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Activity-dependent neuron–glial signaling by ATP and leukemia-inhibitory factor promotes hippocampal glial cell development*

Published online by Cambridge University Press:  09 March 2009

Jonathan E. Cohen
Affiliation:
Nervous Systems Development and Plasticity Section, National Institutes of Health, NICHD, USA
R. Douglas Fields*
Affiliation:
Nervous Systems Development and Plasticity Section, National Institutes of Health, NICHD, USA
*
Correspondence should be addressed to: R. Douglas Fields, Nervous System Development and Plasticity Section, National Institutes of Health, NICHD Bldg. 35, Room 2A211, MSC 3713, 35 Lincoln Drive, Bethesda, MD 20892, USA phone: +1 301 480-3209 fax: +1 496-9630 email: [email protected]

Abstract

Activity-dependent signaling between neurons and astrocytes contributes to experience-dependent plasticity and development of the nervous system. However, mechanisms responsible for neuron–glial interactions and the releasable factors that underlie these processes are not well understood. The pro-inflammatory cytokine, leukemia-inhibitory factor (LIF), is transiently expressed postnatally by glial cells in the hippocampus and rapidly up-regulated by enhanced neural activity following seizures. To test the hypothesis that spontaneous neural activity regulates glial development in hippocampus via LIF signaling, we blocked spontaneous activity with the sodium channel blocker tetrodotoxin (TTX) in mixed hippocampal cell cultures in combination with blockers of LIF and purinergic signaling. TTX decreased the number of GFAP-expressing astrocytes in hippocampal cell culture. Furthermore, blocking purinergic signaling by P2Y receptors contributed to reduced numbers of astrocytes. Blocking activity or purinergic signaling in the presence of function-blocking antibodies to LIF did not further decrease the number of astrocytes. Moreover, hippocampal cell cultures prepared from LIF −/− mice had reduced numbers of astrocytes and activity-dependent neuron–glial signaling promoting differentiation of astrocytes was absent. The results show that endogenous LIF is required for normal development of hippocampal astrocytes, and this process is regulated by spontaneous neural impulse activity through the release of ATP.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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Footnotes

*

Marc R Freeman served as Editor-in-Chief for this manuscript.

References

REFERENCES

Abbracchio, M.P., Ceruti, S., Langfelder, R., Cattabeni, F., Saffrey, M.J. and Burnstock, G. (1995) Effects of ATP analogues and basic fibroblast growth factor on astroglial cell differentiation in primary cultures of rat striatum. International Journal of Developmental Neuroscience 13, 685693.CrossRefGoogle ScholarPubMed
Bamber, B.A., Masters, B.A., Hoyle, G.W., Brinster, R.L. and Palmiter, R.D. (1994) Leukemia inhibitory factor induces neurotransmitter switching in transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 91, 78397843.CrossRefGoogle ScholarPubMed
Barnabe-Heider, F., Wasylnka, J.A., Fernandes, K.J., Porsche, C., Sendtner, M., Kaplan, D.R. et al. (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48, 253265.CrossRefGoogle ScholarPubMed
Barres, B.A. and Raff, M.C. (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361, 258260.CrossRefGoogle ScholarPubMed
Basarsky, T.A., Parpura, V., Haydon, P.G. (1994) Hippocampal synaptogenesis in cell culture: developmental time course of synapse formation, calcium influx, and synaptic protein distribution. Journal of Neuroscience 14, 64026411.CrossRefGoogle ScholarPubMed
Bauer, S., Kerr, B.J. and Patterson, P.H. (2007) The neuropoietic cytokine family in development, plasticity, disease and injury. Nature Reviews Neuroscience 8, 221232.CrossRefGoogle ScholarPubMed
Bolego, C., Ceruti, S., Brambilla, R., Puglisi, L., Cattabeni, F., Burnstock, G. et al. (1997) Characterization of the signalling pathways involved in ATP and basic fibroblast growth factor-induced astrogliosis. British Journal of Pharmacology 121, 16921699.CrossRefGoogle ScholarPubMed
Bonaguidi, M.A., McGuire, T., Hu, M., Kan, L., Samanta, J. and Kessler, J.A. (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132, 55035514.CrossRefGoogle ScholarPubMed
Bugga, L., Gadient, R.A., Kwan, K., Stewart, C.L. and Patterson, P.H. (1998) Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor. Journal of Neurobiology 36, 509524.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Catalani, A., Sabbatini, M., Consoli, C., Cinque, C., Tomassoni, D., Azmitia, E. et al. (2002) Glial fibrillary acidic protein immunoreactive astrocytes in developing rat hippocampus. Mechanisms of Ageing and Development 123, 481490.CrossRefGoogle ScholarPubMed
Djukic, B., Casper, K.B., Philpot, B.D., Chin, L.S. and McCarthy, K.D. (2007) Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. Journal of Neuroscience 27, 1135411365.CrossRefGoogle ScholarPubMed
Fields, R.D. and Burnstock, G. (2006) Purinergic signalling in neuron–glia interactions. Nature Reviews Neuroscience 7, 423436.CrossRefGoogle ScholarPubMed
Fields, R.D. and Stevens, B. (2000) ATP: an extracellular signaling molecule between neurons and glia. Trends in Neuroscience 23, 625633.CrossRefGoogle ScholarPubMed
Friedman, S. and Shatz, C.J. (1990) The effects of prenatal intracranial infusion of tetrodotoxin on naturally occurring retinal ganglion cell death and optic nerve ultrastructure. European Journal of Neuroscience 2, 243253.CrossRefGoogle ScholarPubMed
Gardiner, N.J., Cafferty, W.B., Slack, S.E. and Thompson, S.W. (2002) Expression of gp130 and leukaemia inhibitory factor receptor subunits in adult rat sensory neurones: regulation by nerve injury. Journal of Neurochemistry 83, 100109.CrossRefGoogle ScholarPubMed
Gargini, C., Deplano, S., Bisti, S. and Stone, J. (1998) Evidence that the influence of ganglion cell axons on astrocyte morphology is mediated by action spike activity during development. Brain Research Developmental Brain Research 110, 177184.CrossRefGoogle ScholarPubMed
Ge, W.P. and Duan, S. (2007) Persistent enhancement of neuron–glia signaling mediated by increased extracellular K+ accompanying long-term synaptic potentiation. Journal of Neurophysiology 97, 25642569.CrossRefGoogle ScholarPubMed
Goldman, S. (2003) Glia as neural progenitor cells. Trends in Neuroscience 26, 590596.CrossRefGoogle ScholarPubMed
Hawrylak, N. and Greenough, W.T. (1995) Monocular deprivation alters the morphology of glial fibrillary acidic protein-immunoreactive astrocytes in the rat visual cortex. Brain Research 683, 187199.CrossRefGoogle ScholarPubMed
Haydon, P.G. and Carmignoto, G. (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiological Reviews 86, 10091031.CrossRefGoogle ScholarPubMed
Holmberg, K.H. and Patterson, P.H. (2006) Leukemia inhibitory factor is a key regulator of astrocytic, microglial and neuronal responses in a low-dose pilocarpine injury model. Brain Research 1075, 2635.CrossRefGoogle Scholar
Ishibashi, T., Dakin, K.A., Stevens, B., Lee, P.R., Kozlov, S.V., Stewart, C.L. et al. (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49, 823832.CrossRefGoogle ScholarPubMed
Jankowsky, J.L. and Patterson, P.H. (1999) Differential regulation of cytokine expression following pilocarpine-induced seizure. Experimental Neurology 159, 333346.CrossRefGoogle ScholarPubMed
Jones, T.A., Hawrylak, N. and Greenough, W.T. (1996) Rapid laminar-dependent changes in GFAP immunoreactive astrocytes in the visual cortex of rats reared in a complex environment. Psychoneuroendocrinology 21, 189201.CrossRefGoogle Scholar
Koblar, S.A., Turnley, A.M., Classon, B.J., Reid, K.L., Ware, C.B., Cheema, S.S. et al. (1998) Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor. Proceedings of the National Academy of Sciences of the United States of America 95, 31783181.CrossRefGoogle ScholarPubMed
Kronenberg, G., Wang, L.P., Geraerts, M., Babu, H., Synowitz, M., Vicens, P. et al. (2007) Local origin and activity-dependent generation of nestin-expressing protoplasmic astrocytes in CA1. Brain Structure and Function 212, 1935.CrossRefGoogle ScholarPubMed
Lemke, R., Gadient, R.A., Schliebs, R., Bigl, V. and Patterson, P.H. (1996) Neuronal expression of leukemia inhibitory factor (LIF) in the rat brain. Neuroscience Letters 215, 205208.CrossRefGoogle ScholarPubMed
Lin, J.H., Takano, T., Arcuino, G., Wang, X., Hu, F., Darzynkiewicz, Z. et al. (2007) Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Developmental Biology 302, 356366.CrossRefGoogle ScholarPubMed
Minami, M., Maekawa, K., Yamakuni, H., Katayama, T., Nakamura, J. and Satoh, M. (2002) Kainic acid induces leukemia inhibitory factor mRNA expression in the rat brain: differences in the time course of mRNA expression between the dentate gyrus and hippocampal CA1/CA3 subfields. Brain Research Molecular Brain Research 107, 3946.CrossRefGoogle ScholarPubMed
Muller, C.M. (1990) Dark-rearing retards the maturation of astrocytes in restricted layers of cat visual cortex. Glia 3, 487494.CrossRefGoogle ScholarPubMed
Muller, S., Chakrapani, B.P., Schwegler, H., Hofmann, H.D. and Kirsch, M. (2008) Neurogenesis in the dentate gyrus depends on CNTF and STAT3 signaling. Stem Cells Express, published online November 20, 2008; doi:10.1634/stemcells.2008-0234Google Scholar
Neary, J.T., Baker, L., Jorgensen, S.L. and Norenberg, M.D. (1994) Extracellular ATP induces stellation and increases glial fibrillary acidic protein content and DNA synthesis in primary astrocyte cultures. Acta Neuropathologica 87, 813.CrossRefGoogle ScholarPubMed
North, R.A. and Verkhratsky, A. (2006) Purinergic transmission in the central nervous system. Pflugers Archives 452, 479485.CrossRefGoogle ScholarPubMed
Panatier, A., Theodosis, D.T., Mothet, J.P., Touquet, B., Pollegioni, L., Poulain, D.A. et al. (2006) Glia-derived d-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775784.CrossRefGoogle ScholarPubMed
Pascual, O., Casper, K.B., Kubera, C., Zhang, J., Revilla-Sanchez, R., Sul, J.Y. et al. (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113116.CrossRefGoogle ScholarPubMed
Pechnick, R.N., Chesnokova, V.M., Kariagina, A., Price, S., Bresee, C.J. and Poland, R.E. (2004) Reduced immobility in the forced swim test in mice with a targeted deletion of the leukemia inhibitory factor (LIF) gene. Neuropsychopharmacology 29, 770776.CrossRefGoogle ScholarPubMed
Pfrieger, F.W. and Barres, B.A. (1997) Synaptic efficacy enhanced by glial cells in vitro. Science 277, 16841687.CrossRefGoogle ScholarPubMed
Raponi, E., Agenes, F., Delphin, C., Assard, N., Baudier, J., Legraverend, C. et al. (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55, 165177.CrossRefGoogle Scholar
Rosell, D.R., Nacher, J., Akama, K.T. and McEwen, B.S. (2003) Spatiotemporal distribution of gp130 cytokines and their receptors after status epilepticus: comparison with neuronal degeneration and microglial activation. Neuroscience 122, 329348.CrossRefGoogle ScholarPubMed
Sirevaag, A.M. and Greenough, W.T. (1991) Plasticity of GFAP-immunoreactive astrocyte size and number in visual cortex of rats reared in complex environments. Brain Research 540, 273278.CrossRefGoogle ScholarPubMed
Spitzer, N.C. (2006) Electrical activity in early neuronal development. Nature 444, 707712.CrossRefGoogle ScholarPubMed
Stewart, C.L., Kaspar, P., Brunet, L.J., Bhatt, H., Gadi, I., Kontgen, F. et al. (1992) Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 7679.CrossRefGoogle ScholarPubMed
Ullian, E.M., Sapperstein, S.K., Christopherson, K.S. and Barres, B.A. (2001) Control of synapse number by glia. Science 291, 657661.CrossRefGoogle ScholarPubMed
Wallraff, A., Kohling, R., Heinemann, U., Theis, M., Willecke, K. and Steinhauser, C. (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. Journal of Neuroscience 26, 54385447.CrossRefGoogle ScholarPubMed
Watanabe, Y., Hashimoto, S., Kakita, A., Takahashi, H., Ko, J., Mizuno, M. et al. (2004) Neonatal impact of leukemia inhibitory factor on neurobehavioral development in rats. Neuroscience Research 48, 345353.CrossRefGoogle ScholarPubMed
Wei, L.C., Shi, M., Chen, L.W., Cao, R., Zhang, P. and Chan, Y.S. (2002) Nestin-containing cells express glial fibrillary acidic protein in the proliferative regions of central nervous system of postnatal developing and adult mice. Brain Research Developmental Brain Research 139, 917.CrossRefGoogle ScholarPubMed
Weissman, T.A., Riquelme, P.A., Ivic, L., Flint, A.C. and Kriegstein, A.R. (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43, 647661.CrossRefGoogle ScholarPubMed
Yamakuni, H., Kawaguchi, N., Ohtani, Y., Nakamura, J., Katayama, T., Nakagawa, T. et al. (2002) ATP induces leukemia inhibitory factor mRNA in cultured rat astrocytes. Journal of Neuroimmunology 129, 4350.CrossRefGoogle ScholarPubMed
Yamakuni, H., Minami, M. and Satoh, M. (1996) Localization of mRNA for leukemia inhibitory factor receptor in the adult rat brain. Journal of Neuroimmunology 70, 4553.Google ScholarPubMed
Yamamori, T., Fukada, K., Aebersold, R., Korsching, S., Fann, M.J. and Patterson, P.H. (1989) The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246, 14121416.CrossRefGoogle ScholarPubMed
Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C. et al. (2003) Contribution of astrocytes to hippocampal long-term potentiation through release of d-serine. Proceedings of the National Academy of Sciences of the United States of America 100, 1519415199.CrossRefGoogle ScholarPubMed
Zhu, Y. and Kimelberg, H.K. (2004) Cellular expression of P2Y and beta-AR receptor mRNAs and proteins in freshly isolated astrocytes and tissue sections from the CA1 region of P8–12 rat hippocampus. Brain Research Developmental Brain Research 148, 7787.CrossRefGoogle ScholarPubMed
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