Clinical practice and experimental studies have shown that the states of elevated anxiety and depression are often accompanied by impairments to immunity. Investigations over many years have shown that chronic social stress induced by repeated experience of social defeats in daily intermale confrontations leads to the formation of mixed anxiety/depression disorder in mice, which is accompanied by the development of immunosuppression, apparent as a decrease in overall resistance, impairments to humoral and cellular immunity and to proliferation and apoptosis processes in immunocompetent organs, and intensification of oncogenic processes. Primary treatment using anxiolytics and antidepressants to correct psychoemotional status was found to be more effective in the complex correction of psychoneuroimmune impairments than attempts to restore immune measures with the aim of producing therapeutic influences on anxious-depressive states and immunity. A model is proposed for studies of the mechanisms of psychogenic immunodeficiency induced by chronic emotional social stress.
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Anderson, G. and Maes, M., “Bipolar disorder: role of immune-inflammatory cytokines, oxidative and nitrosative stress and tryptophan catabolites,” Curr. Psychiatry Rep., 17, No. 2, 8 (2015).
Anisman, H. and Merali, Z., “Anhedonic and anxiogenic effects of cytokine exposure,” Adv. Exp. Med. Biol., 461, 199–233 (1999).
Avgustinovich, D. F., Alekseenko, O. V., Bakshtanovskaya, et al., “Dynamic changes in the serotoninergic and dopaminergic activity of the brain in the processes of development of anxious depression: an experimental study,” Usp. Fiziol. Nauk., 35, No. 4, 19–40 (2004).
Azpiroz, A., Garmendia, L., Fano, E., and Sanchez-Martin, J. R., “Relations between aggressive behavior, immune activity, and disease susceptibility,” Aggress. Violent Behav., 8, 433–453 (2003).
Azzinnari, D., Sigrist, H., Staehli, S., et al., “Mouse social stress induces increased fear conditioning, helplessness and fatigue to physical challenge together with markers of altered immune and dopamine function,” Neuropharmacology, 85, 328–341 (2014).
Bartolomucci, A., Cabassi, A., Govoni, P., et al., “Metabolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress,” PLoS One, 4, No. 1, e4331 (2009).
Beitia, G., Garmendia, L., Azpiroz, A., et al., “Time-dependent behavioral, neurochemical, and immune consequences of repeated experiences of social defeat stress in male mice and the ameliorative effects of fluoxetine,” Brain Behav. Immun., 19, No. 6, 530–539 (2005).
Borodin, J. I., Kudryavtseva, N. N., Tenditnik, M. V., et al., “Behavioral effects of novel enterosorbent Noolit on mice with mixed depression/anxiety-like state,” Pharmacol. Biochem. Behav., 72, No. 1, 131–141 (2002).
Boyarskikh, U. A., Bondar, N. P., Filipenko, M. L., and Kudryavtseva, N. N., “Downregulation of serotonergic genes expression in the raphe nuclei of midbrain in under chronic social defeat stress in male mice,” Mol. Neurobiol., 48, No. 1, 13–21 (2013).
Brower, V., “Mechanistic research illuminating connection among depression, stress, and survival,” J. Natl. Cancer Inst., 106, No. 3, dju069 (2014).
Carvalho, L. A., Juruena, M. F., Papadopoulos, A. S., et al., “Clomipramine in vitro reduces glucocorticoid receptor function in healthy subjects but not in patients with major depression,” Neuropsychopharmacology, 33, No. 13, 3182–3189 (2008).
Castle, S., Wilkins, S., Heck, E., et al., “Depression in caregivers of demented patients is associated with altered immunity: impaired proliferative capacity, increased CD8+, and a decline in lymphocytes with surface signal transduction molecules (CD38+) and a cytotoxicity marker,” Clin. Exp. Immunol., 101, No. 3, 487–493 (1995).
Davydova, S. M., Cheido, M. A., Gevorgyan, M. M., and Idova, G. V., “Effects of 5-HT2A receptor stimulation and blocking on immune response,” Bull. Exp. Biol. Med., 150, No. 2, 219–221 (2010).
De Miguel, Z., Vegas, O., Garmendia, L., et al., “Behavioral coping strategies in response to social stress are associated with distinct neuroendocrine, monoaminergic and immune response profiles in mice,” Behav. Brain Res., 225, No. 2, 554–561 (2011).
Debnath, M. and Venkatasubramanian, G., “Recent advances in psychoneuroimmunology relevant to schizophrenia therapeutics,” Curr. Opin. Psychiatry, 26, No. 5, 433–439 (2013).
Devoino, L. V., Idova, G. V., Al’perina, E. L., and Cheido, M. A., “The neurochemical system of the brain – an extraimmune mechanism of psychoneuromodulation,” Vestn. RAMN, 9, 19–24 (1998).
Devoino, L. V., Idova, G. V., and Al’perina, E. L., “Psychoneuroimmunomodulation: behavior and immunity,” in: The Role of the Neurotransmitter Set of the Brain, Nauka, Novosibirsk (2009).
Devoino, L., Alperina, E., and Pavina, T., “Immunological consequences of the reversal of social status in C57BL/6J mice,” Brain Behav. Immun., 17, No. 1, 28–34 (2003).
Devoino, L., Alperina, E., Kudryavtseva, N., and Popova, N., “Immune responses in male mice with aggressive and submissive behavior patterns: strain differences,” Brain Behav. Immun., 7, No. 1, 91–96 (1993).
Dhabhar, F. S., “Effects of stress on immune function: the good, the bad, and the beautiful,” Immunol. Res, 58, No. 2–3, 193–210 (2014).
Dhabhar, F. S., Saul, A. N., Holmes, T. H., et al., “High-anxious individuals show increased chronic stress burden, decreased protective immunity, and increased cancer progression in a mouse model of squamous cell carcinoma,” PLoS One, 7, No. 4, e33069 (2012).
Diniz, B. S., Butters, M. A., Albert, S. M., et al., “Late-life depression and risk of vascular dementia and Alzheimer’s disease: systematic review and meta-analysis of community-based cohort studies,” Br. J. Psychiatry, 202, No. 5, 329–335 (2013).
Dowlati, Y., Herrmann, N., Swardfager, W., et al., “A meta-analysis of cytokines in major depression,” Biol. Psychiatry, 67, 446–457 (2010).
DSM-V. Diagnostic and Statistical Manual of Mental Disorders, American Psychiatric Association, Washington DC (2013).
Dubrovina, N. I., Shurlygina, A. V., Litvinenko, G. I., et al., “Behavior, memory, and immunological status in mice with a model of desynchronosis,” Ros. Fiziol. Zh., 101, No. 5, 586–598 (2015).
Duggal, N. A., Beswetherick, A., Upton, J., et al., “Depressive symptoms in hip fracture patients are associated with reduced monocyte superoxide production,” Exp. Gerontol., 54, 27–34 (2014).
Dunn, A. J., Swiergiel, A. H. and de Beaurepaire, R., “Cytokines as mediators of depression: What can we learn from animal studies?” Neurosci. Behav. Rev., 29, 891–909 (2005).
Engler, H., Engler, A., Bailey, M. T., and Sheridan, J. F., “Tissue-specific alterations in the glucocorticoid sensitivity of immune cells following repeated social defeat in mice,” J. Neuroimmunol., 163, No. 1–2, 110–119 (2005).
Fawzy, F. I. and Fawzy, N. W., “A structured psychoeducational intervention for cancer patients,” Gen. Hosp. Psychiatry, 16, No. 3, 149–192 (1994).
Ferragud, A., Haro, A., Sylvain, A., et al., “Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress,” Behav. Brain Res., 210, No. 1, 134–139 (2010).
Fleshner, M., Laudenslager, M. L., Simons, L., and Maier, S. F., “Reduced serum antibodies associated with social defeat in rats,” Physiol. Behav., 45, No. 6, 1183–1187 (1989).
Frank, D., Gauthier, A., and Bergeron, R., “Placebo-controlled doubleblind clomipramine trial for the treatment of anxiety or fear in beagles during ground transport,” Can. Vet. J., 47, No. 11, 1102–1108 (2006).
Freidlin, I. S. and Totolyan, A. A., Cells of the Immune System, St. Petersburg (2001).
Galyamina, A. G., Kovalenko, I. L., Smagin, D. A., and Kudryavtseva, N. N., “The interaction of anxiety and depression in the development of mixed anxious/depressive disorder. An experimental study of the mechanisms of comorbidity. A review,” Zh. Vyssh. Nerv. Deyat., 66, No. 2, 181–201 (2016).
Galyamina, A. G., Kovalenko, I. L., Smagin, D. A., and Kudryavtseva, N. N., “Changes in the expression of neurotransmitter system genes in the ventral tegmental area in depressive mice: RNA-Seq data,” Zh. Vyssh. Nerv. Deyat., 1, 113–118 (2017).
Galyamina, A. G., Smagin, D. A., Kovalenko, I. L., et al., “Effects of diazepam on mixed anxious/depressive disorder in mice,” Ros. Fiziol. Zh., 99, No. 11, 1240–1249 (2013).
Ghosh, M., Garcia-Castillo, D., Aguirre, V., et al., “Proinflammatory cytokine regulation of cyclic AMP-phosphodiesterase 4 signaling in microglia in vitro and following CNS injury,” Glia, 60, No. 12, 1839–1859 (2012).
Gomez-Lazaro, E., Arregi, A., Beitia, G., et al., “Individual differences in chronically defeated male mice: behavioral, endocrine, immune, and neurotrophic changes as markers of vulnerability to the effects of stress,” Stress, 14, No. 5, 537–48 (2011).
Griffiths, J., Ravindran, A. V., Merali, Z., and Anisman, H., “Neuroendocrine measures and lymphocyte subsets in depressive illness: influence of a clinical interview concerning life experiences,” Psychoneuroendocrinology, 22, No. 4, 225–236 (1997).
Grigsby, A. B., Anderson, R. J., Freedland, K. E., et al., “Prevalence of anxiety in adults with diabetes: a systematic review,” J. Psychosom. Res., 53, 1053–1060 (2002).
Gryazeva, N. I., Shurlygina, A. V., Verbitskaya, L. V., et al., “Changes in lactate dehydrogenase and succinate dehydrogenase activities in males with aggressive and submissive types of behavior,” Byull. Eksperim. Biol. Med., 129, No. 10, 53–55 (2000).
Gur, T. L. and Bailey, M. T., “Effects of stress on commensal microbes and immune system activity,” Adv. Exp. Med. Biol., 874, 289–300 (2016).
Gust, D. A., Gordon, T. P., Wilson, M. E., et al., “Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems,” Brain Behav. Immun., 5, No. 3, 296–307 (1991).
Habig, B. and Archie, E. A., “Social status, immune response and parasitism in males: a meta-analysis,” Philos. Trans. R. Soc. Lond. B Biol. Sci., 370, No. 1669, 20140109 (2015).
Herbert, T. B. and Cohen, S., “Depression and immunity: a meta-analytic review,” Psychol. Bull., 113, No. 3, 472–486 (1993).
Holden, J. R., Pakula, I. S., and Mooney, P. A., “A neuroimmunological model of schizophrenia and major depression: a review,” Human Psychopharmacol. Clin. Exp., 12, No. 3, 177–201 (1997).
Howren, M. B., Lamkin, D. M., and Suls, J., “Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis,” Psychosom. Med., 71, No. 2,171–186 (2009).
Idova, G. V., Alperina, E. L., and Cheido, M. A., “Contribution of brain dopamine, serotonin and opioid receptors in the mechanisms of neuroimmunomodulation: evidence from pharmacological analysis,” Int. Immunopharmacol., 12, No. 4, 618–625 (2012).
Idova, G. V., Jur’ev, D. V., Zhukova, E. N., and Kuznetsova, S. M., “Immune response during activation of pre-and postsynaptic serotonin 5-HT(1A) receptors in C57Bl/6J mice at various stages of a depression-like state,” Bull. Exp. Biol. Med., 151, No. 3, 356–358 (2011).
Idova, G. V., Yur’ev, D. V., and Kuznetsova, S. M., “The immune response in inactivation of pre- and postsynaptic serotonin 5-HT1A receptors in mice with a depression-like state,” Ros. Fiziol. Zh., 96, No. 11, 1097–1102 (2010).
Il’nitskaya, S. I., Nikolin, V. P., Popova, N. A., et al., “Effects of ethanol on metastatic process in Lewis adenocarcinoma in male mice with different emotional states,” Ros. Fiziol. Zh., 95, No. 1, 74–78 (2009).
Inglot, A. D., Leszek, J., Piasecki, E., and Sypula, A., “Interferon responses in schizophrenia and major depressive disorders,” Biol. Psychiatry, 35, No. 7, 464–473 (1994).
Irwin, M., Mascovich, A., Gillin, J. C., et al., “Partial sleep deprivation reduces natural killer cell activity in humans,” Psychosom. Med., 56, No. 6, 493–498 (1994).
Ishihara, Y., Matsunaga, K., Iijima, H., et al., “Time-dependent effects of stressor application on metastasis of tumor cells in the lung and its regulation by an immunomodulator in mice,” Psychoneuroendocrinology, 24, 713–726 (1999).
Ito, Y., Mine, K., Ago, Y., et al., “Attack stress and IgE antibody production in rats,” Pharmacol. Biochem. Behav., 19, No. 5, 883–886 (1983).
Iversen, M. M., Nefs, G., Tell, G. S., et al., “Anxiety and depressive symptoms as predictors of all-cause mortality among people with insulin-naïve type 2 diabetes: 17-year follow-up of the second Nord-Trøndelag Health Survey (HUNT2), Norway,” PLoS One, 11, No. 8, e0160861 (2016).
Jaremka, L. M., Lindgren, M. E., and Kiecolt-Glaser, J. K., “Synergistic relationships among stress, depression, and troubled relationships: insights from psychoneuroimmunology,” Depress. Anxiety, 30, No. 4, 288–296 (2013).
Joyce, P. R., Hawes, C. R., Mulder, R. T., et al., “Elevated levels of acute phase plasma proteins in major depression,” Biol. Psychiatry, 32, No. 11, 1035–1041 (1992).
Kaledin, V. I. and Kudryavtseva, N. N., “Social conflict and tumor growth,” Dokl. Akad. Nauk., 234, No. 5, 1117–1120 (1992).
Kaledin, V. I., Ilnitskaya, S. I., Nikolin, V. P., et al., “Limiting effect of diazepam on Lewis lung carcinoma metastasis in anxious male mice,” Exp. Oncol., 31, No. 1, 62–64 (2009).
Kaledin, V. I., Tenditnik, M. V., Nikolin, V. P., et al., “Effects of psychoemotional state on the growth and metastasis of Lewis tumors in mice,” Dokl. Akad. Nauk., 406, No. 2, 272–274 (2006).
Kalueff, A. V. and Murphy, D. L., “The importance of cognitive phenotypes in experimental modeling of animal anxiety and depression,” Neural Plast., 52087 (2007).
Karrenbauer, B. D., Müller, C. P., Ho, Y. J., et al., “Time-dependent in-vivo effects of interleukin-2 on neurotransmitters in various cortices: relationships with depressive-related and anxiety-like behavior,” J. Neuroimmunol., 237, No. 1–2, 23–32 (2011).
Kassano, G. B. and Savino, M., “Depressive syndromes and concomitant anxiety disorders,” Medikografiya, 16, 6–9 (1994).
Katon, W., Pedersen, H. S., Ribe, A. R., et al., “Effect of depression and diabetes mellitus on the risk for dementia: a national population-based cohort study,” JAMA Psychiatry, 72, No. 6, 612–619 (2015).
Kauffman, H. F. and Korf, J., “Lymphocytes as a neural probe: potential for studying psychiatric disorders,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 3, 559–576 (2004).
Kaufman, J. and Charney, D., “Effects of early stress on brain structure and function: implications for understanding the relationship between child maltreatment and depression,” Dev. Psychopathol., 13, No. 3, 451–471 (2001).
Keeney, A. J. and Hogg, S., “Behavioural consequences of repeated social defeat in the mouse: preliminary evaluation of a potential animal model of depression,” Behav. Pharmacol., 10, No. 8, 753–764 (1999).
Kiecolt-Glaser, J. K., Cacioppo, J. T., Malarkey, W. B., and Glaser, R., “Acute psychological stressors and short-term immune changes what, why, for whom, and to what extent?” Psychosom. Med., 54, No. 6, 680–685 (1992).
Knyazev, G. G., Savostyanov, A. N., Bocharov, A. V., and Rimareva, J. M., “Anxiety, depression, and oscillatory dynamics in a social interaction model,” Brain Res., 1644, 62–69 (2016).
Kovalenko, I. L. and Kudryavtseva, N. N., “Development of autistic spectrum symptoms in response to chronic social stress in anxious male mice: effects of diazepam,” Psikhofarmakol. Biol. Narkol., 10, No. 1–2, 2624–2635 (2010).
Kudryavtseva, N. N. and Avgustinovich, D. F., “Behavioral and physiological markers of experimental depression induced by social conflicts (DISC),” Aggress. Behav., 24, 271–286 (1998).
Kudryavtseva, N. N. and Bakshtanovskaya, I. V., “Neurochemical control of aggression and subordination,” Zh. Vyssh. Nerv. Deyat., 41, No. 5, 459–466 (1991).
Kudryavtseva, N. N., Avgustinovich, D. F., Bondar, N. P., et al., “An experimental approach for the study of psychotropic drug effects in simulated clinical conditions,” Curr. Drug Metab., 9, No. 4, 352–360 (2008).
Kudryavtseva, N. N., Bakshtanovskaya, I. V., and Koryakina, L. A., “Social model of depression in mice of C57BL/6J strain,” Pharmacol. Biochem. Behav., 38, 315–320 (1991).
Kudryavtseva, N. N., Shurlygina, A. V., Mel’nikova, E. V., and Trufakin, V. A., “Cell cycle impairments in the thymus and spleen in male mice exposed to chronic social stress: effects of diazepam,” Bull. Exp. Biol. Med., 151, No. 4, 391–394 (2011).
Kudryavtseva, N. N., Shurlygina, A. V., Mel’nikova, E. V., et al., “Cell cycle impairments in the thymus and spleen in male mice in response to chronic social stress: effects of diazepam,” Byull. Eksperim. Biol. Med., 151, No. 4, 391–394 (2011b).
Kudryavtseva, N. N., Smagin, D. A., Galyamina, A. G., et al., “Effects of clomipramine on changes in the subpopulation composition of lymphocytes and the cell cycle in the thymus and spleen arising in depressive male mice in response to chronic social stress,” Psikhofarmakol. Biol. Narkol., 11, No. 1–2, 2677–2687 (2011a).
Kudryavtseva, N. N., Smagin, D. A., Kovalenko, I. L., and Vishnivetskaya, G. B., “Repeated positive fighting experience in male inbred mice,” Nat. Protoc., 9, No. 11, 2705–2017 (2014).
Kudryavtseva, N. N., Smagin, D. A., Kovalenko, I. L., et al., Differentially Expressing Genes in the Brains of C57BL/6J Mice Associated with Agonistic Interactions: Databases. A Collective Monograph, Siberian Branch of the Russian Academy of Sciences Press, Novosibirsk (2016).
Kudryavtseva, N. N., Smagin, D. A., Kovalenko, I. L., et al., “Serotoninergic genes in the development of anxious-depressive behavior in male mice: RNA-Seq data,” Mol. Biol., 51, No. 2, 288–300 (2017).
Kudryavtseva, N. N., Tenditnik, M. V., Nikolin, V. P., et al., “The influence of psychoemotional status on metastasis of Lewis lung carcinoma and hepatocarcinoma-29 in mice of C57BL/6J and CBA/Lac strains,” Exp. Oncol., 29, No. 1, 35–38 (2007).
Kusnecov, A. W. and Rabin, B. S., “Stressor-induced alterations of immune function: mechanisms and issues,” Int. Arch. Allergy Immunol., 105, No. 2, 107–121 (1994).
Laberge, S., Cruikshank, W. W., Beer, D. J., and Center, D. M., “Secretion of IL-16 (lymphocyte chemoattractant factor) from serotonin-stimulated CD8+ T cells in vitro,” J. Immunol., 156, No. 1, 310–315 (1996).
Lacosta, S., Merali, Z., and Anisman, H., “Influence of acute and repeated interleukin-2 administration on spatial learning, locomotor activity, exploratory behaviors, and anxiety,” Behav. Neurosci., 113, No. 5, 1030–1041 (1999).
Lyte, M., Nelson, S. G., and Thompson, M. L., “Innate and adaptive immune responses in a social conflict paradigm,” Clin. Immunol. Immunopathol., 57, No. 1, 137–147 (1990).
Maier, S. F., Watkins, L. R., and Fleshner, M., “Psychoneuroimmunology. The interface between behavior, brain, and immunity,” Am. Psychol., 49, No. 12, 1004–1017 (1994).
Mashkovskii, M. D., Medicines, Novaya Volna, Moscow (2008).
McKinney, W. T. and Bunney, W. E., “Animal model of and depression I. Review of evidence: implications for research,” Arch. Gen. Psychiatry, 21, No. 2, 240–248 (1969).
Morris, G., Berk, M., Galecki, P., et al., “The neuro-immune pathophysiology of central and peripheral fatigue in systemic immune-inflammatory and neuro-immune diseases,” Mol. Neurobiol., 53, No. 2, 1195–219 (2016).
Moynihan, J. A. and Ader, R., “Psychoneuroimmunology: animal models of disease,” Psychosom. Med., 58, No. 6, 546–558 (1996).
Myint, A. M., Schwarz, M. J., Steinbusch, H. W., and Leonard, B. E., “Neuropsychiatric disorders related to interferon and interleukins treatment,” Metab. Brain. Dis., 24, No. 1, 55–68 (2009).
Nagata, T., Yamada, H., Iketani, T., and Kiriike, N. J., “Relationship between plasma concentrations of cytokines, ratio of CD4 and CD8, lymphocyte proliferative responses, and depressive and anxiety state in bulimia nervosa,” Psychosom. Res., 60, No. 1, 99–103 (2006).
O’Connor, T. J. and Leonard, B. E., “Depression, stress and immunological activation: the role of cytokines in depressive disorders,” Life Sci., 62, No. 7, 583–606 (1998).
Popova, N. A., Il’nitskaya, S. I., Kolesnikova, L. A., et al., “Effects of chronic social conflicts on various measures of nonspecific resistance in mice,” Ros. Fiziol. Zh., 82, No. 12, 14–19 (1996).
Prigerson, H. G., Bierhals, A. J., Kasl, S. V., et al., “Traumatic grief as a risk factor for mental and physical morbidity,” Am. J. Psychiatry, 154, No. 5, 616–623 (1997).
Raab, A., Dantzer, R., Michaud, B., et al., “Behavioural, physiological and immunological consequences of social status and aggression in chronically coexisting resident-intruder dyads of male rats,” Physiol. Behav., 36, No. 2, 223–228 (1986).
Ravindran, A. V., Griffiths, J., Merali, Z., and Anisman, H., “Lymphocyte subsets associated with major depression and dysthymia: modification by antidepressant treatment,” Psychosom. Med., 57, No. 6, 555–563 (1995).
Ruesch, M., Helmes, A. W., and Bengel, J., “Immediate help through group therapy for patients with somatic diseases and depressive or adjustment disorders in outpatient care: study protocol for a randomized controlled trial,” Trials, 16, 287 (2015).
Shurlygina, A. V., Galyamina, A. G., Mel’nikova, E. V., et al., “Effects of Roncoleukin on immune deficiency and the anxious-depressive state,” Ros. Fiziol. Zh., 100, No. 2, 201–214 (2014).
Smagin, D. A., Galyamina, A. G., Bondar’, N. P., and Kudryavtseva, N. N., “Effects of clomipramine on the anxious-depressive state induced by chronic social stress in male mice,” Psikhofarmakol. Biol. Narkol., 11, No. 1–2, 2666–2676 (2011).
Smagin, D. A., Galyamina, A. G., Kovalenko, I. L., et al., “Changes in the expression of neurotransmitter genes in the dorsal striatum in mice with motor impairments,” Zh. Vyssh. Nerv. Deyat. (2017) (in press).
Smagin, D. A., Kovalenko, I. L., Galyamina, A. G., et al., “Dysfunction in ribosomal gene expression in the hypothalamus and hippocampus following chronic social defeat stress in male mice as revealed by RNA-seq,” Neural Plast., 3289187 (2016).
Sommershof, A., Basler, M., Riether, C., et al., “Attenuation of the cytotoxic T lymphocyte response to lymphocytic choriomeningitis virus in mice subjected to chronic social stress,” Brain Behav. Immun., 25, No. 2, 340–348 (2011).
Spiegel, D. and Sephton, S. E., “Psychoneuroimmune and endocrine pathways in cancer: effects of stress and support,” Semin. Clin. Neuropsychiatry, 6, 252–265 (2001).
Stefanski, V., Knopf, G., and Schulz, S., “Long-term colony housing in Long Evans rats: immunological, hormonal, and behavioral consequences,” J. Neuroimmunol., 114, No. 1–2, 122–130 (2001).
Stefanski, V., Peschel, A., and Reber, S., “Social stress affects migration of blood T cells into lymphoid organs,” J. Neuroimmunol., 138, No. 1–2, 17–24 (2003).
Stein, M., Miller, A. H., and Trestman, R. L., “Depression, the immune system, and health and illness. Findings in search of meaning,” Arch. Gen. Psychiatry, 48, No. 2, 171–177 (1991).
Stewart, A. M., Roy, S., Wong, K., et al., “Cytokine and endocrine parameters in mouse chronic social defeat: implications for translational ‘cross-domain’ modeling of stress-related brain disorders,” Behav. Brain Res., 276, 84–91 (2015).
Strange, K. S., Kerr, L. R., Andrews, H. N., et al., “Psychosocial stressors and mammary tumor growth: an animal model,” Neurotoxicol. Teratol., 22, 89–102 (2000).
Taler, M., Bar, M., Korob, I., et al., “Evidence for an inhibitory immunomodulatory effect of selected antidepressants on rat splenocytes: possible relevance to depression and hyperactive-immune disorders,” Int. Immunopharmacol., 8, No. 4, 526-533 (2008).
Tam, C. W. and Lam, L. C., “Cognitive function, functional performance and severity of depression in Chinese older persons with late-onset depression,” East Asian Arch. Psychiatry, 22, No. 1, 12–71 (2012).
Tenditnik, M. V., Shurlygina, A. V., Mel’nikova, E. V., et al., “Changes in the lymphocyte subpopulation composition in the immunocompetent organs of I mean, ice in response to chronic social stress,” Ros. Fiziol. Zh., 90, No. 12, 1522–1529 (2004).
Tenditnik, M. V., Shurlygina, A. V., Mel’nikova, E. V., et al., “Effects of diazepam on the lymphocyte subpopulation composition in the organs of anxious male mice,” Byull. Sib. Otdel Ross. Akad. Med. Nauk., 30, No. 4, 46–50 (2010).
Tsankova, N. M., Berton, O., Renthal, W., et al., “Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action,” Nat. Neurosci., 9, No. 4, 519–525 (2006).
Van Bokhoven, P., Oomen, C. A., Hoogendijk, W. J., et al., “Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment,” Eur. J. Neurosci., 33, No. 10, 1833–1840 (2011).
Vegas, O., Beitia, G., Sánchez-Martin, J. R., et al., “Behavioral and neurochemical responses in mice bearing tumors submitted to social stress,” Behav. Brain Res., 155, 125–134 (2004).
Vegas, O., Garmendia, L., Arregi, A., et al., “Effects of antalarmin and nadolol on the relationship between social stress and pulmonary metastasis development in male OF1 mice,” Behav. Brain Res., 205, No. 1, 200–206 (2009).
Wong, K., Tan, J., Cachet, J., et al., “Cytokine profiling of chronic social defeat in mice,” FASEB J., 24, No. 1, 768, 2 (2010).
Zachariae, R., “Psychoneuroimmunology: a bio-psycho-social approach to health and disease.” Scand. J. Psychol., 50, No. 6, 645–651 (2009).
Zhu, J., Bengtsson, B. O., Mix, E., et al., “Clomipramine and imipramine suppress clinical signs and T and B cell response to myelin proteins in experimental autoimmune neuritis in Lewis rats,” J. Autoimmun., 11, No. 4, 319–327 (1998).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 67, No. 6, pp. 671–692, November–December, 2017.
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Kudryavtseva, N.N., Shurlygina, A.V., Galyamina, A.G. et al. Immunopathology of Mixed Anxiety/Depression Disorders: An Experimental Approach to Studies of Immunodeficiency States (review). Neurosci Behav Physi 49, 384–398 (2019). https://doi.org/10.1007/s11055-019-00745-9
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DOI: https://doi.org/10.1007/s11055-019-00745-9