Skip to main content

Advertisement

Log in

Gap Junctions Couple Astrocytes and Oligodendrocytes

  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

In vertebrates, a family of related proteins called connexins form gap junctions (GJs), which are intercellular channels. In the central nervous system (CNS), GJs couple oligodendrocytes and astrocytes (O/A junctions) and adjacent astrocytes (A/A junctions), but not adjacent oligodendrocytes, forming a “glial syncytium.” Oligodendrocytes and astrocytes each express different connexins. Mutations of these connexin genes demonstrate that the proper functioning of myelin and oligodendrocytes requires the expression of these connexins. The physiological function of O/A and A/A junctions, however, remains to be illuminated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8
Figure 9

Similar content being viewed by others

References

  • Abrams, C. K., Oh, S., Ri, Y., & Bargiello, T. A. (2000). Mutations in connexin 32: The molecular and biophysical bases for the X-linked form of Charcot–Marie–Tooth disease. Brain Research Reviews, 32, 203–214.

    PubMed  CAS  Google Scholar 

  • Ahmad, S., Chen, S. P., Sun, J. J., & Lin, X. (2003). Connexins 26 and 30 are co-assembled to form gap junctions in the cochlea of mice. Biochemical and Biophysical Research Communications, 307, 362–368.

    PubMed  CAS  Google Scholar 

  • Ahn, M., Lee, J., Gustafsson, A., et al. (2008). Cx29 and Cx32, two connexins expressed by myelinating glia, do not interact and are functionally distinct. Journal of Neuroscience Research (in press).

  • Altevogt, B. M., Kleopa, K. A., Postma, F. R., Scherer, S. S., & Paul, D. L. (2002). Cx29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. Journal of Neuroscience, 22, 6458–6470.

    PubMed  CAS  Google Scholar 

  • Altevogt, B. M., & Paul, D. L. (2004). Four classes of intercellular channels between glial cells in the CNS. Journal of Neuroscience, 24, 4313–4323.

    PubMed  CAS  Google Scholar 

  • Balice-Gordon, R. J., Bone, L. J., & Scherer, S. S. (1998). Functional gap junctions in the Schwann cell myelin sheath. Journal of Cell Biology, 142, 1095–1104.

    PubMed  CAS  Google Scholar 

  • Banks, E. A., Yu, X. S., Shi, Q., & Jiang, J. X. (2007). Promotion of lens epithelial-fiber differentiation by the C terminus of connexin 45.6 a role independent of gap junction communication. Journal of Cell Science, 120, 3602–3612.

    PubMed  CAS  Google Scholar 

  • Barbe, M. T., Monyer, H., & Bruzzone, R. (2006). Cell–cell communication beyond connexins: The pannexin channels. Physiology, 21, 103–114.

    PubMed  CAS  Google Scholar 

  • Barrio, L. C., Suchyna, T., Bargiello, T., et al. (1991). Gap junctions formed by connexins 26 and 32 alone and in combination are differently affected by applied voltage. Proceedings of the National Academy of Sciences of the United States of America, 88, 8410–8414.

    PubMed  CAS  Google Scholar 

  • Bedner, P., Niessen, H., Odermatt, B., Kretz, M., Willecke, K., & Harz, H. (2006). Selective permeability of different connexin channels to the second messenger cyclic AMP. Journal of Biological Chemistry, 281, 6673–6681.

    PubMed  CAS  Google Scholar 

  • Brink, P. R., Cronin, K., Banach, K., et al. (1997). Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. American Journal of Physiology - Cell Physiology, 42, C1386–C1396.

    Google Scholar 

  • Bruzzone, R., Hormuzdi, S. G., Barbe, M. T., Herb, A., & Monyer, H. (2003). Pannexins, a family of gap junction proteins expressed in brain. Proceedings of the National Academy of Sciences of the United States of America, 100, 13644–13649.

    PubMed  CAS  Google Scholar 

  • Bruzzone, R., White, T. W., & Paul, D. L. (1996). Connections with connexins: The molecular basis of direct intercellular signaling. European Journal of Biochemistry, 238, 1–27.

    PubMed  CAS  Google Scholar 

  • Bugiani, M., Al Shahwan, S., Lamantea, E., et al. (2006). GJA12 mutations in children with recessive hypomyelinating leukoencephalopathy. Neurology, 67, 273–279.

    PubMed  CAS  Google Scholar 

  • Bukauskas, F. F., Angele, A. B., Verselis, V. K., & Bennett, M. V. L. (2002). Coupling asymmetry of heterotypic connexin 45/connexin 43-EGFP gap junctions: Properties of fast and slow gating mechanisms. Proceedings of the National Academy of Sciences of the United States of America, 99, 7113–7118.

    PubMed  CAS  Google Scholar 

  • Bukauskas, F. F., Elfgang, C., Willecke, K., & Weingart, R. (1995). Heterotypic gap junction channels (connexin26–connexin32) violate the paradigm of unitary conductance. Pflügers Archiv—European Journal of Physiology, 429, 870–872.

    PubMed  CAS  Google Scholar 

  • Butt, A. M., & Ransom, B. R. (1989). Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. Glia, 2, 470–475.

    PubMed  CAS  Google Scholar 

  • Butt, A. M., & Ransom, B. R. (1993). Morphology of astrocytes and oligodendrocytes during development in the intact rat optic nerve. Journal of Comparative Neurology, 338, 141–158.

    PubMed  CAS  Google Scholar 

  • Charles, A. (1998). Intercellular calcium waves in glia. Glia, 24, 39–49.

    PubMed  CAS  Google Scholar 

  • Charles, A. C., Merrill, J. E., Dirksen, E. R., & Sandersont, M. J. (1991). Intercellular signaling in glial cells: Calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron, 6, 983–992.

    PubMed  CAS  Google Scholar 

  • Chvatal, A., Pastor, A., Mauch, M., Sykova, E., & Kettenmann, H. (1995). Distinct populations of identified glial cells in the developing rat spinal cord splice: Ion channel properties and cell morphology. European Journal of Neuroscience, 7, 129–142.

    PubMed  CAS  Google Scholar 

  • Connors, N. C., Adams, M. E., Froehner, S. C., & Kofuji, P. (2004). The potassium channel Kir4.1 associates with the dystrophin–glycoprotein complex via α-syntrophin in glia. Journal of Biological Chemistry, 279, 28387–28392.

    PubMed  CAS  Google Scholar 

  • Connors, B. W., & Long, M. A. (2004). Electrical synapses in the mammalian brain. Annual Review of Neuroscience, 27, 393–418.

    PubMed  CAS  Google Scholar 

  • Connors, B. W., Ransom, B. R., Kunis, D. M., & Gutnick, M. J. (1982). Activity-dependent K accumulation in the developing rat optic nerve. Science, 216, 1341–1343.

    PubMed  CAS  Google Scholar 

  • Cornell-Bell, A. H., & Finkbeiner, S. M. (1991). Ca2+ waves in astrocytes. Cell Calcium, 12, 185–204.

    PubMed  CAS  Google Scholar 

  • Cornell-Bell, A. H., Finkbeiner, S. M., Cooper, M. S., & Smith, S. J. (1990). Glutamate induces calcium waves in cultured astrocytes: Long-range glial signaling. Science, 247, 470–473.

    PubMed  CAS  Google Scholar 

  • Cottrell, G. T., & Burt, J. M. (2005). Functional consequences of heterogeneous gap junction channel formation and its influence in health and disease. Biochimica et Biophysica Acta Biomembranes, 1711, 126–141.

    CAS  Google Scholar 

  • Dahl, E., Manthey, D., Chen, Y., et al. (1996). Molecular cloning and functional expression of mouse connexin-30, a gap junction gene highly expressed in adult brain and skin. Journal of Biological Chemistry, 271, 17903–17910.

    PubMed  CAS  Google Scholar 

  • Dani, J. W., Chernjavsky, A., & Smith, S. J. (1992). Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron, 8, 429–440.

    PubMed  CAS  Google Scholar 

  • Das Sarma, J., Wang, F. S., & Koval, M. (2002). Targeted gap junction protein constructs reveal connexin-specific differences in oligomerization. Journal of Biological Chemistry, 277, 20911–20918.

    CAS  PubMed  Google Scholar 

  • Dermietzel, R., Farooq, M., Kessler, J. A., Althaus, H., Hertzberg, E. L., & Spray, D. C. (1997). Oligodendrocytes express gap junction proteins connexin32 and connexin45. Glia, 20, 101–114.

    PubMed  CAS  Google Scholar 

  • Dermietzel, R., Schunke, D., & Leibstein, A. (1978). The oligodendrocyte junctional complex. Cell & Tissue Research, 193, 61–72.

    CAS  Google Scholar 

  • Dermietzel, R., Traub, O., Hwang, T. K., et al. (1989). Differential expression of three gap junction proteins in developing and mature brain tissues. Proceedings of the National Academy of Sciences of the United States of America, 86, 10148–10152.

    PubMed  CAS  Google Scholar 

  • Di, W. L., Gu, Y., Common, J. E. A., et al. (2005). Connexin interaction patterns in keratinocytes revealed morphologically and by FRET analysis. Journal of Cell Science, 118, 1505–1514.

    PubMed  CAS  Google Scholar 

  • Djukic, B., Casper, K. B., Philpot, B. D., Chin, L.-S., & 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, 11354–11365.

    PubMed  CAS  Google Scholar 

  • Elfgang, C., Eckert, R., Lichternberg-Frate, H., et al. (1995). Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. Journal of Cell Biology, 129, 805–817.

    PubMed  CAS  Google Scholar 

  • Elias, L. A. B., Wang, D. D., & Kriegstein, A. R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature, 448, 901–907.

    PubMed  CAS  Google Scholar 

  • Enkvist, M. O. K., & McCarthy, K. D. (1994). Astroglial gap junction communication is increased by treatment with either glutamate or high K+ concentration. Journal of Neurochemistry, 62, 489–495.

    PubMed  CAS  Google Scholar 

  • Filippov, M. A., Hormuzdi, S. G., Fuchs, E. C., & Monyer, H. (2003). A reporter allele for investigating connexin 26 gene expression in the mouse brain. European Journal of Neuroscience, 18, 3183–3192.

    PubMed  Google Scholar 

  • Fink, D. J., Knapp, P. E., & Mata, M. (1996). Differential expression of Na,K-ATPase isoforms in oligodendrocytes and astrocytes. Developmental Neuroscience, 18, 319–326.

    PubMed  CAS  Google Scholar 

  • Finkbeiner, S. (1992). Calcium waves in astrocytes-filling in the gaps. Neuron, 8, 1101–1108.

    PubMed  CAS  Google Scholar 

  • Finkelstein, A., Meister, M., Buehler, L., Robinson, S. R., & Hampson, E. C. G. M. (1994). Gap junction and intercellular communications. Science, 265, 1017–1020.

    PubMed  CAS  Google Scholar 

  • Flenniken, A. M., Osborne, L. R., Anderson, N., et al. (2005). A Gja1 missense mutation in a mouse model of oculodentodigital dysplasia. Development, 132, 4375–4386.

    PubMed  CAS  Google Scholar 

  • Forge, A., Becker, D., Casalotti, S., Edwards, J., Marziano, N., & Nevill, G. (2003). Gap junctions in the inner ear: Comparison of distribution patterns in different vertebrates and assessment of connexin composition in mammals. Journal of Comparative Neurology, 467, 207–229.

    PubMed  Google Scholar 

  • Fry, T., Evans, J. H., & Sanderson, M. J. (2001). Propagation of intercellular calcium waves in C6 glioma cells transfected with connexins 43 or 32. Microscopy Research and Technique, 52, 289–300.

    PubMed  CAS  Google Scholar 

  • Garbern, J., Cambi, F., Shy, M., & Kamholz, J. (1999). The molecular pathogenesis of Pelizaeus–Merzbacher disease. Archives of Neurology, 56, 1210–1214.

    PubMed  CAS  Google Scholar 

  • Giepmans, B. N. G. (2004). Gap junctions and connexin-interacting proteins. Cardiovascular Research, 62, 233–245.

    PubMed  CAS  Google Scholar 

  • Giepmans, B. N. G., & Moolenaar, W. H. (1998). The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein. Current Biology, 8, 931–934.

    PubMed  CAS  Google Scholar 

  • Goldberg, G. S., Moreno, A. P., & Lampe, P. D. (2002). Gap junctions between cells expressing connexin 43 or 32 show inverse permselectivity to adenosine and ATP. Journal of Biological Chemistry, 277, 36725–36730.

    PubMed  CAS  Google Scholar 

  • Gonatas, N. K., Hirayama, M., Stieber, A., & Silberberg, D. H. (1982). The ultrastructure of isolated rat oligodendroglial cell cultures. Journal of Neurocytology, 11, 997–1008.

    PubMed  CAS  Google Scholar 

  • Gong, X.-Q., Shao, Q., Langlois, S., Bai, D., & Laird, D. W. (2007). Differential potency of dominant negative connexin43 mutants in oculodentodigital dysplasia. Journal of Biological Chemistry, 282, 19190–19202.

    PubMed  CAS  Google Scholar 

  • Gow, A., Southwood, C. M., Li, J. S., et al. (1999). CNS myelin and Sertoli cell tight junctions strands are absent in Osp/claudin-11 null mice. Cell, 99, 649–659.

    PubMed  CAS  Google Scholar 

  • Guadagno, E., & Moukhles, H. (2004). Laminin-induced aggregation of the inwardly rectifying potassium channel, Kir4.1, and the water-permeable channel, AQP4, via a dystroglycan-containing complex in astrocytes. Glia, 47, 138–149.

    PubMed  Google Scholar 

  • Guan, X., Cravatt, B. F., Ehring, G. R., et al. (1997). The sleep-inducing lipid oleamide deconvolutes gap junction communication and calcium wave transmission in glial cells. Journal of Cell Biology, 139, 1785–1792.

    PubMed  CAS  Google Scholar 

  • Haas, B., Schipke, C. G., Peters, O., Sohl, G., Willecke, K., & Kettenmann, H. (2006). Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cerebral Cortex, 16, 237–246.

    PubMed  Google Scholar 

  • Hahn, A. F., Ainsworth, P. J., Naus, C. C. G., Mao, J., & Bolton, C. F. (2000). Clinical and pathological observations in men lacking the gap junction protein connexin 32. Muscle & Nerve, 23, S39–S48.

    Google Scholar 

  • Halassa, M. M., Fellin, T., Takano, H., Dong, J.-H., & Haydon, P. G. (2007). Synaptic islands defined by the territory of a single astrocyte. Journal of Neuroscience, 27, 6473–6477.

    PubMed  CAS  Google Scholar 

  • Hampson, E. C. G. M., & Robinson, S. R. (1995). Heterogeneous morphology and tracer coupling patterns of retinal oligodendrocytes. Philosophical Transactions: Biological Sciences, 349, 353–364.

    CAS  Google Scholar 

  • Harris, A. L. (2007). Connexin channel permeability to cytoplasmic molecules. Progress in Biophysics and Molecular Biology, 94, 120–143.

    PubMed  CAS  Google Scholar 

  • Hassinger, T. D., Guthrie, P. B., Atkinson, P. B., Bennett, M. V. L., & Kater, S. B. (1996). An extracellular signaling component in propagation of astrocytic calcium waves. Proceedings of the National Academy of Sciences of the United States of America, 93, 13268–13273.

    PubMed  CAS  Google Scholar 

  • Higashi, K., Fujita, A., Inanobe, A., et al. (2001). An inwardly rectifying K+ channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. American Journal of Physiology - Cell Physiology, 281, C922–C931.

    PubMed  CAS  Google Scholar 

  • Holthoff, K., & Witte, O. W. (2000). Directed spatial potassium redistribution in rat neocortex. Glia, 29, 288–292.

    PubMed  CAS  Google Scholar 

  • Huang, Y., Grinspan, J. B., Abrams, C. K., & Scherer, S. S. (2007). Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia, 55, 46–56.

    PubMed  Google Scholar 

  • Huang, Y., Sirkowski, E. E., Stickney, J. T., & Scherer, S. S. (2005). Prenylation-defective human connexin32 mutants are normally localized and function equivalently to wild-type connexin32 in myelinating Schwann cells. Journal of Neuroscience, 25, 7111–7120.

    PubMed  CAS  Google Scholar 

  • Hurtley, S. M., & Helenius, A. (1989). Protein oligomerization in the endoplasmic reticulum. Annual Review of Cell Biology, 5, 277–307.

    PubMed  CAS  Google Scholar 

  • Ishibashi, T., Dakin, K. A., Stevens, B., et al. (2006). Astrocytes promote myelination in response to electrical impulses. Neuron, 49, 823–832.

    PubMed  CAS  Google Scholar 

  • Jeng, L. B. J., Balice-Gordon, R. J., Messing, A., Fischbeck, K. H., & Scherer, S. S. (2006). The effects of a dominant connexin32 mutant in myelinating Schwann cells. Molecular and Cellular Neuroscience, 32, 283–298.

    PubMed  CAS  Google Scholar 

  • Juhaszova, M., & Blaustein, M. P. (1997). Na+ pump low and high ouabain affinity α subunit isoforms are differentially distributed in cells. Proceedings of the National Academy of Sciences of the United States of America, 94, 1800–1805.

    PubMed  CAS  Google Scholar 

  • Kalsi, A. S., Greenwood, K., Wilkin, G., & Butt, A. M. (2004). Kir4.1 expression by astrocytes and oligodendrocytes in CNS white matter: A developmental study in the rat optic nerve. Journal of Anatomy, 204, 475–485.

    PubMed  Google Scholar 

  • Kamasawa, N., Sik, A., Morita, M., et al. (2005). Connexin-47 and connexin-32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops and Schmidt–Lanterman incisures: Implications for ionic homeostasis and potassium siphoning. Neuroscience, 136, 65–86.

    PubMed  CAS  Google Scholar 

  • Kettenmann, H., & Ransom, B. R. (1988). Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia, 1, 64–73.

    PubMed  CAS  Google Scholar 

  • Kikuchi, T., Kimura, R. S., Paul, D. L., & Adams, J. C. (1995). Gap junctions in the rat cochlea: Immunohistochemical and ultrastructural analysis. Anatomy and Embryology, 191, 101–118.

    PubMed  CAS  Google Scholar 

  • Kleopa, K. A., Orthmann, J. L., Enriquez, A., Paul, D. L., & Scherer, S. S. (2004). Unique distributions of the gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia, 47, 346–357.

    PubMed  Google Scholar 

  • Kleopa, K. A., Yum, S. W., & Scherer, S. S. (2002). Cellular mechanisms of connexin32 mutations associated with CNS manifestations. Journal of Neuroscience Research, 68, 522–534.

    PubMed  CAS  Google Scholar 

  • Kofuji, P., Ceelen, P., Zahs, K. R., Surbeck, L. W., Lestern, H. A., & Newman, E. A. (2000). Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. Journal of Neuroscience, 20, 5733–5740.

    PubMed  CAS  Google Scholar 

  • Kofuji, P., & Newman, E. A. (2004). Potassium buffering in the central nervous system. Neuroscience, 129, 1043–1054.

    Google Scholar 

  • Kruger, O., Plum, A., Kim, J. S., et al. (2000). Defective vascular development in connexin 45-deficient mice. Development, 127, 4179–4193.

    PubMed  CAS  Google Scholar 

  • Kumar, N. M., Friend, D. S., & Gilula, N. B. (1995). Synthesis and assembly of human β1 gap junctions in BHK cells by DNA transfection with the human β1 cDNA. Journal of Cell Science, 108, 3725–3734.

    PubMed  CAS  Google Scholar 

  • Kumar, N. M., & Gilula, N. B. (1996). The gap junction communication channel. Cell, 84, 381–389.

    PubMed  CAS  Google Scholar 

  • Kunzelmann, P., Blumcke, I., Traub, O., Dermietzel, R., & Willecke, K. (1997). Coexpression of connexin45 and -32 in oligodendrocytes of rat brain. Journal of Neurocytology, 26, 17–22.

    PubMed  CAS  Google Scholar 

  • Kunzelmann, P., Schroder, W., Traub, O., Steinhauser, C., Dermietzel, R., & Willecke, K. (1999). Late onset and increasing expression of the gap junction protein connexin30 in adult murine brain and long-term cultured astrocytes. Glia, 25, 111–119.

    PubMed  CAS  Google Scholar 

  • Lautermann, J., tenCate, W. J. F., Altenhoff, P., et al. (1998). Expression of the gap-junction connexins 26 and 30 in the rat cochlea. Cell & Tissue Research, 294, 415–420.

    CAS  Google Scholar 

  • Lee, S. H., Kim, W. T., Cornell-Bell, A. H., & Sontheimer, H. (1994). Astrocytes exhibit regional specificity in gap-junction coupling. Glia, 11, 315–325.

    PubMed  CAS  Google Scholar 

  • Lee, M. J., Nelson, I., Houlden, H., et al. (2002). Six novel connexin32 (GJB1) mutations in X-linked Charcot–Marie–Tooth disease. Journal of Neurology, Neurosurgery and Psychiatry, 73, 304–306.

    Google Scholar 

  • Li, J., Hertzberg, E. L., & Nagy, J. I. (1997). Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. Journal of Comparative Neurology, 379, 571–591.

    PubMed  CAS  Google Scholar 

  • Li, X., Ionescu, A. V., Lynn, B. D., et al. (2004). Connexin47, connexin29 and connexin32 co-expression in oligodendrocytes and Cx47 association with zonula occludens-1 (ZO-1) in mouse brain. Neuroscience, 126, 611–630.

    PubMed  CAS  Google Scholar 

  • Li, X., Lynn, B. D., Olson, C., et al. (2002). Connexin29 expression, immunocytochemistry and freeze-fracture replica immunogold labelling (FRIL) in sciatic nerve. European Journal of Neuroscience, 16, 795–806.

    PubMed  Google Scholar 

  • Locovei, S., Bao, L., & Dahl, G. (2006). Pannexin 1 in erythrocytes: Function without a gap. Proceedings of the National Academy of Sciences of the United States of America, 103, 7655–7659.

    PubMed  CAS  Google Scholar 

  • Loddenkemper, T., Grote, K., Evers, S., Oelerich, M., & Stoghauer, F. (2002). Neurological manifestations of the oculodentodigital dysplasia syndrome. Journal of Neurology, 249, 584–595.

    PubMed  Google Scholar 

  • MacKenzie, M. L., Ghabriel, M. N., & Allt, G. (1984). Nodes of Ranvier and Schmidt–Lanterman incisures: An in vivo lanthanum tracer study. Journal of Neurocytology, 13, 1043–1055.

    PubMed  CAS  Google Scholar 

  • MacVicar, B. A., Feighan, D., Brown, A., & Ransom, B. R. (2002). Intrinsic optical signals in the rat optic nerve: Role for K+ uptake via NKCC1 and swelling of astrocytes. Glia, 37, 114–123.

    PubMed  Google Scholar 

  • Marrero, H., & Orkand, R. K. (1996). Nerve impulses increase glial intercellular permeability. Glia, 16, 285–289.

    PubMed  CAS  Google Scholar 

  • Massa, P. T., & Mugnaini, E. (1982). Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: A freeze-fracture study. Neuroscience, 7, 523–538.

    PubMed  CAS  Google Scholar 

  • Massa, P. T., Szuchet, S., & Mugnaini, E. (1984). Cell–cell interactions of isolated and cultured oligodendrocytes: Formation of linear occluding junctions and expression of peculiar intramembrane particles. Journal of Neuroscience, 4, 3128–3139.

    PubMed  CAS  Google Scholar 

  • Meier, C., Dermietzel, R., Davidson, K. G. V., Yasumura, T., & Rash, J. E. (2004). Connexin32-containing gap junctions in Schwann cells at the internodal zone of partial myelin compaction and in Schmidt–Lanterman incisures. Journal of Neuroscience, 24, 3186–3198.

    PubMed  CAS  Google Scholar 

  • Menichella, D. M., Goodenough, D. A., Sirkowski, E., Scherer, S. S., & Paul, D. L. (2003). Connexins are critical for normal myelination in the central nervous system. Journal of Neuroscience, 23, 5963–5973.

    PubMed  CAS  Google Scholar 

  • Menichella, D. M., Majdan, M., Awatramani, R., et al. (2006). Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. Journal of Neuroscience, 26, 10984–10991.

    PubMed  CAS  Google Scholar 

  • Metea, M. R., Kofuji, P., & Newman, E. A. (2007). Neurovascular coupling is not mediated by potassium siphoning from glial cells. Journal of Neuroscience, 27, 2468–2471.

    PubMed  CAS  Google Scholar 

  • Micevych, P. E., & Abelson, L. (1991). Distribution of mRNAs coding for liver and heart gap junction proteins in the rat central nervous system. Journal of Comparative Neurology, 305, 96–118.

    PubMed  CAS  Google Scholar 

  • Morita, K., Sasaki, H., Fujimoto, K., Furuse, M., & Tsukita, S. (1999). Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. Journal of Cell Biology, 145, 579–588.

    PubMed  CAS  Google Scholar 

  • Mugnaini, E. (1986). Cell junctions of astrocytes, ependyma, and related cells in the mammalian central nervous system, with emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In S. Federoff, & A. Vernadakis (Eds.) Astrocytes (vol. vol. 1, (pp. 329–371)). Orlando: Academic.

    Google Scholar 

  • Musil, L. S., & Goodenough, D. A. (1993). Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell, 74, 1075–1077.

    Google Scholar 

  • Nagy, J. I., Dudek, F. E., & Rash, J. E. (2004). Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Research Reviews, 47, 191–215.

    PubMed  CAS  Google Scholar 

  • Nagy, J. I., Ionescu, A. V., Lynn, B. D., & Rash, J. E. (2003a). Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system. Journal of Comparative Neurology, 464, 356–370.

    PubMed  CAS  Google Scholar 

  • Nagy, J. I., Ionescu, A. V., Lynn, B. D., & Rash, J. E. (2003b). Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: Implications from normal and connexin32 knockout mice. Glia, 44, 205–218.

    PubMed  CAS  Google Scholar 

  • Nagy, J. I., Li, X. B., Rempel, J., et al. (2001). Connexin26 in adult rodent central nervous system: Demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43. Journal of Comparative Neurology, 441, 302–323.

    PubMed  CAS  Google Scholar 

  • Nagy, J. I., Ochalski, P. A. Y., Li, J., & Hertzberg, E. L. (1997). Evidence for the co-localization of another connexin with connexin-43 at astrocytic gap junctions in rat brain. Neuroscience, 78, 533–548.

    PubMed  CAS  Google Scholar 

  • Nagy, J. I., Patel, D., Ochalski, P. A. Y., & Stelmack, G. L. (1999). Connexin30 in rodent, cat and human brain: Selective expression in gray matter astrocytes, co-localization with connexin43 at gap junctions and late developmental appearance. Neuroscience, 88, 447–468.

    PubMed  CAS  Google Scholar 

  • Naus, C. C. G., Bechberger, J. F., Zhang, Y. C., et al. (1997). Altered gap junctional communication, intercellular signaling, and growth in cultured astrocytes deficient in connexin43. Journal of Neuroscience Research, 49, 528–540.

    PubMed  CAS  Google Scholar 

  • Nedergaard, M. (1994). Direct signaling from astrocytes to neurons in cultures of mammalian brain cells. Science, 263, 1768–1771.

    PubMed  CAS  Google Scholar 

  • Neusch, C., Rozengurt, N., Jacobs, R. E., Lester, H. A., & Kofuji, P. (2001). Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. Journal of Neuroscience, 21, 5429–5438.

    PubMed  CAS  Google Scholar 

  • Newman, E. A., & Zahs, K. R. (1997). Calcium waves in retinal glial cells. Science, 275, 844–847.

    PubMed  CAS  Google Scholar 

  • Nicholson, G., & Corbett, A. (1996). Slowing of central conduction in X-linked Charcot–Marie–Tooth neuropathy shown by brain auditory evoked responses. Journal of Neurology, Neurosurgery and Psychiatry, 61, 43–46.

    Article  CAS  Google Scholar 

  • Niessen, H., Harz, H., Bedner, P., Kramer, K., & Willecke, K. (2000). Selective permeability of different connexin channels to the second messenger inositol 1,4,5-trisphosphate. Journal of Cell Science, 113, 1365–1372.

    PubMed  CAS  Google Scholar 

  • Norton, K. K., Carey, J. C., & Gutman, D. H. (1995). Oculodentodigital dysplasia with cerebral white matter abnormalities in a two-generation family. American Journal of Medical Genetics, 57, 458–461.

    PubMed  CAS  Google Scholar 

  • Odermatt, B., Wellershaus, K., Wallraff, A., et al. (2003). Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. Journal of Neuroscience, 23, 4549–4559.

    PubMed  CAS  Google Scholar 

  • Olsen, M. L., Higashimori, H., Campbell, S. L., Hablitz, J. J., & Sontheimer, H. (2006). Functional expression of Kir4.1 channels in spinal cord astrocytes. Glia, 53, 516–528.

    PubMed  CAS  Google Scholar 

  • Opjordsmoen, S., & Nyberg-Hansen, R. (1980). Hereditary spastic paraplegia with neurogenic bladder disturbances and syndactylia. Acta Neurologica Scandinavica, 61, 35–41.

    Article  PubMed  CAS  Google Scholar 

  • Orkand, R. K. (1986). Glial-interstitial fluid exchange. Annals of the New York Academy of Sciences, 481, 269–272.

    PubMed  CAS  Google Scholar 

  • Orkand, P. M., Nicholls, J. G., & Kuffler, S. W. (1966). Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. Journal of Neurophysiology, 29, 788–806.

    PubMed  CAS  Google Scholar 

  • Orthmann-Murphy, J. L., Enriquez, A. D., Abrams, C. K., & Scherer, S. S. (2007a). Loss-of-function GJA12/Connexin47 mutations cause Pelizaeus–Merzbacher-like disease. Molecular and Cellular Neuroscience, 34, 629–641.

    PubMed  CAS  Google Scholar 

  • Orthmann-Murphy, J. L., Fischer, E., Freidin, M., Scherer, S. S., & Abrams, C. K. (2007b). Two distinct heterotypic channels mediate gap junction coupling between astrocyte and oligodendrocyte connexins. Journal of Neuroscience, 27, 13949–13957.

    PubMed  CAS  Google Scholar 

  • Panchin, Y. V. (2005). Evolution of gap junction proteins—The pannexin alternative. Journal of Experimental Biology, 208, 1415–1419.

    PubMed  CAS  Google Scholar 

  • Panchin, Y., Kelmanson, I., Matz, , Lukyanov, K., Usman, N., & Lukyanov, S. (2000). A ubiquitous family of putative gap junction molecules. Current Biology, 10, R473–R474.

    PubMed  CAS  Google Scholar 

  • Pastor, A., Kremer, M., Moller, T., Kettenmann, H., & Dermietzel, R. (1998). Dye coupling between spinal cord oligodendrocytes: Differences in coupling efficiency between gray and white matter. Glia, 24, 108–120.

    PubMed  CAS  Google Scholar 

  • Paznekas, W. A., Boyadjiev, S. A., Shapiro, R. E., et al. (2003). Connexin 43 (GJA1) mutations cause the pleiotropic phenotype of oculodentodigital dysplasia. American Journal of Human Genetics, 72, 408–418.

    PubMed  CAS  Google Scholar 

  • Pelegrin, P., & Surprenant, A. (2006). Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO Journal, 25, 5071–5082.

    PubMed  CAS  Google Scholar 

  • Peters, A., Palay S. L., & Webster H. d. (1991). The Fine Structure of the Nervous System: Neurons and their Supporting Cells. Oxford University Press, New York.

  • Penuela, S., Bhalla, R., Gong, X.-Q., et al. (2007). Pannexin 1 and pannexin 3 are glycoproteins that exhibit many distinct characteristics from the connexin family of gap junction proteins. Journal of Cell Science, 120, 3772–3783.

    CAS  Google Scholar 

  • Phelan, P., Bacon, J. P. A., Davies, J., Stebbings, L. A., & Todman, M. G. (1998a). Innexins: A family of invertebrate gap-junction proteins. Trends in Genetics, 14, 348–349.

    PubMed  CAS  Google Scholar 

  • Phelan, P., Stebbings, L. A., Baines, R. A., Bacon, J. P., Davies, J. A., & Ford, C. (1998b). Drosophila Shaking-B protein forms gap junctions in paired Xenopus oocytes. Nature, 391, 181–184.

    PubMed  CAS  Google Scholar 

  • Plantard, L., Huber, M., Macari, F., Meda, P., & Hohl, D. (2003). Molecular interaction of connexin 30.3 and connexin 31 suggests a dominant-negative mechanism associated with erythrokeratodermia variabilis. Human Molecular Genetics, 12, 3287–3294.

    PubMed  CAS  Google Scholar 

  • Poopalasundaram, S., Knott, C., Shamotienko, O. G., et al. (2000). Glial heterogeneity in expression of the inwardly rectifying K+ channel, Kir4.1, in adult rat CNS. Glia, 30, 362–372.

    PubMed  CAS  Google Scholar 

  • Ransom, B. R., & Kettenmann, H. (1990). Electrical coupling, without dye coupling, between mammalian astrocytes and oligodendrocytes in cell culture. Glia, 3, 258–266.

    PubMed  CAS  Google Scholar 

  • Ransom, C. B., Ransom, B. R., & Sontheimer, H. (2000). Activity-dependent extracellular K+ accumulation in rat optic nerve: The role of glial and axonal Na+ pumps. Journal of Physiology, 522, 427–442.

    PubMed  CAS  Google Scholar 

  • Ransom, B. R., Yamate, C. L., & Connors, B. W. (1985). Activity-dependent shrinkage of extracellular space in rat optic nerve: A developmental study. Journal of Neuroscience, 5, 532–535.

    PubMed  CAS  Google Scholar 

  • Rash, J. E., Duffy, H. S., Dudek, F. E., Bilhartz, B. L., Whalen, L. R., & Yasumura, T. (1997). Grid-mapped freeze-fracture analysis of gap junctions in gray and white matter of adult rat central nervous system, with evidence for a “'panglial syncytium” that is not coupled to neurons. Journal of Comparative Neurology, 388, 265–292.

    PubMed  CAS  Google Scholar 

  • Rash, J. E., Olson, C. O., Davidson, K. G. V., Yasumura, T., Kamasawa, N., & Nagy, J. I. (2007a). Identification of connexin36 in gap junctions between neurons in rodent locus coeruleus. Neuroscience, 147, 938–956.

    PubMed  CAS  Google Scholar 

  • Rash, J. E., Olson, C. O., Pouliot, W. A., et al. (2007b). Connexin36 vs. connexin32, “miniature” neuronal gap junctions, and limited electrotonic coupling in rodent suprachiasmatic nucleus. Neuroscience, 149, 350–371.

    PubMed  CAS  Google Scholar 

  • Rash, J. E., Yasumura, T., Dudek, F. E., & Nagy, J. I. (2001). Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. Journal of Neuroscience, 21, 1983–2000.

    PubMed  CAS  Google Scholar 

  • Ray, A., Zoidl, G., Weickert, S., Wahle, P., & Dermietzel, R. (2005). Site-specific and developmental expression of pannexin1 in the mouse nervous system. European Journal of Neuroscience, 21, 3277–3290.

    PubMed  Google Scholar 

  • Reaume, A. G., de Sousa, P. A., Kulkarni, S., et al. (1995). Cardiac malformation in neonatal mice lacking connexin43. Science, 267, 1831–1834.

    PubMed  CAS  Google Scholar 

  • Robinson, S. R., Hampson, E. C. G. M., Munro, M. N., & Vaney, D. I. (1993). Unidirectional coupling of gap junctions between neuroglia. Science, 262, 1072–1074.

    PubMed  CAS  Google Scholar 

  • Rohr, S. (2004). Role of gap junctions in the propagation of the cardiac action potential. Cardiovascular Research, 62, 309–322.

    PubMed  CAS  Google Scholar 

  • Roscoe, W., Veitch, G. I. L., Gong, X. Q., et al. (2005). Oculodentodigital dysplasia-causing connexin43 mutants are non-functional and exhibit dominant effects on wild-type connexin43. Journal of Biological Chemistry, 280, 11458–11466.

    PubMed  CAS  Google Scholar 

  • Rose, J. K., & Doms, R. W. (1988). Regulation of protein export from the endoplasmic reticulum. Annual Review of Cell Biology, 4, 257–288.

    PubMed  CAS  Google Scholar 

  • Sandri, C., Van Buren, J. M., & Akert, K. (1982). Membrane morphology of the vertebrate nervous system. Progress in Brain Research, 46, 201–265.

    Google Scholar 

  • Scemes, E., & Giaume, C. (2006). Astrocyte calcium waves: What they are and what they do. Glia, 54, 716–725.

    PubMed  Google Scholar 

  • Scherer, S. S., Arroyo, E. J., & Peles, E. (2004). Functional organization of the nodes of Ranvier. In R. L. Lazzarini (Ed.) Myelin biology and disorders (vol. 1, (pp. 89–116)). San Diego: Elsevier.

    Google Scholar 

  • Scherer, S. S., Deschênes, S. M., Xu, Y.-T., Grinspan, J. B., Fischbeck, K. H., & Paul, D. L. (1995). Connexin32 is a myelin-related protein in the PNS and CNS. Journal of Neuroscience, 15, 8281–8294.

    PubMed  CAS  Google Scholar 

  • Scherer, S. S., & Kleopa, K. A. (2005). X-linked Charcot–Marie–Tooth disease. In P. J. Dyck, & P. K. Thomas (Eds.) Peripheral neuropathy (vol. 2, (pp. 1791–1804)). Philadelphia: Saunders.

    Google Scholar 

  • Scherer, S. S., Xu, Y.-T., Nelles, E., Fischbeck, K., Willecke, K., & Bone, L. J. (1998). Connexin32-null mice develop a demyelinating peripheral neuropathy. Glia, 24, 8–20.

    PubMed  CAS  Google Scholar 

  • Seki, A., Coombs, W., Taffet, S., & Delmar, M. (2004). Loss of electrical communication, but not plaque formation, after mutations in the cytoplasmic loop of connexin43. Heart Rhythm, 1, 227–233.

    PubMed  Google Scholar 

  • Shapiro, R. E., Griffin, J. W., & Stine, O. C. (1997). Evidence for genetic anticipation in the oculodentodigital syndrome. American Journal of Medical Genetics, 71, 36–41.

    PubMed  CAS  Google Scholar 

  • Shibayama, J., Paznekas, W., Seki, A., et al. (2005). Functional characterization of connexin43 mutations found in patients with oculodentodigital dysplasia. Circulation Research, 96, e83–e91.

    PubMed  CAS  Google Scholar 

  • Stanislaw, C. L., Narvaez, C., Roger, R. G., & Woodard, C. S. (1998). Oculodentodigital dysplasia with cerebral white matter abnormalities: An additional case. Proceedings of the Greenwood Genetic Center, 17, 20–24.

    Google Scholar 

  • Stout, C. E., Costantin, J. L., Naus, C. C. G., & Charles, A. C. (2002). Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. Journal of Biological Chemistry, 277, 10482–10488.

    PubMed  CAS  Google Scholar 

  • Suadicani, S. O., Brosnan, C. F., & Scemes, E. (2006). P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2 signaling. Journal of Neuroscience, 26, 1378–1385.

    PubMed  CAS  Google Scholar 

  • Sun, J., Ahmad, S., Chen, S., et al. (2005). Cochlear gap junctions coassembled from Cx26 and 30 show faster intercellular Ca2+ signaling than homomeric counterparts. American Journal of Physiology - Cell Physiology, 288, C613–C623.

    PubMed  CAS  Google Scholar 

  • Swenson, K. I., Jordan, J. R., Beyer, E. C., & Paul, D. L. (1989). Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell, 57, 145–155.

    PubMed  CAS  Google Scholar 

  • Taylor, R. A., Simon, E. M., Marks, H. G., & Scherer, S. S. (2003). The CNS phenotype of X-linked Charcot–Marie–Tooth disease: More than a peripheral problem. Neurology, 61, 1475–1478.

    PubMed  Google Scholar 

  • Uhlenberg, B., Schuelke, M., Ruschendorf, F., et al. (2004). Mutations in the gene encoding gap junction protein alpha 12 (connexin 46.6) cause Pelizaeus–Merzbacher-like disease. American Journal of Human Genetics, 75, 251–260.

    PubMed  CAS  Google Scholar 

  • Valiunas, V., Weingart, R., & Brink, P. R. (2000). Formation of heterotypic gap junction channels by connexins 40 and 43. Circulation Research, 86, 42e–49e.

    Google Scholar 

  • Venance, L., Cordier, J., Monge, M., Zalc, B., Glowinski, J., & Giaume, C. (1995). Homotypic and heterotypic coupling mediated by gap junctions during glial cell differentiation in vitro. European Journal of Neuroscience, 7, 451–461.

    PubMed  CAS  Google Scholar 

  • Vogt, A., Hormuzdi, S. G., & Monyer, H. (2005). Pannexin1 and pannexin2 expression in the developing and mature rat brain. Molecular Brain Research, 141, 113–120.

    PubMed  CAS  Google Scholar 

  • von Blankenfeld, G., Ransom, B. R., & Kettenmann, H. (1993). Development of cell–cell coupling among cells of the oligodendrocyte lineage. Glia, 7, 322–328.

    Google Scholar 

  • Wallraff, A., Kohling, R., Heinemann, U., Theis, M., Willecke, K., & Steinhauser, C. (2006). The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. Journal of Neuroscience, 26, 5438–5447.

    PubMed  CAS  Google Scholar 

  • Walz, W. (2000). Role of astrocytes in the clearance of excess extracellular potassium. Neurochemistry International, 36, 291–300.

    PubMed  CAS  Google Scholar 

  • Waxman, S. G., & Sims, T. J. (1984). Specificity in central myelination: Evidence for local regulation of myelin thickness. Brain Research, 292, 179–185.

    PubMed  CAS  Google Scholar 

  • Weber, P. A., Chang, H.-C., Spaeth, K. E., Nitsche, J. M., & Nicholson, B. J. (2004). The permeability of gap junction channels to probes of different size Is dependent on connexin composition and permeant-pore affinities. Biophysical Journal, 87, 958–973.

    PubMed  CAS  Google Scholar 

  • Werner, R., Levine, E., Rabadan-Diehl, C., & Dahl, G. (1989). Formation of hybrid cell–cell channels. Proceedings of the National Academy of Sciences of the United States of America, 86, 5380–5384.

    PubMed  CAS  Google Scholar 

  • White, T. W., Paul, D. L., Goodenough, D. A., & Bruzzone, R. (1995). Functional analysis of selective interactions among rodent connexins. Molecular Biology of the Cell, 6, 459–470.

    PubMed  CAS  Google Scholar 

  • White, T. W., Wang, H., Mui, R., Litteral, J., & Brink, P. R. (2004). Cloning and functional expression of invertebrate connexins from Halocynthia pyriformis. FEBS Letters, 577, 42–48.

    PubMed  CAS  Google Scholar 

  • Wiest, T., Herrmann, O., Stogbauer, F., et al. (2006). Clinical and genetic variability of oculodentodigital dysplasia. Clinical Genetics, 70, 71–72.

    PubMed  CAS  Google Scholar 

  • Willecke, K., Eiberger, J., Degen, J., et al. (2002). Structural and functional diversity of connexin genes in the mouse and human genome. Biological Chemistry, 383, 725–737.

    PubMed  CAS  Google Scholar 

  • Yamamoto, T., Ochalski, A., Hertzberg, E. L., & Nagy, J. I. (1990a). LM and EM immunolocalization of the gap junctional protein connexin 43 in rat brain. Brain Research, 508, 313–319.

    PubMed  CAS  Google Scholar 

  • Yamamoto, T., Ochalski, A., Hertzberg, E. L., & Nagy, J. L. (1990b). On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. Journal of Comparative Neurology, 302, 853–883.

    PubMed  CAS  Google Scholar 

  • Yeager, M., & Nicholson, B. J. (1996). Structure of gap junction intercellular channels. Current Opinion in Structural Biology, 6, 183–192.

    PubMed  CAS  Google Scholar 

  • Yeager, M., Unger, V. M., & Falk, M. M. (1998). Synthesis, assembly and structure of gap junction intercellular channels. Current Opinion in Structural Biology, 8, 517–524.

    PubMed  CAS  Google Scholar 

  • Yum, S. W., Kleopa, K. A., Shumas, S., & Scherer, S. S. (2002). Diverse trafficking abnormalities for connexin32 mutants causing CMTX. Neurobiology of Disease, 11, 43–52.

    PubMed  CAS  Google Scholar 

  • Yum, S. W., Zhang, J., Valiunas, V., et al. (2007). Human connexin26 and connexin30 form functional heteromeric and heterotypic channels. American Journal of Physiology - Cell Physiology, 293, C1032–C1048.

    PubMed  CAS  Google Scholar 

  • Zahs, K. R., Kofuji, P., Meier, C., & Dermietzel, R. (2003). Connexin immunoreactivity in glial cells of the rat retina. Journal of Comparative Neurology, 455, 531–546.

    PubMed  Google Scholar 

  • Zanotti, S., & Charles, A. (1997). Extracellular calcium sensing by glial cells: Low extracellular calcium induces intracellular calcium release and intercellular signaling. Journal of Neurochemistry, 69, 594–602.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the National Multiple Sclerosis Society and the following NIH grants: NS054363 (to J.L.O.-M.), NS55284 and NS043560 (to S.S.S.), and NS50345 and NS050705 (to C.K.A.). We thank Dr. Bruce Altevogt, Dr. Michael Bennett, Dr. Kleopas Kleopa, Dr. Michael Koval, Dr. Daniela Menichella, Dr. David Paul, and Dr. Sabrina Yum for their many informative discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jennifer L. Orthmann-Murphy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Orthmann-Murphy, J.L., Abrams, C.K. & Scherer, S.S. Gap Junctions Couple Astrocytes and Oligodendrocytes. J Mol Neurosci 35, 101–116 (2008). https://doi.org/10.1007/s12031-007-9027-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12031-007-9027-5

Keywords

Navigation