{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T07:59:30Z","timestamp":1777363170947,"version":"3.51.4"},"reference-count":61,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2023,6,7]],"date-time":"2023-06-07T00:00:00Z","timestamp":1686096000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Inserm","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"University of Lorraine","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"CHRU Nancy","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"FHU ARRIMAGE","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"French Agence Nationale de la Recherche","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"PIA project","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"Lorraine Universit\u00e9 d\u2019Excellence (LUE)","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"OMAGE","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"region GrandEST of France","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"FEDER","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"European Union","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]},{"name":"French Ministry of Higher Education","award":["ANR-15-IDEX-04-LUE"],"award-info":[{"award-number":["ANR-15-IDEX-04-LUE"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Vitamin B9 (folate)\/B12 (cobalamin) deficiency is known to induce brain structural and\/or functional retardations. In many countries, folate supplementation, targeting the most severe outcomes such as neural tube defects, is discontinued after the first trimester. However, adverse effects may occur after birth because of some mild misregulations. Various hormonal receptors were shown to be deregulated in brain tissue under these conditions. The glucocorticoid receptor (GR) is particularly sensitive to epigenetic regulation and post-translational modifications. In a mother\u2013offspring rat model of vitamin B9\/B12 deficiency, we investigated whether a prolonged folate supplementation could restore the GR signaling in the hypothalamus. Our data showed that a deficiency of folate and vitamin B12 during the in-utero and early postnatal periods was associated with reduced GR expression in the hypothalamus. We also described for the first time a novel post-translational modification of GR that impaired ligand binding and GR activation, leading to decrease expression of one of the GR targets in the hypothalamus, AgRP. Moreover, this brain-impaired GR signaling pathway was associated with behavioral perturbations during offspring growth. Importantly, perinatal and postnatal supplementation with folic acid helped restore GR mRNA levels and activity in hypothalamus cells and improved behavioral deficits.<\/jats:p>","DOI":"10.3390\/ijms24129847","type":"journal-article","created":{"date-parts":[[2023,6,7]],"date-time":"2023-06-07T03:04:49Z","timestamp":1686107089000},"page":"9847","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Folate and Cobalamin Deficiencies during Pregnancy Disrupt the Glucocorticoid Response in Hypothalamus through N-Homocysteinilation of the Glucocorticoid Receptor"],"prefix":"10.3390","volume":"24","author":[{"given":"Arnaud","family":"Michel","sequence":"first","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tunay","family":"Kokten","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7794-5975","authenticated-orcid":false,"given":"Lynda","family":"Saber-Cherif","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8591-0721","authenticated-orcid":false,"given":"R\u00e9my","family":"Umoret","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jean-Marc","family":"Alberto","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"D\u00e9borah","family":"Helle","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Am\u00e9lia","family":"Julien","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jean-Luc","family":"Daval","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5067-042X","authenticated-orcid":false,"given":"Jean-Louis","family":"Gu\u00e9ant","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"},{"name":"National Center of Inborn Errors of Metabolism, University Regional Hospital of Nancy, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Carine","family":"Bossenmeyer-Pouri\u00e9","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0452-5026","authenticated-orcid":false,"given":"Gr\u00e9gory","family":"Pouri\u00e9","sequence":"additional","affiliation":[{"name":"Inserm UMRS 1256 NGERE-Nutrition, Genetics, and Environmental Risk Exposure, University of Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,6,7]]},"reference":[{"key":"ref_1","first-page":"397","article-title":"The effects of maternal nutrition around the time of conception on the health of the offspring","volume":"64","author":"Oliver","year":"2007","journal-title":"Soc. Reprod. Fertil."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/j.biochi.2013.01.020","article-title":"Molecular and cellular effects of vitamin B12 in brain, myocardium and liver through its role as co-factor of methionine synthase","volume":"95","author":"Alberto","year":"2013","journal-title":"Biochimie"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1002\/jimd.12171","article-title":"Early neurodevelopmental characterization in children with cobalamin C\/defect","volume":"43","author":"Ricci","year":"2020","journal-title":"J. Inherit. Metab. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/S0166-2236(03)00032-8","article-title":"Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders","volume":"26","author":"Mattson","year":"2003","journal-title":"Trends Neurosci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"667","DOI":"10.2353\/ajpath.2007.060339","article-title":"Gestational vitamin B deficiency leads to homocysteine-associated brain apoptosis and alters neurobehavioral development in rats","volume":"170","author":"Blaise","year":"2007","journal-title":"Am. J. Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"12474","DOI":"10.1073\/pnas.0805350105","article-title":"B-vitamin deficiency causes hyperhomocysteinemia and vascular cognitive impairment in mice","volume":"105","author":"Troen","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_7","first-page":"106","article-title":"Vitamin B deficiency causes neural cell loss and cognitive impairment in the developing rat","volume":"6","author":"Daval","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1111\/gbb.12207","article-title":"Methyl-donor deficiency in adolescence affects memory and epigenetic status in the mouse hippocampus","volume":"14","author":"Tomizawa","year":"2015","journal-title":"Genes Brain Behav."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Geoffroy, A., Saber-Cherif, L., Pouri\u00e9, G., Helle, D., Umoret, R., Gu\u00e9ant, J.L., Bossenmeyer-Pouri\u00e9, C., and Daval, J.L. (2019). Developmental Impairments in a Rat Model of Methyl Donor Deficiency: Effects of a Late Maternal Supplementation with Folic Acid. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20040973"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3713","DOI":"10.1096\/fj.14-264267","article-title":"Folate- and vitamin B12-deficient diet during gestation and lactation alters cerebellar synapsin expression via impaired influence of estrogen nuclear receptor \u03b1","volume":"29","author":"Martin","year":"2015","journal-title":"FASEB J."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Hassan, Z., Coelho, D., Kokten, T., Alberto, J.M., Umoret, R., Daval, J.L., Gu\u00e9ant, J.L., Bossenmeyer-Pouri\u00e9, C., and Pouri\u00e9, G. (2019). Brain Susceptibility to Methyl Donor Deficiency: From Fetal Programming to Aging Outcome in Rats. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20225692"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"21930","DOI":"10.1073\/pnas.0811794106","article-title":"Vitamin B12 deficiency reduces proliferation and promotes differentiation of neuroblastoma cells and up-regulates PP2A, proNGF, and TACE","volume":"106","author":"Akchiche","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1002\/hipo.20690","article-title":"Differentiation and neural integration of hippocampal neuronal progenitors: Signaling pathways sequentially involved","volume":"20","author":"Akchiche","year":"2010","journal-title":"Hippocampus"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1515\/cclm-2012-0673","article-title":"Genetic defects in folate and cobalamin pathways affecting the brain","volume":"51","author":"Kirsch","year":"2013","journal-title":"Clin. Chem. Lab. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e755","DOI":"10.1038\/cddis.2013.278","article-title":"Early methyl donor deficiency may induce persistent brain defects by reducing Stat3 signaling targeted by miR-124","volume":"4","author":"Kerek","year":"2013","journal-title":"Cell Death Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1007\/s12035-018-1128-3","article-title":"Wnt Signaling Pathways Are Dysregulated in Rat Female Cerebellum Following Early Methyl Donor Deficiency","volume":"56","author":"Willekens","year":"2019","journal-title":"Mol. Neurobiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1309","DOI":"10.1111\/j.1471-4159.2009.06417.x","article-title":"Vitamin-regulated cytokines and growth factors in the CNS and elsewhere","volume":"111","author":"Scalabrino","year":"2009","journal-title":"J. Neurochem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"229","DOI":"10.5483\/BMBRep.2015.48.4.272","article-title":"Network of hypothalamic neurons that control appetite","volume":"48","author":"Sohn","year":"2015","journal-title":"BMB Rep."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1038\/nrn2647","article-title":"Neural regulation of endocrine and autonomic stress responses","volume":"10","author":"Herman","year":"2009","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"16065","DOI":"10.1038\/nrdp.2016.65","article-title":"Major depressive disorder","volume":"2","author":"Otte","year":"2016","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/mp.2016.120","article-title":"HPA axis in major depression: Cortisol, clinical symptomatology and genetic variation predict cognition","volume":"22","author":"Keller","year":"2017","journal-title":"Mol. Psychiatry"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1159\/000360508","article-title":"Developmental programming of appetite\/satiety","volume":"64","author":"Ross","year":"2014","journal-title":"Ann. Nutr. Metab."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.yfrne.2015.09.002","article-title":"Developmental programming of hypothalamic neuroendocrine systems","volume":"39","author":"Ralevski","year":"2015","journal-title":"Front. Neuroendocrinol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijdevneu.2017.04.001","article-title":"Prenatal stress and depression associated neuronal development in neonates","volume":"60","author":"Fatima","year":"2017","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1097\/GRF.0b013e31829e5b15","article-title":"Development and programming of the hypothalamus-pituitary-adrenal axis","volume":"56","author":"Wood","year":"2013","journal-title":"Clin. Obstet. Gynecol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"5017","DOI":"10.1007\/s12035-016-0035-8","article-title":"Late Maternal Folate Supplementation Rescues from Methyl Donor Deficiency-Associated Brain Defects by Restoring Let-7 and miR-34 Pathways","volume":"54","author":"Geoffroy","year":"2017","journal-title":"Mol. Neurobiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"601939","DOI":"10.3389\/fnbeh.2020.601939","article-title":"The Hypothalamic-Pituitary-Adrenal Axis: Development, Programming Actions of Hormones, and Maternal-Fetal Interactions","volume":"14","author":"Sheng","year":"2021","journal-title":"Front. Behav. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Saber Cherif, L., Pouri\u00e9, G., Geoffroy, A., Julien, A., Helle, D., Robert, A., Umoret, R., Gu\u00e9ant, J.L., Bossenmeyer-Pouri\u00e9, C., and Daval, J.L. (2019). Methyl Donor Deficiency during Gestation and Lactation in the Rat Affects the Expression of Neuropeptides and Related Receptors in the Hypothalamus. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20205097"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1159\/000362736","article-title":"Stress, the stress system and the role of glucocorticoids","volume":"22","author":"Nicolaides","year":"2015","journal-title":"Neuroimmunomodulation"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1002\/cphy.c150015","article-title":"Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response","volume":"6","author":"Herman","year":"2016","journal-title":"Compr. Physiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1111\/j.1749-6632.2012.06633.x","article-title":"Glucocorticoid regulation of inflammation and its functional correlates: From HPA axis to glucocorticoid receptor dysfunction","volume":"1261","author":"Silverman","year":"2012","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1080\/10253890.2018.1470238","article-title":"Role of glucocorticoid negative feedback in the regulation of HPA axis pulsatility","volume":"21","author":"Gjerstad","year":"2018","journal-title":"Stress"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4544","DOI":"10.1210\/en.2008-0229","article-title":"Glucocorticoids increase neuropeptide Y and agouti-related peptide gene expression via adenosine monophosphate-activated protein kinase signaling in the arcuate nucleus of rats","volume":"149","author":"Shimizu","year":"2008","journal-title":"Endocrinology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"5395","DOI":"10.1210\/en.2010-0681","article-title":"Corticosterone regulates synaptic input organization of POMC and NPY\/AgRP neurons in adult mice","volume":"151","author":"Gyengesi","year":"2010","journal-title":"Endocrinology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"139","DOI":"10.2152\/jmi.51.139","article-title":"Stress control and human nutrition","volume":"51","author":"Takeda","year":"2004","journal-title":"J. Med. Investig."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1210\/en.2008-1426","article-title":"Palatable foods, stress, and energy stores sculpt corticotropin-releasing factor, adrenocorticotropin, and corticosterone concentrations after restraint","volume":"150","author":"Foster","year":"2009","journal-title":"Endocrinology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1038\/nrm.2016.152","article-title":"Glucocorticoid receptor control of transcription: Precision and plasticity via allostery","volume":"18","author":"Weikum","year":"2017","journal-title":"Nat. Rev. Mol. Cell. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1016\/S1474-4422(06)70598-1","article-title":"Vitamin B12, folic acid, and the nervous system","volume":"5","author":"Reynolds","year":"2006","journal-title":"Lancet Neurol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.ymgme.2009.06.004","article-title":"Vitamin B(12) and birth defects","volume":"98","author":"Li","year":"2009","journal-title":"Mol. Genet. Metab."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Rubini, E., Baijens, I.M.M., Hor\u00e1nszky, A., Schoenmakers, S., Sinclair, K.D., Zana, M., Dinny\u00e9s, A., Steegers-Theunissen, R.P.M., and Rousian, M. (2021). Maternal One-Carbon Metabolism during the Periconceptional Period and Human Foetal Brain Growth: A Systematic Review. Genes, 12.","DOI":"10.3390\/genes12101634"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1017\/S0007114519001272","article-title":"The association of maternal dietary folate intake and folic acid supplementation with small-for-gestational-age births: A cross-sectional study in Northwest China","volume":"122","author":"Li","year":"2019","journal-title":"Br. J. Nutr."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/j.braindev.2015.10.008","article-title":"Activity-dependent synaptic plasticity modulates the critical phase of brain development","volume":"38","author":"Chaudhury","year":"2016","journal-title":"Brain Dev."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.pneurobio.2018.04.001","article-title":"Regulation and function of neurogenesis in the adult mammalian hypothalamus","volume":"170","author":"Yoo","year":"2018","journal-title":"Prog. Neurobiol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1038\/s41593-022-01065-x","article-title":"Hypothalamic modulation of adult hippocampal neurogenesis in mice confers activity-dependent regulation of memory and anxiety-like behavior","volume":"25","author":"Li","year":"2022","journal-title":"Nat. Neurosci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1017\/S0007114513003553","article-title":"Gestational methyl donor deficiency alters key proteins involved in neurosteroidogenesis in the olfactory bulbs of newborn female rats and is associated with impaired olfactory performance","volume":"111","author":"Martin","year":"2014","journal-title":"Br. J. Nutr."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"153992","DOI":"10.1016\/j.metabol.2019.153992","article-title":"SIRT1 activation rescues the mislocalization of RNA-binding proteins and cognitive defects induced by inherited cobalamin disorders","volume":"101","author":"Ghemrawi","year":"2019","journal-title":"Metabolism"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.1007\/s12035-020-02163-2","article-title":"Glucocorticoid Receptor Activation Restores Learning Memory by Modulating Hippocampal Plasticity in a Mouse Model of Brain Vitamin B12 Deficiency","volume":"58","author":"Dreumont","year":"2021","journal-title":"Mol. Neurobiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1002\/path.5254","article-title":"N-homocysteinylation of tau and MAP1 is increased in autopsy specimens of Alzheimer\u2019s disease and vascular dementia","volume":"248","author":"Smith","year":"2019","journal-title":"J. Pathol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2239","DOI":"10.1016\/j.bbagen.2015.08.013","article-title":"Protein N-homocysteinylation: From cellular toxicity to neurodegeneration","volume":"1850","author":"Sharma","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Wis\u0142owska-Stanek, A., Ko\u0142osowska, K., and Maciejak, P. (2021). Neurobiological Basis of Increased Risk for Suicidal Behaviour. Cells, 10.","DOI":"10.3390\/cells10102519"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Masuo, Y., Satou, T., Takemoto, H., and Koike, K. (2021). Smell and Stress Response in the Brain: Review of the Connection between Chemistry and Neuropharmacology. Molecules, 26.","DOI":"10.3390\/molecules26092571"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"6718","DOI":"10.1523\/JNEUROSCI.4287-11.2012","article-title":"Olfactory deficits cause anxiety-like behaviors in mice","volume":"32","author":"Glinka","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"15324","DOI":"10.1523\/JNEUROSCI.1835-13.2013","article-title":"When the sense of smell meets emotion: Anxiety-state-dependent olfactory processing and neural circuitry adaptation","volume":"33","author":"Krusemark","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"49","DOI":"10.3389\/fnbeh.2018.00049","article-title":"Elevated Anxiety and Impaired Attention in Super-Smeller, Kv1.3 Knockout Mice","volume":"12","author":"Huang","year":"2018","journal-title":"Front. Behav. Neurosci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.biopsych.2014.11.022","article-title":"Effects of the Social Environment and Stress on Glucocorticoid Receptor Gene Methylation: A Systematic Review","volume":"79","author":"Turecki","year":"2016","journal-title":"Biol. Psychiatry"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.neubiorev.2021.03.003","article-title":"Glucocorticoid receptor gene (NR3C1) methylation during the first thousand days: Environmental exposures and developmental outcomes","volume":"125","author":"Berretta","year":"2021","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1093\/nutrit\/nuy007","article-title":"Effect of supplementation with methyl-donor nutrients on neurodevelopment and cognition: Considerations for future research","volume":"76","author":"McKee","year":"2018","journal-title":"Nutr. Rev."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1515\/cclm.2002.193","article-title":"Hyperhomocysteinemia is related to a decreased blood level of vitamin B12 in the second and third trimester of normal pregnancy","volume":"40","author":"Chery","year":"2002","journal-title":"Clin. Chem. Lab. Med."},{"key":"ref_59","unstructured":"Paxinos, G., and Watson, C. (2013). The Rat Brain in Stereotaxic Coordinates, Elsevier. [7th ed.]."},{"key":"ref_60","first-page":"56652","article-title":"Synthesis and Mass Spectrometry Analysis of Oligo-peptoids","volume":"132","author":"Ren","year":"2018","journal-title":"J. Vis. Exp."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.pnpbp.2005.06.006","article-title":"Postnatal development of rat pups is altered by prenatal methamphetamine exposure","volume":"30","year":"2006","journal-title":"Prog. Neuro-Psychopharmacol. Biol. Psychiatry"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/12\/9847\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:49:45Z","timestamp":1760125785000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/12\/9847"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,7]]},"references-count":61,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2023,6]]}},"alternative-id":["ijms24129847"],"URL":"https:\/\/doi.org\/10.3390\/ijms24129847","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,7]]}}}