{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T10:46:37Z","timestamp":1787481997977,"version":"build-2736575974"},"reference-count":66,"publisher":"Springer Science and Business Media LLC","issue":"11","license":[{"start":{"date-parts":[[2021,5,13]],"date-time":"2021-05-13T00:00:00Z","timestamp":1620864000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,5,13]],"date-time":"2021-05-13T00:00:00Z","timestamp":1620864000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000026","name":"National Institute on Drug Abuse","doi-asserted-by":"publisher","award":["DA044579, DA039576, DA040537, DA050528, DA047157"],"award-info":[{"award-number":["DA044579, DA039576, DA040537, DA050528, DA047157"]}],"id":[{"id":"10.13039\/100000026","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","award":["MH122235, MH072567"],"award-info":[{"award-number":["MH122235, MH072567"]}],"id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000050","name":"National Heart, Lung, and Blood Institute","doi-asserted-by":"publisher","award":["HL126559"],"award-info":[{"award-number":["HL126559"]}],"id":[{"id":"10.13039\/100000050","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Mol Neurobiol"],"published-print":{"date-parts":[[2021,11]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Maintaining an intact pool of neural progenitor cells (NPCs) is crucial for generating new and functionally active neurons. Methamphetamine (METH) can exacerbate the HIV-induced deficit of adult neurogenesis; however, potential mechanisms of this influence are still poorly understood. In the present study, we present evidence that chronic exposure to METH combined with brain infection by EcoHIV results in enhanced proliferation of NPCs in the subventricular zone (SVZ) in mice. This effect was long-lasting as it was preserved ex vivo in NPCs isolated from the exposed mice over several passages in the absence of additional treatments. Increased proliferation in response to METH plus HIV was associated with dysregulation of cyclin B1 and cyclin D. Transcriptomic studies indicated that 27 out of the top 30 differentially expressed genes in response to METH plus EcoHIV were targets of the forkhead box O transcriptional factor (FOXO) and primarily FOXO3. Additional ex vivo studies and in vitro experiments using human NPCs exposed to METH and infected with HIV revealed upregulation of the CXCL12-CXCR4 axis, leading to activation of downstream pAkt and pErk, the pathways that can phosphorylate FOXO3 and force its exports from the nuclei into the cytoplasm. Indeed, nuclear expulsion of FOXO3 was demonstrated both in mice exposed to METH and infected with EcoHIV and in cell cultures of human NPCs. These results provide novel information that exposure to METH combined with HIV infection can induce aberrant proliferation of SVZ-derived NPCs and identifies CXCL12-CXCR4-Akt-1-mediated phosphorylation of FOXO3 as the mechanism responsible for this effect.<\/jats:p>","DOI":"10.1007\/s12035-021-02407-9","type":"journal-article","created":{"date-parts":[[2021,5,13]],"date-time":"2021-05-13T04:03:00Z","timestamp":1620878580000},"page":"5421-5436","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["Methamphetamine Enhances HIV-Induced Aberrant Proliferation of Neural Progenitor Cells via the FOXO3-Mediated Mechanism"],"prefix":"10.1007","volume":"58","author":[{"given":"Minseon","family":"Park","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Baker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dilraj","family":"Cambow","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danielle","family":"Gogerty","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Rachel","family":"Leda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bridget","family":"Herlihy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darya","family":"Pavlenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Schuyler","family":"Van Den Nieuwenhuizen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4475-2119","authenticated-orcid":false,"given":"Michal","family":"Toborek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,5,13]]},"reference":[{"key":"2407_CR1","doi-asserted-by":"crossref","unstructured":"Volkow N, Chang L, Wang G, Fowler J, Franceschi D, Sedler M, Gatley S, Miller E et al (2001) Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J Neurosci 24:9414\u20139418","DOI":"10.1523\/JNEUROSCI.21-23-09414.2001"},{"key":"2407_CR2","unstructured":"NIDA (https:\/\/www.drugabuse.gov\/publications\/drugfacts\/methamphetamine) Methamphetamine. National Institute on Drug Abuse website. Accessed January 24 2019"},{"issue":"3","key":"2407_CR3","doi-asserted-by":"publisher","first-page":"203","DOI":"10.2190\/DE.43.3.a","volume":"43","author":"DJ Eitle","year":"2013","unstructured":"Eitle DJ, Eitle TM (2013) Methamphetamine use among rural white and native american adolescents: an application of the stress process model. J Drug Educ 43(3):203\u2013221. https:\/\/doi.org\/10.2190\/DE.43.3.a","journal-title":"J Drug Educ"},{"issue":"4","key":"2407_CR4","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1111\/ajr.12331","volume":"25","author":"A Roche","year":"2017","unstructured":"Roche A, McEntee A (2017) Ice and the outback: patterns and prevalence of methamphetamine use in rural Australia. Aust J Rural Health 25(4):200\u2013209. https:\/\/doi.org\/10.1111\/ajr.12331","journal-title":"Aust J Rural Health"},{"key":"2407_CR5","doi-asserted-by":"publisher","first-page":"194","DOI":"10.1007\/s11904-005-0016-4","volume":"2","author":"G Colfax","year":"2005","unstructured":"Colfax G, Shoptaw S (2005) The methamphetamine epidemic: implications for HIV prevention and treatment. Curr HIV\/AIDS Rep 2:194\u2013199","journal-title":"Curr HIV\/AIDS Rep"},{"key":"2407_CR6","doi-asserted-by":"publisher","first-page":"S37","DOI":"10.1097\/01.aids.0000167350.00503.db","volume":"19","author":"DW Purcell","year":"2005","unstructured":"Purcell DW, Moss S, Remien RH, Woods WJ, Parsons JT (2005) Illicit substance use, sexual risk, and HIV-positive gay and bisexual men: differences by serostatus of casual partners. AIDS 19:S37\u2013S47. https:\/\/doi.org\/10.1097\/01.aids.0000167350.00503.db","journal-title":"AIDS"},{"issue":"2","key":"2407_CR7","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1176\/appi.ajp.162.2.361","volume":"162","author":"L Chang","year":"2005","unstructured":"Chang L, Ernst T, Speck O, Grob CS (2005) Additive effects of HIV and chronic methamphetamine use on brain metabolite abnormalities. Am J Psychiatry 162(2):361\u2013369. https:\/\/doi.org\/10.1176\/appi.ajp.162.2.361","journal-title":"Am J Psychiatry"},{"key":"2407_CR8","doi-asserted-by":"publisher","first-page":"612","DOI":"10.1523\/JNEUROSCI.22-03-00612.2002","volume":"3","author":"F Gage","year":"2002","unstructured":"Gage F (2002) Neurogenesis in the adult brain. J Neurosci 3:612\u2013613","journal-title":"J Neurosci"},{"key":"2407_CR9","doi-asserted-by":"publisher","unstructured":"Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D, Kelley KW, James D, Mayer S et al (2018) Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555(7696):377\u2013381. https:\/\/doi.org\/10.1038\/nature25975","DOI":"10.1038\/nature25975"},{"key":"2407_CR10","doi-asserted-by":"publisher","unstructured":"Boldrini M, Fulmore CA, Tartt AN, Simeon LR, Pavlova I, Poposka V, Rosoklija GB, Stankov A et al (2018) Human Hippocampal Neurogenesis Persists throughout Aging. Cell Stem Cell 22(4):589\u2013599.e585. https:\/\/doi.org\/10.1016\/j.stem.2018.03.015","DOI":"10.1016\/j.stem.2018.03.015"},{"key":"2407_CR11","doi-asserted-by":"publisher","unstructured":"Nogueira AB, Nogueira AB, Veiga JCE, Teixeira MJ (2018)\u00a0Letter: Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults.Neurosurgery 83(3):E133\u2013E137. https:\/\/doi.org\/10.1093\/neuros\/nyy252","DOI":"10.1093\/neuros\/nyy252"},{"issue":"4","key":"2407_CR12","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1016\/j.cell.2008.01.033","volume":"132","author":"C Zhao","year":"2008","unstructured":"Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132(4):645\u2013660. https:\/\/doi.org\/10.1016\/j.cell.2008.01.033","journal-title":"Cell"},{"issue":"10","key":"2407_CR13","doi-asserted-by":"publisher","first-page":"1388","DOI":"10.1016\/j.freeradbiomed.2010.02.023","volume":"48","author":"A Banerjee","year":"2010","unstructured":"Banerjee A, Zhang X, Manda KR, Banks WA, Ercal N (2010) HIV proteins (gp120 and Tat) and methamphetamine in oxidative stress-induced damage in the brain: Potential role of the thiol antioxidant N-acetylcysteine amide. Free Radic Biol Med 48(10):1388\u20131398. https:\/\/doi.org\/10.1016\/j.freeradbiomed.2010.02.023","journal-title":"Free Radic Biol Med"},{"key":"2407_CR14","doi-asserted-by":"publisher","unstructured":"Chang SL, Connaghan KP, Wei Y, Li MD (2014) Chapter Thirteen - neuroHIV and use of addictive substances. In: Cui C, Shurtleff D, Harris RA (eds) International Review of Neurobiology, vol 118. Academic Press, pp. 403\u2013440. https:\/\/doi.org\/10.1016\/B978-0-12-801284-0.00013-0","DOI":"10.1016\/B978-0-12-801284-0.00013-0"},{"issue":"17","key":"2407_CR15","doi-asserted-by":"publisher","first-page":"2271","DOI":"10.1097\/QAD.0b013e3282f12f27","volume":"21","author":"I Rothenaigner","year":"2007","unstructured":"Rothenaigner I, Kramer S, Ziegler M, Wolff H, Kleinschmidt A, Brack-Werner R (2007) Long-term HIV-1 infection of neural progenitor populations. AIDS 21(17):2271\u20132281. https:\/\/doi.org\/10.1097\/QAD.0b013e3282f12f27","journal-title":"AIDS"},{"issue":"1","key":"2407_CR16","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1074\/jbc.RA117.000795","volume":"293","author":"M Skowronska","year":"2018","unstructured":"Skowronska M, McDonald M, Velichkovska M, Leda AR, Park M, Toborek M (2018) Methamphetamine increases HIV infectivity in neural progenitor cells. J Biol Chem 293(1):296\u2013311. https:\/\/doi.org\/10.1074\/jbc.RA117.000795","journal-title":"J Biol Chem"},{"key":"2407_CR17","doi-asserted-by":"publisher","unstructured":"Leda AR, Dygert L, Bertrand L, Toborek M (2017) Mouse microsurgery infusion technique for targeted substance delivery into the CNS via the internal carotid artery. J Vis Exp 119. https:\/\/doi.org\/10.3791\/54804","DOI":"10.3791\/54804"},{"key":"2407_CR18","doi-asserted-by":"publisher","first-page":"34111","DOI":"10.1038\/srep34111","volume":"6","author":"M Park","year":"2016","unstructured":"Park M, Levine H, Toborek M (2016) Exercise protects against methamphetamine-induced aberrant neurogenesis. Sci Rep 6:34111. https:\/\/doi.org\/10.1038\/srep34111","journal-title":"Sci Rep"},{"key":"2407_CR19","doi-asserted-by":"publisher","unstructured":"Walker TL, Kempermann G (2014) One mouse, two cultures: isolation and culture of adult neural stem cells from the two neurogenic zones of individual mice. J Vis Exp (84):e51225. https:\/\/doi.org\/10.3791\/51225","DOI":"10.3791\/51225"},{"key":"2407_CR20","doi-asserted-by":"publisher","unstructured":"Salic A, Mitchison TJ (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci 105(7):2415\u20132420. https:\/\/doi.org\/10.1073\/pnas.0712168105","DOI":"10.1073\/pnas.0712168105"},{"issue":"12","key":"2407_CR21","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https:\/\/doi.org\/10.1186\/s13059-014-0550-8","journal-title":"Genome Biol"},{"key":"2407_CR22","doi-asserted-by":"publisher","first-page":"1070","DOI":"10.12688\/f1000research.7035.1","volume":"4","author":"MI Love","year":"2015","unstructured":"Love MI, Anders S, Kim V, Huber W (2015) RNA-Seq workflow: gene-level exploratory analysis and differential expression. F1000Res 4:1070\u20131070. https:\/\/doi.org\/10.12688\/f1000research.7035.1","journal-title":"F1000Res"},{"issue":"5","key":"2407_CR23","doi-asserted-by":"publisher","first-page":"392","DOI":"10.2174\/157016212802138832","volume":"10","author":"IE Cisneros","year":"2012","unstructured":"Cisneros IE, Ghorpade A (2012) HIV-1, Methamphetamine and astrocyte glutamate regulation: combined excitotoxic implications for neuro-AIDS. Curr HIV Res 10(5):392\u2013406. https:\/\/doi.org\/10.2174\/157016212802138832","journal-title":"Curr HIV Res"},{"issue":"3","key":"2407_CR24","doi-asserted-by":"publisher","first-page":"e1","DOI":"10.1042\/bj20130176","volume":"450","author":"G Thiel","year":"2013","unstructured":"Thiel G (2013) How Sox2 maintains neural stem cell identity. Biochem J 450(3):e1\u2013e2. https:\/\/doi.org\/10.1042\/bj20130176","journal-title":"Biochem J"},{"key":"2407_CR25","doi-asserted-by":"publisher","unstructured":"Paik JH, Ding Z, Narurkar R, Ramkissoon S, Muller F, Kamoun WS, Chae SS, Zheng H et al (2009) FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5(5):540\u2013553. https:\/\/doi.org\/10.1016\/j.stem.2009.09.013","DOI":"10.1016\/j.stem.2009.09.013"},{"issue":"4","key":"2407_CR26","doi-asserted-by":"publisher","first-page":"1157","DOI":"10.1111\/j.1471-4159.2009.06043.x","volume":"109","author":"Y Wu","year":"2009","unstructured":"Wu Y, Peng H, Cui M, Whitney NP, Huang Y, Zheng JC (2009) CXCL12 increases human neural progenitor cell proliferation through Akt-1\/FOXO3a signaling pathway. J Neurochem 109(4):1157\u20131167. https:\/\/doi.org\/10.1111\/j.1471-4159.2009.06043.x","journal-title":"J Neurochem"},{"key":"2407_CR27","doi-asserted-by":"publisher","unstructured":"Jiao Y, Song Y, Kou B, Wang R, Liu Z, Huang X, Chen D, Zhang T et al (2012) Primary CXCR4 co-receptor use in acute HIV infection leads to rapid disease progression in the AE subtype. Viral Immunol 25(4):262\u2013267. https:\/\/doi.org\/10.1089\/vim.2012.0035","DOI":"10.1089\/vim.2012.0035"},{"key":"2407_CR28","doi-asserted-by":"publisher","unstructured":"Jo H, Mondal S, Tan D, Nagata E, Takizawa S, Sharma AK, Hou Q, Shanmugasundaram K et al (2012) Small molecule-induced cytosolic activation of protein kinase Akt rescues ischemia-elicited neuronal death. Proc Natl Acad Sci USA 109(26):10581\u201310586. https:\/\/doi.org\/10.1073\/pnas.1202810109","DOI":"10.1073\/pnas.1202810109"},{"key":"2407_CR29","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.bbi.2018.04.018","volume":"71","author":"AR Nookala","year":"2018","unstructured":"Nookala AR, Schwartz DC, Chaudhari NS, Glazyrin A, Stephens EB, Berman NEJ, Kumar A (2018) Methamphetamine augment HIV-1 Tat mediated memory deficits by altering the expression of synaptic proteins and neurotrophic factors. Brain Behav Immun 71:37\u201351. https:\/\/doi.org\/10.1016\/j.bbi.2018.04.018","journal-title":"Brain Behav Immun"},{"key":"2407_CR30","doi-asserted-by":"publisher","unstructured":"Sanchez AB, Varano GP, de Rozieres CM, Maung R, Catalan IC, Dowling CC, Sejbuk NE, Hoefer MM et al (2016) Antiretrovirals, methamphetamine, and HIV-1 envelope protein gp120 compromise neuronal energy homeostasis in association with various degrees of synaptic and neuritic damage. Antimicrob Agents Chemother 60(1):168\u2013179. https:\/\/doi.org\/10.1128\/aac.01632-15","DOI":"10.1128\/aac.01632-15"},{"key":"2407_CR31","doi-asserted-by":"publisher","first-page":"e850","DOI":"10.1038\/cddis.2013.374","volume":"4","author":"A Shah","year":"2013","unstructured":"Shah A, Kumar S, Simon SD, Singh DP, Kumar A (2013) HIV gp120- and methamphetamine-mediated oxidative stress induces astrocyte apoptosis via cytochrome P450 2E1. Cell Death &Amp; Disease 4:e850. https:\/\/doi.org\/10.1038\/cddis.2013.374https:\/\/www.nature.com\/articles\/cddis2013374#supplementary-information","journal-title":"Cell Death &Amp; Disease"},{"key":"2407_CR32","doi-asserted-by":"publisher","unstructured":"Krathwohl MD, Kaiser JL (2004) HIV-1 promotes quiescence in human neural progenitor cells. The J Infect Dis 190(2):216\u2013226. https:\/\/doi.org\/10.1086\/422008","DOI":"10.1086\/422008"},{"issue":"11","key":"2407_CR33","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0111453","volume":"9","author":"OL Bordiuk","year":"2014","unstructured":"Bordiuk OL, Smith K, Morin PJ, Semenov MV (2014) Cell proliferation and neurogenesis in adult mouse brain. PLoS One 9(11):e111453. https:\/\/doi.org\/10.1371\/journal.pone.0111453","journal-title":"PLoS One"},{"issue":"6459","key":"2407_CR34","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1038\/367188a0","volume":"367","author":"SM Toggas","year":"1994","unstructured":"Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367(6459):188\u2013193. https:\/\/doi.org\/10.1038\/367188a0","journal-title":"Nature"},{"issue":"5","key":"2407_CR35","doi-asserted-by":"publisher","first-page":"1693","DOI":"10.1016\/s0002-9440(10)64304-0","volume":"162","author":"BO Kim","year":"2003","unstructured":"Kim BO, Liu Y, Ruan Y, Xu ZC, Schantz L, He JJ (2003) Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am J Pathol 162(5):1693\u20131707. https:\/\/doi.org\/10.1016\/s0002-9440(10)64304-0","journal-title":"Am J Pathol"},{"key":"2407_CR36","doi-asserted-by":"publisher","unstructured":"Jones GJ, Barsby NL, Cohen EA, Holden J, Harris K, Dickie P, Jhamandas J, Power C (2007) HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J Neurosci : the official journal of the Society for Neuroscience 27(14):3703\u20133711. https:\/\/doi.org\/10.1523\/jneurosci.5522-06.2007","DOI":"10.1523\/jneurosci.5522-06.2007"},{"key":"2407_CR37","doi-asserted-by":"publisher","unstructured":"Potash MJ, Chao W, Bentsman G, Paris N, Saini M, Nitkiewicz J, Belem P, Sharer L et al (2005) A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc Natl Acad Sci USA 102(10):3760\u20133765. https:\/\/doi.org\/10.1073\/pnas.0500649102","DOI":"10.1073\/pnas.0500649102"},{"key":"2407_CR38","doi-asserted-by":"publisher","unstructured":"Osborne O, Peyravian N, Nair M, Daunert S, Toborek M (2020) The paradox of HIV blood-brain barrier penetrance and antiretroviral drug delivery deficiencies. Trends Neurosci 43(9):695\u2013708. https:\/\/doi.org\/10.1016\/j.tins.2020.06.007","DOI":"10.1016\/j.tins.2020.06.007"},{"key":"2407_CR39","doi-asserted-by":"publisher","unstructured":"Marcondes MC, Flynn C, Watry DD, Zandonatti M, Fox HS (2010) Methamphetamine increases brain viral load and activates natural killer cells in simian immunodeficiency virus-infected monkeys. Am J Pathol:177. https:\/\/doi.org\/10.2353\/ajpath.2010.090953","DOI":"10.2353\/ajpath.2010.090953"},{"issue":"4","key":"2407_CR40","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1007\/s11481-009-9174-2","volume":"4","author":"A Yadav","year":"2009","unstructured":"Yadav A, Collman RG (2009) CNS inflammation and macrophage\/microglial biology associated with HIV-1 infection. J NeuroImmune Pharmacol 4(4):430\u2013447. https:\/\/doi.org\/10.1007\/s11481-009-9174-2","journal-title":"J NeuroImmune Pharmacol"},{"key":"2407_CR41","doi-asserted-by":"publisher","unstructured":"Ho EL, Ronquillo R, Altmeppen H, Spudich SS, Price RW, Sinclair E (2013) Cellular composition of cerebrospinal fluid in HIV-1 infected and uninfected Subjects. PLoS One 8(6):e66188\u2013e66188. https:\/\/doi.org\/10.1371\/journal.pone.0066188","DOI":"10.1371\/journal.pone.0066188"},{"key":"2407_CR42","doi-asserted-by":"publisher","unstructured":"Ren C, Yin P, Ren N, Wang Z, Wang J, Zhang C, Ge W, Geng D et al (2018) Cerebrospinal fluid-stem cell interactions may pave the path for cell-based therapy in neurological diseases. Stem Cell Res Ther 9(1):66\u201366. https:\/\/doi.org\/10.1186\/s13287-018-0807-3","DOI":"10.1186\/s13287-018-0807-3"},{"key":"2407_CR43","doi-asserted-by":"publisher","unstructured":"Mishra M, Taneja M, Malik S, Khalique H, Seth P (2010) Human immunodeficiency virus type 1 Tat modulates proliferation and differentiation of human neural precursor cells: implication in NeuroAIDS. J Neurovirol 16(5):355\u2013367. https:\/\/doi.org\/10.3109\/13550284.2010.513028","DOI":"10.3109\/13550284.2010.513028"},{"issue":"2","key":"2407_CR44","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1016\/j.cellimm.2011.07.005","volume":"271","author":"J Shi","year":"2011","unstructured":"Shi J, Qin X, Zhao L, Wang G, Liu C (2011) Human immunodeficiency virus type 1 Tat induces B7-H1 expression via ERK\/MAPK signaling pathway. Cell Immunol 271(2):280\u2013285. https:\/\/doi.org\/10.1016\/j.cellimm.2011.07.005","journal-title":"Cell Immunol"},{"issue":"11","key":"2407_CR45","doi-asserted-by":"publisher","first-page":"1953","DOI":"10.1002\/glia.22865","volume":"63","author":"GS Youn","year":"2015","unstructured":"Youn GS, Ju SM, Choi SY, Park J (2015) HDAC6 mediates HIV-1 tat-induced proinflammatory responses by regulating MAPK-NF-kappaB\/AP-1 pathways in astrocytes. Glia 63(11):1953\u20131965. https:\/\/doi.org\/10.1002\/glia.22865","journal-title":"Glia"},{"key":"2407_CR46","doi-asserted-by":"publisher","unstructured":"Cargnello M, Roux PP (2011) Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75(1):50\u201383. https:\/\/doi.org\/10.1128\/mmbr.00031-10","DOI":"10.1128\/mmbr.00031-10"},{"issue":"12","key":"2407_CR47","doi-asserted-by":"publisher","first-page":"1871","DOI":"10.1002\/glia.22403","volume":"60","author":"YK Hahn","year":"2012","unstructured":"Hahn YK, Podhaizer EM, Hauser KF, Knapp PE (2012) HIV-1 alters neural and glial progenitor cell dynamics in the central nervous system: Coordinated response to opiates during maturation. Glia 60(12):1871\u20131887. https:\/\/doi.org\/10.1002\/glia.22403","journal-title":"Glia"},{"key":"2407_CR48","doi-asserted-by":"crossref","unstructured":"Lee M, Wang T, Jang M, Steiner J, Haughey N, Ming G, Song H, Nath A et al (2011) Rescue of adult hippocampal neurogenesis in a mouse model of HIV neurologic disease. Neurobiol Dis 41:678\u2013687","DOI":"10.1016\/j.nbd.2010.12.002"},{"issue":"1","key":"2407_CR49","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1186\/1750-1326-8-22","volume":"8","author":"M Toborek","year":"2013","unstructured":"Toborek M, Seelbach M, Rashid C, Andras I, Chen L, Park M, Esser K (2013) Voluntary exercise protects against methamphetamine-induced oxidative stress in brain microvasculature and disruption of the blood-brain barrier. Mol Neurodegener 8(1):22","journal-title":"Mol Neurodegener"},{"key":"2407_CR50","doi-asserted-by":"publisher","unstructured":"Bertrand L, Dygert L, Toborek M (2017) Induction of ischemic stroke and ischemia-reperfusion in mice using the middle artery occlusion technique and visualization of infarct area. J Vis Exp 120. https:\/\/doi.org\/10.3791\/54805","DOI":"10.3791\/54805"},{"key":"2407_CR51","doi-asserted-by":"publisher","unstructured":"Li\u015bkiewicz A, Przyby\u0142a M, Park M, Li\u015bkiewicz D, Nowacka-Chmielewska M, Ma\u0142ecki A, Barski J, Lewin-Kowalik J et al (2019) Methamphetamine-associated cognitive decline is attenuated by neutralizing IL-1 signaling. Brain Behav Immun 80:247\u2013254. https:\/\/doi.org\/10.1016\/j.bbi.2019.03.016","DOI":"10.1016\/j.bbi.2019.03.016"},{"issue":"2","key":"2407_CR52","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/j.nbd.2009.11.002","volume":"37","author":"SG Kernie","year":"2010","unstructured":"Kernie SG, Parent JM (2010) Forebrain neurogenesis after focal Ischemic and traumatic brain injury. Neurobiol Dis 37(2):267\u2013274. https:\/\/doi.org\/10.1016\/j.nbd.2009.11.002","journal-title":"Neurobiol Dis"},{"issue":"9","key":"2407_CR53","doi-asserted-by":"publisher","first-page":"2361","DOI":"10.1634\/stemcells.2007-0914","volume":"26","author":"L Bernardino","year":"2008","unstructured":"Bernardino L, Agasse F, Silva B, Ferreira R, Grade S, Malva JO (2008) Tumor Necrosis Factor-\u03b1 Modulates Survival, Proliferation, and Neuronal Differentiation in Neonatal Subventricular Zone Cell Cultures. Stem Cells 26(9):2361\u20132371. https:\/\/doi.org\/10.1634\/stemcells.2007-0914","journal-title":"Stem Cells"},{"issue":"8","key":"2407_CR54","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1002\/glia.20665","volume":"56","author":"H Peng","year":"2008","unstructured":"Peng H, Whitney N, Wu Y, Tian C, Dou H, Zhou Y, Zheng J (2008) HIV-1-infected and\/or immune-activated macrophage-secreted TNF-\u03b1 affects human fetal cortical neural progenitor cell proliferation and differentiation. Glia 56(8):903\u2013916. https:\/\/doi.org\/10.1002\/glia.20665","journal-title":"Glia"},{"key":"2407_CR55","doi-asserted-by":"publisher","unstructured":"Williams JL, Holman DW, Klein RS (2014) Chemokines in the balance: maintenance of homeostasis and protection at CNS barriers. Front Cell Neurosci 8(154). https:\/\/doi.org\/10.3389\/fncel.2014.00154","DOI":"10.3389\/fncel.2014.00154"},{"issue":"10","key":"2407_CR56","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1016\/S0166-2236(99)01408-3","volume":"22","author":"RJ Miller","year":"1999","unstructured":"Miller RJ, Meucci O (1999) AIDS and the brain: is there a chemokine connection? Trends Neurosci 22(10):471\u2013479","journal-title":"Trends Neurosci"},{"key":"2407_CR57","doi-asserted-by":"publisher","unstructured":"Ikegawa M, Yuan J, Matsumoto K, Herrmann S, Iwamoto A, Nakamura T, Matsushita S, Kimura T et al (2001) Elevated Plasma Stromal Cell-Derived Factor 1 Protein Level in the Progression of HIV Type 1 Infection\/AIDS. AIDS Res Hum Retrovir 17(7):587\u2013595. https:\/\/doi.org\/10.1089\/088922201300119680","DOI":"10.1089\/088922201300119680"},{"issue":"11","key":"2407_CR58","doi-asserted-by":"publisher","first-page":"875","DOI":"10.1007\/s13238-012-2092-8","volume":"3","author":"H Peng","year":"2012","unstructured":"Peng H, Wu Y, Duan Z, Ciborowski P, Zheng JC (2012) Proteolytic processing of SDF-1alpha by matrix metalloproteinase-2 impairs CXCR4 signaling and reduces neural progenitor cell migration. Protein & cell 3(11):875\u2013882. https:\/\/doi.org\/10.1007\/s13238-012-2092-8","journal-title":"Protein & cell"},{"key":"2407_CR59","doi-asserted-by":"publisher","unstructured":"Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC et al (1999) Akt Promotes Cell Survival by Phosphorylating and Inhibiting a Forkhead Transcription Factor. Cell 96(6):857\u2013868. https:\/\/doi.org\/10.1016\/S0092-8674(00)80595-4","DOI":"10.1016\/S0092-8674(00)80595-4"},{"key":"2407_CR60","doi-asserted-by":"publisher","unstructured":"Renault VM, Rafalski VA, Morgan AA, Salih DAM, Brett JO, Webb AE, Villeda SA, Thekkat PU et al (2009) FoxO3 Regulates Neural Stem Cell Homeostasis. Cell Stem Cell 5(5):527\u2013539. https:\/\/doi.org\/10.1016\/j.stem.2009.09.014","DOI":"10.1016\/j.stem.2009.09.014"},{"key":"2407_CR61","doi-asserted-by":"publisher","unstructured":"Wilk A, Urbanska K, Yang S, Wang JY, Amini S, Del Valle L, Peruzzi F, Meggs L et al (2011) Insulin-like growth factor-I-forkhead box O transcription factor 3a counteracts high glucose\/tumor necrosis factor-\u03b1-mediated neuronal damage: implications for human immunodeficiency virus encephalitis. J Neurosci Res 89(2):183\u2013198. https:\/\/doi.org\/10.1002\/jnr.22542","DOI":"10.1002\/jnr.22542"},{"key":"2407_CR62","doi-asserted-by":"publisher","unstructured":"Waseem NH, Low S, Shah AZ, Avisetti D, Ostergaard P, Simpson M, Niemiec KA, Martin-Martin B et al (2020) Mutations in SPATA13\/ASEF2 cause primary angle closure glaucoma. PLoS Genet 16(4):e1008721. https:\/\/doi.org\/10.1371\/journal.pgen.1008721","DOI":"10.1371\/journal.pgen.1008721"},{"key":"2407_CR63","doi-asserted-by":"publisher","unstructured":"Bal\u00e1zs R, Hack N, J\u2205rgensen OS (1988) Stimulation of the N-methyl-d-aspartate receptor has a trophic effect on differentiating cerebellar granule cells. Neurosci Lett 87(1):80\u201386. https:\/\/doi.org\/10.1016\/0304-3940(88)90149-8","DOI":"10.1016\/0304-3940(88)90149-8"},{"issue":"20","key":"2407_CR64","doi-asserted-by":"publisher","first-page":"8027","DOI":"10.1073\/pnas.87.20.8027","volume":"87","author":"MG Blanton","year":"1990","unstructured":"Blanton MG, Lo Turco JJ, Kriegstein AR (1990) Endogenous neurotransmitter activates N-methyl-D-aspartate receptors on differentiating neurons in embryonic cortex. Proc Natl Acad Sci USA 87(20):8027\u20138030. https:\/\/doi.org\/10.1073\/pnas.87.20.8027","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"2407_CR65","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/0165-3806(90)90258-Z","volume":"51","author":"DE Brenneman","year":"1990","unstructured":"Brenneman DE, Forsythe ID, Nicol T, Nelson PG (1990) N-methyl-d-aspartate receptors influence neuronal survival in developing spinal cord cultures. Dev Brain Res 51(1):63\u201368. https:\/\/doi.org\/10.1016\/0165-3806(90)90258-Z","journal-title":"Dev Brain Res"},{"issue":"5-6","key":"2407_CR66","doi-asserted-by":"publisher","first-page":"528","DOI":"10.1111\/j.1440-1681.2007.04609.x","volume":"34","author":"MA Curtis","year":"2007","unstructured":"Curtis MA, Eriksson PS, Faull RL (2007) Progenitor cells and adult neurogenesis in neurodegenerative diseases and injuries of the basal ganglia. Clin Exp Pharmacol Physiol 34(5-6):528\u2013532. https:\/\/doi.org\/10.1111\/j.1440-1681.2007.04609.x","journal-title":"Clin Exp Pharmacol Physiol"}],"updated-by":[{"DOI":"10.1007\/s12035-021-02577-6","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2021,10,6]],"date-time":"2021-10-06T00:00:00Z","timestamp":1633478400000}}],"container-title":["Molecular Neurobiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12035-021-02407-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s12035-021-02407-9\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12035-021-02407-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,11,17]],"date-time":"2021-11-17T15:14:52Z","timestamp":1637162092000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s12035-021-02407-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,13]]},"references-count":66,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2021,11]]}},"alternative-id":["2407"],"URL":"https:\/\/doi.org\/10.1007\/s12035-021-02407-9","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-107347\/v1","asserted-by":"object"}]},"ISSN":["0893-7648","1559-1182"],"issn-type":[{"value":"0893-7648","type":"print"},{"value":"1559-1182","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,13]]},"assertion":[{"value":"8 December 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 April 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 May 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 October 2021","order":4,"name":"change_date","label":"Change Date","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Correction","order":5,"name":"change_type","label":"Change Type","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"A Correction to this paper has been published:","order":6,"name":"change_details","label":"Change Details","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"https:\/\/doi.org\/10.1007\/s12035-021-02577-6","URL":"https:\/\/doi.org\/10.1007\/s12035-021-02577-6","order":7,"name":"change_details","label":"Change Details","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":"Conflict of interests"}}]}}