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Current Neuropharmacology


ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

General Review Article

Implication of Hippocampal Neurogenesis in Autism Spectrum Disorder: Pathogenesis and Therapeutic Implications

Author(s): Chuanqi Liu, Jiayin Liu, Hong Gong, Tianyao Liu, Xin Li* and Xiaotang Fan*

Volume 21, Issue 11, 2023

Published on: 13 January, 2023

Page: [2266 - 2282] Pages: 17

DOI: 10.2174/1570159X21666221220155455

Price: $65


Autism spectrum disorder (ASD) is a cluster of heterogeneous neurodevelopmental conditions with atypical social communication and repetitive sensory-motor behaviors. The formation of new neurons from neural precursors in the hippocampus has been unequivocally demonstrated in the dentate gyrus of rodents and non-human primates. Accumulating evidence sheds light on how the deficits in the hippocampal neurogenesis may underlie some of the abnormal behavioral phenotypes in ASD. In this review, we describe the current evidence concerning pre-clinical and clinical studies supporting the significant role of hippocampal neurogenesis in ASD pathogenesis, discuss the possibility of improving hippocampal neurogenesis as a new strategy for treating ASD, and highlight the prospect of emerging pro‐neurogenic therapies for ASD.

Keywords: Autism, hippocampus, dentate gyrus, neurogenesis, stem cell, neurodevelopment.

Graphical Abstract
Güeita-Rodríguez, J.; Ogonowska-Slodownik, A.; Morgulec-Adamowicz, N.; Martín-Prades, M.L.; Cuenca-Zaldívar, J.N.; Palacios-Ceña, D. Effects of aquatic therapy for children with autism spectrum disorder on social competence and quality of life: A mixed methods study. Int. J. Environ. Res. Public Health, 2021, 18(6), 3126.
[] [PMID: 33803581]
Hyman, S.L.; Levy, S.E.; Myers, S.M.; Kuo, D.Z.; Apkon, S.; Davidson, L.F.; Ellerbeck, K.A.; Foster, J.E.A.; Noritz, G.H.; Leppert, M.O.C.; Saunders, B.S.; Stille, C.; Yin, L.; Weitzman, C.C.; Childers, D.O., Jr; Levine, J.M.; Peralta-Carcelen, A.M.; Poon, J.K.; Smith, P.J.; Blum, N.J.; Takayama, J.I.; Baum, R.; Voigt, R.G.; Bridgemohan, C. Identification, evaluation, and management of children with autism spectrum disorder. Pediatrics, 2020, 145(1), e20193447.
Loomes, R.; Hull, L.; Mandy, W.P.L. What is the male-to-female ratio in autism spectrum disorder? A systematic review and meta-analysis. J. Am. Acad. Child Adolesc. Psychiatry, 2017, 56(6), 466-474.
[] [PMID: 28545751]
Bai, D.; Yip, B.H.K.; Windham, G.C.; Sourander, A.; Francis, R.; Yoffe, R.; Glasson, E.; Mahjani, B.; Suominen, A.; Leonard, H.; Gissler, M.; Buxbaum, J.D.; Wong, K.; Schendel, D.; Kodesh, A.; Breshnahan, M.; Levine, S.Z.; Parner, E.T.; Hansen, S.N.; Hultman, C.; Reichenberg, A.; Sandin, S. Association of genetic and environmental factors with autism in a 5-country cohort. JAMA Psychiatry, 2019, 76(10), 1035-1043.
[] [PMID: 31314057]
Ecker, C.; Bookheimer, S.Y.; Murphy, D.G.M. Neuroimaging in autism spectrum disorder: Brain structure and function across the lifespan. Lancet Neurol., 2015, 14(11), 1121-1134.
[] [PMID: 25891007]
Ecker, C.; Rocha-Rego, V.; Johnston, P.; Mourao-Miranda, J.; Marquand, A.; Daly, E.M.; Brammer, M.J.; Murphy, C.; Murphy, D.G. Investigating the predictive value of whole-brain structural MR scans in autism: A pattern classification approach. Neuroimage, 2010, 49(1), 44-56.
[] [PMID: 19683584]
Makale, M.T.; McDonald, C.R.; Hattangadi-Gluth, J.A.; Kesari, S. Mechanisms of radiotherapy-associated cognitive disability in patients with brain tumours. Nat. Rev. Neurol., 2017, 13(1), 52-64.
[] [PMID: 27982041]
Goel, V.; Makale, M.; Grafman, J. The hippocampal system mediates logical reasoning about familiar spatial environments. J. Cogn. Neurosci., 2004, 16(4), 654-664.
[] [PMID: 15165354]
Yassa, M.A.; Stark, C.E.L. Pattern separation in the hippocampus. Trends Neurosci., 2011, 34(10), 515-525.
[] [PMID: 21788086]
Zeidman, P.; Maguire, E.A. Anterior hippocampus: The anatomy of perception, imagination and episodic memory. Nat. Rev. Neurosci., 2016, 17(3), 173-182.
[] [PMID: 26865022]
Felix-Ortiz, A.C.; Tye, K.M. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J. Neurosci., 2014, 34(2), 586-595.
[] [PMID: 24403157]
Lavenex, P.; Banta Lavenex, P.; Favre, G. What animals can teach clinicians about the hippocampus. Front Neurol. Neurosci., 2014, 34, 36-50.
[] [PMID: 24777129]
Knickmeyer, R.C.; Gouttard, S.; Kang, C.; Evans, D.; Wilber, K.; Smith, J.K.; Hamer, R.M.; Lin, W.; Gerig, G.; Gilmore, J.H. A structural MRI study of human brain development from birth to 2 years. J. Neurosci., 2008, 28(47), 12176-12182.
[] [PMID: 19020011]
Christensen, D.L.; Baio, J.; Braun, K.V.N.; Bilder, D.; Charles, J.; Constantino, J.N.; Daniels, J.; Durkin, M.S.; Fitzgerald, R.T.; Kurzius-Spencer, M.; Lee, L.C.; Pettygrove, S.; Robinson, C.; Schulz, E.; Wells, C.; Wingate, M.S.; Zahorodny, W.; Yeargin-Allsopp, M. Prevalence and characteristics of autism spectrum disorder among children aged 8 years--autism and developmental disabilities monitoring network, 11 sites, united states, 2012. MMWR Surveill. Summ., 2016, 65(3), 1-23.
[] [PMID: 27031587]
Kempermann, G.; Gage, F.H.; Aigner, L.; Song, H.; Curtis, M.A.; Thuret, S.; Kuhn, H.G.; Jessberger, S.; Frankland, P.W.; Cameron, H.A.; Gould, E.; Hen, R.; Abrous, D.N.; Toni, N.; Schinder, A.F.; Zhao, X.; Lucassen, P.J.; Frisén, J. Human adult neurogenesis: Evidence and remaining questions. Cell Stem Cell, 2018, 23(1), 25-30.
[] [PMID: 29681514]
Mellios, N.; Feldman, D.A.; Sheridan, S.D.; Ip, J.P.K.; Kwok, S.; Amoah, S.K.; Rosen, B.; Rodriguez, B.A.; Crawford, B.; Swaminathan, R.; Chou, S.; Li, Y.; Ziats, M.; Ernst, C.; Jaenisch, R.; Haggarty, S.J.; Sur, M. MeCP2-regulated miRNAs control early human neurogenesis through differential effects on ERK and AKT signaling. Mol. Psychiatry, 2018, 23(4), 1051-1065.
[] [PMID: 28439102]
Peng, L.; Bonaguidi, M.A. Function and dysfunction of adult hippocampal neurogenesis in regeneration and disease. Am. J. Pathol., 2018, 188(1), 23-28.
[] [PMID: 29030053]
Thompson, A.; Boekhoorn, K.; Van Dam, A.M.; Lucassen, P.J. Changes in adult neurogenesis in neurodegenerative diseases: Cause or consequence? Genes Brain Behav., 2008, 7(Suppl. 1), 28-42.
[] [PMID: 18184368]
Zhong, H.; Xiao, R.; Ruan, R.; Liu, H.; Li, X.; Cai, Y.; Zhao, J.; Fan, X. Neonatal curcumin treatment restores hippocampal neurogenesis and improves autism-related behaviors in a mouse model of autism. Psychopharmacology (Berl.), 2020, 237(12), 3539-3552.
[] [PMID: 32803366]
Zhang, R.; Cai, Y.; Xiao, R.; Zhong, H.; Li, X.; Guo, L.; Xu, H.; Fan, X. Human amniotic epithelial cell transplantation promotes neurogenesis and ameliorates social deficits in BTBR mice. Stem Cell Res. Ther., 2019, 10(1), 153.
[] [PMID: 31151403]
Banker, S.M.; Gu, X.; Schiller, D.; Foss-Feig, J.H. Hippocampal contributions to social and cognitive deficits in autism spectrum disorder. Trends Neurosci., 2021, 44(10), 793-807.
[] [PMID: 34521563]
Hochgerner, H.; Zeisel, A.; Lönnerberg, P.; Linnarsson, S. Conserved properties of dentate gyrus neurogenesis across postnatal development revealed by single-cell RNA sequencing. Nat. Neurosci., 2018, 21(2), 290-299.
[] [PMID: 29335606]
Niklison-Chirou, M.V.; Agostini, M.; Amelio, I.; Melino, G. Regulation of adult neurogenesis in mammalian brain. Int. J. Mol. Sci., 2020, 21(14), 4869.
[] [PMID: 32660154]
Covey, M.V.; Loporchio, D.; Buono, K.D.; Levison, S.W. Opposite effect of inflammation on subventricular zone versus hippocampal precursors in brain injury. Ann. Neurol., 2011, 70(4), 616-626.
[] [PMID: 21710624]
Kumari, E.; Velloso, F.J.; Nasuhidehnavi, A.; Somasundaram, A.; Savanur, V.H.; Buono, K.D.; Levison, S.W. Developmental il-6 exposure favors production of pdgf-responsive multipotential progenitors at the expense of neural stem cells and other progenitors. Stem Cell Reports, 2020, 14(5), 861-875.
[] [PMID: 32302560]
Storer, M.A.; Gallagher, D.; Fatt, M.P.; Simonetta, J.V.; Kaplan, D.R.; Miller, F.D. Interleukin-6 regulates adult neural stem cell numbers during normal and abnormal post-natal development. Stem Cell Reports, 2018, 10(5), 1464-1480.
[] [PMID: 29628394]
Nicola, Z.; Fabel, K.; Kempermann, G. Development of the adult neurogenic niche in the hippocampus of mice. Front. Neuroanat., 2015, 9, 53.
[] [PMID: 25999820]
Radic, T.; Frieß, L.; Vijikumar, A.; Jungenitz, T.; Deller, T.; Schwarzacher, S.W. Differential postnatal expression of neuronal maturation markers in the dentate gyrus of mice and rats. Front. Neuroanat., 2017, 11, 104.
[] [PMID: 29184486]
Bonaguidi, M.A.; Wheeler, M.A.; Shapiro, J.S.; Stadel, R.P.; Sun, G.J.; Ming, G.; Song, H. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell, 2011, 145(7), 1142-1155.
[] [PMID: 21664664]
Gao, Z.; Ure, K.; Ables, J.L.; Lagace, D.C.; Nave, K.A.; Goebbels, S.; Eisch, A.J.; Hsieh, J. Neurod1 is essential for the survival and maturation of adult-born neurons. Nat. Neurosci., 2009, 12(9), 1090-1092.
[] [PMID: 19701197]
Lavado, A.; Lagutin, O.V.; Chow, L.M.L.; Baker, S.J.; Oliver, G. Prox1 is required for granule cell maturation and intermediate progenitor maintenance during brain neurogenesis. PLoS Biol., 2010, 8(8), e1000460.
[] [PMID: 20808958]
Zhao, C.; Teng, E.M.; Summers, R.G., Jr; Ming, G.L.; Gage, F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci., 2006, 26(1), 3-11.
[] [PMID: 16399667]
Gros, A.; Veyrac, A.; Laroche, S. Brain and memory: New neurons to remember. Biol. Aujourdhui, 2015, 209(3), 229-248.
[] [PMID: 26820830]
Aimone, J.B.; Li, Y.; Lee, S.W.; Clemenson, G.D.; Deng, W.; Gage, F.H. Regulation and function of adult neurogenesis: from genes to cognition. Physiol. Rev., 2014, 94(4), 991-1026.
[] [PMID: 25287858]
Bath, K.G.; Jing, D.Q.; Dincheva, I.; Neeb, C.C.; Pattwell, S.S.; Chao, M.V.; Lee, F.S.; Ninan, I. BDNF Val66Met impairs fluoxetine-induced enhancement of adult hippocampus plasticity. Neuropsychopharmacology, 2012, 37(5), 1297-1304.
[] [PMID: 22218094]
Luhach, K.; Kulkarni, G.T.; Singh, V.P.; Sharma, B. Vinpocetine amended prenatal valproic acid induced features of ASD possibly by altering markers of neuronal function, inflammation, and oxidative stress. Autism Res., 2021, 14(11), 2270-2286.
[] [PMID: 34415116]
Camuso, S.; La Rosa, P.; Fiorenza, M.T.; Canterini, S. Pleiotropic effects of BDNF on the cerebellum and hippocampus: Implications for neurodevelopmental disorders. Neurobiol. Dis., 2022, 163, 105606.
[] [PMID: 34974125]
Bagheri-Mohammadi, S. Adult neurogenesis and the molecular signalling pathways in brain: The role of stem cells in adult hippocampal neurogenesis. Int. J. Neurosci., 2022, 132(12), 1165-1177.
[PMID: 33350876]
Araki, T.; Ikegaya, Y.; Koyama, R. The effects of microglia‐ and astrocyte‐derived factors on neurogenesis in health and disease. Eur. J. Neurosci., 2021, 54(5), 5880-5901.
[] [PMID: 32920880]
Zonis, S.; Breunig, J.J.; Mamelak, A.; Wawrowsky, K.; Bresee, C.; Ginzburg, N.; Chesnokova, V. Inflammation-induced Gro1 triggers senescence in neuronal progenitors: effects of estradiol. J. Neuroinflammation, 2018, 15(1), 260.
[] [PMID: 30201019]
Liu, X.; Fan, B.; Chopp, M.; Zhang, Z. Epigenetic mechanisms underlying adult post stroke neurogenesis. Int. J. Mol. Sci., 2020, 21(17), 6179.
[] [PMID: 32867041]
Arredondo, S.B.; Guerrero, F.G.; Herrera-Soto, A.; Jensen-Flores, J.; Bustamante, D.B.; Oñate-Ponce, A.; Henny, P.; Varas-Godoy, M.; Inestrosa, N.C.; Varela-Nallar, L. Wnt5a promotes differentiation and development of adult-born neurons in the hippocampus by noncanonical Wnt signaling. Stem Cells, 2020, 38(3), 422-436.
[] [PMID: 31721364]
Huang, E.J.; Reichardt, L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci., 2001, 24(1), 677-736.
[] [PMID: 11520916]
Beckervordersandforth, R.; Zhang, C.L.; Lie, D.C. Transcription-factor-dependent control of adult hippocampal neurogenesis. Cold Spring Harb. Perspect. Biol., 2015, 7(10), a018879.
[] [PMID: 26430216]
Zhong, H.; Rong, J.; Zhu, C.; Liang, M.; Li, Y.; Zhou, R. Epigenetic modifications of gabaergic interneurons contribute to deficits in adult hippocampus neurogenesis and depression-like behavior in prenatally stressed mice. Int. J. Neuropsychopharmacol., 2020, 23(4), 274-285.
[] [PMID: 32211762]
Gómez, R.L.; Edgin, J.O. The extended trajectory of hippocampal development: Implications for early memory development and disorder. Dev. Cogn. Neurosci., 2016, 18, 57-69.
[] [PMID: 26437910]
Aylward, E.H.; Minshew, N.J.; Goldstein, G.; Honeycutt, N.A.; Augustine, A.M.; Yates, K.O.; Barta, P.E.; Pearlson, G.D. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology, 1999, 53(9), 2145-2150.
[] [PMID: 10599796]
Maier, S.; Tebartz van Elst, L.; Beier, D.; Ebert, D.; Fangmeier, T.; Radtke, M.; Perlov, E.; Riedel, A. Increased hippocampal volumes in adults with high functioning autism spectrum disorder and an IQ>100: A manual morphometric study. Psychiatry Res. Neuroimaging, 2015, 234(1), 152-155.
[] [PMID: 26337007]
Sussman, D.; Leung, R.C.; Vogan, V.M.; Lee, W.; Trelle, S.; Lin, S.; Cassel, D.B.; Chakravarty, M.M.; Lerch, J.P.; Anagnostou, E.; Taylor, M.J. The autism puzzle: Diffuse but not pervasive neuroanatomical abnormalities in children with ASD. Neuroimage Clin., 2015, 8, 170-179.
[] [PMID: 26106541]
Trontel, H.; Duffield, T.; Bigler, E.; Froehlich, A.; Prigge, M.; Nielsen, J.; Cooperrider, J.; Cariello, A.; Travers, B.; Anderson, J.; Zielinski, B.; Alexander, A.; Lange, N.; Lainhart, J. Fusiform correlates of facial memory in autism. Behav. Sci. (Basel), 2013, 3(3), 348-371.
[] [PMID: 24761228]
Schumann, C.M.; Hamstra, J.; Goodlin-Jones, B.L.; Lotspeich, L.J.; Kwon, H.; Buonocore, M.H.; Lammers, C.R.; Reiss, A.L.; Amaral, D.G. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J. Neurosci., 2004, 24(28), 6392-6401.
[] [PMID: 15254095]
Richards, R.; Greimel, E.; Kliemann, D.; Koerte, I.K.; Schulte-Körne, G.; Reuter, M.; Wachinger, C. Increased hippocampal shape asymmetry and volumetric ventricular asymmetry in autism spectrum disorder. Neuroimage Clin., 2020, 26, 102207.
[] [PMID: 32092683]
Liu, J.; Okada, N.J.; Cummings, K.K.; Jung, J.; Patterson, G.; Bookheimer, S.Y.; Jeste, S.S.; Dapretto, M. Emerging atypicalities in functional connectivity of language-related networks in young infants at high familial risk for ASD. Dev. Cogn. Neurosci., 2020, 45, 100814.
[] [PMID: 32658762]
Blasi, A.; Lloyd-Fox, S.; Sethna, V.; Brammer, M.J.; Mercure, E.; Murray, L.; Williams, S.C.R.; Simmons, A.; Murphy, D.G.M.; Johnson, M.H. Atypical processing of voice sounds in infants at risk for autism spectrum disorder. Cortex, 2015, 71, 122-133.
[] [PMID: 26200892]
Gaigg, S.B.; Bowler, D.M.; Ecker, C.; Calvo-Merino, B.; Murphy, D.G. Episodic recollection difficulties in asd result from atypical relational encoding: Behavioral and neural evidence. Autism Res., 2015, 8(3), 317-327.
[] [PMID: 25630307]
Rudie, J.D.; Shehzad, Z.; Hernandez, L.M.; Colich, N.L.; Bookheimer, S.Y.; Iacoboni, M.; Dapretto, M. Reduced functional integration and segregation of distributed neural systems underlying social and emotional information processing in autism spectrum disorders. Cereb. Cortex, 2012, 22(5), 1025-1037.
[] [PMID: 21784971]
Williams, R.S.; Hauser, S.L.; Purpura, D.P.; DeLong, G.R.; Swisher, C.N. Autism and mental retardation: Neuropathologic studies performed in four retarded persons with autistic behavior. Arch. Neurol., 1980, 37(12), 749-753.
[] [PMID: 7447762]
Greco, C.M.; Navarro, C.S.; Hunsaker, M.R.; Maezawa, I.; Shuler, J.F.; Tassone, F.; Delany, M.; Au, J.W.; Berman, R.F.; Jin, L.W.; Schumann, C.; Hagerman, P.J.; Hagerman, R.J. Neuropathologic features in the hippocampus and cerebellum of three older men with fragile X syndrome. Mol. Autism, 2011, 2(1), 2.
[] [PMID: 21303513]
Saitoh, O.; Karns, C.M.; Courchesne, E. Development of the hippocampal formation from2 to 42 years: MRI evidence of smaller area dentata in autism. Brain, 2001, 124(7), 1317-1324.
[] [PMID: 11408327]
Groen, W.; Teluij, M.; Buitelaar, J.; Tendolkar, I. Amygdala and hippocampus enlargement during adolescence in autism. J. Am. Acad. Child Adolesc. Psychiatry, 2010, 49(6), 552-560.
[PMID: 20494265]
Wegiel, J.; Kuchna, I.; Nowicki, K.; Imaki, H.; Wegiel, J.; Marchi, E.; Ma, S.Y.; Chauhan, A.; Chauhan, V.; Bobrowicz, T.W.; de Leon, M.; Louis, L.A.S.; Cohen, I.L.; London, E.; Brown, W.T.; Wisniewski, T. The neuropathology of autism: Defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol., 2010, 119(6), 755-770.
[] [PMID: 20198484]
Mazur-Kolecka, B.; Cohen, I.L.; Jenkins, E.C.; Kaczmarski, W.; Flory, M.; Frackowiak, J. Altered development of neuronal progenitor cells after stimulation with autistic blood sera. Brain Res., 2007, 1168, 11-20.
[] [PMID: 17706942]
Mazur-Kolecka, B.; Cohen, I.L.; Jenkins, E.C.; Flory, M.; Merz, G.; Ted Brown, W.; Frackowiak, J. Sera from children with autism alter proliferation of human neuronal progenitor cells exposed to oxidation. Neurotox. Res., 2009, 16(1), 87-95.
[] [PMID: 19526302]
Meyza, K.Z.; Blanchard, D.C. The btbr mouse model of idiopathic autism - current view on mechanisms. Neurosci Biobehav Rev, 2017, 76(Pt A), 99-110.
Stephenson, D.T.; O’Neill, S.M.; Narayan, S.; Tiwari, A.; Arnold, E.; Samaroo, H.D.; Du, F.; Ring, R.H.; Campbell, B.; Pletcher, M.; Vaidya, V.A.; Morton, D. Histopathologic characterization of the BTBR mouse model of autistic-like behavior reveals selective changes in neurodevelopmental proteins and adult hippocampal neurogenesis. Mol. Autism, 2011, 2(1), 7.
[] [PMID: 21575186]
Bjørk, M.H.; Zoega, H.; Leinonen, M.K.; Cohen, J.M.; Dreier, J.W.; Furu, K.; Gilhus, N.E.; Gissler, M.; Hálfdánarson, Ó.; Igland, J.; Sun, Y.; Tomson, T.; Alvestad, S.; Christensen, J. Association of prenatal exposure to antiseizure medication with risk of autism and intellectual disability. JAMA Neurol., 2022, 79(7), 672-681.
[] [PMID: 35639399]
Christensen, J.; Grønborg, T.K.; Sørensen, M.J.; Schendel, D.; Parner, E.T.; Pedersen, L.H.; Vestergaard, M. Prenatal valproate exposure and risk of autism spectrum disorders and childhood autism. JAMA, 2013, 309(16), 1696-1703.
[] [PMID: 23613074]
Watanabe, Y.; Murakami, T.; Kawashima, M.; Hasegawa-Baba, Y.; Mizukami, S.; Imatanaka, N.; Akahori, Y.; Yoshida, T.; Shibutani, M. Maternal exposure to valproic acid primarily targets interneurons followed by late effects on neurogenesis in the hippocampal dentate gyrus in rat offspring. Neurotox. Res., 2017, 31(1), 46-62.
[] [PMID: 27566479]
Mimura, K.; Oga, T.; Sasaki, T.; Nakagaki, K.; Sato, C.; Sumida, K.; Hoshino, K.; Saito, K.; Miyawaki, I.; Suhara, T.; Aoki, I.; Minamimoto, T.; Ichinohe, N. Abnormal axon guidance signals and reduced interhemispheric connection via anterior commissure in neonates of marmoset ASD model. Neuroimage, 2019, 195, 243-251.
[] [PMID: 30953832]
Sawada, K.; Kamiya, S.; Aoki, I. The proliferation of dentate gyrus progenitors in the ferret hippocampus by neonatal exposure to valproic acid. Front. Neurosci., 2021, 15, 736313.
[] [PMID: 34650400]
Wagner, G.C.; Reuhl, K.R.; Cheh, M.; McRae, P.; Halladay, A.K. A new neurobehavioral model of autism in mice: pre- and postnatal exposure to sodium valproate. J. Autism Dev. Disord., 2006, 36(6), 779-793.
[] [PMID: 16609825]
Kataoka, S.; Takuma, K.; Hara, Y.; Maeda, Y.; Ago, Y.; Matsuda, T. Autism-like behaviours with transient histone hyperacetylation in mice treated prenatally with valproic acid. Int. J. Neuropsychopharmacol., 2013, 16(1), 91-103.
[] [PMID: 22093185]
Kim, K.C.; Kim, P.; Go, H.S.; Choi, C.S.; Yang, S.I.; Cheong, J.H.; Shin, C.Y.; Ko, K.H. The critical period of valproate exposure to induce autistic symptoms in Sprague–Dawley rats. Toxicol. Lett., 2011, 201(2), 137-142.
[] [PMID: 21195144]
Luhach, K.; Kulkarni, G.T.; Singh, V.P.; Sharma, B. Attenuation of neurobehavioural abnormalities by papaverine in prenatal valproic acid rat model of ASD. Eur. J. Pharmacol., 2021, 890, 173663.
[] [PMID: 33127361]
Yochum, C.L.; Dowling, P.; Reuhl, K.R.; Wagner, G.C.; Ming, X. VPA-induced apoptosis and behavioral deficits in neonatal mice. Brain Res., 2008, 1203, 126-132.
[] [PMID: 18316065]
Juliandi, B.; Tanemura, K.; Igarashi, K.; Tominaga, T.; Furukawa, Y.; Otsuka, M.; Moriyama, N.; Ikegami, D.; Abematsu, M.; Sanosaka, T.; Tsujimura, K.; Narita, M.; Kanno, J.; Nakashima, K. Reduced adult hippocampal neurogenesis and cognitive impairments following prenatal treatment of the antiepileptic drug valproic acid. Stem Cell Reports, 2015, 5(6), 996-1009.
[] [PMID: 26677766]
Lee, G.A.; Lin, Y.K.; Lai, J.H.; Lo, Y.C.; Yang, Y.C.S.H.; Ye, S.Y.; Lee, C.J.; Wang, C.C.; Chiang, Y.H.; Tseng, S.H. Maternal immune activation causes social behavior deficits and hypomyelination in male rat offspring with an autism-like microbiota profile. Brain Sci., 2021, 11(8), 1085.
[] [PMID: 34439704]
Okano, H.; Takashima, K.; Takahashi, Y.; Ojiro, R.; Tang, Q.; Ozawa, S.; Ogawa, B.; Koyanagi, M.; Maronpot, R.R.; Yoshida, T.; Shibutani, M. Ameliorating effect of continuous alpha-glycosyl isoquercitrin treatment starting from late gestation in a rat autism model induced by postnatal injection of lipopolysaccharides. Chem. Biol. Interact., 2022, 351, 109767.
[] [PMID: 34863679]
Ishizuka, K.; Fujita, Y.; Kawabata, T.; Kimura, H.; Iwayama, Y.; Inada, T.; Okahisa, Y.; Egawa, J.; Usami, M.; Kushima, I.; Uno, Y.; Okada, T.; Ikeda, M.; Aleksic, B.; Mori, D.; Someya, T.; Yoshikawa, T.; Iwata, N.; Nakamura, H.; Yamashita, T.; Ozaki, N. Rare genetic variants in CX3CR1 and their contribution to the increased risk of schizophrenia and autism spectrum disorders. Transl. Psychiatry, 2017, 7(8), e1184.
[] [PMID: 28763059]
Zhan, Y.; Paolicelli, R.C.; Sforazzini, F.; Weinhard, L.; Bolasco, G.; Pagani, F.; Vyssotski, A.L.; Bifone, A.; Gozzi, A.; Ragozzino, D.; Gross, C.T. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci., 2014, 17(3), 400-406.
[] [PMID: 24487234]
Jiang, X.; Xiao, F.; Xu, J. CX3 chemokine receptor 1 defciency leads to reduced dendritic complexity and delayed maturation of newborn neurons in the adult mouse hippocampus. Neural Regen. Res., 2015, 10(5), 772-777.
[] [PMID: 26109952]
Bolós, M.; Perea, J.R.; Terreros-Roncal, J.; Pallas-Bazarra, N.; Jurado-Arjona, J.; Ávila, J.; Llorens-Martín, M. Absence of microglial CX3CR1 impairs the synaptic integration of adult-born hippocampal granule neurons. Brain Behav. Immun., 2018, 68, 76-89.
[] [PMID: 29017970]
Fernández de Cossío, L.; Guzmán, A.; van der Veldt, S.; Luheshi, G.N. Prenatal infection leads to ASD-like behavior and altered synaptic pruning in the mouse offspring. Brain Behav. Immun., 2017, 63, 88-98.
[] [PMID: 27697456]
Lee, J.H.; Espinera, A.R.; Chen, D.; Choi, K.E.; Caslin, A.Y.; Won, S.; Pecoraro, V.; Xu, G.Y.; Wei, L.; Yu, S.P. Neonatal inflammatory pain and systemic inflammatory responses as possible environmental factors in the development of autism spectrum disorder of juvenile rats. J. Neuroinflammation, 2016, 13(1), 109.
[] [PMID: 27184741]
Cole, T.B.; Chang, Y.C.; Dao, K.; Daza, R.; Hevner, R.; Costa, L.G. Developmental exposure to diesel exhaust upregulates transcription factor expression, decreases hippocampal neurogenesis, and alters cortical lamina organization: relevance to neurodevelopmental disorders. J. Neurodev. Disord., 2020, 12(1), 41.
[] [PMID: 33327933]
Wang, T.; Zhang, T.; Sun, L.; Li, W.; Zhang, C.; Yu, L.; Guan, Y. Gestational B-vitamin supplementation alleviates PM2.5-induced autism-like behavior and hippocampal neurodevelopmental impairment in mice offspring. Ecotoxicol. Environ. Saf., 2019, 185, 109686.
[] [PMID: 31546205]
Fu, J.; Gao, J.; Gong, L.; Ma, Y.; Xu, H.; Gu, Z.; Zhu, J.; Fan, X. Silica nanoparticle exposure during the neonatal period impairs hippocampal precursor proliferation and social behavior later in life. Int. J. Nanomedicine, 2018, 13, 3593-3608.
[] [PMID: 29950837]
Boukhris, T.; Sheehy, O.; Mottron, L.; Bérard, A. Antidepressant use during pregnancy and the risk of autism spectrum disorder in children. JAMA Pediatr., 2016, 170(2), 117-124.
[] [PMID: 26660917]
Dragioti, E.; Solmi, M.; Favaro, A.; Fusar-Poli, P.; Dazzan, P.; Thompson, T.; Stubbs, B.; Firth, J.; Fornaro, M.; Tsartsalis, D.; Carvalho, A.F.; Vieta, E.; McGuire, P.; Young, A.H.; Shin, J.I.; Correll, C.U.; Evangelou, E. Association of antidepressant use with adverse health outcomes: A systematic umbrella review. JAMA Psychiatry, 2019, 76(12), 1241-1255.
[] [PMID: 31577342]
Leshem, R.; Bar-Oz, B.; Diav-Citrin, O.; Gbaly, S.; Soliman, J.; Renoux, C.; Matok, I. Selective serotonin reuptake inhibitors (ssris) and serotonin norepinephrine reuptake inhibitors (snris) during pregnancy and the risk for autism spectrum disorder (asd) and attention deficit hyperactivity disorder (adhd) in the offspring: A true effect or a bias? A systematic review & meta-analysis. Curr. Neuropharmacol., 2021, 19(6), 896-906.
[] [PMID: 33655866]
Kim, J.Y.; Son, M.J.; Son, C.Y.; Radua, J.; Eisenhut, M.; Gressier, F.; Koyanagi, A.; Carvalho, A.F.; Stubbs, B.; Solmi, M.; Rais, T.B.; Lee, K.H.; Kronbichler, A.; Dragioti, E.; Shin, J.I.; Fusar-Poli, P. Environmental risk factors and biomarkers for autism spectrum disorder: an umbrella review of the evidence. Lancet Psychiatry, 2019, 6(7), 590-600.
[] [PMID: 31230684]
Mezzacappa, A.; Lasica, P.A.; Gianfagna, F.; Cazas, O.; Hardy, P.; Falissard, B.; Sutter-Dallay, A.L.; Gressier, F. Risk for autism spectrum disorders according to period of prenatal antidepressant exposure: A systematic review and meta-analysis. JAMA Pediatr., 2017, 171(6), 555-563.
[] [PMID: 28418571]
Ames, J.L.; Ladd-Acosta, C.; Fallin, M.D.; Qian, Y.; Schieve, L.A.; DiGuiseppi, C.; Lee, L.C.; Kasten, E.P.; Zhou, G.; Pinto-Martin, J.; Howerton, E.M.; Eaton, C.L.; Croen, L.A. Maternal psychiatric conditions, treatment with selective serotonin reuptake inhibitors, and neurodevelopmental disorders. Biol. Psychiatry, 2021, 90(4), 253-262.
[] [PMID: 34116791]
Zahra, A.; Jiang, J.; Chen, Y.; Long, C.; Yang, L. Memantine rescues prenatal citalopram exposure-induced striatal and social abnormalities in mice. Exp. Neurol., 2018, 307, 145-154.
[] [PMID: 29913137]
Bond, C.M.; Johnson, J.C.; Chaudhary, V.; McCarthy, E.M.; McWhorter, M.L.; Woehrle, N.S. Perinatal fluoxetine exposure results in social deficits and reduced monoamine oxidase gene expression in mice. Brain Res., 2020, 1727, 146282.
[] [PMID: 31170382]
Gemmel, M.; Hazlett, M.; Bögi, E.; De Lacalle, S.; Hill, L.A.; Kokras, N.; Hammond, G.L.; Dalla, C.; Charlier, T.D.; Pawluski, J.L. Perinatal fluoxetine effects on social play, the HPA system, and hippocampal plasticity in pre-adolescent male and female rats: Interactions with pre-gestational maternal stress. Psychoneuroendocrinology, 2017, 84, 159-171.
[] [PMID: 28735226]
Qiu, W.; Go, K.A.; Wen, Y.; Duarte-Guterman, P.; Eid, R.S.; Galea, L.A.M. Maternal fluoxetine reduces hippocampal inflammation and neurogenesis in adult offspring with sex-specific effects of periadolescent oxytocin. Brain Behav. Immun., 2021, 97, 394-409.
[] [PMID: 34174336]
Bonora, E.; Graziano, C.; Minopoli, F.; Bacchelli, E.; Magini, P.; Diquigiovanni, C.; Lomartire, S.; Bianco, F.; Vargiolu, M.; Parchi, P.; Marasco, E.; Mantovani, V.; Rampoldi, L.; Trudu, M.; Parmeggiani, A.; Battaglia, A.; Mazzone, L.; Tortora, G.; Maestrini, E.; Seri, M.; Romeo, G. Maternally inherited genetic variants ofCADPS 2 are present in Autism Spectrum Disorders and Intellectual Disability patients. EMBO Mol. Med., 2014, 6(6), 795-809.
[] [PMID: 24737869]
Sadakata, T.; Washida, M.; Iwayama, Y.; Shoji, S.; Sato, Y.; Ohkura, T.; Katoh-Semba, R.; Nakajima, M.; Sekine, Y.; Tanaka, M.; Nakamura, K.; Iwata, Y.; Tsuchiya, K.J.; Mori, N.; Detera-Wadleigh, S.D.; Ichikawa, H.; Itohara, S.; Yoshikawa, T.; Furuichi, T. Autistic-like phenotypes in Cadps2-knockout mice and aberrant CADPS2 splicing in autistic patients. J. Clin. Invest., 2007, 117(4), 931-943.
[] [PMID: 17380209]
Fujima, S.; Yamaga, R.; Minami, H.; Mizuno, S.; Shinoda, Y.; Sadakata, T.; Abe, M.; Sakimura, K.; Sano, Y.; Furuichi, T. Caps2 deficiency impairs the release of the social peptide oxytocin, as well as oxytocin-associated social behavior. J. Neurosci., 2021, 41(20), 4524-4535.
[] [PMID: 33846232]
Sadakata, T.; Furuichi, T. Ca2+-dependent activator protein for secretion 2 and autistic-like phenotypes. Neurosci. Res., 2010, 67(3), 197-202.
[] [PMID: 20302894]
Yagishita, K.; Suzuki, R.; Mizuno, S.; Katoh-Semba, R.; Sadakata, T.; Sano, Y.; Furuichi, T.; Shinoda, Y. CAPS2 deficiency affects environmental enrichment-induced adult neurogenesis and differentiation/survival of newborn neurons in the hippocampal dentate gyrus. Neurosci. Lett., 2017, 661, 121-125.
[] [PMID: 28963059]
Shinoda, Y.; Sadakata, T.; Nakao, K.; Katoh-Semba, R.; Kinameri, E.; Furuya, A.; Yanagawa, Y.; Hirase, H.; Furuichi, T. Calcium-dependent activator protein for secretion 2 (CAPS2) promotes BDNF secretion and is critical for the development of GABAergic interneuron network. Proc. Natl. Acad. Sci. USA, 2011, 108(1), 373-378.
[] [PMID: 21173225]
Gharani, N.; Benayed, R.; Mancuso, V.; Brzustowicz, L.M.; Millonig, J.H. Association of the homeobox transcription factor, ENGRAILED 2, 3, with autism spectrum disorder. Mol. Psychiatry, 2004, 9(5), 474-484.
[] [PMID: 15024396]
Benayed, R.; Gharani, N.; Rossman, I.; Mancuso, V.; Lazar, G.; Kamdar, S.; Bruse, S.E.; Tischfield, S.; Smith, B.J.; Zimmerman, R.A.; DiCicco-Bloom, E.; Brzustowicz, L.M.; Millonig, J.H. Support for the homeobox transcription factor gene ENGRAILED 2 as an autism spectrum disorder susceptibility locus. Am. J. Hum. Genet., 2005, 77(5), 851-868.
[] [PMID: 16252243]
Benayed, R.; Choi, J.; Matteson, P.G.; Gharani, N.; Kamdar, S.; Brzustowicz, L.M.; Millonig, J.H. Autism-associated haplotype affects the regulation of the homeobox gene, ENGRAILED 2. Biol. Psychiatry, 2009, 66(10), 911-917.
[] [PMID: 19615670]
Cheh, M.A.; Millonig, J.H.; Roselli, L.M.; Ming, X.; Jacobsen, E.; Kamdar, S.; Wagner, G.C. En2 knockout mice display neurobehavioral and neurochemical alterations relevant to autism spectrum disorder. Brain Res., 2006, 1116(1), 166-176.
[] [PMID: 16935268]
Genestine, M.; Lin, L.; Durens, M.; Yan, Y.; Jiang, Y.; Prem, S.; Bailoor, K.; Kelly, B.; Sonsalla, P.K.; Matteson, P.G.; Silverman, J.; Crawley, J.N.; Millonig, J.H.; DiCicco-Bloom, E. Engrailed-2 (En2) deletion produces multiple neurodevelopmental defects in monoamine systems, forebrain structures and neurogenesis and behavior. Hum. Mol. Genet., 2015, 24(20), 5805-5827.
[] [PMID: 26220976]
Durens, M.; Soliman, M.; Millonig, J.; DiCicco-Bloom, E. Engrailed‐2 is a cell autonomous regulator of neurogenesis in cultured hippocampal neural stem cells. Dev. Neurobiol., 2021, 81(5), 724-735.
[] [PMID: 33852756]
Feng, C.; Chen, Y.; Zhang, Y.; Yan, Y.; Yang, M.; Gui, H.; Wang, M. Pten regulates mitochondrial biogenesis via the akt/gsk-3β/pgc-1α pathway in autism. Neuroscience, 2021, 465, 85-94.
[] [PMID: 33895342]
Sgadò, P.; Genovesi, S.; Kalinovsky, A.; Zunino, G.; Macchi, F.; Allegra, M.; Murenu, E.; Provenzano, G.; Tripathi, P.P.; Casarosa, S.; Joyner, A.L.; Bozzi, Y. Loss of GABAergic neurons in the hippocampus and cerebral cortex of Engrailed-2 null mutant mice: Implications for autism spectrum disorders. Exp. Neurol., 2013, 247, 496-505.
[] [PMID: 23360806]
Amiri, A.; Cho, W.; Zhou, J.; Birnbaum, S.G.; Sinton, C.M.; McKay, R.M.; Parada, L.F. Pten deletion in adult hippocampal neural stem/progenitor cells causes cellular abnormalities and alters neurogenesis. J. Neurosci., 2012, 32(17), 5880-5890.
[] [PMID: 22539849]
Wang, J.; Cui, Y.; Yu, Z.; Wang, W.; Cheng, X.; Ji, W.; Guo, S.; Zhou, Q.; Wu, N.; Chen, Y.; Chen, Y.; Song, X.; Jiang, H.; Wang, Y.; Lan, Y.; Zhou, B.; Mao, L.; Li, J.; Yang, H.; Guo, W.; Yang, X. Brain endothelial cells maintain lactate homeostasis and control adult hippocampal neurogenesis. Cell Stem Cell, 2019, 25(6), 754-767.e9.
[] [PMID: 31761722]
Pinar, C.; Yau, S.; Sharp, Z.; Shamei, A.; Fontaine, C.J.; Meconi, A.L.; Lottenberg, C.P.; Christie, B.R. Effects of voluntary exercise on cell proliferation and neurogenesis in the dentate gyrus of adult fmr1 knockout mice. Brain Plast., 2018, 4(2), 185-195.
[] [PMID: 30598869]
Pieretti, M.; Zhang, F.; Fu, Y.H.; Warren, S.T.; Oostra, B.A.; Caskey, C.T.; Nelson, D.L. Absence of expression of the FMR-1 gene in fragile X syndrome. Cell, 1991, 66(4), 817-822.
[] [PMID: 1878973]
Wang, T.; Bray, S.M.; Warren, S.T. New perspectives on the biology of fragile X syndrome. Curr. Opin. Genet. Dev., 2012, 22(3), 256-263.
[] [PMID: 22382129]
Luo, Y.; Shan, G.; Guo, W.; Smrt, R.D.; Johnson, E.B.; Li, X.; Pfeiffer, R.L.; Szulwach, K.E.; Duan, R.; Barkho, B.Z.; Li, W.; Liu, C.; Jin, P.; Zhao, X. Fragile x mental retardation protein regulates proliferation and differentiation of adult neural stem/progenitor cells. PLoS Genet., 2010, 6(4), e1000898.
[] [PMID: 20386739]
Guo, W.; Allan, A.M.; Zong, R.; Zhang, L.; Johnson, E.B.; Schaller, E.G.; Murthy, A.C.; Goggin, S.L.; Eisch, A.J.; Oostra, B.A.; Nelson, D.L.; Jin, P.; Zhao, X. Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning. Nat. Med., 2011, 17(5), 559-565.
[] [PMID: 21516088]
Eadie, B.D.; Zhang, W.N.; Boehme, F.; Gil-Mohapel, J.; Kainer, L.; Simpson, J.M.; Christie, B.R. Fmr1 knockout mice show reduced anxiety and alterations in neurogenesis that are specific to the ventral dentate gyrus. Neurobiol. Dis., 2009, 36(2), 361-373.
[] [PMID: 19666116]
Franklin, A.V.; King, M.K.; Palomo, V.; Martinez, A.; McMahon, L.L.; Jope, R.S. Glycogen synthase kinase-3 inhibitors reverse deficits in long-term potentiation and cognition in fragile X mice. Biol. Psychiatry, 2014, 75(3), 198-206.
[] [PMID: 24041505]
Pathania, M.; Davenport, E.C.; Muir, J.; Sheehan, D.F.; López-Doménech, G.; Kittler, J.T. The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines. Transl. Psychiatry, 2014, 4(3), e374.
[] [PMID: 24667445]
Cox, D.; Butler, M. The 15q11.2 BP1-BP2 microdeletion syndrome: A review. Int. J. Mol. Sci., 2015, 16(2), 4068-4082.
[] [PMID: 25689425]
Haan, N.; Westacott, L.J.; Carter, J.; Owen, M.J.; Gray, W.P.; Hall, J.; Wilkinson, L.S. Haploinsufficiency of the schizophrenia and autism risk gene Cyfip1 causes abnormal postnatal hippocampal neurogenesis through microglial and Arp2/3 mediated actin dependent mechanisms. Transl. Psychiatry, 2021, 11(1), 313.
[] [PMID: 34031371]
Peng, Z.; Deng, B.; Jia, J.; Hou, W.; Hu, S.; Deng, J.; Lin, W.; Hou, L.; Sang, H. Liver X receptor β in the hippocampus: A potential novel target for the treatment of major depressive disorder? Neuropharmacology, 2018, 135, 514-528.
[] [PMID: 29654801]
Xu, P.; Li, D.; Tang, X.; Bao, X.; Huang, J.; Tang, Y.; Yang, Y.; Xu, H.; Fan, X. LXR agonists: new potential therapeutic drug for neurodegenerative diseases. Mol. Neurobiol., 2013, 48(3), 715-728.
[] [PMID: 23625315]
Li, X.; Zhong, H.; Wang, Z.; Xiao, R.; Antonson, P.; Liu, T.; Wu, C.; Zou, J.; Wang, L.; Nalvarte, I.; Xu, H.; Warner, M.; Gustafsson, J.A.; Fan, X. Loss of liver X receptor β in astrocytes leads to anxiety-like behaviors via regulating synaptic transmission in the medial prefrontal cortex in mice. Mol. Psychiatry, 2021, 26(11), 6380-6393.
[] [PMID: 33963286]
Fan, X.; Kim, H.J.; Bouton, D.; Warner, M.; Gustafsson, J.Å. Expression of liver X receptor β is essential for formation of superficial cortical layers and migration of later-born neurons. Proc. Natl. Acad. Sci. USA, 2008, 105(36), 13445-13450.
[] [PMID: 18768805]
Xing, Y.; Fan, X.; Ying, D. Liver X receptor agonist treatment promotes the migration of granule neurons during cerebellar development. J. Neurochem., 2010, 115(6), 1486-1494.
[] [PMID: 20950333]
Xu, P.; Xu, H.; Tang, X.; Xu, L.; Wang, Y.; Guo, L.; Yang, Z.; Xing, Y.; Wu, Y.; Warner, M.; Gustafsson, J-A.; Fan, X. Liver X receptor β is essential for the differentiation of radial glial cells to oligodendrocytes in the dorsal cortex. Mol. Psychiatry, 2014, 19(8), 947-957.
[] [PMID: 24934178]
Guo, L.; Xu, P.; Tang, X.; Wu, Q.; Xing, Y.; Gustafsson, J.A.; Xu, H.; Fan, X. Liver X receptor β delays transformation of radial glial cells into astrocytes during mouse cerebral cortical development. Neurochem. Int., 2014, 71, 8-16.
[] [PMID: 24662373]
Cai, Y.; Tang, X.; Chen, X.; Li, X.; Wang, Y.; Bao, X.; Wang, L.; Sun, D.; Zhao, J.; Xing, Y.; Warner, M.; Xu, H.; Gustafsson, J.Å.; Fan, X. Liver X receptor β regulates the development of the dentate gyrus and autistic-like behavior in the mouse. Proc. Natl. Acad. Sci. USA, 2018, 115(12), E2725-E2733.
[] [PMID: 29507213]
Stoll, G.; Pietiläinen, O.P.H.; Linder, B.; Suvisaari, J.; Brosi, C.; Hennah, W.; Leppä, V.; Torniainen, M.; Ripatti, S.; Ala-Mello, S.; Plöttner, O.; Rehnström, K.; Tuulio-Henriksson, A.; Varilo, T.; Tallila, J.; Kristiansson, K.; Isohanni, M.; Kaprio, J.; Eriksson, J.G.; Raitakari, O.T.; Lehtimäki, T.; Jarvelin, M.R.; Salomaa, V.; Hurles, M.; Stefansson, H.; Peltonen, L.; Sullivan, P.F.; Paunio, T.; Lönnqvist, J.; Daly, M.J.; Fischer, U.; Freimer, N.B.; Palotie, A. Deletion of TOP3β a component of FMRP-containing mRNPs, contributes to neurodevelopmental disorders. Nat. Neurosci., 2013, 16(9), 1228-1237.
[] [PMID: 23912948]
Joo, Y.; Xue, Y.; Wang, Y.; McDevitt, R.A.; Sah, N.; Bossi, S.; Su, S.; Lee, S.K.; Peng, W.; Xie, A.; Zhang, Y.; Ding, Y.; Ku, W.L.; Ghosh, S.; Fishbein, K.; Shen, W.; Spencer, R.; Becker, K.; Zhao, K.; Mattson, M.P.; van Praag, H.; Sharov, A.; Wang, W. Topoisomerase 3β knockout mice show transcriptional and behavioural impairments associated with neurogenesis and synaptic plasticity. Nat. Commun., 2020, 11(1), 3143.
[] [PMID: 32561719]
Xu, D.; Shen, W.; Guo, R.; Xue, Y.; Peng, W.; Sima, J.; Yang, J.; Sharov, A.; Srikantan, S.; Yang, J.; Fox, D., III; Qian, Y.; Martindale, J.L.; Piao, Y.; Machamer, J.; Joshi, S.R.; Mohanty, S.; Shaw, A.C.; Lloyd, T.E.; Brown, G.W.; Ko, M.S.H.; Gorospe, M.; Zou, S.; Wang, W. Top3β is an RNA topoisomerase that works with fragile X syndrome protein to promote synapse formation. Nat. Neurosci., 2013, 16(9), 1238-1247.
[] [PMID: 23912945]
Ahmad, M.; Shen, W.; Li, W.; Xue, Y.; Zou, S.; Xu, D.; Wang, W. Topoisomerase 3β is the major topoisomerase for mRNAs and linked to neurodevelopment and mental dysfunction. Nucleic Acids Res., 2017, 45(5), 2704-2713.
[PMID: 28039324]
Rahman, F.U.; Kim, Y.R.; Kim, E.K.; Kim, H.; Cho, S.M.; Lee, C.S.; Kim, S.J.; Araki, K.; Yamamura, K.; Lee, M.N.; Park, S.G.; Yoon, W.K.; Lee, K.; Won, Y.S.; Kim, H.C.; Lee, Y.; Lee, H.Y.; Nam, K.H. Topoisomerase iiiβ deficiency induces neuro-behavioral changes and brain connectivity alterations in mice. Int. J. Mol. Sci., 2021, 22(23), 12806.
[] [PMID: 34884616]
Plummer, J.T.; Evgrafov, O.V.; Bergman, M.Y.; Friez, M.; Haiman, C.A.; Levitt, P.; Aldinger, K.A. Transcriptional regulation of the MET receptor tyrosine kinase gene by MeCP2 and sex-specific expression in autism and Rett syndrome. Transl. Psychiatry, 2013, 3(10), e316.
[] [PMID: 24150225]
Wen, Z.; Cheng, T.L.; Li, G.; Sun, S.B.; Yu, S.Y.; Zhang, Y.; Du, Y.S.; Qiu, Z. Identification of autism-related MECP2 mutations by whole-exome sequencing and functional validation. Mol. Autism, 2017, 8(1), 43.
[] [PMID: 28785396]
Bertoldi, M.L.; Zalosnik, M.I.; Fabio, M.C.; Aja, S.; Roth, G.A.; Ronnett, G.V.; Degano, A.L. Mecp2 deficiency disrupts kainate-induced presynaptic plasticity in the mossy fiber projections in the hippocampus. Front. Cell. Neurosci., 2019, 13, 286.
[] [PMID: 31333414]
Liu, Z.; Li, X.; Zhang, J.T.; Cai, Y.J.; Cheng, T.L.; Cheng, C.; Wang, Y.; Zhang, C.C.; Nie, Y.H.; Chen, Z.F.; Bian, W.J.; Zhang, L.; Xiao, J.; Lu, B.; Zhang, Y.F.; Zhang, X.D.; Sang, X.; Wu, J.J.; Xu, X.; Xiong, Z.Q.; Zhang, F.; Yu, X.; Gong, N.; Zhou, W.H.; Sun, Q.; Qiu, Z. Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. Nature, 2016, 530(7588), 98-102.
[] [PMID: 26808898]
Qiu, Z. Deciphering MECP2 -associated disorders: Disrupted circuits and the hope for repair. Curr. Opin. Neurobiol., 2018, 48, 30-36.
[] [PMID: 28961504]
Chen, Z.; Li, X.; Zhou, J.; Yuan, B.; Yu, B.; Tong, D.; Cheng, C.; Shao, Y.; Xia, S.; Zhang, R.; Lyu, J.; Yu, X.; Dong, C.; Zhou, W.H.; Qiu, Z. Accumulated quiescent neural stem cells in adult hippocampus of the mouse model for the MECP2 duplication syndrome. Sci. Rep., 2017, 7(1), 41701.
[] [PMID: 28139724]
Allan, A.M.; Liang, X.; Luo, Y.; Pak, C.; Li, X.; Szulwach, K.E.; Chen, D.; Jin, P.; Zhao, X. The loss of methyl-CpG binding protein 1 leads to autism-like behavioral deficits. Hum. Mol. Genet., 2008, 17(13), 2047-2057.
[] [PMID: 18385101]
Liu, C.; Teng, Z.Q.; Santistevan, N.J.; Szulwach, K.E.; Guo, W.; Jin, P.; Zhao, X. Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell, 2010, 6(5), 433-444.
[] [PMID: 20452318]
Jobe, E.M.; Gao, Y.; Eisinger, B.E.; Mladucky, J.K.; Giuliani, C.C.; Kelnhofer, L.E.; Zhao, X. Methyl-cpg-binding protein mbd1 regulates neuronal lineage commitment through maintaining adult neural stem cell identity. J. Neurosci., 2017, 37(3), 523-536.
[] [PMID: 28100736]
Jalal, R.; Nair, A.; Lin, A.; Eckfeld, A.; Kushan, L.; Zinberg, J.; Karlsgodt, K.H.; Cannon, T.D.; Bearden, C.E. Social cognition in 22q11.2 deletion syndrome and idiopathic developmental neuropsychiatric disorders. J. Neurodev. Disord., 2021, 13(1), 15.
[] [PMID: 33863277]
Baldini, A. The 22q11.2 deletion syndrome: a gene dosage perspective. Sci. World J., 2006, 6, 1881-1887.
[] [PMID: 17205194]
Hiramoto, T.; Kang, G.; Suzuki, G.; Satoh, Y.; Kucherlapati, R.; Watanabe, Y.; Hiroi, N. Tbx1: identification of a 22q11.2 gene as a risk factor for autism spectrum disorder in a mouse model. Hum. Mol. Genet., 2011, 20(24), 4775-4785.
[] [PMID: 21908517]
Boku, S.; Izumi, T.; Abe, S.; Takahashi, T.; Nishi, A.; Nomaru, H.; Naka, Y.; Kang, G.; Nagashima, M.; Hishimoto, A.; Enomoto, S.; Duran-Torres, G.; Tanigaki, K.; Zhang, J.; Ye, K.; Kato, S.; Männistö, P.T.; Kobayashi, K.; Hiroi, N. Copy number elevation of 22q11.2 genes arrests the developmental maturation of working memory capacity and adult hippocampal neurogenesis. Mol. Psychiatry, 2018, 23(4), 985-992.
[] [PMID: 28827761]
Gradari, S.; Herrera, A.; Tezanos, P.; Fontán-Lozano, Á.; Pons, S.; Trejo, J.L. The role of smad2 in adult neuroplasticity as seen through hippocampal-dependent spatial learning/memory and neurogenesis. J. Neurosci., 2021, 41(32), 6836-6849.
[] [PMID: 34210778]
Sippel, D.; Schwabedal, J.; Snyder, J.C.; Oyanedel, C.N.; Bernas, S.N.; Garthe, A.; Tröndle, A.; Storch, A.; Kempermann, G.; Brandt, M.D. Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis. Sci. Rep., 2020, 10(1), 16467.
[] [PMID: 33020501]
Walgrave, H.; Balusu, S.; Snoeck, S.; Vanden Eynden, E.; Craessaerts, K.; Thrupp, N.; Wolfs, L.; Horré, K.; Fourne, Y.; Ronisz, A.; Silajdžić, E.; Penning, A.; Tosoni, G.; Callaerts-Vegh, Z.; D'Hooge, R.; Thal, D.R.; Zetterberg, H.; Thuret, S.; Fiers, M.; Frigerio, C.S.; De Strooper, B.; Salta, E. Restoring mir-132 expression rescues adult hippocampal neurogenesis and memory deficits in alzheimer's disease. Cell Stem Cell, 2021, 28(10), 1805-1821.
Tokatly Latzer, I.; Leitner, Y.; Karnieli-Miller, O. Core experiences of parents of children with autism during the COVID-19 pandemic lockdown. Autism, 2021, 25(4), 1047-1059.
[] [PMID: 33435701]
Steiner, H.; Kertesz, Z. Effects of therapeutic horse riding on gait cycle parameters and some aspects of behavior of children with autism. Acta Physiol. Hung., 2015, 102(3), 324-335.
[] [PMID: 26551748]
Cai, Y.; Zhong, H.; Li, X.; Xiao, R.; Wang, L.; Fan, X. The liver x receptor agonist to901317 ameliorates behavioral deficits in two mouse models of autism. Front. Cell. Neurosci., 2019, 13, 213.
[] [PMID: 31139052]
Cai, K.L.; Wang, J.G.; Liu, Z.M.; Zhu, L.N.; Xiong, X.; Klich, S.; Maszczyk, A.; Chen, A.G. Mini-basketball training program improves physical fitness and social communication in preschool children with autism spectrum disorders. J. Hum. Kinet., 2020, 73(1), 267-278.
[] [PMID: 32774558]
Seo, T.B.; Cho, H.S.; Shin, M.S.; Kim, C.J.; Ji, E.S.; Baek, S.S. Treadmill exercise improves behavioral outcomes and spatial learning memory through up-regulation of reelin signaling pathway in autistic rats. J. Exerc. Rehabil., 2013, 9(2), 220-229.
[] [PMID: 24278864]
Javadi, S.; Li, Y.; Sheng, J.; Zhao, L.; Fu, Y.; Wang, D.; Zhao, X. Sustained correction of hippocampal neurogenic and cognitive deficits after a brief treatment by Nutlin-3 in a mouse model of fragile X syndrome. BMC Med., 2022, 20(1), 163.
[] [PMID: 35549943]
Luhach, K.; Kulkarni, G.T.; Singh, V.P.; Sharma, B. Vinpocetine ameliorates developmental hyperserotonemia induced behavioral and biochemical changes: role of neuronal function, inflammation, and oxidative stress. Acta Neurobiol. Exp. (Warsz.), 2022, 82(1), 35-51.
[] [PMID: 35451422]
Cheng, Y.; Wang, Z.M.; Tan, W.; Wang, X.; Li, Y.; Bai, B.; Li, Y.; Zhang, S.F.; Yan, H.L.; Chen, Z.L.; Liu, C.M.; Mi, T.W.; Xia, S.; Zhou, Z.; Liu, A.; Tang, G.B.; Liu, C.; Dai, Z.J.; Wang, Y.Y.; Wang, H.; Wang, X.; Kang, Y.; Lin, L.; Chen, Z.; Xie, N.; Sun, Q.; Xie, W.; Peng, J.; Chen, D.; Teng, Z.Q.; Jin, P. Partial loss of psychiatric risk gene Mir137 in mice causes repetitive behavior and impairs sociability and learning via increased Pde10a. Nat. Neurosci., 2018, 21(12), 1689-1703.
[] [PMID: 30397325]
Luhach, K.; Kulkarni, G.T.; Singh, V.P.; Sharma, B. Effect of papaverine on developmental hyperserotonemia induced autism spectrum disorder related behavioural phenotypes by altering markers of neuronal function, inflammation, and oxidative stress in rats. Clin. Exp. Pharmacol. Physiol., 2021, 48(4), 614-625.
[] [PMID: 33480092]
Fernández de Cossío, L.; Lacabanne, C.; Bordeleau, M.; Castino, G.; Kyriakakis, P.; Tremblay, M.È. Lipopolysaccharide-induced maternal immune activation modulates microglial CX3CR1 protein expression and morphological phenotype in the hippocampus and dentate gyrus, resulting in cognitive inflexibility during late adolescence. Brain Behav. Immun., 2021, 97, 440-454.
[] [PMID: 34343619]
Chen, C.; Whitsel, E.A.; Espeland, M.A.; Snetselaar, L.; Hayden, K.M.; Lamichhane, A.P.; Serre, M.L.; Vizuete, W.; Kaufman, J.D.; Wang, X.; Chui, H.C.; D’Alton, M.E.; Chen, J.C.; Kahe, K. B vitamin intakes modify the association between particulate air pollutants and incidence of all‐cause dementia: Findings from the Women’s Health Initiative Memory Study. Alzheimers Dement., 2022, 18(11), 2188-2198.
[] [PMID: 35103387]
Philippot, G.; Hellsten, S.V.; Viberg, H.; Fredriksson, R. Evaluation of the dentate gyrus in adult mice exposed to acetaminophen (paracetamol) on postnatal day 10. Int. J. Dev. Neurosci., 2021, 81(1), 91-97.
[] [PMID: 33222217]
Otellin, V.A.; Khozhaĭ, L.I.; Vataeva, L.A. Effect of hypoxia in early perinatal ontogenesis on behavior and structural characteristics of the rat brain. Zh. Evol. Biokhim. Fiziol., 2012, 48(5), 467-473.
[PMID: 23136755]
Bhat, A.; Mahalakshmi, A.M.; Ray, B.; Tuladhar, S.; Hediyal, T.A.; Manthiannem, E.; Padamati, J.; Chandra, R.; Chidambaram, S.B.; Sakharkar, M.K. Benefits of curcumin in brain disorders. Biofactors, 2019, 45(5), 666-689.
[] [PMID: 31185140]
Li, J.; Wang, H.; Qing, W.; Liu, F.; Zeng, N.; Wu, F.; Shi, Y.; Gao, X.; Cheng, M.; Li, H.; Shen, W.; Meng, F.; He, Y.; Chen, M.; Li, Z.; Zhou, H.; Wang, Q. Congenitally underdeveloped intestine drives autism-related gut microbiota and behavior. Brain Behav. Immun., 2022, 105, 15-26.
[] [PMID: 35714916]
Liu, G.; Yu, Q.; Tan, B.; Ke, X.; Zhang, C.; Li, H.; Zhang, T.; Lu, Y. Gut dysbiosis impairs hippocampal plasticity and behaviors by remodeling serum metabolome. Gut Microbes, 2022, 14(1), 2104089.
[] [PMID: 35876011]
De Gioia, R.; Biella, F.; Citterio, G.; Rizzo, F.; Abati, E.; Nizzardo, M.; Bresolin, N.; Comi, G.P.; Corti, S. Neural stem cell transplantation for neurodegenerative diseases. Int. J. Mol. Sci., 2020, 21(9), 3103.
[] [PMID: 32354178]
Chang, B.L.; Chang, K.H. Stem cell therapy in treating epilepsy. Front. Neurosci., 2022, 16, 934507.
[] [PMID: 35833086]
Parmar, M.; Grealish, S.; Henchcliffe, C. The future of stem cell therapies for Parkinson disease. Nat. Rev. Neurosci., 2020, 21(2), 103-115.
[] [PMID: 31907406]
Villarreal-Martínez, L.; González-Martínez, G.; Sáenz-Flores, M.; Bautista-Gómez, A.J.; González-Martínez, A.; Ortiz-Castillo, M.; Robles-Sáenz, D.A.; Garza-López, E. Stem cell therapy in the treatment of patients with autism spectrum disorder: A systematic review and meta-analysis. Stem Cell Rev. Rep., 2022, 18(1), 155-164.
[] [PMID: 34515938]
Qu, J.; Liu, Z.; Li, L.; Zou, Z.; He, Z.; Zhou, L.; Luo, Y.; Zhang, M.; Ye, J. Efficacy and safety of stem cell therapy in children with autism spectrum disorders: A systematic review and meta-analysis. Front Pediatr., 2022, 10, 897398.
[] [PMID: 35601435]
Kobinia, G.S.; Zaknun, J.J.; Pabinger, C.; Laky, B. Case report: Autologous bone marrow derived intrathecal stem cell transplant for autistic children - a report of four cases and literature review. Front Pediatr., 2021, 9, 620188.
[] [PMID: 34692600]
Maltman, D.J.; Hardy, S.A.; Przyborski, S.A. Role of mesenchymal stem cells in neurogenesis and nervous system repair. Neurochem. Int., 2011, 59(3), 347-356.
[] [PMID: 21718735]
Segal-Gavish, H.; Karvat, G.; Barak, N.; Barzilay, R.; Ganz, J.; Edry, L.; Aharony, I.; Offen, D.; Kimchi, T. Mesenchymal stem cell transplantation promotes neurogenesis and ameliorates autism related behaviors in btbr mice. Autism Res., 2016, 9(1), 17-32.
[] [PMID: 26257137]
Dawson, G.; Sun, J.M.; Baker, J.; Carpenter, K.; Compton, S.; Deaver, M.; Franz, L.; Heilbron, N.; Herold, B.; Horrigan, J.; Howard, J.; Kosinski, A.; Major, S.; Murias, M.; Page, K.; Prasad, V.K.; Sabatos-DeVito, M.; Sanfilippo, F.; Sikich, L.; Simmons, R.; Song, A.; Vermeer, S.; Waters-Pick, B.; Troy, J.; Kurtzberg, J. A phase ii randomized clinical trial of the safety and efficacy of intravenous umbilical cord blood infusion for treatment of children with autism spectrum disorder. J. Pediatr., 2020, 222, 164-173.e5.
[] [PMID: 32444220]
Dawson, G.; Sun, J.M.; Davlantis, K.S.; Murias, M.; Franz, L.; Troy, J.; Simmons, R.; Sabatos-DeVito, M.; Durham, R.; Kurtzberg, J. Autologous cord blood infusions are safe and feasible in young children with autism spectrum disorder: Results of a single-center phase i open-label trial. Stem Cells Transl. Med., 2017, 6(5), 1332-1339.
[] [PMID: 28378499]
Liang, Y.; Duan, L.; Xu, X.; Li, X.; Liu, M.; Chen, H.; Lu, J.; Xia, J. Mesenchymal stem cell-derived exosomes for treatment of autism spectrum disorder. ACS Appl. Bio Mater., 2020, 3(9), 6384-6393.
[] [PMID: 35021769]
Perets, N.; Segal-Gavish, H.; Gothelf, Y.; Barzilay, R.; Barhum, Y.; Abramov, N.; Hertz, S.; Morozov, D.; London, M.; Offen, D. Long term beneficial effect of neurotrophic factors-secreting mesenchymal stem cells transplantation in the BTBR mouse model of autism. Behav. Brain Res., 2017, 331, 254-260.
[] [PMID: 28392323]
Gobshtis, N.; Tfilin, M.; Wolfson, M.; Fraifeld, V.E.; Turgeman, G. Transplantation of mesenchymal stem cells reverses behavioural deficits and impaired neurogenesis caused by prenatal exposure to valproic acid. Oncotarget, 2017, 8(11), 17443-17452.
[] [PMID: 28407680]
Yang, P.; Yuan, W.; Liu, J.; Li, J.; Tan, B.; Qiu, C.; Zhu, X.; Qiu, C.; Lai, D.; Guo, L.; Yu, L. Biological characterization of human amniotic epithelial cells in a serum-free system and their safety evaluation. Acta Pharmacol. Sin., 2018, 39(8), 1305-1316.
[] [PMID: 29565036]
Xu, H.; Zhang, J.; Tsang, K.S.; Yang, H.; Gao, W.Q. Therapeutic potential of human amniotic epithelial cells on injuries and disorders in the central nervous system. Stem Cells Int., 2019, 2019, 1-11.
[] [PMID: 31827529]

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