Schwann cells and astrocytes induce synapse formation by spinal motor neurons in culture

被引:138
作者
Ullian, EM
Harris, BT
Wu, A
Chan, JR
Barres, BA
机构
[1] Stanford Univ, Sch Med, Dept Neurobiol, Stanford, CA 94305 USA
[2] Stanford Med Sch, Dept Pathol, Stanford, CA USA
关键词
D O I
10.1016/j.mcn.2003.10.011
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Glia constitute 90% of cells in the human nervous system, but relatively little is known about their functions. We have been focusing on the potential synaptic roles of glia in the CNS. We recently found that astrocytes increase the number of mature, functional synapses on retinal ganglion cells (RGCs) by sevenfold and are required for synaptic maintenance in vitro. These observations raised the question of whether glia similarly enhance synapse formation by other neuron types. Here we have investigated whether highly purified motor neurons isolated from developing rat spinal cords are able to form synapses in the absence of glia or whether glia similarly enhance synapse number. We show that spinal motor neurons (SMNs) form few synapses unless Schwann cells or astrocytes are present. Schwann cells increase the number of functional synapses by ninefold as measured by immunostaining, and increase spontaneous synaptic activity by several hundredfold. Surprisingly, the synapses formed between spinal motor neurons were primarily glutamatergic, as they could be blocked by CNQX. This synapse-promoting activity is not mediated by direct glial-neuronal cell contact but rather is mediated by secreted molecule(s) from the Schwann cells, as we previously found for astrocytes. Interestingly, the synapse-promoting activity from astrocytes and Schwann cells was functionally similar: Schwann cells also promoted synapse formation between retinal ganglion cells, and astrocytes promoted synapse formation between spinal motor neurons. These studies show that both astrocytes and Schwann cells strongly promote synapse formation between spinal motor neurons and demonstrate that glial regulation of synaptogenesis extends to other neuron types. (C) 2004 Elsevier Inc. All rights reserved.
引用
收藏
页码:241 / 251
页数:11
相关论文
共 61 条
[1]   Tripartite synapses: glia, the unacknowledged partner [J].
Araque, A ;
Parpura, V ;
Sanzgiri, RP ;
Haydon, PG .
TRENDS IN NEUROSCIENCES, 1999, 22 (05) :208-215
[2]   Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons [J].
Araque, A ;
Parpura, V ;
Sanzgiri, RP ;
Haydon, PG .
EUROPEAN JOURNAL OF NEUROSCIENCE, 1998, 10 (06) :2129-2142
[3]   Cultured motor neurons possess calcium-permeable AMPA/kainate receptors [J].
Bar-Peled, O ;
O'Brien, RJ ;
Morrison, JH ;
Rothstein, JD .
NEUROREPORT, 1999, 10 (04) :855-859
[4]   IMMUNOLOGICAL, MORPHOLOGICAL, AND ELECTROPHYSIOLOGICAL VARIATION AMONG RETINAL GANGLION-CELLS PURIFIED BY PANNING [J].
BARRES, BA ;
SILVERSTEIN, BE ;
COREY, DP ;
CHUN, LLY .
NEURON, 1988, 1 (09) :791-803
[5]   EXCITATORY AND INHIBITORY AUTAPTIC CURRENTS IN ISOLATED HIPPOCAMPAL-NEURONS MAINTAINED IN CELL-CULTURE [J].
BEKKERS, JM ;
STEVENS, CF .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1991, 88 (17) :7834-7838
[6]  
Bergles DE, 1998, J NEUROSCI, V18, P7709
[7]   PURIFICATION OF EMBRYONIC RAT MOTONEURONS BY PANNING ON A MONOCLONAL-ANTIBODY TO THE LOW-AFFINITY NGF RECEPTOR [J].
CAMU, W ;
HENDERSON, CE .
JOURNAL OF NEUROSCIENCE METHODS, 1992, 44 (01) :59-70
[8]   Nicotinic excitation of rat hypoglossal motoneurons [J].
Chamberlin, NL ;
Bocchiaro, CM ;
Greene, RW ;
Feldman, JL .
NEUROSCIENCE, 2002, 115 (03) :861-870
[9]   Progesterone synthesized by Schwann cells during myelin formation regulates neuronal gene expression [J].
Chan, JR ;
Rodriguez-Waitkus, PM ;
Ng, BK ;
Liang, P ;
Glaser, M .
MOLECULAR BIOLOGY OF THE CELL, 2000, 11 (07) :2283-2295
[10]   Neuroscience - New insights into neuron-glia communication [J].
Fields, RD ;
Stevens-Graham, B .
SCIENCE, 2002, 298 (5593) :556-562