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Glial imaging during synapse remodeling at the neuromuscular junction

Published online by Cambridge University Press:  25 November 2009

Yi Zuo  and
Derron Bishop
Yi Zuo*
Affiliation:
Department of Molecular, Cell and Developmental Biology, University of California Santa Cruz, Santa Cruz, CA, USA
Derron Bishop*
Affiliation:
Department of Medical Education, Indiana University School of Medicine – Muncie, Muncie, IN, USA
*
Correspondence should be addressed to: Yi Zuo, Department of Molecular, Cell and Developmental Biology, University of California Santa Cruz, Santa Cruz, CA 95064, USA phone: (831) 459-3812 email: [email protected] Derron Bishop, Department of Medical Education, Indiana University School of Medicine – Muncie, Muncie, IN 47306, USA phone: (765) 751-5233 email: [email protected]
Correspondence should be addressed to: Yi Zuo, Department of Molecular, Cell and Developmental Biology, University of California Santa Cruz, Santa Cruz, CA 95064, USA phone: (831) 459-3812 email: [email protected] Derron Bishop, Department of Medical Education, Indiana University School of Medicine – Muncie, Muncie, IN 47306, USA phone: (765) 751-5233 email: [email protected]
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Abstract

Glia are an indispensable structural and functional component of the synapse. They modulate synaptic transmission and also play important roles in synapse formation and maintenance. The vertebrate neuromuscular junction (NMJ) is a classic model synapse. Due to its large size, simplicity and accessibility, the NMJ has contributed greatly to our understanding of synapse development and organization. In the past decade, the NMJ has also emerged as an effective model for studying glia–synapse interactions, in part due to the development of various labeling techniques that permit NMJs and associated Schwann cells (the glia at NMJs) to be visualized in vitro and in vivo. These approaches have demonstrated that Schwann cells are actively involved in synapse remodeling both during early development and in post-injury reinnervation. In vivo imaging has also recently been combined with serial section transmission electron microscopic (ssTEM) reconstruction to directly examine the ultrastructural organization of remodeling NMJs. In this review, we focus on the anatomical studies of Schwann cell dynamics and their roles in formation, maturation and remodeling of vertebrate NMJs using the highest temporal and spatial resolution methods currently available.

Keywords

Schwann cellsynapse eliminationreinnervationin vivo imagingssTEM reconstruction
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 4 , November 2008 , pp. 319 - 326
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Allen, N.J. and Barres, B.A. (2005) Signaling between glia and neurons: focus on synaptic plasticity. Current Opinion in Neurobiology 15, 542–548.CrossRefGoogle ScholarPubMed
Allore, R.J., Friend, W.C., O'Hanlon, D., Neilson, K.M., Baumal, R., Dunn, R.J. et al. (1990) Cloning and expression of the human S100 beta gene. Journal of Biological Chemistry 265, 15537–15543.CrossRefGoogle ScholarPubMed
Astrow, S.H., Qiang, H. and Ko, C.P. (1998) Perisynaptic Schwann cells at neuromuscular junctions revealed by a novel monoclonal antibody. Journal of Neurocytology 27, 667–681.CrossRefGoogle ScholarPubMed
Balice-Gordon, R.J. and Lichtman, J.W. (1990) In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse. Journal of Neuroscience 10, 894–908.CrossRefGoogle ScholarPubMed
Barres, B.A. and Barde, Y. (2000) Neuronal and glial cell biology. Current Opinion in Neurobiology 10, 642–648.CrossRefGoogle ScholarPubMed
Bevan, S., Miledi, R. and Grampp, W. (1973) Induced transmitter release from Schwann cells and its suppression by actinomycin D. Nature New Biology 241, 85–86.CrossRefGoogle ScholarPubMed
Birks, R., Huxley, H.E. and Katz, B. (1960a) The fine structure of the neuromuscular junction of the frog. Journal of Physiology 150, 134–144.CrossRefGoogle ScholarPubMed
Birks, R., Katz, B. and Miledi, R. (1960b) Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration. Journal of Physiology 150, 145–168.CrossRefGoogle ScholarPubMed
Bishop, D.L., Misgeld, T., Walsh, M.K., Gan, W.B. and Lichtman, J.W. (2004) Axon branch removal at developing synapses by axosome shedding. Neuron 44, 651–661.CrossRefGoogle ScholarPubMed
Bixby, J.L., Lilien, J. and Reichardt, L.F. (1988) Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. Journal of Cell Biology 107, 353–361.CrossRefGoogle ScholarPubMed
Calabrese, R.L. and Maranto, A.R. (1986) Cholinergic action on the heart of the leech, Hirudo medicinalis. Journal of Experimental Biology 125, 205–224.CrossRefGoogle ScholarPubMed
Castets, F., Griffin, W.S., Marks, A. and Van Eldik, L.J. (1997) Transcriptional regulation of the human S100 beta gene. Brain Research. Molecular Brain Research 46, 208–216.CrossRefGoogle ScholarPubMed
Castonguay, A. and Robitaille, R. (2001) Differential regulation of transmitter release by presynaptic and glial Ca2+ internal stores at the neuromuscular synapse. Journal of Neuroscience 21, 1911–1922.CrossRefGoogle ScholarPubMed
Chen, L. and Ko, C.P. (1994) Extension of synaptic extracellular matrix during nerve terminal sprouting in living frog neuromuscular junctions. Journal of Neuroscience 14, 796–808.CrossRefGoogle ScholarPubMed
Chen, L.L., Folsom, D.B. and Ko, C.P. (1991) The remodeling of synaptic extracellular matrix and its dynamic relationship with nerve terminals at living frog neuromuscular junctions. Journal of Neuroscience 11, 2920–2930.CrossRefGoogle ScholarPubMed
Davalos, D., Grutzendler, J., Yang, G., Kim, J.V., Zuo, Y., Jung, S. et al. (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nature Neuroscience 8, 752–758.CrossRefGoogle ScholarPubMed
Desaki, J. and Uehara, Y. (1981) The overall morphology of neuromuscular junctions as revealed by scanning electron microscopy. Journal of Neurocytology 10, 101–110.CrossRefGoogle ScholarPubMed
Dunaevsky, A., Blazeski, R., Yuste, R. and Mason, C. (2001) Spine motility with synaptic contact. Nature Neuroscience 4, 685–686.CrossRefGoogle ScholarPubMed
Fallon, J.R. (1985) Neurite guidance by non-neuronal cells in culture: preferential outgrowth of peripheral neurites on glial as compared to nonglial cell surfaces. Journal of Neuroscience 5, 3169–3177.CrossRefGoogle ScholarPubMed
Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M. et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41–51.CrossRefGoogle ScholarPubMed
Feng, Z., Koirala, S. and Ko, C.P. (2005) Synapse-glia interactions at the vertebrate neuromuscular junction. Neuroscientist 11, 503–513.CrossRefGoogle ScholarPubMed
Gan, W.B., Bishop, D.L., Turney, S.G. and Lichtman, J.W. (1999) Vital imaging and ultrastructural analysis of individual axon terminals labeled by iontophoretic application of lipophilic dye. Journal of Neuroscience Methods 93, 13–20.CrossRefGoogle ScholarPubMed
Grutzendler, J., Kasthuri, N. and Gan, W.B. (2002) Long-term dendritic spine stability in the adult cortex. Nature 420, 812–816.CrossRefGoogle ScholarPubMed
Halassa, M.M., Fellin, T. and Haydon, P.G. (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends in Molecular Medicine 13, 54–63.CrossRefGoogle ScholarPubMed
Halstead, S.K., Morrison, I., O'Hanlon, G.M., Humphreys, P.D., Goodfellow, J.A., Plomp, J.J. et al. (2005) Anti-disialosyl antibodies mediate selective neuronal or Schwann cell injury at mouse neuromuscular junctions. Glia 52, 177–189.CrossRefGoogle ScholarPubMed
Haydon, P.G. (2001) GLIA: listening and talking to the synapse. Nature Reviews. Neuroscience 2, 185–193.CrossRefGoogle Scholar
Hayworth, C.R., Moody, S.E., Chodosh, L.A., Krieg, P., Rimer, M. and Thompson, W.J. (2006) Induction of neuregulin signaling in mouse Schwann cells in vivo mimics responses to denervation. Journal of Neuroscience 26, 6873–6884.CrossRefGoogle ScholarPubMed
Herrmann, K., Antonini, A. and Shatz, C.J. (1994) Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons. European of Journal of Neuroscience 6, 1729–1742.CrossRefGoogle ScholarPubMed
Heuser, J.E. and Reese, T.S. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. Journal of Cell Biology 57, 315–344.CrossRefGoogle ScholarPubMed
Heuser, J.E., Reese, T.S. and Landis, D.M. (1976) Preservation of synaptic structure by rapid freezing. Cold Spring Harbor Symposia on Quantitative Biology 40, 17–24.CrossRefGoogle ScholarPubMed
Holtmaat, A.J., Trachtenberg, J.T., Wilbrecht, L., Shepherd, G.M., Zhang, X., Knott, G.W. et al. (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45, 279–291.CrossRefGoogle ScholarPubMed
Jahromi, B.S., Robitaille, R. and Charlton, M.P. (1992) Transmitter release increases intracellular calcium in perisynaptic Schwann cells in situ. Neuron 8, 1069–1077.CrossRefGoogle ScholarPubMed
Jessen, K.R. and Mirsky, R. (2005) The origin and development of glial cells in peripheral nerves. Nature Reviews. Neuroscience 6, 671–682.CrossRefGoogle ScholarPubMed
Jiang, H., Shah, S. and Hilt, D.C. (1993) Organization, sequence, and expression of the murine S100 beta gene. Transcriptional regulation by cell type-specific cis-acting regulatory elements. Journal of Biological Chemistry 268, 20502–20511.CrossRefGoogle ScholarPubMed
Jirmanová, I. (1975) Ultrastructure of motor end-plates during pharmacologically-induced degeneration and subsequent regeneration of skeletal muscle. Journal of Neurocytology 4, 141–155.CrossRefGoogle ScholarPubMed
Kang, H., Tian, L. and Thompson, W. (2003) Terminal Schwann cells guide the reinnervation of muscle after nerve injury. Journal of Neurocytology 32, 975–985.CrossRefGoogle ScholarPubMed
Keller-Peck, C.R., Walsh, M.K., Gan, W.B., Feng, G., Sanes, J.R. and Lichtman, J.W. (2001) Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31, 381–394.CrossRefGoogle ScholarPubMed
Kerschensteiner, M., Reuter, M.S., Lichtman, J.W. and Misgeld, T. (2008) Ex vivo imaging of motor axon dynamics in murine triangularis sterni explants. Nature Protocols 3, 1645–1653.CrossRefGoogle ScholarPubMed
Ko, C.P. (1987) A lectin, peanut agglutinin, as a probe for the extracellular matrix in living neuromuscular junctions. Journal of Neurocytology 16, 567–576.CrossRefGoogle ScholarPubMed
Ko, C.P. and Chen, L. (1996) Synaptic remodeling revealed by repeated in vivo observations and electron microscopy of identified frog neuromuscular junctions. Journal of Neuroscience 16, 1780–1790.CrossRefGoogle ScholarPubMed
Lin, W., Sanchez, H.B., Deerinck, T., Morris, J.K., Ellisman, M. and Lee, K.F. (2000) Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proceedings of the National Academy of Sciences of the U.S.A. 97, 1299–1304.CrossRefGoogle ScholarPubMed
Livet, J., Weissman, T.A., Kang, H., Draft, R.W., Lu, J., Bennis, R.A. et al. (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature 450, 56–62.CrossRefGoogle ScholarPubMed
Love, F.M., Son, Y.J. and Thompson, W.J. (2003) Activity alters muscle reinnervation and terminal sprouting by reducing the number of Schwann cell pathways that grow to link synaptic sites. Journal of Neurobiology 54, 566–576.CrossRefGoogle ScholarPubMed
Lubischer, J.L. and Bebinger, D.M. (1999) Regulation of terminal Schwann cell number at the adult neuromuscular junction. The Journal of Neuroscience 19, RC46.CrossRefGoogle ScholarPubMed
Lubke, J. (1993) Photoconversion of diaminobenzidine with different fluorescent neuronal markers into a light and electron microscopic dense reaction product. Microscopy Research and Technique 24, 2–14.CrossRefGoogle ScholarPubMed
Ludwin, S.K., Kosek, J.C. and Eng, L.F. (1976) The topographical distribution of S-100 and GFA proteins in the adult rat brain: an immunohistochemical study using horseradish peroxidase-labelled antibodies. Journal of Comparative Neurology 165, 197–207.CrossRefGoogle Scholar
Macleod, G.T., Dickens, P.A. and Bennett, M.R. (2001) Formation and function of synapses with respect to Schwann cells at the end of motor nerve terminal branches on mature amphibian (Bufo marinus) muscle. Journal of Neuroscience 21, 2380–2392.CrossRefGoogle ScholarPubMed
Maranto, A.R. (1982) Neuronal mapping: a photooxidation reaction makes Lucifer yellow useful for electron microscopy. Science 217, 953–955.CrossRefGoogle ScholarPubMed
Martini, R. (2001) The effect of myelinating Schwann cells on axons. Muscle Nerve 24, 456–466.CrossRefGoogle ScholarPubMed
Miledi, R. and Slater, C.R. (1968) Electrophysiology and electron-microscopy of rat neuromuscular junctions after nerve degeneration. Proceedings of the Royal Society of London – Series B: Biological Sciences 169, 289–306.Google ScholarPubMed
Miledi, R. and Slater, C.R. (1970) On the degeneration of rat neuromuscular junctions after nerve section. Journal of Physiology 207, 507–528.CrossRefGoogle ScholarPubMed
Morris, J.K., Lin, W., Hauser, C., Marchuk, Y., Getman, D. and Lee, K.F. (1999) Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 23, 273–283.CrossRefGoogle ScholarPubMed
Nguyen, Q.T., Sanes, J.R. and Lichtman, J.W. (2002) Pre-existing pathways promote precise projection patterns. Nature Neuroscience 5, 861–867.CrossRefGoogle ScholarPubMed
Nimmerjahn, A., Kirchhoff, F. and Helmchen, F. (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308, 1314–1318.CrossRefGoogle ScholarPubMed
Noakes, P.G., Gautam, M., Mudd, J., Sanes, J.R. and Merlie, J.P. (1995) Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374, 258–262.CrossRefGoogle ScholarPubMed
O'Brien, R.A., Ostberg, A.J. and Vrbova, G. (1978) Observations on the elimination of polyneuronal innervation in developing mammalian skeletal muscle. Journal of Physiology 282, 571–582.CrossRefGoogle ScholarPubMed
O'Malley, J.P., Waran, M.T. and Balice-Gordon, R.J. (1999) In vivo observations of terminal Schwann cells at normal, denervated, and reinnervated mouse neuromuscular junctions. Journal of Neurobiology 38, 270–286.3.0.CO;2-F>CrossRefGoogle ScholarPubMed
Pakkenberg, B., Pelvig, D., Marner, L., Bundgaard, M.J., Gundersen, H.J., Nyengaard, J.R. et al. (2003) Aging and the human neocortex. Experimental Gerontology 38, 95–99.CrossRefGoogle ScholarPubMed
Pan, F. and Gan, W.B. (2008) Two-photon imaging of dendritic spine development in the mouse cortex. Developmental Neurobiology 68, 771–778.CrossRefGoogle ScholarPubMed
Patton, B.L., Chiu, A.Y. and Sanes, J.R. (1998) Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393, 698–701.CrossRefGoogle ScholarPubMed
Portera-Cailliau, C., Weimer, R.M., De Paola, V., Caroni, P. and Svoboda, K. (2005) Diverse modes of axon elaboration in the developing neocortex. PLoS Biology 3, e272.CrossRefGoogle ScholarPubMed
Ransom, B., Behar, T. and Nedergaard, M. (2003) New roles for astrocytes (stars at last). Trends in Neuroscience 26, 520–522.CrossRefGoogle ScholarPubMed
Reddy, L.V., Koirala, S., Sugiura, Y., Herrera, A.A. and Ko, C.P. (2003) Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40, 563–580.CrossRefGoogle ScholarPubMed
Reist, N.E. and Smith, S.J. (1992) Neurally evoked calcium transients in terminal Schwann cells at the neuromuscular junction. Proceedings of the National Academy of Sciences of the U.S.A. 89, 7625–7629.CrossRefGoogle ScholarPubMed
Riley, D.A. (1981) Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat soleus muscle. Journal of Neurocytology 10, 425–440.CrossRefGoogle ScholarPubMed
Robitaille, R. (1998) Modulation of synaptic efficacy and synaptic depression by glial cells at the frog neuromuscular junction. Neuron 21, 847–855.CrossRefGoogle ScholarPubMed
Robitaille, R., Jahromi, B.S. and Charlton, M.P. (1997) Muscarinic Ca2+ responses resistant to muscarinic antagonists at perisynaptic Schwann cells of the frog neuromuscular junction. Journal of Physiology 504, 337–347.CrossRefGoogle ScholarPubMed
Rousse, I. and Robitaille, R. (2006) Calcium signaling in Schwann cells at synaptic and extra-synaptic sites: active glial modulation of neuronal activity. Glia 54, 691–699.CrossRefGoogle ScholarPubMed
Scherer, S. (1999) Axonal pathology in demyelinating diseases. Annals of Neurology 45, 6–7.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Scherer, S.S. (1997) The biology and pathobiology of Schwann cells. Current Opinion in Neurology 10, 386–397.CrossRefGoogle ScholarPubMed
Son, Y.J. and Thompson, W.J. (1995) Schwann cell processes guide regeneration of peripheral axons. Neuron 14, 125–132.CrossRefGoogle ScholarPubMed
Song, J.W., Misgeld, T., Kang, H., Knecht, S., Lu, J., Cao, Y. et al. (2008) Lysosomal activity associated with developmental axon pruning. Journal of Neuroscience 28, 8993–9001.CrossRefGoogle ScholarPubMed
Stefansson, K., Wollmann, R.L. and Moore, B.W. (1982) Distribution of S-100 protein outside the central nervous system. Brain Research 234, 309–317.CrossRefGoogle ScholarPubMed
Trachtenberg, J.T., Chen, B.E., Knott, G.W., Feng, G., Sanes, J.R., Welker, E. et al. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788–794.CrossRefGoogle ScholarPubMed
Trachtenberg, J.T. and Thompson, W.J. (1996) Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379, 174–177.CrossRefGoogle ScholarPubMed
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews. Neuroscience 6, 626–640.CrossRefGoogle ScholarPubMed
Woldeyesus, M.T., Britsch, S., Riethmacher, D., Xu, L., Sonnenberg-Riethmacher, E., Abou-Rebyeh, F. et al. (1999) Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes & Development 13, 2538–2548.CrossRefGoogle ScholarPubMed
Wolpowitz, D., Mason, T.B., Dietrich, P., Mendelsohn, M., Talmage, D.A. and Role, L.W. (2000) Cysteine-rich domain isoforms of the neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron 25, 79–91.CrossRefGoogle ScholarPubMed
Yin, X., Kidd, G.J., Pioro, E.P., McDonough, J., Dutta, R., Feltri, M.L. et al. (2004) Dysmyelinated lower motor neurons retract and regenerate dysfunctional synaptic terminals. Journal of Neuroscience 24, 3890–3898.CrossRefGoogle ScholarPubMed
Zuo, Y., Lin, A., Chang, P. and Gan, W.B. (2005) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46, 181–189.CrossRefGoogle ScholarPubMed
Zuo, Y., Lubischer, J.L., Kang, H., Tian, L., Mikesh, M., Marks, A. et al. (2004) Fluorescent proteins expressed in mouse transgenic lines mark subsets of glia, neurons, macrophages, and dendritic cells for vital examination. Journal of Neuroscience 24, 10999–11009.CrossRefGoogle ScholarPubMed