Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-24T12:12:03.116Z Has data issue: false hasContentIssue false
  • English
  • Français

Integration of NG2-glia (synantocytes) into the neuroglial network

Published online by Cambridge University Press:  29 September 2009

Rebekah Wigley  and
Arthur M. Butt
Rebekah Wigley
Affiliation:
Institute for Biomedical and Biomolecular Sciences, School of Pharmacy and Biomedical Sciences, University of Portsmouth, UK
Arthur M. Butt*
Affiliation:
Institute for Biomedical and Biomolecular Sciences, School of Pharmacy and Biomedical Sciences, University of Portsmouth, UK
*
Correspondence should be addressed to: Arthur M. Butt, Institute for Biomedical and Biomolecular Sciences, School of Pharmacy and Biomedical Sciences, University of Portsmouth, UK email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

NG2-glia are a distinct class of CNS glial cells that are generally classed as oligodendrocyte progenitor cells. However, in the adult CNS a large fraction of NG2 cells does not appear to divide or generate oligodendrocytes. The functions of these adult NG2-glia, which we have termed synantocytes, are unknown. NG2-glia (synantocytes) form interactive domains with astrocytes and neurons. Within their domains, NG2-glia and astrocytes contact the same neurons, form multiple heterologous contacts with each other, and contact pericytes which regulate cerebral blood flow. NG2-glia receive presynaptic input from neurons and respond to neurotransmitters released at synapses. In addition, NG2-glia are intimately associated with astroglia and respond to astroglial signals, a hitherto neglected aspect of NG2-glial cell physiology. The non-overlapping domain organisation of astrocytes is believed to be important in isolating and integrating activity at the synapses and blood vessels within their domains. The domains of NG2-glia overlap with astrocytes, suggesting they could play a role in integrating non-overlapping astrocyte domains.

Keywords

NG2astrocytesynantocyteneuronsynapsepericytecerebral blood vessel
Type
Research Article
Information
Neuron Glia Biology , Volume 5 , Special Issue 1-2: NG2-Glia, Part I: NG2 Cells as Components of Neural Circuits , May 2009 , pp. 21 - 28
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aguirre, A.A., Chittajallu, R., Belachew, S. and Gallo, V. (2004) NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. Journal of Cell Biology 165, 575–589.CrossRefGoogle ScholarPubMed
Araque, A., Parpura, V., Sanzgiri, R.P. and Haydon, P.G. (1999) Tripartite synapses: glia, the unacknowledged partner. Trends in Neuroscience 22, 208–215.CrossRefGoogle ScholarPubMed
Bakiri, Y., Attwell, D. and Káradóttir, R. (2009) Electrical signalling properties of oligodendrocyte precursor cells. Neuron Glia Biology, 10.1017/S1740925X09990202.CrossRefGoogle ScholarPubMed
Belachew, S., Chittajallu, R., Aguirre, A.A., Yuan, X., Kirby, M., Anderson, S. et al. (2003) Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. Journal of Cell Biology 161, 169–186.CrossRefGoogle ScholarPubMed
Bergles, D.E., Roberts, J.D., Somogyi, P. and Jahr, C.E. (2000) Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405, 187–191.CrossRefGoogle ScholarPubMed
Bushong, E.A., Martone, M.E., Jones, Y.Z. and Ellisman, M.H. (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. Journal of Neuroscience 22, 183–192.CrossRefGoogle ScholarPubMed
Butt, A.M., Duncan, A., Hornby, M.F., Kirvell, S.L., Hunter, A., Levine, J.M. et al. (1999) Cells expressing the NG2 antigen contact nodes of Ranvier in adult CNS white matter. Glia 26, 84–91.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Butt, A.M., Hamilton, N., Hubbard, P., Pugh, M. and Ibrahim, M. (2005) Synantocytes: the fifth element. Journal of Anatomy 207, 695–706.CrossRefGoogle ScholarPubMed
Butt, A.M., Kiff, J., Hubbard, P. and Berry, M. (2002) Synantocytes: new functions for novel NG2 expressing glia. Journal of Neurocytology 31, 551–565.CrossRefGoogle ScholarPubMed
Dayer, A.G., Cleaver, K.M., Abouantoun, T. and Cameron, H.A. (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. Journal of Cell Biology 168, 415–427.CrossRefGoogle ScholarPubMed
Dore-Duffy, P., Katychev, A., Wang, X. and Van Buren, E. (2006) CNS microvascular pericytes exhibit multipotential stem cell activity. Journal of Cerebral Blood Flow and Metabolism 26, 613–624.CrossRefGoogle ScholarPubMed
Ge, W.P., Yang, X.J., Zhang, Z., Wang, H.K., Shen, W., Deng, Q.D. et al. (2006) Long-term potentiation of neuron-glia synapses mediated by Ca2+-permeable AMPA receptors. Science 312, 1533–1537.CrossRefGoogle ScholarPubMed
Ge, W.P., Zhou, W., Luo, Q., Jan, L.Y. and Jan, Y.N. (2009) Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proceedings of the National Academy of Sciences of the U.S.A. 106, 328–333.CrossRefGoogle ScholarPubMed
Gerhardt, H. and Betsholtz, C. (2003) Endothelial-pericyte interactions in angiogenesis. Cell Tissue Research 314, 15–23.CrossRefGoogle ScholarPubMed
Grass, D., Pawlowski, P.G., Hirrlinger, J., Papadopoulos, N., Richter, D.W., Kirchhoff, F. et al. (2004) Diversity of functional astroglial properties in the respiratory network. Journal of Neuroscience 24, 1358–1365.CrossRefGoogle ScholarPubMed
Grosche, J., Kettenmann, H. and Reichenbach, A. (2002) Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. Journal of Neuroscience Research 68, 138–149.CrossRefGoogle ScholarPubMed
Grosche, J., Matyash, V., Moller, T., Verkhratsky, A., Reichenbach, A. and Kettenmann, H. (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nature Neuroscience 2, 139–143.CrossRefGoogle ScholarPubMed
Halassa, M.M., Fellin, T. and Haydon, P.G. (2007a) The tripartite synapse: roles for gliotransmission in health and disease. Trends in Molecular Medicine 13, 54–63.CrossRefGoogle ScholarPubMed
Halassa, M.M., Fellin, T., Takano, H., Dong, J.H. and Haydon, P.G. (2007b) Synaptic islands defined by the territory of a single astrocyte. Journal of Neuroscience 27, 6473–6477.CrossRefGoogle ScholarPubMed
Hamilton, N., Vayro, S., Kirchhoff, F., Verkhratsky, A., Robbins, J., Gorecki, D. et al. (2008) Mechanisms of ATP- and glutamate-mediated calcium signaling in white matter astrocytes. Glia 56, 734–749.CrossRefGoogle ScholarPubMed
Hamilton, N., Vayro, S., Wigley, R., Robbins, J. and Butt, A.M. (2009) Axons and astrocytes release glutamate and ATP to evoke calcium signals in NG2-glia. Glia in press.Google Scholar
Houades, V., Koulakoff, A., Ezan, P., Seif, I. and Giaume, C. (2008) Gap junction-mediated astrocytic networks in the mouse barrel cortex. Journal of Neuroscience 28, 5207–5217.CrossRefGoogle ScholarPubMed
Káradóttir, R., Cavelier, P., Bergersen, L.H. and Attwell, D. (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438, 1162–1166.CrossRefGoogle ScholarPubMed
Káradóttir, R., Hamilton, N.B., Bakiri, Y. and Attwell, D. (2008) Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nature Neuroscience 11, 450–456.CrossRefGoogle ScholarPubMed
Leoni, G., Rattray, M. and Butt, A.M. (2009) NG2 cells differentiate into astrocytes in cerebellar slices. Molecular and Cellular Neurosciences 42, 208–218.CrossRefGoogle ScholarPubMed
Lin, S.C. and Bergles, D.E. (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nature Neuroscience 7, 24–32.CrossRefGoogle ScholarPubMed
Lin, S.C., Huck, J.H., Roberts, J.D., Macklin, W.B., Somogyi, P. and Bergles, D.E. (2005) Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46, 773–785.CrossRefGoogle ScholarPubMed
Nedergaard, M., Ransom, B. and Goldman, S.A. (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends in Neuroscience 26, 523–530.CrossRefGoogle ScholarPubMed
Nishiyama, A., Lin, X., Giese, N., Heldin, C. and Stallcup, W. (1996) Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. Journal of Neuroscience Research 43, 299–314.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Nolte, C., Matyash, M., Pivneva, T., Schipke, C.G., Ohlemeyer, C., Hanisch, U.K. et al. (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33, 72–86.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Oberheim, N.A., Wang, X., Goldman, S. and Nedergaard, M. (2006) Astrocytic complexity distinguishes the human brain. Trends in Neuroscience 29, 547–553.CrossRefGoogle ScholarPubMed
Ozerdem, U., Monosov, E. and Stallcup, W.B. (2002) NG2 proteoglycan expression by pericytes in pathological microvasculature. Microvascular Research 63, 129–134.CrossRefGoogle ScholarPubMed
Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S. and Haydon, P.G. (1994) Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747.CrossRefGoogle ScholarPubMed
Peppiatt, C.M., Howarth, C., Mobbs, P. and Attwell, D. (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443, 700–704.CrossRefGoogle ScholarPubMed
Psachoulia, K., Young, K.M. and Richardson, W.D. (2009) Separate populations of dividing and non-dividing NG2 cells in the postnatal mouse brain. Neuron Glia Biology, in press.Google Scholar
Rivers, L.E., Young, K.M., Rizzi, M., Jamen, F., Psachoulia, K., Wade, A. et al. (2008) PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nature Neuroscience 11, 1392–1401.CrossRefGoogle ScholarPubMed
Rouach, N., Koulakoff, A., Abudara, V., Willecke, K. and Giaume, C. (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322, 1551–1555.CrossRefGoogle ScholarPubMed
Wang, L.Y., Cai, W.Q., Chen, P.H., Deng, Q.Y. and Zhao, C.M. (2009) Downregulation of P2X7 receptor expression in rat oligodendrocyte precursor cells after hypoxia ischemia. Glia 57, 307–319.CrossRefGoogle ScholarPubMed
Wigley, R., Hamilton, N., Nishiyama, A., Kirchhoff, F. and Butt, A.M. (2007) Morphological and physiological interactions of NG2-glia with astrocytes and neurons. Journal of Anatomy 210, 661–670.CrossRefGoogle ScholarPubMed
Zhu, X., Bergles, D.E. and Nishiyama, A. (2008) NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145–157.CrossRefGoogle ScholarPubMed
Ziskin, J.L., Nishiyama, A., Rubio, M., Fukaya, M. and Bergles, D.E. (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nature Neuroscience 10, 321–330.CrossRefGoogle ScholarPubMed