Nerve cells developmental processes and the dynamic role of cytokine signaling.
Cytokine dysregulation
Cytokines
Gliogenesis
Microglia
Neurogenesis
Journal
International journal of developmental neuroscience : the official journal of the International Society for Developmental Neuroscience
ISSN: 1873-474X
Titre abrégé: Int J Dev Neurosci
Pays: United States
ID NLM: 8401784
Informations de publication
Date de publication:
Oct 2019
Oct 2019
Historique:
received:
27
07
2018
revised:
13
11
2018
accepted:
14
11
2018
pubmed:
23
11
2018
medline:
22
4
2020
entrez:
23
11
2018
Statut:
ppublish
Résumé
The stunning diversity of neurons and glial cells makes possible the higher functions of the central nervous system (CNS), allowing the organism to sense, interpret and respond appropriately to the external environment. This cellular diversity derives from a single primary progenitor cell type initiating lineage leading to the formation of both differentiated neurons and glial cells. The processes governing the differentiation of the progenitor pool of cells into mature nerve cells will be here briefly reviewed. They involve morphological transformations, specialized modes of cell division, migration, and controlled cell death, and are regulated through cell-cell interactions and cues provided by the extracellular matrix, as well as by humoral factors from the cerebrospinal fluid and the blood system. In this respect, a quite large body of studies have been focused on cytokines, proteins representing the main signaling network that coordinates immune defense and the maintenance of homeostasis. At the same time, they are deeply involved in CNS development as regulatory factors. This dual role in the nervous system appears of particular relevance for CNS pathology, since cytokine dysregulation (occurring as a consequence of maternal infection, exposure to environmental factors or prenatal hypoxia) can profoundly impact on neurodevelopment and likely influence the response of the adult tissue during neuroinflammatory events.
Identifiants
pubmed: 30465872
doi: 10.1016/j.ijdevneu.2018.11.003
doi:
Substances chimiques
Cytokines
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
3-17Informations de copyright
Copyright © 2018 ISDN. Published by Elsevier Ltd. All rights reserved.
Références
E. Aaku-Saraste, A. Hellwig, W.B. Huttner. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure - remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol. 180: 1996; 664-679
J. Aarum, K. Sandberg, S.L. Haeberlein, M.A. Persson. Migration and differentiation of neural precursor cells can be directed by microglia. Proc. Natl. Acad. Sci. U. S. A. 100: 2003; 15983-15988
T. Adachi, H. Takanaga, M. Kunimoto, H. Asou. Influence of LIF and BMP-2 on differentiation and development of glial cells in primary cultures of embryonic rat cerebral hemisphere. J. Neurosci. Res. 79: 2005; 608-615
L.F. Agnati, D. Guidolin, M. Guescini, S. Genedani, K. Fuxe. Understanding wiring and volume transmission. Brain Res. Rev. 64: 2010; 137-159
L.F. Agnati, M. Marcoli, G. Maura, A. Woods, D. Guidolin. The brain as a “hyper-network”: the key role of neural networks as main producers of the integrated brain actions especially via the “broadcasted” neuroconnectomics. J. Neural Transm. 125: 2018; 883-897
H. Akiyama, P.L. McGeer. Brain microglia constitutively express b-2 integrins. J. Neuroimmunol. 30: 1990; 81-93
J. Altman, G.D. Das. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124: 1965; 319-335
A. Alvarez-Buylla, A. Kriegstein. Neural stem cells among glia J. Rubenstein, P. Rakic. Patterning and Cell Type Specification in the Developing CNS and PNS. Comprehensive Developmental Neuroscience 1. 2013; Elsevier: New York; 685-705
E.R. Andersson, N. Prakash, L. Cajanek, E. Minina, V. Bryja, L. Bryjova, T.P. Yamaguchi, A.C. Hall, W. Wurst, E. Arenas. Wnt5a regulates ventral midbrain morphogenesis and the development of A9-A10 dopaminergic cells in vivo. PLoS One. 3: 2008; e3517
D. Bachiller, J. Klingensmith, C. Kemp, J.A. Belo, R.M. Anderson, S.R. May, J.A. McMahon, A.P. McMahon, R.M. Harland, J. Rossant, E.M. De Robertis. The organizer factors Chordin and Noggin are required for mouse forebrain development. Nature. 403: 2000; 658-661
B. Badie, J. Schartner, J. Vorpahl, K. Preston. Interferon-gamma induces apoptosis and augments the expression of Fas and Fas ligand by microglia in vitro. Exp. Neurol. 162: 2000; 290-296
V. Barker, G. Middleton, F. Davey, A.M. Davies. TNFalpha contributes to the death of NGF-dependent neurons during development. Nat. Neurosci. 4: 2001; 1194-1198
F. Barnabé-Heider, J.A. Wasylnka, K.J. Fernandes, C. Porsche, M. Sendtner, D.R. Kaplan, F.D. Miller. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron. 48: 2005; 253-265
A.P. Barnes, F. Polleux. Establishment of axon-dendrite polarity in developing neurons. Ann. Rev. Neurosci. 32: 2009; 347-381
B.A. Barres, I.K. Hart, H.S. Coles, J.F. Burne, J.T. Voyvodic, W.D. Richardson, M.C. Raff. Cell death and control of cell survival in the oligodendrocyte lineage. Cell. 70: 1992; 31-46
B.A. Barres, M.C. Raff. Control of oligodendrocyte number in the developing rat optic nerve. Neuron. 12: 1994; 935-942
B.A. Barres. The mystery and magic of glia: a perspective on their roles in health and disease. Neuron. 60: 2008; 430-440
S.L. Barrow, A.K. McAllister. Molecular composition of developing glutamatergic synapses J. Rubenstein, P. Rakic. Cellular Migration and Formation of Neuronal Connections. Comprehensive Developmental Neuroscience 2. 2013; Elsevier: New York; 497-520
B. Batinic, A. Santrac, B. Divovic, T. Timic, T. Stankovic, A. Obradovic, S. Joksimovic, M.M. Savic. Lipopolysaccharide exposure during late embryogenesis results in diminished locomotor activity and amphetamine response in females and spatial cognition impairment in males in adult, but not adolescent rat offspring. Behav. Brain Res. 299: 2016; 72-80
S. Bauer. Cytokine control of adult neural stem cells. Ann. N. Y. Acad. Sci. U. S. A. 1153: 2009; 48-56
R. Beattie, S. Hippenmeyer. Mechanisms of radial glia progenitor cell lineage progression. FEBS Lett. 591: 2017; 3993-4008
B. Becher, S. Spath, J. Goverman. Cytokine networks in neuroinflammation. Nat. Rev. Immunol. 17: 2017; 49-59
M. Bentivoglio, P. Mazzarello. The history of radial glia. Brain Res. Bull. 49: 1999; 305-315
A.R. Bialas, B. Stevens. TGF-beta signaling regulates neuronal Clq expression and developmental synaptic refinement. Nat. Neurosci. 16: 2013; 1773-1782
S.D. Bilbo, C.L. Block, J.L. Bolton, R. Hanamsagar, P.K. Tran. Beyond infection - maternal immune activation by environmental factors, microglial development, and relevance for autistic spectrum disorders. Exp. Neurol. 299: 2018; 241-251
C.J. Bissonnette, L. Lyass, B.J. Bhattacharyya, A. Belmadani, R.J. Miller, J.A. Kessler. The controlled generation of functional basal forebrain cholinergic neurons from human embryonic stem cells. Stem Cells. 29: 2011; 802-811
M.A. Bonaguidi, T. McGuire, M. Hu, L. Kan, J. Samanta, J.A. Kessler. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development. 132: 2005; 5503-5514
M.A. Bonaguidi, M.A. Wheeler, J.S. Shapiro, R.P. Stadel, G.J. Sun, G.L. Ming, H. Song. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell. 145: 2011; 1142-1155
A.M. Bond, O.G. Bhalala, J.A. Kessler. The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Dev. Neurobiol. 72: 2012; 1068-1074
A.M. Bond, G. Ming, H. Song. Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell. 17: 2015; 385-395
A. Bonni, Y. Sun, M. Nadal-Vicens, A. Bhatt, D.A. Frank, I. Rozovsky, N. Stahl, G.D. Yancopoulos, M.E. Greenberg. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science. 278: 1997; 477-483
D.O. Borroto-Escuela, A.O. Tarakanov, K. Bechter, K. Fuxe. IL1R2, CCR2, and CXCR4 may form heteroreceptor complexes with NMDAR and D2R: relevance for schizophrenia. Front. Psychiatry. 8: 2017; 24
A. Borsini, P.A. Zunszain, S. Thuret, C.M. Pariante. The role of inflammatory cytokines as key modulators of neurogenesis. Trends Neurosci. 38: 2015; 145-157
L.M. Boulanger. Immune proteins in brain development and synaptic plasiticity. Neuron. 64: 2009; 93-109
J. Breton, Y. Mao-Draayer. Impact of cytokines on neural stem/progenitor cell fate. J. Neurol. Neurophysiol. 2011: 2011; S4
A.S. Brown, J. Hooton, C.A. Schaefer, H. Zhang, E. Petkova, V. Babulas, M. Perrin, J.M. Gorman, E.S. Susser. Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. Am. J. Psychiatry. 161: 2004; 889-895
S.E. Canetta, A.S. Brown. Prenatal infection, maternal immune activation, and risk for schizophrenia. Transl. Neurosci. 3: 2012; 320-327
L.S. Campos, A.J. Duarte, T. Branco, D. Henrique. mDll1 and mDll3 expression in the developing mouse brain: Role in the establishment of the early cortex. J. Neurosci. Res. 64: 2001; 590-598
K. Campbell, M. Götz. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 25: 2002; 235-238
A.E. Cardona, R.M. Ransohoff, K. Akassoglou. Microglia J. Rubenstein, P. Rakic. Cellular Migration and Formation of Neuronal Connections. Comprehensive Developmental Neuroscience 2. 2013; Elsevier: New York; 803-817
P.A. Carpentier, T.D. Palmer. Immune influence on adult neural stem cell regulation and function. Neuron. 64: 2009; 79-92
C.J. Carter, R.A. Blizard. Autism genes are selectively targeted by environmental pollutants including pesticides, heavy metals, bisphenol A, phthalates and many others in food, cosmetics or household products. Neurochem. Int. 101: 2016; 83-109
S.H. Chalasani, K.A. Sabelko, R.J. Sunshine, D.R. Littman, J.A. Raper. A Chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon path finding. J. Neurosci. 23: 2003; 1360-1371
D. Checchin, F. Sennlaub, E. Levavasseur, M. Leduc, S. Chemtob. Potential role of microglia in retinal blood vessel formation. Invest. Ophthalmol. Vis. Sci. 47: 2006; 3595
A. Chenn, C.A. Walsh. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 297: 2002; 365-369
T.H. Cheung, T.A. Rando. Molecular regulation of stem cell quiescence. Nat. Rev. Mol. Cell Biol. 14: 2013; 329-340
A. Chojnacki, T. Shimazaki, C. Gregg, G. Weinmaster, S. Weiss. Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J. Neurosci. 23: 2003; 1730-1741
K.M. Christian, H. Song, G.L. Ming. Functions and dysfunctions of adult hippocampal neurogenesis. Annu. Rev. Neurosci. 37: 2014; 243-262
J.C. Conover, R.Q. Notti. The neural stem cell niche. Cell Tissue Res. 331: 2008; 211-224
M.R. Costa, O. Bucholz, T. Schroeder, M. Götz. Late origin of glia-restricted progenitors in the developing mouse cerebral cortex. Cereb. Cortex. 19(Suppl. 1): 2009; i135-i143
C.L. Cunningham, V. Martínez-Cerdeño, S.C. Noctor. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33: 2013; 4216-4233
M. Czeh, P. Gressens, A.M. Kaindl. The yin and yang of microglia. Dev. Neurosci. 33: 2011; 199-209
I. Dalmau, B. Finsen, N. Tønder, J. Zimmer, B. González, B. Castellano. Development of microglia in the prenatal rat hippocampus. J. Comp. Neurol. 377: 1997; 70-84
A. de la Mano, A. Gato, M. Alonso, E. Carnicero, C. Martin, J.A. Moro. Role of interleukin-1beta in the control of neuroepithelial proliferation and differentiation of the spinal cord during development. Cytokine. 37: 2007; 128-137
W. Deng, J. Pleasure, D. Pleasure. Progress in periventricular leukomalacia. Arch. Neurol. 65: 2008; 1291-1295
L.P. Diniz, J.C. Almeida, V. Tortelli, C. Vargas Lopes, P. Setti-Perdigao, J. Stipursky, S.A. Kahn, L.F. Romão, J. de Miranda, S.V. Alves-Leon, J.M. de Souza, N.G. Castro, R. Panizzutti, F.C. Gomes. Astrocyte-induced synaptogenesis is mediated by transforming growth factor beta signaling through modulation of D-serine levels in cerebral cortex neurons. J. Biol. Chem. 287: 2012; 41432-41445
F. Doetsch, I. Caillé, D.A. Lim, J.M. Garcìa-Verdugo, A. Alvarez-Buylla. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97: 1999; 703-716
J. Falsig, J. van Beek, C. Hermann, M. Leist. Molecular basis for detection of invading pathogens in the brain. J. Neurosci. Res. 86: 2008; 1434-1447
L.M. Farkas, W.B. Huttner. The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr. Opin. Cell Biol. 20: 2008; 707-715
S.A. Fietz, I. Kelava, J. Vogt, M. Wilsch-Bräuninger, D. Stenzel, J.L. Fish, D. Corbeil, A. Riehn, W. Distler, R. Nitsch, W.B. Huttner. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13: 2010; 690-699
R.H. Fontaine, O. Cases, V. Lelièvre, B. Mesplés, J.C. Renauld, G. Loron, V. Degos, P. Dournaud, O. Baud, P. Gressens. IL-9/IL-9 receptor signaling selectively protects cortical neurons against developmental apoptosis. Cell Death Differ. 15: 2008; 1542-1552
M.G. Frank, M.D. Weber, L.R. Watkins, S.F. Maier. Stress-induced neuroinflammatory priming: a liability factor in the etiology of psychiatric disorders. Neurobiol. Stress. 4: 2016; 62-70
E.E. Frost, Z. Zhou, K. Krasnesky, R.C. Armstrong. Initiation of oligodendrocyte progenitor cell migration by a PDGF-A activated extracellular regulated kinase (ERK) signaling pathway. Neurochem. Res. 34: 2009; 169-181
L. Gao, R.H. Miller. Specification of optic nerve oligodendrocyte precursors by retinal ganglion cell axons. J. Neurosci. 29: 2006; 7619-7628
P. Gao, M.P. Postiglione, T.G. Krieger, L. Hernandez, C. Wang, Z. Han, C. Streicher, E. Papusheva, R. Insolera, K. Chugh, O. Kodish, K. Huang, B.D. Simons, L. Luo, S. Hippenmeyer, S.H. Shi. Deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell. 159: 2014; 775-788
G.A. Garden, T. Möller. Microglia biology in health and disease. J. Neuroimmune Pharmacol. 1: 2006; 127-137
P. Gasque, J.W. Neal, S.K. Singhrao, E.P. McGreal, Y.D. Dean, B.J. Van, B.P. Morgan. Roles of the complement system in human neurodegenerative disorders: pro-inflammatory and tissue remodeling activities. Mol. Neurobiol. 25: 2002; 1-17
S. Ge, K.A. Sailor, G.L. Ming, H. Song. Synaptic integration and plasticity of new neurons in the adult hippocampus. J. Physiol. 586: 2008; 3759-3765
F. Ginhoux, M. Prinz. Origin of microglia: current concepts and past controversies. Cold Spring Harb. Perspect. Biol. 7: 2015; a020537
D. Giulian, D.G. Young, J. Woodward, D.C. Brown, L.B. Lachman. Interleukin-1 is an astroglial growth factor in the developing brain. J. Neurosci. 8: 1988; 709-714
T. Goldmann, T. Blank, M. Prinz. Fine-tuning of type I IFN-signaling in microglia - implications for homeostasis, CNS autoimmunity and interferonopathies. Curr. Opin. Neurobiol. 36: 2016; 38-42
Y.N. Gorodilov. The fate of Spemann's organizer. Zool. Sci. 17: 2000; 1197-1220
M. Götz, W.B. Huttner. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6: 2005; 777-788
C. Gregg, S. Weiss. CNTF/LIF/gp130 receptor complex signaling maintains a VZ precursor differentiation gradient in the developing ventral forebrain. Development. 132: 2005; 565-578
E.A. Grove, E.S. Monuki. Morphogens, patterning centers, and their mechanism of action J. Rubenstein, P. Rakic. Patterning and Cell Type Specification in the Developing CNS and PNS. Comprehensive Developmental Neuroscience 1. 2013; Elsevier: New York; 25-43
T.I. Gudz, H. Komuro, W.B. Macklin. Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J. Neurosci. 26: 2006; 2458-2466
N. Guérout, X. Li, F. Barnabé-Heider. Cell fate control in the developing central nervous system. Exp. Cell Res. 321: 2014; 77-83
D. Guidolin, M. Marcoli, G. Maura, L.F. Agnati. New dimensions of connectomics and network plasticity in the central nervous system. Rev. Neurosci. 28: 2017; 113-132
D. Guidolin, M. Marcoli, C. Tortorella, M. Maura, L.F. Agnati. G protein-coupled receptor-receptor interactions give integrative dynamics to intercellular communication. Rev. Neurosci. 2018 10.1515/revneuro-2017-0087
W. Halfter, S. Dong, Y.P. Yip, M. Willem, U. Mayer. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 22: 2002; 6029-6040
U.K. Hanisch. Microglia as a source and target of cytokines. Glia. 40: 2002; 140-155
U.K. Hanisch, H. Kettenmann. Microglia: active sensors and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10: 2007; 1387-1394
D. Hartmann, B. De Strooper, P. Saftig. Presenilin-1 deficiency leads to loss of Cajal-Retzius neurons and cortical dysplasia similar to human type 2 lissencephaly. Curr. Biol. 9: 1999; 719-727
J. Hatakeyama, Y. Bessho, K. Katoh, S. Ookawara, M. Fujioka, F. Guillemot, R. Kageyama. Hes genes regulate size, shape and histogenesis of the nervous system by control of the timing of neural stem cell differentiation. Development. 131: 2004; 5539-5550
T. Hatta, K. Moriyama, K. Nakashima, T. Taga, H. Otani. The role of gp130 in cerebral cortical development: in vivo functional analysis in a mouse ex utero system. J. Neurosci. 22: 2002; 5516-5524
C. Hermann, J. Hohmeister, S. Demirakca, K. Zohsel, H. Flor. Long-term alteration of pain sensitivity in school-aged children with early pain experiences. Pain. 125: 2006; 278-285
S.E. Hickman, N.D. Kingery, T.K. Ohsumi, M.L. Borowsky, L.-C. Wang, T.K. Means, El.J. Khoury. The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16: 2013; 1896-1905
S. Hitoshi, T. Alexon, V. Tropepe, D. Donoviel, A.J. Elia, J.S. Nye, R.A. Conlon, T.W. Mak, A. Bernstein, D. van der Kooy. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 16: 2002; 846-858
B. Holtmann, S. Wiese, M. Samsam, K. Grohmann, D. Pennica, R. Martini, M. Sendtner. Triple knock-out of CNTF, LIF, and CT-1 defines cooperative and distinct roles of these neurotrophic factors for motoneuron maintenance and function. J. Neurosci. 25: 2005; 1778-1787
S. Hong, M.-R. Song. STAT3 but not STAT1 is required for astrocyte differentiation. PLoS One. 9: 2014; e86851
G.S. Huh, L.M. Boulanger, H. Du, P.A. Riquelme, T.M. Brotz, C.J. Shatz. Functional requirement for class I MHC in CNS development and plasticity. Science. 290: 2000; 2155-2159
N.Y. Ip, J. McClain, N.X. Barrezueta, T.H. Aldrich, L. Pan, Y. Li, S.J. Wiegand, B. Friedman, S. Davis, G.D. Yancopoulos. The alpha component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development. Neuron. 10: 1993; 89-102
A. Ishimura, R. Maeda, M. Takeda, M. Kikkawa, I.O. Daar, M. Maeno. Involvement of BMP-4/msx-1 and FGF pathways in neural induction in the Xenopus embryo. Dev. Growth Differ. 42: 2000; 307-316
A.A. Jarjour, T.E. Kennedy. Oligodendrocyte precursors on the move: mechanisms directing migration. Neuroscientist. 10: 2004; 99-105
G.M. Jonakait. The effects of maternal inflammation on neuronal development: possible mechanisms. Int. J. Dev. Neurosci. 25: 2007; 415-425
M. Kaneko, D. Stellwagen, R.C. Malenka, M.P. Stryker. Tumor necrosis factor-alpha mediates one component of competitive, experience dependent plasticity in developing visual cortex. Neuron. 58: 2008; 673-680
G. Kempermann, F.H. Gage. New nerve cells for the adult brain. Sci. Am. 280: 1999; 48-53
A. Kerever, J. Schnack, D. Vellinga, N. Ichikawa, C. Moon, E. Arikawa-Hirasawa, J.T. Efird, F. Mercier. Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells. 25: 2007; 2146-2157
I.J. Kim, H.N. Beck, P.J. Lein, D. Higgins. Interferon gamma induces retrograde dendritic retraction and inhibits synapse formation. J. Neurosci. 22: 2002; 4530-4539
R.S. Klein, J.B. Rubin, H.D. Gibson, E.N. DeHaan, X. Alvarez-Hernandez, R.A. Segal, A.D. Luster. SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development. 128: 2001; 1971-1981
E. Kokovay, Q. Shen, S. Temple. The incredible elastic brain: how neural stem cells expand our minds. Neuron. 60: 2008; 420-429
E. Kokovay, Y. Wang, G. Kusek, R. Wurster, P. Lederman, N. Lowry, Q. Shen, S. Temple. VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. Cell Stem Cell. 11: 2012; 220-230
H. Konishi, H. Kiyama, M. Ueno. Dual functions of microglia in the formation and refinement of neural circuits during development. Int. J. Dev. Neurosci. 2018 10.1016/j.ijdevneu.2018.09.009
C.T. Kuo, Z. Mirzadeh, M. Soriano-Navarro, M. Rasin, D. Wang, J. Shen, N. Sestan, J. Garcia-Verdugo, A. Alvarez-Buylla, L.Y. Jan, Y.N. Jan. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell. 127: 2006; 1253-1264
F.M. LaFerla, M.C. Sugarman, T.E. Lane, M.A. Leissring. Regional hypomyelination and dysplasia in transgenic mice with astrocyte-directed expression of interferon-gamma. J. Mol. Neurosci. 15: 2000; 45-59
D.C. Lagace, M.C. Whitman, M.A. Noonan, J.L. Ables, N.A. DeCarolis, A.A. Arguello, M.H. Donovan, S.J. Fischer, L.A. Farnbauch, R.D. Beech, R.J. DiLeone, C.A. Greer, C.D. Mandyam, A.J. Eisch. Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J. Neurosci. 27: 2007; 12623-12629
J.L. Laprairie, A.Z. Murphy. Neonatal injury alters adult pain sensitivity by increasing opioid tone in the periaqueductal gray. Front. Behav. Neurosci. 3: 2009; 31
M.K. Lehtinen, M.W. Zappaterra, X. Chen, Y.J. Yang, A.D. Hill, M. Lun, T. Maynard, D. Gonzalez, S. Kim, P. Ye, A.J. D'Ercole, E.T. Wong, A.S. La Mantia, C.A. Walsh. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron. 69: 2011; 893-905
M. Li, M. Sendtner, A. Smith. Essential function of LIF receptor in motor neurons. Nature. 378: 1995; 724-727
I. Lieberam, D. Agalliu, T. Nagasawa, J. Ericson, T. Jessell. A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron. 47: 2005; 667-679
D.A. Lim, A. Alvarez-Buylla. Adult neural stem cells stake their ground. Trends Neurosci. 37: 2014; 563-571
M. Lu, E.A. Grove, R.J. Miller. Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc. Natl Acad. Sci. 99: 2002; 7090-7095
A. Majumder, S. Banerjee, J.A. Harrill, D.W. Machacek, O. Mohamad, M. Bacanamwo, W.R. Mundy, L. Wei, S.K. Dhara, S.L. Stice. Neurotrophic effects of leukemia inhibitory factor on neural cells derived from human embryonic stem cells. Stem Cells. 30: 2012; 2387-2399
P. Malatesta, I. Appolloni, F. Calzolari. Radial glia and neural stem cells. Cell Tissue Res. 331: 2008; 165-178
N. Manabe, S. Hirai, F. Imai, H. Nakanishi, Y. Takay, S. Ohno. Association of ASIP/mPAR-3 with adherens junctions of mouse neuroepithelial cells. Dev. Dyn. 225: 2002; 61-69
N. Marichal, C. Reali, O. Trujillo-Cenòz, R.E. Russo. Spinal cord stem cells in their microenvironment: the ependyma as a stem cell niche. Adv. Exp. Med. Biol. 1041: 2017; 55-79
T.K. Matsui, R. Mori. Microglia support neural stem cell maintenance and growth. Biochem. Biophys. Res. Commun. 503: 2018; 1880-1884
P.L. McGeer, E.G. McGeer. The possible role of complement activation in Alzheimer disease. Trends Mol. Med. 8: 2002; 519-523
J.P. Medelnik, K. Roensch, S. Okawa, A. Del Sol, O. Chara, L. Mchedlishvili, E.M. Tanaka. Signaling-dependent control of apical membrane size and self-renewal in rosette-stage human neuroepithelial stem cells. Stem Cell Rep. 10: 2018; 1751-1765
M.F. Mehler, P.C. Mabie, G. Zhu, S. Gokhan, J.A. Kessler. Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate. Dev. Neurosci. 22: 2000; 74-85
K. Meletis, F. Barnabe-Heider, M. Carlen, E. Evergren, N. Tomilin, O. Shupliakov, J. Frisen. Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol. 6: 2008; e182
D.A. Menassa, D. Gomez-Nicola. Microglial dynamics during human brain development. Front. Immunol. 9: 2018; 1014
F.T. Merkle, Z. Mirzadeh, A. Alvarez-Buylla. Mosaic organization of neural stem cells in the adult brain. Science. 317: 2007; 381-384
L.C. Miller, S. Isa, G. LoPreste, J.G. Schaller, C.A. Dinarello. Neonatal interleukin-1 beta, interleukin-6, and tumor necrosis factor: cord blood levels and cellular production. J. Pediatr. 117: 1990; 961-965
R.H. Miller. Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol. 67: 2002; 451-467
R.H. Miller. Signaling pathways that regulate glial development and early migration - oligodendrocytes J. Rubenstein, P. Rakic. Cellular Migration and Formation of Neuronal Connections. Comprehensive Developmental Neuroscience 2. 2013; Elsevier: New York; 771-785
G.L. Ming, H. Song. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 70: 2011; 687-702
Z. Mirzadeh, F.T. Merkle, M. Soriano-Navarro, J.M. Garcia-Verdugo, A. Alvarez-Buylla. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell. 3: 2008; 265-278
T. Miyata, A. Kawaguchi, K. Saito, M. Kawano, T. Muto, M. Ogawa. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development. 131: 2004; 3133-3145
A.V. Molofsky, C. Hochstim, B. Deneen, D. Rowitch. Mechanisms of astrocyte development J. Rubenstein, P. Rakic. Cellular Migration and Formation of Neuronal Connections. Comprehensive Developmental Neuroscience 2. 2013; Elsevier: New York; 723-742
B.S. Moon, J.Y. Yoon, M.Y. Kim, S.H. Lee, T. Choi, K.Y. Choi. Bone morphogenetic protein 4 stimulates neuronal differentiation of neuronal stem cells through the ERK pathway. Exp. Mol. Med. 41: 2009; 116-125
L. Morizur, A. Chicheportiche, L.R. Gauthier, M. Daynac, F.D. Boussin, M.A. Mouthon. Distinct molecular signatures of quiescent and activated adult neural stem cells reveal specific interactions with their microenvironment. Stem Cell Rep. 11: 2018; 565-577
A. Mottahedin, M. Ardalan, T. Chumak, I. Riebe, J. Ek, G. Mallard. Effect of neuroinflammation on synaptic organization and function in the developing brain: implications for neurodevelopmental and neurodegenerative disorders. Front. Cell. Neurosci. 11: 2017; 190
A. Mousa, M. Bakhiet. Role of cytokine signaling during nervous system development. Int. J. Mol. Sci. 14: 2013; 13931-13957
A. Mukhopadhyay, T. McGuire, C.Y. Peng, J.A. Kessler. Differential effects of BMP signaling on parvalbumin and somatostatin interneuron differentiation. Development. 136: 2009; 2633-2642
H. Naka, S. Nakamura, T. Shimazaki, H. Okano. Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat. Neurosci. 11: 2008; 1014-1023
K. Nakashima, M. Yanagisawa, H. Arakawa, N. Kimura, T. Hisatsune, M. Kawabata, K. Miyazono, T. Taga. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science. 284: 1999; 479-482
K. Nakashima, S. Wiese, M. Yanagisawa, H. Arakawa, N. Kimura, T. Hisatsune, K. Yoshida, T. Kishimoto, M. Sendtner, T. Taga. Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J. Neurosci. 19: 1999; 5429-5434
M. Namihira, J. Kohyama, K. Semi, T. Sanosaka, B. Deneen, T. Taga, K. Nakashima. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev. Cell. 16: 2009; 245-255
M. Namihira, K. Nakashima. Mechanisms of astrocytogenesis in the mammalian brain. Curr. Opin. Neurobiol. 23: 2013; 921-927
E.A. Newman. Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. J. Neurosci. 21: 2001; 2215-2223
A. Nishiyama, X.H. Lin, N. Giese, C.H. Heldin, W.B. Stallcup. Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J. Neurosci. Res. 43: 1996; 299-314
A. Nishiyama, M. Komitova, R. Suzuki, X. Zhu. Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity. Nat. Rev. Neurosci. 10: 2009; 9-22
T. Otani, M.C. Marchetto, F.H. Gage, B.D. Simons, F.J. Livesey. 2D and 3D stem cell models of primate cortical development identify species-specific differences in progenitor behavior contributing to brain size. Cell Stem Cell. 18: 2016; 467-480
T.D. Palmer, J. Takahashi, F.H. Gage. The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci. 8: 1997; 389-404
R.C. Paolicelli, G. Bolasco, F. Pagani, L. Maggi, M. Scianni, P. Panzanelli, M. Giustetto, T.A. Ferreira, E. Guiducci, L. Dumas, D. Ragozzino, C.T. Gross. Synaptic pruning by microglia is necessary for normal brain development. Science. 333: 2011; 1456-1458
R.C. Paolicelli, M.T. Ferretti. Function and dysfunction of microglia during brain development: consequences for synapses and neural circuits. Front. Syn. Neurosci. 9: 2018; 9
P.H. Patterson. Immune involvement in schizophrenia and autism: etiology, pathology and animal models. Behav. Brain Res. 204: 2009; 313-321
A. Pereira, F.A. Furlan. Astrocytes and human cognition: modeling information integration and modulation of neuronal activity. Progr. Neurobiol. 92: 2010; 405-420
E.M. Perez Villegas, C. Olivier, N. Spassky, C. Poncet, P. Cochard, B. Zalc, J.L. Thomas, S. Martínez. Early specification of oligodendrocytes in the chick embryonic brain. Dev. Biol. 216: 1999; 98-113
F. Polleux. Development of neural polarity in vivo J. Rubenstein, P. Rakic. Cellular Migration and Formation of Neuronal Connections. Comprehensive Developmental Neuroscience 2. 2013; Elsevier: New York; 3-18
C. Porcheri, U. Suter, S. Jessberger. Dissecting integrin-dependent regulation of neural stem cell proliferation in the adult brain. J. Neurosci. 34: 2014; 5222-5232
M. Prinz, A. Mildner. Microglia in the CNS: immigrants from another world. Glia. 59: 2011; 177-187
X. Qian, Q. Shen, S.K. Goderie, W. He, A. Capela, A.A. Davis, S. Temple. Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron. 28: 2000; 69-80
M.C. Raff, R.H. Miller, M. Noble. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature. 303: 1983; 390-396
P. Rakic. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10: 2009; 724-735
R.M. Ransohoff, D. Schafer, A. Vincent, N.E. Blachère, A. Bar-Or. Neuroinflammation: ways in which the immune system affects the brain. Neurotherapeutics. 12: 2015; 896-909
M.S. Rao, M. Jacobson. Developmental Neurobiology. 2005; Kluwer Academic/Plenum: New York
J.A. Raper. Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol. 10: 2000; 88-94
M.R. Rasin, V.R. Gazula, J.J. Breunig, K.Y. Kwan, M.B. Johnson, S. Liu-Chen, H.-S. Li, L.Y. Jan, P. Rakic, N. Sestan. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 10: 2007; 819-827
B.A. Reynolds, S. Weiss. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255: 1992; 1707-1710
P. Rezaie. Microglia in the human nervous system during development. Neuroembriology. 2: 2003; 18-31
W.D. Richardson, N. Pringle, M.J. Mosley, B. Westermark, M. Dubois-Daicq. A role for platelet-derived growth factor in normal gliogenesis in the central nervous system. Cell. 53: 1988; 309-319
J.L.R. Rubenstein, P. Rakic. Patterning and Cell Types Specification in the Developing CNS and PNS. 2013; Elsevier: San Diego
A. Saito, S. Kanemoto, N. Kawasaki, R. Asada, H. Iwamoto, M. Oki, H. Miyagi, S. Izumi, T. Sanosaka, K. Nakashima, K. Imaizumi. Unfolded protein response, activated by OASIS family transcription factors, promotes astrocyte differentiation. Nat. Commun. 3: 2012; 967
J.M. Sanz, F. Di Virgilio. Kinetics and mechanism of ATP-dependent IL-1β release from microglial cells. J. Immunol. 164(4893): 2000; 4898
F. Sedel, C. Béchade, S. Vyas, A. Triller. Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death. J. Neurosci. 24: 2004; 2236-2246
J. See, P. Mamontov, K. Ahn, L. Wine-Lee, E.B. Crenshaw, J.B. Grinspan. BMP signaling mutant mice exhibit glial cell maturation defects. Mol. Cell. Neurosci. 35: 2007; 171-182
B. Seri, J.M. Garcia-Verdugo, L. Collado-Morente, B.S. McEwen, A. Alvarez-Buylla. Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J. Comp. Neurol. 478: 2004; 359-378
M. Shelly, L. Cancedda, S. Heilshorn, G. Sumbre, M.M. Poo. LKB1/STRAD promotes axon initiation during neuronal polarization. Cell. 129: 2007; 565-577
L. Shi, S.H. Fatemi, R.W. Sidwell, P.H. Patterson. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23: 2003; 297-302
L. Shi, S.E. Smith, N. Malkova, D. Tse, Y. Su, P.H. Patterson. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav. Immun. 23: 2009; 116-123
J. Shin, D.A. Berg, Y. Zhu, J.Y. Shin, J. Song, M.A. Bonaguidi, G. Enikolopov, D.W. Nauen, K.M. Christian, G.L. Ming, H. Song. Single-cell RNA-Seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell. 17: 2015; 360-372
J.A. Siegenthaler, A.M. Ashique, K. Zarbalis, K.P. Patterson, J.H. Hecht, M.A. Kane, A.E. Folias, Y. Choe, S.R. May, T. Kume, J.L. Napoli, A.S. Peterson, S.J. Pleasure. Retinoic acid from the meninges regulates cortical neuron generation. Cell. 139: 2009; 597-609
J.C. Silbereis, S. Pochareddy, Y. Zhu, M. Li, N. Sestan. The cellular and molecular landscapes of the developing human central nervous system. Neuron. 89: 2016; 248-268
S.D. Skaper, L. Facci, M. Zusso, P. Giusti. An inflammation-centric view of neurological disease: beyond the neuron. Front. Cell. Neurosci. 12: 2018; 72
J.A. Smith, A. Das, S.K. Ray, N.L. Banik. Role of proinflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull. 87: 2012; 10-20
L.K. Smith, Y. He, J.S. Park, G. Bieri, C.E. Snethlage, K. Lin, G. Gontier, R. Wabl, K.E. Plambeck, J. Udeochu, E.G. Wheatley, J. Bouchard, A. Eggel, R. Narasimha, J.L. Grant, J. Luo, T. Wyss-Coray, S.A. Villeda. b2-microglobulin is a systemic pro-aging factor that impairs cognitive function and neurogenesis. Nat. Med. 21: 2015; 932-937
M.V. Sofroniew, H.V. Vinters. Astrocytes: biology and pathology. Acta Neuropathol. 119: 2010; 7-35
M.N. Spann, A. Sourander, H.M. Surcel, S. Hinkka-Yli-Salomaki, A.S. Brown. Prenatal toxoplasmosis antibody and childhood autism. Autism Res. 10: 2017; 769-777
N. Spassky, F. de Castro, B. Le Bras, K. Heydon, F. Quéraud-LeSaux, E. Bloch-Gallego, A. Chédotal, B. Zalc, J.L. Thomas. Directional guidance of oligodendroglial migration by class 3 semaphorins and netrin-1. J. Neurosci. 22: 2002; 5992-6004
N. Spassky, F.T. Merkle, N. Flames, A.D. Tramontin, J.M. Garcia-Verdugo, A. Alvarez-Buylla. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci. 25: 2005; 10-18
P. Squarzoni, G. Oller, G. Hoeffel, L. Pont-Lezica, P. Rostaing, D. Low, B. Bessis, F. Ginhoux, S. Garel. Microglia modulate wiring of the embryonic forebrain. Cell Rep. 8: 2014; 1271-1279
M. Stangel, A. Compston. Polyclonal immunoglobulins (IVIg) modulate nitric oxide production and microglial functions in vitro via Fc receptors. J. Neuroimmunol. 112: 2001; 63-71
B. Steiner, G. Kronenberg, S. Jessberger, M.D. Brandt, K. Reuter, G. Kempermann. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia. 46: 2004; 41-52
D. Stellwagen, R.C. Malenka. Synaptic scaling mediated by glial TNF-alpha. Nature. 440: 2006; 1054-1059
B. Stevens, N.J. Allen, L.E. Vazquez, G.R. Howell, K.S. Christopherson, N. Nouri, K.D. Micheva, A.K. Mehalow, A.D. Huberman, B. Stafford, A. Sher, A.M. Litke, J.D. Lambris, S.J. Smithm, S.W. John, B.A. Barres. The classical complement cascade mediates CNS synapse elimination. Cell. 131: 2007; 1164-1178
H.B. Stolp. Neuropoietic cytokines in normal brain development and neurodevelopmental disorders. Mol. Cell. Neurosci. 53: 2013; 63-68
D. Stubbs, J. Deproto, K. Nie, C. Englund, I. Mahmud, R. Hevner, Z. Molnár. Neurovascular congruence during cerebral cortical development. Cereb. Cortex. 19(Supp.1): 2009; i32-i41
H. Suh, A. Consiglio, J. Ray, T. Sawai, K.A. D'Amour, F.H. Gage. In vivo fate analysis reveals the multipotent and self-renewal capacities of sox2(þ) neural stem cells in the adult hippocampus. Cell Stem Cell. 1: 2007; 515-528
Y. Sun, M. Nadal-Vicens, S. Misono, M.Z. Lin, A. Zubiaga, X. Hua, G. Fan, M.E. Greenberg. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell. 104: 2001; 365-376
T. Takizawa, K. Nakashima, M. Namihira, W. Ochiai, A. Uemura, M. Yanagisawa, N. Fujita, M. Nakao, T. Taga. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell. 1: 2001; 749-758
S. Temple, Q. Shen. Cell biology of neuronal progenitor cells J. Rubenstein, P. Rakic. Patterning and Cell Type Specification in the Developing CNS and PNS. Comprehensive Developmental Neuroscience 1. 2013; Elsevier: San Diego; 261-283
P.B. Tran, R.J. Miller. Chemokine receptors: signposts to brain development and disease. Nat. Rev. Neurosci. 4: 2003; 444-455
H.H. Tsai, E. Frost, V. To, S. Robinson, C. Ffrench-Constant, R. Geertman, R.M. Ransohoff, R.H. Miller. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell. 110: 2002; 373-383
H.-H. Tsai, M. Tessier-Lavinge, R.H. Miller. Netrin I mediates spinal cord oligodendrocyte precursor dispersal. Development. 130: 2003; 2095-2105
F.M. Vaccarino, M.L. Schwartz, R. Raballo, J. Nilsen, J. Rhee, M. Zhou, T. Doetschman, J.D. Coffin, J.J. Wyland, Y.T. Hung. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat. Neurosci. 2: 1999; 246-253
S.U. Vay, L.J. Flitsch, M. Rabenstein, R. Rogall, S. Blaschke, J. Kleinhaus, N. Reinert, A. Bach, G.R. Fink, M. Schroeter, M.A. Rueger. The plasticity of primary microglia and their multifaceted effects on endogenous neural stem cells in vitro and in vivo. J. Neuroinflamm. 15: 2018; 226
C. Verney, A. Monier, C. Fallet-Bianco, P. Gressens. Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J. Anat. 217: 2010; 436-448
C.S. von Bartheld, J. Bahnev, S. Herculano-Houzel. The search for true numbers of neurons and glial cells in the human brain: a review of 150 years of cell counting. J. Comp. Neurol. 524: 2016; 3865-3895
N. Vunnam, C.H. Lo, B.D. Grant, D.D. Thomas, J.N. Sachs. Soluble extracellular domain of death receptor 5 inhibits TRAIL-Induced apoptosis by disrupting receptor-Receptor interactions. J. Mol. Biol. 429: 2017; 2943-2953
B.C. Warf, J. Fok-Seang, R.H. Miller. Evidence for the ventral origin of oligodendrocyte precursors in the rat spinal cord. J. Neurosci. 11: 1991; 2477-2488
G.E. White, D.R. Greaves. Fractalkine: one chemokine, many functions. Blood. 113: 2009; 767-768
A. Wodarz, W.B. Huttner. Asymmetric cell division during neurogenesis in Drosophila and vertebrates. Mech. Dev. 120: 2003; 1297-1309
Y. Wu, L. Dissing-Olesen, B.A. MacVicar, B. Stevens. Microglia: dynamic mediators of synapse development and plasticity. Trends Immunol. 36: 2015; 605-613
L. Xiao, N. Michalski, E. Kronander, E. Gjoni, C. Genoud, G. Knott, R. Schneggenburger. BMP signaling specifies the development of a large and fast CNS synapse. Nat. Neurosci. 16: 2013; 856-864
Y.L. Xing, P.T. Röth, J.A. Stratton, B.H. Chuang, J. Danne, S.L. Ellis, S.W. Ng, T.J. Kilpatrick, T.D. Merson. Adult neural precursor cells from the subventricular zone contribute significantly to oligodendrocyte regeneration and remyelination. J. Neurosci. 34: 2014; 14128-14146
W. Ye, K. Shimamura, J.L. Rubenstein, M.A. Hynes, A. Rosenthal. FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell. 93: 1998; 755-766
J.J. Yi, A.P. Barnes, R. Hand, F. Polleux, M.D. Ehlers. TGF-β signaling specifies axons during brain development. Cell. 142: 2010; 144-157
B.H. Yoon, R. Romero, C.J. Kim, J.K. Jun, R. Gomez, J.H. Choi, H.C. Syn. Amniotic fluid interleukin-6: a sensitive test for antenatal diagnosis of acute inflammatory lesions of preterm placenta and prediction of perinatal morbidity. Am. J. Obstet. Gynecol. 172: 1995; 960-970
K.J. Yoon, B.K. Koo, S.K. Im, H.W. Jeong, J. Ghim, M.C. Kwon, J.S. Moon, T. Miyata, Y.Y. Kong. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron. 58: 2008; 519-531
A.M.H. Young, B. Chakrabarti, D. Roberts, M.-C. Lai, J. Suckling, S. Baron-Cohen. From molecules to neural morphology: understanding neuroinflammation in autism spectrum condition. Mol. Autism. 7: 2016; 9
O. Zerbo, Y. Qian, C. Yoshida, J.K. Grether, J. Van de Water, L.A. Croen. Maternal infection during pregnancy and autism Spectrum disorders. J. Autism Dev. Disord. 45: 2015; 4015-4025
A.B. Zhadanov, D.W. Provance, C.A. Speer, J.D. Coffin, D. Goss, J.A. Blixt, C.M. Reichert, J.A. Mercer. Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development. Curr. Biol. 9: 1999; 880-888
Y. Zhang, C. Taveggia, C. Melendez-Vasquez, S. Einheber, C.S. Raine, J.L. Salzer, C.F. Brosnan, G.R. John. Interleukin-11 potentiates oligodendrocyte survival and maturation, and myelin formation. J. Neurosci. 26: 2006; 12174-12185
Y. Zhu, T. Yu, X. Zhang, T. Nagasawa, J.Y. Wu, Y. Rao. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat. Neurosci. 5: 2002; 719
H. Zuo, A. Nishiyama. Polydendrocytes in development and myelin repair. Neurosci. Bull. 29: 2013; 165-176
M. Zusso, P. Debetto, D. Guidolin, M. Barbierato, H. Manev, P. Giusti. Fluoxetine-induced proliferation and differentiation of neural progenitors cells isolated from rat postnatal cerebellum. Biochem. Pharmacol. 76: 2008; 391-403