Hostname: page-component-848d4c4894-v5vhk Total loading time: 0 Render date: 2024-06-20T04:02:37.918Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal resistance to diet-induced obesity partially protects newborn and post-weaning male mice offspring from metabolic disturbances

Published online by Cambridge University Press:  07 October 2020

Laís Angélica de Paula Simino Open the ORCID record for Laís Angélica de Paula Simino [Opens in a new window] ,
Carolina Panzarin Open the ORCID record for Carolina Panzarin [Opens in a new window] ,
Marcio Alberto Torsoni Open the ORCID record for Marcio Alberto Torsoni [Opens in a new window] ,
Letícia Martins Ignácio-Souza Open the ORCID record for Letícia Martins Ignácio-Souza [Opens in a new window] ,
Marciane Milanski Open the ORCID record for Marciane Milanski [Opens in a new window]  and
Adriana Souza Torsoni Open the ORCID record for Adriana Souza Torsoni [Opens in a new window]
Laís Angélica de Paula Simino
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Carolina Panzarin
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Marcio Alberto Torsoni
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Letícia Martins Ignácio-Souza
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Marciane Milanski
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
Adriana Souza Torsoni*
Affiliation:
Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil
*
Address for correspondence: Adriana Souza Torsoni, Laboratory of Metabolic Disorders, School of Applied Sciences, University of Campinas – UNICAMP, Limeira, São Paulo, Brazil. Email: atorsoni@unicamp.br
Get access Rights & Permissions [Opens in a new window]

Abstract

The rising rate of childhood overweight follows the increase in maternal obesity, since perinatal events impact offspring in a diversity of metabolic disorders. Despite many studies that have linked dietary consumption, overnutrition, or maternal obesity as the mediators of fetal metabolic programming, there are gaps regarding the knowledge about the contribution of different maternal phenotypes to the development of metabolic disturbances in offspring. This study aimed to investigate whether maternal high-fat diet (HFD) consumption without the development of the obese phenotype would protect offspring from metabolic disturbances. Female mice were fed standard chow diet or a HFD for 4 weeks before mating. HFD females were classified into obesity-resistant (OR) or obesity-prone (OP), according to weight gain. OP females presented with higher adiposity, fasting serum glucose and insulin, cholesterol and non-esterified fatty acid (NEFA). Newborn offspring from OP dams showed higher serum glucose and insulin and alteration in hepatic gene expression that may have contributed to the rise in hepatic fat content and decline of glycogen levels in the liver. Despite offspring from OR and OP females having showed similar growth after the day of delivery, offspring from OP females had higher caloric intake, fasting glucose, serum triglycerides and altered hepatic gene expression, as well as glucose and pyruvate intolerance and lower insulin sensitivity at d28 compared with offspring from OR females. Maternal pre-pregnancy serum glucose, insulin, and NEFA positively correlated with serum glucose and fat liver content and negatively correlated with hepatic glycogen in offspring. In conclusion, our results show that maternal resistance to diet-induced obesity partially protects offspring from early metabolic disturbances.

Keywords

Maternal programminghigh-fat dietobesity-resistantobesity-prone
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 4 , August 2021 , pp. 660 - 670
Check for updates
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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

World Health Organization. Obesity and overweight fact sheet 2016. Available at: http://www.who.int/mediacentre/factsheets/fs311/en/.Google Scholar
Brasil M da SS de V em SD de A de S de SM da SS de G. Vigitel Brasil 2018: vigilância de fatores de risco e proteção para doenças crônicas por inquerito telefônico: estimativas sobre frequência e distribuição sociodemográfica de fatores de proteção para doenças crônicas nas capitais dos 26 estados brasileiro. 2019. http://bvsms.saude.gov.br/bvs/publicacoes/vigitel_brasil_2011_fatores_risco_doencas_cronicas.pdf.CrossRefGoogle Scholar
Hu, Z, Tylavsky, FA, Han, JC, et al. Maternal metabolic factors during pregnancy predict early childhood growth trajectories and obesity risk: the CANDLE Study. Int J Obes. 2019; 43, 1914–1922.CrossRefGoogle ScholarPubMed
Nicholas, LM, Rattanatray, L, Maclaughlin, SM, et al. Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin-signaling pathways in the offspring. FASEB J. 2013; 27, 3786–3796.CrossRefGoogle ScholarPubMed
McCurdy, CE, Bishop, JM, Williams, SM, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009; 119, 323–335.Google ScholarPubMed
White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol – Regul Integr Comp Physiol. 2009; 296, 1464–1472.CrossRefGoogle ScholarPubMed
Frihauf, JB, Fekete, ÉM, Nagy, TR, Levin, BE, Zorrilla, EP. Maternal western diet increases adiposity even in male offspring of obesityresistant rat dams: early endocrine risk markers. Am J Physiol – Regul Integr Comp Physiol. 2016; 311, R1045–R1059.CrossRefGoogle ScholarPubMed
Benatti, RO, Melo, AM, Borges, FO, et al. Maternal high-fat diet consumption modulates hepatic lipid metabolism and microRNA-122 (miR-122) and microRNA-370 (miR-370) expression in offspring. Br J Nutr. 2014; 111, 2112–2122.CrossRefGoogle ScholarPubMed
de Paula Simino, LA, de Fante, T, Figueiredo Fontana, M, et al. Lipid overload during gestation and lactation can independently alter lipid homeostasis in offspring and promote metabolic impairment after new challenge to high-fat diet. Nutr Metab (Lond). 2017; 14, 16.CrossRefGoogle ScholarPubMed
Reginato, A, de Fante, T, Portovedo, M, et al. Autophagy proteins are modulated in the liver and hypothalamus of the offspring of mice with diet-induced obesity. J Nutr Biochem. 2016; 34, 30–41.CrossRefGoogle ScholarPubMed
Catalano, PM, Presley, L, Minium, J, de Mouzon, SH. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care. 2009; 32, 1076–1080.CrossRefGoogle ScholarPubMed
Saben, J, Lindsey, F, Zhong, Y, et al. Maternal obesity is associated with a lipotoxic placental environment. Placenta. 2014; 35, 171–177.CrossRefGoogle ScholarPubMed
Thorn, SR, Baquero, KC, Newsom, SA, et al. Early life exposure to maternal insulin resistance has persistent effects on hepatic NAFLD in juvenile nonhuman primates. Diabetes. 2014; 63, 2702–2713.CrossRefGoogle ScholarPubMed
Ashino, NG, Saito, KN, Souza, FD, et al. Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver. J Nutr Biochem. 2012; 23, 341–348.CrossRefGoogle ScholarPubMed
Melo, AM, Benatti, RO, Ignacio-Souza, LM, et al. Hypothalamic endoplasmic reticulum stress and insulin resistance in offspring of mice dams fed high-fat diet during pregnancy and lactation. Metabolism. 2014; 63, 682–692.CrossRefGoogle ScholarPubMed
Payolla, TB, Lemes, SF, de Fante, T, et al. High-fat diet during pregnancy and lactation impairs the cholinergic anti-inflammatory pathway in the liver and white adipose tissue of mouse offspring. Mol Cell Endocrinol. 2016; 422, 192–202.CrossRefGoogle ScholarPubMed
Fante, T, Simino, LA, Reginato, A, et al. Diet-induced maternal obesity alters insulin signalling in male mice offspring rechallenged with a high-fat diet in adulthood. PLoS One. 2016; 11, e0160184.CrossRefGoogle ScholarPubMed
Lemes, SF, de Souza, ACP, Payolla, TB, et al. Maternal consumption of high-fat diet in mice alters hypothalamic notch pathway, NPY cell population and food intake in offspring. Neuroscience. 2018; 371, 1–15.CrossRefGoogle ScholarPubMed
Locke, AE, Kahali, B, Berndt, SI, et al. Genetic studies of body mass index yield new insights for obesity biology. Nature. 2015; 518, 197–206.CrossRefGoogle ScholarPubMed
Yengo, L, Sidorenko, J, Kemper, KE, et al. Meta-analysis of genome-wide association studies for height and body mass index in ∼700000 individuals of European ancestry. Hum Mol Genet. 2018; 27, 3641–3649.CrossRefGoogle ScholarPubMed
Ranadive, SA, Vaisse, C. Lessons from extreme human obesity: monogenic disorders. Endocrinol Metab Clin North Am. 2008; 37, 733–751.CrossRefGoogle ScholarPubMed
Valassi, E, Scacchi, M, Cavagnini, F. Neuroendocrine control of food intake. Nutr Metab Cardiovasc Dis. 2008; 18, 158–168.CrossRefGoogle ScholarPubMed
Chambers, AP, Sandoval, DA, Seeley, RJ. Integration of satiety signals by the central nervous system. Curr Biol. 2013; 23, R379–R388.CrossRefGoogle ScholarPubMed
Moraes, JC, Coope, A, Morari, J, et al. High-fat diet induces apoptosis of hypothalamic neurons. PLoS One. 2009; 4, e5045.CrossRefGoogle ScholarPubMed
Boitard, C, Parkes, SL, Cavaroc, A, et al. Switching adolescent high-fat diet to adult control diet restores neurocognitive alterations. Front Behav Neurosci. 2016; 10, 225.CrossRefGoogle ScholarPubMed
Robison, LS, Albert, NM, Camargo, LA, et al. High-fat diet-induced obesity causes sex-specific deficits in adult hippocampal neurogenesis in mice. eNeuro. 2020; 7, 1–17.CrossRefGoogle ScholarPubMed
Milanski, M, Degasperi, G, Coope, A, et al. Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: Implications for the pathogenesis of obesity. J Neurosci. 2009; 29, 359–370.CrossRefGoogle ScholarPubMed
Souza, GFP, Solon, C, Nascimento, LF, et al. Defective regulation of POMC precedes hypothalamic inflammation in diet-induced obesity. Sci Rep. 2016; 6, 1–9.CrossRefGoogle ScholarPubMed
Desai, M, Jellyman, JK, Ross, MG. Epigenomics, gestational programming and risk of metabolic syndrome. Int J Obes (Lond). 2015; 39, 633–641.CrossRefGoogle ScholarPubMed
Desai, M, Beall, MB, Ross, MGR. Developmental origins of obesity. Int J Gynecol Obstet. 2013; 119, S236.Google Scholar
Parlee, SD, MacDougald, OA. Maternal nutrition and risk of obesity in offspring: the Trojan horse of developmental plasticity. Biochim Biophys Acta – Mol Basis Dis. 2014; 1842, 495–506.CrossRefGoogle ScholarPubMed
Chao, HW, Chao, SW, Lin, H, Ku, HC, Cheng, CF. Homeostasis of glucose and lipid in non-alcoholic fatty liver disease. Int J Mol Sci. 2019; 20, 298.CrossRefGoogle ScholarPubMed
Utzschneider, KM, Kahn, SE. Review: the role of insulin resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2006; 91, 4753–4761.CrossRefGoogle ScholarPubMed
Yki-Järvinen, H. Liver fat in the pathogenesis of insulin resistance and type 2 diabetes. Dig Dis. 2010; 28, 203–209.CrossRefGoogle ScholarPubMed
Zhou, Y, Peng, H, Xu, H, et al. Maternal diet intervention before pregnancy primes offspring lipid metabolism in liver. Lab Investig. 2020; 100, 553–569.CrossRefGoogle ScholarPubMed
Duan, Y, Sun, F, Que, S, Li, Y, Yang, S, Liu, G. Prepregnancy maternal diabetes combined with obesity impairs placental mitochondrial function involving Nrf2/ARE pathway and detrimentally alters metabolism of offspring. Obes Res Clin Pract. 2018; 12, 90–100.CrossRefGoogle ScholarPubMed
Monks, J, Orlicky, DJ, Stefanski, AL, et al. Maternal obesity during lactation may protect offspring from high fat diet-induced metabolic dysfunction. Nutr Diabetes. 2018; 8, 18.CrossRefGoogle ScholarPubMed
Wilcox, G. Insulin and insulin resistance. Clin Biochem Rev. 2005; 26, 19–39.Google ScholarPubMed
Karpe, F, Dickmann, JR, Frayn, KN. Fatty acids, obesity, and insulin resistance: time for a reevaluation. Diabetes. 2011; 60, 2441–2449.CrossRefGoogle Scholar
Isganaitis, E, Woo, M, Ma, H, et al. Developmental programming by maternal insulin resistance: hyperinsulinemia, glucose intolerance, and dysregulated lipid metabolism in male offspring of insulin-resistant mice. Diabetes. 2014; 63, 688–700.CrossRefGoogle ScholarPubMed
Keleher, MR, Zaidi, R, Shah, S, et al. Maternal high-fat diet associated with altered gene expression, DNA methylation, and obesity risk in mouse offspring. PLoS One. 2018; 13, 1–28.CrossRefGoogle ScholarPubMed
Seki, Y, Suzuki, M, Guo, X, et al. In utero exposure to a high-fat diet programs hepatic. Endocrinology. 2017; 158, 2860–2872.CrossRefGoogle ScholarPubMed
Ivanova, E, Chen, JH, Segonds-Pichon, A, Ozanne, SE, Kelsey, G. DNA methylation at differentially methylated regions of imprinted genes is resistant to developmental programming by maternal nutrition. Epigenetics. 2012; 7, 1200–1210.CrossRefGoogle Scholar
Supplementary material: File

Simino et al. supplementary material

Simino et al. supplementary material

Download Simino et al. supplementary material(File)
File 3.2 MB