MDMA administration attenuates hippocampal IL-β immunoreactivity and subsequent stress-enhanced fear learning: An animal model of PTSD

Brain, Behavior, & Immunity - Health - Tập 26 - Trang 100542 - 2022
Shveta V. Parekh1, Lydia O. Adams1, Gillian A. Barkell1, Donald T. Lysle1
1Department of Psychology and Neuroscience, University of North Carolina at Chapel Hill, CB#3720, Chapel Hill, NC, 27599-3270, USA

Tài liệu tham khảo

Abad, 2019, Effects of MDMA on neuroplasticity, amyloid burden and phospho-tau expression in APPswe/PS1dE9 mice, J. Psychopharmacol., 33, 1170, 10.1177/0269881119855987 Acheson, 2012, Hippocampal dysfunction effects on context memory: possible etiology for posttraumatic stress disorder, Neuropharmacology, 62, 674, 10.1016/j.neuropharm.2011.04.029 Aguirre, 1999, Alpha-lipoic acid prevents 3,4-methylenedioxy-methamphetamine (MDMA)-induced neurotoxicity, Neuroreport, 10, 3675, 10.1097/00001756-199911260-00039 Alexander, 2012, Pharmacotherapy for post-traumatic stress disorder in combat veterans: focus on antidepressants and atypical antipsychotic agents, P T, 37, 32 Alshammari, 2020, Systemic TNF-alpha blockade attenuates anxiety and depressive-like behaviors in db/db mice through downregulation of inflammatory signaling in peripheral immune cells, Saudi Pharmaceut. J., 28, 621, 10.1016/j.jsps.2020.04.001 Anagnostaras, 2001, Hippocampus and contextual fear conditioning: recent controversies and advances, Hippocampus, 11, 8, 10.1002/1098-1063(2001)11:1<8::AID-HIPO1015>3.0.CO;2-7 Ardito, 2011, Therapeutic alliance and outcome of psychotherapy: historical excursus, measurements, and prospects for research, Front. Psychol., 2, 270, 10.3389/fpsyg.2011.00270 Arluk, 2022, MDMA treatment paired with a trauma-cue promotes adaptive stress responses in a translational model of PTSD in rats, Transl. Psychiatry, 12, 181, 10.1038/s41398-022-01952-8 Barrett, 2021, Chronic stress primes innate immune responses in mice and humans, Cell Rep., 36, 10.1016/j.celrep.2021.109595 Barrientos, 2004, BDNF mRNA expression in rat hippocampus following contextual learning is blocked by intrahippocampal IL-1beta administration, J. Neuroimmunol., 155, 119, 10.1016/j.jneuroim.2004.06.009 Borissova, 2021, Acute effects of MDMA on trust, cooperative behaviour and empathy: a double-blind, placebo-controlled experiment, J. Psychopharmacol., 35, 547, 10.1177/0269881120926673 Boudewyns, 1991, Co-morbidity and treatment outcomes of inpatients with chronic combat-related PTSD, Hosp. Community Psychiatr., 42, 847 Bourgognon, 2020, The role of cytokines in modulating learning and memory and brain plasticity, Brain Neurosci Adv, 4, 10.1177/2398212820979802 Boyle, 2007, MDMA ("Ecstasy") suppresses the innate IFN-gamma response in vivo: a critical role for the anti-inflammatory cytokine IL-10, Eur. J. Pharmacol., 572, 228, 10.1016/j.ejphar.2007.07.020 Bremner, 1996, Chronic PTSD in Vietnam combat veterans: course of illness and substance abuse, Am. J. Psychiatr., 153, 369, 10.1176/ajp.153.3.369 Buchert, 2001, Long-term effects of 'ecstasy' abuse on the human brain studied by FDG PET, Nucl. Med. Commun., 22, 889, 10.1097/00006231-200108000-00007 Carta, 2017, Dysregulated IL-1beta secretion in autoinflammatory diseases: a matter of stress?, Front. Immunol., 8, 345, 10.3389/fimmu.2017.00345 Caso, 2007, Involvement of IL-1beta in acute stress-induced worsening of cerebral ischaemia in rats, Eur. Neuropsychopharmacol, 17, 600, 10.1016/j.euroneuro.2007.02.009 Cekanaviciute, 2016, Astrocytes: integrative regulators of neuroinflammation in stroke and other neurological diseases, Neurotherapeutics, 13, 685, 10.1007/s13311-016-0477-8 Cheng, 2015, A pre-conditioning stress accelerates increases in mouse plasma inflammatory cytokines induced by stress, BMC Neurosci., 16, 31, 10.1186/s12868-015-0169-z Choi, 2014, Human astrocytes: secretome profiles of cytokines and chemokines, PLoS One, 9, 10.1371/journal.pone.0092325 Connor, 2004, Methylenedioxymethamphetamine (MDMA, 'Ecstasy'): a stressor on the immune system, Immunology, 111, 357, 10.1111/j.0019-2805.2004.01847.x Connor, 2000, Methylenedioxymethamphetamine (MDMA; Ecstasy) suppresses IL-1beta and TNF-alpha secretion following an in vivo lipopolysaccharide challenge, Life Sci., 67, 1601, 10.1016/S0024-3205(00)00743-8 Connor, 2001, Methylenedioxymethamphetamine-induced suppression of interleukin-1beta and tumour necrosis factor-alpha is not mediated by serotonin, Eur. J. Pharmacol., 418, 147, 10.1016/S0014-2999(01)00928-1 de Almeida, 2000, [History, effects and mechanisms of action of ecstasy (3,4-methylenedioxyamphetamine): review of the literature], Rev. Panam. Salud Públic, 8, 393 de la Torre, 2004, Human pharmacology of MDMA: pharmacokinetics, metabolism, and disposition, Ther. Drug Monit., 26, 137, 10.1097/00007691-200404000-00009 Deslauriers, 2017, Immune signaling mechanisms of PTSD risk and symptom development: insights from animal models, Curr Opin Behav Sci, 14, 123, 10.1016/j.cobeha.2017.01.005 Dib, 2021, TNF-alpha as an initiator of allodynia and anxiety-like behaviors in a preclinical model of PTSD and comorbid pain, Front. Psychiatr., 12, 10.3389/fpsyt.2021.721999 Enomoto, 2021, Involvement of microglia in disturbed fear memory regulation: possible microglial contribution to the pathophysiology of posttraumatic stress disorder, Neurochem. Int., 142, 10.1016/j.neuint.2020.104921 Freire-Garabal, 1992, Effects of amphetamine on the activity of phagocytosis in mice, Life Sci., 51, PL145, 10.1016/0024-3205(92)90362-S Gill, 2009, PTSD is associated with an excess of inflammatory immune activities, Psychiatr. Care, 45, 262 Goshen, 2009, Interleukin-1 (IL-1): a central regulator of stress responses, Front. Neuroendocrinol., 30, 30, 10.1016/j.yfrne.2008.10.001 Goshen, 2007, A dual role for interleukin-1 in hippocampal-dependent memory processes, Psychoneuroendocrinology, 32, 1106, 10.1016/j.psyneuen.2007.09.004 Green, 2003, The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"), Pharmacol. Rev., 55, 463, 10.1124/pr.55.3.3 Habbas, 2015, Neuroinflammatory TNFalpha impairs memory via astrocyte signaling, Cell, 163, 1730, 10.1016/j.cell.2015.11.023 Hake, 2019, 3,4-methylenedioxymethamphetamine (MDMA) impairs the extinction and reconsolidation of fear memory in rats, Physiol. Behav., 199, 343, 10.1016/j.physbeh.2018.12.007 Himmerich, 2019, Cytokine research in depression: principles, challenges, and open questions, Front. Psychiatr., 10, 30, 10.3389/fpsyt.2019.00030 Huckleberry, 2018, Dorsal and ventral hippocampal adult-born neurons contribute to context fear memory, Neuropsychopharmacology, 43, 2487, 10.1038/s41386-018-0109-6 Hussein, 2017, A systematic review of tumor necrosis factor-alpha in post-traumatic stress disorder: evidence from human and animal studies, Psychiatr. Danub., 29, 407, 10.24869/psyd.2017.407 Izquierdo, 2016, Fear memory, Physiol. Rev., 96, 695, 10.1152/physrev.00018.2015 Jahanshahi, 2013, Effects of repeated administration of 3,4-methylenedioxymethamphetamine (MDMA) on avoidance memory and cell density in rats' Hippocampus, Basic Clin. Neurosci., 4, 57 Johnson, 2019, Neuroendocrine regulation of brain cytokines after psychological stress, J Endocr Soc, 3, 1302, 10.1210/js.2019-00053 Jones, 2015, The role of brain interleukin-1 in stress-enhanced fear learning, Neuropsychopharmacology, 40, 1289, 10.1038/npp.2014.317 Jones, 2018, Hippocampal interleukin-1 mediates stress-enhanced fear learning: a potential role for astrocyte-derived interleukin-1beta, Brain Behav. Immun., 67, 355, 10.1016/j.bbi.2017.09.016 Jones, 2018, Chemogenetic manipulation of dorsal hippocampal astrocytes protects against the development of stress-enhanced fear learning, Neuroscience, 10.1016/j.neuroscience.2018.07.015 Kalant, 2001, The pharmacology and toxicology of "ecstasy" (MDMA) and related drugs, CMAJ (Can. Med. Assoc. J.), 165, 917 Khakh, 2015, Diversity of astrocyte functions and phenotypes in neural circuits, Nat. Neurosci., 18, 942, 10.1038/nn.4043 Kim, 2006, Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease, Exp. Mol. Med., 38, 333, 10.1038/emm.2006.40 Kim, 2020, Inflammation in post-traumatic stress disorder (PTSD): a review of potential correlates of PTSD with a neurological perspective, Antioxidants, 9, 10.3390/antiox9020107 Koo, 2008, IL-1beta is an essential mediator of the antineurogenic and anhedonic effects of stress, Proc. Natl. Acad. Sci. U. S. A., 105, 751, 10.1073/pnas.0708092105 Lau, 2001, Astrocytes produce and release interleukin-1, interleukin-6, tumor necrosis factor alpha and interferon-gamma following traumatic and metabolic injury, J. Neurotrauma, 18, 351, 10.1089/08977150151071035 Li, 2020, Activation of astrocytes in hippocampus decreases fear memory through adenosine A1 receptors, Elife, 9 Li, 2021, Microglial deletion and inhibition alleviate behavior of post-traumatic stress disorder in mice, J. Neuroinflammation, 18, 7, 10.1186/s12974-020-02069-9 Li, 2022, Astrocytes in post-traumatic stress disorder, Neurosci. Bull. Lissek, 2015, Learning models of PTSD: theoretical accounts and psychobiological evidence, Int. J. Psychophysiol., 98, 594, 10.1016/j.ijpsycho.2014.11.006 Ma, 2015, The effect of isoliquiritigenin on learning and memory impairments induced by high-fat diet via inhibiting TNF-alpha/JNK/IRS signaling, Biochem. Biophys. Res. Commun., 464, 1090, 10.1016/j.bbrc.2015.07.081 Mitchell, 2021, MDMA-assisted therapy for severe PTSD: a randomized, double-blind, placebo-controlled phase 3 study, Nat. Med., 27, 1025, 10.1038/s41591-021-01336-3 Miyazaki, 2016, Serotonin 1A receptors on astrocytes as a potential target for the treatment of Parkinson's disease, Curr. Med. Chem., 23, 686, 10.2174/0929867323666160122115057 Moore, 2009, Sustained expression of interleukin-1beta in mouse hippocampus impairs spatial memory, Neuroscience, 164, 1484, 10.1016/j.neuroscience.2009.08.073 Morgan, 2020, MDMA-assisted psychotherapy for people diagnosed with treatment-resistant PTSD: what it is and what it isn't, Ann. Gen. Psychiatr., 19, 33, 10.1186/s12991-020-00283-6 Muhie, 2017, Molecular indicators of stress-induced neuroinflammation in a mouse model simulating features of post-traumatic stress disorder, Transl. Psychiatry, 7, e1135, 10.1038/tp.2017.91 Munshi, 2020, Repeated stress induces a pro-inflammatory state, increases amygdala neuronal and microglial activation, and causes anxiety in adult male rats, Brain Behav. Immun., 84, 180, 10.1016/j.bbi.2019.11.023 Nardou, 2019, Oxytocin-dependent reopening of a social reward learning critical period with MDMA, Nature, 569, 116, 10.1038/s41586-019-1075-9 Neigh, 2016, Co-morbidity of PTSD and immune system dysfunction: opportunities for treatment, Curr. Opin. Pharmacol., 29, 104, 10.1016/j.coph.2016.07.011 Noorbakhshnia, 2017, Portulaca oleracea L. prevents lipopolysaccharide-induced passive avoidance learning and memory and TNF-alpha impairments in hippocampus of rat, Physiol. Behav., 169, 69, 10.1016/j.physbeh.2016.11.027 Ot'alora, 2018, 3,4-Methylenedioxymethamphetamine-assisted psychotherapy for treatment of chronic posttraumatic stress disorder: a randomized phase 2 controlled trial, J. Psychopharmacol., 32, 1295, 10.1177/0269881118806297 Pacifici, 2001, Acute effects of 3,4-methylenedioxymethamphetamine alone and in combination with ethanol on the immune system in humans, J. Pharmacol. Exp. Therapeut., 296, 207 Parekh, 2020, Dorsal hippocampal interleukin-1 signaling mediates heroin withdrawal-enhanced fear learning, Psychopharmacology (Berl), 237, 3653, 10.1007/s00213-020-05645-2 Parekh, 2021, Hippocampal TNF-alpha signaling mediates heroin withdrawal-enhanced fear learning and withdrawal-induced weight loss, Mol. Neurobiol., 58, 2963, 10.1007/s12035-021-02322-z Passos, 2015, Inflammatory markers in post-traumatic stress disorder: a systematic review, meta-analysis, and meta-regression, Lancet Psychiatr., 2, 1002, 10.1016/S2215-0366(15)00309-0 Pham, 2009, Automated scoring of fear-related behavior using EthoVision software, J. Neurosci. Methods, 178, 323, 10.1016/j.jneumeth.2008.12.021 Ponomarev, 2010, Amygdala transcriptome and cellular mechanisms underlying stress-enhanced fear learning in a rat model of posttraumatic stress disorder, Neuropsychopharmacology, 35, 1402, 10.1038/npp.2010.10 Pooley, 2018, Sex differences in the traumatic stress response: PTSD symptoms in women recapitulated in female rats, Biol. Sex Differ., 9, 31, 10.1186/s13293-018-0191-9 Pubill, 2003, Different glial response to methamphetamine- and methylenedioxymethamphetamine-induced neurotoxicity, Naunyn-Schmiedeberg’s Arch. Pharmacol., 367, 490, 10.1007/s00210-003-0747-y Pugh, 1999, Role of interleukin-1 beta in impairment of contextual fear conditioning caused by social isolation, Behav. Brain Res., 106, 109, 10.1016/S0166-4328(99)00098-4 Rau, 2005, Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder, Neurosci. Biobehav. Rev., 29, 1207, 10.1016/j.neubiorev.2005.04.010 Richter-Levin, 2019, Animal models of PTSD: a challenge to be met, Mol. Psychiatr., 24, 1135, 10.1038/s41380-018-0272-5 Schottenbauer, 2008, Nonresponse and dropout rates in outcome studies on PTSD: review and methodological considerations, Psychiatry, 71, 134, 10.1521/psyc.2008.71.2.134 Sessa, 2017, Why psychiatry needs 3,4-methylenedioxymethamphetamine: a child psychiatrist's perspective, Neurotherapeutics, 14, 741, 10.1007/s13311-017-0531-1 Simmler, 2018, Pharmacology of MDMA- and amphetamine-like new psychoactive substances, Handb. Exp. Pharmacol., 252, 143, 10.1007/164_2018_113 Smid, 2015, Cytokine production as a putative biological mechanism underlying stress sensitization in high combat exposed soldiers, Psychoneuroendocrinology, 51, 534, 10.1016/j.psyneuen.2014.07.010 Sugama, 2007, Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18, Neuroscience, 146, 1388, 10.1016/j.neuroscience.2007.02.043 Swiergiel, 2007, Effects of interleukin-1beta and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests, Pharmacol. Biochem. Behav., 86, 651, 10.1016/j.pbb.2007.02.010 Szczytkowski-Thomson, 2013, Morphine prevents the development of stress-enhanced fear learning, Pharmacol. Biochem. Behav., 103, 672, 10.1016/j.pbb.2012.10.013 Takahashi, 2021, Tumor necrosis factor alpha negatively regulates the retrieval and reconsolidation of hippocampus-dependent memory, Brain Behav. Immun., 94, 79, 10.1016/j.bbi.2021.02.033 Takemiya, 2017, Brain interleukin-1 facilitates learning of a water maze spatial memory task in young mice, Front. Behav. Neurosci., 11, 202, 10.3389/fnbeh.2017.00202 Tomaz, 2020, Antidepressants of different classes cause distinct behavioral and brain pro- and anti-inflammatory changes in mice submitted to an inflammatory model of depression, J. Affect. Disord., 268, 188, 10.1016/j.jad.2020.03.022 Tsoory, 2008, Amygdala modulation of memory-related processes in the hippocampus: potential relevance to PTSD, Prog. Brain Res., 167, 35, 10.1016/S0079-6123(07)67003-4 Wallensten, 2022, Plasma levels of S100B and neurofilament light chain protein in stress-related mental disorders, Sci. Rep., 12, 8339, 10.1038/s41598-022-12287-1 Wang, 2018, Microglial activation mediates chronic mild stress-induced depressive- and anxiety-like behavior in adult rats, J. Neuroinflammation, 15, 21, 10.1186/s12974-018-1054-3 Whitaker, 2014, Animal models of post-traumatic stress disorder and recent neurobiological insights, Behav. Pharmacol., 25, 398, 10.1097/FBP.0000000000000069 Wilson, 2013, Inflammation and oxidative stress are elevated in the brain, blood, and adrenal glands during the progression of post-traumatic stress disorder in a predator exposure animal model, PLoS One, 8, 10.1371/journal.pone.0076146 Young, 2015, 3,4-Methylenedioxymethamphetamine facilitates fear extinction learning, Transl. Psychiatry, 5, e634, 10.1038/tp.2015.138 Zack, 1977, Automatic measurement of sister chromatid exchange frequency, J. Histochem. Cytochem., 25, 741, 10.1177/25.7.70454