Effect of maternal variable stress on oxidative status and glucose metabolism in pubertal male rats

authors:

avatar Roya Ranjbar Saber , avatar Roxana Karbaschi ORCID , avatar Homeira Zardooz ORCID , *


how to cite: Ranjbar Saber R, Karbaschi R, Zardooz H. Effect of maternal variable stress on oxidative status and glucose metabolism in pubertal male rats. koomesh. 2021;23(1):e153252. 

Abstract

Introduction: Metabolic disorders are affected by negative stress experiences in the early stages of life. Accordingly, in this study, the effects of stress during pregnancy on oxidative status and glucose homeostasis in pubertal male Wistar rats were investigated. Materials and Methods: After pregnancy, female rats (200±30 g) were divided into 2 groups (6 rats per group) of stress and non-stress. Animals in the stress group received variable stress from the fourteenth day to the end of pregnancy. At the end of stress procedure (on the 22nd day of pregnancy), blood was taken from the tail of the dam and the plasma concentration of corticosterone was determined. Blood samples were also collected from male offspring of each group (6 rats per group), at 45 days of age, to measure plasma concentrations of corticosterone, malondialdehyde (MDA), glucose, and insulin, moreover HOMA-IR (an insulin resistance index) was calculated. Results: Stress during pregnancy increased the plasma concentrations of corticosterone in the dam and the pubertal offspring of these dams. Moreover, in these offspring, the plasma concentration of MDA increased, while without observing any change in plasma glucose concentration, plasma insulin concentration, HOMA-IR index, and food intake and body weight decreased. Conclusion: Our findings indicate that stress during pregnancy increased plasma corticosterone concentration and induced oxidative stress, which followed by decreased plasma insulin concentration in pubertal male offspring. Conspicuously, it is possible that the increase in plasma levels of corticosterone of dam, via changing the embryonic neuroendocrine, oxidative, and metabolic systems, induces these impairments.

References

  • 1.

    Lesage J, Del-Favero F, Leonhardt M, Louvart H, Maccari S, Vieau D, et al. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinology 2004; 181: 291-296.

  • 2.

    Maccari S, Darnaudery M, Morley-Fletcher S, Zuena A, Cinque C, Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev 2003; 27: 119-127.

  • 3.

    Owen D, Andrews MH, Matthews SG. RETRACTED: Maternal adversity, glucocorticoids and programming of neuroendocrine function and behaviour. Neurosci Biobehav Rev 2005; 29: 209-226.

  • 4.

    Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 2005; 19: 296-308.

  • 5.

    Holemans K, Aerts L, Assche Fv. Lifetime consequences of abnormal fetal pancreatic development. J Physiol 2003; 547: 11-20.

  • 6.

    Mairesse J, Lesage J, Breton C, Brant B, Hahn T, Darnaudry M, et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endoc Metab 2007; 292: E1526-E133.

  • 7.

    Ingvorsen C, Brix S, Ozanne S, Hellgren L. The effect of maternal inflammation on foetal programming of metabolic disease. Acta Physiol 2015; 214: 440-449.

  • 8.

    Cleasby ME, Livingstone DE, Nyirenda MJ, Seckl JR, Walker BR. Is programming of glucocorticoid receptor expression by prenatal dexamethasone in the rat secondary to metabolic derangement in adulthood? Eur J Endoc 2003; 148: 129-138.

  • 9.

    Lindsay R, Lindsay R, Waddell B, Seckl J. Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 b-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia 1996; 39: 1299-1305.

  • 10.

    Moss TJ, Sloboda DM, Gurrin LC, Harding R, Challis JR, Newnham JP. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol 2001; 281: R960-R970.

  • 11.

    Cao-Lei L, Dancause KN, Elgbeili G, Laplante DP, Szyf M, King S. DNA methylation mediates the effect of maternal cognitive appraisal of a disaster in pregnancy on the childs C-peptide secretion in adolescence: Project Ice Storm. PloS One 2018; 13.

  • 12.

    Entringer S, Wst S, Kumsta R, Layes IM, Nelson EL, Hellhammer DH, et al. Prenatal psychosocial stress exposure is associated with insulin resistance in young adults. Am J Obstet Gynecol 2008; 199: 498. e1-e7.

  • 13.

    Maccari S, Piazza PV, Kabbaj M, Barbazanges A, Simon H, Le Moal M. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J Neuroscience 1995; 15: 110-116.

  • 14.

    WARD IL, WEISZ J. Differential effects of maternal stress on circulating levels of corticosterone, progesterone, and testosterone in male and female rat fetuses and their mothers*. Endocrinology 1984; 114: 1635-1644.

  • 15.

    Sadau Y, Adelaiye A, Magaji R, Ayo J, Mabrouk M, Isa A. Role of selenium and Vitamin E on gastric mucosal damage induced by water-immersion restraint stress in wistar rats.

  • 16.

    Kashif S, Zaidi R, Al-Qirim TM, Hoda N, Banu N. Modulation of restraint stress induced oxidative changes in rats by antioxidant vitamins. J Nutr Biochem 2003; 14: 633-636.

  • 17.

    Costantini D, Marasco V, Mller AP. A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. J Comp Physiol B 2011; 181: 447-456.

  • 18.

    Wilson CB, McLaughlin LD, Nair A, Ebenezer PJ, Dange R, Francis J. Inflammation and oxidative stress are elevated in the brain, blood, and adrenal glands during the progression of post-traumatic stress disorder in a predator exposure animal model. PloS One 2013; 8.

  • 19.

    Sameni HR, Kavakebian F, Amjad MH, Bandegi AR, Yousefi B, Taherian AA. Effects of hydroalcoholic extract of Propolis on oxidative stress indices of rat fetal brain induced by chronic prenatal stress. Koomesh 2014; 482-492. (Persian).

  • 20.

    Haussmann MF, Longenecker AS, Marchetto NM, Juliano SA, Bowden RM. Embryonic exposure to corticosterone modifies the juvenile stress response, oxidative stress and telomere length. Proc Biol Sci 2012; 279: 1447-1456.

  • 21.

    Song L, Zheng J, Li H, Jia N, Suo Z, Cai Q, et al. Prenatal stress causes oxidative damage to mitochondrial DNA in hippocampus of offspring rats. Neurochem Res 2009; 34: 739-745.

  • 22.

    Madhyastha S, Sahu SS, Rao G. Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons. J Basic Clin Physiol Pharmacol 2014; 25: 63-72.

  • 23.

    Cao K, Zheng A, Xu J, Li H, Liu J, Peng Y, et al. AMPK activation prevents prenatal stress-induced cognitive impairment: Modulation of mitochondrial content and oxidative stress. Free Radical Biol Med 2014;75: 156-166.

  • 24.

    Gatford KL, Simmons RA. Prenatal programming of insulin secretion in intrauterine growth restriction. Clin Obstet Gynecol 2013; 56: 520.

  • 25.

    Pristov JB, Spasojevic I, Mikovic , Mandic V, Cerovic N, Spasic M. Antioxidative defense enzymes in placenta protect placenta and fetus in inherited thrombophilia from hydrogen peroxide. Oxid Med Cell Longev 2009; 2: 14-18.

  • 26.

    Hracsko Z, Orvos H, Novak Z, Pal A, Varga IS. Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation. Redox Report 2008; 13: 11-16.

  • 27.

    Chen L, Chen R, Wang H, Liang F. Mechanisms linking inflammation to insulin resistance. Int J Endoc 2015; 2015.

  • 28.

    Simmons RA, Suponitsky-Kroyter I, Selak MA. Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to -cell failure. J Biol Chem 2005; 280: 28785-28791.

  • 29.

    Ihara Y, Yamada Y, Toyokuni S, Miyawaki K, Ban N, Adachi T, et al. Antioxidant -tocopherol ameliorates glycemic control of GK rats, a model of type 2 diabetes. FEBS Lett 2000; 473: 24-26.

  • 30.

    Rostamkhani F, Zardooz H, Zahediasl S, Farrokhi B. Comparison of the effects of acute and chronic psychological stress on metabolic features in rats. J Zhejiang Univ Sci B. 2012; 13: 904-912. (Persian).

  • 31.

    Zardooz H, Asl SZ, Naseri MG. Effect of chronic psychological stress on insulin release from rat isolated pancreatic islets. Life Sci 2006; 79: 57-62.

  • 32.

    Jorgensen A, Maigaard K, Wrtwein G, Hageman I, Henriksen T, Weimann A, et al. Chronic restraint stress in rats causes sustained increase in urinary corticosterone excretion without affecting cerebral or systemic oxidatively generated DNA/RNA damage. Prog Neuropsychopharmacol Biol Psychiatry 2013; 40: 30-37.

  • 33.

    Michel C, Duclos M, Cabanac M, Richard D. Chronic stress reduces body fat content in both obesity-prone and obesity-resistant strains of mice. Horm Behav 2005; 48: 172-179.

  • 34.

    Herman J. Neural control of chronic stress adaptation. Front Behav Neurosci 2013; 7: 61.

  • 35.

    Wilson CA, Vazdarjanova A, Terry AV, Jr. Exposure to variable prenatal stress in rats: effects on anxiety-related behaviors, innate and contextual fear, and fear extinction. Behav Brain Res 2013; 238: 279-288.

  • 36.

    Sahu SS, Madhyastha S, Rao GM. Neuroprotective effect of resveratrol against prenatal stress induced cognitive impairment and possible involvement of Na+, K+-ATPase activity. Pharmacol Biochem Behav 2013; 103: 520-525.

  • 37.

    Tamashiro KL, Terrillion CE, Hyun J, Koenig JI, Moran TH. Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 2009; 58: 1116-1125.

  • 38.

    Karagiannides I, Golovatscka V, Bakirtzi K, Sideri A, Salas M, Stavrakis D, et al. Chronic unpredictable stress regulates visceral adipocytemediated glucose metabolism and inflammatory circuits in male rats. Physiol Rep 2014; 2: e00284.

  • 39.

    Sadeghimahalli F, Karbaschi R, Zardooz H, Khodagholi F, Rostamkhani F. Effect of early life stress on pancreatic isolated islets insulin secretion in young adult male rats subjected to chronic stress. Endocrine 2015; 48: 493-503.

  • 40.

    Maghami S, Sadeghimahalli F, Zardooz H. Effects of maternal separation stress on glucose homeostasis in pubertal male rats. Koomesh 2017; 19.

  • 41.

    Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 2003; 54: 1025-1034.

  • 42.

    Kapoor A, Matthews SG. Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitary-adrenal axis activity in male guinea pig offspring. J Physiol 2005; 566: 967-977.

  • 43.

    McGowan PO, Matthews SG. Prenatal stress, glucocorticoids, and developmental programming of the stress response. Endocrinology 2018; 159: 69-82.

  • 44.

    Thompson LP, Al-Hasan Y. Impact of oxidative stress in fetal programming. J Pregnancy 2012; 2012.

  • 45.

    Luo ZC, Delvin E, Fraser WD, Audibert F, Deal CI, Julien P, et al. Maternal glucose tolerance in pregnancy affects fetal insulin sensitivity. Diabet Care 2010; 33: 2055-2061.

  • 46.

    Fetita LS, Sobngwi E, Serradas P, Calvo F, Gautier JF. Consequences of fetal exposure to maternal diabetes in offspring. J Clin Endoc Metab 2006; 91: 3718.

  • 47.

    Portha B, Chavey A, Movassat J. Early-life origins of type 2 diabetes: fetal programming of the beta-cell mass. Exp Diabetes Res 2011; 2011: 05076.

  • 48.

    Beaudry JL, Riddell MC. Effects of glucocorticoids and exercise on pancreatic -cell function and diabetes development. Diabetes Metab Res Rev 2012; 28: 560-573.

  • 49.

    Gatford KL, Simmons RA. Prenatal programming of insulin secretion in intrauterine growth restriction. Clin Obstet Gynecol 2013; 56: 520.

  • 50.

    Sadeghimahalli F, Karbaschi R, Salimi M, Khodagholi F, Zardooz H. Pancreatic HB9 protein level is affected by early life stress in young adult rats: possible involvement of TNF- and corticosterone. Arch Physiol Biochem 2019; 1-8.

  • 51.

    Nirupama R, Rajaraman B, Yajurvedi H. Stress and Glucose metabolism: A Review. Imaging J Clin Med Sci 2018; 5: 008-12.

  • 52.

    Schenk S, Harber MP, Shrivastava CR, Burant CF, Horowitz JF. Improved insulin sensitivity after weight loss and exercise training is mediated by a reduction in plasma fatty acid mobilization, not enhanced oxidative capacity. J Physiology 2009; 587: 4949-4961.

  • 53.

    Gower BA, Weinsier RL, Jordan JM, Hunter GR, Desmond R. Effects of weight loss on changes in insulin sensitivity and lipid concentrations in premenopausal African American and white women. Am J Clin Nutr 2002; 76: 923-927.

  • 54.

    Burgueo AL, Juarez YR, Genaro AM, Tellechea ML. Prenatal stress and later metabolic consequences: systematic review and meta-analysis in rodents. Psychoneuroendocrinology 2019; 104560.

  • 55.

    Paternain L, De La Garza A, Batlle M, Milagro F, Martinez JA, Campion J. Prenatal stress increases the obesogenic effects of a high-fat-sucrose diet in adult rats in a sex-specific manner. Stress 2013; 16: 220-232.

  • 56.

    Zhu Z, Cao F, Li X. Epigenetic programming and fetal metabolic programming. Front Endocrinol 2019; 10: 764.

  • 57.

    Fernandez-Twinn DS, Hjort L, Novakovic B, Ozanne SE, Saffery R. Intrauterine programming of obesity and type 2 diabetes. Diabetologia 2019; 1-13.

  • 58.

    Franko K, Forhead A, Fowden A. Differential effects of prenatal stress and glucocorticoid administration on postnatal growth and glucose metabolism in rats. J Endocrinology 2010; 204: 319-329.

  • 59.

    Szoke E, Shrayyef MZ, Messing S, Woerle HJ, Van Haeften TW, Meyer C, et al. Effect of aging on glucose homeostasis: accelerated deterioration of -cell function in individuals with impaired glucose tolerance. Diabetes Care 2008; 31: 539-543.

  • 60.

    Iozzo P, Beck-Nielsen H, Laakso M, Smith U, Yki-Jarvinen H, Ferrannini E, et al. Independent influence of age on basal insulin secretion in nondiabetic humans. J Clin Endoc Metab 1999; 84: 863-868.

  • 61.

    Karakelides H, Irving BA, Short KR, O'Brien P, Nair KS. Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes 2010; 59: 89-97.

  • 62.

    Portha B, Chavey A, Movassat J. Early-life origins of type 2 diabetes: fetal programming of the beta-cell mass. Exp Diabetes Res 2011; 2011.

  • 63.

    Cederroth CR, Nef S. Fetal programming of adult glucose homeostasis in mice. PLoS One 2009; 4.

  • 64.

    Hao XQ, Du JX, Li Y, Li M, Zhang SY. Prenatal exposure to lipopolysaccharide combined with pre-and postnatal high-fat diet result in lowered blood pressure and insulin resistance in offspring rats. PLoS One 2014; 9.