{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,2]],"date-time":"2026-04-02T10:26:56Z","timestamp":1775125616146,"version":"3.50.1"},"reference-count":79,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2016,5,4]],"date-time":"2016-05-04T00:00:00Z","timestamp":1462320000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BD\/78440\/2011"],"award-info":[{"award-number":["SFRH\/BD\/78440\/2011"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["IF\/00185\/2012"],"award-info":[{"award-number":["IF\/00185\/2012"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["ANR\/NEU-NMC\/0022\/2012"],"award-info":[{"award-number":["ANR\/NEU-NMC\/0022\/2012"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0154781","type":"journal-article","created":{"date-parts":[[2016,5,4]],"date-time":"2016-05-04T14:07:23Z","timestamp":1462370843000},"page":"e0154781","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":31,"title":["Carbon Monoxide Releasing Molecule-A1 (CORM-A1) Improves Neurogenesis: Increase of Neuronal Differentiation Yield by Preventing Cell Death"],"prefix":"10.1371","volume":"11","author":[{"given":"Ana S.","family":"Almeida","sequence":"first","affiliation":[]},{"given":"Nuno L.","family":"Soares","sequence":"additional","affiliation":[]},{"given":"Melissa","family":"Vieira","sequence":"additional","affiliation":[]},{"given":"Jan Bert","family":"Gramsbergen","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9415-3742","authenticated-orcid":true,"given":"Helena L. A.","family":"Vieira","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2016,5,4]]},"reference":[{"issue":"no. 3","key":"ref1","first-page":"232","article-title":"Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology","volume":"vol. 33","author":"D. T. Balu","year":"2009"},{"issue":"no. 1","key":"ref2","first-page":"125","article-title":"Stem Cells for Ischemic Brain Injury:A Critical Review","volume":"vol. 515","author":"T. C. Burns","year":"2009"},{"issue":"no. 6128","key":"ref3","first-page":"39","article-title":"Developmental biology. Programmed cell death in neuronal development","volume":"vol. 340","author":"M. P. J. Dekkers","year":"2013"},{"issue":"no. 4","key":"ref4","first-page":"281","article-title":"Cell death in early neural life","volume":"vol. 75","author":"P. Boya","year":"2005"},{"issue":"no. 14","key":"ref5","first-page":"3207","article-title":"An acquired sensitivity to H2O2-induced apoptosis during neuronal differentiation of NT2\/D1 cells","volume":"vol. 9","author":"S. Wang","year":"1998"},{"issue":"no. 7422","key":"ref6","first-page":"109","article-title":"Intrinsically determined cell death of developing cortical interneurons","volume":"vol. 491","author":"D. G. Southwell","year":"2012"},{"issue":"no. 2","key":"ref7","first-page":"583","article-title":"Heme oxygenase-1\/carbon monoxide: from basic science to therapeutic applications","volume":"vol. 86","author":"S. W. Ryter","year":"2006"},{"issue":"no. 22","key":"ref8","first-page":"17077","article-title":"Glutathionylation of adenine nucleotide translocase induced by carbon monoxide prevents mitochondrial membrane permeabilization and apoptosis","volume":"vol. 285","author":"C. S. F. Queiroga","year":"2010"},{"issue":"no. 14","key":"ref9","first-page":"10761","article-title":"Carbon monoxide modulates apoptosis by reinforcing oxidative metabolism in astrocytes: role of BCL-2","volume":"vol. 287","author":"A. S. Almeida","year":"2012"},{"issue":"no. 4","key":"ref10","first-page":"e60672","article-title":"Carbon monoxide abrogates ischemic insult to neuronal cells via the soluble guanylate cyclase-cGMP pathway","volume":"vol. 8","author":"N. Schallner","year":"2013"},{"key":"ref11","first-page":"1927","article-title":"A Cytoprotective Role for the Heme Oxygenase-1 \/ CO Pathway During Neural Differentiation of Human Mesenchymal Stem Cells","volume":"vol. 86","author":"I. Barbagallo","year":"2008"},{"issue":"no. 2","key":"ref12","first-page":"375","article-title":"Pre-conditioning induced by carbon monoxide provides neuronal protection against apoptosis","volume":"vol. 107","author":"H. L. a Vieira","year":"2008"},{"issue":"no. 9","key":"ref13","first-page":"2605","article-title":"Carbon monoxide-activated Nrf2 pathway leads to protection against permanent focal cerebral ischemia","volume":"vol. 42","author":"B. Wang","year":"2011"},{"key":"ref14","article-title":"Carbon monoxide and the CNS: challenges and achievements","author":"C. S. F. Queiroga","year":"2014"},{"issue":"no. 4","key":"ref15","first-page":"1099","article-title":"Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species","volume":"vol. 21","author":"B. S. Zuckerbraun","year":"2007"},{"key":"ref16","first-page":"146","article-title":"Carbon monoxide activates NF- \u03ba B via ROS generation and Akt pathways to protect against cell death of hepatocytes","volume":"vol. 295","author":"H. S. Kim","year":"2008"},{"issue":"no. Pt 2","key":"ref17","first-page":"299","article-title":"A new activating role for CO in cardiac mitochondrial biogenesis","volume":"vol. 120","author":"H. B. Suliman","year":"2007"},{"issue":"no. 2","key":"ref18","first-page":"641","article-title":"Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis","volume":"vol. 329","author":"S. Lancel","year":"2009"},{"issue":"no. 1","key":"ref19","first-page":"228","article-title":"Carbon monoxide induces a late preconditioning-mimetic cardioprotective and antiapoptotic milieu in the myocardium","volume":"vol. 52","author":"A. B. Stein","year":"2012"},{"issue":"no. 5","key":"ref20","first-page":"270","article-title":"Preconditioning of carbon monoxide releasing molecule-derived CO attenuates LPS-induced activation of HUVEC","volume":"vol. 4","author":"B. Sun","year":"2008"},{"key":"ref21","first-page":"e42632","article-title":"<italic>Preconditioning Triggered by Carbon Monoxide (CO) Provides Neuronal Protection Following Perinatal Hypoxia-Ischemia<\/italic>","volume":"vol. 7","author":"C. S. F. Queiroga","year":"2012"},{"issue":"no. 11","key":"ref22","first-page":"1827","article-title":"Role of heme oxygenase-1 in postnatal differentiation of stem cells: a possible cross-talk with microRNAs","volume":"vol. 20","author":"M. Kozakowska","year":"2014"},{"issue":"no. 6","key":"ref23","article-title":"Heme oxygenase-1 accelerates cutaneous wound healing in mice","volume":"vol. 4","author":"A. Grochot-Przeczek","year":"2009"},{"issue":"no. 1","key":"ref24","first-page":"236","article-title":"HO-1 expression increases mesenchymal stem cell-derived osteoblasts but decreases adipocyte lineage","volume":"vol. 46","author":"L. Vanella","year":"2010"},{"key":"ref25","first-page":"890671","article-title":"Oxidative stress and heme oxygenase-1 regulated human mesenchymal stem cells differentiation","volume":"vol. 2012","author":"L. Vanella","year":"2012"},{"issue":"no. 2","key":"ref26","first-page":"113","article-title":"Heme Oxygenase-1 Inhibits Myoblast Differentiation by Targeting Myomirs","volume":"vol. 16","author":"M. Kozakowska","year":"2012"},{"issue":"no. 1","key":"ref27","article-title":"Myoblast-conditioned media improve regeneration and revascularization of ischemic muscles in diabetic mice","volume":"vol. 6","author":"M. Kozakowska","year":"2015"},{"issue":"no. 1","key":"ref28","first-page":"115","article-title":"Pre-emptive hypoxia-regulated HO-1 gene therapy improves post-ischaemic limb perfusion and tissue regeneration in mice","volume":"vol. 97","author":"A. Jazwa","year":"2013"},{"key":"ref29","first-page":"1","article-title":"HIF-regulated HO-1 gene transfer improves the post-ischemic limb recovery and diminishes TLR-triggered immune responses\u2014effects modified by concomitant VEGF overexpression","author":"A. Jazwa","year":"2015"},{"key":"ref30","first-page":"e1139","article-title":"Heme oxygenase-1 derived carbon monoxide permits maturation of myeloid cells","volume":"vol. 5","author":"B. Wegiel","year":"2014"},{"issue":"no. 2","key":"ref31","first-page":"95","article-title":"Carbon Monoxide-Releasing Molecule-A1 Inhibits Th1\/Th17 and Stimulates Th2 Differentiation In vitro","volume":"vol. 80","author":"I. Nikolic","year":"2014"},{"issue":"no. 3","key":"ref32","first-page":"267","article-title":"Heme oxygenase and carbon monoxide initiate homeostatic signaling","volume":"vol. 86","author":"M. Bilban","year":"2008"},{"issue":"no. 3","key":"ref33","first-page":"444","article-title":"Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species","volume":"vol. 93","author":"H. L. a Vieira","year":"2011"},{"issue":"no. 3","key":"ref34","first-page":"1","article-title":"Upregulation of mitochondrial function and antioxidant defense in the differentiation of stem cells","volume":"vol. 1800","author":"C. T. Chen","year":"2009"},{"key":"ref35","first-page":"1472","article-title":"Dynamic changes in mitochondrial biogenesis and antioxidant enzymes during the spontaneous differentiation of human embryonic stem cells","volume":"vol. 348","author":"Y. M. Cho","year":"2006"},{"issue":"no. 2","key":"ref36","first-page":"284","article-title":"CORM-A1: a new pharmacologically active carbon monoxide-releasing molecule","volume":"vol. 19","author":"R. Motterlini","year":"2005"},{"issue":"no. 9","key":"ref37","first-page":"728","article-title":"The therapeutic potential of carbon monoxide","volume":"vol. 9","author":"R. Motterlini","year":"2010"},{"key":"ref38","first-page":"9","article-title":"Considerations for the Use of SH\u2014SY5Y Neuroblastoma Cells in Neurobiology","volume":"vol. 1078","author":"J. Kovalevich","year":"2013"},{"key":"ref39","first-page":"25","article-title":"Human neuroblastoma cells in culture: a model for neuronal cell differentiation and function","volume":"vol. 592","author":"S. Pahlman","year":"1990"},{"issue":"no. 72","key":"ref40","first-page":"17","article-title":"Neuronal differentiation and long-term culture of the human neuroblastoma line SH-SY5Y","author":"R. Constantinescu","year":"2007"},{"issue":"no. 5","key":"ref41","first-page":"1802","article-title":"Pure, Postmitotic, Polarized Human Neurons Derived from NTera 2 Cells Provide a System for Expressing Exogenous Proteins in Terminally Differentiated Neurons","volume":"vol. 12","author":"S. Pleasure","year":"1992"},{"issue":"no. 7","key":"ref42","article-title":"Differential expression of Bcl-2-related proteins in differentiating NT2 cells","volume":"vol. 11","author":"I. Guillemain","year":"2000"},{"issue":"no. 6","key":"ref43","first-page":"585","article-title":"NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell","volume":"vol. 35","author":"S. J. Pleasure","year":"1993"},{"issue":"no. 2","key":"ref44","first-page":"333","article-title":"Expression of glutamic acid decarboxylase during human neuronal differentiation: Studies using the NTera-2 culture system","volume":"vol. 767","author":"A. Yoshioka","year":"1997"},{"issue":"no. August","key":"ref45","first-page":"404","article-title":"Differential effects of spinal cord gray and white matter on process outgrowth from grafted human NTERA2 neurons (NT2N, hNT)","volume":"vol. 415","author":"R. S. Hartley","year":"1999"},{"issue":"no. 2","key":"ref46","first-page":"121","article-title":"Immature human NT2 cells grafted into mouse brain differentiate into neuronal and glial cell types","volume":"vol. 486","author":"A. Ferrari","year":"2000"},{"issue":"no. 4","key":"ref47","first-page":"368","article-title":"Genetically modified NT2N human neuronal cells mediate long-term gene expression as CNS grafts in vivo and improve functional cognitive outcome following experimental traumatic brain injury","volume":"vol. 62","author":"D. J. Watson","year":"2003"},{"issue":"no. 4","key":"ref48","first-page":"565","article-title":"Transplantation of cultured human neuronal cells for patients with stroke","volume":"vol. 55","author":"D. Kondziolka","year":"2000"},{"issue":"no. 1","key":"ref49","first-page":"94","article-title":"Transient modulation of cytoplasmic and nuclear retinoid receptors expression in differentiating human teratocarcinoma NT2 cells","volume":"vol. 84","author":"R. Borghi","year":"2003"},{"issue":"no. 1","key":"ref50","first-page":"34","article-title":"Expression of retinoid receptors during the retinoic acid-induced neuronal differentiation of human embryonal carcinoma cells","volume":"vol. 75","author":"W. M. Cheung","year":"2000"},{"issue":"no. 2","key":"ref51","first-page":"240","article-title":"Retinoic acid receptors and tissue-transglutaminase mediate short-term effect of retinoic acid on migration and invasion of neuroblastoma SH-SY5Y cells","volume":"vol. 25","author":"S. Joshi","year":"2006"},{"issue":"no. 9","key":"ref52","first-page":"1187","article-title":"Characterization of the NT2-derived neuronal and astrocytic cell lines as alternative in vitro models for primary human neurons and astrocytes","volume":"vol. 92","author":"Y. Haile","year":"2014"},{"issue":"no. 12","key":"ref53","first-page":"1521","article-title":"Organotypic hippocampal slice cultures: a model system to study basic cellular and molecular mechanisms of neuronal cell death, neuroprotection, and synaptic plasticity","volume":"vol. 30","author":"I. E. Holopainen","year":"2005"},{"issue":"no. 4","key":"ref54","first-page":"435","article-title":"Organotypic hippocampal slice cultures for studies of brain damage, neuroprotection and neurorepair","volume":"vol. 4","author":"J. Noraberg","year":"2005"},{"issue":"no. 14","key":"ref55","article-title":"Organotypic cultures as tools for functional screening in the CNS to act as an important link between high-throughput approaches and animal models. REVIEWS","volume":"vol. 10","author":"L. Sundstrom","year":"2005"},{"issue":"no. 2","key":"ref56","first-page":"337","article-title":"Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat","volume":"vol. 56","author":"H. A. Cameron","year":"1993"},{"issue":"no. 8","key":"ref57","first-page":"1704","article-title":"Postnatal neurogenesis in hippocampal slice cultures: Early in vitro labeling of neural precursor cells leads to efficient neuronal production","volume":"vol. 85","author":"T. Namba","year":"2007"},{"issue":"no. 2","key":"ref58","first-page":"241","article-title":"Neurogenesis in hippocampal slice cultures","volume":"vol. 26","author":"O. Raineteau","year":"2004"},{"issue":"no. 2","key":"ref59","first-page":"e1074","article-title":"Cell differentiation versus cell death: extracellular glucose is a key determinant of cell fate following oxidative stress exposure","volume":"vol. 5","author":"R. C. Poulsen","year":"2014"},{"key":"ref60","first-page":"278","article-title":"Markers for neuronal degeneration in organotypic slice cultures","author":"J. Noraberg","year":"1999","journal-title":"Markers for neuronal degeneration in organotypic slice cultures"},{"issue":"no. 2","key":"ref61","first-page":"E17","article-title":"Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities","volume":"vol. 90","author":"R. Motterlini","year":"2002"},{"key":"ref62","first-page":"117","article-title":"Gas-liquid chromatography and mass spectral analysis of mono-, di- and tricarboxylates as their tert.-butyldimethylsilyl derivatives","volume":"vol. 361","author":"T. P. Mawhinney","year":"1986"},{"key":"ref63","first-page":"n\/a","article-title":"Characterization of glucose-related metabolic pathways in differentiated rat oligodendrocyte lineage cells","author":"A. I. Amaral","year":"2015"},{"issue":"no. 2","key":"ref64","first-page":"98","article-title":"The Application of Mass Spectrometry in Organic Chemistry: Determination of the Structure of Natural Products","volume":"vol. 1","author":"K. Biemann","year":"1962"},{"issue":"no. August","key":"ref65","first-page":"311","article-title":"The Ki-67 Protein: From the Known and","volume":"vol. 322","author":"T. Scholzen","year":"2000"},{"issue":"no. 1","key":"ref66","first-page":"10","article-title":"Carbon monoxide prevents hepatic mitochondrial membrane permeabilization","volume":"vol. 12","author":"C. S. F. Queiroga","year":"2011"},{"issue":"no. 1","key":"ref67","first-page":"21","article-title":"The neurogenesis hypothesis of affective and anxiety disorders: are we mistaking the scaffolding for the building?","volume":"vol. 62","author":"D. Petrik","year":"2012"},{"issue":"no. 12","key":"ref68","first-page":"3730","article-title":"The CO \/ HO system reverses inhibition of mitochondrial biogenesis and prevents murine doxorubicin cardiomyopathy","volume":"vol. 117","author":"H. B. Suliman","year":"2007"},{"issue":"no. 23","key":"ref69","first-page":"7009","article-title":"Carbon monoxide expedites metabolic exhaustion to inhibit tumor growth","volume":"vol. 73","author":"B. Wegiel","year":"2013"},{"issue":"no. 52","key":"ref70","first-page":"32804","article-title":"Carbon monoxide controls the proliferation of hypoxic vascular smooth muscle cells","volume":"vol. 272","author":"T. Morita","year":"1997"},{"issue":"no. 27","key":"ref71","first-page":"25350","article-title":"Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle","volume":"vol. 280","author":"C. Taill\u00e9","year":"2005"},{"issue":"no. 4","key":"ref72","first-page":"369","article-title":"Antiproliferative effects of carbon monoxide on pancreatic cancer","volume":"vol. 46","author":"L. V\u00edtek","year":"2014"},{"issue":"no. 1","key":"ref73","first-page":"55","article-title":"The induction of heme oxygenase-1 suppresses heat shock protein 90 and the proliferation of human breast cancer cells through its byproduct carbon monoxide","volume":"vol. 274","author":"W.-Y. Lee","year":"2014"},{"issue":"no. 2","key":"ref74","first-page":"329","article-title":"Carbon monoxide inhibits sprouting angiogenesis and vascular endothelial growth factor receptor-2 phosphorylation","volume":"vol. 113","author":"S. Ahmad","year":"2015"},{"issue":"no. 5","key":"ref75","first-page":"1247","article-title":"Heme oxygenase-1 and heme oxygenase-2 have distinct roles in the proliferation and survival of olfactory receptor neurons mediated by cGMP and bilirubin, respectively","volume":"vol. 85","author":"J. Chen","year":"2003"},{"issue":"no. 10","key":"ref76","first-page":"454","article-title":"Cell death in early neural development: beyond the neurotrophic theory","volume":"vol. 23","author":"E. J. de la Rosa","year":"2000"},{"issue":"no. 2","key":"ref77","first-page":"233","article-title":"Early neural cell death: Dying to become neurons","volume":"vol. 274","author":"W. Yeo","year":"2004"},{"key":"ref78","first-page":"191","article-title":"Special Review Based on a Presentation made at the 16th International Congress of the IFAA Role of programmed cell death in normal neuronal development and function","volume":"vol. 79","author":"R. Buss","year":"2004"},{"issue":"no. 14","key":"ref79","first-page":"4408","article-title":"Neural stem and progenitor cells retain their potential for proliferation and differentiation into functional neurons despite lower number in aged brain","volume":"vol. 29","author":"H. Ahlenius","year":"2009"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0154781","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2018,10,24]],"date-time":"2018-10-24T00:18:24Z","timestamp":1540340304000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0154781"}},"subtitle":[],"editor":[{"given":"Jozef","family":"Dulak","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2016,5,4]]},"references-count":79,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2016,5,4]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0154781","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,5,4]]}}}