Aoe
Affiliation:
Department of Home Economics, Otsuma Women's University, 12, Sanban-cho, Chiyoda-ku, Tokyo, Japan
H. Itoh
Affiliation:
Department of Obstetrics and Gynecology, Hamamatsu University, School of Medicine, Hamamatsu, Japan
N. Sagawa
Affiliation:
Department of Obstetrics and Gynecology, Mie University Graduate School of Medicine, Tsu, Japan
S. Fujii
Affiliation:
Department of Gynecology and Obstetrics, National Hospital Organization, Kyoto Medical Center, Kyoto, Japan
I. Konishi
Affiliation:
Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, Kyoto, Japan
*
*Address for correspondence: S. Yura, MD, PhD, Department of Gynecology and Obstetrics, Kyoto University Graduate School of Medicine, 54 Shogoin Kawahara-cho, Sakyo-ku, Kyoto 606-8507, Japan. (Email psuka@kuhp.kyoto-u.ac.jp)

Abstract

Maternal food restriction is known to cause developmental hypertension in offspring. We have previously shown that maternal high-protein diet can reverse fetal programming of hypertension and that branched-chain amino acid (BCAA) concentrations in maternal and fetal plasma were increased by maternal high-protein intake. Then, we hypothesized that isocaloric supplementation with BCAA to a maternal food restriction can reverse the adverse outcome. Pregnant rats were divided into four groups at 7.5 days postcoitum: normally nourished (NN) and 70% undernourished (UN) groups with and without BCAA supplementation (NN–standard diet (SD), NN–BCAA, UN–SD and UN–BCAA groups). Compared with pups in the NN groups, those in the UN–SD group had significantly increased systolic blood pressure (SBP) at 8 and 16 weeks of age (P < 0.05). However, the elevation of SBP was not observed in offspring in the UN–BCAA group. Offspring glomeruli number of the UN groups was significantly lower (P < 0.05) than that of the NN groups, independent of BCAA supplementation. Angiotensin II receptor type 2 (ATR2) mRNA and protein expression in the kidney was significantly augmented in the UN–BCAA group at 30 weeks of age. In conclusion, BCAA supplementation during maternal food restriction prevents developmental hypertension together with increased ATR2 expression in adult offspring kidney.

Type
Original Articles
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183187.Google Scholar
2. Langley-Evans, SC. Developmental programming of health and disease. Proc Nutr Soc. 2006; 65, 97105.Google Scholar
3. Brennan, KA, Olson, DM, Symonds, ME. Maternal nutrient restriction alters renal development and blood pressure regulation of the offspring. Proc Nutr Soc. 2006; 65, 116124.Google Scholar
4. Ozaki, T, Nishina, H, Hanson, MA, Poston, L. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol. 2001; 530, 141152.CrossRefGoogle ScholarPubMed
5. 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, 12181225.Google Scholar
6. Kawamura, M, Itoh, H, Yura, S, et al. Isocaloric high-protein diet ameliorates systolic blood pressure increase and cardiac remodeling caused by maternal caloric restriction in adult mouse offspring. Endocr J. 2009; 56, 679689.Google Scholar
7. Nair, KS, Short, KR. Hormonal and signaling role of branched-chain amino acids. J Nutr. 2005; 135, 1547S1552S.Google Scholar
8. Mogami, H, Yura, S, Itoh, H, et al. Isocaloric high-protein diet as well as branched-chain amino acids supplemented diet partially alleviates adverse consequences of maternal undernutrition on fetal growth. Growth Horm IGF Res. 2009; 19, 478485.Google Scholar
9. Langley-Evans, SC, Welham, SJ, Jackson, AA. Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 1999; 64, 965974.CrossRefGoogle ScholarPubMed
10. McMullen, S, Gardner, DS, Langley-Evans, SC. Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br J Nutr. 2004; 91, 133140.Google Scholar
11. Pham, TD, MacLennan, NK, Chiu, CT, et al. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol. 2003; 285, R962R970.Google Scholar
12. Singh, RR, Cullen-McEwen, LA, Kett, MM, et al. Prenatal corticosterone exposure results in altered AT1/AT2, nephron deficit and hypertension in the rat offspring. J Physiol. 2007; 579, 503513.Google Scholar
13. Vehaskari, VM, Aviles, DH, Manning, J. Prenatal programming of adult hypertension in the rat. Kidney Int. 2001; 59, 238245.Google Scholar
14. Woods, LL, Weeks, DA, Rasch, R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004; 65, 13391348.Google Scholar
15. Carey, RM, Padia, SH. Angiotensin AT2 receptors: control of renal sodium excretion and blood pressure. Trends Endocrinol Metab. 2008; 19, 8487.Google Scholar
16. Pladys, P, Lahaie, I, Cambonie, G, et al. Role of brain and peripheral angiotensin II in hypertension and altered arterial baroreflex programmed during fetal life in rat. Pediatr Res. 2004; 55, 10421049.Google Scholar
17. Bogdarina, I, Welham, S, King, PJ, Burns, SP, Clark, AJ. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ Res. 2007; 100, 520526.Google Scholar
18. Bassan, H, Trejo, LL, Kariv, N, et al. Experimental intrauterine growth retardation alters renal development. Pediatr Nephrol. 2000; 15, 192195.Google Scholar
19. Chevalier, RL, Goyal, S, Thornhill, BA. EGF improves recovery following relief of unilateral ureteral obstruction in the neonatal rat. J Urol. 1999; 162, 15321536.CrossRefGoogle ScholarPubMed
20. McVary, KT, Maizels, M. Urinary obstruction reduces glomerulogenesis in the developing kidney: a model in the rabbit. J Urol. 1989; 142, 646651; discussion 667–648.Google Scholar
21. Miyata, N, Park, F, Li, XF, Cowley, AW Jr. Distribution of angiotensin AT1 and AT2 receptor subtypes in the rat kidney. Am J Physiol. 1999; 277, F437F446.Google Scholar
22. Brawley, L, Itoh, S, Torrens, C, et al. Dietary protein restriction in pregnancy induces hypertension and vascular defects in rat male offspring. Pediatr Res. 2003; 54, 8390.Google Scholar
23. Holemans, K, Aerts, L, Van Assche, FA. Fetal growth restriction and consequences for the offspring in animal models. J Soc Gynecol Investig. 2003; 10, 392399.Google Scholar
24. Vickers, MH, Ikenasio, BA, Breier, BH. Adult growth hormone treatment reduces hypertension and obesity induced by an adverse prenatal environment. J Endocrinol. 2002; 175, 615623.Google Scholar
25. Krechowec, SO, Vickers, M, Gertler, A, Breier, BH. Prenatal influences on leptin sensitivity and susceptibility to diet-induced obesity. J Endocrinol. 2006; 189, 355363.Google Scholar
26. Hoy, WE, Hughson, MD, Bertram, JF, Douglas-Denton, R, Amann, K. Nephron number, hypertension, renal disease, and renal failure. J Am Soc Nephrol. 2005; 16, 25572564.Google Scholar
27. Wlodek, ME, Westcott, K, Siebel, AL, Owens, JA, Moritz, KM. Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 2008; 74, 187195.Google Scholar
28. 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, 16881696.Google Scholar
29. Zohdi, V, Moritz, KM, Bubb, KJ, et al. Nephrogenesis and the renal renin-angiotensin system in fetal sheep: effects of intrauterine growth restriction during late gestation. Am J Physiol Regul Integr Comp Physiol. 2007; 293, R1267R1273.Google Scholar
30. Hoppe, CC, Evans, RG, Bertram, JF, Moritz, KM. Effects of dietary protein restriction on nephron number in the mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1768R1774.CrossRefGoogle ScholarPubMed
31. Sahajpal, V, Ashton, N. Increased glomerular angiotensin II binding in rats exposed to a maternal low protein diet in utero. J Physiol. 2005; 563, 193201.Google Scholar
32. Vehaskari, VM, Stewart, T, Lafont, D, et al. Kidney angiotensin and angiotensin receptor expression in prenatally programmed hypertension. Am J Physiol Renal Physiol. 2004; 287, F262F267.Google Scholar
33. Ruiz-Ortega, M, Esteban, V, Suzuki, Y, et al. Renal expression of angiotensin type 2 (AT2) receptors during kidney damage. Kidney Int Suppl. 2003; 86, S21S26.Google Scholar
34. Ichiki, T, Kambayashi, Y, Inagami, T. Multiple growth factors modulate mRNA expression of angiotensin II type-2 receptor in R3T3 cells. Circ Res. 1995; 77, 10701076.CrossRefGoogle ScholarPubMed
35. Kambayashi, Y, Nagata, K, Ichiki, T, Inagami, T. Insulin and insulin-like growth factors induce expression of angiotensin type-2 receptor in vascular-smooth-muscle cells. Eur J Biochem. 1996; 239, 558565.Google Scholar
36. Floyd, JC Jr, Fajans, SS, Conn, JW, Knopf, RF, Rull, J. Stimulation of insulin secretion by amino acids. J Clin Invest. 1966; 45, 14871502.Google Scholar
37. Kimball, SR, Jefferson, LS. Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr. 2006; 136, 227S231S.Google Scholar
38. Tsutsumi, Y, Matsubara, H, Masaki, H, et al. Angiotensin II type 2 receptor overexpression activates the vascular kinin system and causes vasodilation. J Clin Invest. 1999; 104, 925935.Google Scholar
39. Li, H, Gao, Y, Grobe, JL, et al. Potentiation of the antihypertensive action of losartan by peripheral overexpression of the ANG II type 2 receptor. Am J Physiol Heart Circ Physiol. 2007; 292, H727H735.Google Scholar
40. Augustyniak, RA, Singh, K, Zeldes, D, Singh, M, Rossi, NF. Maternal protein restriction leads to hyper-responsiveness to stress and salt-sensitive hypertension in male offspring. Am J Physiol Regul Integr Comp Physiol. 2010; 298, R1375R1382.Google Scholar
41. Wenzel, UO, Krebs, C, Benndorf, R. The angiotensin II type 2 receptor in renal disease. J Renin Angiotensin Aldosterone Syst. 2010; 11, 3741.Google Scholar
42. Brawley, L, Torrens, C, Anthony, FW, et al. Glycine rectifies vascular dysfunction induced by dietary protein imbalance during pregnancy. J Physiol. 2004; 554, 497504.CrossRefGoogle ScholarPubMed
43. Tain, YL, Hsieh, CS, Lin, IC, et al. Effects of maternal L-citrulline supplementation on renal function and blood pressure in offspring exposed to maternal caloric restriction: the impact of nitric oxide pathway. Nitric Oxide. 2010; 23, 3441.CrossRefGoogle ScholarPubMed
44. Ogata, ES, Bussey, ME, Finley, S. Altered gas exchange, limited glucose and branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism. 1986; 35, 970977.Google Scholar
45. Cetin, I, Marconi, AM, Bozzetti, P, et al. Umbilical amino acid concentrations in appropriate and small for gestational age infants: a biochemical difference present in utero. Am J Obstet Gynecol. 1988; 158, 120126.Google Scholar
46. Hokken-Koelega, AC, De Ridder, MA, Lemmen, RJ, et al. Children born small for gestational age: do they catch up? Pediatr Res. 1995; 38, 267271.Google Scholar
Supplementary material: File

Yura Supplementary Material

Yura Supplementary Table

Download Yura Supplementary Material(File)
File 49.7 KB