A pre-conditioning stress accelerates increases in mouse plasma inflammatory cytokines induced by stress

BMC Neuroscience

Eleonore Beurel¹  Richard S Jope¹  Yuyan Cheng¹ 

[1] Department of Psychiatry and Behavioral Sciences and Department of Biochemistry and Molecular Biology, Miller School of Medicine, University of Miami, 1011 NW 15th Street, Gautier Building room 416, Miami 33136, FL, USA

关键词: Tumor necrosis factor-α;    Stress;    Pre-conditioning;    Inflammation;    Depression;    Cytokines;   

Others  :  1210187
DOI  :  10.1186/s12868-015-0169-z

 received in 2014-10-21, accepted in 2015-04-22,  发布年份 2015

【 摘 要 】

Background

Major depressive disorder is a prevalent disease that is inadequately treated with currently available interventions. Stress increases susceptibility to depression in patients and rodent models. Depression is also associated with aberrant activation of inflammation, such as increases in circulating levels of interleukin (IL)-1β, IL-6, and tumor necrosis factor-α (TNFα). The two main goals of this study were (i) to identify cytokine changes measuring a broad panel of 19 cytokines, and (ii) to test if a pre-conditioning stress altered the inflammatory response to a subsequent stress.

Result

Stress-induced changes in mouse plasma cytokines were measured by multiplex following administration of one or two daily stresses of inescapable foot shocks using the learned helplessness paradigm for modeling depression-like behavior.

Administration of inescapable foot shocks increased plasma levels of IL-1β, IL-6, TNFα, IL-3, IL-10, IL-13, IL-17A, IL-5, GM-CSF, IL-12(p70), IFN-γ, MIP-1α, MIP-1β, IL-1α, IL-2, KC, RANTES and G-CSF, with peak levels occurring in the range of 6 to 12 hr after stress. Pre-conditioning the mice 24 hr before with an equivalent inescapable foot shock stress resulted in similar magnitudes of increases in most cytokines as occurred after a single stress, but accelerated the increase, causing the levels of most cytokines to peak 1 hr after stress. These results demonstrate that a single stress induces the expression of many cytokines, and that sequential, daily stresses accelerates the rate of cytokine production.

Conclusions

Acute stress broadly activates inflammation in mice, and the inflammatory response is more rapid following repeated stress, actions that may contribute to deleterious effects of stress on depression and other stress-linked diseases.

【 授权许可】

   
2015 Cheng et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Belmaker RH, Agam G: Major depressive disorder. N Engl J Med 2008, 358:55-68.
• [2]Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM: Neurobiology of depression. Neuron 2002, 34:13-25.
• [3]Dantzer R, Kelley KW: Twenty years of research on cytokine-induced sickness behavior. Brain Behav Immun 2007, 21:153-60.
• [4]Miller AH, Maletic V, Raison CL: Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biol Psychiat 2009, 65:732-41.
• [5]Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, et al.: A meta-analysis of cytokines in major depression. Biol Psychiat 2010, 67:446-57.
• [6]Liu Y, Ho RCM, Mak A: Interleukin (IL)-6, tumour necrosis factor α (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: a meta-analysis and meta-regression. J Affective Disorders 2012, 139:230-9.
• [7]Pace T, Mletzko T, Alagbe O, Musselman D, Nemeroff C, Miller A, et al.: Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. American J Psychiat 2006, 163:1630-3.
• [8]Steptoe A, Hamer M, Chida Y: The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav Immun 2007, 21:901-12.
• [9]Dieperink E, Ho SB, Thuras P, Willenbring ML: A prospective study of neuropsychiatric symptoms associated with interferon-alpha-2b and ribavirin therapy for patients with chronic hepatitis C. Psychosomatics 2003, 44:104-12.
• [10]Hayley S, Poulter MO, Merali Z, Anisman H: The pathogenesis of clinical depression: stressor- and cytokine-induced alterations of neuroplasticity. Neuroscience 2005, 135:659-78.
• [11]Lotrich FE, Ferrell RE, Rabinovitz M, Pollock BG: Risk for depression during interferon-alpha treatment is affected by the serotonin transporter polymorphism. Biol Psychiatry 2009, 65:344-8.
• [12]Eisenberger NI, Inagaki TK, Mashal NM, Irwin MR: Inflammation and social experience: an inflammatory challenge induces feelings of social disconnection in addition to depressed mood. Brain Behav Immun 2004, 24:558-63.
• [13]DellaGioia N, Hannestad J: A critical review of human endotoxin administration as an experimental paradigm of depression. Neurosci Biobehav Rev 2010, 34:130-43.
• [14]Kullmann JS, Grigoleit JS, Lichte P, Kobbe P, Rosenberger C, Banner C, et al.: Neural response to emotional stimuli during experimental human endotoxemia. Hum Brain Mapp 2013, 34:2217-27.
• [15]De La Garza R 2nd: Endotoxin- or pro-inflammatory cytokine-induced sickness behavior as an animal model of depression: focus on anhedonia. Neurosci Biobehav Rev 2005, 29:761-70.
• [16]Chourbaji S, Urani A, Inta I, Sanchis-Segura C, Brandwein C, Zink M, et al.: IL-6 knockout mice exhibit resistance to stress-induced development of depression-like behaviors. Neurobiol Dis 2006, 23:587-94.
• [17]Simen BB, Duman CH, Simen AA, Duman RS: TNFα signaling in depression and anxiety: behavioral consequences of individual receptor targeting. Biol Psychiat 2006, 59:775-85.
• [18]Koo JW, Duman RS: IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc Natl Acad Sci U S A 2008, 105:751-6.
• [19]Zhou D, Kusnecov AW, Shurin MR, DePaoli M, Rabin BS: Exposure to physical and psychological stressors elevates plasma interleukin 6: relationship to the activation of hypothalamic-pituitary-adrenal axis. Endocrinology 1993, 133:2523-30.
• [20]Nguyen KT, Deak T, Will MJ, Hansen MK, Hunsaker BN, Fleshner M, et al.: Timecourse and corticosterone sensitivity of the brain, pituitary, and serum interleukin-1β protein response to acute stress. Brain Res 2000, 859:193-201.
• [21]Johnson JD, Campisi J, Sharkey CM, Kennedy SL, Nickerson M, Greenwood BN, et al.: Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 2005, 135:1295-307.
• [22]Manikowska K, Mikołajczyk M, Mikołajczak PŁ, Bobkiewicz-Kozłowska T: The influence of mianserin on TNF-α, IL-6 and IL-10 serum levels in rats under chronic mild stress. Pharmacol Rep 2014, 66:22-7.
• [23]Johnson JD, O’Connor KA, Deak T, Stark M, Watkins LR, Maier SF: Prior stressor exposure sensitizes LPS-induced cytokine production. Brain Behav Immun 2002, 16:461-76.
• [24]Johnson JD, O’Connor KA, Hansen MK, Watkins LR, Maier SF: Effects of prior stress on LPS-induced cytokine and sickness responses. Am J Physiol Regul Integr Comp Physiol 2003, 284:422-32.
• [25]Johnson JD, O’Connor KA, Stark M, Watkins LR, Maier SF: The role of IL-1β in stress-induced sensitization of proinflammatory cytokine and corticosterone responses. Neuroscience 2004, 127:569-77.
• [26]Quan N, Avitsur R, Stark JL, He L, Shah M, Caligiuri M, et al.: Social stress increases the susceptibility to endotoxic shock. J Neuroimmunol 2011, 115:36-45.
• [27]Munhoz CD, Lepsch LB, Kawamoto EM, Malta MB, de Sá LL, Avellar MCW, et al.: Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-κB in the frontal cortex and hippocampus via glucocorticoid secretion. J Neuroscience 2006, 26:3813-20.
• [28]Frank MG, Baratta MV, Sprunger DB, Watkins LR, Maier SF: Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav Immun 2007, 21:47-59.
• [29]Espinosa-Oliva AM, De Pablos RM, Villarán RF, Argüelles S, Venero JL, Machado A, et al.: Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol Aging 2011, 32:85-102.
• [30]Polter A, Beurel E, Garner R, Song L, Miller C, Sweatt JD, et al.: Deficiency in the inhibitory serine-phosphorylation of glycogen synthase kinase-3 increases sensitivity to mood disturbances. Neuropsychopharmacology 2010, 35:1761-74.
• [31]Beurel E, Harrington LE, Jope RS: Inflammatory T helper 17 cells promote depression-like behavior in mice. Biol Psychiatry 2013, 73:622-30.
• [32]LeMay LG, Vander AJ, Kluger MJ: The effects of psychological stress on plasma interleukin-6 activity in rats. Physiol Behav 1990, 47:957-61.
• [33]Kitamura H, Konno A, Morimatsu M, Jung BD, Kimura K, Saito M: Immobilization stress increases hepatic IL-6 expression in mice. Biochem Biophys Res Comm 1997, 238:707-11.
• [34]Ando T, Rivier J, Yanaihara H, Arimura A: Peripheral corticotropin-releasing factor mediates the elevation of plasma IL-6 by immobilization stress in rats. Am J Physiol 1998, 275:1461-7.
• [35]Jung BD, Kimura K, Kitamura H, Makondo K, Kanehira K, Saito M: Sympathetic activation of hepatic and splenic IL-1beta mRNA expression during oscillation stress in the rat. J Vet Med Sci 2000, 62:409-13.
• [36]Moraska A, Campisi J, Nguyen KT, Maier SF, Watkins LR, Fleshner M: Elevated IL-1β contributes to antibody suppression produced by stress. J Applied Physiology 2002, 93:207-15.
• [37]Deak T, Bellamy C, D’Agostino LG: Exposure to forced swim stress does not alter central production of IL-1. Brain Res 2003, 972:53-63.
• [38]O’Connor KA, Johnson JD, Hansen MK, Wieseler Frank JL, Maksimova E, Watkins LR, et al.: Peripheral and central proinflammatory cytokine response to a severe acute stressor. Brain Res 2003, 991:123-32.
• [39]Blandino P Jr, Barnum CJ, Deak T: The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1β responses to stress. J Neuroimmunology 2006, 173:87-95.
• [40]Blandino P Jr, Barnum CJ, Solomon LG, Larish Y, Lankow BS, Deak T: Gene expression changes in the hypothalamus provide evidence for regionally-selective changes in IL-1 and microglial markers after acute stress. Brain Behav Immun 2009, 23:958-68.
• [41]Reiche EMV, Nunes SOV, Morimoto HK: Stress, depression, the immune system, and cancer. Lancet Oncol 2004, 5:617-25.
• [42]Miller DB, O’Callaghan JP: Aging, stress and the hippocampus. Ageing Res Rev 2005, 4:123-40.
• [43]Chida Y, Hamer M, Wardle J, Steptoe A: Do stress-related psychosocial factors contribute to cancer incidence and survival? Nat Clin Pract Oncol 2008, 5:466-75.
• [44]Dimsdale JE: Psychological stress and cardiovascular disease. J Am Coll Cardiol 2008, 51:1237-46.
• [45]Avitsur R, Padgett DA, Dhabhar FS, Stark JL, Kramer KA, Engler H, et al.: Expression of glucocorticoid resistance following social stress requires a second signal. J Leukocyte Biol 2003, 74:507-13.
• [46]Stark JL, Avitsur R, Hunzeker J, Padgett DA, Sheridan JF: Interleukin-6 and the development of social disruption-induced glucocorticoid resistance. J Neuroimmunology 2002, 124:9-15.
• [47]Avitsur R, Kavelaars A, Heijnen C, Sheridan JF: Social stress and the regulation of tumor necrosis factor-α secretion. Brain Behav Immun 2005, 19:311-7.
• [48]Bailey MT, Kinsey SG, Padgett DA, Sheridan JF, Leblebicioglu B: Social stress enhances IL-1β and TNF-α production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b + cells. Physiol Behav 2009, 98:351-8.
• [49]Frank MG, Miguel ZD, Watkins LR, Maier SF: Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav Immun 2010, 24:19-30.
• [50]Frank MG, Thompson BM, Watkins LR, Maier SF: Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses. Brain Behav Immun 2012, 26:337-45.