{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T16:35:03Z","timestamp":1789058103903,"version":"build-2803163510"},"reference-count":56,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2019,12,26]],"date-time":"2019-12-26T00:00:00Z","timestamp":1577318400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["1R01NS106907-01"],"award-info":[{"award-number":["1R01NS106907-01"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Extracellular vesicles (EVs) derived from human bone marrow mesenchymal stem cells (hMSCs) have great promise as biologics to treat neurological and neurodegenerative conditions due to their robust antiinflammatory and neuroprotective properties. Besides, intranasal (IN) administration of EVs has caught much attention because the procedure is noninvasive, amenable for repetitive dispensation, and leads to a quick penetration of EVs into multiple regions of the forebrain. Nonetheless, it is unknown whether brain injury-induced signals are essential for the entry of IN-administered EVs into different brain regions. Therefore, in this study, we investigated the distribution of IN-administered hMSC-derived EVs into neurons and microglia in the intact and status epilepticus (SE) injured rat forebrain. Ten billion EVs labeled with PKH26 were dispensed unilaterally into the left nostril of na\u00efve rats, and rats that experienced two hours of kainate-induced SE. Six hours later, PKH26 + EVs were quantified from multiple forebrain regions using serial brain sections processed for different neural cell markers and confocal microscopy. Remarkably, EVs were seen bilaterally in virtually all regions of intact and SE-injured forebrain. The percentage of neurons incorporating EVs were comparable for most forebrain regions. However, in animals that underwent SE, a higher percentage of neurons incorporated EVs in the hippocampal CA1 subfield and the entorhinal cortex, the regions that typically display neurodegeneration after SE. In contrast, the incorporation of EVs by microglia was highly comparable in every region of the forebrain measured. Thus, unilateral IN administration of EVs is efficient for delivering EVs bilaterally into neurons and microglia in multiple regions in the intact or injured forebrain. Furthermore, incorporation of EVs by neurons is higher in areas of brain injury, implying that injury-related signals likely play a role in targeting of EVs into neurons, which may be beneficial for EV therapy in various neurodegenerative conditions including traumatic brain injury, stroke, multiple sclerosis, and Alzheimer\u2019s disease.<\/jats:p>","DOI":"10.3390\/ijms21010181","type":"journal-article","created":{"date-parts":[[2019,12,27]],"date-time":"2019-12-27T05:37:08Z","timestamp":1577425028000},"page":"181","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":103,"title":["Intranasally Administered Human MSC-Derived Extracellular Vesicles Pervasively Incorporate into Neurons and Microglia in both Intact and Status Epilepticus Injured Forebrain"],"prefix":"10.3390","volume":"21","author":[{"given":"Maheedhar","family":"Kodali","sequence":"first","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1874-509X","authenticated-orcid":false,"given":"Olagide W.","family":"Castro","sequence":"additional","affiliation":[{"name":"Health Science Center, Federal University of Alagoas, Maceio 57072900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dong-Ki","family":"Kim","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alicia","family":"Thomas","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bing","family":"Shuai","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sahithi","family":"Attaluri","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raghavendra","family":"Upadhya","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7056-2373","authenticated-orcid":false,"given":"Daniel","family":"Gitai","sequence":"additional","affiliation":[{"name":"Health Science Center, Federal University of Alagoas, Maceio 57072900, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leelavathi N.","family":"Madhu","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darwin J.","family":"Prockop","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashok K.","family":"Shetty","sequence":"additional","affiliation":[{"name":"Institute for Regenerative Medicine, Department of Molecular and Cellular Medicine, Texas A&amp;M University College of Medicine, 1114 TAMU, College Station, TX 77842, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2019,12,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Thery, C., Witwer, K.W., Aikawa, E., Alcaraz, M.J., Anderson, J.D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., and Atkin-Smith, G.K. (2018). Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J. Extracell. Vesicles.","DOI":"10.1080\/20013078.2018.1535750"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1089\/ars.2017.7265","article-title":"Extracellular Vesicles: Mechanisms in Human Health and Disease","volume":"30","author":"Malloci","year":"2019","journal-title":"Antioxid. Redox Signal."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1083\/jcb.201211138","article-title":"Extracellular vesicles: Exosomes, microvesicles, and friends","volume":"200","author":"Raposo","year":"2013","journal-title":"J. Cell Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1667\/RR14482.1","article-title":"Extracellular Vesicles and Vascular Injury: New Insights for Radiation Exposure","volume":"186","author":"Flamant","year":"2016","journal-title":"Radiat. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"14240","DOI":"10.3390\/ijms140714240","article-title":"Intercellular communication by exosome-derived microRNAs in cancer","volume":"14","author":"Hannafon","year":"2013","journal-title":"Int. J. Mol. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1182\/blood-2011-02-338004","article-title":"Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes","volume":"119","author":"Montecalvo","year":"2012","journal-title":"Blood"},{"key":"ref_7","unstructured":"Upadhya, D., and Shetty, A.K. (2019). Promise of extracellular vesicles for diagnosis and treatment of epilepsy. Epilepsy Behav."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Upadhya, D., and Shetty, A.K. (2019). Extracellular Vesicles as Therapeutics for Brain Injury and Disease. Curr. Pharm. Des.","DOI":"10.2174\/1381612825666191014164950"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Katsu, M., Hama, Y., Utsumi, J., Takashina, K., Yasumatsu, H., Mori, F., Wakabayashi, K., Shoji, M., and Sasaki, H. (2019). MicroRNA expression profiles of neuron-derived extracellular vesicles in plasma from patients with amyotrophic lateral sclerosis. Neurosci. Lett.","DOI":"10.1016\/j.neulet.2019.03.048"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Ko, J., Hemphill, M., Yang, Z., Beard, K., Sewell, E., Shallcross, J., Schweizer, M., Sandsmark, D.K., Diaz-Arrastia, R., and Kim, J. (2019). Multi-Dimensional Mapping of Brain-Derived Extracellular Vesicle MicroRNA Biomarker for Traumatic Brain Injury Diagnostics. J. Neurotrauma.","DOI":"10.1089\/neu.2018.6220"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3842","DOI":"10.1074\/jbc.M111.277061","article-title":"Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease","volume":"287","author":"Saman","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1212\/WNL.0000000000001702","article-title":"Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease","volume":"85","author":"Goetzl","year":"2015","journal-title":"Neurology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"4141","DOI":"10.1096\/fj.201600816R","article-title":"Decreased synaptic proteins in neuronal exosomes of frontotemporal dementia and Alzheimer\u2019s disease","volume":"30","author":"Goetzl","year":"2016","journal-title":"FASEB J."},{"key":"ref_14","first-page":"63","article-title":"Prediction of conversion from mild cognitive impairment to dementia with neuronally derived blood exosome protein profile","volume":"3","author":"Winston","year":"2016","journal-title":"Alzheimer\u2019s Dement."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1007\/s00401-014-1314-y","article-title":"Plasma exosomal alpha-synuclein is likely CNS-derived and increased in Parkinson\u2019s disease","volume":"128","author":"Shi","year":"2014","journal-title":"Acta Neuropathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1016\/j.bbi.2019.06.040","article-title":"Neuroinflammation in Gulf War Illness is linked with HMGB1 and complement activation, which can be discerned from brain-derived extracellular vesicles in the blood","volume":"81","author":"Madhu","year":"2019","journal-title":"BrainBehav. Immun."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.ebiom.2018.11.026","article-title":"Neural stem cell derived extracellular vesicles: Attributes and prospects for treating neurodegenerative disorders","volume":"38","author":"Vogel","year":"2018","journal-title":"Ebiomedicine"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Park, K.S., Bandeira, E., Shelke, G.V., Lasser, C., and Lotvall, J. (2019). Enhancement of therapeutic potential of mesenchymal stem cell-derived extracellular vesicles. Stem Cell Res. Ther.","DOI":"10.1186\/s13287-019-1398-3"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"856","DOI":"10.3171\/2014.11.JNS14770","article-title":"Effect of exosomes derived from multipluripotent mesenchymal stromal cells on functional recovery and neurovascular plasticity in rats after traumatic brain injury","volume":"122","author":"Zhang","year":"2015","journal-title":"J. Neurosurg."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1073\/pnas.1522297113","article-title":"Chromatographically isolated CD63 + CD81+ extracellular vesicles from mesenchymal stromal cells rescue cognitive impairments after TBI","volume":"113","author":"Kim","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1161\/STROKEAHA.117.020353","article-title":"Human Neural Stem Cell Extracellular Vesicles Improve Recovery in a Porcine Model of Ischemic Stroke","volume":"49","author":"Webb","year":"2018","journal-title":"Stroke"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1007\/s12975-017-0599-2","article-title":"Human Neural Stem Cell Extracellular Vesicles Improve Tissue and Functional Recovery in the Murine Thromboembolic Stroke Model","volume":"9","author":"Webb","year":"2018","journal-title":"Transl. Stroke Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Dabrowska, S., Andrzejewska, A., Lukomska, B., and Janowski, M. (2019). Neuroinflammation as a target for treatment of stroke using mesenchymal stem cells and extracellular vesicles. J. Neuroinflamm.","DOI":"10.1186\/s12974-019-1571-8"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e3536","DOI":"10.1073\/pnas.1703920114","article-title":"Intranasal MSC-derived A1-exosomes ease inflammation, and prevent abnormal neurogenesis and memory dysfunction after status epilepticus","volume":"114","author":"Long","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"6670","DOI":"10.1021\/acsnano.9b01004","article-title":"Stem Cell-Derived Exosomes as Nanotherapeutics for Autoimmune and Neurodegenerative Disorders","volume":"13","author":"Riazifar","year":"2019","journal-title":"ACS Nano"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.3233\/JAD-170848","article-title":"Mesenchymal Stem Cell-Derived Extracellular Vesicles Suppresses iNOS Expression and Ameliorates Neural Impairment in Alzheimer\u2019s Disease Mice","volume":"61","author":"Wang","year":"2018","journal-title":"J. Alzheimer\u2019s Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3389\/fnins.2019.00209","article-title":"Bone Mesenchymal Stem Cell-Derived Extracellular Vesicles Promote Recovery Following Spinal Cord Injury via Improvement of the Integrity of the Blood-Spinal Cord Barrier","volume":"13","author":"Lu","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1016\/j.nbd.2007.03.016","article-title":"Strategies for promoting anti-seizure effects of hippocampal fetal cells grafted into the hippocampus of rats exhibiting chronic temporal lobe epilepsy","volume":"27","author":"Rao","year":"2007","journal-title":"Neurobiol. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1002\/hipo.20449","article-title":"Status epilepticus during old age is not associated with enhanced hippocampal neurogenesis","volume":"18","author":"Rao","year":"2008","journal-title":"Hippocampus"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"915","DOI":"10.14336\/AD.2019.0720","article-title":"A Model of Chronic Temporal Lobe Epilepsy Presenting Constantly Rhythmic and Robust Spontaneous Seizures, Co-morbidities and Hippocampal Neuropathology","volume":"10","author":"Upadhya","year":"2019","journal-title":"Aging Dis."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1769","DOI":"10.1038\/mt.2011.164","article-title":"Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain","volume":"19","author":"Zhuang","year":"2011","journal-title":"Mol. Ther. J. Am. Soc. Gene Ther."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.jconrel.2015.03.033","article-title":"Exosomes as drug delivery vehicles for Parkinson\u2019s disease therapy","volume":"207","author":"Haney","year":"2015","journal-title":"J. Control. Release Off. J. Control. Release Soc."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1016\/j.biocel.2016.09.002","article-title":"Curcumin-loaded embryonic stem cell exosomes restored neurovascular unit following ischemia-reperfusion injury","volume":"79","author":"Kalani","year":"2016","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"99263","DOI":"10.1172\/jci.insight.99263","article-title":"Generation and testing of clinical-grade exosomes for pancreatic cancer","volume":"3","author":"Mendt","year":"2018","journal-title":"Jci Insight"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1182\/blood-2014-03-562439","article-title":"Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells","volume":"124","author":"Wang","year":"2014","journal-title":"Blood"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"26316","DOI":"10.3402\/jev.v4.26316","article-title":"Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting","volume":"4","author":"Wiklander","year":"2015","journal-title":"J. Extracell. Vesicles."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/1743-8454-1-2","article-title":"Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species","volume":"1","author":"Johnston","year":"2004","journal-title":"Cereb. Fluid Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1089\/lrb.2004.2.139","article-title":"Lymphatic vessels gain access to cerebrospinal fluid through unique association with olfactory nerves","volume":"2","author":"Zakharov","year":"2004","journal-title":"Lymphat. Res. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"13853","DOI":"10.1021\/acsnano.9b04397","article-title":"Tumor-Derived Extracellular Vesicles Breach the Intact Blood-Brain Barrier via Transcytosis","volume":"13","author":"Morad","year":"2019","journal-title":"ACS Nano"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1002\/jnr.20802","article-title":"Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy","volume":"83","author":"Rao","year":"2006","journal-title":"J. Neurosci. Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"4613","DOI":"10.1523\/JNEUROSCI.0064-06.2006","article-title":"Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy","volume":"26","author":"Kumar","year":"2006","journal-title":"J. Neurosci. Off. J. Soc. Neurosci."},{"key":"ref_42","first-page":"1","article-title":"Acute Seizures in Old Age Leads to a Greater Loss of CA1 Pyramidal Neurons, an Increased Propensity for Developing Chronic TLE and a Severe Cognitive Dysfunction","volume":"2","author":"Hattiangady","year":"2011","journal-title":"Aging Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"806","DOI":"10.1016\/j.neuropharm.2012.06.009","article-title":"Sequel of spontaneous seizures after kainic acid-induced status epilepticus and associated neuropathological changes in the subiculum and entorhinal cortex","volume":"63","author":"Drexel","year":"2012","journal-title":"Neuropharmacology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"17807","DOI":"10.1038\/srep17807","article-title":"Resveratrol Treatment after Status Epilepticus Restrains Neurodegeneration and Abnormal Neurogenesis with Suppression of Oxidative Stress and Inflammation","volume":"5","author":"Mishra","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1242\/jcs.074088","article-title":"Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis","volume":"124","author":"Fitzner","year":"2011","journal-title":"J. Cell Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1111\/j.1600-0854.2010.01041.x","article-title":"Cellular internalization of exosomes occurs through phagocytosis","volume":"11","author":"Feng","year":"2010","journal-title":"Traffic (Cph. Den.)"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"182","DOI":"10.3389\/fncel.2013.00182","article-title":"Extracellular vesicles as mediators of neuron-glia communication","volume":"7","author":"Fruhbeis","year":"2013","journal-title":"Front. Cell. Neurosci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1111\/j.1600-0854.2009.00878.x","article-title":"Defining macropinocytosis","volume":"10","author":"Kerr","year":"2009","journal-title":"Traffic (Cph. Den.)"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1038\/ncb0509-510","article-title":"Virus entry by macropinocytosis","volume":"11","author":"Mercer","year":"2009","journal-title":"Nat. Cell Biol."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Loerke, D., Mettlen, M., Yarar, D., Jaqaman, K., Jaqaman, H., Danuser, G., and Schmid, S.L. (2009). Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol., 7.","DOI":"10.1371\/journal.pbio.1000057"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3389\/fnmol.2014.00091","article-title":"Synaptic vesicles are \u201cprimed\u201d for fast clathrin-mediated endocytosis at the ribbon synapse","volume":"7","author":"Pelassa","year":"2014","journal-title":"Front. Mol. Neurosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1002\/(SICI)1096-9861(19991115)414:2<238::AID-CNE7>3.0.CO;2-A","article-title":"Aging impairs axonal sprouting response of dentate granule cells following target loss and partial deafferentation","volume":"414","author":"Shetty","year":"1999","journal-title":"J. Comp. Neurol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1073\/pnas.1814185115","article-title":"Human induced pluripotent stem cell-derived MGE cell grafting after status epilepticus attenuates chronic epilepsy and comorbidities via synaptic integration","volume":"116","author":"Upadhya","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.bbi.2018.01.009","article-title":"Curcumin treatment leads to better cognitive and mood function in a model of Gulf War Illness with enhanced neurogenesis, and alleviation of inflammation and mitochondrial dysfunction in the hippocampus","volume":"69","author":"Kodali","year":"2018","journal-title":"Brain Behav. Immunity"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"101389","DOI":"10.1016\/j.redox.2019.101389","article-title":"Redox Biology Monosodium luminol reinstates redox homeostasis, improves cognition, mood and neurogenesis, and alleviates neuro- and systemic inflammation in a model of Gulf War Illness","volume":"28","author":"Shetty","year":"2020","journal-title":"Redox Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"696","DOI":"10.5966\/sctm.2012-0050","article-title":"Neural stem cell grafting counteracts hippocampal injury-mediated impairments in mood, memory, and neurogenesis","volume":"9","author":"Hattiangady","year":"2012","journal-title":"Stem Cell. Transl. Med."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/1\/181\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:45:50Z","timestamp":1760190350000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/1\/181"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,26]]},"references-count":56,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,1]]}},"alternative-id":["ijms21010181"],"URL":"https:\/\/doi.org\/10.3390\/ijms21010181","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,26]]}}}