Brain stars take the lead during critical periods of early postnatal brain development: relevance of astrocytes in health and mental disorders
Bandeira F, Lent R, Herculano-Houzel S. Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci. 2009;106:14108–13.
Google Scholar
Khakh BS, Sofroniew MV. Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci. 2015;18:942–52.
Google Scholar
Semyanov A, Verkhratsky A. Astrocytic processes: from tripartite synapses to the active milieu. Trends Neurosci. 2021;44:781–92.
Google Scholar
Magistretti PJ, Allaman I. Lactate in the brain: from metabolic end-product to signalling molecule. Nat Rev Neurosci. 2018;19:235–49.
Google Scholar
Allen NJ, Eroglu C. Cell Biology of Astrocyte-Synapse Interactions. Neuron. 2017;96:697–708.
Google Scholar
Bosworth AP, Allen NJ. The diverse actions of astrocytes during synaptic development. Curr Opin Neurobiol. 2017;47:38–43.
Google Scholar
Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive Astrocytes Protect Tissue and Preserve Function after Spinal Cord Injury. J Neurosci. 2004;24:2143–55.
Google Scholar
Iram T, Frenkel D. Targeting the Role of Astrocytes in the Progression of Alzheimers Disease. Curr Signal Transduct Ther. 2012;7:20–7.
Google Scholar
Molofsky AV, Kelley KW, Tsai HH, Redmond SA, Chang SM, Madireddy L, et al. Astrocyte-encoded positional cues maintain sensorimotor circuit integrity. Nature 2014;509:189–94.
Google Scholar
Cabezas R, Ávila M, Gonzalez J, El-Bachá RS, Báez E, García-Segura LM, et al. Astrocytic modulation of blood brain barrier: perspectives on Parkinson´s disease. Front Cell Neurosci. 2014;8. Available from: http://journal.frontiersin.org/article/10.3389/fncel.2014.00211/abstract.
Boulay AC, Saubaméa B, Adam N, Chasseigneaux S, Mazaré N, Gilbert A, et al. Translation in astrocyte distal processes sets molecular heterogeneity at the gliovascular interface. Cell Discov. 2017;3:17005.
Google Scholar
Alvarez JI, Katayama T, Prat A. Glial influence on the blood brain barrier. Glia. 2013;61:1939–58.
Google Scholar
Eroglu C, Barres BA. Regulation of synaptic connectivity by glia. Nature. 2010;468:223–31.
Google Scholar
Vasile F, Dossi E, Rouach N. Human astrocytes: structure and functions in the healthy brain. Brain Struct Funct. 2017;222:2017–29.
Google Scholar
Oberheim NA, Takano T, Han X, He W, Lin JHC, Wang F, et al. Uniquely Hominid Features of Adult Human Astrocytes. J Neurosci. 2009;29:3276–87.
Google Scholar
Mohn TC, Koob AO. Adult Astrogenesis and the Etiology of Cortical Neurodegeneration. J Exp Neurosci. 2015;9s2:JEN.S25520.
Google Scholar
Verkhratsky A, Nedergaard M. Physiology of Astroglia. Physiol Rev. 2018;98:239–389.
Google Scholar
Verkhratsky A, Bush N, Nedergaard M, Butt A. The Special Case of Human Astrocytes. Neuroglia. 2018;1:21–9.
Google Scholar
Götz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 2005;6:777–88.
Google Scholar
Takouda J, Katada S, Nakashima K. Emerging mechanisms underlying astrogenesis in the developing mammalian brain. Proc Jpn Acad Ser B 2017;93:386–98.
Google Scholar
Ever L, Gaiano N. Radial ‘glial’ progenitors: neurogenesis and signaling. Curr Opin Neurobiol. 2005;15:29–33.
Google Scholar
Zhou CJ, Zhao C, Pleasure SJ. Wnt Signaling Mutants Have Decreased Dentate Granule Cell Production and Radial Glial Scaffolding Abnormalities. J Neurosci. 2004;24:121–6.
Google Scholar
Rowitch DH, Kriegstein AR. Developmental genetics of vertebrate glial–cell specification. Nature 2010;468:214–22.
Google Scholar
Eze UC, Bhaduri A, Haeussler M, Nowakowski TJ, Kriegstein AR. Single-cell atlas of early human brain development highlights heterogeneity of human neuroepithelial cells and early radial glia. Nat Neurosci. 2021;24:584–94.
Google Scholar
Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C, Nicholas CR, et al. Molecular Identity of Human Outer Radial Glia during Cortical Development. Cell. 2015;163:55–67.
Google Scholar
Miller FD, Gauthier AS. Timing is everything: making neurons versus glia in the developing cortex. Neuron. 2007;54:357–69.
Google Scholar
Morrow T, Song MR, Ghosh A. Sequential specification of neurons and glia by developmentally regulated extracellular factors. Dev Camb Engl. 2001;128:3585–94.
Google Scholar
Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY. Local generation of glia is a major astrocyte source in postnatal cortex. Nature. 2012;484:376–80.
Google Scholar
De Zeeuw CI, Hoogland TM. Reappraisal of Bergmann glial cells as modulators of cerebellar circuit function. Front Cell Neurosci. 2015;9. Available from: http://journal.frontiersin.org/Article/10.3389/fncel.2015.00246/abstract.
Güngör Kobat S. Importance of Müller Cells. Beyoglu Eye J. 2020; Available from: http://beyoglueye.com/jvi.aspx?un=BEJ-28290&volume=.
Choi BH, Lapham LW. Evolution of Bergman glia in developing human fetal cerebellum: A Golgi, electron microscopic and immunofluorescent study. Brain Res. 1980;190:369–83.
Google Scholar
Reichenbach A, Bringmann A. Glia of the human retina. Glia. 2020;68:768–96.
Google Scholar
Martinotti F. Contributo allo studio della corteccia cerebrale, ed all ́origine centrale dei nervi. Fratelli Bocca; 1889.
Andriezen WL. The Neuroglia Elements in the Human Brain. BMJ. 1893;2:227–30.
Google Scholar
Retzius G. Die neuroglia des Gehirns beim Menschen und bei Saeugethieren. Jena: Chemie; 1894.
Colombo JA, Yáñez A, Puissant V, Lipina S. Long, interlaminar astroglial cell processes in the cortex of adult monkeys. J Neurosci Res. 1995;40:551–6.
Google Scholar
Colombo JA. Interlaminar Astroglial Processes in the Cerebral Cortex of Adult Monkeys But Not of Adult Rats. Cells Tissues Organs. 1996;155:57–62.
Google Scholar
Colombo JA, Yáñez A, Lipina SJ. Interlaminar astroglial processes in the cerebral cortex of non human primates: response to injury. J Hirnforsch. 1997;38:503–12.
Google Scholar
Colombo JA, Reisin HD. Interlaminar astroglia of the cerebral cortex: a marker of the primate brain. Brain Res. 2004;1006:126–31.
Google Scholar
Falcone C, Penna E, Hong T, Tarantal AF, Hof PR, Hopkins WD, et al. Cortical Interlaminar Astrocytes Are Generated Prenatally, Mature Postnatally, and Express Unique Markers in Human and Nonhuman Primates. Cereb Cortex. 2021;31:379–95.
Google Scholar
Falcone C, Martínez-Cerdeño V. Astrocyte evolution and human specificity. Neural Regen Res. 2023;18:131.
Google Scholar
Falcone C, McBride EL, Hopkins WD, Hof PR, Manger PR, Sherwood CC, et al. Redefining varicose projection astrocytes in primates. Glia. 2022;70:145–54.
Google Scholar
Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, et al. Forebrain Engraftment by Human Glial Progenitor Cells Enhances Synaptic Plasticity and Learning in Adult Mice. Cell Stem Cell. 2013;12:342–53.
Google Scholar
Azevedo FAC, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, Leite REP, et al. Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol. 2009;513:532–41.
Google Scholar
Falcone C. Evolution of astrocytes: From invertebrates to vertebrates. Front Cell Dev Biol. 2022;10:931311.
Google Scholar
Degl’Innocenti E, Dell’Anno MT. Human and mouse cortical astrocytes: a comparative view from development to morphological and functional characterization. Front Neuroanat. 2023;17:1130729.
Google Scholar
Namba T, Huttner WB. Neural progenitor cells and their role in the development and evolutionary expansion of the neocortex. WIREs Dev Biol. 2017;6:e256.
Google Scholar
Shinmyo Y, Saito K, Hamabe-Horiike T, Kameya N, Ando A, Kawasaki K, et al. Localized astrogenesis regulates gyrification of the cerebral cortex. Sci Adv. 2022;8:eabi5209.
Google Scholar
Zilles K, Palomero-Gallagher N, Amunts K. Development of cortical folding during evolution and ontogeny. Trends Neurosci. 2013;36:275–84.
Google Scholar
Farmer WT, Murai K. Resolving Astrocyte Heterogeneity in the CNS. Front Cell Neurosci. 2017;11:300.
Google Scholar
Holt MG. Astrocyte heterogeneity and interactions with local neural circuits. Essays Biochem. 2023;67:93–106.
Miller SJ. Astrocyte Heterogeneity in the Adult Central Nervous System. Front Cell Neurosci. 2018;12:401.
Google Scholar
Oliveria JP, Li ZJ. critical role of astrogenesis and neurodevelopment in Fragile X Syndrome and Rett Syndrome. McMaster Univ Med J. 2020;17. Available from: https://journals.mcmaster.ca/mumj/article/view/2338.
Kanski R, Van Strien ME, Van Tijn P, Hol EM. A star is born: new insights into the mechanism of astrogenesis. Cell Mol Life Sci. 2014;71:433–47.
Google Scholar
Yoon K, Nery S, Rutlin ML, Radtke F, Fishell G, Gaiano N. Fibroblast Growth Factor Receptor Signaling Promotes Radial Glial Identity and Interacts with Notch1 Signaling in Telencephalic Progenitors. J Neurosci. 2004;24:9497–506.
Google Scholar
Fan G, Martinowich K, Chin MH, He F, Fouse SD, Hutnick L, et al. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development. 2005;132:3345–56.
Google Scholar
Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, et al. Neurogenin Promotes Neurogenesis and Inhibits Glial Differentiation by Independent Mechanisms. Cell. 2001;104:365–76.
Google Scholar
Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, et al. Regulation of Gliogenesis in the Central Nervous System by the JAK-STAT Signaling Pathway. Science. 1997;278:477–83.
Google Scholar
Nieto M, Schuurmans C, Britz O, Guillemot F. Neural bHLH Genes Control the Neuronal versus Glial Fate Decision in Cortical Progenitors. Neuron. 2001;29:401–13.
Google Scholar
Zhang Y, Pak C, Han Y, Ahlenius H, Zhang Z, Chanda S, et al. Rapid Single-Step Induction of Functional Neurons from Human Pluripotent Stem Cells. Neuron. 2013;78:785–98.
Google Scholar
Yang N, Chanda S, Marro S, Ng YH, Janas JA, Haag D, et al. Generation of pure GABAergic neurons by transcription factor programming. Nat Methods. 2017;14:621–8.
Google Scholar
Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Südhof TC, Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature. 2010;463:1035–41.
Google Scholar
Hatakeyama J, Bessho Y, Katoh K, Ookawara S, Fujioka M, Guillemot F, et al. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development. 2004;131:5539–50.
Google Scholar
Mizutani KI, Saito T. Progenitors resume generating neurons after temporary inhibition of neurogenesis by Notch activation in the mammalian cerebral cortex. Development. 2005;132:1295–304.
Google Scholar
Hoch RV, Rubenstein JLR, Pleasure S. Genes and signaling events that establish regional patterning of the mammalian forebrain. Semin Cell Dev Biol. 2009;20:378–86.
Google Scholar
Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK. The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol. 2008;18:28–35.
Google Scholar
Guillemot F. Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol. 2005;17:639–47.
Google Scholar
He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, et al. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci. 2005;8:616–25.
Google Scholar
Tomita K. Mammalian achaete-scute and atonal homologs regulate neuronal versus glial fate determination in the central nervous system. EMBO J. 2000;19:5460–72.
Google Scholar
Llorca A, Deogracias R. Origin, Development, and Synaptogenesis of Cortical Interneurons. Front Neurosci. 2022;16:929469.
Google Scholar
Styr B, Slutsky I. Imbalance between firing homeostasis and synaptic plasticity drives early-phase Alzheimer’s disease. Nat Neurosci. 2018;21:463–73.
Google Scholar
Rubenstein JLR, Merzenich MM. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003;2:255–67.
Google Scholar
Foss-Feig JH, Adkinson BD, Ji JL, Yang G, Srihari VH, McPartland JC, et al. Searching for Cross-Diagnostic Convergence: Neural Mechanisms Governing Excitation and Inhibition Balance in Schizophrenia and Autism Spectrum Disorders. Biol Psychiatry. 2017;81:848–61.
Google Scholar
Barnabé-Heider F, Wasylnka JA, Fernandes KJL, Porsche C, Sendtner M, Kaplan DR, et al. Evidence that Embryonic Neurons Regulate the Onset of Cortical Gliogenesis via Cardiotrophin-1. Neuron. 2005;48:253–65.
Google Scholar
Farmer WT, Abrahamsson T, Chierzi S, Lui C, Zaelzer C, Jones EV, et al. Neurons diversify astrocytes in the adult brain through sonic hedgehog signaling. Science. 2016;351:849–54.
Google Scholar
Voss AJ, Lanjewar SN, Sampson MM, King A, Hill EJ, Sing A, et al. Identification of ligand-receptor pairs that drive human astrocyte development. Nat Neurosci. 2023;26:1339–51.
Google Scholar
Bayraktar OA, Bartels T, Holmqvist S, Kleshchevnikov V, Martirosyan A, Polioudakis D, et al. Astrocyte layers in the mammalian cerebral cortex revealed by a single-cell in situ transcriptomic map. Nat Neurosci. 2020;23:500–9.
Google Scholar
Berardi N, Pizzorusso T, Maffei L. Critical periods during sensory development. Curr Opin Neurobiol. 2000;10:138–45.
Google Scholar
Chugani HT. A Critical Period of Brain Development: Studies of Cerebral Glucose Utilization with PET. Prev Med. 1998;27:184–8.
Google Scholar
Sengpiel F. The critical period. Curr Biol. 2007;17:R742–3.
Google Scholar
Knudsen EI. Sensitive Periods in the Development of the Brain and Behavior. J Cogn Neurosci. 2004;16:1412–25.
Google Scholar
Nelson CA, Gabard-Durnam LJ. Early Adversity and Critical Periods: Neurodevelopmental Consequences of Violating the Expectable Environment. Trends Neurosci. 2020;43:133–43.
Google Scholar
Virolainen SJ, VonHandorf A. Viel KCMF, Weirauch MT, Kottyan LC. Gene–environment interactions and their impact on human health. Genes Immun. 2022;24:1–11.
Google Scholar
Milbocker KA, Campbell TS, Collins N, Kim S, Smith IF, Roth TL, et al. Glia-Driven Brain Circuit Refinement Is Altered by Early-Life Adversity: Behavioral Outcomes. Front Behav Neurosci. 2021;15:786234.
Google Scholar
Christopherson KS, Ullian EM, Stokes CCA, Mullowney CE, Hell JW, Agah A, et al. Thrombospondins Are Astrocyte-Secreted Proteins that Promote CNS Synaptogenesis. Cell. 2005;120:421–33.
Google Scholar
Pfrieger FW, Barres BA. Synaptic Efficacy Enhanced by Glial Cells in Vitro. Science. 1997;277:1684–7.
Google Scholar
Mauch DH, Nägler K, Schumacher S, Göritz C, Müller EC, Otto A, et al. CNS Synaptogenesis Promoted by Glia-Derived Cholesterol. Science. 2001;294:1354–7.
Google Scholar
Eroglu Ç, Allen NJ, Susman MW, O’Rourke NA, Park CY, Özkan E, et al. Gabapentin Receptor α2δ-1 Is a Neuronal Thrombospondin Receptor Responsible for Excitatory CNS Synaptogenesis. Cell. 2009;139:380–92.
Google Scholar
Fossati G, Pozzi D, Canzi A, Mirabella F, Valentino S, Morini R, et al. Pentraxin 3 regulates synaptic function by inducing AMPA receptor clustering via ECM remodeling and β1‐integrin. EMBO J. 2019;38:e99529.
Google Scholar
Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, et al. Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature. 2012;486:410–4.
Google Scholar
Diniz LP, Almeida JC, Tortelli V, Vargas Lopes C, Setti-Perdigão P, Stipursky J, et al. Astrocyte-induced Synaptogenesis Is Mediated by Transforming Growth Factor β Signaling through Modulation of d-Serine Levels in Cerebral Cortex Neurons. J Biol Chem. 2012;287:41432–45.
Google Scholar
Diniz LP, Tortelli V, Garcia MN, Araújo APB, Melo HM, Seixas Da Silva GS, et al. Astrocyte transforming growth factor beta 1 promotes inhibitory synapse formation via CaM kinase II signaling. Glia. 2014;62:1917–31.
Google Scholar
Gómez-Casati ME, Murtie JC, Rio C, Stankovic K, Liberman MC, Corfas G. Nonneuronal cells regulate synapse formation in the vestibular sensory epithelium via erbB-dependent BDNF expression. Proc Natl Acad Sci. 2010;107:17005–10.
Google Scholar
Shan L, Zhang T, Fan K, Cai W, Liu H. Astrocyte-Neuron Signaling in Synaptogenesis. Front Cell Dev Biol. 2021;9:680301.
Google Scholar
Tan CX, Burrus Lane CJ, Eroglu C. Role of astrocytes in synapse formation and maturation. In: Current Topics in Developmental Biology. Elsevier; 2021;371–407. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0070215320301435.
Konishi H, Koizumi S, Kiyama H. Phagocytic astrocytes: Emerging from the shadows of microglia. Glia 2022;70:1009–26.
Google Scholar
Juraska JM, Willing J. Pubertal onset as a critical transition for neural development and cognition. Brain Res. 2017;1654:87–94.
Google Scholar
Huttenlocher PR, Dabholkar AS. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol. 1997;387:167–78.
Google Scholar
Peter RH. Synaptic density in human frontal cortex — Developmental changes and effects of aging. Brain Res. 1979;163:195–205.
Google Scholar
Dosenbach NUF, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, et al. Prediction of Individual Brain Maturity Using fMRI. Science. 2010;329:1358–61.
Google Scholar
Petanjek Z, Judaš M, Šimić G, Rašin MR, Uylings HBM, Rakic P, et al. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci. 2011;108:13281–6.
Google Scholar
Antoine MW, Langberg T, Schnepel P, Feldman DE. Increased Excitation-Inhibition Ratio Stabilizes Synapse and Circuit Excitability in Four Autism Mouse Models. Neuron. 2019;101:648–61.e4.
Google Scholar
Aida T, Yoshida J, Nomura M, Tanimura A, Iino Y, Soma M, et al. Astroglial Glutamate Transporter Deficiency Increases Synaptic Excitability and Leads to Pathological Repetitive Behaviors in Mice. Neuropsychopharmacology. 2015;40:1569–79.
Google Scholar
Ortinski PI, Dong J, Mungenast A, Yue C, Takano H, Watson DJ, et al. Selective induction of astrocytic gliosis generates deficits in neuronal inhibition. Nat Neurosci. 2010;13:584–91.
Google Scholar
Escartin C, Galea E, Lakatos A, O’Callaghan JP, Petzold GC, Serrano-Pozo A, et al. Reactive astrocyte nomenclature, definitions, and future directions. Nat Neurosci. 2021;24:312–25.
Google Scholar
Eltokhi A, Janmaat IE, Genedi M, Haarman BCM, Sommer IEC. Dysregulation of synaptic pruning as a possible link between intestinal microbiota dysbiosis and neuropsychiatric disorders. J Neurosci Res. 2020;98:1335–69.
Google Scholar
Cardozo PL, De Lima IBQ, Maciel EMA, Silva NC, Dobransky T, Ribeiro FM. Synaptic Elimination in Neurological Disorders. Curr Neuropharmacol. 2019;17:1071–95.
Google Scholar
Zhuang Y, Xu X, Li H, Niu F, Yang M, Ge Q, et al. Megf10‐related engulfment of excitatory postsynapses by astrocytes following severe brain injury. CNS Neurosci Ther. 2023;29:2873–83.
Iram T, Ramirez-Ortiz Z, Byrne MH, Coleman UA, Kingery ND, Means TK, et al. Megf10 Is a Receptor for C1Q That Mediates Clearance of Apoptotic Cells by Astrocytes. J Neurosci. 2016;36:5185–92.
Google Scholar
Pattwell SS, Liston C, Jing D, Ninan I, Yang RR, Witztum J, et al. Dynamic changes in neural circuitry during adolescence are associated with persistent attenuation of fear memories. Nat Commun. 2016;7:11475.
Google Scholar
Honeycutt JA, Demaestri C, Peterzell S, Silveri MM, Cai X, Kulkarni P, et al. Altered corticolimbic connectivity reveals sex-specific adolescent outcomes in a rat model of early life adversity. eLife. 2020;9:e52651.
Google Scholar
Karpova NN, Pickenhagen A, Lindholm J, Tiraboschi E, Kulesskaya N, Ágústsdóttir A, et al. Fear Erasure in Mice Requires Synergy Between Antidepressant Drugs and Extinction Training. Science. 2011;334:1731–4.
Google Scholar
Vetencourt JFM, Sale A, Viegi A, Baroncelli L, De Pasquale RF, et al. The Antidepressant Fluoxetine Restores Plasticity in the Adult Visual Cortex. Science. 2008;320:385–8.
Google Scholar
Ribot J, Breton R, Calvo CF, Moulard J, Ezan P, Zapata J, et al. Astrocytes close the mouse critical period for visual plasticity. Science. 2021;373:77–81.
Google Scholar
Müller CM, Best J. Ocular dominance plasticity in adult cat visual cortex after transplantation of cultured astrocytes. Nature. 1989;342:427–30.
Google Scholar
Ghézali G, Calvo CF, Pillet LE, Llense F, Ezan P, Pannasch U, et al. Connexin 30 controls astroglial polarization during postnatal brain development. Development. 2018;145:dev155275.
Google Scholar
Abbink MR, Deijk AF, Heine VM, Verheijen MH, Korosi A. The involvement of astrocytes in early‐life adversity induced programming of the brain. Glia. 2019;67:1637–53.
Codeluppi SA, Chatterjee D, Prevot TD, Bansal Y, Misquitta KA, Sibille E, et al. Chronic Stress Alters Astrocyte Morphology in Mouse Prefrontal Cortex. Int J Neuropsychopharmacol. 2021;24:842–53.
Google Scholar
Woodburn SC, Bollinger JL, Wohleb ES. Synaptic and behavioral effects of chronic stress are linked to dynamic and sex-specific changes in microglia function and astrocyte dystrophy. Neurobiol Stress. 2021;14:100312.
Google Scholar
Dolotov OV, Inozemtseva LS, Myasoedov NF, Grivennikov IA. Stress-Induced Depression and Alzheimer’s Disease: Focus on Astrocytes. Int J Mol Sci. 2022;23:4999.
Google Scholar
Naskar S, Chattarji S. Stress Elicits Contrasting Effects on the Structure and Number of Astrocytes in the Amygdala versus Hippocampus. eNeuro. 2019;6:ENEURO.0338-18.2019.
Google Scholar
Murphy‐Royal C, Gordon GR, Bains JS. Stress‐induced structural and functional modifications of astrocytes—Further implicating glia in the central response to stress. Glia. 2019;67:1806–20.
Google Scholar
Yoshino K, Oda Y, Kimura M, Kimura H, Nangaku M, Shirayama Y, et al. The alterations of glutamate transporter 1 and glutamine synthetase in the rat brain of a learned helplessness model of depression. Psychopharmacology. 2020;237:2547–53.
Google Scholar
Tynan RJ, Beynon SB, Hinwood M, Johnson SJ, Nilsson M, Woods JJ, et al. Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathol. 2013;126:75–91.
Google Scholar
Virmani G, D’almeida P, Nandi A, Marathe S. Subfield‐specific effects of chronic mild unpredictable stress on hippocampal astrocytes. Eur J Neurosci. 2021;54:5730–46.
Lu CL, Ren J, Mo JW, Fan J, Guo F, Chen LY, et al. Glucocorticoid Receptor–Dependent Astrocytes Mediate Stress Vulnerability. Biol Psychiatry. 2022;92:204–15.
Google Scholar
Huang D, Li C, Zhang W, Qin J, Jiang W, Hu C. Dysfunction of astrocytic connexins 30 and 43 in the medial prefrontal cortex and hippocampus mediates depressive-like behaviours. Behav Brain Res. 2019;372:111950.
Google Scholar
Byun YG, Kim NS, Kim G, Jeon YS, Choi JB, Park CW, et al. Stress induces behavioral abnormalities by increasing expression of phagocytic receptor MERTK in astrocytes to promote synapse phagocytosis. Immunity. 2023;56:2105–20.e13.
Google Scholar
Miguel-Hidalgo JJ, Moulana M, Deloach PH, Rajkowska G. Chronic Unpredictable Stress Reduces Immunostaining for Connexins 43 and 30 and Myelin Basic Protein in the Rat Prelimbic and Orbitofrontal Cortices. Chronic Stress. 2018;2:247054701881418.
Google Scholar
Kang Y, Kang W, Kim A, Tae WS, Ham BJ, Han KM. Decreased cortical gyrification in major depressive disorder. Psychol Med. 2023;53:7512–24.
Google Scholar
Ning M, Li C, Gao L, Fan J. Core-Symptom-Defined Cortical Gyrification Differences in Autism Spectrum Disorder. Front Psychiatry. 2021;12:619367.
Google Scholar
Takayanagi Y, Sasabayashi D, Takahashi T, Komori Y, Furuichi A, Kido M, et al. Altered brain gyrification in deficit and non-deficit schizophrenia. Psychol Med. 2019;49:573–80.
Google Scholar
Cao B, Mwangi B, Passos IC, Wu MJ, Keser Z, Zunta-Soares GB, et al. Lifespan Gyrification Trajectories of Human Brain in Healthy Individuals and Patients with Major Psychiatric Disorders. Sci Rep. 2017;7:511.
Google Scholar
Sasabayashi D, Takahashi T, Takayanagi Y, Suzuki M. Anomalous brain gyrification patterns in major psychiatric disorders: a systematic review and transdiagnostic integration. Transl Psychiatry. 2021;11:176.
Google Scholar
Rajkowska G, Miguel-Hidalgo JJ. Glial Pathology in Major Depressive Disorder: An Approach to Investigate the Coverage of Blood Vessels by Astrocyte Endfeet in Human Postmortem Brain. In: Di Benedetto B, editor. Astrocytes. New York, NY: Springer New York; 2019. p. 247–54. (Methods in Molecular Biology; vol. 1938). Available from: http://link.springer.com/10.1007/978-1-4939-9068-9_17.
Di Benedetto B, Rupprecht R. Targeting Glia Cells: Novel Perspectives for the Treatment of Neuropsychiatric Diseases. Curr Neuropharmacol. 2013;11:171–85.
Google Scholar
Roman C, Egert L, Di Benedetto B. Astrocytic‐neuronal crosstalk gets jammed: Alternative perspectives on the onset of neuropsychiatric disorders. Eur J Neurosci. 2021;54:5717–29.
Google Scholar
Nagy C, Suderman M, Yang J, Szyf M, Mechawar N, Ernst C, et al. Astrocytic abnormalities and global DNA methylation patterns in depression and suicide. Mol Psychiatry. 2015;20:320–8.
Google Scholar
Martins-Macedo J, Salgado AJ, Gomes ED, Pinto L. Adult brain cytogenesis in the context of mood disorders: From neurogenesis to the emergent role of gliogenesis. Neurosci Biobehav Rev. 2021;131:411–28.
Google Scholar
Feresten AH, Barakauskas V, Ypsilanti A, Barr AM, Beasley CL. Increased expression of glial fibrillary acidic protein in prefrontal cortex in psychotic illness. Schizophr Res. 2013;150:252–7.
Google Scholar
Tarasov VV, Svistunov AA, Chubarev VN, Sologova SS, Mukhortova P, Levushkin D, et al. Alterations of Astrocytes in the Context of Schizophrenic Dementia. Front Pharm. 2020;10:1612.
Google Scholar
Notter T. Astrocytes in schizophrenia. Brain Neurosci Adv. 2021;5:239821282110091.
Google Scholar
Vakilzadeh G, Martinez-Cerdeño V. Pathology and Astrocytes in Autism. Neuropsychiatr Dis Treat. 2023;19:841–50.
Google Scholar
Allen M, Huang BS, Notaras MJ, Lodhi A, Barrio-Alonso E, Lituma PJ, et al. Astrocytes derived from ASD individuals alter behavior and destabilize neuronal activity through aberrant Ca2+ signaling. Mol Psychiatry. 2022;27:2470–84.
Google Scholar
Rajkowska G, Miguel-Hidalgo J. Gliogenesis and Glial Pathology in Depression. CNS Neurol Disord – Drug Targets. 2007;6:219–33.
Google Scholar
Belleau EL, Treadway MT, Pizzagalli DA. The Impact of Stress and Major Depressive Disorder on Hippocampal and Medial Prefrontal Cortex Morphology. Biol Psychiatry. 2019;85:443–53.
Google Scholar
Malykhin NV, Carter R, Seres P, Coupland NJ. Structural changes in the hippocampus in major depressive disorder: contributions of disease and treatment. J Psychiatry Neurosci. 2010;35:337–43.
Google Scholar
Geng R, Huang X. Identification of major depressive disorder disease-related genes and functional pathways based on system dynamic changes of network connectivity. BMC Med Genomics. 2021;14:55.
Google Scholar
Czéh B, Simon M, Schmelting B, Hiemke C, Fuchs E. Astroglial Plasticity in the Hippocampus is Affected by Chronic Psychosocial Stress and Concomitant Fluoxetine Treatment. Neuropsychopharmacology. 2006;31:1616–26.
Google Scholar
Czéh B, Di Benedetto B. Antidepressants act directly on astrocytes: Evidences and functional consequences. Eur Neuropsychopharmacol. 2013;23:171–85.
Google Scholar
Czéh B, Nagy SA. Clinical Findings Documenting Cellular and Molecular Abnormalities of Glia in Depressive Disorders. Front Mol Neurosci. 2018;11:56.
Google Scholar
Papouin T, Ladépêche L, Ruel J, Sacchi S, Labasque M, Hanini M, et al. Synaptic and Extrasynaptic NMDA Receptors Are Gated by Different Endogenous Coagonists. Cell. 2012;150:633–46.
Google Scholar
Henneberger C, Papouin T, Oliet SHR, Rusakov DA. Long-term potentiation depends on release of d-serine from astrocytes. Nature. 2010;463:232–6.
Google Scholar
Blanco-Suarez E, Liu TF, Kopelevich A, Allen NJ. Astrocyte-Secreted Chordin-like 1 Drives Synapse Maturation and Limits Plasticity by Increasing Synaptic GluA2 AMPA Receptors. Neuron. 2018;100:1116–32.e13.
Google Scholar
Caldwell ALM, Sancho L, Deng J, Bosworth A, Miglietta A, Diedrich JK, et al. Aberrant astrocyte protein secretion contributes to altered neuronal development in multiple models of neurodevelopmental disorders. Nat Neurosci. 2022;25:1163–78.
Google Scholar
Heresco-Levy U, Javitt DC, Ebstein R, Vass A, Lichtenberg P, Bar G, et al. D-serine efficacy as add-on pharmacotherapy to risperidone and olanzapine for treatment-refractory schizophrenia. Biol Psychiatry. 2005;57:577–85.
Google Scholar
Kantrowitz JT, Malhotra AK, Cornblatt B, Silipo G, Balla A, Suckow RF, et al. High dose D-serine in the treatment of schizophrenia. Schizophr Res. 2010;121:125–30.
Google Scholar
Ma TM, Abazyan S, Abazyan B, Nomura J, Yang C, Seshadri S, et al. Pathogenic disruption of DISC1-serine racemase binding elicits schizophrenia-like behavior via D-serine depletion. Mol Psychiatry. 2013;18:557–67.
Google Scholar
Cardno AG. Gottesman II. Twin studies of schizophrenia: From bow-and-arrow concordances to Star Wars Mx and functional genomics. Am J Med Genet. 2000;97:12–7.
Google Scholar
Walker EF, Trotman HD, Pearce BD, Addington J, Cadenhead KS, Cornblatt BA, et al. Cortisol Levels and Risk for Psychosis: Initial Findings from the North American Prodrome Longitudinal Study. Biol Psychiatry. 2013;74:410–7.
Google Scholar
Selemon LD, Zecevic N. Schizophrenia: a tale of two critical periods for prefrontal cortical development. Transl Psychiatry. 2015;5:e623.
Google Scholar
Sheu JR, Hsieh CY, Jayakumar T, Tseng MF, Lee HN, Huang SW, et al. A Critical Period for the Development of Schizophrenia-Like Pathology by Aberrant Postnatal Neurogenesis. Front Neurosci. 2019;13:635.
Google Scholar
De Oliveira Figueiredo EC, Calì C, Petrelli F, Bezzi P. Emerging evidence for astrocyte dysfunction in schizophrenia. Glia. 2022;70:1585–604.
Google Scholar
Russo FB, Freitas BC, Pignatari GC, Fernandes IR, Sebat J, Muotri AR, et al. Modeling the Interplay Between Neurons and Astrocytes in Autism Using Human Induced Pluripotent Stem Cells. Biol Psychiatry. 2018;83:569–78.
Google Scholar
Berger JM, Rohn TT, Oxford JT. Autism as the Early Closure of a Neuroplastic Critical Period Normally Seen in Adolescence. Biol Syst Open Access. 2012;02. Available from: https://www.omicsgroup.org/journals/autism-as-the-early-closure-of-a-neuroplastic-critical-period-normally-seen-in-adolescence-2329-6577-1000118.php?aid=43859.
Hashimoto Y, Greene C, Munnich A, Campbell M. The CLDN5 gene at the blood-brain barrier in health and disease. Fluids Barriers CNS. 2023;20:22.
Google Scholar
Igarashi Y, Utsumi H, Chiba H, Yamada-Sasamori Y, Tobioka H, Kamimura Y, et al. Glial Cell Line-Derived Neurotrophic Factor Induces Barrier Function of Endothelial Cells Forming the Blood–Brain Barrier. Biochem Biophys Res Commun. 1999;261:108–12.
Google Scholar
Rajkowska G, Hughes J, Stockmeier CA, Javier Miguel-Hidalgo J, Maciag D. Coverage of Blood Vessels by Astrocytic Endfeet Is Reduced in Major Depressive Disorder. Biol Psychiatry. 2013;73:613–21.
Google Scholar
Lee E, Chung WS. Glial Control of Synapse Number in Healthy and Diseased Brain. Front Cell Neurosci. 2019;13:42.
Google Scholar
Di Benedetto B, Malik VA, Begum S, Jablonowski L, Gómez-González GB, Neumann ID, et al. Fluoxetine Requires the Endfeet Protein Aquaporin-4 to Enhance Plasticity of Astrocyte Processes. Front Cell Neurosci. 2016;10. Available from: http://journal.frontiersin.org/Article/10.3389/fncel.2016.00008/abstract.
Malik VA, Zajicek F, Mittmann LA, Klaus J, Unterseer S, Rajkumar S, et al. GDF15 promotes simultaneous astrocyte remodeling and tight junction strengthening at the blood–brain barrier. J Neurosci Res. 2020;98:1433–56.
Google Scholar
Williams BP, Price J. Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron. 1995;14:1181–8.
Google Scholar
Chung WS, Allen NJ, Eroglu C. Astrocytes Control Synapse Formation, Function, and Elimination. Cold Spring Harb Perspect Biol. 2015;7:a020370.
Google Scholar
Chung WS, Clarke LE, Wang GX, Stafford BK, Sher A, Chakraborty C, et al. Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature. 2013;504:394–400.
Google Scholar
Logan MA, Freeman MR. The scoop on the fly brain: glial engulfment functions in Drosophila. Neuron Glia Biol. 2007;3:63–74.
Google Scholar
Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ. Unwrapping Glial Biology. Neuron. 2003;38:567–80.
Google Scholar
Reddien PW, Horvitz HR. The engulfment process of programmed cell death in Caenorhabditis elegans. Annu Rev Cell Dev Biol. 2004;20:193–221.
Google Scholar
Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, et al. The Classical Complement Cascade Mediates CNS Synapse Elimination. Cell. 2007;131:1164–78.
Google Scholar
Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, et al. Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner. Neuron. 2012;74:691–705.
Google Scholar
Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, et al. Synaptic Pruning by Microglia Is Necessary for Normal Brain Development. Science. 2011;333:1456–8.
Google Scholar
Dejanovic B, Wu T, Tsai MC, Graykowski D, Gandham VD, Rose CM, et al. Complement C1q-dependent excitatory and inhibitory synapse elimination by astrocytes and microglia in Alzheimer’s disease mouse models. Nat Aging. 2022;2:837–50.
Google Scholar
Favuzzi E, Huang S, Saldi GA, Binan L, Ibrahim LA, Fernández-Otero M, et al. GABA-receptive microglia selectively sculpt developing inhibitory circuits. Cell. 2021;184:4048–63.e32.
Google Scholar
Park J, Choi Y, Jung E, Lee S, Sohn J, Chung W. Microglial MERTK eliminates phosphatidylserine‐displaying inhibitory post‐synapses. EMBO J. 2021;40:e107121.
Google Scholar
Scott‐Hewitt N, Perrucci F, Morini R, Erreni M, Mahoney M, Witkowska A, et al. Local externalization of phosphatidylserine mediates developmental synaptic pruning by microglia. EMBO J. 2020;39:e105380.
Google Scholar
Schmidtner AK, Slattery DA, Gläsner J, Hiergeist A, Gryksa K, Malik VA, et al. Minocycline alters behavior, microglia and the gut microbiome in a trait-anxiety-dependent manner. Transl Psychiatry. 2019;9:223.
Google Scholar
Cullheim S, Thams S. The microglial networks of the brain and their role in neuronal network plasticity after lesion. Brain Res Rev. 2007;55:89–96.
Google Scholar
Datta D, Leslie SN, Morozov YM, Duque A, Rakic P, Van Dyck CH, et al. Classical complement cascade initiating C1q protein within neurons in the aged rhesus macaque dorsolateral prefrontal cortex. J Neuroinflammation. 2020;17:8.
Google Scholar
Geloso MC, D’Ambrosi N. Microglial Pruning: Relevance for Synaptic Dysfunction in Multiple Sclerosis and Related Experimental Models. Cells. 2021;10:686.
Google Scholar
Hammond TR, Robinton D, Stevens B. Microglia and the Brain: Complementary Partners in Development and Disease. Annu Rev Cell Dev Biol. 2018;34:523–44.
Google Scholar
Lee JH, Kim JY, Noh S, Lee H, Lee SY, Mun JY, et al. Astrocytes phagocytose adult hippocampal synapses for circuit homeostasis. Nature. 2021;590:612–7.
Google Scholar
Damisah EC, Hill RA, Rai A, Chen F, Rothlin CV, Ghosh S, et al. Astrocytes and microglia play orchestrated roles and respect phagocytic territories during neuronal corpse removal in vivo. Sci Adv. 2020;6:eaba3239.
Google Scholar
Eladl E, Tremblay-LeMay R, Rastgoo N, Musani R, Chen W, Liu A, et al. Role of CD47 in Hematological Malignancies. J Hematol OncolJ Hematol Oncol. 2020;13:96.
Google Scholar
Lehrman EK, Wilton DK, Litvina EY, Welsh CA, Chang ST, Frouin A, et al. CD47 Protects Synapses from Excess Microglia-Mediated Pruning during Development. Neuron. 2018;100:120–34.e6.
Google Scholar
Li J, Brickler T, Banuelos A, Marjon K, Shcherbina A, Banerjee S, et al. Overexpression of CD47 is associated with brain overgrowth and 16p11.2 deletion syndrome. Proc Natl Acad Sci. 2021;118:e2005483118.
Google Scholar
Chu Y, Jin X, Parada I, Pesic A, Stevens B, Barres B, et al. Enhanced synaptic connectivity and epilepsy in C1q knockout mice. Proc Natl Acad Sci. 2010;107:7975–80.
Google Scholar
Hong S, Beja-Glasser VF, Nfonoyim BM, Frouin A, Li S, Ramakrishnan S, et al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science. 2016;352:712–6.
Google Scholar
Dion-Albert L, Bandeira Binder L, Daigle B, Hong-Minh A, Lebel M, Menard C. Sex differences in the blood-brain barrier: implications for mental health. Front Neuroendocrinol. 2022;65:100989.
Google Scholar
Blokland GAM, Grove J, Chen CY, Cotsapas C, Tobet S, Handa R, et al. Sex-Dependent Shared and Nonshared Genetic Architecture Across Mood and Psychotic Disorders. Biol Psychiatry. 2022;91:102–17.
Google Scholar
Riecher-Rössler A. Sex and gender differences in mental disorders. Lancet Psychiatry. 2017;4:8–9.
Google Scholar
Ramiro L, Faura J, Simats A, García-Rodríguez P, Ma F, Martín L, et al. Influence of sex, age and diabetes on brain transcriptome and proteome modifications following cerebral ischemia. BMC Neurosci. 2023;24:7.
Google Scholar
Iturria-Medina Y, Adewale Q, Khan AF, Ducharme S, Rosa-Neto P, O’Donnell K, et al. Unified epigenomic, transcriptomic, proteomic, and metabolomic taxonomy of Alzheimer’s disease progression and heterogeneity. Sci Adv. 2022;8:eabo6764.
Google Scholar
López-Cerdán A, Andreu Z, Hidalgo MR, Grillo-Risco R, Català-Senent JF, Soler-Sáez I, et al. Unveiling sex-based differences in Parkinson’s disease: a comprehensive meta-analysis of transcriptomic studies. Biol Sex Differ. 2022;13:68.
Google Scholar
Maitra M, Mitsuhashi H, Rahimian R, Chawla A, Yang J, Fiori LM, et al. Cell type specific transcriptomic differences in depression show similar patterns between males and females but implicate distinct cell types and genes. Nat Commun. 2023;14:2912.
Google Scholar
Hyer MM, Phillips LL, Neigh GN. Sex Differences in Synaptic Plasticity: Hormones and Beyond. Front Mol Neurosci. 2018;11:266.
Google Scholar
Rutter M, Caspi A, Moffitt TE. Using sex differences in psychopathology to study causal mechanisms: unifying issues and research strategies: Using sex differences in psychopathology to study causal mechanisms. J Child Psychol Psychiatry. 2003;44:1092–115.
Google Scholar
Ziemka-Nalecz M, Pawelec P, Ziabska K, Zalewska T. Sex Differences in Brain Disorders. Int J Mol Sci. 2023;24:14571.
Google Scholar
Ruigrok ANV, Salimi-Khorshidi G, Lai MC, Baron-Cohen S, Lombardo MV, Tait RJ, et al. A meta-analysis of sex differences in human brain structure. Neurosci Biobehav Rev. 2014;39:34–50.
Google Scholar
Knickmeyer RC, Styner M, Short SJ, Lubach GR, Kang C, Hamer R, et al. Maturational Trajectories of Cortical Brain Development through the Pubertal Transition: Unique Species and Sex Differences in the Monkey Revealed through Structural Magnetic Resonance Imaging. Cereb Cortex. 2010;20:1053–63.
Google Scholar
Dehorter N, Del Pino I. Shifting Developmental Trajectories During Critical Periods of Brain Formation. Front Cell Neurosci. 2020;14:283.
Google Scholar
Rurak GM, Simard S, Freitas-Andrade M, Lacoste B, Charih F, Van Geel A, et al. Sex differences in developmental patterns of neocortical astroglia: A mouse translatome database. Cell Rep. 2022;38:110310.
Google Scholar
Clarkson J, Herbison AE. Hypothalamic control of the male neonatal testosterone surge. Philos Trans R Soc Lond B Biol Sci. 2016;371:20150115.
Google Scholar
Acaz-Fonseca E, Avila-Rodriguez M, Garcia-Segura LM, Barreto GE. Regulation of astroglia by gonadal steroid hormones under physiological and pathological conditions. Prog Neurobiol. 2016;144:5–26.
Google Scholar
Rurak GM, Woodside B, Aguilar-Valles A, Salmaso N. Astroglial cells as neuroendocrine targets in forebrain development: Implications for sex differences in psychiatric disease. Front Neuroendocrinol. 2021;60:100897.
Google Scholar
link
:quality(85):upscale()/2024/03/19/762/n/1922729/76003d6a65f9c8ba2968a9.89873204_.jpg "What Causes Postpartum Body Odor?")
