Neuroscience and Behavioral Physiology

, Volume 49, Issue 3, pp 384–398 | Cite as

Immunopathology of Mixed Anxiety/Depression Disorders: An Experimental Approach to Studies of Immunodeficiency States (review)

  • N. N. KudryavtsevaEmail author
  • A. V. Shurlygina
  • A. G. Galyamina
  • D. A. Smagin
  • I. L. Kovalenko
  • N. A. Popova
  • V. P. Nikolin
  • S. I. Ilnitskaya
  • E. V. Melnikova
  • V. A. Trufakin

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.


depression anxiety chronic social stress immunodeficient states 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 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).Google Scholar
  2. Anisman, H. and Merali, Z., “Anhedonic and anxiogenic effects of cytokine exposure,” Adv. Exp. Med. Biol., 461, 199–233 (1999).Google Scholar
  3. 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).Google Scholar
  4. 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).Google Scholar
  5. 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).Google Scholar
  6. 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).Google Scholar
  7. 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).Google Scholar
  8. 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).Google Scholar
  9. 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).Google Scholar
  10. Brower, V., “Mechanistic research illuminating connection among depression, stress, and survival,” J. Natl. Cancer Inst., 106, No. 3, dju069 (2014).Google Scholar
  11. 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).Google Scholar
  12. 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).Google Scholar
  13. 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).Google Scholar
  14. 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).Google Scholar
  15. Debnath, M. and Venkatasubramanian, G., “Recent advances in psychoneuroimmunology relevant to schizophrenia therapeutics,” Curr. Opin. Psychiatry, 26, No. 5, 433–439 (2013).Google Scholar
  16. 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).Google Scholar
  17. 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).Google Scholar
  18. 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).Google Scholar
  19. 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).Google Scholar
  20. 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).Google Scholar
  21. 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).Google Scholar
  22. 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).Google Scholar
  23. Dowlati, Y., Herrmann, N., Swardfager, W., et al., “A meta-analysis of cytokines in major depression,” Biol. Psychiatry, 67, 446–457 (2010).Google Scholar
  24. DSM-V. Diagnostic and Statistical Manual of Mental Disorders, American Psychiatric Association, Washington DC (2013).Google Scholar
  25. 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).Google Scholar
  26. 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).Google Scholar
  27. 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).Google Scholar
  28. 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).Google Scholar
  29. Fawzy, F. I. and Fawzy, N. W., “A structured psychoeducational intervention for cancer patients,” Gen. Hosp. Psychiatry, 16, No. 3, 149–192 (1994).Google Scholar
  30. 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).Google Scholar
  31. 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).Google Scholar
  32. 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).Google Scholar
  33. Freidlin, I. S. and Totolyan, A. A., Cells of the Immune System, St. Petersburg (2001).Google Scholar
  34. 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).Google Scholar
  35. 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).Google Scholar
  36. 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).Google Scholar
  37. 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).Google Scholar
  38. 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).Google Scholar
  39. 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).Google Scholar
  40. 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).Google Scholar
  41. 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).Google Scholar
  42. 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).Google Scholar
  43. 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).Google Scholar
  44. 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).Google Scholar
  45. Herbert, T. B. and Cohen, S., “Depression and immunity: a meta-analytic review,” Psychol. Bull., 113, No. 3, 472–486 (1993).Google Scholar
  46. 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).Google Scholar
  47. 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).Google Scholar
  48. 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).Google Scholar
  49. 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).Google Scholar
  50. 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).Google Scholar
  51. 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).Google Scholar
  52. 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).Google Scholar
  53. 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).Google Scholar
  54. 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).Google Scholar
  55. 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).Google Scholar
  56. 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).Google Scholar
  57. 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).Google Scholar
  58. 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).Google Scholar
  59. Kaledin, V. I. and Kudryavtseva, N. N., “Social conflict and tumor growth,” Dokl. Akad. Nauk., 234, No. 5, 1117–1120 (1992).Google Scholar
  60. 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).Google Scholar
  61. 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).Google Scholar
  62. Kalueff, A. V. and Murphy, D. L., “The importance of cognitive phenotypes in experimental modeling of animal anxiety and depression,” Neural Plast., 52087 (2007).Google Scholar
  63. 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).Google Scholar
  64. Kassano, G. B. and Savino, M., “Depressive syndromes and concomitant anxiety disorders,” Medikografiya, 16, 6–9 (1994).Google Scholar
  65. 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).Google Scholar
  66. Kauffman, H. F. and Korf, J., “Lymphocytes as a neural probe: potential for studying psychiatric disorders,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 3, 559–576 (2004).Google Scholar
  67. 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).Google Scholar
  68. 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).Google Scholar
  69. 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).Google Scholar
  70. 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).Google Scholar
  71. 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).Google Scholar
  72. 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).Google Scholar
  73. Kudryavtseva, N. N. and Bakshtanovskaya, I. V., “Neurochemical control of aggression and subordination,” Zh. Vyssh. Nerv. Deyat., 41, No. 5, 459–466 (1991).Google Scholar
  74. 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).Google Scholar
  75. 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).Google Scholar
  76. 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).Google Scholar
  77. 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).Google Scholar
  78. 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).Google Scholar
  79. 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).Google Scholar
  80. 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).Google Scholar
  81. 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).Google Scholar
  82. 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).Google Scholar
  83. 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).Google Scholar
  84. 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).Google Scholar
  85. 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).Google Scholar
  86. 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).Google Scholar
  87. 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).Google Scholar
  88. Mashkovskii, M. D., Medicines, Novaya Volna, Moscow (2008).Google Scholar
  89. 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).Google Scholar
  90. 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).Google Scholar
  91. Moynihan, J. A. and Ader, R., “Psychoneuroimmunology: animal models of disease,” Psychosom. Med., 58, No. 6, 546–558 (1996).Google Scholar
  92. 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).Google Scholar
  93. 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).Google Scholar
  94. 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).Google Scholar
  95. 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).Google Scholar
  96. 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).Google Scholar
  97. 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).Google Scholar
  98. 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).Google Scholar
  99. 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).Google Scholar
  100. 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).Google Scholar
  101. 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).Google Scholar
  102. 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).Google Scholar
  103. 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).Google Scholar
  104. 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).Google Scholar
  105. Spiegel, D. and Sephton, S. E., “Psychoneuroimmune and endocrine pathways in cancer: effects of stress and support,” Semin. Clin. Neuropsychiatry, 6, 252–265 (2001).Google Scholar
  106. 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).Google Scholar
  107. 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).Google Scholar
  108. 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).Google Scholar
  109. 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).Google Scholar
  110. 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).Google Scholar
  111. 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).Google Scholar
  112. 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).Google Scholar
  113. 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).Google Scholar
  114. 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).Google Scholar
  115. 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).Google Scholar
  116. 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).Google Scholar
  117. 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).Google Scholar
  118. 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).Google Scholar
  119. Wong, K., Tan, J., Cachet, J., et al., “Cytokine profiling of chronic social defeat in mice,” FASEB J., 24, No. 1, 768, 2 (2010).Google Scholar
  120. Zachariae, R., “Psychoneuroimmunology: a bio-psycho-social approach to health and disease.” Scand. J. Psychol., 50, No. 6, 645–651 (2009).Google Scholar
  121. 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).Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • N. N. Kudryavtseva
    • 1
    Email author
  • A. V. Shurlygina
    • 2
  • A. G. Galyamina
    • 1
  • D. A. Smagin
    • 1
  • I. L. Kovalenko
    • 1
  • N. A. Popova
    • 1
  • V. P. Nikolin
    • 1
  • S. I. Ilnitskaya
    • 1
  • E. V. Melnikova
    • 2
  • V. A. Trufakin
    • 2
  1. 1.Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of SciencesNovosibirskRussia
  2. 2.Research Institute of Clinical and Experimental Lymphology, Branch of the Institute of Cytology and Genetics, Siberian Branch, Russian Academy of SciencesNovosibirskRussia

Personalised recommendations