The protective effects of resveratrol on social stress-induced cytokine release and depressive-like behavior

Brain, Behavior, and Immunity

Volumn 59, Issue , 2017, Pages 147-157

  Finnell, Julie E ^a   Lombard, Calliandra M ^a   Melson, Michael N ^a   Singh, Narendra P ^a   Nagarkatti, Mitzi ^a   Nagarkatti, Prakash ^a   Fadel, James R ^a   Wood, Christopher S ^a   Wood, Susan K ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Coping; Depression; Inflammation; Resveratrol; Social stress

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; RESVERATROL; SEROTONIN; SIRTUIN 1; TUMOR NECROSIS FACTOR; ANTIOXIDANT; CYTOKINE; STILBENE DERIVATIVE;

ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDEPRESSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; COPING BEHAVIOR; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEPRESSION; DORSAL RAPHE NUCLEUS; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INFLAMMATION; LOCUS CERULEUS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; REMISSION; RISK FACTOR; SOCIAL STRESS; SPLEEN CELL; SUCROSE PREFERENCE TEST; ANIMAL; DOSE RESPONSE; LONG EVANS RAT; MALE; MENTAL STRESS; METABOLISM; PSYCHOLOGY; RAPHE NUCLEUS; SOCIAL ENVIRONMENT; SPLEEN; SPRAGUE DAWLEY RAT;

ADAPTATION, PSYCHOLOGICAL; ANHEDONIA; ANIMALS; ANTIOXIDANTS; CYTOKINES; DEPRESSIVE DISORDER; DOSE-RESPONSE RELATIONSHIP, DRUG; LOCUS COERULEUS; MALE; RAPHE NUCLEI; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; SOCIAL ENVIRONMENT; SPLEEN; STILBENES; STRESS, PSYCHOLOGICAL;

EID: 84994844569     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.08.019     Document Type: Article

References (102)

1. Ahmed, R.F., Abdel-Rahman, R.F., Farid, O.a.H.a., El-Marasy, S.a., Hessin, A.F., Combined hepatoprotective and antidepressant effects of resveratrol in an acute model of depression. Bull. Fac. Pharm., Cairo University 52 (2014), 191–197.
2. Alesci, S., Martinez, P.E., Kelkar, S., Ilias, I., Ronsaville, D.S., Listwak, S.J., Ayala, A.R., Licinio, J., Gold, H.K., Kling, M.A., Chrousos, G.P., Gold, P.W., Major depression is associated with significant diurnal elevations in plasma interleukin-6 levels, a shift of its circadian rhythm, and loss of physiological complexity in its secretion: clinical implications. J. Clin. Endocrinol. Metab. 90 (2005), 2522–2530.
3. Almeida, D.M., Resilience and vulnerability to daily stressors assessed via diary methods. Curr. Dir. Psychol. Sci. 14 (2005), 64–68.
4. Almeida, L., Vaz-da-Silva, M., Falcao, A., Soares, E., Costa, R., Loureiro, A.I., Fernandes-Lopes, C., Rocha, J.F., Nunes, T., Wright, L., Soares-da-Silva, P., Pharmacokinetic and safety profile of trans-resveratrol in a rising multiple-dose study in healthy volunteers. Mol. Nutr. Food Res. 53:Suppl. 1 (2009), S7–S15.
5. Aston-Jones, G., Shipley, M.T., Grzanna, R., The locus coeruleus, A5 and A7 noradrenergic cell groups. Paxinos, G., (eds.) The Rat Brain, 1995, Academic Press, 183–213.
6. Audet, M.C., Jacobson-Pick, S., Wann, B.P., Anisman, H., Social defeat promotes specific cytokine variations within the prefrontal cortex upon subsequent aggressive or endotoxin challenges. Brain Behav. Immun. 25 (2011), 1197–1205.
7. Bagul, P.K., Deepthi, N., Sultana, R., Banerjee, S.K., Resveratrol ameliorates cardiac oxidative stress in diabetes through deacetylation of NFkB-p65 and histone 3. J. Nutr. Biochem. 26 (2015), 1298–1307.
8. Borra, M.T., Smith, B.C., Denu, J.M., Mechanism of human SIRT1 activation by resveratrol. J. Biol. Chem. 280 (2005), 17187–17195.
9. Borsody, M.K., Weiss, J.M., Alteration of locus coeruleus neuronal activity by interleukin-1 and the involvement of endogenous corticotropin-releasing hormone. NeuroImmunoModulation 10 (2002), 101–121.
10. Borsody, M.K., Weiss, J.M., The effects of endogenous interleukin-1 bioactivity on locus coeruleus neurons in response to bacterial and viral substances. Brain Res. 1007 (2004), 39–56.
11. Bouhuys, A.L., Flentge, F., Oldehinkel, A.J., van den Berg, M.D., Potential psychosocial mechanisms linking depression to immune function in elderly subjects. Psychiatry Res. 127 (2004), 237–245.
12. Cairns, K.E., Yap, M.B., Pilkington, P.D., Jorm, A.F., Risk and protective factors for depression that adolescents can modify: a systematic review and meta-analysis of longitudinal studies. J. Affect. Disord. 169 (2014), 61–75.
13. Chaijale, N.N., Curtis, A.L., Wood, S.K., Zhang, X.Y., Bhatnagar, S., Reyes, B.A., Van Bockstaele, E.J., Valentino, R.J., Social stress engages opioid regulation of locus coeruleus norepinephrine neurons and induces a state of cellular and physical opiate dependence. Neuropsychopharmacology 38 (2013), 1833–1843.
14. Cheng, F.C., Kuo, J.S., Chia, L.G., Tsai, T.H., Chen, C.F., Rapid measurement of the monoamine content in small volumes of rat plasma. J. Chromatogr. B, Biomed. Appl. 654 (1994), 177–183.
15. de la Lastra, C.A., Villegas, I., Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Mol. Nutr. Food Res. 49 (2005), 405–430.
16. De Miguel, Z., Vegas, O., Garmendia, L., Arregi, A., Beitia, G., Azpiroz, A., Behavioral coping strategies in response to social stress are associated with distinct neuroendocrine, monoaminergic and immune response profiles in mice. Behav. Brain Res. 225 (2011), 554–561.
17. Devorak, J., Torres-Platas, S.G., Davoli, M.A., Prud'homme, J., Turecki, G., Mechawar, N., Cellular and molecular inflammatory profile of the choroid plexus in depression and suicide. Front. Psychiatry, 6, 2015, 138.
18. Dominguez-Gerpe, L., Rey-Mendez, M., Alterations induced by chronic stress in lymphocyte subsets of blood and primary and secondary immune organs of mice. BMC Immunol., 2, 2001, 7.
19. Donnelly, L.E., Newton, R., Kennedy, G.E., Fenwick, P.S., Leung, R.H., Ito, K., Russell, R.E., Barnes, P.J., Anti-inflammatory effects of resveratrol in lung epithelial cells: molecular mechanisms. Am. J. Physiol. Lung Cell. Mol. Physiol. 287 (2004), L774–L783.
20. Duggal, N.A., Upton, J., Phillips, A.C., Hampson, P., Lord, J.M., Depressive symptoms post hip fracture in older adults are associated with phenotypic and functional alterations in T cells. Immun. Ageing: I & A, 11, 2014, 25.
21. DuPage, M., Bluestone, J.A., Harnessing the plasticity of CD4(+) T cells to treat immune-mediated disease. Nat. Rev. Immunol. 16 (2016), 149–163.
22. Eilat, E., Mendlovic, S., Doron, A., Zakuth, V., Spirer, Z., Increased apoptosis in patients with major depression: a preliminary study. J. Immunol. (Baltimore, Md.: 1950) 163 (1999), 533–534.
23. Eyre, H.A., Air, T., Proctor, S., Rositano, S., Baune, B.T., A critical review of the efficacy of non-steroidal anti-inflammatory drugs in depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 57 (2015), 11–16.
24. Falchetti, R., Fuggetta, M.P., Lanzilli, G., Tricarico, M., Ravagnan, G., Effects of resveratrol on human immune cell function. Life Sci. 70 (2001), 81–96.
25. Fonken, L.K., Weber, M.D., Daut, R.A., Kitt, M.M., Frank, M.G., Watkins, L.R., Maier, S.F., Stress-induced neuroinflammatory priming is time of day dependent. Psychoneuroendocrinology 66 (2016), 82–90.
26. Fordham, J.B., Naqvi, A.R., Nares, S., Leukocyte production of inflammatory mediators is inhibited by the antioxidants phloretin, silymarin, hesperetin, and resveratrol. Mediators Inflamm., 2014, 2014, 938712.
27. Foxwell, A.R., Kyd, J.M., Cripps, A.W., Kinetics of inflammatory cytokines in the clearance of non-typeable Haemophilus influenzae from the lung. Immunol. Cell Biol. 76 (1998), 556–559.
28. Frank, M.G., Watkins, L.R., Maier, S.F., Stress- and glucocorticoid-induced priming of neuroinflammatory responses: potential mechanisms of stress-induced vulnerability to drugs of abuse. Brain Behav. Immun. 25:Suppl. 1 (2011), S21–S28.
29. Frank, M.G., Thompson, B.M., Watkins, L.R., Maier, S.F., Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav. Immun. 26 (2012), 337–345.
30. Fuertig, R., Azzinnari, D., Bergamini, G., Cathomas, F., Sigrist, H., Seifritz, E., Vavassori, S., Luippold, A., Hengerer, B., Ceci, A., Pryce, C.R., Mouse chronic social stress increases blood and brain kynurenine pathway activity and fear behaviour: both effects are reversed by inhibition of indoleamine 2,3-dioxygenase. Brain Behav. Immun. 54 (2016), 59–72.
31. Gillies, S.D., Young, D., Lo, K.M., Roberts, S., Biological activity and in vivo clearance of antitumor antibody/cytokine fusion proteins. Bioconjug. Chem. 4 (1993), 230–235.
32. Gomez-Lazaro, E., Arregi, A., Beitia, G., Vegas, O., Azpiroz, A., Garmendia, L., Individual differences in chronically defeated male mice: behavioral, endocrine, immune, and neurotrophic changes as markers of vulnerability to the effects of stress. Stress (Amsterdam, Netherlands) 14 (2011), 537–548.
33. Guillemin, G.J., Smith, D.G., Smythe, G.A., Armati, P.J., Brew, B.J., Expression of the kynurenine pathway enzymes in human microglia and macrophages. Adv. Exp. Med. Biol. 527 (2003), 105–112.
34. Hammels, C., Pishva, E., De Vry, J., van den Hove, D.L., Prickaerts, J., van Winkel, R., Selten, J.P., Lesch, K.P., Daskalakis, N.P., Steinbusch, H.W., van Os, J., Kenis, G., Rutten, B.P., Defeat stress in rodents: from behavior to molecules. Neurosci. Biobehav. Rev. 59 (2015), 111–140.
35. Haslund-Vinding, J., McBean, G., Jaquet, V., Vilhardt, F., NADPH oxidases in microglia oxidant production: activating receptors, pharmacology, and association with disease. Br. J. Pharmacol., 2016.
36. Heidt, T., Sager, H.B., Courties, G., Dutta, P., Iwamoto, Y., Zaltsman, A., von Zur Muhlen, C., Bode, C., Fricchione, G.L., Denninger, J., Lin, C.P., Vinegoni, C., Libby, P., Swirski, F.K., Weissleder, R., Nahrendorf, M., Chronic variable stress activates hematopoietic stem cells. Nat. Med. 20 (2014), 754–758.
37. Hochstrasser, T., Ullrich, C., Sperner-Unterweger, B., Humpel, C., Inflammatory stimuli reduce survival of serotonergic neurons and induce neuronal expression of indoleamine 2,3-dioxygenase in rat dorsal raphe nucleus organotypic brain slices. Neuroscience 184 (2011), 128–138.
38. Hodes, G.E., Pfau, M.L., Leboeuf, M., Golden, S.A., Christoffel, D.J., Bregman, D., Rebusi, N., Heshmati, M., Aleyasin, H., Warren, B.L., Lebonte, B., Horn, S., Lapidus, K.A., Stelzhammer, V., Wong, E.H., Bahn, S., Krishnan, V., Bolanos-Guzman, C.A., Murrough, J.W., Merad, M., Russo, S.J., Individual differences in the peripheral immune system promote resilience versus susceptibility to social stress. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 16136–16141.
39. Hong, S.P., Choi, D.H., Choi, J.S., Effects of resveratrol on the pharmacokinetics of diltiazem and its major metabolite, desacetyldiltiazem, in rats. Cardiovasc. Ther. 26 (2008), 269–275.
40. Hurley, L.L., Akinfiresoye, L., Kalejaiye, O., Tizabi, Y., Antidepressant effects of resveratrol in an animal model of depression. Behav. Brain Res. 268 (2014), 1–7.
41. Ivanova, S.A., Semke, V.Y., Vetlugina, T.P., Rakitina, N.M., Kudyakova, T.A., Simutkin, G.G., Signs of apoptosis of immunocompetent cells in patients with depression. Neurosci. Behav. Physiol. 37 (2007), 527–530.
42. Kamikawa, H., Hori, T., Nakane, H., Aou, S., Tashiro, N., IL-1beta increases norepinephrine level in rat frontal cortex: involvement of prostanoids, NO, and glutamate. Am. J. Physiol. 275 (1998), R803–R810.
43. Kanarik, M., Alttoa, A., Matrov, D., Koiv, K., Sharp, T., Panksepp, J., Harro, J., Brain responses to chronic social defeat stress: effects on regional oxidative metabolism as a function of a hedonic trait, and gene expression in susceptible and resilient rats. Eur. Neuropsychopharmacol. 21 (2011), 92–107.
44. Kern, S., Skoog, I., Borjesson-Hanson, A., Blennow, K., Zetterberg, H., Ostling, S., Kern, J., Gudmundsson, P., Marlow, T., Rosengren, L., Waern, M., Higher CSF interleukin-6 and CSF interleukin-8 in current depression in older women. Results from a population-based sample. Brain Behav. Immun. 41 (2014), 55–58.
45. Kessler, R.C., Berglund, P., Demler, O., Jin, R., Merikangas, K.R., Walters, E.E., Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch. Gen. Psychiatry 62 (2005), 593–602.
46. Korte, S.M., Buwalda, B., Bouws, G.A., Koolhaas, J.M., Maes, F.W., Bohus, B., Conditioned neuroendocrine and cardiovascular stress responsiveness accompanying behavioral passivity and activity in aged and in young rats. Physiol. Behav. 51 (1992), 815–822.
47. Krishnan, V., Nestler, E.J., The molecular neurobiology of depression. Nature 455 (2008), 894–902.
48. la Porte, C., Voduc, N., Zhang, G., Seguin, I., Tardiff, D., Singhal, N., Cameron, D.W., Steady-state pharmacokinetics and tolerability of trans-resveratrol 2000 mg twice daily with food, quercetin and alcohol (ethanol) in healthy human subjects. Clin. Pharmacokinet. 49 (2010), 449–454.
49. Langcake, P., Pryce, R.J., The production of resveratrol by Vitis vinifera and other members of the Vitaceae as a response to infection or injury. Physiol. Plant Pathol. 9 (1976), 77–86.
50. Lechin, F., van der Dijs, B., Hernandez-Adrian, G., Dorsal raphe vs. median raphe serotonergic antagonism. Anatomical, physiological, behavioral, neuroendocrinological, neuropharmacological and clinical evidences: relevance for neuropharmacological therapy. Prog. Neuropsychopharmacol. Biol. Psychiatry 30 (2006), 565–585.
51. Lestage, J., Verrier, D., Palin, K., Dantzer, R., The enzyme indoleamine 2,3-dioxygenase is induced in the mouse brain in response to peripheral administration of lipopolysaccharide and superantigen. Brain Behav. Immun. 16 (2002), 596–601.
52. Li, R., Zhao, D., Qu, R., Fu, Q., Ma, S., The effects of apigenin on lipopolysaccharide-induced depressive-like behavior in mice. Neurosci. Lett. 594 (2015), 17–22.
53. Llorens-Martin, M., Jurado-Arjona, J., Bolos, M., Pallas-Bazarra, N., Avila, J., Forced swimming sabotages the morphological and synaptic maturation of newborn granule neurons and triggers a unique pro-inflammatory milieu in the hippocampus. Brain Behav. Immun. 53 (2016), 242–254.
54. Maes, M., Bosmans, E., De Jongh, R., Kenis, G., Vandoolaeghe, E., Neels, H., Increased serum IL-6 and IL-1 receptor antagonist concentrations in major depression and treatment resistant depression. Cytokine 9 (1997), 853–858.
55. Matin, A., Streete, I.M., Jamie, I.M., Truscott, R.J., Jamie, J.F., A fluorescence-based assay for indoleamine 2,3-dioxygenase. Anal. Biochem. 349 (2006), 96–102.
56. Miczek, K.A., A new test for aggression in rats without aversive stimulation: differential effects of d-amphetamine and cocaine. Psychopharmacol. Berl. 60 (1979), 253–259.
57. Miller, G.E., Stetler, C.A., Carney, R.M., Freedland, K.E., Banks, W.A., Clinical depression and inflammatory risk markers for coronary heart disease. Am. J. Cardiol. 90 (2002), 1279–1283.
58. Motivala, S.J., Sarfatti, A., Olmos, L., Irwin, M.R., Inflammatory markers and sleep disturbance in major depression. Psychosom. Med. 67 (2005), 187–194.
59. Musselman, D.L., Miller, A.H., Porter, M.R., Manatunga, A., Gao, F., Penna, S., Pearce, B.D., Landry, J., Glover, S., McDaniel, J.S., Nemeroff, C.B., Higher than normal plasma interleukin-6 concentrations in cancer patients with depression: preliminary findings. Am. J. Psychiatry 158 (2001), 1252–1257.
60. National Institute of Mental Health, 2013a. Major Depression among Adolescents. http://www.nimh.nih.gov/health/statistics/prevalence/major-depression-among-adolescents.shtml.
61. National Institute of Mental Health, 2013b. Major Depression Among Adults. http://www.nimh.nih.gov/health/statistics/prevelence/major-depression-amongadults.shtml.
62. Olas, B., Wachowicz, B., Resveratrol reduces oxidative stress induced by platinum compounds in blood platelets. Gen. Physiol. Biophys. 23 (2004), 315–326.
63. Pablos, P., Mendiguren, A., Pineda, J., Contribution of nitric oxide-dependent guanylate cyclase and reactive oxygen species signaling pathways to desensitization of mu-opioid receptors in the rat locus coeruleus. Neuropharmacology 99 (2015), 422–431.
64. Page, M.E., Abercrombie, E.D., Discrete local application of corticotropin-releasing factor increases locus coeruleus discharge and extracellular norepinephrine in rat hippocampus. Synapse 33 (1999), 304–313.
65. Patki, G., Allam, F.H., Atrooz, F., Dao, A.T., Solanki, N., Chugh, G., Asghar, M., Jafri, F., Bohat, R., Alkadhi, K.A., Salim, S., Grape powder intake prevents ovariectomy-induced anxiety-like behavior, memory impairment and high blood pressure in female Wistar rats. PLoS ONE, 8, 2013, e74522.
66. Patki, G., Solanki, N., Atrooz, F., Allam, F., Salim, S., Depression, anxiety-like behavior and memory impairment are associated with increased oxidative stress and inflammation in a rat model of social stress. Brain Res. 1539 (2013), 73–86.
67. Perez-Tejada, J., Arregi, A., Gomez-Lazaro, E., Vegas, O., Azpiroz, A., Garmendia, L., Coping with chronic social stress in mice: hypothalamic-pituitary-adrenal/sympathetic-adrenal-medullary axis activity, behavioral changes and effects of antalarmin treatment: implications for the study of stress-related psychopathologies. Neuroendocrinology 98 (2013), 73–88.
68. Pfau, M.L., Russo, S.J., Peripheral and central mechanisms of stress resilience. Neurobiol. Stress 1 (2015), 66–79.
69. Raison, C.L., Rutherford, R.E., Woolwine, B.J., Shuo, C., Schettler, P., Drake, D.F., Haroon, E., Miller, A.H., A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: the role of baseline inflammatory biomarkers. JAMA Psychiatry 70 (2013), 31–41.
70. Renthal, W., Maze, I., Krishnan, V., Covington, H.E. 3rd, Xiao, G., Kumar, A., Russo, S.J., Graham, A., Tsankova, N., Kippin, T.E., Kerstetter, K.A., Neve, R.L., Haggarty, S.J., McKinsey, T.A., Bassel-Duby, R., Olson, E.N., Nestler, E.J., Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56 (2007), 517–529.
71. Ressler, K.J., Nemeroff, C.B., Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress. Anxiety 12:Suppl. 1 (2000), 2–19.
72. Reyes, B.A., Zitnik, G., Foster, C., Van Bockstaele, E.J., Valentino, R.J., Social stress engages neurochemically-distinct afferents to the rat locus coeruleus depending on coping strategy. eNeuro, 2015, 2.
73. Robinson, C.M., Hale, P.T., Carlin, J.M., The role of IFN-gamma and TNF-alpha-responsive regulatory elements in the synergistic induction of indoleamine dioxygenase. J. Interferon Cytokine Res. 25 (2005), 20–30.
74. Roche, M., Commons, K.G., Peoples, A., Valentino, R.J., Circuitry underlying regulation of the serotonergic system by swim stress. J. Neurosci. 23 (2003), 970–977.
75. Sarubbo, F., Ramis, M.R., Aparicio, S., Ruiz, L., Esteban, S., Miralles, A., Moranta, D., Improving effect of chronic resveratrol treatment on central monoamine synthesis and cognition in aged rats. Age (Dordrecht, Netherlands), 37, 2015, 9777.
76. Sasayama, D., Hattori, K., Wakabayashi, C., Teraishi, T., Hori, H., Ota, M., Yoshida, S., Arima, K., Higuchi, T., Amano, N., Kunugi, H., Increased cerebrospinal fluid interleukin-6 levels in patients with schizophrenia and those with major depressive disorder. J. Psychiatr. Res. 47 (2013), 401–406.
77. Setiawan, E., Wilson, A.A., Mizrahi, R., Rusjan, P.M., Miler, L., Rajkowska, G., Suridjan, I., Kennedy, J.L., Rekkas, P.V., Houle, S., Meyer, J.H., Role of translocator protein density, a marker of neuroinflammation, in the brain during major depressive episodes. JAMA Psychiatry 72 (2015), 268–275.
78. Singleton, R.H., Yan, H.Q., Fellows-Mayle, W., Dixon, C.E., Resveratrol attenuates behavioral impairments and reduces cortical and hippocampal loss in a rat controlled cortical impact model of traumatic brain injury. J. Neurotrauma 27 (2010), 1091–1099.
79. Solanki, N., Alkadhi, I., Atrooz, F., Patki, G., Salim, S., Grape powder prevents cognitive, behavioral, and biochemical impairments in a rat model of posttraumatic stress disorder. Nutr. Res. (New York, N.Y.) 35 (2015), 65–75.
80. Stefanski, V., Engler, H., Effects of acute and chronic social stress on blood cellular immunity in rats. Physiol. Behav. 64 (1998), 733–741.
81. Stuart, M.J., Singhal, G., Baune, B.T., Systematic review of the neurobiological relevance of chemokines to psychiatric disorders. Front. Cell. Neurosci., 9, 2015, 357.
82. Swanson, L.W., Hartman, B.K., The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat using dopamine-B-hydroxylase as a marker. J. Comp. Neurol. 163 (1976), 467–506.
83. Szuster-Ciesielska, A., Slotwinska, M., Stachura, A., Marmurowska-Michalowska, H., Dubas-Slemp, H., Bojarska-Junak, A., Kandefer-Szerszen, M., Accelerated apoptosis of blood leukocytes and oxidative stress in blood of patients with major depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 32 (2008), 686–694.
84. Toben, C., Baune, B.T., An act of balance between adaptive and maladaptive immunity in depression: a role for T lymphocytes. J. Neuroimmune Pharmacol. 10 (2015), 595–609.
85. Ueyama, J., Kitaichi, K., Iwase, M., Takagi, K., Takagi, K., Hasegawa, T., Application of ultrafiltration method to measurement of catecholamines in plasma of human and rodents by high-performance liquid chromatography. J. Chromatogr. B, Anal. Technol. Biomed. Life Sci. 798 (2003), 35–41.
86. Uher, R., Tansey, K.E., Dew, T., Maier, W., Mors, O., Hauser, J., Dernovsek, M.Z., Henigsberg, N., Souery, D., Farmer, A., McGuffin, P., An inflammatory biomarker as a differential predictor of outcome of depression treatment with escitalopram and nortriptyline. Am. J. Psychiatry 171 (2014), 1278–1286.
87. Veenema, A.H., Meijer, O.C., de Kloet, E.R., Koolhaas, J.M., Genetic selection for coping style predicts stressor susceptibility. J. Neuroendocrinol. 15 (2003), 256–267.
88. Vilhardt, F., Haslund-Vinding, J., Jaquet, V., McBean, G., Microglia antioxidant systems and redox signaling. Br. J. Pharmacol., 2016.
89. Wang, Q., Xu, J., Rottinghaus, G.E., Simonyi, A., Lubahn, D., Sun, G.Y., Sun, A.Y., Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 958 (2002), 439–447.
90. Weber, M.D., Frank, M.G., Sobesky, J.L., Watkins, L.R., Maier, S.F., Blocking toll-like receptor 2 and 4 signaling during a stressor prevents stress-induced priming of neuroinflammatory responses to a subsequent immune challenge. Brain Behav. Immun. 32 (2013), 112–121.
91. Wohleb, E.S., Hanke, M.L., Corona, A.W., Powell, N.D., Stiner, L.M., Bailey, M.T., Nelson, R.J., Godbout, J.P., Sheridan, J.F., Beta-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J. Neurosci. 31 (2011), 6277–6288.
92. Wohleb, E.S., Fenn, A.M., Pacenta, A.M., Powell, N.D., Sheridan, J.F., Godbout, J.P., Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice. Psychoneuroendocrinology 37 (2012), 1491–1505.
93. Wohleb, E.S., Powell, N.D., Godbout, J.P., Sheridan, J.F., Stress-induced recruitment of bone marrow-derived monocytes to the brain promotes anxiety-like behavior. J. Neurosci. 33 (2013), 13820–13833.
94. Wohleb, E.S., McKim, D.B., Sheridan, J.F., Godbout, J.P., Monocyte trafficking to the brain with stress and inflammation: a novel axis of immune-to-brain communication that influences mood and behavior. Front. Neurosci., 8, 2014, 447.
95. Wohleb, E.S., Patterson, J.M., Sharma, V., Quan, N., Godbout, J.P., Sheridan, J.F., Knockdown of interleukin-1 receptor type-1 on endothelial cells attenuated stress-induced neuroinflammation and prevented anxiety-like behavior. J. Neurosci. 34 (2014), 2583–2591.
96. Wong, M.L., Kling, M.A., Munson, P.J., Listwak, S., Licinio, J., Prolo, P., Karp, B., McCutcheon, I.E., Geracioti, T.D. Jr., DeBellis, M.D., Rice, K.C., Goldstein, D.S., Veldhuis, J.D., Chrousos, G.P., Oldfield, E.H., McCann, S.M., Gold, P.W., Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc. Natl. Acad. Sci. U.S.A. 97 (2000), 325–330.
97. Wood, S.K., Walker, H.E., Valentino, R.J., Bhatnagar, S., Individual differences in reactivity to social stress predict susceptibility and resilience to a depressive phenotype: role of corticotropin-releasing factor. Endocrinology 151 (2010), 1795–1805.
98. Wood, S.K., Zhang, X.Y., Reyes, B.A., Lee, C.S., Van Bockstaele, E.J., Valentino, R.J., Cellular adaptations of dorsal raphe serotonin neurons associated with the development of active coping in response to social stress. Biol. Psychiatry 73 (2013), 1087–1094.
99. Wood, S.K., Wood, C.S., Lombard, C.M., Lee, C.S., Zhang, X.Y., Finnell, J.E., Valentino, R.J., Inflammatory factors mediate vulnerability to a social stress-induced depressive-like phenotype in passive coping rats. Biol. Psychiatry 78 (2015), 38–48.
100. Xu, Y., Wang, Z., You, W., Zhang, X., Li, S., Barish, P.A., Vernon, M.M., Du, X., Li, G., Pan, J., Ogle, W.O., Antidepressant-like effect of trans-resveratrol: involvement of serotonin and noradrenaline system. Eur. Neuropsychopharmacol. 20 (2010), 405–413.
101. Yanez, M., Fraiz, N., Cano, E., Orallo, F., Inhibitory effects of cis- and trans-resveratrol on noradrenaline and 5-hydroxytryptamine uptake and on monoamine oxidase activity. Biochem. Biophys. Res. Commun. 344 (2006), 688–695.
102. Zhang, F., Liu, J., Shi, J.S., Anti-inflammatory activities of resveratrol in the brain: role of resveratrol in microglial activation. Eur. J. Pharmacol. 636 (2010), 1–7.