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Published in: European Journal of Nutrition 4/2016

01-06-2016 | Original Contribution

Grape skin extract-derived polyphenols modify programming-induced renal endowment in prenatal protein-restricted male mouse offspring

Authors: Mariana Ribeiro Costa, Karla Maria Pereira Pires, Mariane Nogueira Nalbones-Barbosa, Samuel dos Santos Valença, Ângela Castro Resende, Roberto Soares de Moura

Published in: European Journal of Nutrition | Issue 4/2016

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Abstract

Purpose

Protein-restricted diet during pregnancy is related to oxidative stress and, as a consequence, damage to nephrogenesis. We investigated the effects of vinifera grape skin extract (ACH09)-derived polyphenols on preserving renal morphology of maternal protein-restricted 1-day-old offspring.

Methods

Female C57/Bl-6 mice were fed two different isocaloric diets: control diet (19.3 % protein) and low-protein diet (6 % protein) with access to water or to the extract dissolved in drinking water (19.3 % protein plus ACH09 200 mg kg−1 day−1 and 6 % protein plus ACH09 200 mg kg−1 day−1) throughout gestation. Renal morphology—glomerular number N[glom]; renal maturity—vascular glomeruli and avascular glomeruli ratio (v–N[glom]/a-N[glom]); medullar and cortical volumes, as well as mean glomerular volume, were analyzed in male offspring. Hepatic superoxide dismutase and catalase (CAT) activities were evaluated, and renal lipid peroxidation levels were measured.

Results

Maternal protein restriction affected birth weight and naso-anal length in low-protein offspring compared to control and ACH09 restored both parameters. Protein restriction increased lipid peroxidation in kidney and liver and reduced CAT activity in low-protein group compared to control. Supplementation with ACH09 reduced the kidney oxidative damage and restored the antioxidant activity of CAT. ACH09 prevented glomerular loss and renal immaturity in the offspring.

Conclusion

The treatment of low-protein-fed dams during pregnancy with ACH09 provides protection from early-life deleterious renal morphological changes. The protective effect of ACH09 may involve antioxidant action and vasodilator effect of the extract.
Literature
1.
go back to reference Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35(7):595–601CrossRef Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35(7):595–601CrossRef
2.
go back to reference Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20CrossRef Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20CrossRef
3.
go back to reference Woods LL (2007) Maternal nutrition and predisposition to later kidney disease. Curr Drug Targets 8(8):906–913CrossRef Woods LL (2007) Maternal nutrition and predisposition to later kidney disease. Curr Drug Targets 8(8):906–913CrossRef
4.
go back to reference Hall SM, Zeman FJ (1968) Kidney function of the progeny of rats fed a low protein diet. J Nutr 95(1):49–54 Hall SM, Zeman FJ (1968) Kidney function of the progeny of rats fed a low protein diet. J Nutr 95(1):49–54
5.
go back to reference Zeman FJ (1968) Effects of maternal protein restriction on the kidney of the newborn young of rats. J Nutr 94(2):111–116 Zeman FJ (1968) Effects of maternal protein restriction on the kidney of the newborn young of rats. J Nutr 94(2):111–116
6.
go back to reference Nuyt AM (2008) Mechanisms underlying developmental programming of elevated blood pressure and vascular dysfunction: evidence from human studies and experimental animal models. Clin Sci 114(1):1–17CrossRef Nuyt AM (2008) Mechanisms underlying developmental programming of elevated blood pressure and vascular dysfunction: evidence from human studies and experimental animal models. Clin Sci 114(1):1–17CrossRef
7.
go back to reference Luo ZC, Fraser WD, Julien P, Deal CL, Audibert F, Smith GN, Xiong X, Walker M (2006) Tracing the origins of “fetal origins” of adult diseases: programming by oxidative stress? Med Hypotheses 66(1):38–44CrossRef Luo ZC, Fraser WD, Julien P, Deal CL, Audibert F, Smith GN, Xiong X, Walker M (2006) Tracing the origins of “fetal origins” of adult diseases: programming by oxidative stress? Med Hypotheses 66(1):38–44CrossRef
8.
go back to reference Cambonie G, Comte B, Yzydorczyk C, Ntimbane T, Germain N, Lê NL, Pladys P, Gauthier C, Lahaie I, Abran D, Lavoie JC, Nuyt AM (2007) 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 292(3):R1236–R1245CrossRef Cambonie G, Comte B, Yzydorczyk C, Ntimbane T, Germain N, Lê NL, Pladys P, Gauthier C, Lahaie I, Abran D, Lavoie JC, Nuyt AM (2007) 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 292(3):R1236–R1245CrossRef
9.
go back to reference Frankel EN et al (1993) Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet 341(8843):454–457CrossRef Frankel EN et al (1993) Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet 341(8843):454–457CrossRef
10.
go back to reference Madeira SV, de Castro Resende A, Ognibene DT, de Sousa MA, Soares de Moura R (2005) Mechanism of the endothelium-dependent vasodilator effect of an alcohol-free extract obtained from a vinifera grape skin. Pharmacol Res 52(4):321–327CrossRef Madeira SV, de Castro Resende A, Ognibene DT, de Sousa MA, Soares de Moura R (2005) Mechanism of the endothelium-dependent vasodilator effect of an alcohol-free extract obtained from a vinifera grape skin. Pharmacol Res 52(4):321–327CrossRef
11.
go back to reference Resende AC, Moura AS, Maradei MF (2007) Protective action of a hydroalcoholic extract of a vinifera grape skin on experimental preeclampsia in rats. Hypertens Pregnancy 26(1):89–100CrossRef Resende AC, Moura AS, Maradei MF (2007) Protective action of a hydroalcoholic extract of a vinifera grape skin on experimental preeclampsia in rats. Hypertens Pregnancy 26(1):89–100CrossRef
12.
go back to reference Madeira SV, Auger C, Anselm E, Chataigneau M, Chataigneau T, Soares de Moura R, Schini-Kerth VB (2009) eNOS activation induced by a polyphenol-rich grape skin extract in porcine coronary arteries. J Vasc Res 46(5):406–416CrossRef Madeira SV, Auger C, Anselm E, Chataigneau M, Chataigneau T, Soares de Moura R, Schini-Kerth VB (2009) eNOS activation induced by a polyphenol-rich grape skin extract in porcine coronary arteries. J Vasc Res 46(5):406–416CrossRef
13.
go back to reference Soares De Moura R, Costa Viana FS, Souza MA, Kovary K, Guedes DC, Oliveira EP, Rubenich LM, Carvalho LC, Oliveira RM, Tano T, Gusmão Correia ML (2002) Antihypertensive, vasodilator and antioxidant effects of a vinifera grape skin extract. J Pharm Pharmacol 54(11):1515–1520CrossRef Soares De Moura R, Costa Viana FS, Souza MA, Kovary K, Guedes DC, Oliveira EP, Rubenich LM, Carvalho LC, Oliveira RM, Tano T, Gusmão Correia ML (2002) Antihypertensive, vasodilator and antioxidant effects of a vinifera grape skin extract. J Pharm Pharmacol 54(11):1515–1520CrossRef
14.
go back to reference Resende AC, Emiliano AF, Cordeiro VS, de Bem GF, de Cavalho LC, de Oliveira PR, Neto ML, Costa CA, Boaventura GT, de Moura RS (2013) Grape skin extract protects against programmed changes in the adult rat offspring caused by maternal high-fat diet during lactation. J Nutr Biochem 24(12):2119–2126CrossRef Resende AC, Emiliano AF, Cordeiro VS, de Bem GF, de Cavalho LC, de Oliveira PR, Neto ML, Costa CA, Boaventura GT, de Moura RS (2013) Grape skin extract protects against programmed changes in the adult rat offspring caused by maternal high-fat diet during lactation. J Nutr Biochem 24(12):2119–2126CrossRef
15.
go back to reference Soares de Moura R, da Costa GF, Moreira AS, Queiroz EF, Moreira DD, Garcia-Souza EP, Resende AC, Moura AS, Teixeira MT (2012) Vitis vinifera L grape skin extract activates the insulin-signalling cascade and reduces hyperglycaemia in alloxan-induced diabetic mice. J Pharm Pharmacol 64(2):268–276CrossRef Soares de Moura R, da Costa GF, Moreira AS, Queiroz EF, Moreira DD, Garcia-Souza EP, Resende AC, Moura AS, Teixeira MT (2012) Vitis vinifera L grape skin extract activates the insulin-signalling cascade and reduces hyperglycaemia in alloxan-induced diabetic mice. J Pharm Pharmacol 64(2):268–276CrossRef
16.
go back to reference Wang H, Race EJ, Shrikhande AJ (2003) Characterization of anthocyanins in grape juices by ion trap liquid chromatography-mass spectrometry. J Agric Food Chem 51(7):1839–1844CrossRef Wang H, Race EJ, Shrikhande AJ (2003) Characterization of anthocyanins in grape juices by ion trap liquid chromatography-mass spectrometry. J Agric Food Chem 51(7):1839–1844CrossRef
17.
go back to reference Garcia-Beneytez EF, Cabello F, Revilla E (2003) Analysis of grape and wine anthocyanins by HPLC-MS. J Agric Food Chem 51(19):5622–5629CrossRef Garcia-Beneytez EF, Cabello F, Revilla E (2003) Analysis of grape and wine anthocyanins by HPLC-MS. J Agric Food Chem 51(19):5622–5629CrossRef
18.
go back to reference Reeves PG, Nielsen FH, Fahey GC (1993) 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 123(11):1939–1951 Reeves PG, Nielsen FH, Fahey GC (1993) 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 123(11):1939–1951
19.
go back to reference Woods LL, Ingelfinger JR, Rasch R (2005) Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol 289(4):R1131–R1136CrossRef Woods LL, Ingelfinger JR, Rasch R (2005) Modest maternal protein restriction fails to program adult hypertension in female rats. Am J Physiol Regul Integr Comp Physiol 289(4):R1131–R1136CrossRef
20.
go back to reference Koca R, Armutcu F, Altinyazar C, Gürel A. (2005) Evaluation of lipid peroxidation, oxidant/antioxidant status, and serum nitric oxide levels in alopecia areata. Med Sci Monit 11(6):CR296-CR299 Koca R, Armutcu F, Altinyazar C, Gürel A. (2005) Evaluation of lipid peroxidation, oxidant/antioxidant status, and serum nitric oxide levels in alopecia areata. Med Sci Monit 11(6):CR296-CR299
22.
go back to reference Bannister JV, Calabrese L (1987) Assays for superoxide dismutase. Methods Biochem Anal 32:279–312CrossRef Bannister JV, Calabrese L (1987) Assays for superoxide dismutase. Methods Biochem Anal 32:279–312CrossRef
23.
go back to reference Pires KM, Aguila MB, Mandarim-de-Lacerda CA (2006) Early renal structure alteration in rat offspring from dams fed low protein diet. Life Sci 79(22):2128–2134CrossRef Pires KM, Aguila MB, Mandarim-de-Lacerda CA (2006) Early renal structure alteration in rat offspring from dams fed low protein diet. Life Sci 79(22):2128–2134CrossRef
24.
go back to reference Jolicoeur P, Heusner AA (1986) Log-normal variation belts for growth curves. Biometrics 42(4):785–794CrossRef Jolicoeur P, Heusner AA (1986) Log-normal variation belts for growth curves. Biometrics 42(4):785–794CrossRef
25.
go back to reference Davis FC (1989) Daily variation in maternal and fetal weight gain in mice and hamsters. J Exp Zool 250(3):273–282CrossRef Davis FC (1989) Daily variation in maternal and fetal weight gain in mice and hamsters. J Exp Zool 250(3):273–282CrossRef
26.
go back to reference Rashid K, Sinha K, Sil PC (2013) An update on oxidative stress-mediated organ pathophysiology. Food Chem Toxicol 62:584–600CrossRef Rashid K, Sinha K, Sil PC (2013) An update on oxidative stress-mediated organ pathophysiology. Food Chem Toxicol 62:584–600CrossRef
27.
go back to reference Georgeson GD, Szony BJ, Streitman K, Varga IS, Kovács A, Kovács L, László A (2002) Antioxidant enzyme activities are decreased in preterm infants and in neonates born via caesarean section. Eur J Obstet Gynecol Reprod Biol 103(2):136–139CrossRef Georgeson GD, Szony BJ, Streitman K, Varga IS, Kovács A, Kovács L, László A (2002) Antioxidant enzyme activities are decreased in preterm infants and in neonates born via caesarean section. Eur J Obstet Gynecol Reprod Biol 103(2):136–139CrossRef
28.
go back to reference Fetoui H, Garoui M, Zeghal N (2009) Protein restriction in pregnant- and lactating rats-induced oxidative stress and hypohomocysteinaemia in their offspring. J Anim Physiol Anim Nutr 93(2):263–270CrossRef Fetoui H, Garoui M, Zeghal N (2009) Protein restriction in pregnant- and lactating rats-induced oxidative stress and hypohomocysteinaemia in their offspring. J Anim Physiol Anim Nutr 93(2):263–270CrossRef
29.
go back to reference Toescu V, Nuttall SL, Martin U, Kendall MJ, Dunne F (2002) Oxidative stress and normal pregnancy. Clin Endocrinol 57(5):609–613CrossRef Toescu V, Nuttall SL, Martin U, Kendall MJ, Dunne F (2002) Oxidative stress and normal pregnancy. Clin Endocrinol 57(5):609–613CrossRef
30.
go back to reference Pires KM, Valença SS, Resende ÂC, Porto LC, Queiroz EF, Moreira DD, de Moura RS (2011) Grape skin extract reduced pulmonary oxidative response in mice exposed to cigarette smoke. Med Sci Monit 17(8):BR87–BR195CrossRef Pires KM, Valença SS, Resende ÂC, Porto LC, Queiroz EF, Moreira DD, de Moura RS (2011) Grape skin extract reduced pulmonary oxidative response in mice exposed to cigarette smoke. Med Sci Monit 17(8):BR87–BR195CrossRef
31.
go back to reference Ashour MN, Salem SI, El-Gadban HM, Elwan NM, Basu TK (1999) Antioxidant status in children with protein-energy malnutrition (PEM) living in Cairo, Egypt. Eur J Clin Nutr 53(8):669–6673CrossRef Ashour MN, Salem SI, El-Gadban HM, Elwan NM, Basu TK (1999) Antioxidant status in children with protein-energy malnutrition (PEM) living in Cairo, Egypt. Eur J Clin Nutr 53(8):669–6673CrossRef
32.
go back to reference Schroder-van der Elst JP, van der Heide D, Rokos H, Morreale de Escobar G, Köhrle J (1998) Synthetic flavonoids cross the placenta in the rat and are found in fetal brain. Am J Physiol 274(2 Pt 1):E253–E256 Schroder-van der Elst JP, van der Heide D, Rokos H, Morreale de Escobar G, Köhrle J (1998) Synthetic flavonoids cross the placenta in the rat and are found in fetal brain. Am J Physiol 274(2 Pt 1):E253–E256
33.
go back to reference Langley-Evans SC, Welham SJ, Jackson AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64(11):965–974CrossRef Langley-Evans SC, Welham SJ, Jackson AA (1999) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 64(11):965–974CrossRef
34.
go back to reference Woods LL, Weeks DA, Rasch R (2004) Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 65(4):1339–1348CrossRef Woods LL, Weeks DA, Rasch R (2004) Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int 65(4):1339–1348CrossRef
35.
go back to reference Nwagwu MO, Cook A, Langley-Evans SC (2000) Evidence of progressive deterioration of renal function in rats exposed to a maternal low-protein diet in utero. Br J Nutr 83(1):79–85 Nwagwu MO, Cook A, Langley-Evans SC (2000) Evidence of progressive deterioration of renal function in rats exposed to a maternal low-protein diet in utero. Br J Nutr 83(1):79–85
36.
go back to reference de Moura RS, Miranda DZ, Pinto AC, Sicca RF, Souza MA, Rubenich LM, Carvalho LC, Rangel BM, Tano T, Madeira SV, Resende AC (2004) Mechanism of the endothelium-dependent vasodilation and the antihypertensive effect of Brazilian red wine. J Cardiovasc Pharmacol 44(3):302–309CrossRef de Moura RS, Miranda DZ, Pinto AC, Sicca RF, Souza MA, Rubenich LM, Carvalho LC, Rangel BM, Tano T, Madeira SV, Resende AC (2004) Mechanism of the endothelium-dependent vasodilation and the antihypertensive effect of Brazilian red wine. J Cardiovasc Pharmacol 44(3):302–309CrossRef
37.
go back to reference Kim CH (2013) Expression of extracellular superoxide dismutase protein in diabetes. Arch Plast Surg 40(5):517–521CrossRef Kim CH (2013) Expression of extracellular superoxide dismutase protein in diabetes. Arch Plast Surg 40(5):517–521CrossRef
Metadata
Title
Grape skin extract-derived polyphenols modify programming-induced renal endowment in prenatal protein-restricted male mouse offspring
Authors
Mariana Ribeiro Costa
Karla Maria Pereira Pires
Mariane Nogueira Nalbones-Barbosa
Samuel dos Santos Valença
Ângela Castro Resende
Roberto Soares de Moura
Publication date
01-06-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 4/2016
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-0963-5

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