Nonpregnant and pregnant adult female rats affected by maternal diabetes environment

References

• Aerts L, Van Assche FA. 2006. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol. 38(5–6):894–903.
   PubMed Web of Science ®Google Scholar
• Agnish ND, Keller KA. 1997. The rationale for culling of rodent litters. Fundam Appl Toxicol. 38(1):2–6.
   PubMedGoogle Scholar
• American Diabetes Association. 2021. Classification and diagnosis of diabetes. Diabetes Care. 44:S15–S33.
   PubMed Web of Science ®Google Scholar
• Aref AB, Ahmed OM, Ali LA, Semmler M. 2013. Maternal rat diabetes mellitus deleteriously affects insulin sensitivity and beta-cell function in the offspring. J Diabetes Res. 2013:429154.
   PubMed Web of Science ®Google Scholar
• Baeyens L, Hindi S, Sorenson RL, German MS. 2016. β‐Cell adaptation in pregnancy. Diabetes Obes Metab. 18(1):63–70.
   PubMedGoogle Scholar
• Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA, Gluckman P, Godfrey K, Kirkwood T, Lahr MM, et al. 2004. Developmental plasticity and human health. Nature. 430(6998):419–421.
   PubMed Web of Science ®Google Scholar
• Bequer L, Gomez T, Molina JL, Alvarez A, Chaviano C, Clapes S. 2018. Experimental diabetes impairs maternal reproductive performance in pregnant Wistar rats and their offspring. Syst Biol Reprod Med. 64(1):60–70.
   PubMed Web of Science ®Google Scholar
• Bhatia P, Chhabra S. 2018. Physiological and anatomical changes of pregnancy: implications for anaesthesia. Indian J Anaesth. 62(9):651–657.
   PubMed Web of Science ®Google Scholar
• Briana DD, Malamitsi-Puchner A. 2009. Intrauterine growth restriction and adult disease: the role of adipocytokines. Eur J Endocrinol. 160(3):337–347.
   PubMed Web of Science ®Google Scholar
• Bueno A, Sinzato YK, Volpato GT, Gallego FQ, Perecin F, Rodrigues T, Damasceno DC. 2020. Severity of prepregnancy diabetes on the fetal malformations and viability associated with early embryos in rats. Biol Reprod. 103(5):938–950.
   PubMed Web of Science ®Google Scholar
• Calkins K, Devaskar SU. 2011. Fetal origins of adult disease. Curr Probl Pediatr Adolesc Health Care. 41(6):158–176.
   PubMed Web of Science ®Google Scholar
• Canavan JP, Goldspink DF. 1988. Maternal diabetes in rats: II. Effects on fetal growth and protein turnover. Diabetes. 37(12):1671–1677.
   PubMed Web of Science ®Google Scholar
• Cederberg J, Galli J, Luthman H, Eriksson UJ. 2000. Increased mRNA levels of Mn-SOD and catalase in embryos of diabetic rats from a malformation-resistant strain. Diabetes. 49(1):101–107.
   PubMed Web of Science ®Google Scholar
• Chen G, Liu C, Xue Y, Mao X, Xu K, Liu C. 2011. Molecular mechanism of pancreatic β-cell adaptive proliferation: studies during pregnancy in rats and in vitro. Endocrine. 39(2):118–127.
   PubMed Web of Science ®Google Scholar
• Cheong JN, Wlodek ME, Moritz KM, Cuffe JS. 2016. Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations. J Physiol. 594(17):4727–4740.
   PubMed Web of Science ®Google Scholar
• Damasceno DC, Sinzato YK, Lima PH, de Souza MS, Campos KE, Dallaqua B, Calderon IM, Rudge MV, Volpato GT. 2011. Effects of exposure to cigarette smoke prior to pregnancy in diabetic rats. Diabetol Metab Syndr. 3:20.
   PubMed Web of Science ®Google Scholar
• Damasceno DC, Netto AO, Iessi IL, Gallego FQ, Corvino SB, Dallaqua B, Sinzato YK, Bueno A, Calderon IMP, Rudge MVC. 2014. Streptozotocin-induced diabetes models: pathophysiological mechanisms and fetal outcomes. Biomed Res Int. 2014(819065):819065.
   PubMedGoogle Scholar
• De Souza MDSS, Sinzato YK, Lima PHO, Calderon IMP, Rudge MVC, Damasceno DC. 2010. Oxidative stress status and lipid profiles of diabetic pregnant rats exposed to cigarette smoke. Reprod Biomed Online. 20(4):547–552.
   PubMed Web of Science ®Google Scholar
• Faria-Neto HC, Santos BF. 2008. Fármacos usados em animais de laboratório–anestésicos e analgésicos. In: Conceição-Silva F, Presgrave AF, editors. Manual de utilização de animais. vol. 1. Brazil: FIOCRUZ; p. 20–27.
   Google Scholar
• Gallego FQ, Sinzato YK, Miranda CA, Iessi IL, Dallaqua B, Volpato GT, Scarano WR, SanMartín S, Damasceno DC. 2018. Pancreatic islet response to diabetes during pregnancy in rats. Life Sci. 214:1–10.
   PubMed Web of Science ®Google Scholar
• Gitto E, Reiter RJ, Karbownik M, Tan D, Gitto P, Barberi S, Barberi I. 2002. Causes of oxidative stress in the pre- and perinatal period. Biol Neonate. 81(3):146–157.
   PubMedGoogle Scholar
• Gluckman PD, Hanson MA. 2007. Developmental plasticity and human disease: research directions. J Intern Med. 261(5):461–471.
   PubMed Web of Science ®Google Scholar
• Greco EA, Lenzi A, Migliaccio S, Gessani S. 2019. Epigenetic modifications induced by nutrients in early life phases: gender differences in metabolic alteration in adulthood. Front Genet. 10:795.
   PubMed Web of Science ®Google Scholar
• Hales CN, Barker DJ. 1992. Type 2 (non–insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 35(7):595–601.
   PubMed Web of Science ®Google Scholar
• Hanafi MY, Abdelkhalek TM, Saad MI, Saleh MM, Haiba MM, Kamel MA. 2016. Diabetes-induced perturbations are subject to intergenerational transmission through maternal line. J Physiol Biochem. 72(2):315–326.
   PubMed Web of Science ®Google Scholar
• Hanson RL, Elston RC, Pettitt DJ, Bennett PH, Knowler WC. 1995. Segregation analysis of non-insulin-dependent diabetes mellitus in Pima Indians: evidence for a major-gene effect. Am J Hum Genet. 57(1):160–170.
   PubMed Web of Science ®Google Scholar
• Haugaard CT, Bauer MK. 2001. Rodent models of intrauterine growth restriction. J Am Assoc Lab Anim Sci. 28(3):10–22.
   Google Scholar
• Hayward CE, Lean S, Sibley CP, Jones RL, Wareing M, Greenwood SL, Dilworth MR. 2016. Placental adaptation: what can we learn from birthweight: placental weight ratio? Front Physiol. 7(28)
   Google Scholar
• Hoffman DJ, Powell TL, Barrett ES, Hardy DB. 2021. Developmental origins of metabolic diseases. Physiol Rev. 101(3):739–795.
   PubMed Web of Science ®Google Scholar
• Jawerbaum A, White V. 2017. Review on intrauterine programming: consequences in rodent models of mild diabetes and mild fat overfeeding are not mild. Placenta. 52:21–32.
   PubMed Web of Science ®Google Scholar
• Kellogg DL, III, McCammon KM, Hinchee-Rodriguez KS, Adamo ML, Roman LJ. 2017. Neuronal nitric oxide synthase mediates insulin- and oxidative stress-induced glucose uptake in skeletal muscle myotubes. Free Radic Biol Med. 110:261–269.
   PubMed Web of Science ®Google Scholar
• Kinsley CH, Lambert KG. 2006. The maternal brain. Sci Am. 294(1):72–79.
   PubMed Web of Science ®Google Scholar
• Lain KY, Catalano PM. 2007. Metabolic changes in pregnancy. Clin Obstet Gynecol. 50(4):938–948.
   PubMed Web of Science ®Google Scholar
• Lawlor DA, Lichtenstein P, Långström N. 2011. Association of maternal diabetes mellitus in pregnancy with offspring adiposity into early adulthood: sibling study in a prospective cohort of 280 866 men from 248 293 families. Circulation. 123(3):258–265.
   PubMed Web of Science ®Google Scholar
• Liu M, Xu L, Yin L, Qi Y, Xu Y, Han X, Zhao Y, Sun H, Yao J, Lin Y, et al. 2015. Potent effects of dioscin against obesity in mice. Sci Rep. 5:7973.
   PubMed Web of Science ®Google Scholar
• Luc K, Schramm-Luc A, Guzi TJ, Mikolajczyk TP. 2019. Oxidative stress and inflammatory markers in prediabetes and diabetes. J Physiol Pharmacol. 70(6):111–113.
   Web of Science ®Google Scholar
• Lumey LH, Ravelli ACJ, Wiessing LG, Koppe JG, Treffers PE, Stein ZA. 1993. The dutch famine birth cohort study: design, validation of exposure, and selected characteristics of subjects after 43 years follow-up. Paediatr Perinat Epidemiol. 7(4):354–367.
   PubMedGoogle Scholar
• Matthews VB, Allen TL, Risis S, Chan MH, Henstridge DC, Watson N, Zaffino LA, Babb JR, Boon J, Meikle PJ, et al. 2010. Interleukin-6-deficient mice develop hepatic inflammation and systemic insulin resistance. Diabetologia. 53(11):2431–2441.
   PubMed Web of Science ®Google Scholar
• Motosko CC, Bieber AK, Pomeranz MK, Stein JA, Martires KJ. 2017. Physiologic changes of pregnancy: a review of the literature. Int J Womens Dermatol. 3(4):219–224.
   PubMedGoogle Scholar
• Myatt L, Cui X. 2004. Oxidative stress in the placenta. Histochem Cell Biol. 122(4):369–382.
   PubMed Web of Science ®Google Scholar
• Navarro E, Funtikova AN, Fíto M, Schröder H. 2017. Prenatal nutrition and the risk of adult obesity: long-term effects of nutrition on epigenetic mechanisms regulating gene expression. J Nutr Biochem. 39:1–14.
   PubMed Web of Science ®Google Scholar
• Netto AO, Gelaleti RB, Corvino SB, Serrano RG, Hernández SC, Volpato GT, Rudge MVC, Braz MG, Damasceno DC. 2018. Small-for-pregnancy-age rats submitted to exercise: DNA damage in mothers and newborns, measured by the comet assay. Mutat Res Genet Toxicol Environ Mutagen. 835:11–15.
   PubMed Web of Science ®Google Scholar
• Nolan CJ, Proietto J. 1994. The feto-placental glucose steal phenomenon is a major cause of maternal metabolic adaptation during late pregnancy in the rat. Diabetologia. 37(10):976–984.
   PubMed Web of Science ®Google Scholar
• Paula VG, Sinzato YK, Moraes-Souza RQ, Soares TS, Souza FQG, Karki B, Paes AMA, Corrente JE, Damasceno DC, Volpato GT. 2022. Metabolic changes in female rats exposed to intrauterine hyperglycemia and post-weaning consumption of high-fat diet. Biol Reprod. 106(1):200–212.
   PubMed Web of Science ®Google Scholar
• Pavethynath S, Imai C, Jin X, Hichiwa N, Takimoto H, Okamitsu M, Tarui I, Aoyama T, Yago S, Fudono A, et al. 2019. Metabolic and immunological shifts during mid-to-late gestation influence maternal blood methylation of CPT1A and SREBF1. IJMS. 20(5):1066.
   Google Scholar
• Pettitt DJ, Nelson RG, Saad MF, Bennett PH, Knowler WC. 1993. Diabetes and obesity in the offspring of Pima Indian women with diabetes during pregnancy. Diabetes Care. 16(1):310–314.
   PubMed Web of Science ®Google Scholar
• Rahman T, Hosen I, Islam M, Shekhar H. 2012. Oxidative stress and human health. ABB. 03(07):997–1019.
   Google Scholar
• Rashid CS, Bansal A, Simmons RA. 2018. Oxidative stress, intrauterine growth restriction, and developmental programming of type 2 diabetes. Physiology. 33(5):348–359.
   PubMed Web of Science ®Google Scholar
• Reusens B, Ozanne SE, Remacle C. 2007. Fetal determinants of type 2 diabetes. Curr Drug Targets. 8(8):935–941.
   PubMed Web of Science ®Google Scholar
• Roseboom TJ, Van Der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. 2001. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Twin Res. 4(5):293–298.
   PubMedGoogle Scholar
• Saker M, Soulimane MN, Merzouk SA, Merzouk H, Belarbi B, Narce M. 2008. Oxidant and antioxidant status in mothers and their newborns according to birthweight. Eur J Obstet Gynecol Reprod Biol. 141(2):95–99.
   PubMed Web of Science ®Google Scholar
• Sinzato YK, Klöppel E, Miranda CA, Paula VG, Alves LF, Nascimento LL, Campos AP, Karki B, Hampl V, Volpato GT, et al. 2021. Comparison of streptozotocin-induced diabetes at different moments of the life of female rats for translational studies. Lab Anim. 55(4):329–340.
   PubMedGoogle Scholar
• Sinzato YK, Volpato GT, Iessi IL, Bueno A, Calderon IMP, Rudge MVC, Damasceno DC. 2012. Neonatally induced mild diabetes in rats and its effect on maternal, placental, and fetal parameters. Exp Diabetes Res. 2012(108163):108163.
   PubMedGoogle Scholar
• Smith PG, Morrow RH, Ross DA. 2015. Outcome measures and case definition. In: Field trials of health interventions: a toolbox. 3rd ed. Oxford: OUP.
   Google Scholar
• Sousa FJ, Correia RG, Cruz AF, Martins JM, Rodrigues MS, Gomes CA, Ambrósio AF, Baptista FI. 2020. Sex differences in offspring neurodevelopment, cognitive performance and microglia morphology associated with maternal diabetes: putative targets for insulin therapy. Brain Behav Immun Health. 5(100075):100075.
   PubMedGoogle Scholar
• Spada APM, Damasceno DC, Sinzato YK, Campos KE, Faria PA, Dallaqua B, Calderon IMP, Rudge MVC, Rodrigues T. 2014. Oxidative stress in maternal blood and placenta from mild diabetic rats. Reprod Sci. 21(8):973–977.
   PubMed Web of Science ®Google Scholar
• Tai MM. 1994. A mathematical model for the determination of total area under glucose tolerance and other metabolic curves. Diabetes Care. 17(2):152–154.
   PubMed Web of Science ®Google Scholar
• Tentor L, Salvati AM. 1981. Hemoglobinometry in human blood. Methods Enzymol. 76:707–715.
   PubMedGoogle Scholar
• Tozour J, Hughes F, Carrier A, Vieau D, Delahaye F. 2020. Prenatal hyperglycemia exposure and cellular stress, a sugar-coated view of early programming of metabolic diseases. Biomolecules. 10(10):1359.
   Web of Science ®Google Scholar
• Van Assche FA, Holemans K, Aerts L. 2001. Long-term consequences for offspring of diabetes during pregnancy. Br Med Bull. 60(1):173–182.
   PubMedGoogle Scholar
• Weydert CJ, Cullen JJ. 2010. Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc. 5(1):51–66.
   PubMed Web of Science ®Google Scholar
• Yessoufou A, Soulaimann N, Merzouk SA, Moutairou K, Ahissou H, Prost J, Simonin AM, Merzouk H, Hichami A, Khan NA. 2006. N-3 fatty acids modulate antioxidant status in diabetic rats and their macrosomic offspring. Int J Obes. 30(5):739–750.
   Web of Science ®Google Scholar