{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T04:26:22Z","timestamp":1780633582057,"version":"3.54.1"},"reference-count":71,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,11,30]],"date-time":"2024-11-30T00:00:00Z","timestamp":1732924800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,11,30]],"date-time":"2024-11-30T00:00:00Z","timestamp":1732924800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100006942","name":"Medical University of South Carolina","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100006942","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Neurochem Res"],"published-print":{"date-parts":[[2025,2]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:p>Spinal cord injury (SCI) is a complex debilitating condition leading to permanent life-long neurological deficits. Estrogen (E2) treatment is known to be neuroprotectant in SCI. This hormone is highly pleiotropic and has been shown to decrease apoptosis, modulate calcium signaling, regulate growth factor expression, act as an anti-inflammatory, and drive angiogenesis. These beneficial effects were found in our earlier study at the low dose of 10\u00a0\u00b5g\/kg E2 in rats. However, the dose remains non-physiologic, which poses a safety hurdle for clinical use. Thus, we recently devised\/constructed a fast release nanoparticle (NP) estrogen embedded (FNP-E2) construct and tested a focal delivery system in a contused SCI rat model which showed protection in the short run. In the current study, we have developed a novel slow-release NP estrogen (SNP-E2) delivery system that shows sustained release of E2 in the injured spinal cord and no systemic exposure in the host. The study of E2 release and kinetics of this SNP-E2 construct in vitro and in vivo supported this claim. Delivery of E2 to the injured spinal cord via this approach reduced inflammation and gliosis, and induced microglial differentiation of M1 to M2 in rats after SCI. Analysis of spinal cord samples showed improved myelination and survival signals (AKT) as demonstrated by western blot analysis. SNP-E2 treatment also induced astrocytic differentiation into neuron-like (MAP2\/NeuN) cells, supported the survival of oligodendrocyte precursor cells (OPC), and improved bladder and locomotor function in rats following SCI. These data suggest that this novel delivery strategy of SNP-E2 to the injured spinal cord may provide a safe and effective therapeutic approach to treat individuals suffering from SCI.<\/jats:p>","DOI":"10.1007\/s11064-024-04289-4","type":"journal-article","created":{"date-parts":[[2024,11,30]],"date-time":"2024-11-30T02:08:53Z","timestamp":1732932533000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Induction of Neural Differentiation and Protection by a Novel Slow-Release Nanoparticle Estrogen Construct in a Rat Model of Spinal Cord Injury"],"prefix":"10.1007","volume":"50","author":[{"given":"Azizul","family":"Haque","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vandana","family":"Zaman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kelsey P.","family":"Drasites","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Denise","family":"Matzelle","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sushant","family":"Sawant","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexey","family":"Vertegel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abhay","family":"Varma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Naren L.","family":"Banik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,11,30]]},"reference":[{"key":"4289_CR1","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1016\/j.pmr.2007.07.010","volume":"18","author":"F Branco","year":"2007","unstructured":"Branco F, Cardenas DD, Svircev JN (2007) Spinal cord injury: a comprehensive review. Phys Med Rehabil Clin N Am 18:651\u2013679 v","journal-title":"Phys Med Rehabil Clin N Am"},{"key":"4289_CR2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3171\/2018.9.SPINE18682","volume":"30","author":"JH Badhiwala","year":"2018","unstructured":"Badhiwala JH, Ahuja CS, Fehlings MG (2018) Time is spine: a review of translational advances in spinal cord injury. J Neurosurg Spine 30:1\u201318","journal-title":"J Neurosurg Spine"},{"key":"4289_CR3","doi-asserted-by":"crossref","first-page":"698736","DOI":"10.3389\/fsurg.2021.698736","volume":"8","author":"TY Wang","year":"2021","unstructured":"Wang TY, Park C, Zhang H, Rahimpour S, Murphy KR, Goodwin CR, Karikari IO, Than KD, Shaffrey CI, Foster N, Abd-El-Barr MM (2021) Management of Acute traumatic spinal cord Injury: a review of the literature. Front Surg 8:698736","journal-title":"Front Surg"},{"key":"4289_CR4","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1016\/j.nec.2021.03.003","volume":"32","author":"AF Haddad","year":"2021","unstructured":"Haddad AF, Burke JF, Dhall SS (2021) The natural history of spinal cord Injury. Neurosurg Clin N Am 32:315\u2013321","journal-title":"Neurosurg Clin N Am"},{"key":"4289_CR5","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1007\/BF02834292","volume":"7","author":"NL Banik","year":"1987","unstructured":"Banik NL, Hogan EL, Hsu CY (1987) The multimolecular cascade of spinal cord injury. Studies on prostanoids, calcium, and proteinases. Neurochem Pathol 7:57\u201377","journal-title":"Neurochem Pathol"},{"key":"4289_CR6","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1038\/s41392-023-01477-6","volume":"8","author":"X Hu","year":"2023","unstructured":"Hu X, Xu W, Ren Y, Wang Z, He X, Huang R, Ma B, Zhao J, Zhu R, Cheng L (2023) Spinal cord injury: molecular mechanisms and therapeutic interventions. Signal Transduct Target Ther 8:245","journal-title":"Signal Transduct Target Ther"},{"key":"4289_CR7","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1089\/neu.2020.7473","volume":"38","author":"S Kirshblum","year":"2021","unstructured":"Kirshblum S, Snider B, Eren F, Guest J (2021) Characterizing natural recovery after traumatic spinal cord Injury. J Neurotrauma 38:1267\u20131284","journal-title":"J Neurotrauma"},{"key":"4289_CR8","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3389\/fnsys.2019.00037","volume":"13","author":"E Akhmetzyanova","year":"2019","unstructured":"Akhmetzyanova E, Kletenkov K, Mukhamedshina Y, Rizvanov A (2019) Different approaches to modulation of Microglia Phenotypes after spinal cord Injury. Front Syst Neurosci 13:37","journal-title":"Front Syst Neurosci"},{"key":"4289_CR9","doi-asserted-by":"crossref","first-page":"815347","DOI":"10.3389\/fnagi.2022.815347","volume":"14","author":"S Guo","year":"2022","unstructured":"Guo S, Wang H, Yin Y (2022) Microglia polarization from M1 to M2 in neurodegenerative diseases. Front Aging Neurosci 14:815347","journal-title":"Front Aging Neurosci"},{"key":"4289_CR10","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1186\/1742-2094-11-98","volume":"11","author":"JD Cherry","year":"2014","unstructured":"Cherry JD, Olschowka JA, O\u2019Banion MK (2014) Neuroinflammation and M2 microglia: the good, the bad, and the inflamed. J Neuroinflammation 11:98","journal-title":"J Neuroinflammation"},{"key":"4289_CR11","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1097\/BRS.0000000000000297","volume":"39","author":"GD Schroeder","year":"2014","unstructured":"Schroeder GD, Kwon BK, Eck JC, Savage JW, Hsu WK, Patel AA (2014) Survey of Cervical Spine Research Society members on the use of high-dose steroids for acute spinal cord injuries. Spine 39:971\u2013977","journal-title":"Spine"},{"key":"4289_CR12","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1097\/PEC.0b013e3182724434","volume":"28","author":"K Breslin","year":"2012","unstructured":"Breslin K, Agrawal D (2012) The use of methylprednisolone in acute spinal cord injury: a review of the evidence, controversies, and recommendations. Pediatr Emerg Care 28:1238\u20131245 quiz 1246\u2013\u20091238","journal-title":"Pediatr Emerg Care"},{"key":"4289_CR13","first-page":"CD001046","volume":"1","author":"MB Bracken","year":"2012","unstructured":"Bracken MB (2012) Steroids for acute spinal cord injury. Cochrane Database Syst Rev 1:CD001046","journal-title":"Cochrane Database Syst Rev"},{"key":"4289_CR14","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1111\/j.1749-6632.2003.tb07521.x","volume":"993","author":"EA Sribnick","year":"2003","unstructured":"Sribnick EA, Wingrave JM, Matzelle DD, Ray SK, Banik NL (2003) Estrogen as a neuroprotective agent in the treatment of spinal cord injury. Ann N Y Acad Sci 993:125\u2013133 discussion 159\u2013160","journal-title":"Ann N Y Acad Sci"},{"key":"4289_CR15","doi-asserted-by":"crossref","first-page":"1064","DOI":"10.1111\/jnc.13464","volume":"136","author":"S Samantaray","year":"2016","unstructured":"Samantaray S, Das A, Matzelle DC, Yu SP, Wei L, Varma A, Ray SK, Banik NL (2016) Administration of low dose estrogen attenuates gliosis and protects neurons in acute spinal cord injury in rats. J Neurochem 136:1064\u20131073","journal-title":"J Neurochem"},{"key":"4289_CR16","doi-asserted-by":"crossref","first-page":"2007","DOI":"10.1007\/s11064-004-6874-0","volume":"29","author":"EA Sribnick","year":"2004","unstructured":"Sribnick EA, Ray SK, Banik NL (2004) Estrogen as a multi-active neuroprotective agent in traumatic injuries. Neurochem Res 29:2007\u20132014","journal-title":"Neurochem Res"},{"key":"4289_CR17","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1111\/j.1749-6632.2009.05357.x","volume":"1199","author":"S Samantaray","year":"2010","unstructured":"Samantaray S, Sribnick EA, Das A, Thakore NP, Matzelle D, Yu SP, Ray SK, Wei L, Banik NL (2010) Neuroprotective efficacy of estrogen in experimental spinal cord injury in rats. Ann N Y Acad Sci 1199:90\u201394","journal-title":"Ann N Y Acad Sci"},{"key":"4289_CR18","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.expneurol.2014.01.008","volume":"259","author":"S Elkabes","year":"2014","unstructured":"Elkabes S, Nicot AB (2014) Sex steroids and neuroprotection in spinal cord injury: a review of preclinical investigations. Exp Neurol 259:28\u201337","journal-title":"Exp Neurol"},{"key":"4289_CR19","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1007\/s12031-013-0137-y","volume":"52","author":"P Habib","year":"2014","unstructured":"Habib P, Slowik A, Zendedel A, Johann S, Dang J, Beyer C (2014) Regulation of hypoxia-induced inflammatory responses and M1-M2 phenotype switch of primary rat microglia by sex steroids. J Mol Neuroscience: MN 52:277\u2013285","journal-title":"J Mol Neuroscience: MN"},{"key":"4289_CR20","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1089\/neu.2014.3730","volume":"32","author":"A Cox","year":"2015","unstructured":"Cox A, Varma A, Barry J, Vertegel A, Banik N (2015) Nanoparticle estrogen in rat spinal cord Injury elicits Rapid Anti-inflammatory effects in plasma, Cerebrospinal Fluid, and tissue. J Neurotrauma 32:1413\u20131421","journal-title":"J Neurotrauma"},{"key":"4289_CR21","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1097\/SHK.0b013e31814545dc","volume":"29","author":"S Cuzzocrea","year":"2008","unstructured":"Cuzzocrea S, Genovese T, Mazzon E, Esposito E, Di Paola R, Muia C, Crisafulli C, Peli A, Bramanti P, Chaudry IH (2008) Effect of 17beta-estradiol on signal transduction pathways and secondary damage in experimental spinal cord trauma. Shock 29:362\u2013371","journal-title":"Shock"},{"key":"4289_CR22","doi-asserted-by":"crossref","first-page":"1738","DOI":"10.1002\/jnr.22337","volume":"88","author":"EA Sribnick","year":"2010","unstructured":"Sribnick EA, Samantaray S, Das A, Smith J, Matzelle DD, Ray SK, Banik NL (2010) Postinjury estrogen treatment of chronic spinal cord injury improves locomotor function in rats. J Neurosci Res 88:1738\u20131750","journal-title":"J Neurosci Res"},{"key":"4289_CR23","doi-asserted-by":"crossref","first-page":"1531","DOI":"10.1089\/neu.2013.2854","volume":"30","author":"NL Day","year":"2013","unstructured":"Day NL, Floyd CL, D\u2019Alessandro TL, Hubbard WJ, Chaudry IH (2013) 17beta-estradiol confers protection after traumatic brain injury in the rat and involves activation of G protein-coupled estrogen receptor 1. J Neurotrauma 30:1531\u20131541","journal-title":"J Neurotrauma"},{"key":"4289_CR24","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.brainres.2012.04.024","volume":"1461","author":"AA Ardelt","year":"2012","unstructured":"Ardelt AA, Carpenter RS, Lobo MR, Zeng H, Solanki RB, Zhang A, Kulesza P, Pike MM (2012) Estradiol modulates post-ischemic cerebral vascular remodeling and improves long-term functional outcome in a rat model of stroke. Brain Res 1461:76\u201386","journal-title":"Brain Res"},{"key":"4289_CR25","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1001\/jama.2011.382","volume":"305","author":"AZ LaCroix","year":"2011","unstructured":"LaCroix AZ, Chlebowski RT, Manson JE, Aragaki AK, Johnson KC, Martin L, Margolis KL, Stefanick ML, Brzyski R, Curb JD, Howard BV, Lewis CE, Wactawski-Wende J, Investigators WHI (2011) Health outcomes after stopping conjugated equine estrogens among postmenopausal women with prior hysterectomy: a randomized controlled trial. JAMA 305:1305\u20131314","journal-title":"JAMA"},{"key":"4289_CR26","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/S0010-7824(01)00307-9","volume":"65","author":"O Lidegaard","year":"2002","unstructured":"Lidegaard O, Edstrom B, Kreiner S (2002) Oral contraceptives and venous thromboembolism: a five-year national case-control study. Contraception 65:187\u2013196","journal-title":"Contraception"},{"key":"4289_CR27","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1007\/s11064-011-0498-y","volume":"36","author":"S Samantaray","year":"2011","unstructured":"Samantaray S, Smith JA, Das A, Matzelle DD, Varma AK, Ray SK, Banik NL (2011) Low dose estrogen prevents neuronal degeneration and microglial reactivity in an acute model of spinal cord injury: effect of dosing, route of administration, and therapy delay. Neurochem Res 36:1809\u20131816","journal-title":"Neurochem Res"},{"key":"4289_CR28","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1111\/jnc.13610","volume":"137","author":"S Samantaray","year":"2016","unstructured":"Samantaray S, Das A, Matzelle DC, Yu SP, Wei L, Varma A, Ray SK, Banik NL (2016) Administration of low dose estrogen attenuates persistent inflammation, promotes angiogenesis, and improves locomotor function following chronic spinal cord injury in rats. J Neurochem 137:604\u2013617","journal-title":"J Neurochem"},{"key":"4289_CR29","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1089\/neu.2020.7047","volume":"38","author":"A Cox","year":"2021","unstructured":"Cox A, Capone M, Matzelle D, Vertegel A, Bredikhin M, Varma A, Haque A, Shields DC, Banik NL (2021) Nanoparticle-based estrogen delivery to spinal cord Injury Site reduces local Parenchymal Destruction and improves functional recovery. J Neurotrauma 38:342\u2013352","journal-title":"J Neurotrauma"},{"key":"4289_CR30","doi-asserted-by":"crossref","first-page":"2979","DOI":"10.1007\/s11064-021-03401-2","volume":"46","author":"A Haque","year":"2021","unstructured":"Haque A, Drasites KP, Cox A, Capone M, Myatich AI, Shams R, Matzelle D, Garner DP, Bredikhin M, Shields DC, Vertegel A, Banik NL (2021) Protective effects of Estrogen via Nanoparticle Delivery to attenuate myelin loss and neuronal death after spinal cord Injury. Neurochem Res 46:2979\u20132990","journal-title":"Neurochem Res"},{"key":"4289_CR31","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.4103\/1673-5374.165213","volume":"10","author":"JP Datto","year":"2015","unstructured":"Datto JP, Yang J, Dietrich WD, Pearse DD (2015) Does being female provide a neuroprotective advantage following spinal cord injury? Neural Regeneration Res 10:1533\u20131536","journal-title":"Neural Regeneration Res"},{"key":"4289_CR32","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1002\/jnr.20622","volume":"82","author":"EA Sribnick","year":"2005","unstructured":"Sribnick EA, Wingrave JM, Matzelle DD, Wilford GG, Ray SK, Banik NL (2005) Estrogen attenuated markers of inflammation and decreased lesion volume in acute spinal cord injury in rats. J Neurosci Res 82:283\u2013293","journal-title":"J Neurosci Res"},{"key":"4289_CR33","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1089\/cns.1987.4.149","volume":"4","author":"PL Perot Jr","year":"1987","unstructured":"Perot PL Jr., Lee WA, Hsu CY, Hogan EL, Cox RD, Gross AJ (1987) Therapeutic model for experimental spinal cord injury in the rat: I. Mortality and motor deficit. Cent Nerv Syst Trauma 4:149\u2013159","journal-title":"Cent Nerv Syst Trauma"},{"key":"4289_CR34","doi-asserted-by":"crossref","unstructured":"Haque A, Das A, Samantaray S, Matzelle D, Capone M, Wallace G, Husarik AN, Taheri S, Reiter RJ, Varma A, Ray SK, Banik NL (2022) Premarin reduces neurodegeneration and promotes improvement of function in an animal model of spinal cord Injury. Int J Mol Sci 23(4):2384","DOI":"10.3390\/ijms23042384"},{"key":"4289_CR35","doi-asserted-by":"crossref","first-page":"104788","DOI":"10.1016\/j.neuint.2020.104788","volume":"139","author":"R Polcyn","year":"2020","unstructured":"Polcyn R, Capone M, Matzelle D, Hossain A, Chandran R, Banik NL, Haque A (2020) Enolase inhibition alters metabolic hormones and inflammatory factors to promote neuroprotection in spinal cord injury. Neurochem Int 139:104788","journal-title":"Neurochem Int"},{"key":"4289_CR36","doi-asserted-by":"crossref","first-page":"505103","DOI":"10.1088\/0957-4484\/22\/50\/505103","volume":"22","author":"R Satishkumar","year":"2011","unstructured":"Satishkumar R, Vertegel AA (2011) Antibody-directed targeting of lysostaphin adsorbed onto polylactide nanoparticles increases its antimicrobial activity against S. Aureus in vitro. Nanotechnology 22:505103","journal-title":"Nanotechnology"},{"key":"4289_CR37","doi-asserted-by":"crossref","first-page":"265103","DOI":"10.1088\/0957-4484\/21\/26\/265103","volume":"21","author":"VD Maximov","year":"2010","unstructured":"Maximov VD, Reukov VV, Barry JN, Cochrane C, Vertegel AA (2010) Protein-nanoparticle conjugates as potential therapeutic agents for the treatment of hyperlipidemia. Nanotechnology 21:265103","journal-title":"Nanotechnology"},{"key":"4289_CR38","doi-asserted-by":"crossref","first-page":"2602","DOI":"10.1021\/acs.chemrev.5b00346","volume":"116","author":"N Kamaly","year":"2016","unstructured":"Kamaly N, Yameen B, Wu J, Farokhzad OC (2016) Degradable controlled-release polymers and polymeric nanoparticles: mechanisms of Controlling Drug Release. Chem Rev 116:2602\u20132663","journal-title":"Chem Rev"},{"key":"4289_CR39","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1186\/s12951-016-0238-1","volume":"15","author":"CM da Luz","year":"2017","unstructured":"da Luz CM, Boyles MS, Falagan-Lotsch P, Pereira MR, Tutumi HR, de Oliveira Santos E, Martins NB, Himly M, Sommer A, Foissner I, Duschl A, Granjeiro JM, Leite PE (2017) Poly-lactic acid nanoparticles (PLA-NP) promote physiological modifications in lung epithelial cells and are internalized by clathrin-coated pits and lipid rafts. J Nanobiotechnol 15:11","journal-title":"J Nanobiotechnol"},{"key":"4289_CR40","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1084\/jem.20011853","volume":"195","author":"MA Haque","year":"2002","unstructured":"Haque MA, Li P, Jackson SK, Zarour HM, Hawes JW, Phan UT, Maric M, Cresswell P, Blum JS (2002) Absence of gamma-interferon-inducible lysosomal thiol reductase in melanomas disrupts T cell recognition of select immunodominant epitopes. J Exp Med 195:1267\u20131277","journal-title":"J Exp Med"},{"key":"4289_CR41","doi-asserted-by":"crossref","first-page":"731","DOI":"10.4049\/jimmunol.173.2.731","volume":"173","author":"PW O\u2019Donnell","year":"2004","unstructured":"O\u2019Donnell PW, Haque A, Klemsz MJ, Kaplan MH, Blum JS (2004) Cutting edge: induction of the antigen-processing enzyme IFN-gamma-inducible lysosomal thiol reductase in melanoma cells is STAT1-dependent but CIITA-independent. J Immunol 173:731\u2013735","journal-title":"J Immunol"},{"key":"4289_CR42","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1007\/s00262-006-0219-6","volume":"56","author":"A Haque","year":"2007","unstructured":"Haque A, Das A, Hajiaghamohseni LM, Younger A, Banik NL, Ray SK (2007) Induction of apoptosis and immune response by all-trans retinoic acid plus interferon-gamma in human malignant glioblastoma T98G and U87MG cells. Cancer Immunol Immunother 56:615\u2013625","journal-title":"Cancer Immunol Immunother"},{"key":"4289_CR43","doi-asserted-by":"crossref","first-page":"2212","DOI":"10.1002\/jcb.26383","volume":"119","author":"JD Hathaway-Schrader","year":"2018","unstructured":"Hathaway-Schrader JD, Doonan BP, Hossain A, Radwan FFY, Zhang L, Haque A (2018) Autophagy-dependent crosstalk between GILT and PAX-3 influences radiation sensitivity of human melanoma cells. J Cell Biochem 119:2212\u20132221","journal-title":"J Cell Biochem"},{"key":"4289_CR44","doi-asserted-by":"crossref","first-page":"2777","DOI":"10.1007\/s11064-017-2291-z","volume":"42","author":"A Haque","year":"2017","unstructured":"Haque A, Capone M, Matzelle D, Cox A, Banik NL (2017) Targeting enolase in reducing secondary damage in Acute spinal cord Injury in rats. Neurochem Res 42:2777\u20132787","journal-title":"Neurochem Res"},{"key":"4289_CR45","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.4049\/jimmunol.1402382","volume":"194","author":"JM God","year":"2015","unstructured":"God JM, Cameron C, Figueroa J, Amria S, Hossain A, Kempkes B, Bornkamm GW, Stuart RK, Blum JS, Haque A (2015) Elevation of c-MYC disrupts HLA class II-mediated immune recognition of human B cell tumors. J Immunol 194:1434\u20131445","journal-title":"J Immunol"},{"key":"4289_CR46","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1016\/j.cellimm.2011.08.007","volume":"271","author":"D Zhao","year":"2011","unstructured":"Zhao D, Amria S, Hossain A, Sundaram K, Komlosi P, Nagarkatti M, Haque A (2011) Enhancement of HLA class II-restricted CD4\u2009+\u2009T cell recognition of human melanoma cells following treatment with bryostatin-1. Cell Immunol 271:392\u2013400","journal-title":"Cell Immunol"},{"key":"4289_CR47","doi-asserted-by":"crossref","first-page":"305","DOI":"10.3109\/10428194.2011.615423","volume":"53","author":"FF Radwan","year":"2012","unstructured":"Radwan FF, Zhang L, Hossain A, Doonan BP, God JM, Haque A (2012) Mechanisms regulating enhanced human leukocyte antigen class II-mediated CD4\u2009+\u2009T cell recognition of human B-cell lymphoma by resveratrol. Leuk Lymphoma 53:305\u2013314","journal-title":"Leuk Lymphoma"},{"key":"4289_CR48","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.1007\/s00262-008-0483-8","volume":"57","author":"OG Goldstein","year":"2008","unstructured":"Goldstein OG, Hajiaghamohseni LM, Amria S, Sundaram K, Reddy SV, Haque A (2008) Gamma-IFN-inducible-lysosomal thiol reductase modulates acidic proteases and HLA class II antigen processing in melanoma. Cancer Immunol Immunotherapy: CII 57:1461\u20131470","journal-title":"Cancer Immunol Immunotherapy: CII"},{"key":"4289_CR49","doi-asserted-by":"crossref","first-page":"7174","DOI":"10.1523\/JNEUROSCI.0150-08.2008","volume":"28","author":"AI Flores","year":"2008","unstructured":"Flores AI, Narayanan SP, Morse EN, Shick HE, Yin X, Kidd G, Avila RL, Kirschner DA, Macklin WB (2008) Constitutively active akt induces enhanced myelination in the CNS. J Neuroscience: Official J Soc Neurosci 28:7174\u20137183","journal-title":"J Neuroscience: Official J Soc Neurosci"},{"key":"4289_CR50","doi-asserted-by":"crossref","first-page":"113881","DOI":"10.1016\/j.biopha.2022.113881","volume":"156","author":"CL Xiao","year":"2022","unstructured":"Xiao CL, Yin WC, Zhong YC, Luo JQ, Liu LL, Liu WY, Zhao K (2022) The role of PI3K\/Akt signalling pathway in spinal cord injury. Biomed Pharmacother 156:113881","journal-title":"Biomed Pharmacother"},{"key":"4289_CR51","doi-asserted-by":"crossref","first-page":"3338","DOI":"10.1038\/ncomms4338","volume":"5","author":"Z Su","year":"2014","unstructured":"Su Z, Niu W, Liu ML, Zou Y, Zhang CL (2014) In vivo conversion of astrocytes to neurons in the injured adult spinal cord. Nat Commun 5:3338","journal-title":"Nat Commun"},{"key":"4289_CR52","first-page":"85","volume":"7","author":"WA Taweel","year":"2015","unstructured":"Taweel WA, Seyam R (2015) Neurogenic bladder in spinal cord injury patients. Res Rep Urol 7:85\u201399","journal-title":"Res Rep Urol"},{"key":"4289_CR53","doi-asserted-by":"crossref","first-page":"57","DOI":"10.12998\/wjcc.v11.i1.57","volume":"11","author":"L Xiang","year":"2023","unstructured":"Xiang L, Li H, Xie QQ, Siau CS, Xie Z, Zhu MT, Zhou B, Li ZP, Wang SB (2023) Rehabilitation care of patients with neurogenic bladder after spinal cord injury: a literature review. World J Clin Cases 11:57\u201364","journal-title":"World J Clin Cases"},{"key":"4289_CR54","doi-asserted-by":"crossref","first-page":"114224","DOI":"10.1016\/j.biopha.2023.114224","volume":"159","author":"G Gu","year":"2023","unstructured":"Gu G, Ren J, Zhu B, Shi Z, Feng S, Wei Z (2023) Multiple mechanisms of curcumin targeting spinal cord injury. Biomed Pharmacother 159:114224","journal-title":"Biomed Pharmacother"},{"key":"4289_CR55","doi-asserted-by":"crossref","first-page":"8532","DOI":"10.1523\/JNEUROSCI.0783-21.2021","volume":"41","author":"KN Fedder-Semmes","year":"2021","unstructured":"Fedder-Semmes KN, Appel B (2021) The Akt-mTOR pathway drives myelin sheath growth by regulating Cap-Dependent translation. J Neuroscience: Official J Soc Neurosci 41:8532\u20138544","journal-title":"J Neuroscience: Official J Soc Neurosci"},{"key":"4289_CR56","doi-asserted-by":"crossref","unstructured":"Zhu Z, Yang C, Iyaswamy A, Krishnamoorthi S, Sreenivasmurthy SG, Liu J, Wang Z, Tong BC, Song J, Lu J, Cheung KH, Li M (2019) Balancing mTOR Signaling and Autophagy in the Treatment of Parkinson\u2019s Disease. Int J Mol Sci 20","DOI":"10.3390\/ijms20030728"},{"key":"4289_CR57","doi-asserted-by":"crossref","first-page":"2096","DOI":"10.1002\/glia.24382","volume":"71","author":"N Pukos","year":"2023","unstructured":"Pukos N, Marion CM, Arnold WD, Noble BT, Popovich PG, McTigue DM (2023) Chronic demyelination and myelin repair after spinal cord injury in mice: a potential link for glutamatergic axon activity. Glia 71:2096\u20132116","journal-title":"Glia"},{"key":"4289_CR58","doi-asserted-by":"crossref","unstructured":"Anjum A, Yazid MD, Fauzi Daud M, Idris J, Ng AMH, Selvi Naicker A, Ismail OHR, Athi Kumar RK, Lokanathan Y (2020) Spinal Cord Injury: Pathophysiology, Multimolecular Interactions, and Underlying Recovery Mechanisms. International journal of molecular sciences 21","DOI":"10.3390\/ijms21207533"},{"key":"4289_CR59","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1038\/nature11314","volume":"487","author":"Y Lee","year":"2012","unstructured":"Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443\u2013448","journal-title":"Nature"},{"key":"4289_CR60","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/j.nurt.2010.05.014","volume":"7","author":"ME Lull","year":"2010","unstructured":"Lull ME, Block ML (2010) Microglial activation and chronic neurodegeneration. Neurotherapeutics 7:354\u2013365","journal-title":"Neurotherapeutics"},{"key":"4289_CR61","doi-asserted-by":"crossref","first-page":"2401","DOI":"10.2147\/NDT.S169940","volume":"14","author":"Y Zhou","year":"2018","unstructured":"Zhou Y, Li N, Zhu L, Lin Y, Cheng H (2018) The microglial activation profile and associated factors after experimental spinal cord injury in rats. Neuropsychiatr Dis Treat 14:2401\u20132413","journal-title":"Neuropsychiatr Dis Treat"},{"key":"4289_CR62","doi-asserted-by":"crossref","unstructured":"Kalafatakis I, Karagogeos D (2021) Oligodendrocytes and Microglia: Key Players in Myelin Development, Damage and Repair. Biomolecules 11","DOI":"10.3390\/biom11071058"},{"key":"4289_CR63","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.neuint.2006.04.007","volume":"49","author":"RN Saha","year":"2006","unstructured":"Saha RN, Pahan K (2006) Signals for the induction of nitric oxide synthase in astrocytes. Neurochem Int 49:154\u2013163","journal-title":"Neurochem Int"},{"key":"4289_CR64","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1002\/glia.20143","volume":"50","author":"CL Gibson","year":"2005","unstructured":"Gibson CL, Coughlan TC, Murphy SP (2005) Glial nitric oxide and ischemia. Glia 50:417\u2013426","journal-title":"Glia"},{"key":"4289_CR65","doi-asserted-by":"crossref","first-page":"957","DOI":"10.1016\/j.immuni.2017.06.006","volume":"46","author":"SA Liddelow","year":"2017","unstructured":"Liddelow SA, Barres BA (2017) Reactive astrocytes: production, function, and therapeutic potential. Immunity 46:957\u2013967","journal-title":"Immunity"},{"key":"4289_CR66","doi-asserted-by":"crossref","unstructured":"Yang K, Liu Y, Zhang M (2024) The diverse roles of reactive astrocytes in the pathogenesis of amyotrophic lateral sclerosis. Brain Sci 14","DOI":"10.3390\/brainsci14020158"},{"key":"4289_CR67","doi-asserted-by":"crossref","unstructured":"Phatnani H, Maniatis T (2015) Astrocytes in neurodegenerative disease. Cold Spring Harb Perspect Biol 7","DOI":"10.1101\/cshperspect.a020628"},{"key":"4289_CR68","doi-asserted-by":"crossref","first-page":"1702","DOI":"10.4103\/1673-5374.306064","volume":"16","author":"ZB Ding","year":"2021","unstructured":"Ding ZB, Song LJ, Wang Q, Kumar G, Yan YQ, Ma CG (2021) Astrocytes: a double-edged sword in neurodegenerative diseases. Neural Regen Res 16:1702\u20131710","journal-title":"Neural Regen Res"},{"key":"4289_CR69","doi-asserted-by":"crossref","first-page":"94","DOI":"10.31083\/j.fbl2903094","volume":"29","author":"A Bilalova","year":"2024","unstructured":"Bilalova A, Tutova O, Mukhamedshina Y, Rizvanov A (2024) Astrocytes in spinal cord Injury: current opportunities and prospects for directional polarization. Front Biosci (Landmark Ed) 29:94","journal-title":"Front Biosci (Landmark Ed)"},{"key":"4289_CR70","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/s41582-020-00436-x","volume":"17","author":"K Fouad","year":"2021","unstructured":"Fouad K, Popovich PG, Kopp MA, Schwab JM (2021) The neuroanatomical-functional paradox in spinal cord injury. Nat Rev Neurol 17:53\u201362","journal-title":"Nat Rev Neurol"},{"key":"4289_CR71","first-page":"363","volume":"30","author":"O Ozsoy","year":"2012","unstructured":"Ozsoy O, Ozsoy U, Stein G, Semler O, Skouras E, Schempf G, Wellmann K, Wirth F, Angelova S, Ankerne J, Ashrafi M, Schonau E, Papamitsou-Sidoropolou T, Jaminet P, Sarikcioglu L, Irintchev A, Dunlop SA, Angelov DN (2012) Functional deficits and morphological changes in the neurogenic bladder match the severity of spinal cord compression. Restor Neurol Neurosci 30:363\u2013381","journal-title":"Restor Neurol Neurosci"}],"container-title":["Neurochemical Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11064-024-04289-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s11064-024-04289-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s11064-024-04289-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,1]],"date-time":"2025-02-01T12:12:03Z","timestamp":1738411923000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s11064-024-04289-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,30]]},"references-count":71,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2025,2]]}},"alternative-id":["4289"],"URL":"https:\/\/doi.org\/10.1007\/s11064-024-04289-4","relation":{},"ISSN":["0364-3190","1573-6903"],"issn-type":[{"value":"0364-3190","type":"print"},{"value":"1573-6903","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,30]]},"assertion":[{"value":"1 August 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 November 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 November 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 November 2024","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"41"}}