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Bergmann glial ensheathment of dendritic spines regulates synapse number without affecting spine motility

Published online by Cambridge University Press:  02 November 2010

Jocelyn J. Lippman Bell ,
Tamar Lordkipanidze ,
Natalie Cobb  and
Anna Dunaevsky
Jocelyn J. Lippman Bell
Affiliation:
Department of Neuroscience, Brown University, Providence, RI, USA
Tamar Lordkipanidze
Affiliation:
Department of Neuroscience, Brown University, Providence, RI, USA
Natalie Cobb
Affiliation:
Department of Neuroscience, Brown University, Providence, RI, USA
Anna Dunaevsky*
Affiliation:
Department of Neuroscience, Brown University, Providence, RI, USA
*
Correspondence should be addressed to: Anna Dunaevsky, Developmental Neuroscience Department, Munroe-Meyer Institute, University of Nebraska Medical Center, 985960 Nebraska Medical Center, Omaha, NE 68198-5960USA email: [email protected]
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Abstract

In the cerebellum, lamellar Bergmann glial (BG) appendages wrap tightly around almost every Purkinje cell dendritic spine. The function of this glial ensheathment of spines is not entirely understood. The development of ensheathment begins near the onset of synaptogenesis, when motility of both BG processes and dendritic spines are high. By the end of the synaptogenic period, ensheathment is complete and motility of the BG processes decreases, correlating with the decreased motility of dendritic spines. We therefore have hypothesized that ensheathment is intimately involved in capping synaptogenesis, possibly by stabilizing synapses. To test this hypothesis, we misexpressed GluR2 in an adenoviral vector in BG towards the end of the synaptogenic period, rendering the BG α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPARs) Ca2+-impermeable and causing glial sheath retraction. We then measured the resulting spine motility, spine density and synapse number. Although we found that decreasing ensheathment at this time does not alter spine motility, we did find a significant increase in both synaptic pucta and dendritic spine density. These results indicate that consistent spine coverage by BG in the cerebellum is not necessary for stabilization of spine dynamics, but is very important in the regulation of synapse number.

Keywords

SynaptogenesisPurkinje cellcerebellumGluR2
Type
Research Article
Information
Neuron Glia Biology , Volume 6 , Issue 3 , August 2010 , pp. 193 - 200
Copyright
Copyright © Cambridge University Press 2010

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Footnotes

*

Current address: Department of Neurology, Children's Hospital Boston and Harvard Medical School, Boston, Massachusetts 02115, USA.

†

Current address: Developmental Neuroscience Department, Munroe-Meyer Institute, University of Nebraska Medical Center, Omaha, NE 68198, USA.

References

REFERENCES

Bourgeron, T. (2009) A synaptic trek to autism. Current Opinion in Neurobiology 19, 231–234.Google Scholar
Deng, J. and Dunaevsky, A. (2005) Dynamics of dendritic spines and their afferent terminals: spines are more motile than presynaptic boutons. Developmental Biology 277, 366–377.Google Scholar
Dunaevsky, A., Tashiro, A., Majewska, A., Mason, C. and Yuste, R. (1999) Developmental regulation of spine motility in the mammalian central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 96, 13438–13443.Google Scholar
Dunaevsky, A., Blazeski, R., Yuste, R. and Mason, C. (2001) Spine motility with synaptic contact. Nature Neuroscience 4, 685–686.Google Scholar
Fiala, J.C. and Harris, K.M. (2001) Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. Journal of American Medical Information Association 8, 1–16.Google Scholar
Fiala, J.C., Kirov, S.A., Feinberg, M.D., Petrak, L.J., George, P., Goddard, C.A. et al. (2003) Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. Journal of Comparative Neurology 465, 90–103.Google Scholar
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.Google Scholar
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.Google Scholar
Haber, M., Zhou, L. and Murai, K.K. (2006) Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. Journal of Neuroscience 26, 8881–8891.Google Scholar
Iino, M., Goto, K., Kakegawa, W., Okado, H., Sudo, M., Ishiuchi, S. et al. (2001) Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia. Science 292, 926–929.CrossRefGoogle ScholarPubMed
Korkotian, E. and Segal, M. (2001) Regulation of dendritic spine motility in cultured hippocampal neurons. Journal of Neuroscience 21, 6115–6124.Google Scholar
Kumar, V., Zhang, M.X., Swank, M.W., Kunz, J. and Wu, G.Y. (2005) Regulation of dendritic morphogenesis by Ras-PI3 K-Akt-mTOR and Ras-MAPK signaling pathways. Journal of Neuroscience 25, 11288–11299.Google Scholar
Lippman, J.J., Lordkipanidze, T., Buell, M.E., Yoon, S.O. and Dunaevsky, A. (2008) Morphogenesis and regulation of Bergmann glial processes during Purkinje cell dendritic spine ensheathment and synaptogenesis. Glia 56, 1463–1477.CrossRefGoogle ScholarPubMed
Murai, K.K., Nguyen, L.N., Irie, F., Yamaguchi, Y. and Pasquale, E.B. (2003) Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nature Neuroscience 6, 153–160.Google Scholar
Nestor, M.W., Mok, L.P., Tulapurkar, M.E. and Thompson, S.M. (2007) Plasticity of neuron–glial interactions mediated by astrocytic EphARs. Journal of Neuroscience 27, 12817–12828.Google Scholar
Nishida, H. and Okabe, S. (2007) Direct astrocytic contacts regulate local maturation of dendritic spines. Journal of Neuroscience 27, 331–340.Google Scholar
Peters, A. and Kaiserman-Abramof, I.R. (1970) The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. American Journal of Anatomy 127, 321–355.Google Scholar
Sandsmark, D.K., Zhang, H., Hegedus, B., Pelletier, C.L., Weber, J.D. and Gutmann, D.H. (2007) Nucleophosmin mediates mammalian target of rapamycin-dependent actin cytoskeleton dynamics and proliferation in neurofibromin-deficient astrocytes. Cancer Research 67, 4790–4799.Google Scholar
Spacek, J. (1985) Three-dimensional analysis of dendritic spines. III. Glial sheath. Anatomy and Embryology 171, 245–252.CrossRefGoogle ScholarPubMed
Ventura, R. and Harris, K.M. (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. Journal of Neuroscience 19, 6897–6906.Google Scholar
Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nature Reviews. Neuroscience 6, 626–640.Google Scholar
Zepeda, R.C., Barrera, I., Castelan, F., Suarez-Pozos, E., Melgarejo, Y., Gonzalez-Mejia, E. et al. (2009) Glutamate-dependent phosphorylation of the mammalian target of rapamycin (mTOR) in Bergmann glial cells. Neurochemistry International 55, 282–287.Google Scholar
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