A peripheral immune response to remembering trauma contributes to the maintenance of fear memory in mice

Psychoneuroendocrinology

Volumn 94, Issue , 2018, Pages 143-151

  Young, Matthew B ^a   Howell, Leonard L ^a   Hopkins, Lauren ^b   Moshfegh, Cassandra ^b   Yu, Zhe ^b   Clubb, Lauren ^b   Seidenberg, Jessica ^b   Park, Jeanie ^d,e   Swiercz, Adam P ^b   Marvar, Paul J ^b,c  

^a EMORY UNIVERSITY   (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Extinction; Fear; Immune system; Inflammation; Interleukin 6; PTSD; Reconsolidation

Indexed keywords

INTERLEUKIN 6; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; FEAR MEMORY; FREEZING; IMMUNE RESPONSE; MEMORY; MEMORY CONSOLIDATION; MOUSE; NEUROPHYSIOLOGY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN TARGETING; REINFORCEMENT; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CONDITIONED REFLEX; DISEASE MODEL; FEAR; IMMUNOLOGY; INJURY; MALE; MENTAL STRESS; METABOLISM; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY; RECALL;

ANIMALS; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; EXTINCTION, PSYCHOLOGICAL; FEAR; INTERLEUKIN-6; MALE; MEMORY; MENTAL RECALL; MICE; MICE, INBRED C57BL; PREFRONTAL CORTEX; STRESS DISORDERS, POST-TRAUMATIC; STRESS, PSYCHOLOGICAL; WOUNDS AND INJURIES;

EID: 85047097760     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2018.05.012     Document Type: Article

References (40)

1. Baker, D.G., Ekhator, N.N., Kasckow, J.W., Hill, K.K., Zoumakis, E., Dashevsky, B.A., Chrousos, G.P., Geracioti, T.D., Plasma and cerebrospinal fluid interleukin-6 concentrations in posttraumatic stress disorder. Neuroimmunomodulation 9 (2001), 209–217.
2. Bi, Q., Shi, L., Yang, P., Wang, J., Qin, L., Minocycline attenuates interferon-α-induced impairments in rat fear extinction. J. Neuroinflammation, 13, 2016, 172, 10.1186/s12974-016-0638-z.
3. Breen, M.S., Maihofer, A.X., Glatt, S.J., Tylee, D.S., Chandler, S.D., Tsuang, M.T., Risbrough, V.B., Baker, D.G., O'Connor, D.T., Nievergelt, C.M., Woelk, C.H., Gene networks specific for innate immunity define post-traumatic stress disorder. Mol. Psychiatry 20 (2015), 1538–1545, 10.1038/mp.2015.9.
4. Breznitz, S., Ben-Zur, H., Berzon, Y., Weiss, D.W., Levitan, G., Tarcic, N., Lischinsky, S., Greenberg, A., Levi, N., Zinder, O., Experimental induction and termination of acute psychological stress in human volunteers: effects on immunological, neuroendocrine, cardiovascular, and psychological parameters. Brain Behav. Immun. 12 (1998), 34–52, 10.1006/brbi.1997.0511.
5. Clark, S.M., Soroka, J.A., Song, C., Li, X., Tonelli, L.H., CD4(+) T cells confer anxiolytic and antidepressant-like effects, but enhance fear memory processes in Rag2(-/-) mice. Stress 19 (2016), 303–311, 10.1080/10253890.2016.1191466.
6. Garcia-Oscos, F., Peña, D., Housini, M., Cheng, D., Lopez, D., Borland, M.S., Salgado-Delgado, R., Salgado, H., D'Mello, S., Kilgard, M.P., Rose-John, S., Atzori, M., Vagal nerve stimulation blocks interleukin 6-dependent synaptic hyperexcitability induced by lipopolysaccharide-induced acute stress in the rodent prefrontal cortex. Brain Behav. Immun. 43 (2015), 149–158, 10.1016/j.bbi.2014.07.020.
7. Gill, J.M., Saligan, L., Woods, S., Page, G., PTSD is associated with an excess of inflammatory immune activities. Perspect. Psychiatr. Care 45 (2009), 262–277, 10.1111/j. 1744–6163.2009.00229.x.
8. Gola, H., Engler, H., Sommershof, A., Adenauer, H., Kolassa, S., Schedlowski, M., Groettrup, M., Elbert, T., Kolassa, I.-T., Posttraumatic stress disorder is associated with an enhanced spontaneous production of pro-inflammatory cytokines by peripheral blood mononuclear cells. BMC Psychiatry, 13, 2013, 40, 10.1186/1471-244X-13-40.
9. Hao, Y., Jing, H., Bi, Q., Zhang, J., Qin, L., Yang, P., Intra-amygdala microinfusion of IL-6 impairs the auditory fear conditioning of rats via JAK/STAT activation. Behav. Brain Res. 275 (2014), 88–95, 10.1016/j.bbr.2014.08.052.
10. 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., Lebonté B., Horn, S., Lapidus, K.A., Stelzhammer, V., Wong, E.H.F., Bahn, S., Krishnan, V., Bolaños-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. 111 (2014), 16136–16141, 10.1073/pnas.1415191111.
11. Hundhausen, C., Roth, A., Whalen, E., Chen, J., Schneider, A., Long, S.A., Wei, S., Rawlings, R., Kinsman, M., Evanko, S.P., Wight, T.N., Greenbaum, C.J., Cerosaletti, K., Buckner, J.H., Enhanced T cell responses to IL-6 in type 1 diabetes are associated with early clinical disease and increased IL-6 receptor expression. Sci. Transl. Med., 8, 2016, 10.1126/scitranslmed.aad9943 (356ra119).
12. Hunter, C.A., Jones, S.A., IL-6 as a keystone cytokine in health anddisease. Nat. Immunol. 16 (2015), 448–457, 10.1038/ni.3153.
13. Jergović M., Bendelja, K., Vidović A., Savić A., Vojvoda, V., Aberle, N., Rabatić S., Jovanovic, T., Sabioncello, A., Patients with posttraumatic stress disorder exhibit an altered phenotype of regulatory T cells. Allerg. Asthma Clin. Immunol., 10, 2014, 43, 10.1186/1710-1492-10-43.
14. Johnson, R.L., Murray, S.T., Camacho, D.K., Wilson, C.G., Vagal nerve stimulation attenuates IL-6 and TNF(expression in respiratory regions of the developing rat brainstem. Respir. Physiol. Neurobiol. 229 (2016), 1–4, 10.1016/j.resp.2016.03.014.
15. Jones, G.W., McLoughlin, R.M., Hammond, V.J., Parker, C.R., Williams, J.D., Malhotra, R., Scheller, J., Williams, A.S., Rose-John, S., Topley, N., Jones, S.A., Loss of CD4+ T cell IL-6R expression during inflammation underlines a role for IL-6 trans signaling in the local maintenance of Th17 cells. J. Immunol. 184 (2010), 2130–2139, 10.4049/jimmunol.0901528.
16. Jones, M.E., Lebonville, C.L., Barrus, D., Lysle, D.T., The role of brain interleukin-1 in stress-enhanced fear learning. Neuropsychopharmacology 40 (2015), 1289–1296, 10.1038/npp.2014.317.
17. Kipnis, J., Gadani, S., Derecki, N.C., Pro-cognitive properties of T cells. Nat. Rev. Immunol. 12 (2012), 663–669, 10.1038/nri3280.
18. Kipnis, J., Multifaceted interactions between adaptive immunity and the central nervous system. Science 353 (2016), 766–771, 10.1126/science.aag2638.
19. Lemieux, A., Coe, C.L., Carnes, M., Symptom severity predicts degree of T cell activation in adult women following childhood maltreatment. Brain Behav. Immun. 22 (2008), 994–1003, 10.1016/j.bbi.2008.02.005.
20. Lindqvist, D., Wolkowitz, O.M., Mellon, S., Yehuda, R., Flory, J.D., Henn-Haase, C., Bierer, L.M., Abu-Amara, D., Coy, M., Neylan, T.C., Makotkine, I., Reus, V.I., Yan, X., Taylor, N.M., Marmar, C.R., Dhabhar, F.S., Proinflammatory milieu in combat-related PTSD is independent of depression and early life stress. Brain Behav. Immun. 42 (2014), 81–88, 10.1016/j.bbi.2014.06.003.
21. Michopoulos, V., Powers, A., Gillespie, C.F., Ressler, K.J., Jovanovic, T., Inflammation in fear- and anxiety-Based disorders: PTSD, GAD and beyond. Neuropsychopharmacology, 2016, 10.1038/npp.2016.146.
22. Milad, M.R., Quirk, G.J., Fear extinction as a model for translational neuroscience: ten years of progress. Annu. Rev. Psychol. 63 (2012), 129–151, 10.1146/annurev.psych.121208.131631.
23. Moberg, C.A., Curtin, J.J., Alcohol selectively reduces anxiety but not fear: startle response during unpredictable versus predictable threat. J. Abnorm. Psychol. 118 (2009), 335–347, 10.1037/a0015636.
24. Monfils, M.-H., Cowansage, K.K., Klann, E., LeDoux, J.E., Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324 (2009), 951–955, 10.1126/science.1167975.
25. Newton, T.L., Fernandez-Botran, R., Miller, J.J., Burns, V.E., Interleukin-6 and soluble interleukin-6 receptor levels in posttraumatic stress disorder: associations with lifetime diagnostic status and psychological context. Biol. Psychol. 99 (2014), 150–159, 10.1016/j.biopsycho.2014.03.009.
26. Nish, S.A., Schenten, D., Wunderlich, F.T., Pope, S.D., Gao, Y., Hoshi, N., Yu, S., Yan, X., Lee, H.K., Pasman, L., Brodsky, I., Yordy, B., Zhao, H., Brüning, J., Medzhitov, R., T cell-intrinsic role of IL-6 signaling in primary and memory responses. Elife, 3, 2014, e01949, 10.7554/eLife.01949.
27. O'Donovan, A., Cohen, B.E., Seal, K.H., Bertenthal, D., Margaretten, M., Nishimi, K., Neylan, T.C., Elevated risk for autoimmune disorders in iraq and afghanistan veterans with posttraumatic stress disorder. Biol. Psychiatry 77 (2015), 365–374, 10.1016/j.biopsych.2014.06.015.
28. Paul, R., Koedel, U., Winkler, F., Kieseier, B.C., Fontana, A., Kopf, M., Hartung, H.-P., Pfister, H.-W., Lack of IL-6 augments inflammatory response but decreases vascular permeability in bacterial meningitis. Brain 126 (2003), 1873–1882, 10.1093/brain/awg171.
29. Peña, D.F., Engineer, N.D., McIntyre, C.K., Rapid remission of conditioned fear expression with extinction training paired with vagus nerve stimulation. Biol. Psychiatry 73 (2013), 1071–1077, 10.1016/j.biopsych.2012.10.021.
30. Rothbaum, B.O., Davis, M., Applying learning principles to the treatment of post-trauma reactions. Ann. N. Y. Acad. Sci. 1008 (2003), 112–121.
31. Rothbaum, B.O., Price, M., Jovanovic, T., Norrholm, S.D., Gerardi, M., Dunlop, B., Davis, M., Bradley, B., Ressler, K.J., A randomized, double-blind evaluation of D-cycloserine or alprazolam combined with virtual reality exposure therapy for posttraumatic stress disorder (PTSD) in Iraq and Afghanistan war veterans. Am. J. Psychiatry 171:Jun. (6) (2014), 640–648.
32. Saija, A., Princi, P., Lanza, M., Scalese, M., Aramnejad, E., De Sarro, A., Systemic cytokine administration can affect blood-brain barrier permeability in the rat. Life Sci. 56 (1995), 775–784.
33. Scholz, B., Doidge, A.N., Barnes, P., Hall, J., Wilkinson, L.S., Thomas, K.L., The regulation of cytokine networks in hippocampal CA1 differentiates extinction from those required for the maintenance of contextual fear memory after recall. PLoS One, 11, 2016, e0153102, 10.1371/journal.pone.0153102.
34. Singewald, N., Schmuckermair, C., Whittle, N., Holmes, A., Ressler, K.J., Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders. Pharmacol. Ther. 149 (2015), 150–190, 10.1016/j.pharmthera.2014.12.004.
35. Tursich, M., Neufeld, R.W.J., Frewen, P.A., Harricharan, S., Kibler, J.L., Rhind, S.G., Lanius, R.A., Association of trauma exposure with proinflammatory activity: a transdiagnostic meta-analysis. Transl. Psychiatry, 4, 2014, e413, 10.1038/tp.2014.56.
36. Walker, D.L., Toufexis, D.J., Davis, M., Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur. J. Pharmacol. 463 (2003), 199–216, 10.1016/S0014-2999(03)01282-2.
37. Yu, Z., Fukushima, H., Ono, C., Sakai, M., Kasahara, Y., Kikuchi, Y., Gunawansa, N., Takahashi, Y., Matsuoka, H., Kida, S., Tomita, H., Microglial production of TNF-alpha is a key element of sustained fear memory. Brain Behav. Immun. 59 (2017), 313–321, 10.1016/j.bbi.2016.08.011.
38. Zhang, J.-C., Yao, W., Dong, C., Yang, C., Ren, Q., Ma, M., Hashimoto, K., Blockade of interleukin-6 receptor in the periphery promotes rapid and sustained antidepressant actions: a possible role of gut-microbiota-brain axis. Transl. Psychiatry, 7, 2017, e1138, 10.1038/tp.2017.112.
39. Zhou, D., Kusnecov, A.W., Shurin, M.R., DePaoli, M., Rabin, B.S., Exposure to physical and psychological stressors elevates plasma interleukin 6: relationship to the activation of hypothalamic-pituitary-adrenal axis. Endocrinology 133 (1993), 2523–2530, 10.1210/endo.133.6.8243274.
40. Zhou, J., Nagarkatti, P., Zhong, Y., Ginsberg, J.P., Singh, N.P., Zhang, J., Nagarkatti, M., Dysregulation in microRNA expression is associated with alterations in immune functions in combat veterans with post-traumatic stress disorder. PLoS One, 9, 2014, e94075, 10.1371/journal.pone.0094075.