Home LiteratureArticle Details
PMID: 10234016 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Muscarinic control of cytoskeleton in perisynaptic glia.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 19 ·No. 10 ·1999-05-15 ·Pages 3836-46

Georgiou J, Robitaille R, Charlton MP

Abstract

Similar to astrocytes at CNS synapses, perisynaptic Schwann cells (PSCs) surround nerve terminals at the neuromuscular junction (NMJ). These special teloglial cells are sensitive to neurotransmitters and upregulate glial fibrillary acidic protein (GFAP) when deprived of synaptic activity. We found that activation of muscarinic acetylcholine receptors (mAChRs) at PSCs, but not purinergic (ATP and adenosine) or peptidergic [substance P (SP) and calcitonin gene-related peptide (CGRP)] receptors, prevented this upregulation. When applied onto single PSCs, muscarine evoked Ca2+ responses that fatigued but prevented upregulation of this glial cytoskeletal protein. Application of ATP onto single PSCs evoked Ca2+ signals that showed little fatigue, and GFAP upregulation occurred. Thus, Ca2+ signals alone cannot prevent GFAP upregulation in the PSCs. After blockade of cholinergic receptors by gallamine, neuronal activity was not effective in maintaining low GFAP levels in the perisynaptic glia. Last, immunohistochemistry disclosed mAChRs on PSCs and nearby fibroblasts. Thus, acetylcholine secreted by the nerve terminal acts on the PSCs via mAChRs to regulate GFAP. Cytoskeletal changes may influence perisynaptic glial functions, including growth, remodeling, and modulation of the synapse.

MeSH Terms
Animals Calcium/metabolism Cytoskeleton/physiology Glial Fibrillary Acidic Protein/metabolism Muscarinic Antagonists/pharmacology Neurotransmitter Agents/physiology Rana pipiens Receptors, Muscarinic/physiology Schwann Cells/metabolism,physiology Signal Transduction/physiology Synapses/physiology Up-Regulation
Chemicals
Glial Fibrillary Acidic Protein Muscarinic Antagonists Neurotransmitter Agents Receptors, Muscarinic Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Georgiou J
Department of Physiology, Medical Research Council Group in Nerve Cells and Synapses, and Neuroscience Network, University of Toronto, Toronto, Ontario, Canada M5S 1A8.
Robitaille R
Charlton M P
References (68)
68 references, click to expand
  1. Astrocyte responses to CNS injury.
    J Neuropathol Exp Neurol. 1994 May;53(3):213-20 PMID: 8176405
  2. The relationship of glial fibrillary acidic protein to the shape, motility, and differentiation of human astrocytoma cells.
    Exp Cell Res. 1982 May;139(1):145-57 PMID: 7200901
  3. Ion channels in vertebrate glia.
    Annu Rev Neurosci. 1990;13:441-74 PMID: 2158266
  4. Induced transmitter release from Schwann cells and its suppression by actinomycin D.
    Nat New Biol. 1973 Jan 17;241(107):85-6 PMID: 4512407
  5. Purinergic receptors and their activation by endogenous purines at perisynaptic glial cells of the frog neuromuscular junction.
    J Neurosci. 1995 Nov;15(11):7121-31 PMID: 7472466
  6. Rapid and reversible astrocytic reaction to afferent activity blockade in chick cochlear nucleus.
    J Neurosci. 1992 Mar;12(3):1001-9 PMID: 1545231
  7. Three-dimensional reconstructions of astroglia and oligodendroglia cells.
    Z Zellforsch Mikrosk Anat. 1971;112(3):430-42 PMID: 5542331
  8. Calcium oscillations increase the efficiency and specificity of gene expression.
    Nature. 1998 Apr 30;392(6679):933-6 PMID: 9582075
  9. Metabolic coupling between glia and neurons.
    J Neurosci. 1996 Feb 1;16(3):877-85 PMID: 8558256
  10. Intermediate filaments: a chemically heterogeneous, developmentally regulated class of proteins.
    Annu Rev Biochem. 1982;51:219-50 PMID: 6180679
  11. The release and uptake of excitatory amino acids.
    Trends Pharmacol Sci. 1990 Nov;11(11):462-8 PMID: 1980041
  12. Endogenous peptidergic modulation of perisynaptic Schwann cells at the frog neuromuscular junction.
    J Physiol. 1998 Oct 1;512 ( Pt 1):197-209 PMID: 9729629
  13. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides.
    Differentiation. 1983;25(2):193-203 PMID: 6198232
  14. Denervation of the motor endplate results in the rapid expression by terminal Schwann cells of the growth-associated protein GAP-43.
    J Neurosci. 1992 Oct;12(10):3999-4010 PMID: 1403096
  15. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells.
    Science. 1994 Mar 25;263(5154):1768-71 PMID: 8134839
  16. Differential effect of alpha-latrotoxin on exocytosis from small synaptic vesicles and from large dense-core vesicles containing calcitonin gene-related peptide at the frog neuromuscular junction.
    Proc Natl Acad Sci U S A. 1988 Oct;85(19):7366-70 PMID: 3050995
  17. Substance P-like immunoreactivity at the frog neuromuscular junction.
    Neuroscience. 1990;37(1):271-5 PMID: 1700842
  18. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia.
    J Neurophysiol. 1966 Jul;29(4):788-806 PMID: 5966435
  19. Suppression by antisense mRNA demonstrates a requirement for the glial fibrillary acidic protein in the formation of stable astrocytic processes in response to neurons.
    J Cell Biol. 1991 Mar;112(6):1205-13 PMID: 1999469
  20. Role of glial cells in the regulation of the brain ion microenvironment.
    Prog Neurobiol. 1989;33(4):309-33 PMID: 2479051
  21. The importance of intermediate filaments in the adaptation of tissues to mechanical stress: evidence from gene knockout studies.
    Biol Cell. 1997 May;89(2):85-97 PMID: 9351189
  22. GABA-activated Cl- channels in astrocytes of hippocampal slices.
    J Neurosci. 1989 Oct;9(10):3577-83 PMID: 2477511
  23. Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction.
    Neuron. 1998 Oct;21(4):847-55 PMID: 9808470
  24. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling.
    Science. 1990 Jan 26;247(4941):470-3 PMID: 1967852
  25. Neuronal activity up-regulates astroglial gene expression.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6819-23 PMID: 1862105
  26. Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions.
    Trends Neurosci. 1996 Jul;19(7):280-5 PMID: 8799973
  27. Transmitter release increases intracellular calcium in perisynaptic Schwann cells in situ.
    Neuron. 1992 Jun;8(6):1069-77 PMID: 1351731
  28. Reduced retinal activity increases GFAP immunoreactivity in rat lateral geniculate nucleus.
    Brain Res. 1994 Nov 14;663(2):206-14 PMID: 7874503
  29. A lectin, peanut agglutinin, as a probe for the extracellular matrix in living neuromuscular junctions.
    J Neurocytol. 1987 Aug;16(4):567-76 PMID: 3500278
  30. Localization of L-type Ca2+ channels at perisynaptic glial cells of the frog neuromuscular junction.
    J Neurosci. 1996 Jan;16(1):148-58 PMID: 8613781
  31. Reactive glia as rivals in regulating neuronal survival.
    Glia. 1993 Jan;7(1):102-10 PMID: 8423057
  32. Synaptic regulation of glial protein expression in vivo.
    Neuron. 1994 Feb;12(2):443-55 PMID: 7906531
  33. Monoclonal antibodies against the native or denatured forms of muscarinic acetylcholine receptors.
    EMBO J. 1984 Jan;3(1):17-21 PMID: 6200320
  34. The physiology of neuroglial cells.
    Ergeb Physiol. 1966;57:1-90 PMID: 5330861
  35. Non-myelin-forming perisynaptic schwann cells express protein zero and myelin-associated glycoprotein.
    Glia. 1999 Aug;27(2):101-9 PMID: 10417810
  36. Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration.
    J Physiol. 1960 Jan;150:145-68 PMID: 13800902
  37. Intrinsic neuronal determinants locally regulate extrasynaptic and synaptic growth at the adult neuromuscular junction.
    J Cell Biol. 1997 Feb 10;136(3):679-92 PMID: 9024697
  38. Dynamic roles at the neuromuscular junction. Schwann cells.
    Curr Biol. 1996 Sep 1;6(9):1054-6 PMID: 8805358
  39. Do astrocytes process neural information?
    Prog Brain Res. 1992;94:119-36 PMID: 1337609
  40. Muscarinic receptor subtypes.
    Annu Rev Pharmacol Toxicol. 1990;30:633-73 PMID: 2188581
  41. Ca2+-sensitive adenylyl cyclases, key integrators of cellular signalling.
    Life Sci. 1998;62(17-18):1647-52 PMID: 9585151
  42. Monoclonal antibodies to purified muscarinic receptor display agonist-like activity.
    Proc Natl Acad Sci U S A. 1984 Jul;81(14):4331-4 PMID: 6087318
  43. Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells.
    Neuron. 1995 Jan;14(1):133-41 PMID: 7826631
  44. Synthesis and release of neuroactive substances by glial cells.
    Glia. 1992;5(2):81-94 PMID: 1349588
  45. New views on synapse-glia interactions.
    Curr Opin Neurobiol. 1996 Oct;6(5):615-21 PMID: 8937825
  46. Functional interactions between neurons and astrocytes I. Turnover and metabolism of putative amino acid transmitters.
    Prog Neurobiol. 1979;13(3):277-323 PMID: 42117
  47. Signalling via ATP in the nervous system.
    Trends Neurosci. 1994 Oct;17(10):420-6 PMID: 7530880
  48. An acidic protein isolated from fibrous astrocytes.
    Brain Res. 1971 May 7;28(2):351-4 PMID: 5113526
  49. Non-selectivity of the monoclonal antibody M35 for subtypes of muscarinic acetylcholine receptors.
    Brain Res Bull. 1997;44(1):25-31 PMID: 9288828
  50. The molecular basis of muscarinic receptor diversity.
    Trends Neurosci. 1989 Apr;12(4):148-51 PMID: 2470172
  51. A monolayer preparation of innervated skeletal muscle fibres of the m. cutaneus pectoris of the frog.
    Pflugers Arch. 1974 Apr 22;348(3):257-62 PMID: 4545882
  52. ATP-evoked increases in intracellular calcium in neurons and glia from the dorsal spinal cord.
    J Neurosci. 1994 Mar;14(3 Pt 2):1563-75 PMID: 8126555
  53. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain.
    Trends Neurosci. 1990 May;13(5):179-84 PMID: 1693236
  54. Plasticity of astrocytes.
    Glia. 1994 Jun;11(2):147-55 PMID: 7927644
  55. Cell accumulation in the junctional region of denervated muscle.
    J Cell Biol. 1987 Jan;104(1):109-20 PMID: 3491825
  56. Glutamate-mediated astrocyte-neuron signalling.
    Nature. 1994 Jun 30;369(6483):744-7 PMID: 7911978
  57. Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate.
    J Neurocytol. 1992 Jan;21(1):50-66 PMID: 1346630
  58. Fibroblasts that proliferate near denervated synaptic sites in skeletal muscle synthesize the adhesive molecules tenascin(J1), N-CAM, fibronectin, and a heparan sulfate proteoglycan.
    J Cell Biol. 1989 May;108(5):1873-90 PMID: 2469680
  59. Neuronal activity triggers calcium waves in hippocampal astrocyte networks.
    Neuron. 1992 Mar;8(3):429-40 PMID: 1347996
  60. Control of the phosphorylation of the astrocyte marker glial fibrillary acidic protein (GFAP) in the immature rat hippocampus by glutamate and calcium ions: possible key factor in astrocytic plasticity.
    Braz J Med Biol Res. 1997 Mar;30(3):325-38 PMID: 9246230
  61. Role of glial filaments in cells and tumors of glial origin: a review.
    J Neurosurg. 1997 Sep;87(3):420-30 PMID: 9285609
  62. Muscarinic Ca2+ responses resistant to muscarinic antagonists at perisynaptic Schwann cells of the frog neuromuscular junction.
    J Physiol. 1997 Oct 15;504 ( Pt 2):337-47 PMID: 9365908
  63. Integration site-dependent expression of a transgene reveals specialized features of cells associated with neuromuscular junctions.
    J Cell Biol. 1991 Jun;113(6):1385-97 PMID: 1904446
  64. Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons.
    J Neurosci. 1998 Sep 1;18(17):6822-9 PMID: 9712653
  65. Glial calcium.
    Glia. 1993 Oct;9(2):83-104 PMID: 8244537
  66. Voltage-dependent ion channels in glial cells.
    Glia. 1994 Jun;11(2):156-72 PMID: 7523291
  67. New roles for glia.
    J Neurosci. 1991 Dec;11(12):3685-94 PMID: 1720814
  68. Spatial regulation of neuronal gene expression in response to nerve growth factor.
    Dev Biol. 1997 Apr 1;184(1):1-9 PMID: 9142978
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
1999-05-15
Pages
3836-46
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782737
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2