{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T15:07:23Z","timestamp":1740150443448,"version":"3.37.3"},"reference-count":111,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2019,12,10]],"date-time":"2019-12-10T00:00:00Z","timestamp":1575936000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"name":"program \u201cSupporting Postdoctoral Researchers\u201d","award":["5001552"],"award-info":[{"award-number":["5001552"]}]},{"DOI":"10.13039\/501100003447","name":"State Scholarships Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003447","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Greek State and European Social Fund"},{"name":"REA Maternity Clinic","award":["11191\/SARG"],"award-info":[{"award-number":["11191\/SARG"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Our previous postmortem studies on neonates with neuropathological injury of perinatal hypoxia\/ischemia (PHI) showed a dramatic reduction of tyrosine hydroxylase expression (dopamine synthesis enzyme) in substantia nigra (SN) neurons, with reduction of their cellular size. In order to investigate if the above observations represent an early stage of SN degeneration, we immunohistochemically studied the expression of cleaved caspase-3 (CCP3), apoptosis inducing factor (AIF), and DNA fragmentation by using terminal deoxynucleotidyltransferase-mediated dUTP-biotin 3\u2032-end-labeling (TUNEL) technique in the SN of 22 autopsied neonates (corrected age ranging from 34 to 46.5 gestational weeks), in relation to the severity\/duration of PHI injury, as estimated by neuropathological criteria. No CCP3-immunoreactive neurons and a limited number of apoptotic TUNEL-positive neurons with pyknotic characteristics were found in the SN. Nuclear AIF staining was revealed only in few SN neurons, indicating the presence of early signs of AIF-mediated degeneration. By contrast, motor neurons of the oculomotor nucleus showed higher cytoplasmic AIF expression and nuclear translocation, possibly attributed to the combined effect of developmental processes and increased oxidative stress induced by antemortem and postmortem factors. Our study indicates the activation of AIF, but not CCP3, in the SN and oculomotor nucleus of the human neonate in the developmentally critical perinatal period.<\/jats:p>","DOI":"10.1093\/jnen\/nlz114","type":"journal-article","created":{"date-parts":[[2019,12,5]],"date-time":"2019-12-05T10:10:47Z","timestamp":1575540647000},"page":"86-101","source":"Crossref","is-referenced-by-count":2,"title":["Apoptotic Markers in the Midbrain of the Human Neonate After Perinatal Hypoxic\/Ischemic Injury"],"prefix":"10.1093","volume":"79","author":[{"given":"Marianna A","family":"Pagida","sequence":"first","affiliation":[{"name":"1st Department of Psychiatry (MPag, MC-P, MPan); Laboratory of Neurobiology and Histochemistry, University Mental Health Research Institute (MPag, MC-P, MPan); and 1st Department of Pathology (AK, EP), National and Kapodistrian University of Athens, Athens, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anastasia E","family":"Konstantinidou","sequence":"additional","affiliation":[{"name":"1st Department of Psychiatry (MPag, MC-P, MPan); Laboratory of Neurobiology and Histochemistry, University Mental Health Research Institute (MPag, MC-P, MPan); and 1st Department of Pathology (AK, EP), National and Kapodistrian University of Athens, Athens, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Margarita A","family":"Chrysanthou-Piterou","sequence":"additional","affiliation":[{"name":"1st Department of Psychiatry (MPag, MC-P, MPan); Laboratory of Neurobiology and Histochemistry, University Mental Health Research Institute (MPag, MC-P, MPan); and 1st Department of Pathology (AK, EP), National and Kapodistrian University of Athens, Athens, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Efstratios S","family":"Patsouris","sequence":"additional","affiliation":[{"name":"1st Department of Psychiatry (MPag, MC-P, MPan); Laboratory of Neurobiology and Histochemistry, University Mental Health Research Institute (MPag, MC-P, MPan); and 1st Department of Pathology (AK, EP), National and Kapodistrian University of Athens, Athens, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria T","family":"Panayotacopoulou","sequence":"additional","affiliation":[{"name":"1st Department of Psychiatry (MPag, MC-P, MPan); Laboratory of Neurobiology and Histochemistry, University Mental Health Research Institute (MPag, MC-P, MPan); and 1st Department of Pathology (AK, EP), National and Kapodistrian University of Athens, Athens, Greece"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2019,12,10]]},"reference":[{"key":"2024032523300381600_nlz114-B1","doi-asserted-by":"crossref","first-page":"78","DOI":"10.3389\/fncel.2017.00078","article-title":"Neonatal hypoxia ischaemia: Mechanisms, models, and therapeutic challenges","volume":"11","author":"Millar","year":"2017","journal-title":"Front Cell Neurosci"},{"key":"2024032523300381600_nlz114-B2","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1002\/bdrc.21139","article-title":"Fetal programming of neuropsychiatric disorders","volume":"108","author":"Faa","year":"2016","journal-title":"Birth Defect Res C"},{"key":"2024032523300381600_nlz114-B3","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s42000-018-0007-7","article-title":"Perinatal hypoxia as a risk factor for psychopathology later in life: The role of dopamine and neurotrophins","volume":"17","author":"Giannopoulou","year":"2018","journal-title":"Hormones (Athens)"},{"key":"2024032523300381600_nlz114-B4","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1093\/schbul\/sbn080","article-title":"Gene-environment interaction and covariation in schizophrenia: The role of obstetric complications","volume":"34","author":"Mittal","year":"2008","journal-title":"Schizophr Bull"},{"key":"2024032523300381600_nlz114-B5","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.siny.2007.07.006","article-title":"Outcome after intrapartum hypoxic ischaemia at term","volume":"12","author":"Rennie","year":"2007","journal-title":"Semin Fetal Neonatal Med"},{"key":"2024032523300381600_nlz114-B6","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1007\/s10519-016-9784-4","article-title":"Pre- and perinatal ischemia-hypoxia, the ischemia-hypoxia response pathway, and ADHD risk","volume":"46","author":"Smith","year":"2016","journal-title":"Behav Genet"},{"key":"2024032523300381600_nlz114-B7","first-page":"441","volume-title":"The Human Nervous System","author":"Halliday","year":"2012","edition":"3rd ed"},{"key":"2024032523300381600_nlz114-B8","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/j.ajpath.2015.09.023","article-title":"Dopaminergic neurons and brain reward pathways: From neurogenesis to circuit assembly","volume":"186","author":"Luo","year":"2016","journal-title":"Am J Pathol"},{"key":"2024032523300381600_nlz114-B9","doi-asserted-by":"crossref","first-page":"110","DOI":"10.3389\/fncir.2017.00110","article-title":"Dopamine and acetylcholine, a circuit point of view in Parkinson\u2019s disease","volume":"11","author":"Rizzi","year":"2017","journal-title":"Front Neural Circuits"},{"key":"2024032523300381600_nlz114-B10","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1177\/0269881114563634","article-title":"Glutamate and dopamine in schizophrenia: An update for the 21st century","volume":"29","author":"Howes","year":"2015","journal-title":"J Psychopharmacol"},{"key":"2024032523300381600_nlz114-B11","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.biopsych.2016.03.2104","article-title":"Pathway-specific dopamine abnormalities in schizophrenia","volume":"81","author":"Weinstein","year":"2017","journal-title":"Biol Psychiatry"},{"key":"2024032523300381600_nlz114-B12","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.tins.2008.09.010","article-title":"The dopaminergic hypothesis of attention-deficit\/hyperactivity disorder needs re-examining","volume":"32","author":"Gonon","year":"2009","journal-title":"Trends Neurosci"},{"key":"2024032523300381600_nlz114-B13","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/S0149-7634(03)00012-5","article-title":"Birth insult interacts with stress at adulthood to alter dopaminergic function in animal models: Possible implications for schizophrenia and other disorders","volume":"27","author":"Boksa","year":"2003","journal-title":"Neurosci Biobehav Rev"},{"key":"2024032523300381600_nlz114-B14","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1016\/0306-4522(92)90447-A","article-title":"Neonatal hypoxic-ischemic or excitotoxic striatal injury results in a decreased adult number of substantia nigra neurons","volume":"50","author":"Burke","year":"1992","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0006-8993(91)91041-X","article-title":"Asphyctic lesion: Proliferation of tyrosine hydroxylase-immunoreactive nerve cell bodies in the rat substantia nigra and functional changes in dopamine neurotransmission","volume":"543","author":"Bjelke","year":"1991","journal-title":"Brain Res"},{"key":"2024032523300381600_nlz114-B16","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/S0304-3940(96)13293-6","article-title":"Perinatal asphyxia-induced changes in rat brain tyrosine hydroxylase-immunoreactive cell body number: Effects of nicotine treatment","volume":"221","author":"Chen","year":"1997","journal-title":"Neurosci Lett"},{"key":"2024032523300381600_nlz114-B17","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/0306-4522(95)00282-N","article-title":"Apoptosis in substantia nigra following developmental hypoxic-ischemic injury","volume":"69","author":"Oo","year":"1995","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B18","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1203\/01.PDR.0000115679.86566.C4","article-title":"Lipid peroxidation, caspase-3 immunoreactivity, and pyknosis in late-gestation fetal sheep brain after umbilical cord occlusion","volume":"55","author":"Castillo-Melendez","year":"2004","journal-title":"Pediatr Res"},{"key":"2024032523300381600_nlz114-B19","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1097\/NEN.0b013e31828b48b3","article-title":"Vulnerability of the mesencephalic dopaminergic neurons of the human neonate to prolonged perinatal hypoxia: An immunohistochemical study of tyrosine hydroxylase expression in autopsy material","volume":"72","author":"Pagida","year":"2013","journal-title":"J Neuropathol Exp Neurol"},{"key":"2024032523300381600_nlz114-B20","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1038\/sj.cdd.4400607","article-title":"Caspases: A decade of death research","volume":"6","author":"Thornberry","year":"1999","journal-title":"Cell Death Differ"},{"key":"2024032523300381600_nlz114-B21","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1083\/jcb.119.3.493","article-title":"Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation","volume":"119","author":"Gavrieli","year":"1992","journal-title":"J Cell Biol"},{"key":"2024032523300381600_nlz114-B22","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/s004410000203","article-title":"Detection of apoptosis in tissue sections","volume":"301","author":"Stadelmann","year":"2000","journal-title":"Cell Tissue Res"},{"key":"2024032523300381600_nlz114-B23","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/S1385-299X(99)00012-4","article-title":"Neuronal apoptosis studied by a sequential TUNEL technique: A method for tract-tracing","volume":"4","author":"Hara","year":"1999","journal-title":"Brain Res Brain Res Protoc"},{"key":"2024032523300381600_nlz114-B24","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.ebiom.2018.03.016","article-title":"Apoptosis-inducing factor (AIF) in physiology and disease: The tale of a repented natural born killer","volume":"30","author":"Bano","year":"2018","journal-title":"EBioMedicine"},{"key":"2024032523300381600_nlz114-B25","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.neulet.2013.08.054","article-title":"Immunohistochemical demonstration of urocortin 1 in Edinger-Westphal nucleus of the human neonate: Colocalization with tyrosine hydroxylase under acute perinatal hypoxia","volume":"554","author":"Pagida","year":"2013","journal-title":"Neurosci Lett"},{"author":"Fallet-Bianco","key":"2024032523300381600_nlz114-B26"},{"key":"2024032523300381600_nlz114-B27","first-page":"2027","volume-title":"Potter's Pathology of the Fetus, Infant and Child","author":"Rorke-Adams","year":"2007","edition":". 2nd ed"},{"key":"2024032523300381600_nlz114-B28","first-page":"171","volume-title":"Pathology and Genetics, Developmental Neuropathology","author":"Squier","year":"2004"},{"key":"2024032523300381600_nlz114-B29","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1159\/000439270","article-title":"The effect of perinatal hypoxic\/ischemic injury on tyrosine hydroxylase expression in the locus coeruleus of the human neonate","volume":"38","author":"Pagida","year":"2016","journal-title":"Dev Neurosci"},{"volume-title":"Atlas of the Human Brainstem","year":"1995","author":"Paxinos","key":"2024032523300381600_nlz114-B30"},{"key":"2024032523300381600_nlz114-B31","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1038\/384368a0","article-title":"Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice","volume":"384","author":"Kuida","year":"1996","journal-title":"Nature"},{"key":"2024032523300381600_nlz114-B32","doi-asserted-by":"crossref","first-page":"2875","DOI":"10.1073\/pnas.040556597","article-title":"Caspase-3: A vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson\u2019s disease","volume":"97","author":"Hartmann","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2024032523300381600_nlz114-B33","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.brainres.2015.10.020","article-title":"Mechanisms of neurodegeneration after severe hypoxic-ischemic injury in the neonatal rat brain","volume":"1629","author":"Askalan","year":"2015","journal-title":"Brain Res"},{"key":"2024032523300381600_nlz114-B34","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1111\/j.1471-4159.2005.03639.x","article-title":"Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia","volume":"96","author":"Zhu","year":"2006","journal-title":"J Neurochem"},{"key":"2024032523300381600_nlz114-B35","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1007\/s10495-007-0754-4","article-title":"Pathological apoptosis in the developing brain","volume":"12","author":"Blomgren","year":"2007","journal-title":"Apoptosis"},{"key":"2024032523300381600_nlz114-B36","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1159\/000047087","article-title":"Caspase-3 activation after neonatal rat cerebral hypoxia-ischemia","volume":"79","author":"Wang","year":"2001","journal-title":"Biol Neonate"},{"key":"2024032523300381600_nlz114-B37","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.neuroscience.2004.03.062","article-title":"Pathogenesis of hippocampal neuronal death after hypoxia-ischemia changes during brain development","volume":"127","author":"Liu","year":"2004","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B38","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/j.nbd.2007.06.009","article-title":"Extended role of necrotic cell death after hypoxia-ischemia-induced neurodegeneration in the neonatal rat","volume":"27","author":"Carloni","year":"2007","journal-title":"Neurobiol Dis"},{"key":"2024032523300381600_nlz114-B39","doi-asserted-by":"crossref","first-page":"7994","DOI":"10.1523\/JNEUROSCI.20-21-07994.2000","article-title":"Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat","volume":"20","author":"Nakajima","year":"2000","journal-title":"J Neurosci"},{"key":"2024032523300381600_nlz114-B40","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1046\/j.1471-4159.2000.0750819.x","article-title":"Correlation between caspase-3 activation and three different markers of DNA damage in neonatal cerebral hypoxia-ischemia","volume":"75","author":"Zhu","year":"2002","journal-title":"J Neurochem"},{"key":"2024032523300381600_nlz114-B41","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1111\/j.1440-1789.2011.01279.x","article-title":"Matrix metalloproteinase-9 expression in the nuclear compartment of neurons and glial cells in aging and stroke","volume":"32","author":"Pirici","year":"2012","journal-title":"Neuropathology"},{"key":"2024032523300381600_nlz114-B42","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1002\/pd.458","article-title":"Ivemark syndrome with agenesis of the corpus callosum: A case report with a review of the literature","volume":"22","author":"Noack","year":"2002","journal-title":"Prenat Diagn"},{"key":"2024032523300381600_nlz114-B43","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1006\/exnr.2000.7489","article-title":"Increased caspase 3 and Bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson\u2019s disease","volume":"166","author":"Tatton","year":"2000","journal-title":"Exp Neurol"},{"key":"2024032523300381600_nlz114-B44","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1038\/nature09788","article-title":"Caspase signalling controls microglia activation and neurotoxicity","volume":"472","author":"Burguillos","year":"2011","journal-title":"Nature"},{"key":"2024032523300381600_nlz114-B45","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1111\/j.1440-1789.2011.01267.x","article-title":"Immunohistochemical analysis of Marinesco bodies, using antibodies against proteins implicated in the ubiquitin-proteasome system, autophagy and aggresome formation","volume":"32","author":"Odagiri","year":"2012","journal-title":"Neuropathology"},{"key":"2024032523300381600_nlz114-B46","doi-asserted-by":"crossref","first-page":"10191","DOI":"10.1074\/jbc.M007807200","article-title":"Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: A mechanism of \u201cpathological apoptosis\u201d?","volume":"276","author":"Blomgren","year":"2001","journal-title":"J Biol Chem"},{"key":"2024032523300381600_nlz114-B47","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1097\/00004647-200009000-00003","article-title":"Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation","volume":"20","author":"Hu","year":"2000","journal-title":"J Cereb Blood Flow Metab"},{"key":"2024032523300381600_nlz114-B48","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1038\/sj.cdd.4401545","article-title":"The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia","volume":"12","author":"Zhu","year":"2005","journal-title":"Cell Death Differ"},{"key":"2024032523300381600_nlz114-B49","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1006\/mcne.1993.1004","article-title":"Naturally occurring cell death during postnatal development of the substantia nigra pars compacta of rat","volume":"4","author":"Janec","year":"1993","journal-title":"Mol Cell Neurosci"},{"key":"2024032523300381600_nlz114-B50","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/S0165-3806(96)00173-3","article-title":"The time course of developmental cell death in phenotypically defined dopaminergic neurons of the substantia nigra","volume":"98","author":"Oo","year":"1997","journal-title":"Brain Res Dev Brain Res"},{"key":"2024032523300381600_nlz114-B51","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/0306-4522(94)90258-5","article-title":"Postnatal changes in the distribution and morphology of rat substantia nigra dopaminergic neurons","volume":"60","author":"Tepper","year":"1994","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B52","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neuroscience.2010.11.037","article-title":"Maternal separation affects the number, proliferation and apoptosis of glia cells in the substantia nigra and ventral tegmental area of juvenile rats","volume":"173","author":"Chocyk","year":"2011","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B53","doi-asserted-by":"crossref","first-page":"14108","DOI":"10.1073\/pnas.0804650106","article-title":"Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat","volume":"106","author":"Bandeira","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2024032523300381600_nlz114-B54","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1002\/(SICI)1097-0029(19990701)46:1<24::AID-JEMT3>3.0.CO;2-E","article-title":"Distribution of the catecholaminergic neurons in the central nervous system of human embryos and fetuses","volume":"46","author":"Verney","year":"1999","journal-title":"Microsc Res Tech"},{"key":"2024032523300381600_nlz114-B55","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1007\/PL00005670","article-title":"Delayed neuronal death following perinatal asphyxia in rat","volume":"115","author":"Dell\u2019Anna","year":"1997","journal-title":"Exp Brain Res"},{"key":"2024032523300381600_nlz114-B56","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1002\/1098-2795(200010)57:2<153::AID-MRD6>3.0.CO;2-7","article-title":"Effect of hypoxia on DNA fragmentation in different brain regions of the newborn piglet","volume":"57","author":"David","year":"2000","journal-title":"Mol Reprod Dev"},{"key":"2024032523300381600_nlz114-B57","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.neuroscience.2014.08.054","article-title":"Neonatal anoxia in rats: Hippocampal cellular and subcellular changes related to cell death and spatial memory","volume":"284","author":"Takada","year":"2015","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B58","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.neulet.2013.11.019","article-title":"Apoptosis-related proteins are potential markers of neonatal hypoxic-ischemic encephalopathy (HIE) injury","volume":"558","author":"Hernandez-Jimenez","year":"2014","journal-title":"Neurosci Lett"},{"key":"2024032523300381600_nlz114-B59","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1111\/j.1365-2990.1997.tb01300.x","article-title":"Cell death in perinatal hypoxic-ischaemic brain injury","volume":"23","author":"Scott","year":"1997","journal-title":"Neuropathol Appl Neurobiol"},{"key":"2024032523300381600_nlz114-B60","doi-asserted-by":"crossref","first-page":"1916","DOI":"10.1161\/01.STR.30.9.1916","article-title":"Inflammatory responses in the cerebral cortex after ischemia in the P7 neonatal Rat","volume":"30","author":"Benjelloun","year":"1999","journal-title":"Stroke"},{"key":"2024032523300381600_nlz114-B61","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.expneurol.2005.10.015","article-title":"Inflammatory responses of the substantia nigra after acute hypoxia in neonatal rats","volume":"197","author":"Ezquer","year":"2006","journal-title":"Exp Neurol"},{"key":"2024032523300381600_nlz114-B62","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/S0197-4580(00)00126-3","article-title":"Morphological and biochemical assessment of DNA damage and apoptosis in Down syndrome and Alzheimer disease, and effect of postmortem tissue archival on TUNEL","volume":"21","author":"Anderson","year":"2000","journal-title":"Neurobiol Aging"},{"key":"2024032523300381600_nlz114-B63","doi-asserted-by":"crossref","first-page":"1710","DOI":"10.1523\/JNEUROSCI.16-05-01710.1996","article-title":"DNA damage and apoptosis in Alzheimer\u2019s disease: Colocalization with c-Jun immunoreactivity, relationship to brain area, and effect of postmortem delay","volume":"16","author":"Anderson","year":"1996","journal-title":"J Neurosci"},{"key":"2024032523300381600_nlz114-B64","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s004010051051","article-title":"Neuronal and glial DNA fragmentation in Pick\u2019s disease","volume":"98","author":"Gleckman","year":"1999","journal-title":"Acta Neuropathol"},{"key":"2024032523300381600_nlz114-B65","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1177\/43.11.7560899","article-title":"Microwave-enhanced in situ end-labeling of fragmented DNA: Parametric studies in relation to postmortem delay and fixation of rat and human brain","volume":"43","author":"Lucassen","year":"1995","journal-title":"J Histochem Cytochem"},{"key":"2024032523300381600_nlz114-B66","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1007\/s00401-004-0957-5","article-title":"Expression pattern of apoptosis-related markers in Huntington\u2019s disease","volume":"109","author":"Vis","year":"2005","journal-title":"Acta Neuropathol"},{"key":"2024032523300381600_nlz114-B67","first-page":"1465","article-title":"In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note","volume":"21","author":"Grasl-Kraupp","year":"1995","journal-title":"Hepatology"},{"key":"2024032523300381600_nlz114-B68","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1177\/002215549804600306","article-title":"TUNEL apoptotic cell detection in tissue sections: Critical evaluation and improvement","volume":"46","author":"Labat-Moleur","year":"1998","journal-title":"J Histochem Cytochem"},{"key":"2024032523300381600_nlz114-B69","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0304-3940(97)00445-X","article-title":"Identification of necrotic cell death by the TUNEL assay in the hypoxic-ischemic neonatal rat brain","volume":"230","author":"de Torres","year":"1997","journal-title":"Neurosci Lett"},{"key":"2024032523300381600_nlz114-B70","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1097\/00005072-199511000-00002","article-title":"Effect of postmortem interval on in situ end-labeling of DNA oligonucleosomes","volume":"54","author":"Petito","year":"1995","journal-title":"J Neuropathol Exp Neurol"},{"key":"2024032523300381600_nlz114-B71","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1002\/mds.870130604","article-title":"DNA fragmentation in human substantia nigra: Apoptosis or perimortem effect?","volume":"13","author":"Kingsbury","year":"1998","journal-title":"Mov Disord"},{"key":"2024032523300381600_nlz114-B72","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.neuroscience.2015.01.027","article-title":"Immunocytochemical localization of DNA double-strand breaks in human and rat brains","volume":"290","author":"Torres","year":"2015","journal-title":"Neuroscience"},{"key":"2024032523300381600_nlz114-B73","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1126\/science.1072221","article-title":"Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor","volume":"297","author":"Yu","year":"2002","journal-title":"Science"},{"key":"2024032523300381600_nlz114-B74","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1002\/bies.20085","article-title":"The PARP superfamily","volume":"26","author":"Ame","year":"2004","journal-title":"BioEssays"},{"key":"2024032523300381600_nlz114-B75","doi-asserted-by":"crossref","first-page":"e3208","DOI":"10.1371\/journal.pone.0003208","article-title":"The variability of the harlequin mouse phenotype resembles that of human mitochondrial-complex I-deficiency syndromes","volume":"3","author":"Benit","year":"2008","journal-title":"PLoS One"},{"key":"2024032523300381600_nlz114-B76","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.redox.2017.02.014","article-title":"Oxidative stress and apoptosis after acute respiratory hypoxia and reoxygenation in rat brain","volume":"12","author":"Coimbra-Costa","year":"2017","journal-title":"Redox Biol"},{"key":"2024032523300381600_nlz114-B77","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.clp.2018.01.015","article-title":"Perinatal brain injury: Mechanisms, prevention, and outcomes","volume":"45","author":"Novak","year":"2018","journal-title":"Clin Perinatol"},{"key":"2024032523300381600_nlz114-B78","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1097\/01.gco.0000192999.12416.95","article-title":"Infection and fetal neurologic injury","volume":"18","author":"Ugwumadu","year":"2006","journal-title":"Curr Opin Obstet Gynecol"},{"key":"2024032523300381600_nlz114-B79","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.ijdevneu.2013.06.008","article-title":"Effect of intrauterine infection on brain development and injury","volume":"31","author":"Zhao","year":"2013","journal-title":"Int J Dev Neurosci"},{"key":"2024032523300381600_nlz114-B80","doi-asserted-by":"crossref","first-page":"4727","DOI":"10.1242\/jcs.00210","article-title":"Apoptosis-inducing factor (AIF): Key to the conserved caspase-independent pathways of cell death?","volume":"115","author":"Cande","year":"2002","journal-title":"J Cell Sci"},{"key":"2024032523300381600_nlz114-B81","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/S1474-4422(03)00503-9","article-title":"The brain in diabetes: Molecular changes in neurons and their implications for end-organ damage","volume":"2","author":"Klein","year":"2003","journal-title":"Lancet Neurol"},{"key":"2024032523300381600_nlz114-B82","doi-asserted-by":"crossref","first-page":"10262","DOI":"10.1523\/JNEUROSCI.2818-05.2005","article-title":"Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia","volume":"25","author":"Culmsee","year":"2005","journal-title":"J Neurosci"},{"key":"2024032523300381600_nlz114-B83","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.2353\/ajpath.2008.080168","article-title":"Causal role of apoptosis-inducing factor for neuronal cell death following traumatic brain injury","volume":"173","author":"Slemmer","year":"2008","journal-title":"Am J Pathol"},{"key":"2024032523300381600_nlz114-B84","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neulet.2011.05.016","article-title":"Role of apoptosis inducing factor (AIF) for hippocampal neuronal cell death following global cerebral ischemia in mice","volume":"499","author":"Thal","year":"2011","journal-title":"Neurosci Lett"},{"key":"2024032523300381600_nlz114-B85","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.nbd.2010.09.005","article-title":"Apoptosis-inducing factor mediates dopaminergic cell death in response to LPS-induced inflammatory stimulus: Evidence in Parkinson\u2019s disease patients","volume":"41","author":"Burguillos","year":"2011","journal-title":"Neurobiol Dis"},{"key":"2024032523300381600_nlz114-B86","doi-asserted-by":"crossref","first-page":"1694","DOI":"10.1002\/jnr.21294","article-title":"Role of nitric oxide in the brain during lipopolysaccharide-evoked systemic inflammation","volume":"85","author":"Czapski","year":"2007","journal-title":"J Neurosci Res"},{"key":"2024032523300381600_nlz114-B87","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1002\/mds.26695","article-title":"Apoptosis-inducing factor in nigral dopamine neurons: Higher levels in primates than in mice","volume":"31","author":"Peneder","year":"2016","journal-title":"Mov Disord"},{"key":"2024032523300381600_nlz114-B88","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1038\/sj.cdd.4402053","article-title":"Apoptosis-inducing factor is a major contributor to neuronal loss induced by neonatal cerebral hypoxia-ischemia","volume":"14","author":"Zhu","year":"2007","journal-title":"Cell Death Differ"},{"key":"2024032523300381600_nlz114-B89","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1016\/j.nucmedbio.2011.05.001","article-title":"Effects of hypoxic-ischemic brain injury on striatal dopamine transporter in newborn piglets: Evaluation of 11C-CFT PET\/CT for DAT quantification","volume":"38","author":"Zhang","year":"2011","journal-title":"Nucl Med Biol"},{"key":"2024032523300381600_nlz114-B90","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1046\/j.1471-4159.2003.01832.x","article-title":"Involvement of apoptosis-inducing factor in neuronal death after hypoxia-ischemia in the neonatal rat brain","volume":"86","author":"Zhu","year":"2004","journal-title":"J Neurochem"},{"key":"2024032523300381600_nlz114-B91","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1097\/00004647-200404000-00011","article-title":"Nuclear translocation of apoptosis-inducing factor after focal cerebral ischemia","volume":"24","author":"Plesnila","year":"2004","journal-title":"J Cereb Blood Flow Metab"},{"key":"2024032523300381600_nlz114-B92","doi-asserted-by":"crossref","first-page":"29362","DOI":"10.1038\/srep29362","article-title":"RIP3 induces ischemic neuronal DNA degradation and programmed necrosis in rat via AIF","volume":"6","author":"Xu","year":"2016","journal-title":"Sci Rep"},{"key":"2024032523300381600_nlz114-B93","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1038\/17135","article-title":"Molecular characterization of mitochondrial apoptosis-inducing factor","volume":"397","author":"Susin","year":"1999","journal-title":"Nature"},{"key":"2024032523300381600_nlz114-B94","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1096\/fasebj.14.5.729","article-title":"Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis","volume":"14","author":"Daugas","year":"2000","journal-title":"FASEB J"},{"key":"2024032523300381600_nlz114-B95","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1038\/cdd.2009.112","article-title":"Alteration of the nuclear pore complex in Ca(2+)-mediated cell death","volume":"17","author":"Bano","year":"2010","journal-title":"Cell Death Differ"},{"key":"2024032523300381600_nlz114-B96","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1084\/jem.185.8.1481","article-title":"Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis","volume":"185","author":"Leist","year":"1997","journal-title":"J Exp Med"},{"key":"2024032523300381600_nlz114-B97","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1097\/WNR.0b013e32801b3ca6","article-title":"Rotenone and MPP+ preferentially redistribute apoptosis-inducing factor in apoptotic dopamine neurons","volume":"18","author":"Lim","year":"2007","journal-title":"NeuroReport"},{"key":"2024032523300381600_nlz114-B98","doi-asserted-by":"crossref","first-page":"e25346","DOI":"10.1371\/journal.pone.0025346","article-title":"Dissociation of progressive dopaminergic neuronal death and behavioral impairments by Bax deletion in a mouse model of Parkinson\u2019s diseases","volume":"6","author":"Kim","year":"2011","journal-title":"PLoS One"},{"key":"2024032523300381600_nlz114-B99","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1111\/j.1749-6632.2003.tb07471.x","article-title":"Apoptosis inducing factor and PARP-mediated injury in the MPTP mouse model of Parkinson\u2019s disease","volume":"991","author":"Wang","year":"2006","journal-title":"Ann N Y Acad Sci"},{"key":"2024032523300381600_nlz114-B100","first-page":"338","volume-title":"The Human Nervous System","author":"Horn","year":"2012","edition":"3rd ed"},{"key":"2024032523300381600_nlz114-B101","doi-asserted-by":"crossref","first-page":"e0175301","DOI":"10.1371\/journal.pone.0175301","article-title":"Effect of hypoxia on the retina and superior colliculus of neonatal pigs","volume":"12","author":"Ruzafa","year":"2017","journal-title":"PLoS One"},{"key":"2024032523300381600_nlz114-B102","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1002\/cne.21598","article-title":"Perioculomotor cell groups in monkey and man defined by their histochemical and functional properties: Reappraisal of the Edinger-Westphal nucleus","volume":"507","author":"Horn","year":"2008","journal-title":"J Comp Neurol"},{"key":"2024032523300381600_nlz114-B103","first-page":"273","article-title":"Copper\/zinc superoxide dismutase expression in the human central nervous system. Correlation with selective neuronal vulnerability","volume":"148","author":"Bergeron","year":"1996","journal-title":"Am J Pathol"},{"key":"2024032523300381600_nlz114-B104","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/j.foodchem.2018.06.032","article-title":"Study on the apoptosis mediated by apoptosis-inducing-factor and influencing factors of bovine muscle during postmortem aging","volume":"266","author":"Zhang","year":"2018","journal-title":"Food Chem"},{"key":"2024032523300381600_nlz114-B105","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1002\/cne.900800105","article-title":"The oculomotor nucleus in the human fetus","volume":"80","author":"Pearson","year":"1944","journal-title":"J Comp Neurol"},{"key":"2024032523300381600_nlz114-B106","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/j.aanat.2014.07.006","article-title":"Development of the human oculomotor nuclear complex: Somatic nuclei","volume":"196","author":"Yamaguchi","year":"2014","journal-title":"Ann Anat"},{"key":"2024032523300381600_nlz114-B107","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/0887-8994(86)90003-2","article-title":"Cortical visual impairment following birth asphyxia","volume":"2","author":"Roland","year":"1986","journal-title":"Pediatr Neurol"},{"key":"2024032523300381600_nlz114-B108","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1111\/j.1469-8749.2002.tb00327.x","article-title":"Oculomotor dysfunction in cerebral visual impairment following perinatal hypoxia","volume":"44","author":"Salati","year":"2007","journal-title":"Dev Med Child Neurol"},{"key":"2024032523300381600_nlz114-B109","first-page":"1350","article-title":"Neurologic symptoms and syndromes in the diagnosis of perinatal brain lesions in newborn children","volume":"79","author":"Tastanbekov","year":"1979","journal-title":"Zh Nevropatol Psikhiatr Im S S Korsakova"},{"key":"2024032523300381600_nlz114-B110","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1097\/WCO.0000000000000274","article-title":"Eye movements in neurodegenerative diseases","volume":"29","author":"MacAskill","year":"2016","journal-title":"Curr Opin Neurol"},{"key":"2024032523300381600_nlz114-B111","doi-asserted-by":"crossref","first-page":"1393","DOI":"10.2147\/NDT.S45931","article-title":"Saccadic eye movement applications for psychiatric disorders","volume":"9","author":"Bittencourt","year":"2013","journal-title":"Neuropsychiatr Dis Treat"}],"container-title":["Journal of Neuropathology &amp; Experimental Neurology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jnen\/article-pdf\/79\/1\/86\/31495728\/nlz114.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jnen\/article-pdf\/79\/1\/86\/31495728\/nlz114.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,25]],"date-time":"2024-03-25T23:41:03Z","timestamp":1711410063000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jnen\/article\/79\/1\/86\/5653101"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,10]]},"references-count":111,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12,10]]},"published-print":{"date-parts":[[2020,1,1]]}},"URL":"https:\/\/doi.org\/10.1093\/jnen\/nlz114","relation":{},"ISSN":["0022-3069","1554-6578"],"issn-type":[{"type":"print","value":"0022-3069"},{"type":"electronic","value":"1554-6578"}],"subject":[],"published-other":{"date-parts":[[2020,1]]},"published":{"date-parts":[[2019,12,10]]}}}