Hostname: page-component-7c8c6479df-24hb2 Total loading time: 0 Render date: 2024-03-19T09:07:41.779Z Has data issue: false hasContentIssue false

High-fat diet consumption by male rat offspring of obese mothers exacerbates adipose tissue hypertrophy and metabolic alterations in adult life

Published online by Cambridge University Press:  22 November 2022

Guadalupe L. Rodríguez-González
Affiliation:
Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Sergio De Los Santos
Affiliation:
Unidad de Investigación en Obesidad, Facultad de Medicina, Universidad Nacional Autónoma de México & Subdirección de Investigación Clínica, Dirección de Investigación, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Dayana Méndez-Sánchez
Affiliation:
Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Luis A. Reyes-Castro
Affiliation:
Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Carlos A. Ibáñez
Affiliation:
Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Patricia Canto
Affiliation:
Unidad de Investigación en Obesidad, Facultad de Medicina, Universidad Nacional Autónoma de México & Subdirección de Investigación Clínica, Dirección de Investigación, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
Elena Zambrano*
Affiliation:
Biología de la Reproducción, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
*
*Corresponding author: Elena Zambrano, Email elena.zambranog@incmnsz.mx

Abstract

Obese mothers’ offspring develop obesity and metabolic alterations in adulthood. Poor postnatal dietary patterns also contribute to obesity and its comorbidities. We aimed to determine whether in obese mothers’ offspring an adverse postnatal environment, such as high-fat diet (HFD) consumption (second hit) exacerbates body fat accumulation, metabolic alterations and adipocyte size distribution. Female Wistar rats ate chow (C-5 %-fat) or HFD (maternal obesity (MO)-25 %-fat) from weaning until the end of lactation. Male offspring were weaned on either control (C/C and MO/C, maternal diet/offspring diet) or HFD (C/HF and MO/HF) diet. At 110 postnatal days, offspring were killed. Fat depots were excised to estimate adiposity index (AI). Serum glucose, triglyceride, leptin, insulin, insulin resistance index (HOMA-IR), corticosterone and dehydroepiandrosterone (DHEA) were determined. Adipocyte size distribution was evaluated in retroperitoneal fat. Body weight was similar in C/C and MO/C but higher in C/HF and MO/HF. AI, leptin, insulin and HOMA-IR were higher in MO/C and C/HF v. C/C but lower than MO/HF. Glucose increased in MO/HF v. MO/C. C/HF and MO/C had higher triglyceride and corticosterone than C/C, but lower corticosterone than MO/HF. DHEA and the DHEA/corticosterone ratio were lower in C/HF and MO/C v. C/C, but higher than MO/HF. Small adipocyte proportion decreased while large adipocyte proportions increased in MO/C and C/HF v. C/C and exacerbated in MO/HF v. C/HF. Postnatal consumption of a HFD by the offspring of obese mothers exacerbates body fat accumulation as well as the decrease of small and the increase of large adipocytes, which leads to larger metabolic abnormalities.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Nutrition Society

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

Chooi, YC, Ding, C & Magkos, F (2019) The epidemiology of obesity. Metabolism 92, 610.CrossRefGoogle ScholarPubMed
Crombie, IK, Irvine, L, Elliott, L, et al. (2009) Targets to tackle the obesity epidemic: a review of twelve developed countries. Public Health Nutr 12, 406413.Google ScholarPubMed
Marincova, L, Safarikova, S & Cahlikova, R (2020) Analysis of main risk factors contributing to obesity in the region of East Africa: meta-analysis. Afr Health Sci 20, 248256.CrossRefGoogle ScholarPubMed
Ng, M, Fleming, T, Robinson, M, et al. (2014) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384, 766781.CrossRefGoogle ScholarPubMed
Barquera, S, Campos-Nonato, I, Hernandez-Barrera, L, et al. (2013) Prevalence of obesity in Mexican adults 2000–2012. Salud Publica Mex 55, S151S160.CrossRefGoogle ScholarPubMed
INEGI-INSP (2019) National Survey of Health and Nutrition (ENSANUT) 2018. Salud Publica Mex.Google Scholar
Catalano, PM, Presley, L, Minium, J, et al. (2009) Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care 32, 10761080.CrossRefGoogle ScholarPubMed
De Los Santos, S, Reyes-Castro, LA, Coral-Vazquez, RM, et al. (2020) (-)-Epicatechin reduces adiposity in male offspring of obese rats. J Dev Orig Health Dis 11, 3743.CrossRefGoogle ScholarPubMed
Lindsay, KL, Brennan, L, Rath, A, et al. (2018) Gestational weight gain in obese pregnancy: impact on maternal and foetal metabolic parameters and birthweight. J Obstet Gynaecol 38, 6065.CrossRefGoogle ScholarPubMed
Rodriguez-Gonzalez, GL, Reyes-Castro, LA, Bautista, CJ, et al. (2019) Maternal obesity accelerates rat offspring metabolic ageing in a sex-dependent manner. J Physiol 597, 55495563.CrossRefGoogle Scholar
Tam, CHT, Ma, RCW, Yuen, LY, et al. (2018) The impact of maternal gestational weight gain on cardiometabolic risk factors in children. Diabetologia 61, 25392548.CrossRefGoogle ScholarPubMed
Vega, CC, Reyes-Castro, LA, Bautista, CJ, et al. (2015) Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes 39, 712719.CrossRefGoogle ScholarPubMed
Voerman, E, Santos, S, Patro Golab, B, et al. (2019) Maternal body mass index, gestational weight gain, and the risk of overweight and obesity across childhood: an individual participant data meta-analysis. PLoS Med 16, e1002744.CrossRefGoogle ScholarPubMed
Rodriguez-Gonzalez, GL, Castro-Rodriguez, DC & Zambrano, E (2018) Pregnancy and lactation: a window of opportunity to improve individual health. Meth Mol Biol 1735, 115144.CrossRefGoogle ScholarPubMed
Zambrano, E & Nathanielsz, PW (2013) Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies. Nutr Rev 71, S42S54.CrossRefGoogle ScholarPubMed
Barker, DJ (2007) The origins of the developmental origins theory. J Intern Med 261, 412417.CrossRefGoogle ScholarPubMed
Breton, C (2013) The hypothalamus-adipose axis is a key target of developmental programming by maternal nutritional manipulation. J Endocrinol 216, R19R31.CrossRefGoogle ScholarPubMed
Nathanielsz, P (2022) Life Before Birth: the Challenges of Fetal Development, 2nd ed. TX, USA: Life Course Health Press, LLC.Google Scholar
Wankhade, UD, Zhong, Y, Kang, P, et al. (2017) Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations. PLoS One 12, e0175675.CrossRefGoogle ScholarPubMed
Williams, L, Seki, Y, Vuguin, PM, et al. (2014) Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta 1842, 507519.CrossRefGoogle ScholarPubMed
Zheng, J, Zhang, L, Gao, Y, et al. (2022) The dynamic effects of maternal high-calorie diet on glycolipid metabolism and gut microbiota from weaning to adulthood in offspring mice. Front Nutr 9, 941969.CrossRefGoogle ScholarPubMed
Bariani, MV, Correa, F, Dominguez Rubio, AP, et al. (2020) Maternal obesogenic diet combined with postnatal exposure to high-fat diet induces metabolic alterations in offspring. J Cell Physiol 235, 82608269.CrossRefGoogle ScholarPubMed
Parente, LB, Aguila, MB & Mandarim-de-Lacerda, CA (2008) Deleterious effects of high-fat diet on perinatal and postweaning periods in adult rat offspring. Clin Nutr 27, 623634.CrossRefGoogle ScholarPubMed
Saullo, C, Cruz, LLD, Damasceno, DC, et al. (2022) Effects of a maternal high-fat diet on adipose tissue in murine offspring: a systematic review and meta-analysis. Biochimie 201, 1832.CrossRefGoogle ScholarPubMed
Sellayah, D, Thomas, H, Lanham, SA, et al. (2019) Maternal obesity during pregnancy and lactation influences offspring obesogenic adipogenesis but not developmental adipogenesis in mice. Nutrients 11, 495.CrossRefGoogle Scholar
Choe, SS, Huh, JY, Hwang, IJ, et al. (2016) Adipose tissue remodeling: its role in energy metabolism and metabolic disorders. Front Endocrinol 7, 30.CrossRefGoogle ScholarPubMed
Palomaki, VA, Koivukangas, V, Merilainen, S, et al. (2022) A straightforward method for adipocyte size and count analysis using open-source software QuPath. Adipocyte 11, 99107.CrossRefGoogle ScholarPubMed
Ibanez, CA, Vazquez-Martinez, M, Leon-Contreras, JC, et al. (2018) Different statistical approaches to characterization of adipocyte size in offspring of obese rats: effects of maternal or offspring exercise intervention. Front Physiol 9, 1571.CrossRefGoogle ScholarPubMed
Stenkula, KG & Erlanson-Albertsson, C (2018) Adipose cell size: importance in health and disease. Am J Physiol Regul Integr Comp Physiol 315, R284R295.CrossRefGoogle ScholarPubMed
Kajita, K, Mori, I, Kitada, Y, et al. (2013) Small proliferative adipocytes: identification of proliferative cells expressing adipocyte markers. Endocr J 60, 931939.CrossRefGoogle ScholarPubMed
Jo, J, Shreif, Z & Periwal, V (2012) Quantitative dynamics of adipose cells. Adipocyte 1, 8088.CrossRefGoogle ScholarPubMed
Grundy, D (2015) Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. Exp Physiol 100, 755758.CrossRefGoogle ScholarPubMed
Kilkenny, C, Browne, WJ, Cuthill, IC, et al. (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. J Pharmacol Pharmacother 1, 9499.CrossRefGoogle ScholarPubMed
Antunes, LC, Elkfury, JL, Jornada, MN, et al. (2016) Validation of HOMA-IR in a model of insulin-resistance induced by a high-fat diet in Wistar rats. Arch Endocrinol Metab 60, 138142.CrossRefGoogle Scholar
Cardiff, RD, Miller, CH & Munn, RJ (2014) Manual hematoxylin and eosin staining of mouse tissue sections. Cold Spring Harb Protoc 2014, 655658.CrossRefGoogle ScholarPubMed
Lecoutre, S, Deracinois, B, Laborie, C, et al. (2016) Depot- and sex-specific effects of maternal obesity in offspring’s adipose tissue. J Endocrinol 230, 3953.CrossRefGoogle ScholarPubMed
Armitage, JA, Poston, L & Taylor, PD (2008) Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res 36, 7384.CrossRefGoogle ScholarPubMed
Azoulay, L, Bouvattier, C & Christin-Maitre, S (2022) Impact of intra-uterine life on future health. Ann Endocrinol 83, 5458.CrossRefGoogle ScholarPubMed
Barker, DJ (1990) The fetal and infant origins of adult disease. BMJ 301, 1111.CrossRefGoogle ScholarPubMed
Barker, DJ (2004) The developmental origins of adult disease. J Am Coll Nutr 23, 588S595S.CrossRefGoogle ScholarPubMed
Barker, DJ & Osmond, C (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1, 10771081.CrossRefGoogle ScholarPubMed
Hales, CN & Barker, DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60, 520.CrossRefGoogle ScholarPubMed
Bray, GA & Popkin, BM (1998) Dietary fat intake does affect obesity! Am J Clin Nutr 68, 11571173.CrossRefGoogle ScholarPubMed
Buettner, R, Scholmerich, J & Bollheimer, LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity 15, 798808.CrossRefGoogle ScholarPubMed
Hariri, N & Thibault, L (2010) High-fat diet-induced obesity in animal models. Nutr Res Rev 23, 270299.CrossRefGoogle ScholarPubMed
Jequier, E (2002) Pathways to obesity. Int J Obes Relat Metab Disord 26, S12S17.CrossRefGoogle ScholarPubMed
Gaillard, R, Felix, JF, Duijts, L, et al. (2014) Childhood consequences of maternal obesity and excessive weight gain during pregnancy. Acta Obstet Gynecol Scand 93, 10851089.CrossRefGoogle ScholarPubMed
Reynolds, RM, Allan, KM, Raja, EA, et al. (2013) Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ 347, f4539.CrossRefGoogle ScholarPubMed
Zaborska, KE, Wareing, M, Edwards, G, et al. (2017) Loss of anti-contractile effect of perivascular adipose tissue in offspring of obese rats. Int J Obes 41, 997.CrossRefGoogle ScholarPubMed
Zambrano, E, Ibanez, C, Martinez-Samayoa, PM, et al. (2016) Maternal obesity: lifelong metabolic outcomes for offspring from poor developmental trajectories during the perinatal period. Arch Med Res 47, 112.CrossRefGoogle ScholarPubMed
Cervantes-Rodriguez, M, Martinez-Gomez, M, Cuevas, E, et al. (2014) Sugared water consumption by adult offspring of mothers fed a protein-restricted diet during pregnancy results in increased offspring adiposity: the second hit effect. Br J Nutr 111, 616624.CrossRefGoogle ScholarPubMed
Souza-Mello, V, Mandarim-de-Lacerda, CA & Aguila, MB (2007) Hepatic structural alteration in adult programmed offspring (severe maternal protein restriction) is aggravated by post-weaning high-fat diet. Br J Nutr 98, 11591169.CrossRefGoogle ScholarPubMed
Elahi, MM, Cagampang, FR, Mukhtar, D, et al. (2009) Long-term maternal high-fat feeding from weaning through pregnancy and lactation predisposes offspring to hypertension, raised plasma lipids and fatty liver in mice. Br J Nutr 102, 514519.CrossRefGoogle ScholarPubMed
Hsu, MH, Sheen, JM, Lin, IC, et al. (2020) Effects of maternal resveratrol on maternal high-fat diet/obesity with or without postnatal high-fat diet. Int J Mol Sci 21, 3428.CrossRefGoogle ScholarPubMed
DiGirolamo, M, Fine, JB, Tagra, K, et al. (1998) Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol 274, R1460R1467.Google ScholarPubMed
Gabriely, I, Ma, XH, Yang, XM, et al. (2002) Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: an adipokine-mediated process? Diabetes 51, 29512958.CrossRefGoogle ScholarPubMed
Matsuzawa, Y, Shimomura, I, Nakamura, T, et al. (1994) Pathophysiology and pathogenesis of visceral fat obesity. Diabetes Res Clin Pract 24, S111S116.CrossRefGoogle ScholarPubMed
Richard, AJ, White, U, , CM, et al. (2000) Adipose Tissue: Physiology to Metabolic Dysfunction. [Updated 2020 Apr 4]. In: Feingold KR, Anawalt B, Boyce A, et al., editors. Endotext [Internet]. South Dartmouth, MA: MDText.com, Inc. Available from: https://www.ncbi.nlm.nih.gov/books/NBK555602/ Google Scholar
Hwang, I & Kim, JB (2019) Two faces of white adipose tissue with heterogeneous adipogenic progenitors. Diabetes Metab J 43, 752762.CrossRefGoogle ScholarPubMed
Kusminski, CM, Bickel, PE & Scherer, PE (2016) Targeting adipose tissue in the treatment of obesity-associated diabetes. Nat Rev Drug Discov 15, 639660.CrossRefGoogle ScholarPubMed
McLaughlin, T, Sherman, A, Tsao, P, et al. (2007) Enhanced proportion of small adipose cells in insulin-resistant v. insulin-sensitive obese individuals implicates impaired adipogenesis. Diabetologia 50, 17071715.CrossRefGoogle Scholar
McLaughlin, T, Allison, G, Abbasi, F, et al. (2004) Prevalence of insulin resistance and associated cardiovascular disease risk factors among normal weight, overweight, and obese individuals. Metabolism 53, 495499.CrossRefGoogle ScholarPubMed
McLaughlin, T, Lamendola, C, Coghlan, N, et al. (2014) Subcutaneous adipose cell size and distribution: relationship to insulin resistance and body fat. Obesity 22, 673680.CrossRefGoogle ScholarPubMed
Fukuhara, S, Nakajima, H, Sugimoto, S, et al. (2019) High-fat diet accelerates extreme obesity with hyperphagia in female heterozygous Mecp2-null mice. PLoS One 14, e0210184.CrossRefGoogle ScholarPubMed
Palhinha, L, Liechocki, S, Hottz, ED, et al. (2019) Leptin Induces proadipogenic and proinflammatory signaling in adipocytes. Front Endocrinol 10, 841.CrossRefGoogle ScholarPubMed
Balland, E & Cowley, MA (2015) New insights in leptin resistance mechanisms in mice. Front Neuroendocrinol 39, 5965.CrossRefGoogle ScholarPubMed
Kirk, SL, Samuelsson, AM, Argenton, M, et al. (2009) Maternal obesity induced by diet in rats permanently influences central processes regulating food intake in offspring. PLoS One 4, e5870.CrossRefGoogle ScholarPubMed
Poher, AL, Arsenijevic, D, Asrih, M, et al. (2016) Preserving of postnatal leptin signaling in obesity-resistant Lou/C rats following a perinatal high-fat diet. PLoS One 11, e0162517.CrossRefGoogle ScholarPubMed
Bose, M, Olivan, B & Laferrere, B (2009) Stress and obesity: the role of the hypothalamic-pituitary-adrenal axis in metabolic disease. Curr Opin Endocrinol Diabetes Obes 16, 340346.CrossRefGoogle ScholarPubMed
Dallman, MF, la Fleur, SE, Pecoraro, NC, et al. (2004) Minireview: glucocorticoids--food intake, abdominal obesity, and wealthy nations in 2004. Endocrinology 145, 26332638.CrossRefGoogle ScholarPubMed
Zambrano, E, Reyes-Castro, LA, Rodriguez-Gonzalez, GL, et al. (2020) Aging endocrine and metabolic phenotypes are programmed by mother’s age at conception in a sex-dependent fashion in the rat. J Gerontol A Biol Sci Med Sci 75, 23042307.CrossRefGoogle Scholar
Balazs, Z, Schweizer, RA, Frey, FJ, et al. (2008) DHEA induces 11 -HSD2 by acting on CCAAT/enhancer-binding proteins. J Am Soc Nephrol 19, 92101.CrossRefGoogle ScholarPubMed