{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T02:01:38Z","timestamp":1788314498318,"version":"build-2803163510"},"reference-count":66,"publisher":"MDPI AG","issue":"17","license":[{"start":{"date-parts":[[2023,8,29]],"date-time":"2023-08-29T00:00:00Z","timestamp":1693267200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100009347","name":"INPRFM","doi-asserted-by":"publisher","award":["2000"],"award-info":[{"award-number":["2000"]}],"id":[{"id":"10.13039\/501100009347","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Melatonin is a hormone synthesized by the pineal gland with neuroprotective and neurodevelopmental effects. Also, melatonin acts as an antidepressant by modulating the generation of new neurons in the dentate gyrus of the hippocampus. The positive effects of melatonin on behavior and neural development may suggest it is used for reverting stress but also for the alterations produced by chemotherapeutic drugs influencing behavior and brain plasticity. In this sense, temozolomide, an alkylating\/anti-proliferating agent used in treating brain cancer, is associated with decreased cognitive functions and depression. We hypothesized that melatonin might prevent the effects of temozolomide on depression- and anxiety-like behavior by modulating some aspects of the neurogenic process in adult Balb\/C mice. Mice were treated with temozolomide (25 mg\/kg) for three days of two weeks, followed by melatonin (8 mg\/kg) for fourteen days. Temozolomide produced short- and long-term decrements in cell proliferation (Ki67-positive cells: 54.89% and 53.38%, respectively) and intermediate stages of the neurogenic process (doublecortin-positive cells: 68.23% and 50.08%, respectively). However, melatonin prevented the long-term effects of temozolomide with the increased number of doublecortin-positive cells (47.21%) and the immunoreactivity of 2\u2032 3\u2032-Cyclic-nucleotide-3 phosphodiesterase (CNPase: 82.66%), an enzyme expressed by mature oligodendrocytes, in the hilar portion of the dentate gyrus. The effects of melatonin in the temozolomide group occurred with decreased immobility in the forced swim test (45.55%) but not anxiety-like behavior. Thus, our results suggest that melatonin prevents the harmful effects of temozolomide by modulating doublecortin cells, hilar oligodendrocytes, and depression-like behavior tested in the forced swim test. Our study could point out melatonin\u2019s beneficial effects for counteracting temozolomide\u2019s side effects.<\/jats:p>","DOI":"10.3390\/ijms241713376","type":"journal-article","created":{"date-parts":[[2023,8,29]],"date-time":"2023-08-29T08:26:52Z","timestamp":1693297612000},"page":"13376","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Melatonin Prevents Depression but Not Anxiety-like Behavior Produced by the Chemotherapeutic Agent Temozolomide: Implication of Doublecortin Cells and Hilar Oligodendrocytes"],"prefix":"10.3390","volume":"24","author":[{"given":"Edith Araceli","family":"Cabrera-Mu\u00f1oz","sequence":"first","affiliation":[{"name":"Laboratorio de Neurog\u00e9nesis, Subdirecci\u00f3n de Investigaciones Cl\u00ednicas, Instituto Nacional de Psiquiatr\u00eda \u201cRam\u00f3n de la Fuente Mu\u00f1iz\u201d, Calzada Mexico-Xochimilco 101, Ciudad de M\u00e9xico 14370, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3243-1588","authenticated-orcid":false,"given":"Gerardo Bernab\u00e9","family":"Ram\u00edrez-Rodr\u00edguez","sequence":"additional","affiliation":[{"name":"Laboratorio de Neurog\u00e9nesis, Subdirecci\u00f3n de Investigaciones Cl\u00ednicas, Instituto Nacional de Psiquiatr\u00eda \u201cRam\u00f3n de la Fuente Mu\u00f1iz\u201d, Calzada Mexico-Xochimilco 101, Ciudad de M\u00e9xico 14370, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lizeth","family":"D\u00edaz-Ya\u00f1ez","sequence":"additional","affiliation":[{"name":"Laboratorio de Neurog\u00e9nesis, Subdirecci\u00f3n de Investigaciones Cl\u00ednicas, Instituto Nacional de Psiquiatr\u00eda \u201cRam\u00f3n de la Fuente Mu\u00f1iz\u201d, Calzada Mexico-Xochimilco 101, Ciudad de M\u00e9xico 14370, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ver\u00f3nica","family":"Reyes-Galindo","sequence":"additional","affiliation":[{"name":"Instituto de Ecolog\u00eda, Universidad Nacional Aut\u00f3noma de M\u00e9xico, Circuito Exterior sin N\u00famero, Ciudad Universitaria, Ciudad de M\u00e9xico 04510, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Meneses-San Juan","sequence":"additional","affiliation":[{"name":"Laboratorio de Neurog\u00e9nesis, Subdirecci\u00f3n de Investigaciones Cl\u00ednicas, Instituto Nacional de Psiquiatr\u00eda \u201cRam\u00f3n de la Fuente Mu\u00f1iz\u201d, Calzada Mexico-Xochimilco 101, Ciudad de M\u00e9xico 14370, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nelly Maritza","family":"Vega-Rivera","sequence":"additional","affiliation":[{"name":"Laboratorio de Neurpsicofarmacolog\u00eda, Direcci\u00f3n de Neurociencias, Instituto Nacional de Psiquiatr\u00eda \u201cRam\u00f3n de la Fuente Mu\u00f1iz\u201d, Calzada Mexico-Xochimilco 101, Ciudad de M\u00e9xico 14370, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2051","DOI":"10.1200\/JCO.2009.26.5520","article-title":"Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study","volume":"28","author":"Perry","year":"2010","journal-title":"J. Clin. Oncol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.1158\/1078-0432.CCR-14-2737","article-title":"MGMT Promoter Methylation Is a Strong Prognostic Biomarker for Benefit from Dose-Intensified Temozolomide Rechallenge in Progressive Glioblastoma: The DIRECTOR Trial","volume":"21","author":"Weller","year":"2015","journal-title":"Clin. Cancer Res."},{"key":"ref_3","unstructured":"(2022, July 03). Available online: https:\/\/gco.iarc.fr\/today\/fact-sheets-cancers."},{"key":"ref_4","unstructured":"(2022, July 03). Available online: https:\/\/www.cancer.net\/cancer-types\/brain-tumor\/types-treatment."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"n1560","DOI":"10.1136\/bmj.n1560","article-title":"Glioblastoma: Clinical presentation, diagnosis, and management","volume":"374","author":"McKinnon","year":"2021","journal-title":"BMJ"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1186\/s13293-021-00372-5","article-title":"Impact of sex in the prevalence and progression of glioblastomas: The role of gonadal steroid hormones","volume":"12","year":"2021","journal-title":"Biol. Sex Differ."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e1241","DOI":"10.1002\/cnr2.1241","article-title":"Sex steroid hormone function in the brain niche: Implications for brain metastatic colonization and progression","volume":"5","author":"Cittelly","year":"2022","journal-title":"Cancer Rep."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e1101","DOI":"10.1038\/tp.2017.68","article-title":"Depletion of adult neurogenesis using the chemotherapy drug temozolomide in mice induces behavioural and biological changes relevant to depression","volume":"7","author":"Egeland","year":"2017","journal-title":"Transl. Psychiatry"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Leung, J.W.-H., Cheung, K.-K., Ngai, S.P.-C., Tsang, H.W.-H., and Lau, B.W.-M. (2020). Protective Effects of Melatonin on Neurogenesis Impairment in Neurological Disorders and Its Relevant Molecular Mechanisms. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21165645"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/j.neuropharm.2015.11.030","article-title":"Chronic administration of a melatonin membrane receptor antagonist, luzindole, affects hippocampal neurogenesis without changes in hopelessness-like behavior in adult mice","volume":"103","year":"2016","journal-title":"Neuropharmacology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.neuro.2016.09.002","article-title":"Melatonin protects against oxygen and glucose deprivation by decreasing extracellular glutamate and Nox-derived ROS in rat hippocampal slices","volume":"57","author":"Parada","year":"2016","journal-title":"Neurotoxicology"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Olivier, P., Fontaine, R.H., Loron, G., Van Steenwinckel, J., Biran, V., Massonneau, V., Kaindl, A., Dalous, J., Charriaut-Marlangue, C., and Aigrot, M.S. (2009). Melatonin Promotes Oligodendroglial Maturation of Injured White Matter in Neonatal Rats. PLoS ONE, 4.","DOI":"10.1371\/annotation\/d6a43156-441c-4dac-ab10-ee85b6215b1e"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1254\/jphs.13R01SR","article-title":"Effects of melatonin on nervous system aging: Neurogenesis and neurodegeneration","volume":"123","author":"Sarlak","year":"2013","journal-title":"J. Pharmacol. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Ram\u00edrez-Rodr\u00edguez, G.B., Olvera-Hern\u00e1ndez, S., Vega-Rivera, N.M., and Ortiz-L\u00f3pez, L. (2018). Melatonin Influences Structural Plasticity in the Axons of Granule Cells in the Dentate Gyrus of Balb\/C Mice. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20010073"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.neuroscience.2020.05.014","article-title":"Melatonin Reverses the Depression-associated Behaviour and Regulates Microglia, Fractalkine Expression and Neurogenesis in Adult Mice Exposed to Chronic Mild Stress","volume":"440","year":"2020","journal-title":"Neuroscience"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.neulet.2012.09.045","article-title":"Melatonin supplementation delays the decline of adult hippocampal neurogenesis during normal aging of mice","volume":"530","year":"2012","journal-title":"Neurosci. Lett."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3521","DOI":"10.1111\/ejn.12007","article-title":"Chemotherapy disrupts learning, neurogenesis and theta activity in the adult brain","volume":"36","author":"Nokia","year":"2012","journal-title":"Eur. J. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Sekeres, M.J., Bradley-Garcia, M., Martinez-Canabal, A., and Winocur, G. (2021). Chemotherapy-Induced Cognitive Impairment and Hippocampal Neurogenesis: A Review of Physiological Mechanisms and Interventions. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222312697"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.comppsych.2016.03.005","article-title":"Differential melatonin alterations in cerebrospinal fluid and serum of patients with major depressive disorder and bipolar disorder","volume":"68","author":"Bumb","year":"2016","journal-title":"Compr. Psychiatry"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1007\/s12264-017-0189-z","article-title":"Melatonin Augments the Effects of Fluoxetine on Depression-Like Behavior and Hippocampal BDNF-TrkB Signaling","volume":"34","author":"Li","year":"2018","journal-title":"Neurosci. Bull."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Hardeland, R. (2021). Melatonin and Microglia. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22158296"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1203\/PDR.0b013e3181fcb40b","article-title":"Melatonin Promotes Myelination by Decreasing White Matter Inflammation after Neonatal Stroke","volume":"69","author":"Villapol","year":"2011","journal-title":"Pediatr. Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Parkitny, L., and Maletic-Savatic, M. (2021). Glial PAMPering and DAMPening of Adult Hippocampal Neurogenesis. Brain Sci., 11.","DOI":"10.3390\/brainsci11101299"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"107","DOI":"10.3389\/fnins.2011.00106","article-title":"Adult hippocampal neurogenesis and plasticity in the infrapyramidal bundle of the mossy fiber projection: I. Co-regulation by activity","volume":"5","author":"Krebs","year":"2011","journal-title":"Front. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"16662","DOI":"10.1074\/jbc.M200415200","article-title":"CalbindinD28k exhibits properties characteristic of a Ca2+ sensor","volume":"277","author":"Miron","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1093\/neuonc\/noaa106","article-title":"Glioblastoma in adults: A Society for Neuro-Oncology (SNO) and European Society of Neuro-Oncology (EANO) consensus review on current management and future directions","volume":"22","author":"Wen","year":"2020","journal-title":"Neuro-Oncology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2813","DOI":"10.1111\/ejn.15139","article-title":"Forced swim stressor: Trends in usage and mechanistic consideration","volume":"55","author":"Molendijk","year":"2022","journal-title":"Eur. J. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2180","DOI":"10.1038\/npp.2009.46","article-title":"Melatonin modulates cell survival of new neurons in the hippocampus of adult mice","volume":"34","author":"Klempin","year":"2009","journal-title":"Neuropsychopharmacology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1038\/aps.2010.80","article-title":"Antidepressant- and anxiolytic effects of the novel melatonin agonist Neu-P11 in rodent models","volume":"31","author":"Tian","year":"2010","journal-title":"Acta Pharmacol. Sin."},{"key":"ref_30","first-page":"e2609","article-title":"Measuring motor coordination in mice","volume":"75","author":"Deacon","year":"2013","journal-title":"J. Vis. Exp."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-1-60761-303-9_1","article-title":"The Open Field Test. In Mood and Anxiety Related Phenotypes in Mice","volume":"Volume 42","author":"Gould","year":"2009","journal-title":"Neuromethods"},{"key":"ref_32","first-page":"e1088","article-title":"Elevated plus maze for mice","volume":"22","author":"Komada","year":"2008","journal-title":"J. Vis. Exp."},{"key":"ref_33","first-page":"e52434","article-title":"Use of the Open Field Maze to measure locomotor and anxiety-like behavior in mice","volume":"96","author":"Seibenhener","year":"2015","journal-title":"J. Vis. Exp."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/0014-2999(93)90273-K","article-title":"Melatonin as an anxiolytic in rats: Time dependence and interaction with the central GABAergic system","volume":"237","author":"Golombek","year":"1993","journal-title":"Eur. J. Pharmacol."},{"key":"ref_35","first-page":"9","article-title":"Anxiolytic-like activity of agomelatine and melatonin in three animal models of anxiety","volume":"17","author":"Papp","year":"2006","journal-title":"Behav. Pharmacol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bbr.2019.02.005","article-title":"Coping with the forced swim stressor: Current state-of-the-art","volume":"364","author":"Molendijk","year":"2019","journal-title":"Behav. Brain Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1111\/jpi.12224","article-title":"Anatomical and cellular localization of melatonin MT1 and MT2 receptors in the adult rat brain","volume":"58","author":"Lacoste","year":"2015","journal-title":"J. Pineal Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"pyu075","DOI":"10.1093\/ijnp\/pyu075","article-title":"Melancholic-Like behaviors and circadian neurobiological abnormalities in melatonin MT1 receptor knockout mice","volume":"18","author":"Comai","year":"2015","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e12653","DOI":"10.1111\/jpi.12653","article-title":"Dysfunction of serotonergic activity and emotional responses across the light-dark cycle in mice lacking melatonin MT2 receptors","volume":"69","author":"Comai","year":"2020","journal-title":"J. Pineal Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/j.pnpbp.2012.07.003","article-title":"Anxiolytic effects of the melatonin MT2 receptor partial agonist UCM765: Comparison with melatonin and diazepam","volume":"39","author":"Rainer","year":"2012","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1038\/mp.2009.15","article-title":"Adult hippocampal neurogenesis is involved in anxiety-related behaviors","volume":"14","author":"Revest","year":"2009","journal-title":"Mol. Psychiatry"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.bbr.2014.01.012","article-title":"Hippocampal biomarkers of fear memory in an animal model of generalized anxiety disorder","volume":"263","author":"Dias","year":"2014","journal-title":"Behav. Brain Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e2227","DOI":"10.1002\/brb3.2227","article-title":"Melatonin salvages lead-induced neuro-cognitive shutdown, anxiety, and depressive-like symptoms via oxido-inflammatory and cholinergic mechanisms","volume":"11","author":"Omeiza","year":"2021","journal-title":"Brain Behav."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1613","DOI":"10.1038\/nn.3262","article-title":"Neurogenesis and generalization: A new approach to stratify and treat anxiety disorders","volume":"15","author":"Kheirbek","year":"2012","journal-title":"Nat. Neurosci."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Garthe, A., Behr, J., and Kempermann, G. (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0005464"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1111\/j.1600-079X.2010.00802.x","article-title":"Chronic treatment with melatonin stimulates dendrite maturation and complexity in adult hippocampal neurogenesis of mice","volume":"50","author":"Kempermann","year":"2011","journal-title":"J. Pineal Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/jpi.12248","article-title":"Melatonin attenuates impairments of structural hippocampal neuroplasticity in OXYS rats during active progression ofAlzheimer\u2019s disease-like pathology","volume":"59","author":"Stefanova","year":"2015","journal-title":"J. Pineal Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1007\/s10571-016-0450-4","article-title":"Melatonin Increases Oligodendrocyte Differentiation in Cultured Neural Stem Cells","volume":"37","author":"Ghareghani","year":"2017","journal-title":"Cell. Mol. Neurobiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/0306-4522(90)90139-U","article-title":"Hippocampal mossy fibers and radial-maze learning in the mouse: A correlation with spatial working memory but not with non-spatial reference memory","volume":"34","author":"Schwegler","year":"1990","journal-title":"Neuroscience"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1038\/nn.2156","article-title":"Neurons born in the adult dentate gyrus form functional synapses with target cells","volume":"11","author":"Toni","year":"2008","journal-title":"Nat. Neurosci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1016\/j.tcb.2009.08.006","article-title":"Control of neuronal polarity and plasticity\u2014A renaissance for microtubules?","volume":"19","author":"Hoogenraad","year":"2009","journal-title":"Trends Cell Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/0166-4328(87)90163-X","article-title":"Hippocampal mossy fiber distribution covaries with open-field habituation inthe mouse","volume":"26","author":"Crusio","year":"1987","journal-title":"Behav. Brain Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1007\/s12035-008-8049-5","article-title":"Targeting the hippocampal mossy fiber synapse for the treatment of psychiatric disorders","volume":"39","author":"Kobayashi","year":"2009","journal-title":"Mol. Neurobiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/cdd.2014.195","article-title":"The MT2 receptor stimulates axonogenesis and enhances synaptic transmission by activating Akt signaling","volume":"22","author":"Liu","year":"2015","journal-title":"Cell Death Differ."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.biomaterials.2018.08.046","article-title":"The role of oligodendrocytes and their progenitors on neural interface technology: A novel perspective on tissue regeneration and repair","volume":"183","author":"Wellman","year":"2018","journal-title":"Biomaterials"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1111\/j.1469-7580.2007.00729.x","article-title":"Morphological and physiological interactions of NG2-glia with astrocytes and neurons","volume":"210","author":"Wigley","year":"2007","journal-title":"J. Anat."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"134916","DOI":"10.1016\/j.neulet.2020.134916","article-title":"Neuron-oligodendroglia interactions: Activity-dependent regulation of cellular signaling","volume":"727","author":"Thornton","year":"2020","journal-title":"Neurosci. Lett."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1038\/s41380-020-00930-0","article-title":"Oligodendrocyte lineage cells and depression","volume":"26","author":"Zhou","year":"2021","journal-title":"Mol. Psychiatry"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"e12415","DOI":"10.1111\/jpi.12415","article-title":"Melatonin enhances neural stem cell differentiation and engraftment by increasing mitochondrial function","volume":"63","author":"Florido","year":"2017","journal-title":"J. Pineal Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3057","DOI":"10.1523\/JNEUROSCI.08-08-03057.1988","article-title":"Immunocytochemical localization by electron microscopy of 2\u20323\u2032-cyclic nucleotide 3\u2032-phosphodiesterase in developing oligodendrocytes of normal and mutant brain","volume":"8","author":"Braun","year":"1988","journal-title":"J. Neurosci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1363","DOI":"10.1016\/0896-6273(94)90451-0","article-title":"Differential regulation of the 20,30-cyclic nucleotide 30-phosphodiesterase gene during oligodendrocyte development","volume":"12","author":"Scherer","year":"1994","journal-title":"Neuron"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1007\/s11064-021-03487-8","article-title":"Environmental Enrichment Differentially Activates Neural Circuits in FVB\/N Mice, Inducing Social Interaction in Females but Agonistic Behavior in Males","volume":"47","year":"2022","journal-title":"Neurochem. Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.bbr.2008.04.021","article-title":"Mouse strain differences in the unpredictable chronic mild stress: A four-antidepressant survey","volume":"193","author":"Yalcin","year":"2008","journal-title":"Behav. Brain Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1038\/npp.2011.230","article-title":"The Neuropeptide Y (NPY)-ergic System is Associated with Behavioral Resilience to Stress Exposure in an Animal Model of Post-Traumatic Stress Disorder","volume":"37","author":"Cohen","year":"2012","journal-title":"Neuropsychopharmacology"},{"key":"ref_65","unstructured":"Alboukadel Kassambara and Fabian Mundt (2020) (2022, August 23). Factoextra: Extract and Visualize the Results of Multivariate Data Analyses. R package version 1.0.7. Available online: https:\/\/CRAN.R-project.org\/package=factoextra."},{"key":"ref_66","unstructured":"R Core Team (2021). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing. Available online: https:\/\/www.R-project.org\/."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/17\/13376\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:41:34Z","timestamp":1760128894000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/17\/13376"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,29]]},"references-count":66,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["ijms241713376"],"URL":"https:\/\/doi.org\/10.3390\/ijms241713376","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,29]]}}}