Effects of maternal separation stress on glucose homeostasis in pubertal male rats

authors:

avatar Soheila Maghami , avatar Forouzan Sadeghimahalli , avatar Homeira Zardooz , *

Koomesh: Vol.19, issue 4; 887-893
published online: December 01, 2017
article type: Research Article
received: March 01, 2017
accepted: May 02, 2017

how to cite: Maghami S, Sadeghimahalli F, Zardooz H. Effects of maternal separation stress on glucose homeostasis in pubertal male rats. koomesh. 2017;19(4):e152946. 

Abstract

Introduction: Exposure to stress in postnatal period of life increases the risk of metabolic, behavioral and psychological disorders in later life. In this regard, the present study investigated the effects of maternal separation stress on plasma glucose and insulin concentrations and HOMA-IR (Homeostasis model assessment of insulin resistance) index, in male rats at puberty. Materials and Methods: After birth, the animals were divided into "stress” and “non-stress " groups. The stressed rats were separated from their mothers at postnatal days (PND 1 to 21, 3h/day), whereas non-stressed rats remained with their mothers. At puberty (day 53), the animals were decapitated and their blood samples collected to measure plasma concentrations of insulin, glucose and corticosterone. Moreover, HOMA-IR index was calculated. Results: Maternal separation stress increased plasma glucose concentration in adult male rats, but did not significantly affect plasma insulin concentration. Notably, the HOMA-IR index in stressed rats showed a significant increase. Meanwhile, in the animals of this group, basal plasma corticosterone levels increased significantly compared to non-stressed animals. Conclusion: This study shows that maternal separation during infancy period, possibly, through changes in HPA axis programming induces insulin resistance and impairs glucose homeostasis in puberty and these changes may predispose the rats to metabolic disorders

References

  • 1.

    Pyykknen A-J, Rikknen K, Tuomi T, Eriksson JG, Groop L, Isomaa B. Stressful life events and the metabolic syndrome. Diabet Care 2010; 33: 378-384.

  • 2.

    Wickrama KA, Lee T-K, O'Neal CW. Stressful life experiences in adolescence and cardiometabolic risk factors in young adulthood. J Adol Health 2015; 56: 456-463.

  • 3.

    Zeugmann S, Quante A, Popova-Zeugmann L, Kssler W, Heuser I, Anghelescu I. Pathways linking early life stress, metabolic syndrome, and the inflammatory marker fibrinogen in depressed inpatients. Psychiatr Danub 2012; 24: 57-65.

  • 4.

    Srinivasan M, Patel MS. Metabolic programming in the immediate postnatal period. Trends Endocrinol Metab 2008; 19: 146-152.

  • 5.

    Fowden AL, Hill DJ. Intra-uterine programming of the endocrine pancreas. Br Med Bull 2001; 60: 123-142.

  • 6.

    Hill D, Strutt B, Arany E, Zaina S, Coukell S, Graham C. Increased and persistent circulating insulin-like growth factor II in neonatal transgenic mice suppresses developmental apoptosis in the pancreatic Islets 1. Endocrinology 2000; 141: 1151-1157.

  • 7.

    Hellerstrm C, Swenne I. Functional maturation and proliferation of fetal pancreatic -cells. Diabetes 1991; 40: 89-93.

  • 8.

    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.

  • 9.

    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.

  • 10.

    Lee C, Tsenkova V, Carr D. Childhood trauma and metabolic syndrome in men and women. Soc Sci Med 2014; 105: 122-130.

  • 11.

    Rich-Edwards JW, Spiegelman D, Hibert ENL, Jun H-J, Todd TJ, Kawachi I, et al. Abuse in childhood and adolescence as a predictor of type 2 diabetes in adult women. Am J Prev Med 2010; 39: 529-536.

  • 12.

    Kaufman D, Banerji MA, Shorman I, Smith EL, Coplan JD, Rosenblum LA, et al. Early-life stress and the development of obesity and insulin resistance in juvenile bonnet macaques. Diabetes 2007; 56: 1382-1386.

  • 13.

    Loizzo S, Campana G, Vella S, Fortuna A, Galietta G, Guarino I, et al. Post-natal stress-induced endocrine and metabolic alterations in mice at adulthood involve different pro-opiomelanocortin-derived peptides. Peptides 2010; 31: 2123-2129.

  • 14.

    McPherson RJ, Mascher-Denen M, Juul SE. Postnatal stress produces hyperglycemia in adult rats exposed to hypoxia-ischemia. Pediatr Res 2009; 66: 278-282.

  • 15.

    Solas M, Aisa B, Mugueta MC, Del Ro J, Tordera RM, Ramrez MJ. Interactions between age, stress and insulin on cognition: implications for Alzheimer's disease. Neuropsychopharmacology 2010; 35: 1664-1673.

  • 16.

    Nilsson C, Jennische E, Ho HP, Eriksson E, Bjorntorp P, Holmang A. Postnatal endotoxin exposure results in increased insulin sensitivity and altered activity of neuroendocrine axes in adult female rats. Eur J Endocrinol 2002; 146: 251-260.

  • 17.

    Sadeghi B, Sahraei H, Zardooz H, Alibeik H, Sarahian N. Effects of intra-amygdala memantine infusion on metabolic symptoms induced by chronic stress in male NMRI mice. Koomesh 2015; 16: 376-383.

  • 18.

    Geer EB, Islam J, Buettner C. Mechanisms of glucocorticoid-induced insulin resistance: focus on adipose tissue function and lipid metabolism. Endocrinol Metab Clin North Am 2014; 43: 75-102.

  • 19.

    Zardooz H, Rostamkhani F, Zaringhalam J, Shahrivar FF. Plasma corticosterone, insulin and glucose changes induced by brief exposure to isoflurane, diethyl ether and CO2 in male rats. Physiol Res 2010; 59: 973.

  • 20.

    Koe AS, Salzberg MR, Morris MJ, OBrien TJ, Jones NC. Early life maternal separation stress augmentation of limbic epileptogenesis: the role of corticosterone and HPA axis programming. Psychoneuroendocrinology 2014; 42: 124-133.

  • 21.

    Daniels W, Fairbairn L, Van Tilburg G, McEvoy C, Zigmond M, Russell V, et al. Maternal separation alters nerve growth factor and corticosterone levels but not the DNA methylation status of the exon 17 glucocorticoid receptor promoter region. Metab Brain Dis 2009; 24: 615-627.

  • 22.

    Uys J, Muller C, Marais L, Harvey B, Stein D, Daniels W. Early life trauma decreases glucocorticoid receptors in rat dentate gyrus upon adult re-stress: reversal by escitalopram. Neuroscience 2006; 137: 619-625.

  • 23.

    Bijani S, Najafi Abedi A, Ranjbaran M, Sadeghi Gharajeh Daghi S, Ghoshooni H, Zardooz H, et al. Effects of noise pollution stress during pregnancy on anatomical and functional brain cortex development of the offsprings of NMRI mice. Koomesh 2013; 14: 192-199.

  • 24.

    Robertson RP. Oxidative stress and impaired insulin secretion in type 2 diabetes. Curr Opin Pharmacol 2006; 6: 615-619.

  • 25.

    Havel PJ, Taborsky GJ Jr. The contribution of the autonomic nervous system to changes of glucagon and insulin secretion during hypoglycemic stress. Endocr Rev 1989; 10: 332-350.

  • 26.

    van Donkelaar EL, Vaessen KR, Pawluski JL, Sierksma AS, Blokland A, Caete R, et al. Long-term corticosterone exposure decreases insulin sensitivity and induces depressive-like behaviour in the C57BL/6NCrl mouse. PLoS One 2014; 9: e106960.

  • 27.

    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.

  • 28.

    Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes 2015; 6: 456-480.