{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,9]],"date-time":"2026-01-09T01:21:55Z","timestamp":1767921715137,"version":"3.49.0"},"reference-count":80,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,8,9]],"date-time":"2023-08-09T00:00:00Z","timestamp":1691539200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurosci."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Mitochondrial dysfunction is postulated to be a central event in fetal alcohol spectrum disorders (FASD). People with the most severe form of FASD, fetal alcohol syndrome (FAS) are estimated to live only 34\u2009years (95% confidence interval, 31 to 37\u2009years), and adults who were born with any form of FASD often develop early aging. Mitochondrial dysfunction and mitochondrial DNA (mtDNA) damage, hallmarks of aging, are postulated central events in FASD. Ethanol (EtOH) can cause mtDNA damage, consequent increased oxidative stress, and changes in the mtDNA repair protein 8-oxoguanine DNA glycosylase-1 (OGG1). Studies of molecular mechanisms are limited by the absence of suitable human models and non-invasive tools.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We compared human and rat EtOH-exposed fetal brain tissues and neuronal cultures, and fetal brain-derived exosomes (FB-Es) from maternal blood. Rat FASD was induced by administering a 6.7% alcohol liquid diet to pregnant dams. Human fetal (11\u201321\u2009weeks) brain tissue was collected and characterized by maternal self-reported EtOH use. mtDNA was amplified by qPCR. OGG1 and Insulin-like growth factor 1 (IGF-1) mRNAs were assayed by qRT-PCR. Exosomal OGG1 was measured by ddPCR.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Maternal EtOH exposure increased mtDNA damage in fetal brain tissue and FB-Es. The damaged mtDNA in FB-Es correlated highly with small eye diameter, an anatomical hallmark of FASD. OGG1-mediated mtDNA repair was inhibited in EtOH-exposed fetal brain tissues. IGF-1 rescued neurons from EtOH-mediated mtDNA damage and OGG1 inhibition.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>The correlation between mtDNA damage and small eye size suggests that the amount of damaged mtDNA in FB-E may serve as a marker to predict which at risk fetuses will be born with FASD. Moreover, IGF-1 might reduce EtOH-caused mtDNA damage and neuronal apoptosis.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fnins.2023.1214958","type":"journal-article","created":{"date-parts":[[2023,8,9]],"date-time":"2023-08-09T07:11:20Z","timestamp":1691565080000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":10,"title":["In utero ethanol exposure induces mitochondrial DNA damage and inhibits mtDNA repair in developing brain"],"prefix":"10.3389","volume":"17","author":[{"given":"Nune","family":"Darbinian","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Armine","family":"Darbinyan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nana","family":"Merabova","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Myrna","family":"Kassem","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gabriel","family":"Tatevosian","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shohreh","family":"Amini","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laura","family":"Goetzl","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael E.","family":"Selzer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2023,8,9]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1196","DOI":"10.3390\/ijms21041196","article-title":"Assessment of nuclear and mitochondrial DNA, expression of mitochondria-related genes in different brain regions in rats after whole-body X-ray irradiation","volume":"21","author":"Abdullaev","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"2623","DOI":"10.1093\/nar\/24.13.2623","article-title":"Jos\u00e9 Costa, Janet Rettig Emanuel, PicoGreen quantitation of DNA: effective evaluation of samples pre-or Psost-PCR","volume":"24","author":"Ahn","year":"1996","journal-title":"Nucleic Acids Res."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1002\/jcp.21903","article-title":"p38SJ, a novel DINGG protein protects neuronal cells from alcohol induced injury and death","volume":"221","author":"Amini","year":"2009","journal-title":"J. Cell. Physiol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"1390","DOI":"10.1111\/acer.12378","article-title":"Maternal and neonatal plasma microRNA biomarkers for fetal alcohol exposure in an ovine model","volume":"38","author":"Balaraman","year":"2014","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"e0165081","DOI":"10.1371\/journal.pone.0165081","article-title":"Plasma miRNA profiles in pregnant women predict infant outcomes following prenatal alcohol exposure","volume":"11","author":"Balaraman","year":"2016","journal-title":"PLoS One"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"E981","DOI":"10.1152\/ajpendo.00354.2020","article-title":"Mitochondrial transformations in the aging human placenta","volume":"319","author":"Bartho","year":"2020","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1186\/1745-6150-8-12","article-title":"Exosomes secreted by human cells transport largely mRNA fragments that are enriched in the 3\u2032-untranslated regions","volume":"8","author":"Batagov","year":"2013","journal-title":"Biol. Direct"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1111\/add.12402","article-title":"Ethyl glucuronide in hair and fingernails as a long-term alcohol biomarker","volume":"109","author":"Berger","year":"2014","journal-title":"Addiction"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1186\/s12967-019-2105-y","article-title":"Placental mitochondrial DNA content is associated with childhood intelligence","volume":"17","author":"Bijnens","year":"2019","journal-title":"J. Transl. Med."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/s03009084(99)80039-x","article-title":"Base excision repair of 8-hydroxyguanine protects DNA from endogenous oxidative stress","volume":"81","author":"Boiteux","year":"1999","journal-title":"Biochimie"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1006\/abbi.2000.1773","article-title":"The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis","volume":"377","author":"Boiteux","year":"2000","journal-title":"Arch. Biochem. Biophys."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1586","DOI":"10.3390\/ijerph16091586","article-title":"Fetal cerebral artery mitochondrion as target of prenatal alcohol exposure","volume":"16","author":"Bukiya","year":"2019","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"1126","DOI":"10.1016\/j.neuron.2014.11.022","article-title":"Mitochondrial DNA: impacting central and peripheral nervous systems","volume":"84","author":"Carelli","year":"2014","journal-title":"Neuron"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"779","DOI":"10.1016\/s0891-5849(00)00172-6","article-title":"DNA damage, repair, and antioxidant systems in brain regions: a correlative study","volume":"28","author":"Cardozo-Pelaez","year":"2000","journal-title":"Free Radic. Biol. Med."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1468","DOI":"10.1086\/429412","article-title":"Anthony de ronde, infection with HIV-1 induces a decrease in mtDNA","volume":"191","author":"Casula","year":"2005","journal-title":"J. Infect. Dis."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1016\/j.bbagrm.2012.06.002","article-title":"Mitochondrial DNA damage and its consequences for mitochondrial gene expression","volume":"1819","author":"Cline","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"811","DOI":"10.1056\/NEJMoa012035","article-title":"Changes in mitochondrial DNA as a marker of nucleoside toxicity in HIV-infected patients","volume":"346","author":"C\u00f4t\u00e9","year":"2002","journal-title":"N. Engl. J. Med."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1089\/rej.2005.8.138","article-title":"Oxidative stress and aging: catalase is a longevity determinant enzyme","volume":"8","author":"Cutler","year":"2005","journal-title":"Rejuvenation Res."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"176","DOI":"10.16966\/2380-5536.176","article-title":"HIV-1 and HIV-1-tat induce mitochondrial DNA damage in human neurons. J HIV","volume":"6","author":"Darbinian","year":"2020","journal-title":"AIDS"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"135","DOI":"10.3390\/ijms24010135","article-title":"Molecular markers in maternal blood exosomes allow early detection of Fetal alcohol Spectrum disorders","volume":"24","author":"Darbinian","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"105181","DOI":"10.1016\/j.nbd.2020.105181","article-title":"Ethanol-mediated alterations in oligodendrocyte differentiation in the developing brain","volume":"148","author":"Darbinian","year":"","journal-title":"Neurobiol. Dis."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1007\/978-1-0716-1437-2_16","article-title":"Fetal brain injury models of Fetal alcohol syndrome (FAS): examination of neuronal morphologic condition using Sholl assay","volume":"2311","author":"Darbinian","year":"","journal-title":"Methods Mol Biol"},{"key":"ref330","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1007\/978-1-0716-1437-2_15","article-title":"Isolation of Primary Human and Rodent Brain Microvascular Endothelial Cells: Culturing, Characterization, and High-Efficiency Transfection","volume":"2311","author":"Darbinian","year":"","journal-title":"Methods Mol. Biol."},{"key":"ref280","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1002\/jcp.24392","article-title":"Neuroprotective activity of pDING in response to HIV-1 Tat","volume":"229","author":"Darbinian","year":"2014","journal-title":"J. Cell Physiol."},{"key":"ref270","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1038\/sj.gt.3302649","article-title":"p27(SJ), a novel protein in St John\u2019s Wort, that suppresses expression of HIV-1 genome","volume":"13","author":"Darbinian-Sarkissian","year":"2006","journal-title":"Gene Ther."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"497","DOI":"10.4103\/1673-5374.314294","article-title":"Oligodendrocyte pathology in the developing brain in Fetal alcohol syndrome","volume":"17","author":"Darbinian","year":"2022","journal-title":"Neural Regen. Res."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1007\/978-1-0716-1437-2_5","article-title":"Isolation and propagation of primary human and rodent embryonic neural progenitor cells and cortical neurons","volume":"2311","author":"Darbinyan","year":"2021","journal-title":"Methods Mol. Biol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1002\/jnr.23135","article-title":"Polyomavirus JC infection inhibits differentiation of oligodendrocyte progenitor cells","volume":"91","author":"Darbinyan","year":"","journal-title":"J. Neurosci. Res."},{"key":"ref26","first-page":"147","article-title":"Compartmentalized neuronal cultures","volume-title":"Methods Mol. Biol.","author":"Darbinyan","year":""},{"key":"ref27","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1007\/s11481-016-9669-6","article-title":"HIV-1 tat and cocaine impair survival of cultured primary neuronal cells via a mitochondrial pathway","volume":"11","author":"De Simone","year":"2016","journal-title":"J. Neuroimmune Pharmacol."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.mrrev.2017.02.001","article-title":"Repair of oxidatively induced DNA damage by DNA glycosylases: mechanisms of action, substrate specificities and excision kinetics","volume":"771","author":"Dizdaroglu","year":"2017","journal-title":"Mutat. Res. Rev. Mutat. Res."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1111\/ppe.12136","article-title":"The safe passage study: design, methods, recruitment, and follow-up approach","volume":"28","author":"Dukes","year":"2014","journal-title":"Paediatr. Perinat. Epidemiol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"14293","DOI":"10.1038\/s41598-017-14301-3","article-title":"Exosomal microRNA signatures in multiple sclerosis reflect disease status","volume":"7","author":"Ebrahimkhani","year":"2017","journal-title":"Sci. Rep."},{"key":"ref31","first-page":"132","volume-title":"Practical statistics for field biology","author":"Fowler","year":"2009"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"119","DOI":"10.3389\/fphys.2012.00119","article-title":"Emerging roles of exosomes in neuronglia communication","volume":"3","author":"Fruhbeis","year":"2012","journal-title":"Front. Physiol."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1007\/978-1-62703-739-6_31","article-title":"Quantitative PCR-based measurement of nuclear and mitochondrial DNA damage and repair in mammalian cells","volume":"1105","author":"Furda","year":"2014","journal-title":"Methods Mol. Biol."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1002\/acn3.296","article-title":"Novel window on early human neurodevelopment via fetal exosomes in maternal blood","volume":"3","author":"Goetzl","year":"2016","journal-title":"Ann Clin Transl Neurol"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1002\/pd.5474","article-title":"Noninvasive assessment of Fetal central nervous system insult: potential application to prenatal diagnosis","volume":"39","author":"Goetzl","year":"","journal-title":"Prenat Diagn"},{"key":"ref500","doi-asserted-by":"publisher","first-page":"e12583","DOI":"10.1111\/gbb.12583","article-title":"Novel biomarkers to assess in utero effects of maternal opioid use: First steps toward understanding short- and long-term neurodevelopmental sequelae","volume":"18","author":"Goetzl","year":"","journal-title":"Genes Brain Behav."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.tox.2017.03.010","article-title":"Simplified qPCR method for detecting excessive mtDNA damage induced by exogenous factors","volume":"382","author":"Gureev","year":"2017","journal-title":"Toxicology"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1016\/j.bpsc.2021.11.003","article-title":"Maternal inflammation during pregnancy and offspring brain development: the role of mitochondria","volume":"7","author":"Gyllenhammer","year":"2022","journal-title":"Biol Psychiatry Cogn Neurosci Neuroimaging"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"2049","DOI":"10.1053\/gast.2002.33613","article-title":"Alcohol and mitochondria: a dysfunctional relationship","volume":"122","author":"Hoek","year":"2002","journal-title":"Gastroenterology"},{"key":"ref39","author":"Hoyme","year":"2016"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"444","DOI":"10.1016\/j.ymeth.2010.01.033","article-title":"The QPCR assay for analysis of mitochondrial DNA damage, repair, and relative copy number","volume":"51","author":"Hunter","year":"2010","journal-title":"Methods"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"2374","DOI":"10.3390\/ijms20102374","article-title":"Role of mitochondrial DNA damage in ROS-mediated pathogenesis of age-related macular degeneration (AMD)","volume":"20","author":"Kaarniranta","year":"2019","journal-title":"Int. J. Mol. Sci."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"19.1.1","DOI":"10.1002\/0471142905.hg1901s62","article-title":"Analysis of oxidative damage by gene-specific quantitative PCR","volume":"62","author":"Kovalenko","year":"2009","journal-title":"Curr. Protoc. Hum. Genet."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1446","DOI":"10.1002\/prca.200700522","article-title":"Oligodendrocytes secrete exosomes containing major myelin and stressprotective proteins: trophic support for axons?","volume":"1","author":"Kramer-Albers","year":"2007","journal-title":"Proteomics Clin. Appl."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1016\/j.ijdevneu.2006.12.006","article-title":"A nontransformed oligodendrocyte precursor cell line, OL-1, facilitates studies of insulin-like growth factor-I signaling during oligodendrocyte development","volume":"25","author":"Lagarde","year":"2007","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"7710","DOI":"10.1523\/JNEUROSCI.23-20-07710.2003","article-title":"Insulin-like growth factor (IGF) signaling through type 1 IGF receptor plays an important role in remyelination","volume":"23","author":"Mason","year":"2003","journal-title":"J. Neurosci."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1002\/ddrr.68","article-title":"Prevalence and epidemiologic characteristics of FASD from various research methods with an emphasis on recent in-school studies","volume":"15","author":"May","year":"2009","journal-title":"Dev. Disabil. Res. Rev."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1542\/peds.2013-3319","article-title":"Prevalence and characteristics of fetal alcohol spectrum disorders","volume":"134","author":"May","year":"2014","journal-title":"Pediatrics"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1001\/jama.2017.21896","article-title":"Prevalence of Fetal alcohol Spectrum disorders in 4 US communities","volume":"319","author":"May","year":"2018","journal-title":"JAMA"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"804","DOI":"10.1007\/s10646-009-0457-4","article-title":"QPCR: a tool for analysis of mitochondrial and nuclear DNA damage in ecotoxicology","volume":"19","author":"Meyer","year":"2010","journal-title":"Ecotoxicology"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1007\/s40474-015-0053-7","article-title":"What happens when children with Fetal alcohol Spectrum disorders become adults?","volume":"2","author":"Moore","year":"2015","journal-title":"Curr. Dev. Disord. Rep."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"1637","DOI":"10.1091\/mbc.10.5.1637","article-title":"Expression and differential intracellular localization of two major forms of human 8-oxoguanine DNA glycosylase encoded by alternatively spliced OGG1 mRNAs","volume":"10","author":"Nishioka","year":"1999","journal-title":"Mol. Biol. Cell"},{"key":"ref52","year":"2015"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"1135","DOI":"10.3390\/ijerph120201135","article-title":"Nuclear and mitochondrial DNA alterations in newborns with prenatal exposure to cigarette smoke","volume":"12","author":"Pirini","year":"2015","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1490","DOI":"10.1002\/jcb.25103","article-title":"Base excision repair in the mitochondria","volume":"116","author":"Prakash","year":"2015","journal-title":"J. Cell. Biochem."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"245","DOI":"10.3102\/10769986014003245","article-title":"Critical values for Spearman's rank order correlation","volume":"14","author":"Ramsey","year":"1989","journal-title":"J. Educ. Statistics Fall"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1016\/j.freeradbiomed.2014.06.023","article-title":"Insulin and IGF-1 improve mitochondrial function in a PI-3K\/Akt-dependent manner and reduce mitochondrial generation of reactive oxygen species in Huntington's disease knock-in striatal cells","volume":"74","author":"Ribeiro","year":"2014","journal-title":"Free Radic. Biol. Med."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"947","DOI":"10.33549\/physiolres.931246","article-title":"The developmental changes in mitochondrial DNA content per cell in human cord blood leukocytes during gestation","volume":"57","author":"Pejznochov\u00e1","year":"2008","journal-title":"Physiol. Res."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"319","DOI":"10.3233\/JAD-131715","article-title":"Mitochondrial DNA copy numbers in pyramidal neurons are decreased and mitochondrial biogenesis transcriptome signaling is disrupted in Alzheimer's disease hippocampi","volume":"40","author":"Rice","year":"2014","journal-title":"J. Alzheimers Dis."},{"key":"ref59","doi-asserted-by":"publisher","first-page":"1470","DOI":"10.1038\/ncb1800","article-title":"Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers","volume":"10","author":"Skog","year":"2008","journal-title":"Nat. Cell Biol."},{"key":"ref590","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1016\/j.ejca.2016.10.011","article-title":"Molecular lipid species in urinary exosomes as potential prostate cancer biomarkers","volume":"70","author":"Skotland","year":"2017","journal-title":"Eur. J. Cancer."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1097\/AOG.0b013e3182255999","article-title":"Timing of indicated latepreterm and early-term birth","volume":"118","author":"Spong","year":"2011","journal-title":"Obstet. Gynecol."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"766","DOI":"10.1038\/cr.2014.44","article-title":"Double-stranded DNA in exosomes: a novel biomarker in cancer detection","volume":"24","author":"Thakur","year":"2014","journal-title":"Cell Res."},{"key":"ref62","doi-asserted-by":"publisher","first-page":"1596","DOI":"10.1080\/15548627.2018.1476810","article-title":"HIV-1 TAT-mediated microglial activation: role of mitochondrial dysfunction and defective mitophagy","volume":"14","author":"Thangaraj","year":"2018","journal-title":"Autophagy"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"1414","DOI":"10.1111\/acer.14066","article-title":"Ethanol exposure increases miR-140 in extracellular vesicles: implications for Fetal neural stem cell proliferation and maturation","volume":"43","author":"Tseng","year":"2019","journal-title":"Alcohol. Clin. Exp. Res."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2022\/7960198","article-title":"Exposure to a pathological condition May be required for the cells to secrete exosomes containing mtDNA aberration","volume":"2022","author":"Vaidya","year":"2022","journal-title":"J Nucleic Acids."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"654","DOI":"10.1038\/ncb1596","article-title":"Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells","volume":"9","author":"Valadi","year":"2007","journal-title":"Nat. Cell Biol."},{"key":"ref66","first-page":"106","article-title":"Focus on: neurotransmitter systems","volume":"34","author":"Valenzuela","year":"2011","journal-title":"Alcohol Res. Health"},{"key":"ref67","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/s09218777(00)00022-7","article-title":"Detection of 8-oxoG DNA glycosylase activity and OGG1 transcripts in the rat CNS","volume":"460","author":"Verjat","year":"2000","journal-title":"Mutat. Res."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.1002\/jcp.24528","article-title":"Involvement of IRS-1 interaction with ADAM10 in the regulation of neurite extension","volume":"229","author":"Wang","year":"2014","journal-title":"J. Cell. Physiol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1007\/s12012-010-9085-8","article-title":"Perinatal tobacco smoke exposure increases vascular oxidative stress and mitochondrial damage in non-human primates","volume":"10","author":"Westbrook","year":"2010","journal-title":"Cardiovasc. Toxicol."},{"key":"ref70","doi-asserted-by":"publisher","first-page":"1396823","DOI":"10.1080\/20013078.2017.1396823","article-title":"Updating the MISEV minimal requirements for extracellular vesicle studies: building bridges to reproducibility","volume":"6","author":"Witwer","year":"2017","journal-title":"J Extracell Vesicles"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"9047","DOI":"10.1523\/JNEUROSCI.2557-08.2008","article-title":"Oxoguanine glycosylase 1 protects against methamphetamine-enhanced fetal brain oxidative DNA damage and neurodevelopmental deficits","volume":"28","author":"Wong","year":"2008","journal-title":"J. Neurosci."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"514","DOI":"10.1073\/pnas.94.2.514","article-title":"Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress","volume":"94","author":"Yakes","year":"1997","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"1110","DOI":"10.1016\/j.dnarep.2008.03.012","article-title":"Mitochondrial DNA damage and repair in neurodegenerative disorders","volume":"7","author":"Yang","year":"2008","journal-title":"DNA Repair (Amst)"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"3063","DOI":"10.1210\/endo.140.7.6754","article-title":"Insulin-like growth factor I protects oligodendrocytes from tumor necrosis factor-alpha-induced injury","volume":"140","author":"Ye","year":"1999","journal-title":"Endocrinology"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"2491","DOI":"10.1021\/acs.chemrestox.0c00083","article-title":"Mitochondrial DNA damage: prevalence, biological consequence, and emerging pathways","volume":"33","author":"Zhao","year":"2020","journal-title":"Chem. Res. 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