Restraint Stress Impairs Glucose Homeostasis Through Altered Insulin Signalling in Sprague-Dawley Rat
Keywords:
Stress, Glucose tolerance, Insulin sensitivity, Glucose transporter-4, CorticosteroneAbstract
Summary: The study investigated the potential alteration in the level of insulin and adiponectin, as well as the expression of insulin receptors (INSR) and glucose transporter 4 GLUT-4 in chronic restraint stress rats. Sprague-Dawley rats were randomly divided into two groups: the control group and stress group in which the rats were exposed to one of the four different restraint stressors; 1 h, twice daily for a period of 7 days (S7D), 14 days (S14D) and 28 days (S28D). Glucose tolerance and insulin sensitivity were evaluated following the final stress exposure. ELISA were performed to assess the level of insulin and adiponectin as well as expression of INSR and GLUT4 protein in skeletal muscle. Plasma corticosterone level was also determined as a marker of stress exposure. Restraint stress for 7 days caused transient glucose intolerance, while S14D rats demonstrated increased glucose intolerance and insulin insensitivity. However, restraint stress for 28 days had no effect on glucose tolerance, but did cause an increase in glucose response to insulin challenge. The serum level of adiponectin was significantly (p< 0.05) lower compared with the control value while insulin remained unchanged except at in S28D rats that had a significant (p<0.05) increase. The expression of INSR and GLUT4 receptors were significantly (p< 0.05) decreased in the skeletal muscle of restraint stress exposed rats. There was a significant (p< 0.05) increase in the plasma corticosterone level of the stress rats compared with their control counterparts. Restraint stress caused glucose intolerance and insulin insensitivity in male Sprague-Dawley rats, which becomes accommodated with prolonged exposure and was likely related to the blunted insulin signalling in skeletal muscle.
References
Björntorp P. Body fat distribution, insulin resistance, and metabolic diseases. Nutrition 1997; 13(9):795-803
Bonner-Weir S, Trent DF, Honey RN, Weir GC. Responses of neonatal rat islets to streptozotocin, limited β cell regeneration and hyperglycemia. Diabetes 1981; 30:64–9.
Brewer PD, Habtemichael EN, Romenskaia I, Corley Mastick C, Coster AC. Insulin-regulated Glut4 translocation: membrane protein trafficking with six distinctive steps. J Biol Chem 2014; 289:17280-17298.
Carrasco GA, Van de Kar LD. Neuroendocrine pharmacology of stress. Eur J Pharmacol 2003; 463:23–72.
Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler Thromb Vasc Biol 2004; 24: 816-823
Chalkley S.M., Hettiarachchi M., Chisholm D.J., Kraegen E.W. Longterm high-fat feeding leads to severe insulin resistance but not diabetes in Wistar rats. Am J Physiol Endocrinol Metab 2002; 282(6):E1231–E1238.
Chalkley SM, Hettiarachchi M, Chisholm DJ, Kraegen EW. Long term high-fat feeding leads to severe insulin resistance but not diabetes in Wistar rats. Am J Physiol Endocrinol Metab 2002; 282(6): E1231–E1238.
Chrousos GP. Stressors, stress, and neuroendocrine integration of the adaptive response: The 1997 Hans Selye Memorial Lecture. Ann NY Acad Sci 1998; 851:311–35.
Donga E, van Dijk M, van Dijk JG, Biermasz NR, Lammers GJ, van Kralingen KW, et al. A single night of partial sleep deprivation induces insulin resistance in multiple metabolic pathways in healthy subjects. J Clin Endocrinol Metab 2010; 95:2963-2968.
Hentiksen EJ., Diamond-Stanic MK, Marchionne EM. Oxidative stress and the etiology of insulin resistance and type 2 diabetes. Free Radic Biol Med 2011; 51 (5): 993–999
Kevetnansky R, Fukuhara K, Pacak K, Cizza G, Goldstein DS, Kopin IJ. Endogenous glucocorticoids restrain catecholamine synthesis and release at rest and during immobilization stress in rats. Endocrinology 1993; 133:1411–9.
Landowski, J. Neurobiology of stress. Neuropsychiatry Neuropsychol 2007; 2: 26–31.
Lay SL, Simard G, Martinez MC, Anriantsitohaina R. Oxidative Stress and Metabolic Pathologies: From an adipocentric point of view. Oxid Med Cell Longev 2014; http://dx.doi.org/10.1155/2014/908539
Malisch JL, Saltzman W, Gomes FR, Rezende EL, Jeske DR, Garland T. Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running. Physiol Biochem Zool 2007; 80(1):146–156.
McEwen BS. Sleep deprivation as a neurobiologic and physiologic stressor: Allostasis and allostatic load. Metabolism 2006; 55: 20-23.
Morakinyo AO, Iranloye BO, Samuel TA, Mofolorunso AM and Adegoke OA. Insulin receptor and glucose transporter-4 expression in the skeletal muscle of chronically stressed rats. J Afr Ass Physiol Sci 2016; 4 (1): 25-31
Nade VS, Kawale LA, Naik RA, Yadav AV. Adaptogenic effect of Morus alba on chronic footshock-induced stress in rats. Indian J Pharmacol. 2009; 41:246–51.
Nakatani Y, Kaneto H, Kawamori D, Yoshiuchi K, Hatazaki M, Matsuoka T, Ozawa K, Ogawa S, Hori M, Yamasaki Y, Matsushisa M. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem 2005; 280: 847-851
Ozcan U, Cao Q, Yilmaz E, Lee A, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Gilmcher LH, Hotamisligi GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004; 306 (5695): 457-461
Pessin J.E and Saltiel A.R. Signaling pathways in insulin action: molecular targets of insulin resistance J Clin Invest 2000; 106 (2):165-169
Pitman DL, Ottenweller JE, Natels BH. Plasma corticosterone levels during repeated presentation of two intensities of restraint stress: Chronic stress and habituation. Physiol Behav 1988; 43(1): 47-55
Rozanski A, Blumenthal JA, Davidson KW, Saab PG, Kubzansky L, et al. The epidemiology, pathophysiology, and management of psychosocial risk factors in cardiac practice: the emerging field of behavioral cardiology. Brain Beh Imm 2005; 20(2):113-9.
Sabban EL, Kvetnansky R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci 2001; 24:91–8.
Samson J, Sheeladevi R, Ravindran R, Senthilvelan M. Stress response in rat brain after different durations of noise exposure. Neurosci Res 2007; 57:143-147.
Soop M, Nygren J, Myrenfors P, Thorel A, Ljungqvist O. Preoperative oral carbohydrate treatment attenuates immediate postoperative insulin resistance. Am J Physiol Endocrinol Metab 2001; 280(4): E576–E583.
Strommer L, Permert J, Arnelo U, Koehler C, Isaksson B, Larsson J, et al. Skeletal muscle insulin resistance after trauma: insulin signaling and glucose transport. Am J Physiol 1998; 275: E351–8.
Toleikis PM, Godin DV. Alteration of antioxidant status in diabetic rats by chronic exposure to restraint stressors. Pharmacol Biochem Behav. 1995; 52:355–66.
van Donkelaar EL, Vaessen KR, Pawluski JL, Sierksma AS, Blokland A, Canete R, et al(2014). Long- term corticosterone exposure decreases insulin sensitivity and induces depressive-like behaviour in the C57BL/6NCrl mouse. PLoS One 2014; 9: e106960.
Vanltallie TB. Stress: a risk factor for serious illness. Metabolism 2002; 1:40-5
Vazquez-Vela ME, Torres N, Tovar AR. White adipose tissue as endocrine organ and its role in obesity. Arch Med Res 2008; 39:715–28.
Wang C, Mao X, Wang L, Liu M, Wetzel MD, Guan KL, Dong LQ, Liu FJ. Adiponectin sensitizes insulin signaling by reducing p70 S6 kinase-mediated serine phosphorylation of IRS-1. Biol Chem 2007; 282(11):7991-6.
Zardooz H, Zahedi Asl S, Gharib Naseri MK, Hedayati M. Effect of chronic restraint stress on carbohydrate metabolism in rat. Physiol Behav 2006; 89:373-378.
Downloads
Published
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
