Skip to main content
Search
Search
    Quick Search anywhere
    Quick search in Citations
Advanced Search
Skip main navigationClose Drawer MenuOpen Drawer Menu
Previous article
Next article
Articles

Rat Strain and Sex Differences in Leptin Responses to Immobilization Stress

Published Online:October 03, 2006https://doi.org/10.1027/1614-0001.27.3.136

Abstract

The effects of immobilization (IM) stress on plasma leptin levels and bodyweight in adult Sprague-Dawley (19 males, 20 females) and Long-Evans (20 males, 20 females) rats were investigated. Following a 10-day baseline period, half the animals from each experimental group were exposed to immobilization stress or no-stress 20 min/day for 21 days. Plasma leptin and corticosterone levels were measured following stress or no-stress exposure on the last day of the experiment. Corticosterone levels confirmed stress exposure. Important interactive effects of stress, strain, and sex on leptin and corticosterone levels were also observed. Specifically, females displayed higher leptin levels than did males, regardless of stress exposure. Strain interacted with stress such that stressed Long-Evans rats displayed higher leptin levels than did stressed Sprague-Dawley rats; there were no strain differences in leptin levels among nonstressed rats. Also, correlations between leptin and corticosterone were strain-specific. Results are discussed with respect to previously unreported strain differences in the effects of immobilization stress on circulating plasma leptin and the relevance to inconsistent findings in the human literature.

References

  • Antoni, M.H., Carrico, A.W., Duran, R.E., Spitzer, S., Penedo, F., Ironson, G., Fletcher, M.A., Klimas, N., Schneiderman, N. (2006). Randomized clinical trial of cognitive behavioral stress management on human immunodeficiency virus viral load in gay men treated with highly active antiretroviral therapy. Psychosomatic Medicine, 68, 143– 51 First citation in articleCrossref, Google Scholar

  • Antoni, M.H., Lutgendorf, S.K., Cole, S.W., Dhabhar, F.S., Sephton, S.E., McDonald, P.G., Stefanek, M., Sood, A.K. (2006). The influence of bio-behavioral factors on tumor biology: Pathways and mechanisms. Nature Reviews Cancer, 6, 240– 248 First citation in articleCrossref, Google Scholar

  • Bielajew, C., Konkle, A.T., Merali, Z. (2002). The effects of chronic mild stress on male Sprague-Dawley and Long-Evans rats: I. Biochemical and physiological analyses. Behavioral Brain Research, 136, 583– 592 First citation in articleCrossref, Google Scholar

  • Bornstein, S.R., Licinio, J., Tauchnitz, R., Engelmann, L., Negrao, A.B., Gold, P., et al. (1998). Plasma leptin levels are increased in survivors of acute sepsis: Associated loss of diurnal rhythm, in corticosteroneisol and leptin secretion. Journal of Clinical Endocrinology and Metabolism, 83, 280– 283 First citation in articleCrossref, Google Scholar

  • Bornstein, S.R., Webster, E.L., Torpy, D.J., Richman, S.J., Mitsiades, N., Igel, M., et al. (1998). Chronic effects of a nonpeptide corticosteroneicotropin-releasing hormone type I receptor antagonist on pituitary-adrenal function, bodyweight, and metabolic regulation. Endocrinology, 139, 1546– 1555 First citation in articleCrossref, Google Scholar

  • Carulli, L., Ferrari, S., Bertolini, M., Tagliafico, E., Del Rio, G. (1999). Regulation of ob gene expression: Evidence for epinephrine-induced suppression in human obesity. The Journal of Clinical Endocrinology and Metabolism, 84, 3309– 3312 First citation in articleCrossref, Google Scholar

  • Chu, N.F., Stampfer, M.J., Spiegelman, D., Rifai, N., Hotamisligil, G.S., Rimm, E.B. (2001). Dietary and lifestyle factors in relation to plasma leptin concentrations among normal weight and overweight men. Int. J. Obes. Relat. Metab. Disord., 25, 106– 114 First citation in articleCrossref, Google Scholar

  • Couillard, C., Mauriege, P., Prud'homme, D., Nadeau, A., Tremblay, A., Bouchard, C., et al. (2002). Plasma leptin response to an epinephrine infusion in lean and obese women. Obesity Research, 10, 6– 13 First citation in articleCrossref, Google Scholar

  • Ebrecht, M., Hextall, J., Kirtley, L.G., Taylor, A., Dyson, M., Weinman, J. (2004). Perceived stress and cortisol levels predict speed of wound healing in healthy male adults. Psychoneuroendocrinology, 29, 798– 809 First citation in articleCrossref, Google Scholar

  • Faraday, M.M., O'Donoghue, V.A., Grunberg, N.E. (1999). Effects of nicotine and stress on startle amplitude and sensory gating depend on rat strain and sex. Pharmacology, Biochemistry, and Behavior, 62, 273– 284 First citation in articleCrossref, Google Scholar

  • Gaillard, R.C., Spinedi, E., Chautard, T., Pralong, F.P. (2000). Cytokines, leptin, and the hypothalamo-pituitary-adrenal axis. Annals of the New York Academy of Sciences, 917, 647– 657 First citation in articleCrossref, Google Scholar

  • Glaser, R., Kiecolt-Glaser, J.K. (2005). Stress-induced immune dysfunction: Implications for health. Nature Reviews Immunology, 5, 243– 251 First citation in articleCrossref, Google Scholar

  • Gomez, F., Houshyar, H., Dallman, M.F. (2002). Marked regulatory shifts in gonadal, adrenal, and metabolic system responses to repeated restraint stress occur within a 3-week period in pubertal male rats. Endocrinology, 143, 2852– 2862 First citation in articleCrossref, Google Scholar

  • Harris, R.B., Mitchell, T.D., Simpson, J., Redmann, S.M., Jr., Youngblood, B.D., Ryan, D.H. (2002). Weight loss in rats exposed to repeated acute restraint stress is independent of energy or leptin status. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 282, R77– R88 First citation in articleGoogle Scholar

  • Harris, R.B., Zhou, J., Youngblood, B.D., Rybkin, II, Smagin, G.N., Ryan, D.H. (1998). Effect of repeated stress on body weight and body composition of rats fed low- and high-fat diets. The American Journal of Physiology, 275(6 Pt 2), R1928– R1938 First citation in articleGoogle Scholar

  • Heiman, M.L., Ahima, R.S., Craft, L.S., Schoner, B., Stephens, T.W., Flier, J.S. (1997). Leptin inhibition of the hypothalamic-pituitary-adrenal axis in response to stress. Endocrinology, 138, 3859– 3863 First citation in articleCrossref, Google Scholar

  • Henry, J.P., Liu, Y.Y., Nadra, W.E., Qian, C.G., Mormede, P., Lemaire, V., et al. (1993). Psychosocial stress can induce chronic hypertension in normotensive strains of rats. Hypertension, 21, 714– 723 First citation in articleCrossref, Google Scholar

  • Hickey, M.S., Israel, R.G., Gardiner, S.N., Considine, R.V., McCammon, M.R., Tyndall, G.L., et al. (1996). Gender differences in serum leptin levels in humans. Biochemical and Molecular Medicine, 59(1), 1– 6 First citation in articleCrossref, Google Scholar

  • Ingalls, A.M., Dickie, M.M., Snell, G.D. (1950). Obese, a new mutation in the house mouse. The Journal of Heredity, 41, 317– 318 First citation in articleCrossref, Google Scholar

  • Isidori, A.M., Strollo, F., More, M., Caprio, M., Aversa, A., Moretti, C., et al. (2000). Leptin and aging: Correlation with endocrine changes in male and female healthy adult populations of different bodyweights. Journal of Clinical Endocrinology and Metabolism, 85, 1954– 1962 First citation in articleCrossref, Google Scholar

  • Kant, G.J., Lenox, R.H., Bunnell, B.N., Mougey, E.H., Pennington, L.L., Meyerhoff, J.L. (1983). Comparison of stress response in male and female rats: Pituitary cyclic amp and plasma prolactin, growth hormone and corticosteroneicosterone. Psychoneuroendocrinology, 8, 421– 428 First citation in articleCrossref, Google Scholar

  • Kant, G.J., Leu, J.R., Anderson, S.M., Mougey, E.H. (1987). Effects of chronic stress on plasma corticosteroneicosterone, ACTH, and prolactin. Physiology & Behavior, 40, 775– 779 First citation in articleCrossref, Google Scholar

  • Lord, G.M., Matarese, G., Howard, J.K., Baker, R.J., Bloom, S.R., Lechler, R.I. (1998). Leptin modulates the t-cell immune response and reverses starvation-induced immunosuppression. Nature, 394(6696), 897– 901 First citation in articleCrossref, Google Scholar

  • Leal-Cerro, A., Soto, A., Martinez, M.A., Dieguez, C., Casanueva, F.F. (2001). Influence of corticosteroneisol status on leptin secretion. Pituitary, 4, 111– 116 First citation in articleCrossref, Google Scholar

  • Malendowicz, L.K., Neri, G., Markowska, A., Hochol, A., Nussdorfer, G.G., Majchrzak, M. (2003). Effects of leptin and leptin fragments on steroid secretion of freshly dispersed rat adrenocorticosteroneical cells. The Journal of Steroid Biochemistry and Molecular Biology, 87, 265– 268 First citation in articleCrossref, Google Scholar

  • Mantovani, G., Maccio, A., Madeddu, C., Mura, L., Gramignano, G., Lusso, M.R., et al. (2002). Quantitative evaluation of oxidative stress, chronic inflammatory indices, and leptin in cancer patients: Correlation with stage and performance status. International Journal of Cancer, 98(1), 84– 91 First citation in articleCrossref, Google Scholar

  • Makino, S., Asaba, K., Nishiyama, M., Hashimoto, K. (1999). Decreased type 2 corticosteroneicotropin-releasing hormone receptor mrna expression in the ventromedial hypothalamus during repeated immobilization stress. Neuroendocrinology, 70, 160– 167 First citation in articleCrossref, Google Scholar

  • Martin, L.J., Mahaney, M.C., Almasy, L., Hixson, J.E., Cole, S.A., MacCluer, J.W., et al. (2002). A quantitative trait locus on chromosome 22 for serum leptin levels adjusted for serum testosterone. Obesity Research, 10, 602– 607 First citation in articleCrossref, Google Scholar

  • McClearn, G.E. (2001). The relevance of animal models for human populations. In C.E.Finch, J.W.Vaupel & K. Kinsella (Eds.), Cells and surveys: Should biological measures be included in social science research? (pp. 213-219). Washington DC: National Academies Press First citation in articleGoogle Scholar

  • McClearn, G.E., Vandenbergh, D.J. (2000). Structures and limits of animal models: Examples from alcohol research. ILAR Journal, 41, 144– 152 First citation in articleCrossref, Google Scholar

  • McConway, M.G., Johnson, D., Kelly, A., Griffin, D., Smith, J., Wallace, A.M. (2000). Differences in circulating concentrations of total, free, and bound leptin relate to gender and body composition in adult humans. Annals of Clinical Biochemistry, 37, 717– 723 First citation in articleCrossref, Google Scholar

  • McEwen, B.S. (1998). Protective and damaging effects of stress mediators. New England Journal of Medicine, 338, 171– 179 First citation in articleCrossref, Google Scholar

  • Meisel, S.R., Ellis, M., Pariente, C., Pauzner, H., Liebowitz, M., David, D., et al. (2001). Serum leptin levels increase following acute myocardial infarction. Cardiology, 95, 206– 211 First citation in articleCrossref, Google Scholar

  • Modan-Moses, D., Ehrlich, S., Kanety, H., Dagan, O., Pariente, C., Esrahi, N., et al. (2001). Circulating leptin and the perioperative neuroendocrinological stress response after pediatric cardiac surgery. Critical Care Medicine, 29, 2377– 2382 First citation in articleCrossref, Google Scholar

  • National Research Center. (1985). Guide for the care and use of laboratory animals: A report of the Institute of Laboratory Animal Resources Committee on Care and Use of Laboratory Animals (Report No. 85-23) . Washington, DC: U.S. Department of Health and Human Services First citation in articleGoogle Scholar

  • Newcomer, J.W., Selke, G., Melson, A.K., Gross, J., Vogler, G.P., Dagogo-Jack, S. (1998). Dose-dependent corticosteroneisol-induced increases in plasma leptin concentration in healthy humans. Archives of General Psychiatry, 55, 995– 1000 First citation in articleCrossref, Google Scholar

  • Riesselmann, A., Baron, A., Fregly, M.J., van Bergen, P. (1992). Hypertension during chronic exposure to cold: Comparison between Sprague-Dawley and Long-Evans strains. Canadian Journal of Physiology and Pharmacology, 70, 701– 708 First citation in articleCrossref, Google Scholar

  • Sanchez-Margalet, V., Martin-Romera, C., Santos-Alvarez, J., Goberna, R., Najib, S., Gonzalex-Yanes, C. (2003). Role of leptin as an immunomodulator of blood mononuclear cells: Mechanisms of action. Clinical Experiments in Immunology, 133(1), 11– 19 First citation in articleCrossref, Google Scholar

  • Schafroth, U., Godang, K., Ueland, T., Bollerslev, J. (2001). Leptin response to endogenous acute stress is independent of pituitary function. European Journal of Endocrinology, 145, 295– 301 First citation in articleCrossref, Google Scholar

  • Scriba, D., Aprath-Husmann, I., Blum, W.F., Hauner, H. (2000). Catecholamines suppress leptin release from in vitro differentiated subcutaneous human adipocytes in primary culture via Beta1- and Beta2-adrenergic receptors. European Journal of Endocrinology, 143, 439– 445 First citation in articleCrossref, Google Scholar

  • Spinedi, E., Gaillard, R.C. (1998). A regulatory loop between the hypothalamo-pituitary-adrenal (HPA) axis and circulating leptin: A physiological role of ACTH. Endocrinology, 139, 4016– 4020 First citation in articleCrossref, Google Scholar

  • Surwit, R.S., van Tilburg, M.A., Zucker, N., McCaskill, C.C., Parekh, P., Feinglos, M.N., Edwards, C.L., Williams, P., Lane, J.D. (2002). Stress management improves long-term glycemic control in type-2 diabetes. Diabetes Care, 25(1), 30– 34 First citation in articleCrossref, Google Scholar

  • Takekoshi, K., Motooka, M., Isobe, K., Nomura, F., Manmoku, T., Ishii, K., et al. (1999). Leptin directly stimulates catecholamine secretion and synthesis in cultured porcine adrenal medullary chromaffin cells. Biochemical Biophysical Research Communications, 261, 426– 431 First citation in articleCrossref, Google Scholar

  • Watanobe, H., Suda, T. (1999). A detailed study on the role of sex steroid milieu in determining plasma leptin concentrations in adult male and female rats. Biochemical Biophysical Research Communications, 259(1), 56– 59 First citation in articleCrossref, Google Scholar

  • Yang, E.V., Glaser, R. (2000). Stress-induced immunomodulation: Impact on immune defences against infectious disease. Biomedicine & Pharmacotherapy, 54, 245– 250 First citation in articleCrossref, Google Scholar

  • Yang, E.V., Glaser, R. (2002). Stress-associated immunomodulation and its implications for responses to vaccination. Expert Reviews of Vaccines, 1, 453– 459 First citation in articleCrossref, Google Scholar

  • Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., Friedman, J.M. (1994). Positional cloning of the mouse obese gene and its human homologue. Nature, 372(6505), 425– 432 First citation in articleCrossref, Google Scholar