Role of glia in synapse development

Recent studies suggest that glial cells regulate certain aspects of synapse development. Neurons can form synapses without glia, but may require glia-derived cholesterol to form numerous and efficient synapses. During synapse maturation, soluble and contact-dependent factors from glia may influence the composition of the postsynaptic density. Finally, synaptic connections appear to require glia to support their structural stability. Given the new evidence, it may be time now to acknowledge glia as a source for synaptogenesis-promoting signals. Scrutinizing the molecular mechanisms underlying this new function of glia and testing its relevance in vivo may help to understand how synapses develop and why they degenerate under pathological conditions.

[1]  S. Oliet.  Functional Consequences of Morphological Neuroglial Changes in the Magnocellular Nuclei of the Hypothalamus , 2002, Journal of neuroendocrinology.

[2]  W. Kakegawa,et al.  Glia-Synapse Interaction Through Ca2+-Permeable AMPA Receptors in Bergmann Glia , 2001, Science.

[3]  C. Lesuisse,et al.  Regulation of agrin expression in hippocampal neurons by cell contact and electrical activity. , 2000, Brain research. Molecular brain research.

[4]  R. Balice-Gordon,et al.  Activity-dependent editing of neuromuscular synaptic connections , 2000, Brain Research Bulletin.

[5]  C. Pariante,et al.  Glial cell abnormalities in major psychiatric disorders: the evidence and implications , 2001, Brain Research Bulletin.

[6]  D. Benson,et al.  Stages of Synapse Development Defined by Dependence on F-Actin , 2001, The Journal of Neuroscience.

[7]  M. Sheng,et al.  Development of neuron–neuron synapses , 2000, Current Opinion in Neurobiology.

[8]  A. Volterra,et al.  A neuron–glia signalling network in the active brain , 2001, Current Opinion in Neurobiology.

[9]  G. Cao,et al.  Schwann Cells Express Active Agrin and Enhance Aggregation of Acetylcholine Receptors on Muscle Fibers , 2001, The Journal of Neuroscience.

[10]  R. Mirsky,et al.  Schwann cells as regulators of nerve development , 2002, Journal of Physiology-Paris.

[11]  Yangzhou Du,et al.  Oligodendrocytes as providers of growth factors , 2002, Journal of neuroscience research.

[12]  T. Deerinck,et al.  Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  G. Lemke,et al.  Glial control of neuronal development. , 2001, Annual review of neuroscience.

[14]  B. Gusterson,et al.  Inducible ablation of astrocytes shows that these cells are required for neuronal survival in the adult brain , 2001, Glia.

[15]  Stephen J. Smith,et al.  Knowing a Nascent Synapse When You See It , 2002, Neuron.

[16]  A. Fagan,et al.  Astrocyte lipoproteins, effects of apoE on neuronal function, and role of apoE in amyloid‐β deposition in vivo , 2000, Microscopy research and technique.

[17]  P. Caroni,et al.  Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. , 1999, Genes & development.

[18]  H. Kimelberg,et al.  Neuronal–glial interactions and behaviour , 2000, Neuroscience & Biobehavioral Reviews.

[19]  A. Araque,et al.  Dynamic signaling between astrocytes and neurons. , 2001, Annual review of physiology.

[20]  L. Mucke,et al.  Genetically-targeted and conditionally-regulated ablation of astroglial cells in the central, enteric and peripheral nervous systems in adult transgenic mice 1 Published on the World Wide Web on 7 June 1999. 1 , 1999, Brain Research.

[21]  Stephen J. Smith,et al.  Stability and Plasticity of Developing Synapses in Hippocampal Neuronal Cultures , 2002, The Journal of Neuroscience.

[22]  L. Garcia-Segura,et al.  Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. , 1999, Journal of neurobiology.

[23]  T. Hummel,et al.  Glial cell development in Drosophila , 2001, International Journal of Developmental Neuroscience.

[24]  M. Bennett,et al.  Formation and Function of Synapses with Respect to Schwann Cells at the End of Motor Nerve Terminal Branches on Mature Amphibian (Bufo marinus) Muscle , 2001, The Journal of Neuroscience.

[25]  F. Pfrieger.  Role of cholesterol in synapse formation and function. , 2003, Biochimica et biophysica acta.

[26]  F. Pfrieger,et al.  Glia‐derived signals induce synapse formation in neurones of the rat central nervous system , 2001, The Journal of physiology.

[27]  John G. Parnavelas,et al.  Modes of neuronal migration in the developing cerebral cortex , 2002, Nature Reviews Neuroscience.

[28]  D. Featherstone,et al.  Surprises from Drosophila: genetic mechanisms of synaptic development and plasticity , 2000, Brain Research Bulletin.

[29]  B. Barres,et al.  Control of synapse number by glia. , 2001, Science.

[30]  R. Malenka,et al.  Control of synaptic strength by glial TNFalpha. , 2002, Science.

[31]  J. Lichtman,et al.  Synapse Elimination and Indelible Memory , 2000, Neuron.

[32]  M. Werle,et al.  Matrix metalloproteinase-3 removes agrin from synaptic basal lamina. , 2000, Journal of neurobiology.

[33]  L. A. Cavalcante,et al.  Synaptogenesis in Retino-Receptive Layers of the Superior Colliculus of the Opossum Didelphis marsupialis , 1999, Brain, Behavior and Evolution.

[34]  F. Gage,et al.  Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons , 2002, Nature Neuroscience.

[35]  J. Trachtenberg,et al.  Nerve Terminal Withdrawal from Rat Neuromuscular Junctions Induced by Neuregulin and Schwann Cells , 1997, The Journal of Neuroscience.

[36]  F. Pfrieger.  Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes? , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  Terrance J. Williams,et al.  Testosterone Regulates Terminal Schwann Cell Number and Junctional Size during Developmental Synapse Elimination , 2002, Developmental Neuroscience.

[38]  J. Sanes,et al.  Synaptic laminin prevents glial entry into the synaptic cleft , 1998, Nature.

[39]  E. Borrelli,et al.  A Transgenic Mouse Model for Inducible and Reversible Dysmyelination , 2000, The Journal of Neuroscience.

[40]  E. Peles,et al.  Molecular domains of myelinated axons , 2000, Current Opinion in Neurobiology.

[41]  Wade Morishita,et al.  Control of Synaptic Strength by Glial TNFα , 2002, Science.

[42]  C. Garner,et al.  The presynaptic cytomatrix of brain synapses , 2001, Cellular and Molecular Life Sciences CMLS.

[43]  J. Lubischer,et al.  Regulation of Terminal Schwann Cell Number at the Adult Neuromuscular Junction , 1999, The Journal of Neuroscience.

[44]  J. Sanes,et al.  An Intrinsic Distinction in Neuromuscular Junction Assembly and Maintenance in Different Skeletal Muscles , 2002, Neuron.

[45]  D. Talmage,et al.  Cysteine-Rich Domain Isoforms of the Neuregulin-1 Gene Are Required for Maintenance of Peripheral Synapses , 2000, Neuron.

[46]  F. Seil,et al.  Interactions between cerebellar Purkinje cells and their associated astrocytes. , 2001, Histology and histopathology.

[47]  M. Svensson,et al.  Glial responses to synaptic damage and plasticity , 1999, Journal of neuroscience research.

[48]  C. Göritz,et al.  Role of glia-derived cholesterol in synaptogenesis: new revelations in the synapse–glia affair , 2002, Journal of Physiology-Paris.

[49]  J. Duncan,et al.  An adaptive coding model of neural function in prefrontal cortex , 2001, Nature Reviews Neuroscience.

[50]  Shiaoping C. Zhu,et al.  A Glia-Derived Signal Regulating Neuronal Differentiation , 2000, The Journal of Neuroscience.

[51]  R. Fields,et al.  ATP: an extracellular signaling molecule between neurons and glia , 2000, Trends in Neurosciences.

[52]  F. Pfrieger,et al.  Synaptic efficacy enhanced by glial cells in vitro. , 1997, Science.

[53]  A. Messing.  Transgenic studies of peripheral and central glia. , 1998, The International journal of developmental biology.

[54]  P. Haydon.  Glia: listening and talking to the synapse , 2001, Nature Reviews Neuroscience.

[55]  B. Barres,et al.  Up a Notch Instructing Gliogenesis , 2000, Neuron.

[56]  M. Nedergaard,et al.  Astrocytes in the aging brain , 2002, Journal of neuroscience research.

[57]  C. Göritz,et al.  CNS synaptogenesis promoted by glia-derived cholesterol. , 2001, Science.

[58]  F. Gomes,et al.  Cross-talk between neurons and glia: highlights on soluble factors. , 2001, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[59]  Yishi Jin,et al.  Synaptogenesis: insights from worm and fly , 2002, Current Opinion in Neurobiology.

[60]  A. Villa,et al.  Agrin Controls Synaptic Differentiation in Hippocampal Neurons , 2000, The Journal of Neuroscience.

[61]  D. Spencer,et al.  Differential neurite growth on astrocyte substrates: interspecies facilitation in green fluorescent protein-transfected rat and human neurons , 1999, Neuroscience.

[62]  J. Sanes,et al.  Development of the vertebrate neuromuscular junction. , 1999, Annual review of neuroscience.

[63]  J. Vanderluit,et al.  Model for focal demyelination of the spinal dorsal columns of transgenic MBP‐LacZ mice by phototargeted ablation of oligodendrocytes , 2000, Journal of neuroscience research.

[64]  K. Belmonte,et al.  Developmental Expression of Muscarinic Acetylcholine Receptors in Chick Retina: Selective Induction of M2 Muscarinic Receptor Expression In Ovo by a Factor Secreted by Müller Glial Cells , 2000, The Journal of Neuroscience.

[65]  C. Ko,et al.  The role of perisynaptic Schwann cells in development of neuromuscular junctions in the frog (Xenopus laevis). , 2000, Journal of neurobiology.

[66]  N. Ziv,et al.  Molecular mechanisms of CNS synaptogenesis , 2002, Trends in Neurosciences.

[67]  Frank W Pfrieger,et al.  New views on synapse—glia interactions , 1996, Current Opinion in Neurobiology.

[68]  D. Poulain,et al.  Maternity leads to morphological synaptic plasticity in the oxytocin system. , 2001, Progress in brain research.

[69]  V. Gallo,et al.  Glutamate receptors in glia: new cells, new inputs and new functions. , 2000, Trends in pharmacological sciences.

[70]  P. Magistretti,et al.  The astrocyte-mediated coupling between synaptic activity and energy metabolism operates through volume transmission. , 2000, Progress in brain research.

[71]  C. Stiles,et al.  Molecular mechanisms controlling cortical gliogenesis , 2002, Current Opinion in Neurobiology.

[72]  R. Robitaille,et al.  Glial cells as active partners in synaptic functions. , 2001, Progress in brain research.

[73]  J. Barker,et al.  Astrocytes regulate the developmental appearance of GABAergic and glutamatergic postsynaptic currents in cultured embryonic rat spinal neurons , 1999, European Journal of Neuroscience.

[74]  戸田 弘紀.  Neurons generated from adult rat hippocampal stem cells form functional glutamatergic and GABAergic synapses in vitro , 2001 .

[75]  J. Sanes,et al.  Induction, assembly, maturation and maintenance of a postsynaptic apparatus , 2001, Nature reviews. Neuroscience.

[76]  D. Benson,et al.  Development and molecular organization of dendritic spines and their synapses , 2000, Hippocampus.

[77]  M. King,et al.  Differentiation of glial cells and motor neurons during the formation of neuromuscular junctions in cocultures of rat spinal cord explant and human muscle , 2001, The Journal of comparative neurology.

[78]  J. Warter,et al.  Cell types required to efficiently innervate human muscle cells in vitro. , 2000, Experimental cell research.