Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-30T16:52:46.896Z Has data issue: false hasContentIssue false
  • English
  • Français

Exposure to maternal hyperglycemia and high-fat diet consumption after weaning in rats: repercussions on periovarian adipose tissue

Published online by Cambridge University Press:  03 December 2021

Carolina M. Saullo ,
Yuri K. Sinzato ,
Verônyca G. Paula ,
Franciane Q. Gallego ,
José E. Corrente ,
Isabela L. Iessi ,
Gustavo T. Volpato  and
Débora C. Damasceno Open the ORCID record for Débora C. Damasceno [Opens in a new window]
Carolina M. Saullo
Affiliation:
Laboratory of Experimental Research on Gynecology and Obstetrics, Postgraduate Course on Tocogynecology, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
Yuri K. Sinzato
Affiliation:
Laboratory of Experimental Research on Gynecology and Obstetrics, Postgraduate Course on Tocogynecology, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
Verônyca G. Paula
Affiliation:
Laboratory of Experimental Research on Gynecology and Obstetrics, Postgraduate Course on Tocogynecology, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
Franciane Q. Gallego
Affiliation:
Laboratory of Experimental Research on Gynecology and Obstetrics, Postgraduate Course on Tocogynecology, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
José E. Corrente
Affiliation:
Research Support Office, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
Isabela L. Iessi
Affiliation:
Laboratory of Experimental Research on Gynecology and Obstetrics, Postgraduate Course on Tocogynecology, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
Gustavo T. Volpato
Affiliation:
Laboratory of System Physiology and Reproductive Toxicology, Institute of Biological and Health Sciences, Federal University of Mato Grosso (UFMT), Barra do Garças, Mato Grosso, Brazil
Débora C. Damasceno*
Affiliation:
Laboratory of Experimental Research on Gynecology and Obstetrics, Postgraduate Course on Tocogynecology, Botucatu Medical School, Sao Paulo State University (Unesp), Botucatu, Sao Paulo, Brazil
*
Address for correspondence: Profa. Dra. Débora C. Damasceno, Laboratório de Pesquisa Experimental em Ginecologia e Obstetrícia, UNIPEX, Faculdade de Medicina de Botucatu, Unesp, Distrito de Rubião Júnior s/n, CEP 18610.879, Botucatu, Estado de São Paulo, Brasil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Clinical and epidemiological studies show that maternal hyperglycemia can change the programming of offspring leading to transgenerational effects. These changes may be related to environmental factors, such as high-fat diet (HFD) consumption, and contribute to the comorbidity onset at the adulthood of the offspring. The objective of this study was to evaluate the hyperglycemic intrauterine environment, associated or not with an HFD administered from weaning to adult life on the periovarian adipose tissue of rat offspring Maternal diabetes was chemically induced by Streptozotocin. Female offsprings were randomly distributed into four experimental groups (n = 5 animals/group): Female offspring from control or diabetic mothers and fed an HFD or standard diet. HFD was prepared with lard enrichment and given from weaning to adulthood. On day 120 of life, the rats were anesthetized and sacrificed to obtain adipose tissue samples. Then, the hyperglycemic intrauterine environment and HFD fed after weaning caused a higher body weight, total fat, and periovarian fat in adult offspring, which could compromise the future reproductive function of these females. These rats showed higher adiposity index and adipocyte area, contributing to hypertrophied adipose tissue. Therefore, maternal diabetes itself causes intergenerational changes and, in association with the HFD consumption after weaning, exacerbated the changes in the adipose tissue of adult female offspring.

Keywords

Diabetesobesityhigh-fat dietoffspringadipose tissue
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 5 , October 2022 , pp. 634 - 641
Check for updates
Copyright
© The Author(s), 2021. 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

Poston, L, Caleyachetty, R, Cnattingius, S, et al. Preconceptional and maternal obesity: epidemiology and health consequences. Lancet Diabetes Endocrinol. 2016; 4(12), 1025–1036.CrossRefGoogle ScholarPubMed
IDF Diabetes Atlas, 9th edition. 2019. https://www.diabetesatlas.org/en/.Google Scholar
American Diabetes Association. Management of diabetes in pregnancy: standards of medical care in diabetes-2021. Diabetes Care. 2021; 44(Suppl 1), S200–S210.CrossRefGoogle Scholar
Aris, IM, Soh, SE, Tint, MT, et al. Effect of maternal glycemia on neonatal adiposity in a multiethnic Asian birth cohort. J Clin Endocrinol Metab. 2014; 99(1), 240–247.CrossRefGoogle Scholar
Metzger, BE, Lowe, LP, Dyer, AR, et al. Hyperglycemia and adverse pregnancy outcome (HAPO) study: associations with neonatal anthropometrics. Diabetes. 2009; 58(2), 453–459.Google Scholar
Lowe, WL, Lowe, LP, Kuang, A, et al. Maternal glucose levels during pregnancy and childhood adiposity in the Hyperglycemia and Adverse Pregnancy Outcome Follow-up Study. Diabetologia. 2019; 62(4), 598–610.CrossRefGoogle ScholarPubMed
Godfrey, KM, Gluckman, PD, Hanson, MA. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab. 2010; 21(4), 199–205.CrossRefGoogle ScholarPubMed
Tam, WH, Ma, RCW, Ozaki, R, et al. In utero exposure to maternal hyperglycemia increases childhood cardiometabolic risk in offspring. Diabetes Care. 2017; 40(5), 679–686.CrossRefGoogle ScholarPubMed
Tellechea, ML, Mensegue, MF, Pirola, CJ. The association between high-fat diet around gestation and metabolic syndrome-related phenotypes in rats: a systematic review and meta-analysis. Sci Rep. 2017; 7(1), 5086.CrossRefGoogle ScholarPubMed
Kiss, AC, Lima, PH, Sinzato, YK, et al. Animal models for clinical and gestational diabetes: maternal and fetal outcomes. Diabetol Metab Syndr. 2009; 1(1), 21.CrossRefGoogle ScholarPubMed
Calkins, K, Devaskar, SU. Fetal origins of adult disease. Curr Probl Pediatr Adolesc Health Care. 2011; 41(6), 158–176.Google ScholarPubMed
Desai, M, Jellyman, JK, Han, G, Beall, M, Lane, RH, Ross, MG. Maternal obesity and high-fat diet program offspring metabolic syndrome. Am J Obstet Gynecol. 2014; 211(3), 237.e1–237.e13.CrossRefGoogle ScholarPubMed
Bueno, A, Sinzato, YK, Volpato, GT, et al. Severity of prepregnancy diabetes on the fetal malformations and viability associated with early embryos in rats. Biol Reprod. 2020; 103(5), 938–950.Google Scholar
Aerts, L, Van Assche, FA. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol. 2006; 38(5-6), 894–903.CrossRefGoogle ScholarPubMed
Tchkonia, T, Thomou, T, Zhu, Y, et al. Mechanisms and metabolic implications of regional differences among fat depots. Cell Metab. 2013; 17(5), 644–656.Google ScholarPubMed
Chusyd, DE, Wang, D, Huffman, DM, Nagy, TR. Relationships between rodent white adipose fat pads and human white adipose fat depots. Front Nutr. 2016; 3(12), 10.CrossRefGoogle ScholarPubMed
Björntorp, P, Sjöström, L. Number and size of adipose tissue fat cells in relation to metabolism in human obesity. Metabolism. 1971; 20(7), 703–713.CrossRefGoogle ScholarPubMed
Ahima, RS, Flier, JS. Adipose tissue as an endocrine organ. Trends Endocrinol Metab. 2000; 11(8), 327–332.CrossRefGoogle ScholarPubMed
Gesta, S, Blühet, M, Yamamoto, Y, et al. Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc Natl Acad Sci U S A. 2006; 103(17), 6676–6681.CrossRefGoogle ScholarPubMed
de Almeida, MM, Dias-Rocha, CP, Reis-Gomes, CF, et al. Maternal high-fat diet up-regulates type-1 cannabinoid receptor with estrogen signaling changes in a sex- and the depot-specific manner in white adipose tissue of adult rat offspring. Eur J Nutr. 2021; 60(3), 1313–1326.CrossRefGoogle Scholar
dos Santos, LS, de Matos, RJB, Cordeiro, GDS, et al. Perinatal and post-weaning exposure to an obesogenic diet promotes greater expression of nuclear factor-κB and tumor necrosis factor-α in white adipose tissue and hypothalamus of adult rats. Nutr Neurosci. 2020; 4, 1–9.Google Scholar
Sellayah, D, Thomas, H, Lanham, SA, Cagampang, FR. Maternal obesity during pregnancy and lactation influences offspring obesogenic adipogenesis but not developmental adipogenesis in mice. Nutrients. 2019; 11(3), 495.CrossRefGoogle Scholar
Lecoutre, S, Deracinois, B, Laborie, C, et al. Depot- and sex-specific effects of maternal obesity in offspring’s adipose tissue. J Endocrinol. 2016; 230(1), 39–53.CrossRefGoogle ScholarPubMed
Litzenburger, T, Huber, EK, Dinger, K, et al. Maternal high-fat diet induces long-term obesity with sex-dependent metabolic programming of adipocyte differentiation, hypertrophy, and dysfunction in the offspring. Clin Sci. 2020; 134(7), 921–939.CrossRefGoogle ScholarPubMed
Parente, LB, Aguila, MB, Mandarim-de-Lacerda, CA. Deleterious effects of high-fat diet on perinatal and postweaning periods in adult rat offspring. Clin Nutr. 2008; 27(4), 623–634.CrossRefGoogle ScholarPubMed
Simpson, J, Kelly, JP. The impact of environmental enrichment in laboratory rats—Behavioural and neurochemical aspects. Behav Brain Res. 2011; 222(1), 246–264.CrossRefGoogle Scholar
Sinzato, YK, Klöppel, E, Miranda, CA, et al. Comparison of streptozotocin-induced diabetes at different moments of the life of female rats for translational studies. Lab Anim. 2021; 55(4), 329–340.CrossRefGoogle ScholarPubMed
Macedo, NCD, Iessi, IL, Gallego, FQ, et al. Swimming program on mildly diabetic rats in pregnancy. Reprod Sci. 2021; 28(8), 2223–2235.CrossRefGoogle ScholarPubMed
American Diabetes Association. Classification and diagnosis of diabetes. Diabetes Care. 2021; 44(Suppl 1), S15–S33.Google Scholar
Araujo-Silva, VC, Santos-Silva, A, Lourenço, AS, et al. Congenital anomalies programmed by maternal diabetes and obesity on offspring of rats. Front Physiol. 2021; 12, 701767.CrossRefGoogle ScholarPubMed
Tai, MM. A Mathematical Model for the Determination of total area under glucose tolerance and other metabolic curves. Diabetes Care. 1994; 17(2), 152–154.CrossRefGoogle ScholarPubMed
Soares, TS, Moraes-Souza, RQ, Carneiro, TB, et al. Maternal-fetal outcomes of exercise applied in rats with mild hyperglycemia after embryonic implantation. Birth Defects Res. 2021; 113(3), 287–298.Google ScholarPubMed
Taylor, BA, Phillips, SJ. Detection of obesity QTLs on mouse chromosomes 1 and 7 by selective DNA pooling. Genomics. 1996; 34(3), 389–398.CrossRefGoogle ScholarPubMed
Ibáñez, CA, Vázquez-Martínez, M, León-Contreras, JC, et al. Different statistical approaches to characterization of adipocyte size in offspring of obese rats: effects of maternal or offspring exercise intervention. Front Physiol. 2018; 9, 1571.CrossRefGoogle ScholarPubMed
Pettitt, DJ, Knowler, WC. Diabetes and obesity in the Pima Indians: a cross-generational vicious cycle. J Obesity Weight Regul. 1988; 7(2), 61–65.Google Scholar
Dabelea, D, Hanson, RL, Bennett, PH, Roumain, J, Knowler, WC, Pettitt, DJ. Increasing prevalence of type II diabetes in American Indian children. Diabetologia. 1998; 41(8), 904–910.CrossRefGoogle ScholarPubMed
Clausen, TD, Mathiesen, ER, Hansen, T, et al. High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational Diabetes mellitus or type 1 diabetes: the role of intrauterine hyperglycemia. Diabetes Care. 2008; 31(2), 340–346.CrossRefGoogle ScholarPubMed
Gustafson, B, Hedjazifar, S, Gogg, S, Hammarstedt, A, Smith, U. Insulin resistance and impaired adipogenesis. Trends Endocrinol Metab. 2015; 26(4), 193–200.CrossRefGoogle ScholarPubMed
Yki-Järvinen, H. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2014; 2(11), 901–910.CrossRefGoogle Scholar
Goossens, GH. The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav. 2008; 94(2), 206–218.CrossRefGoogle ScholarPubMed
Tchkonia, T, Tchoukalova, YD, Giorgadze, N, et al. Abundance of two human preadipocyte subtypes with distinct capacities for replication, adipogenesis, and apoptosis varies among fat depots. Am J Physiol Endocrinol Metab. 2005; 288(1), E267–E277.CrossRefGoogle ScholarPubMed
de Queiroz, JCF, Alonso-Vale, MIC, Curi, R, Lima, FB. Control of adipogenesis by fatty acids. Arq Bras Endocrinol Metabol. 2009; 53(5), 582–594.Google Scholar
Rosenbaum, M, Leibel, RL. Role of leptin in energy homeostasis in humans. J Endocrinol. 2014; 223(1), T83–T96.CrossRefGoogle ScholarPubMed
Bouchard, C. Childhood obesity: are genetic differences involved? Am J Clin Nutr. 2009; 89(5), 1494S–1501S.CrossRefGoogle ScholarPubMed
Swinburn, BA, Sacks, G, Hall, KD, et al. The global obesity pandemic: shaped by global drivers and local environments. Lancet. 2011; 378(9793), 804–814.CrossRefGoogle ScholarPubMed
Chouchani, ET, Kajimura, S. Metabolic adaptation and maladaptation in adipose tissue. Nat Metab. 2019; 1(2), 189–200.CrossRefGoogle ScholarPubMed
Dabelea, D, Crume, T. Maternal environment and the transgenerational cycle of obesity and diabetes. Diabetes. 2011; 60(7), 1849–1855.CrossRefGoogle ScholarPubMed
H.S.C.R. Group. Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study: associations with neonatal anthropometrics. Diabetes. 2009; 58(2), 453–459.CrossRefGoogle Scholar
Muhlhausler, B, Smith, SR. Early-life origins of metabolic dysfunction: role of the adipocyte. Trends Endocrinol Metab. 2009; 20(2), 51–57.CrossRefGoogle ScholarPubMed
Tang, QQ, Lane, MD. Adipogenesis: from stem cell to adipocyte. Annu Rev Biochem. 2012; 81(1), 715–736.CrossRefGoogle Scholar