Transgenerational modification of hippocampus TNF-α and S100B levels in the offspring of rats chronically exposed to morphine during adolescence

References

• Sehgal N, Colson J, Smith HS. Chronic pain treatment with opioid analgesics: benefits versus harms of long-term therapy. Expert Rev Neurother 2013;13:1201–1220.
   PubMed Web of Science ®Google Scholar
• Salsitz EA. Chronic pain, chronic opioid addiction: a complex nexus. J Med Toxicol 2016;12:54–57.
   PubMed Web of Science ®Google Scholar
• Garland EL, Froeliger B, Zeidan F, Partin K, Howard MO. The downward spiral of chronic pain, prescription opioid misuse, and addiction: cognitive, affective, and neuropsychopharmacologic pathways. Neurosci Biobehav Rev 2013;37:2597–2607.
   PubMed Web of Science ®Google Scholar
• Ling W, Mooney L, Hillhouse M. Prescription opioid abuse, pain and addiction: clinical issues and implications. Drug Alcohol Rev 2011;30:300–305.
   PubMed Web of Science ®Google Scholar
• Madsen HB, Brown RM, Lawrence AJ. Neuroplasticity in addiction: cellular and transcriptional perspectives. Front Mol Neurosci 2012;5:99.
   PubMed Web of Science ®Google Scholar
• Williams JT, Christie MJ, Manzoni O. Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 2001;81:299–343.
   PubMed Web of Science ®Google Scholar
• Bodnar RJ. Endogenous Opiates and Behavior: 2015. Peptides 2017;88:126–188.
   Web of Science ®Google Scholar
• Eichenbaum H. Conscious awareness, memory and the hippocampus. Nat Neurosci 1999;2:775–776.
   PubMed Web of Science ®Google Scholar
• Yang SN, Liu CA, Chung MY, Huang HC, Yeh GC, Wong CS, Lin WW, Yang CH, Tao PL. Alterations of postsynaptic density proteins in the hippocampus of rat offspring from the morphine-addicted mother: Beneficial effect of dextromethorphan. Hippocampus 2006;16:521–530.
   PubMed Web of Science ®Google Scholar
• Sadegh M, Fathollahi Y. Repetitive systemic morphine alters activity-dependent plasticity of Schaffer-collateral-CA1 pyramidal cell synapses: involvement of adenosine A1 receptors and adenosine deaminase. J Neurosci Res 2014;92:1395–1408.
   PubMed Web of Science ®Google Scholar
• Sadegh M, Fathollahi Y, Naghdi N, Semnanian S. Morphine deteriorates spatial memory in sodium salicylate treated rats. Eur J Pharmacol 2013;704:1–6.
   PubMed Web of Science ®Google Scholar
• Nestler EJ. Epigenetic mechanisms of drug addiction. Neuropharmacology 2014;76:259–268.
   PubMed Web of Science ®Google Scholar
• Higgins GA, Allyn-Feuer A, Athey BD. Epigenomic mapping and effect sizes of noncoding variants associated with psychotropic drug response. Pharmacogenomics 2015;16:1565–1583.
   PubMed Web of Science ®Google Scholar
• Ciccarelli A, Calza A, Santoru F, Grasso F, Concas A, Sassoe-Pognetto M, Giustetto M. Morphine withdrawal produces ERK-dependent and ERK-independent epigenetic marks in neurons of the nucleus accumbens and lateral septum. Neuropharmacology 2013;70:168–179.
   PubMed Web of Science ®Google Scholar
• Ebrahimi G, Asadikaram G, Akbari H, Nematollahi MH, Abolhassani M, Shahabinejad G, Khodadadnejad L, Hashemi M. Elevated levels of DNA methylation at the OPRM1 promoter region in men with opioid use disorder. Am J Drug Alcohol Abuse 2017;1–7.
   Google Scholar
• Ruffle JK. Molecular neurobiology of addiction: what’s all the (Delta)FosB about? Am J Drug Alcohol Abuse 2014;40:428–437.
   PubMed Web of Science ®Google Scholar
• Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL. Functions of S100 proteins. Curr Mol Med 2013;13:24–57.
   PubMed Web of Science ®Google Scholar
• Rothermundt M, Peters M, Prehn JH, Arolt V. S100B in brain damage and neurodegeneration. Microsc Res Tech 2003;60:614–632.
   PubMed Web of Science ®Google Scholar
• Astrand R, Unden J, Romner B. Clinical use of the calcium-binding S100B protein. Methods Mol Biol 2013;963:373–384.
   PubMedGoogle Scholar
• Kleindienst A, Hesse F, Bullock MR, Buchfelder M. The neurotrophic protein S100B: value as a marker of brain damage and possible therapeutic implications. Prog Brain Res 2007;161:317–325.
   PubMed Web of Science ®Google Scholar
• Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F, Tubaro C, Giambanco I. S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta 2009;1793:1008–1022.
   PubMed Web of Science ®Google Scholar
• Bianchi R, Kastrisianaki E, Giambanco I, Donato R. S100B protein stimulates microglia migration via RAGE-dependent up-regulation of chemokine expression and release. J Biol Chem 2011;286:7214–7226.
   PubMed Web of Science ®Google Scholar
• Park KM, Bowers WJ. Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell Signal 2010;22:977–983.
   PubMed Web of Science ®Google Scholar
• Montgomery SL, Bowers WJ. Tumor necrosis factor-alpha and the roles it plays in homeostatic and degenerative processes within the central nervous system. J Neuroimmune Pharmacol 2012;7:42–59.
   PubMed Web of Science ®Google Scholar
• Olmos G, Llado J. Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity. Mediators Inflamm 2014;2014:861231.
   PubMed Web of Science ®Google Scholar
• Hao S, Liu S, Zheng X, Zheng W, Ouyang H, Mata M, Fink DJ. The role of TNFalpha in the periaqueductal gray during naloxone-precipitated morphine withdrawal in rats. Neuropsychopharmacology 2011;36:664–676.
   PubMed Web of Science ®Google Scholar
• Tian X, Hua F, Sandhu HK, Chao D, Balboni G, Salvadori S, He X, Xia Y. Effect of delta-opioid receptor activation on BDNF-TrkB vs. TNF-alpha in the mouse cortex exposed to prolonged hypoxia. Int J Mol Sci 2013;14:15959–15976.
   Google Scholar
• Himeda T, Kanbara S, Oki C, Kato H, Araki T. Effects of chronic administration with nilvadipine against immunohistochemical changes related to aging in the mouse hippocampus. Metab Brain Dis 2005;20:141–153.
   PubMed Web of Science ®Google Scholar
• Martuscello RT, Spengler RN, Bonoiu AC, Davidson BA, Helinski J, Ding H, Mahajan S, Kumar R, Bergey EJ, Knight PR, Prasad PN, Ignatowski TA. Increasing TNF levels solely in the rat hippocampus produces persistent pain-like symptoms. Pain 2012;153:1871–1882.
   PubMed Web of Science ®Google Scholar
• Krawczyk A, Jaworska-Adamu J, Rycerz K. Immunohistochemical evaluation of hippocampal CA1 region astrocytes in 10-day-old rats after monosodium glutamate treatment. Pol J Vet Sci 2015;18:767–774.
   PubMed Web of Science ®Google Scholar
• Mithbaokar P, Fiorito F, Della Morte R, Maharajan V, Costagliola A. Chronic maternal morphine alters calbindin D-28k expression pattern in postnatal mouse brain. Synapse 2016;70:15–23.
   PubMed Web of Science ®Google Scholar
• Sadegh M, Fathollahi Y, Semnanian S. The chronic treatment in vivo of salicylate or morphine alters excitatory effects of subsequent salicylate or morphine tests in vitro in hippocampus area CA1. Eur J Pharmacol 2013;721:103–108.
   PubMed Web of Science ®Google Scholar
• Hosseinmardi N, Fathollahi Y, Naghdi N, Javan M. Theta pulse stimulation: a natural stimulus pattern can trigger long-term depression but fails to reverse long-term potentiation in morphine withdrawn hippocampus area CA1. Brain Res 2009;1296:1–14.
   PubMed Web of Science ®Google Scholar
• Salmanzadeh F, Fathollahi Y, Semnanian S, Shafizadeh M. Long-term potentiation as an electrophysiological assay for morphine dependence and withdrawal in rats: an in vitro study. J Neurosci Methods 2003;124:189–196.
   PubMed Web of Science ®Google Scholar
• Byrnes JJ, Johnson NL, Carini LM, Byrnes EM. Multigenerational effects of adolescent morphine exposure on dopamine D2 receptor function. Psychopharmacology (Berl) 2013;227:263–272.
   PubMed Web of Science ®Google Scholar
• Byrnes JJ, Babb JA, Scanlan VF, Byrnes EM. Adolescent opioid exposure in female rats: transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav Brain Res 2011;218:200–205.
   PubMed Web of Science ®Google Scholar
• Yohn NL, Bartolomei MS, Blendy JA. Multigenerational and transgenerational inheritance of drug exposure: the effects of alcohol, opiates, cocaine, marijuana, and nicotine. Prog Biophys Mol Biol 2015;118:21–33.
   PubMed Web of Science ®Google Scholar
• Renthal W, Nestler EJ. Epigenetic mechanisms in drug addiction. Trends Mol Med 2008;14:341–350.
   PubMed Web of Science ®Google Scholar
• Doehring A, Oertel BG, Sittl R, Lotsch J. Chronic opioid use is associated with increased DNA methylation correlating with increased clinical pain. Pain 2013;154:15–23.
   PubMed Web of Science ®Google Scholar
• Cicero TJ, Adams ML, Giordano A, Miller BT, O’Connor L, Nock B. Influence of morphine exposure during adolescence on the sexual maturation of male rats and the development of their offspring. J Pharmacol Exp Ther 1991;256:1086–1093.
   PubMed Web of Science ®Google Scholar
• Peterson PK, Molitor TW, Chao CC. The opioid-cytokine connection. J Neuroimmunol 1998;83:63–69.
   PubMed Web of Science ®Google Scholar
• Cao F, Gao F, Xu AJ, Chen ZJ, Chen SS, Yang H, Yu HH, Mei W, Liu XJ, Xiao XP, Yang SB, Tian XB, Wang XR, Tian YK. Regulation of spinal neuroimmune responses by prolonged morphine treatment in a rat model of cancer induced bone pain. Brain Res 2010;1326:162–173.
   PubMed Web of Science ®Google Scholar
• Borner C, Kraus J. Inhibition of NF-kappaB by opioids in T cells. J Immunol 2013;191:4640–4647.
   PubMed Web of Science ®Google Scholar
• Roy S, Barke RA, Loh HH. MU-opioid receptor-knockout mice: role of mu-opioid receptor in morphine mediated immune functions. Brain Res Mol Brain Res 1998;61:190–194.
   PubMedGoogle Scholar
• Rozisky JR, Laste G, de Macedo IC, Santos VS, Krolow R, Noschang C, Vanzella C, Bertoldi K, Lovatel GA, de Souza IC, Siqueira IR, Dalmaz C, Caumo W, Torres IL. Neonatal morphine administration leads to changes in hippocampal BDNF levels and antioxidant enzyme activity in the adult life of rats. Neurochem Res 2013;38:494–503.
   PubMed Web of Science ®Google Scholar
• Sawaya BE, Deshmane SL, Mukerjee R, Fan S, Khalili K. TNF alpha production in morphine-treated human neural cells is NF-kappaB-dependent. J Neuroimmune Pharmacol 2009;4:140–149.
   PubMed Web of Science ®Google Scholar
• Kruglov AA, Kuchmiy A, Grivennikov SI, Tumanov AV, Kuprash DV, Nedospasov SA. Physiological functions of tumor necrosis factor and the consequences of its pathologic overexpression or blockade: mouse models. Cytokine Growth Factor Rev 2008;19:231–244.
   PubMed Web of Science ®Google Scholar
• Pan J, He L, Li X, Li M, Zhang X, Venesky J, Li Y, Peng Y. Activating autophagy in hippocampal cells alleviates the morphine-induced memory impairment. Mol Neurobiol 2016;54:1710–1724.
   PubMed Web of Science ®Google Scholar
• Merighi S, Gessi S, Varani K, Fazzi D, Stefanelli A, Borea PA. Morphine mediates a proinflammatory phenotype via mu-opioid receptor-PKCvarepsilon-Akt-ERK1/2 signaling pathway in activated microglial cells. Biochem Pharmacol 2013;86:487–496.
   PubMed Web of Science ®Google Scholar
• Johnson NL, Carini L, Schenk ME, Stewart M, Byrnes EM. Adolescent opiate exposure in the female rat induces subtle alterations in maternal care and transgenerational effects on play behavior. Front Psychiatry 2011;2:29.
   PubMedGoogle Scholar
• Lynch JL, Banks WA. Opiate modulation of IL-1alpha, IL-2, and TNF-alpha transport across the blood-brain barrier. Brain Behav Immun 2008;22:1096–1102.
   PubMed Web of Science ®Google Scholar
• Granstrem O, Adriani W, Shumilina M, Izykenova G, Dambinova S, Laviola G. Specific changes in levels of autoantibodies to glutamate and opiate receptors induced by morphine administration in rats. Neurosci Lett 2006;403:1–5.
   PubMed Web of Science ®Google Scholar
• Vassoler FM, Byrnes EM, Pierce RC. The impact of exposure to addictive drugs on future generations: physiological and behavioral effects. Neuropharmacology 2014;76:269–275.
   PubMed Web of Science ®Google Scholar
• Edwards MM, Robinson SR. TNF alpha affects the expression of GFAP and S100B: implications for Alzheimer’s disease. J Neural Transm (Vienna) 2006;113:1709–1715.
   PubMed Web of Science ®Google Scholar
• Hayakata T, Shiozaki T, Tasaki O, Ikegawa H, Inoue Y, Toshiyuki F, Hosotubo H, Kieko F, Yamashita T, Tanaka H, Shimazu T, Sugimoto H. Changes in CSF S100B and cytokine concentrations in early-phase severe traumatic brain injury. Shock 2004;22:102–107.
   PubMed Web of Science ®Google Scholar
• Sathe K, Maetzler W, Lang JD, Mounsey RB, Fleckenstein C, Martin HL, Schulte C, Mustafa S, Synofzik M, Vukovic Z, Itohara S, Berg D, Teismann P. S100B is increased in Parkinson’s disease and ablation protects against MPTP-induced toxicity through the RAGE and TNF-alpha pathway. Brain 2012;135:3336–3347.
   PubMed Web of Science ®Google Scholar
• Somera-Molina KC, Nair S, Van Eldik LJ, Watterson DM, Wainwright MS. Enhanced microglial activation and proinflammatory cytokine upregulation are linked to increased susceptibility to seizures and neurologic injury in a ‘two-hit’ seizure model. Brain Res 2009;1282:162–172.
   PubMed Web of Science ®Google Scholar
• Bianchi R, Giambanco I, Donato R. S100B/RAGE-dependent activation of microglia via NF-kappaB and AP-1 Co-regulation of COX-2 expression by S100B, IL-1beta and TNF-alpha. Neurobiol Aging 2010;31:665–677.
   PubMed Web of Science ®Google Scholar