Chronic exposure to methadone impairs memory, induces microgliosis, astrogliosis and neuroinflammation in the hippocampus of adult male rats

Ahmad-Molaei, 2018, Delay-dependent impairments in memory and motor functions after acute methadone overdose in rats, Front. Pharmacol., 1023, 10.3389/fphar.2018.01023 Andersen, 2011, Long-term methadone treatment impairs novelty preference in rats both when present and absent in brain tissue, Pharmacol. Biochem. Behav., 98, 412, 10.1016/j.pbb.2011.02.017 Archer, 1975, Rodent sex differences in emotional and related behavior, Behav. Biol., 14, 10.1016/S0091-6773(75)90636-7 Asanuma, 2003, Methamphetamine-induced neurotoxicity in mouse brain is attenuated by ketoprofen, a non-steroidal anti-inflammatory drug, Neurosci. Lett., 352, 13, 10.1016/j.neulet.2003.08.015 Babbini, 1975, Persistence of chronic morphine effects upon activity in rats 8 months after ceasing the treatment, Neuropharmacology, 14, 611, 10.1016/0028-3908(75)90129-X Best, 1998, Eating too little, smoking and drinking too much: wider lifestyle problems among methadone maintenance patients, Addict. Res., 6, 489, 10.3109/16066359809004367 Boronat, 2001, Chronic morphine induces up‐regulation of the pro‐apoptotic Fas receptor and down‐regulation of the anti‐apoptotic Bcl‐2 oncoprotein in rat brain, Br. J. Pharmacol., 134, 1263, 10.1038/sj.bjp.0704364 Boroujeni, M.E., et al., Inflammatory response leads to neuronal death in human post-mortem cerebral cortex in patients with COVID-19. ACS Chem.l Neurosci., 2021. Bush, 1999, Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice, Neuron, 23, 297, 10.1016/S0896-6273(00)80781-3 Conrad, 1998, Circulating levels of immunoreactive cytokines in women with preeclampsia, Am. J. Reprod. Immunol., 40, 102, 10.1111/j.1600-0897.1998.tb00398.x Darke, 2000, Cognitive impairment among methadone maintenance patients, Addiction, 95, 687, 10.1046/j.1360-0443.2000.9556874.x Davis, 2017, Characterizing microglia activation: a spatial statistics approach to maximize information extraction, Sci. Rep., 7, 1, 10.1038/s41598-017-01747-8 De Vries, 1998, Drug‐induced reinstatement of heroin‐and cocaine‐seeking behaviour following long‐term extinction is associated with expression of behavioural sensitization, Eur. J. Neurosci., 10, 3565, 10.1046/j.1460-9568.1998.00368.x Diz-Chaves, 2012, Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice, J. Neuroinflamm., 9, 1, 10.1186/1742-2094-9-71 Duyckaerts, 2000, Voronoi tessellation to study the numerical density and the spatial distribution of neurones, J. Chem. Neuroanat., 20, 83, 10.1016/S0891-0618(00)00064-8 Eisch, A.J., et al., Opiates inhibit neurogenesis in the adult rat hippocampus. Proce. Natl. Acad. Sci. USA 2000. 97(13) 7579–7584. Emeterio, 2006, Modulation of apoptosis in the mouse brain after morphine treatments and morphine withdrawal, J. Neurosci. Res., 83, 1352, 10.1002/jnr.20812 Faulkner, 2004, Reactive astrocytes protect tissue and preserve function after spinal cord injury, J. Neurosci., 24, 2143, 10.1523/JNEUROSCI.3547-03.2004 Friedl, 2009, Collective cell migration in morphogenesis, regeneration and cancer, Nat. Rev. Mol. Cell Biol., 10, 445, 10.1038/nrm2720 Gallyas, 1992, Formation of “dark”(argyrophilic) neurons of various origin proceeds with a common mechanism of biophysical nature (a novel hypothesis), Acta Neuropathol., 83, 504, 10.1007/BF00310027 García-Fuster, 2003, Modulation of Fas receptor proteins and dynamin during opiate addiction and induction of opiate withdrawal in rat brain, Naunyn-Schmiede ’S. Arch. Pharmacol., 368, 421, 10.1007/s00210-003-0801-9 Gerstein, 1992, The effectiveness of drug treatment, Res. Publ. Assoc. Res. Nerv. Ment. Dis., 70, 253 Griffin, J.W., et al., 20 Axonal degeneration and disorders of the axonal cytoskeleton. The Axon: Structure, Function, and Pathophysiology, 1995, 375. Guo, 2007, Astrocytic pathology in the immune‐mediated motor neuron injury, Amyotroph. Lateral Scler., 8, 230, 10.1080/17482960701278612 Hu, 2002, Morphine induces apoptosis of human microglia and neurons, Neuropharmacology, 42, 829, 10.1016/S0028-3908(02)00030-8 Ishida, 2004, Argyrophilic dark neurons represent various states of neuronal damage in brain insults: some come to die and others survive, Neuroscience, 125, 633, 10.1016/j.neuroscience.2004.02.002 Jamot, 2003, Differential involvement of the mu and kappa opioid receptors in spatial learning, Genes Brain Behav., 2, 80, 10.1034/j.1601-183X.2003.00013.x Jang, 2003, Impaired water maze learning performance in μ-opioid receptor knockout mice, Mol. Brain Res., 117, 68, 10.1016/S0169-328X(03)00291-2 Joseph, 2000, Methadone maintenance treatment (MMT): a review of historical and clinical issues, Mt. Sinai J. Med., N. Y., 67, 347 Kahn, 2005, Repeated morphine treatment alters polysialylated neural cell adhesion molecule, glutamate decarboxylase‐67 expression and cell proliferation in the adult rat hippocampus, Eur. J. Neurosci., 21, 493, 10.1111/j.1460-9568.2005.03883.x Keeley, 2020, From random to regular: variation in the patterning of retinal mosaics, J. Comp. Neurol., 528, 2135, 10.1002/cne.24880 Kwon, 2020, Neuroinflammation in neurodegenerative disorders: the roles of microglia and astrocytes, Transl. Neurodegener., 9, 1, 10.1186/s40035-020-00221-2 Landucci, 2022, Neuronal and astrocytic morphological alterations driven by prolonged exposure with Δ9-tetrahydrocannabinol but not cannabidiol, Toxics, 10, 48, 10.3390/toxics10020048 Langhammer, 2010, Automated Sholl analysis of digitized neuronal morphology at multiple scales: whole cell Sholl analysis versus Sholl analysis of arbor subregions, Cytom. Part A, 77, 1160, 10.1002/cyto.a.20954 LaVoie, 2004, Microglial activation precedes dopamine terminal pathology in methamphetamine-induced neurotoxicity, Exp. Neurol., 187, 47, 10.1016/j.expneurol.2004.01.010 Lemaire, V., et al., Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. USA, 2000. 97(20) 11032–11037. Li, 2016, Methadone-induced damage to white matter integrity in methadone maintenance patients: a longitudinal self-control DTI study, Sci. Rep., 6, 1 Li, 2001, Reversal of morphine-induced memory impairment in mice by withdrawal in Morris water maze: possible involvement of cholinergic system, Pharmacol. Biochem. Behav., 68, 507, 10.1016/S0091-3057(01)00456-7 Lin, 2012, White matter abnormalities correlating with memory and depression in heroin users under methadone maintenance treatment, PLoS One, 7, 10.1371/journal.pone.0033809 Mandyam, 2004, Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone, J. Neurosci. Res., 76, 783, 10.1002/jnr.20090 Mao, 2002, Neuronal apoptosis associated with morphine tolerance: evidence for an opioid-induced neurotoxic mechanism, J. Neurosci., 22, 7650, 10.1523/JNEUROSCI.22-17-07650.2002 Mao, Y., Nearest neighbor distances calculation with ImageJ. 2016. Maragakis, 2006, Mechanisms of disease: astrocytes in neurodegenerative disease, Nat. Clin. Pract. Neurol., 2, 679, 10.1038/ncpneuro0355 Maren, 1994, Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning, Brain Res., 661, 25, 10.1016/0006-8993(94)91176-2 Mattick, 2003, Methadone maintenance versus no opioid replacement therapy for opioid dependence, Cochrane Database Syst. Rev., 2 Mazhari, 2015, Assessment of cognitive functions in methadone maintenance patients, Addict. Health, 7, 109 McEwen, 1992, The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress, Br. J. Psychiatry, 160, 18, 10.1192/S0007125000296645 Meilandt, 2004, Role of hippocampal CA3 μ-opioid receptors in spatial learning and memory, J. Neurosci., 24, 2953, 10.1523/JNEUROSCI.5569-03.2004 Minciacchi, 2009, Voronoi-based spatial analysis reveals selective interneuron changes in the cortex of FALS mice, Exp. Neurol., 215, 77, 10.1016/j.expneurol.2008.09.005 Mintzer, 2005, Opioid abuse and cognitive performance, Drug Alcohol Depend., 78, 225, 10.1016/j.drugalcdep.2004.10.008 Moghaddam, 2021, Elderberry diet ameliorates motor function and prevents oxidative stress-induced cell death in rat models of Huntington disease, Brain Res., 1762, 10.1016/j.brainres.2021.147444 Morris, 1990, Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning, Eur. J. Neurosci., 2, 1016, 10.1111/j.1460-9568.1990.tb00014.x Mulica, 2021, Astrocyte-neuron metabolic crosstalk in neurodegeneration: a mitochondrial perspective, Front. Endocrinol., 12 Muzio, 2021, Microglia in neuroinflammation and neurodegeneration: from understanding to therapy, Front. Neurosci., 15 Mychasiuk, 2012, Prenatal stress alters dendritic morphology and synaptic connectivity in the prefrontal cortex and hippocampus of developing offspring, Synapse, 66, 308, 10.1002/syn.21512 Myer, 2006, Essential protective roles of reactive astrocytes in traumatic brain injury, Brain, 129, 2761, 10.1093/brain/awl165 Norenberg, 2005, Mechanisms of ammonia-induced astrocyte swelling, Metab. Brain Dis., 20, 303, 10.1007/s11011-005-7911-7 Norton, 1992, Quantitative aspects of reactive gliosis: a review, Neurochem. Res., 17, 877, 10.1007/BF00993263 Nouri, 2019, Concomitant abuse of methadone and methamphetamine could impair spatial learning and memory in male rats, Learn. Motiv., 65, 43, 10.1016/j.lmot.2019.01.001 O’callaghan, 1991, Assessment of neurotoxicity: use of glial fibrillary acidic protein as a biomarker, Biomed. Environ. Sci. BES, 4, 197 O’Callaghan, 1994, Biochemical analysis of glial fibrillary acidic protein as a quantitative approach to neurotoxicity assessment: advantages, disadvantages and application to the assessment of NMDA receptor antagonist-induced neurotoxicity, Psychopharmacol. Bull., 30, 549 O’Callaghan, 1992, Enhanced expression of glial fibrillary acidic protein and the cupric silver degeneration reaction can be used as sensitive and early indicators of neurotoxicity, Neurotoxicology, 13, 113 O’Callaghan, 2005, Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity, Expert Opin. Drug Saf., 4, 433, 10.1517/14740338.4.3.433 Oppenheim, 1995, Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF, Nature, 373, 344, 10.1038/373344a0 Oppenheim, 2000, Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes, J. Neurosci., 20, 5001, 10.1523/JNEUROSCI.20-13-05001.2000 Owjfard, 2021, Effect of dimethyl fumarate on the motor function and spatial arrangement of primary motor cortical neurons in the sub-acute phase of stroke in a rat model, J. Stroke Cerebrovasc. Dis., 30, 10.1016/j.jstrokecerebrovasdis.2021.105630 Pannu, 2005, A novel role of lactosylceramide in the regulation of tumor necrosis factor α-mediated proliferation of rat primary astrocytes: Implications for astrogliosis following neurotrauma, J. Biol. Chem., 280, 13742, 10.1074/jbc.M411959200 Pekny, 2014, The dual role of astrocyte activation and reactive gliosis, Neurosci. Lett., 565, 30, 10.1016/j.neulet.2013.12.071 Pollock, 1996, Reexpression of morphine-induced oral stereotypy six months after last morphine sensitizing dose, Pharmacol. Biochem. Behav., 53, 67, 10.1016/0091-3057(95)00199-9 Porter, 1999, Emerging roles of caspase-3 in apoptosis, Cell Death Differ., 6, 99, 10.1038/sj.cdd.4400476 Prosser, 2006, Neuropsychological functioning in opiate-dependent subjects receiving and following methadone maintenance treatment, Drug Alcohol Depend., 84, 240, 10.1016/j.drugalcdep.2006.02.006 Rapeli, 2007, Methadone vs. buprenorphine/naloxone during early opioid substitution treatment: a naturalistic comparison of cognitive performance relative to healthy controls, BMC Clin. Pharmacol., 7, 1, 10.1186/1472-6904-7-5 Rashidiani-Rashidabadi, 2019, Sciatic nerve injury alters the spatial arrangement of neurons and glial cells in the anterior horn of the spinal cord. Neural Regeneration, Research, 14, 1833 Rayen, 2011, Fluoxetine during development reverses the effects of prenatal stress on depressive-like behavior and hippocampal neurogenesis in adolescence, PloS One, 6, 10.1371/journal.pone.0024003 Reinhard, 1988, The neurotoxicant MPTP (1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine) increases glial fibrillary acidic protein and decreases dopamine levels of the mouse striatum: evidence for glial response to injury, Neurosci. Lett., 95, 246, 10.1016/0304-3940(88)90665-9 Renault, 2015, Mitochondrial shape governs BAX-induced membrane permeabilization and apoptosis, Mol. Cell, 57, 69, 10.1016/j.molcel.2014.10.028 Sala, 1994, Chronic morphine affects working memory during treatment and withdrawal in rats: possible residual long-term impairment, Behav. Pharmacol., 10.1097/00008877-199410000-00002 San-Emeterio, 2006, Modulation of brain apoptosis-related proteins by the opioid antagonist naltrexone in mice, Neurosci. Lett., 403, 276, 10.1016/j.neulet.2006.04.053 Sankararaman, 2012, Methadone does not alter key parameters of adult hippocampal neurogenesis in the heroin-naïve rat, Neurosci. Lett., 516, 99, 10.1016/j.neulet.2012.03.066 Sarkala, 2019, Effect of G-CSF on the spatial arrangement of CA1 hippocampal pyramidal neurons after brain ischemia in the male rats, J. Chem. Neuroanat., 98, 80, 10.1016/j.jchemneu.2019.04.007 Sekine, 2008, Methamphetamine causes microglial activation in the brains of human abusers, J. Neurosci., 28, 5756, 10.1523/JNEUROSCI.1179-08.2008 Sendtner, 1992, Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section, Nature, 360, 757, 10.1038/360757a0 Shansky, 2016, Considering sex as a biological variable will be valuable for neuroscience research, J. Neurosci., 36, 11817, 10.1523/JNEUROSCI.1390-16.2016 Smith, 2017, Neuropathogenesis of Zika virus in a highly susceptible immunocompetent mouse model after antibody blockade of type I interferon, PLoS Negl. Trop. Dis., 11, 10.1371/journal.pntd.0005296 Sobue, 2021, Microglial gene signature reveals loss of homeostatic microglia associated with neurodegeneration of Alzheimer’s disease, Acta Neuropathol. Commun., 9, 1, 10.1186/s40478-020-01099-x Sofroniew, 2014, Astrogliosis, Cold Spring Harb. Perspect. Biol., 7, a020420, 10.1101/cshperspect.a020420 Spain, 1991, Chronic opioids impair acquisition of both radial maze and Y-maze choice escape, Psychopharmacology, 105, 101, 10.1007/BF02316870 Stewart, 1993, Effects of drugs, Behav. Pharmacol., 4, 289 Strużyńska, 2009, A glutamatergic component of lead toxicity in adult brain: the role of astrocytic glutamate transporters, Neurochem. Int., 55, 151, 10.1016/j.neuint.2009.01.025 Takuma, 2004, Astrocyte apoptosis: implications for neuroprotection, Prog. Neurobiol., 72, 111, 10.1016/j.pneurobio.2004.02.001 Taracha, 2009, Methadone is substantially less effective than morphine in modifying locomotor and brain Fos responses to subsequent methadone challenge in rats, Prog. Neuro Psychopharmacol. Biol. Psychiatry, 33, 1032, 10.1016/j.pnpbp.2009.05.015 Tegeder, 2004, Opioids as modulators of cell death and survival—unraveling mechanisms and revealing new indications, Pharmacol. Rev., 56, 351, 10.1124/pr.56.3.2 Thom, 2009, Temporal lobe sclerosis associated with hippocampal sclerosis in temporal lobe epilepsy: neuropathological features, J. Neuropathol. Exp. Neurol., 68, 928, 10.1097/NEN.0b013e3181b05d67 Thomas, 2004, Microglial activation is a pharmacologically specific marker for the neurotoxic amphetamines, Neurosci. Lett., 367, 349, 10.1016/j.neulet.2004.06.065 Thomas, 2004, Methamphetamine neurotoxicity in dopamine nerve endings of the striatum is associated with microglial activation, J. Pharmacol. Exp. Ther., 311, 1, 10.1124/jpet.104.070961 Thomas, 2005, Attenuated microglial activation mediates tolerance to the neurotoxic effects of methamphetamine, J. Neurochem., 92, 790, 10.1111/j.1471-4159.2004.02906.x Thomas, 2005, MK-801 and dextromethorphan block microglial activation and protect against methamphetamine-induced neurotoxicity, Brain Res., 1050, 190, 10.1016/j.brainres.2005.05.049 Tilleux, 2007, Neuroinflammation and regulation of glial glutamate uptake in neurological disorders, J. Neurosci. Res., 85, 2059, 10.1002/jnr.21325 Toombs, 2005, Methadone treatment for pain states, Am. Fam. Physician, 71, 1353 Tramullas, 2007, Chronic methadone treatment and repeated withdrawal impair cognition and increase the expression of apoptosis-related proteins in mouse brain, Psychopharmacology, 193, 107, 10.1007/s00213-007-0751-x Uno, 1997, Induction of tumor necrosis factor-α in the mouse hippocampus following transient forebrain ischemia, J. Cereb. Blood Flow. Metab., 17, 491, 10.1097/00004647-199705000-00002 Vaselbehagh, 2021, Coenzyme Q10 modulates apoptotic effects of chronic administration of methadone on NMRI mouse hippocampus, Cell J., 23, 538 Verdejo, 2005, Neuropsychological functioning in methadone maintenance patients versus abstinent heroin abusers, Drug Alcohol Depend., 78, 283, 10.1016/j.drugalcdep.2004.11.006 Volterra, 2005, Astrocytes, from brain glue to communication elements: the revolution continues, Nat. Rev. Neurosci., 6, 626, 10.1038/nrn1722 Wang, 2011, White matter impairment in heroin addicts undergoing methadone maintenance treatment and prolonged abstinence: a preliminary DTI study, Neurosci. Lett., 494, 49, 10.1016/j.neulet.2011.02.053 Yin, 1999, Fas-mediated cell death promoted by opioids, Nature, 397, 10.1038/16612 Yirmiya, 2011, Immune modulation of learning, memory, neural plasticity and neurogenesis, Brain Behav. Immun., 25, 181, 10.1016/j.bbi.2010.10.015 Zhang, 2010, Astrogliosis in CNS pathologies: is there a role for microglia?, Mol. Neurobiol., 41, 232, 10.1007/s12035-010-8098-4 Zhang, 2007, Caffeic acid attenuates neuronal damage, astrogliosis and glial scar formation in mouse brain with cryoinjury, Life Sci., 80, 530, 10.1016/j.lfs.2006.09.039 Zhao, 2004, Overexpression of glial cell line-derived neurotrophic factor in the CNS rescues motoneurons from programmed cell death and promotes their long-term survival following axotomy, Exp. Neurol., 190, 356, 10.1016/j.expneurol.2004.06.015 Zheng, 2002, Effects of scopolamine and physostigmine on acquisition of morphine-treated rats in Morris water maze performance, Acta Pharmacol. Sin., 23, 477