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Maternal soy protein isolate diet during lactation programs deleterious effects on hepatic lipid metabolism, atherogenic indices, and function of adrenal in adult rat offspring

Published online by Cambridge University Press:  12 May 2021

Maíra Schuchter Ferreira Open the ORCID record for Maíra Schuchter Ferreira [Opens in a new window] ,
Sheila Cristina Potente Dutra Luquetti ,
Poliana Guiomar de Almeida Brasiel ,
Kacia Mateus ,
Alice Helena de Souza Paulino ,
Mayara Medeiros de Freitas Carvalho ,
Ana Eliza Andreazzi  and
Aline Silva de Aguiar
Maíra Schuchter Ferreira
Affiliation:
Postgraduate Program in Health and Nutrition, Federal University of Ouro Preto, Ouro Preto, MG, Brazil
Sheila Cristina Potente Dutra Luquetti*
Affiliation:
Department of Nutrition, Institute of Biological Sciences, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil
Poliana Guiomar de Almeida Brasiel
Affiliation:
Department of Nutrition, Institute of Biological Sciences, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil
Kacia Mateus
Affiliation:
Department of Nutrition, Institute of Biological Sciences, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil
Alice Helena de Souza Paulino
Affiliation:
Laboratory of Metabolic Biochemistry, Department of Biological Sciences, Federal University of Ouro Preto, Ouro Preto, MG, Brazil
Mayara Medeiros de Freitas Carvalho
Affiliation:
Laboratory of Metabolic Biochemistry, Department of Biological Sciences, Federal University of Ouro Preto, Ouro Preto, MG, Brazil
Ana Eliza Andreazzi
Affiliation:
Laboratory of Physiology, Department of Physiology, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil
Aline Silva de Aguiar
Affiliation:
Department of Nutrition, Institute of Biological Sciences, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil
*
Address for correspondence: Sheila Cristina Potente Dutra Luquetti, Department of Nutrition, Institute of Biological Sciences, Federal University of Juiz de Fora, Juiz de Fora, MG, Brazil. Email: [email protected]
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Abstract

The benefits of consuming soy and its protein have been reported in many studies. However, its phytoestrogen content raises concerns about consumption during lactation and gestation We therefore examined the effects of soybean or soy protein isolate on the parameters-related cardiovascular pathophysiology in lactating mothers and their offsprings at weaning and adulthood. Lactating rats were divided: casein control (C); soy protein isolate (SPI); and soybean (S). At weaning, half of the litter received commercial ration up to 150 days. The levels of 17-β-estradiol and superoxide dismutase were low in the S mothers. For the SPI mothers, we observed a reduction of thiobarbituric acid reactive substances (TBARS). At weaning, atherogenic indices [1 = total cholesterol (TC)/HDL; 2 = LDL/HDL; 3 = TC-HDL/HDL)] decreased in the S and SPI offsprings compared to the casein control group; TBARS and antioxidant enzymes increased in the S offspring, while reduced/oxidized glutathione ratio increased in the SPI offspring, indicating lower oxidative stress. In adulthood, the SPI offspring showed an increase in liver cholesterol and atherogenic index 1 and 3 (vs. C and S) and 2 (vs. S). In addition, we found a decrease in catecholamines in the adrenal medulla and an increase in caffeine-stimulated secretion, but tyrosine hydroxylase expression remained constant. Maternal consumption of SPI during lactation worsened atherogenic indices of the offsprings in adulthood, which was associated with increased liver cholesterol and decreased catecholamines in the adrenal medulla. Soy consumption had no consistent long-term effects on the evaluated parameters compared to casein consumption. The data suggest that the consumption of SPI during lactation should be done with caution.

Keywords

Soysoy protein isolatemetabolic programmingcatecholaminesantioxidants activity
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 2 , April 2022 , pp. 177 - 186
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Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Kostelac, D, Rechkemmer, G, Briviba, K. Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. J Agric Food Chem. 2003; 51, 7632–7635.CrossRefGoogle Scholar
Sucheta, S, Kaur, M, Goyal, R, Gill, BS. Physical characteristics and nutritional composition of some new soybean (Glycine max (L.) Merrill) genotypes. J Food Sci Technol. 2014; 51, 551–557.Google Scholar
Kuiper, GG, Lemmen, JG, Carlsson, B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocronology. 1998; 139, 4252–4263.CrossRefGoogle ScholarPubMed
Chang, EC, Charn, TH, Park, SH, et al. Estrogen receptors alpha and beta as determinants of gene expression: influence of ligand, dose, and chromatin binding. Mol Endocrinol. 2008; 22, 1032–1043.CrossRefGoogle ScholarPubMed
Mann, GE, Bonacasa, B, Ishii, T, Siow, RC. Targeting the redox sensitive Nrf2-Keap1 defense pathway in cardiovascular disease: protection afforded by dietary isoflavones. Curr Opin Pharmacol. 2009; 9, 139–145.CrossRefGoogle ScholarPubMed
Simmen, FA, Mercado, CP, Zavacki, AM, et al. Soy protein diet alters expression of hepatic genes regulating fatty acid and thyroid hormone metabolism in the male rat. J Nutr Bioquímica. 2010; 21, 1106–113.Google ScholarPubMed
Chi, XX, Zhang, T, Zhang, D, et al. Effects of isoflavones on lipid and apolipoprotein levels in patients with type 2 diabetes in Heilongjiang Province in China. J Clin BiochemNutr. 2016; 59, 134–138.Google ScholarPubMed
Yan, Z, Zhang, X, Li, C, Jiao, S, Dong, W. Association between consumption of soy and risk of cardiovascular disease: A meta-analysis of observational studies. Eur J PrevCardiol. 2017; 24, 735–747.Google ScholarPubMed
Qian, Y, Guan, T, Huang, M, et al. Neuroprotection by the soy isoflavone, genistein, via inhibition of mitochondria-dependent apoptosis pathways and reactive oxygen induced-NF-κB activation in a cerebral ischemia mouse model. Neurochem Int. 2012; 60, 759–767.CrossRefGoogle Scholar
Yoon, G, Parque, S. Antioxidant action of soy isoflavones on oxidative stress and antioxidant enzyme activities in exercised rats. Nutr Res Pract. 2014; 8, 618–624.CrossRefGoogle ScholarPubMed
Ruhlen, RL, Howdeshell, KL, Mao, J, et al. Low phytoestrogen levels in feed increase fetal serum estradiol resulting in the “fetal estrogenization syndrome” and obesity in cd-1 mice. Environ Health Perspect. 2008; 116, 322–328.CrossRefGoogle ScholarPubMed
Rosenfeld, CS. Homage to the ‘H’ in developmental origins of health and disease. J Dev Orig Health Dis. 2017; 8, 8–27.CrossRefGoogle Scholar
Vieira, AM, Brasiel, PGA, Ferreira, MS, Aguiar, AS, Luquetti, SCPD. Relationship between the consumption of soy and its derivatives during critical periods of development and in adulthood and endocrine-metabolic disorders. J Endocrinol Metab. 2017; 7, 135–140.CrossRefGoogle Scholar
Zinkhan, EK, Yu, B, Callaway, CW, McKnight, RA. Intrauterine growth restriction combined with a maternal high-fat diet increased adiposity and serum corticosterone levels in adult rat offspring. J Dev Orig Health Dis. 2018; 9, 315–328.CrossRefGoogle ScholarPubMed
Dutra-Tavares, AC, Silva, JO, Nunes-Freitas, AL, et al. Maternal undernutrition during lactation alters nicotine reward and DOPAC/dopamine ratio in cerebral cortex in adolescent mice, but does not affect nicotine-induced nAChRs upregulation. Int J Dev Neurosci. 2018; 65, 45–53.CrossRefGoogle Scholar
Rodrigues, AL, Moura, EG, Passos, MC, Dutra, SC, Lisboa, PC. Postnatal early overnutrition changes the leptin signaling pathway in the hypothalamic–pituitary–thyroid axis of young and adult rats. J Physiol. 2009; 587, 2647–2661.CrossRefGoogle ScholarPubMed
Jahan–Mihan, A, Smith, CE, Anderson, H. Effect of protein source in diets fed during gestation and lactation on food intake regulation in male offspring of Wistar rats. Am J Physiol Regul Integr Comp Physiol. 2011; 300, 1175–1184.CrossRefGoogle ScholarPubMed
Jahan-mihan, A, Szeto, IMY, Luhovyy, BL, Huot, PSP, Anderson, GH. Soya protein-and casein-based nutritionally complete diets fed during gestation and lactation differ in effects on characteristics of the metabolic syndrome in male offspring of Wistar rats. Br J Nutr. 2012; 107, 284–294.CrossRefGoogle ScholarPubMed
Desai, M, Jellyman, JK, Han, G, Lane, RH. Programmed regulation of rat offspring adipogenic transcription factor (PPARγ) by maternal nutrition. J Dev Orig Health Dis. 2015; 6, 530–538.CrossRefGoogle ScholarPubMed
Kaludjerovic, J, Ward, WE. Bone-specific gene expression patterns and whole bone tissue of female mice are programmed by early life exposure to soy isoflavones and folic acid. J NutrBiochem. 2015; 26, 1068–1076.Google Scholar
Peixoto, TC, Moura, EG, de Oliveira, E, et al. Cranberry (Vacciniummacrocarpon) extracttreatment improves triglyceridemia, livercholesterol, liversteatosis, oxidativedamage,andcorticosteronemia in ratsrenderedobesebya high-fat diet. Eur J Nutr. 2018; 57, 1829–1844.CrossRefGoogle Scholar
Vieira, AM, Brasiel, PGA, Ferreira, MS, et al. Maternal soybean diet during lactation alters breast milk composition and programs the lipid profile in adult male rat offspring. Endocrine. 2018; 60, 272–281.CrossRefGoogle ScholarPubMed
Brasiel, PGA, Ferreira, MS, Vieira, AM, et al. Maternal soy protein isolate diet during lactation programmes to higher metabolic risk in adult male offspring. Int J Food Sci Nutr. 2020; 1–11.Google Scholar
Fishbeck, KL, Rasmussen, KM. Effect of repeated cycles on maternal nutritional status, lactational performance, and litter growth in ad libitum-fed and chronically food-restricted rats. J Nutr. 1987; 117, 1967–1975.CrossRefGoogle Scholar
Reeves, PG, Nielsen, FH, Fahey, GC. 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, 1939–1951.CrossRefGoogle Scholar
Soares, LL, Lucas, AM, Boaventura, GT. Can organic and transgenic soy be used as a substitute for animal protein by rats? Braz J Med Biol Res. 2005; 38, 583–586.CrossRefGoogle ScholarPubMed
Association of official analytical chemists (AOAC): Official Methods of Analysis 14a ed. 1984.Google Scholar
Barbosa, ACL, Lajolo, FM, Genovese, MI. Isoflavone content and profile and antioxidant activity of soy and soy products. Ciênc Tecnol Aliment. 2006; 26, 921–926.CrossRefGoogle Scholar
Choi, JS, Suh, SS, Jovem, HS, Park, HJ. Hypolipemic and hypoglycemic activities of Prunus davidiana in high fat fed rats. Arch Pharm Res. 1991; 14, 44–47.CrossRefGoogle ScholarPubMed
Yang, RL, Shi, YH, Hao, G, Li, W, Le, GW. Increasing oxidative stress with progressive hyperlipidemia in human: the relation between malondialdehyde and atherogenic index. J Clin Biochem Nutr. 2008; 43, 154–158.CrossRefGoogle ScholarPubMed
Buege, JA, Aust, SD. Microsomal lipid peroxidation. Methods Enzymol. 1978; 52, 302–310.CrossRefGoogle ScholarPubMed
Griffith, OW. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem. 1980; 106, 207–212.CrossRefGoogle ScholarPubMed
Carlberg, I, Mannervik, B. Glutathione reductase. In Methods Enzymol (ed. Alton, M), 1985; 113, pp. 484–490. Academic Press. https://doi.org/10.1016/S0076-6879(85)13062-4.Google Scholar
Paglia, DE, Valentine, WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med. 1967; 70, 158–169.Google ScholarPubMed
Marklund, S, Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974; 47, 469–474.CrossRefGoogle Scholar
Aebi, H. Catalase in vitro. Methods Enzymol. 1984; 105, 121–126.CrossRefGoogle ScholarPubMed
Martins, AC, Souza, KL, Shio, MT, et al. Adrenal medullary function and expression of catecholamine-synthesizing enzymes in mice with hypothalamic obesity. Life Sci. 2004; 74, 3211–3222.CrossRefGoogle ScholarPubMed
Kelner, KL, Levine, RA, Morita, K, Pollard, HB. A comparison of trihydroxyindole and HPLC/electrochemical methods for catecholamines measurement in adrenal chromaffin cells. Neurochem Int. 1985; 7, 373–378.CrossRefGoogle ScholarPubMed
Trevenzoli, IH, Valle, MMR, Machado, FB, et al. Neonatal hyperleptinaemia programmes adrenal medullary function in adult rats: effects on cardiovascular parameters. J Physiol. 2007; 580, 629–637.CrossRefGoogle ScholarPubMed
Charan, J, Kantharia, ND. How to calculate sample size in animal studies? J Pharmacol Pharmacother. 2013; 4, 303–306.CrossRefGoogle ScholarPubMed
Yang, H, Lia, F, Xionga, X, et al. Soy isoflavones modulate adipokines and myokines to regulate lipid metabolism in adipose tissue, skeletal muscle, and liver of male Huanjiang mini-pigs. Mol Cell Endocrinol. 2012; 365, 44–51.CrossRefGoogle ScholarPubMed
Palacios-González, B, Zarain-Herzberg, A, Flores-Galiza, I, et al. Genistein stimulates fatty acid oxidation in a leptin receptor-independent manner through the JAK2-mediated phosphorylation and activation of AMPK in skeletal muscle. Biochimica et Biophysica Acta. 2014; 1841, 132–140.CrossRefGoogle Scholar
Torres, N, Torre-Villalvazo, I, Tovar, AR. Regulation of lipid metabolism by soy protein and its implication in diseases mediated by lipid disorders. J Nutr Biochem. 2006; 17, 365–73.CrossRefGoogle ScholarPubMed
Tovar, RA, Murguía, F, Cruz, C, et al. A Soy Protein Diet Alters Hepatic Lipid Metabolism Gene Expression and Reduces Serum Lipids and Renal Fibrogenic Cytokines in Rats with Chronic Nephrotic Syndrome. J Nutr. 2002; 132, 2562–2569.CrossRefGoogle ScholarPubMed
Han, A, Won, SB, Kwon, YH. Different Effects of Maternal Low-Isoflavone Soy Protein and Genistein Consumption on Hepatic Lipid Metabolism of 21-Day-Old Male Rat. Offspring. Nutrients. 2017; 9, 1039.CrossRefGoogle ScholarPubMed
Rizzello, CG, Tagluazucchi, D, Badini, E, et al. Bioactive peptides from vegetable food matrices. Research trends and novel biotechnologies for synthesis and recovery. J Funct Foods. 2016; 27, 549–569.CrossRefGoogle Scholar
Erba, D, Casiraghi, MC, Martinez-Conesa, C, Goi, L, Massaccesi, L. Isoflavone supplementation reduces DNA oxidative damage and increases O-β-N-acetyl-D-glucosaminidase activity in healthy women. Res Nutr. 2012; 32, 233–240.CrossRefGoogle ScholarPubMed
Javanbakht, MH, Sadria, R, Djalali, H, et al. Soy protein and genistein improves renal antioxidant status in experimental nephrotic syndrome. Nefrologia. 2014; 34, 483–490.Google ScholarPubMed
Lima, SMRR, Belló-Klein, A, Flues, K, et al. Efeitos da suplementação do 17β-estradiol no dano oxidativo cardíaco de ratas submetidas à privação dos hormônios ovarianos. Rev Bras Ginecol Obstet. 2007; 29, 27–33.CrossRefGoogle Scholar
Giacomini, MM, Hahn, S, Siqueira, LO. Análise de correlação do perfil lipídico e dano oxidativo em pacientes diabéticos. Rev Ciênc Farm BásicaApl. 2013; 34, 251–255.Google Scholar
Yoon, M, Won, SB, Kwon, YH. Altered lipid metabolism in rat offspring of dams fed a low-protein diet containing soy protein isolate. Life Sci. 2017; 147, 1–7.CrossRefGoogle Scholar
Smaranayaka, AGP, Li-Chan, ECY. Food-derived peptidic antioxidants: A review of their production, assessment, and potential application. J Funct Foods. 2011; 3, 229–254.CrossRefGoogle Scholar
Singh, BP, Vij, S, Hati, S. Functional significance of bioactive peptides derived from soybean. Peptides. 2014; 54, 171–179.CrossRefGoogle ScholarPubMed
Liu, M, Yanagihara, N, Toyohira, Y, et al. Dual effects of daidzein, a soy isoflavone, on catecholamine synthesis and secretion in cultured bovine adrenal medullary cells. Endocrinology. 2007; 148, 5348–5354.CrossRefGoogle ScholarPubMed
Yanagihara, N, Toyohira, Y, Shinohara, Y. Insights into the pharmacological potential of estrogens and phytoestrogens on catecholamine signaling. Ann NY Acad Sci. 2008; 1129, 96–104.CrossRefGoogle ScholarPubMed
Garcia, AG, García-De-Diego, AM, Gandía, L, Borges, R, García-Sancho, J. Calcium Signaling and Exocytosis in Adrenal Chromaffin Cells. Physiol Rev. 2006; 86, 1093–1131.CrossRefGoogle Scholar
Revankar, CM, Cimino, DF, Sklar, LA, Arterburn, JB, Prossnitz, ER. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005; 307, 1625–1630.CrossRefGoogle ScholarPubMed
Nilsson, B, Olde, B, Leeb-Lundberg, LMF. G protein-coupled oestrogen receptor 1 (GPER1)/GPR30: a new player in cardiovascular and metabolic oestrogenicsignalling. Br J Pharmacol. 2011; 163, 1131–1139.CrossRefGoogle Scholar
Hegazy, AM, Abdel-Azeem, AS, Zeidan, HM, Ibrahim, KS, SAyed EE. Hypolipidemic and hepatoprotective activities of rosemary and thyme in gentamicin-treated rats. Hum Exp Toxicol. 2018; 37, 420–430.CrossRefGoogle ScholarPubMed
Im, KH, Choi, J, Baek, SA, Lee, TS. Hyperlipidemic Inhibitory Effects of Phellinus pini in Rats Fed with a High Fat and Cholesterol Diet. Mycobiology. 2018; 46, 159–167.CrossRefGoogle ScholarPubMed
Halima, BH, Sonia, G, Sarra, K, et al. Apple Cider Vinegar Attenuates Oxidative Stress and Reduces the Risk of Obesity in High-Fat-Fed Male Wistar Rats. J Med Food. 2018; 21, 70–80.CrossRefGoogle ScholarPubMed
Passos, MCF, Ramos, FC, Mouço, T, Moura, EG. Increase of T3 secreted through the milk in protein restricted lactating rats. Nutr Res. 2001; 21, 917–924.CrossRefGoogle Scholar
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