Individual Differences in Stress Responsiveness of the Hypothalamic-Pituitary-Adrenal Axis and Its Vasopressinergic Regulation in Old Monkeys

Abstract

Stress adaptation is fundamental for health, and the hypothalamic-pituitary-adrenal axis (HPA) is one of its main mechanisms. Considerable data indicate that arginine vasopressin (AVP) related disturbances of stress adaptation can occur with aging. However, most studies of such kind have been performed on rodents, give contradictory results and fail to consider individual characteristics of the animals. The purpose of this study was to investigate individual HPA responsiveness to acute stress and its vasopressinergic regulation in old female rhesus monkeys that differ in their behavioral responses to stress. Animals with depression-like or anxiety-like behavior (DAB) responded with higher plasma levels of ACTH and AVP, lower levels of corticosteroids and higher cortisol/DHEAS molar ratios to restraint stress and to insulin-induced hypoglycemia compared with animals with healthy adaptive behavior. AVP and ACTH dynamics were closely correlated in most animals. AVP treatment produced differences in HPA responses similar to those produced by the stressors. The ACTH response to hypoglycemic stress in the DAB animal with highest HPA responsiveness was dramatically reduced by prior administration of a V1b receptor antagonist. These results suggest that the dysfunctions of HPA observed in old animals with DAB are caused by increased tone of the vasopressinergic system in regulation of HPA stress reactivity.

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Goncharova, N. , Marenin, V. and Oganyan, T. (2015) Individual Differences in Stress Responsiveness of the Hypothalamic-Pituitary-Adrenal Axis and Its Vasopressinergic Regulation in Old Monkeys. Journal of Behavioral and Brain Science, 5, 280-294. doi: 10.4236/jbbs.2015.57029.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Сizza, G., Calogero, A.E., Brady, L.S., Bagdy, G., Bergamini, E., Blackman, M.R., Chrousos, G.P. and Gold, P.W. (1994) Male Fischer 344/N Rats Show a Progressive Central Impairment of the Hypothalamic-Pituitary-Adrenal Axis with Advancing Age. Endocrinology, 134, 1611-1621.
[2] Goncharova, N.D. (2009) The Hypothalamic-Pituitary-Adrenal Axis in Nonhuman Primates: Circadian Rhythms of Stress Responsiveness and Aging. In: Potocki, E. and Krasinski, J., Eds., Primatology: Theories, Methods and Research, Nova Science Publishers Inc., New York, 29-52.
[3] Goncharova, N.D. (2013) Stress Responsiveness of the Hypothalamic-Pituitary-Adrenal Axis: Age-Related Features of the Vasopressinergic Regulation. Frontiers in Endocrinology, 4, 26.
http://dx.doi.org/10.3389/fendo.2013.00026
[4] Goncharova, N.D. (2014) Age-Related Changes in the Hypothalamic-Pituitary-Adrenal Axis: Experimental Studies in Primates. Advances in Gerontology, 4, 266-270.
http://dx.doi.org/10.1134/S2079057014040109
[5] Hatzinger, M., Wotjak, C.T., Naruo, T., Simchen, R., Kewck, M.E., Landgraf, R., Holsboer, F. and Neumann, I.D. (2000) Endogenous Vasopressin Contributes to Hypothalamic-Pituitary-Adrenocortical Alterations in Aged Rats. Journal of Endocrinology, 164, 197-205.
http://dx.doi.org/10.1677/joe.0.1640197
[6] Haugert, B.L., Thrivikraman, K.V. and Plotsky, P.M. (1994) Age-Related Alterations of Hypothalamic-Pituitary-Adrenal Axis Function in Male Fischer 344 Rats. Endocrinology, 134, 1528-1536.
[7] Keck, M.E., Hatzinger, M., Wotjak, C.T., Landgraf, R., Holsboer, F. and Neumann, I.D. (2000) Ageing Alters Intrahypothalamic Release Patterns of Vasopressin and Oxytocin in Rats. European Journal of Neuroscience, 12, 1487-1494.
http://dx.doi.org/10.1046/j.1460-9568.2000.00030.x
[8] Keck, M.E., Wigger, A., Welt, T., Muller, M.B., Gesing, A., Reul, J.M.H.M., Holsboer, F., Landgraf, R. and Neumann, I.D. (2002) Vasopressin Mediates the Response of the Combined Dexamethasone/CRH Test in Hyper-Anxious Rats: Implications for Pathogenesis of Affective Disorders. Neuropsychopharmacology, 26, 94-105.
http://dx.doi.org/10.1016/S0893-133X(01)00351-7
[9] Meijer, J.C., Topic, D., Steenbergen, P.J., Jochan, G., Huston, J.P. and Oitzl, M.S. (2005) Correlations between Hypothalamic-Pituitrary-Adrenal Axis Paremeters Depend on Age and Learning Capacity. Endocrinology, 146, 1372-1381.
http://dx.doi.org/10.1210/en.2004-0416
[10] Zhang, L., Hernandez, V.S., Liu, B., Medina, M.P., Nava-Kopp, A.T., Irles, C. and Morales, M. (2012) Hypothalamic Vasopressin System Regulation by Maternal Separation: Its Impact on Anxiety in Rats. Neuroscience, 215, 135-148.
http://dx.doi.org/10.1016/j.neuroscience.2012.03.046
[11] Boyle, M.P., Kolber, B.J., Vogt, S.K., Wozniak, D.F. and Muglia, L.J. (2006) Forebrain Glucocorticoid Receptors Modulate Anxiety-Associated Locomotor Activation and Adrenal Responsiveness. Journal of Neuroscience, 26, 1971-1978.
http://dx.doi.org/10.1523/JNEUROSCI.2173-05.2006
[12] Goncharova, N.D. (2009) Individual Life History, Behavior, and Biomarkers of Ageing. Journal of Nutrition, Health, and Aging, 13, S215.
[13] Goncharova, N.D., Marenin, V.Y. and Oganyan, T.E. (2010) Aging of the Hypothalamic-Pituitary-Adrenal Axis in Nonhuman Primates with Depression-Like and Aggressive Behavior. Aging, 2, 854-866.
[14] Maestripieri, D. and Georgiev, A.V. (2015) What Cortisol Can Tell Us about the Costs of Sociality and Reproduction among Free-Ranging Rhesus Macaque Females on Cayo Santiago. American Journal of Primatology, Published Online.
http://dx.doi.org/10.1002/ajp.22368
[15] Beluche, I., Chaudieu, I., Norton, J., Carriere, I., Boulenger, J.P., Ritchie, K. and Ancelin, M.L. (2009) Persistence of Abnormal Cortisol Levels in Elderly Persons after Recovery from Major Depression. Journal of Psychiatric Research, 43, 777-783.
http://dx.doi.org/10.1016/j.jpsychires.2008.10.011
[16] Burke, H.M., Davis, M.C., Otte, C. and Mohr, D.C. (2005) Depression and Cortisol Responses to Psychological Stress: A Meta-Analysis. Psychoneuroendocrinology, 30, 846-856.
http://dx.doi.org/10.1016/j.psyneuen.2005.02.010
[17] Swaab, D.F., Bao, A.M. and Lucassen, P.J. (2005) The Stress System in the Human Brain in Depression and Neurodegeneration. Ageing Research Reviews, 4, 141-194.
http://dx.doi.org/10.1016/j.arr.2005.03.003
[18] Vreeburg, S.A., Hoogendijk, W.J., van Pelt, J., Derijk, R.H., Verhagen, J.C., van Dyck, R., Smit, J.H., Zitman, F.G. and Penninx, B.W. (2009) Major Depressive Disorder and Hypothalamic-Pituitary-Adrenal Axis Activity: Results from a Large Cohort Study. Archives of General Psychiatry, 66, 617-626.
http://dx.doi.org/10.1001/archgenpsychiatry.2009.50
[19] Genud, R., Merenlender, A., Gispan-Herman, I., Maayan, R., Weizman, A. and Yadid, G. (2009) DHEA Lessen Depressive-Like Behavior via GABA-Ergic Modulation of the Mesolimbic System. Neuropsychopharmacology, 34, 577-584.
http://dx.doi.org/10.1038/npp.2008.46
[20] Genazzani, A.R. and Pluchino, N. (2010) DHEA Therapy in Postmenopausal Women: The Need to Move forward beyond the Lack of Evidence. Climacteric, 13, 314-316.
http://dx.doi.org/10.3109/13697137.2010.492496
[21] Micheal, A. (2000) Altered Salivary Dehydroepiandrosterone Levels in Major Depression in Adults. Biological Psychiatry, 48, 989-995.
http://dx.doi.org/10.1016/S0006-3223(00)00955-0
[22] Goncharova, N.D., Oganyan, T.E. and Marenin, V.Y. (2015) Age-Specific and Individual Features of Vasopressinergic Regulation of the Hypothalamic-Pituitary-Adrenal System in Primates. Bulletin of Experimental Biology and Medicine, 134, 804-807.
http://dx.doi.org/10.1007/s10517-015-2866-0
[23] Belvederi Murri, B.M., Pariante, C., Mondelli, V., Masotti, M., Atti, A.R., Mellacqua, Z., Antonioli, M., Ghio, L., Menchetti, M., Zanetidou, S., Innamorati, M. and Amore, M. (2014) HPA Axis and Aging in Depression: Systematic Review and Meta-Analysis. Psychoneuroendocrinology, 41, 46-62.
http://dx.doi.org/10.1016/j.psyneuen.2013.12.004
[24] Hankin, B.L., Badanas, L.S., Abela, J.R.Z. and Watamura, S.E. (2010) Hypothalamic-Pituitary-Adrenal Axis Dysregulation in Disphoric Children and Adolescents: Cortisol Reactivity to Psychosocial Stress from Preschool through Middle Adolescence. Biological Psychiatry, 68, 484-490.
http://dx.doi.org/10.1016/j.biopsych.2010.04.004
[25] Shah, J.L. and Malla, A.K. (2015) Much Ado about Much: Stress, Dynamic Biomarkers and HPA Axis Dysregulation along the Trajectory to Psychosis. Schizophrenia Research, 162, 253-260.
http://dx.doi.org/10.1016/j.schres.2015.01.010
[26] Ferrari, A.J., Charlson, F.J., Norman, R.E., Patten, S.B., Freedman, G., Murray, C.J., Vos, T. and Whiteford, H.A. (2013) Burden of Depressive Disorders by Country, Sex, Age, and Year: Findings from the Global Burden of Disease Study 2010. PLoS Medicine, 10, e1001547.
http://dx.doi.org/10.1371/journal.pmed.1001547
[27] Hidaka, B.H. (2012) Depression as a Disease of Modernity: Explanations for Increasing Prevalence. Journal of Affective Disorders, 140, 205-214.
http://dx.doi.org/10.1016/j.jad.2011.12.036
[28] Landgraf, R. and Wigger, A. (2002) High vs. Low Anxiety-Related Behavior in Rats: An Animal Model of Extremes in Trait Anxiety. Behavior Genetics, 32, 301-314.
http://dx.doi.org/10.1023/A:1020258104318
[29] de Winter, R.F., van Hemert, A.M., DeRijk, R.H., Zwinderman, K.H., Frankhuijzen-Sierevogel, A.C., Wiegant, V.M. and Goekoop, J.G. (2003) Anxious-Retarded Depression: Relation with Plasma Vasopressin and Cortisol. Neuropsychopharmacology, 28, 140-147.
http://dx.doi.org/10.1038/sj.npp.1300002
[30] Dinan, T.G., O’Brien, S., Lavelle, E. and Scott, L.V. (2004) Further Neuroendocrine Evidence of Enhanced Vasopressin V3 Receptor Responses in Melancholic Depression. Psychological Medicine, 34, 169-172.
http://dx.doi.org/10.1017/S0033291703001004
[31] McKinney, W.T., Moran, G.W. and Kraemer, G.W. (1984) Neurobiology and Mood Disorders. In: Post, R. and Ballenger, J., Eds., Separation in Non-Human Primates as a Model for Human Depression: Neurobiological Implications, Williams and Wilkins, Baltimore, 393-406.
[32] Boccia, M.L., Laudenslager, M.L. and Reite, M.L. (1995) Individual Differences in Macaques’ Responses to Stressors Based on Social and Physiological Factors: Implications for Primates Welfare and Research Outcomes. Laboratory Animals, 29, 250-257.
http://dx.doi.org/10.1258/002367795781088315
[33] Goncharova, N.D., Marenin, V.Y. and Vengerin, A.A. (2013) Age-Related Changes in the Reliability of Antioxidant Enzyme Defense in Monkeys with Different Types of Adaptive Behavior. Current Aging Science, 6, 163-169.
http://dx.doi.org/10.2174/18746098112059990004
[34] Vygodsky, M.Y. (1962) Guide to Higher Mathematics. State Publishing Company of Physical and Mathematical Literature, Moscow.
[35] Petrides, J.S., Gold, P.W., Mueller, G.P., Singh, A., Stratakis, C., Chrousos, G.P. and Deuster, P.A. (1997) Marked Differences in Functioning of the Hypothalamic-Pituitary-Adrenal Axis between Groups of Men. Journal Applied Physiology, 82, 1979-1988.
[36] Lekkakou, L., Tzanela, M., Lymberi, M., Consoulas, C., Tsagarakis, S. and Koutsilieris, M. (2013) Effects of Gender and Age on Hypothalamic-Pituitary-Adrenal Reactivity after Pharmacological Challenge with Low-Dose 1-μg ACTH Test: A Prospective Study in Healthy Adults. Clinical Endocrinology, 79, 683-688.
http://dx.doi.org/10.1111/cen.12198
[37] Duggal, N.A., Upton, J., Phillips, A.C., Hampson, P. and Lord, J.M. (2013) Depressive Symptoms Are Associated with Reduced Neutrophil Function in Hip Fracture Patients. Brain, Behavior, Immunity, 33, 173-182.
http://dx.doi.org/10.1016/j.bbi.2013.07.004
[38] Ferrari, E., Cravello, L., Muzzoni, B., Casarotti, D., Paltro, M., Solerte, S.B., Fioravanti, M., Cuzzoni, G., Pontiggia, B. and Magri, F. (2001) Age-Related Changes of the Hypothalamic-Pituitary-Adrenal Axis: Pathophysiological Correlates. European Journal of Endocrinology, 144, 319-329.
http://dx.doi.org/10.1530/eje.0.1440319
[39] Grillon, C., Pine, D.S., Baas, J.M., Lawley, M., Ellis, V. and Charney, D. (2006) Cortisol and DHEA-S Are Associated with Startle Potentiation during Aversive Conditioning in Humans. Psychopharmacology, 186, 434-441.
http://dx.doi.org/10.1007/s00213-005-0124-2
[40] Perez-Neri, I., Montes, S., Ojeda-Lopez, C., Ramirez-Bermudez, J. and Rios, C. (2008) Modulation of Neurotransmitter Systems by Dehydroepiandrosterone and Dehydroepiandrosterone Sulfate: Mechanism of Action and Relevance to Psychiatric Disorders. Progress in Neuropsychopharmacology and Biological Psychiatry, 32, 1118-1130.
http://dx.doi.org/10.1016/j.pnpbp.2007.12.001
[41] Kassi, E.N. and Chrousos, G.P. (2013) The Central CLOCK System and Stress Axis in Health and Disease. Hormones, 12, 172-191.
http://dx.doi.org/10.14310/horm.2002.1402
[42] Blevins, J.K., Coxworth, J.E., Herndon, J.G. and Hawkes, K. (2013) Adrenal Androgens and Aging: Female Chimpanzees (Pan troglodytes) Compared with Women. American Journal of Physical Anthropology, 151, 643-648.
http://dx.doi.org/10.1002/ajpa.22300
[43] Takeshita, R.S.C., Huffman, M.A., Bercovitch, F.B., Mouri, K. and Shimizu, K. (2013) The Influence of Age and Season on Fecal Dehydroepiandrosterone-Sulfate (DHEAS) Concentrations in Japanese Macaques (Macaca fuscata). General and Comparative Endocrinology, 191, 39-43.
http://dx.doi.org/10.1016/j.ygcen.2013.05.019
[44] Sorwell, K.G., Kohama, S.G. and Urbanski, H.F. (2014) Testosterone Increases Circulating Dehydroepiandrosterone Sulfate Levels in the Male Rhesus Macaque. Frontiers in Endocrinology, 5, 101.
http://dx.doi.org/10.3389/fendo.2014.00101
[45] Petrides, J.S., Mueller, G.P., Kalogeros, K.T., Chrousos, G.P., Gold, P.W. and Deuster, P.A. (1994) Exercise-Induced Activation of the Hypothalamic-Pituitary-Adrenal Axis: Marked Differences in the Sensitivity to Glucocorticoid Suppression. Journal of Clinical Endocrinology and Metabolism, 79, 377-383.
[46] van Londen, L., Goekoop, J.G., van Kempen, G.M., Frankhuijzen-Sierevogel, A.C., Wiegant, V.M., van der Velde, E.A. and De Wied, D. (1997) Plasma Levels of Arginine Vasopressin Elevated in Patients with Major Depression. Neuropsychopharmacology, 17, 284-292.
http://dx.doi.org/10.1016/S0893-133X(97)00054-7
[47] Antoni, F., Fink, G. and Sheward, W. (1990) Corticotrophin-Releasing Peptides in Rat Hypophysial Portal Blood after Paraventricular Lesions: A Marked Reduction in the Concentration of 41-Residue Corticotropin-Releasing Factor, but No Change in Vasopressin. Journal of Endocrinology, 125, 75-183.
http://dx.doi.org/10.1677/joe.0.1250175
[48] Dinan, T.G. and Scott, L.V. (2005) Anatomy of Melancholia: Focus on Hypothalamic-Pituitary-Adrenal Axis Overactivity and the Role of Vasopressin. Journal of Anatomy, 207, 259-264.
http://dx.doi.org/10.1111/j.1469-7580.2005.00443.x
[49] Kalogeras, K.T., Nieman, L.K., Friedman, T.C., Doppman, J.L., Cutler, G.B., Chrousos, G.P., Wilder, R.L., Gold, P.W. and Yanovski, J.A. (1996) Inferior Petrosal Sinus Sampling in Healthy Subjects Reveals a Unilateral Corticotrophin-Releasing Hormone-Induced Arginine Vasopressin Release Associated with Ipsilateral Adrenocorticotropin Secretion. Journal of Clinical Investigations, 97, 2045-2050.
http://dx.doi.org/10.1172/JCI118640
[50] Murgatroyd, C., Patchev, A.V., Wu, Y., Micale, V., Bockmuhl, Y., Fischer, D., Holsboer, F., Wotjak, C.T., Almeida, O.F. and Spengler, D. (2009) Dynamic DNA Methylation Programs Persistent Adverse Effects of Early-Life Stress. Nature Neuroscience, 12, 1559-1566.
http://dx.doi.org/10.1038/nn.2436
[51] Murgatroyd, C. and Spengler, D. (2014) Plycomb Binding Precedes Early-Life Stress Responsive DNA Methylation at the Avp Enhancer. PLoS ONE, 9, e90277.
[52] Purba, J.S., Hoogendijk, W.J., Hofman, M.A. and Swaab, D.F. (1996) Increased Number of Vasopressin- and Oxytocin-Expressing Neurons in the Paraventricular Nucleus of the Hypothalamus in Depression. Archives of General Psychiatry, 53, 137-143.
http://dx.doi.org/10.1001/archpsyc.1996.01830020055007
[53] Aguilera, G. (2011) HPA Axis Responsiveness to Stress: Implications for Healthy Aging. Experimental Gerontology, 46, 90-95.
http://dx.doi.org/10.1016/j.exger.2010.08.023
[54] Roper, J.A., O’Carroll, A.-M., Young, W.S. and Lolait, S.J. (2011) The Vasopressin Avpr1b Receptor: Molecular and Pharmacological Studies. Stress, 14, 98-115.
[55] Serradeil-Le Gal, C., Derick, S., Brossard, G., Manning, M., Simiand, J., Gaillard, R., Griebel, G. and Guillon, G. (2003) Functional and Pharmacological Characterization of the First Specific Agonist and Antagonist for the V1b Receptor in Mammals. Stress, 6, 199-206.
http://dx.doi.org/10.1080/1025389032000114524
[56] Thomson, F. and Craighead, M. (2008) Innovative Approaches for the Treatment of Depression: Targeting the HPA Axis. Neurochemical Research, 33, 691-707.
http://dx.doi.org/10.1007/s11064-007-9518-3

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