Cx32 and Cx47 mediate oligodendrocyte:astrocyte and oligodendrocyte:oligodendrocyte gap junction coupling

Neurobiology of Disease

Volumn 42, Issue 3, 2011, Pages 506-513

  Wasseff, Sameh K ^a   Scherer, Steven S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Astrocyte; Connexins; Gap junctions; Oligodendrocyte

Indexed keywords

CONNEXIN 32; CONNEXIN 47;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CELL INTERACTION; CONTROLLED STUDY; CORPUS CALLOSUM; GAP JUNCTION; MOUSE; NEOCORTEX; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL;

ANIMALS; ASTROCYTES; CELL COMMUNICATION; CONNEXINS; CORPUS CALLOSUM; FLUORESCENT DYES; GAP JUNCTIONS; MICE; MICROSCOPY, ELECTRON; NEOCORTEX; OLIGODENDROGLIA;

EID: 79954633706     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.03.003     Document Type: Article

References (67)

1. Ahn M., Lee J., Gustafsson A., Enriquez A., Lancaster E., Sul J.Y., Haydon P.G., Paul D.L., Huang Y., Abrams C.K., Scherer S.S. Cx29 and Cx32, two connexins expressed by myelinating glia, do not interact and are functionally distinct. J. Neurosci. Res. 2008, 86:992-1006.
2. Akimoto C., Morita M., Yamamoto M., Nakano I. A novel mutation in X-linked Charcot-Marie-tooth (CMTXI) disease associated with central conduction slowing on brainstem auditory evoked potential (BAEP). Rinsho Shinkeigaku 2010, 50:399-403.
3. Altevogt B.M., Paul D.L. Four classes of intercellular channels between glial cells in the CNS. J. Neurosci. 2004, 24:4313-4323.
4. Altevogt B.M., Paul D.L. Four classes of intercellular channels between glial cells in the CNS. J. Neurosci. 2004, 24:4313-4323.
5. Altevogt B.M., Kleopa K.A., Postma F.R., Scherer S.S., Paul D.L. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J. Neurosci. 2002, 22:6458-6470.
6. Bahr M., Andres F., Timmerman V., Nelis M.E., Van Broeckhoven C., Dichgans J. Central visual, acoustic, and motor pathway involvement in a Charcot-Marie-Tooth family with an Asn205Ser mutation in the connexin 32 gene. J. Neurol. Neurosurg. Psychiatry 1999, 66:202-206.
7. Berger T., Schnitzer J., Kettenmann H. Developmental changes in the membrane current pattern, K+buffer capacity, and morphology of glial cells in the corpus callosum slice. J. Neurosci. 1991, 11:3008-3024.
8. Bugiani M., Al Shahwan S., Lamantea E., Bizzi A., Bakhsh E., Moroni I., Balestrini M.R., Uziel G., Zeviani M. GJA12 mutations in children with recessive hypomyelinating leukoencephalopathy. Neurology 2006, 67:273-279.
9. Butt A.M., Ransom B.R. Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. Glia 1989, 2:470-475.
10. Chvatal A., Anderova M., Ziak D., Sykova E. Glial depolarization evokes a larger potassium accumulation around oligodendrocytes than around astrocytes in gray matter of rat spinal cord slices. J. Neurosci. Res. 1999, 56:493-505.
11. Emsley J.G., Macklis J.D. Astroglial heterogeneity closely reflects the neuronal-defined anatomy of the adult murine CNS. Neuron Glia Biol. 2006, 2:175-186.
12. Filippov M.A., Hormuzdi S.G., Fuchs E.C., Monyer H. A reporter allele for investigating connexin 26 gene expression in the mouse brain. Eur. J. Neurosci. 2003, 18:3183-3192.
13. Frankenhaeuser B., Hodgkin A.L. The after-effects of impulses in the giant nerve fibres of Loligo. J. Physiol. 1956, 131:341-376.
14. Haas B., Schipke C.G., Peters O., Sohl G., Willecke K., Kettenmann H. Activity-dependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb. Cortex 2006, 16:237-246.
15. Houades V., Rouach N., Ezan P., Kirchhoff F., Koulakoff A., Giaume C. Shapes of astrocyte networks in the juvenile brain. Neuron Glia Biol. 2006, 2:3-14.
16. Houades V., Koulakoff A., Ezan P., Seif I., Giaume C. Gap junction-mediated astrocytic networks in the mouse barrel cortex. J. Neurosci. 2008, 28:5207-5217.
17. Imamoto K., Paterson J.A., Leblond C.P. Radioautographic investigation of gliogenesis in the corpus callosum of young rats. I. Sequential changes in oligodendrocytes. J. Comp. Neurol. 1978, 180(115-28):132-137.
18. Kafitz K.W., Meier S.D., Stephan J., Rose C.R. Developmental profile and properties of sulforhodamine 101-labeled glial cells in acute brain slices of rat hippocampus. J. Neurosci. Methods 2008, 169:84-92.
19. Kamasawa N., Sik A., Morita M., Yasumura T., Davidson K.G., Nagy J.I., Rash J.E. 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 2005, 136:65-86.
20. Kleopa K.A., Scherer S.S. Molecular genetics of X-linked Charcot-Marie-Tooth disease. Neuromolecular Med. 2006, 8:107-122.
21. Kleopa K.A., Yum S.W., Scherer S.S. Cellular mechanisms of connexin32 mutations associated with CNS manifestations. J. Neurosci. Res. 2002, 68:522-534.
22. Kleopa K.A., Orthmann J.L., Enriquez A., Paul D.L., Scherer S.S. Unique distributions of the gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia 2004, 47:346-357.
23. Kleopa K.A., Zamba-Papanicolaou E., Alevra X., Nicolaou P., Georgiou D.M., Hadjisavvas A., Kyriakides T., Christodoulou K. Phenotypic and cellular expression of two novel connexin32 mutations causing CMT1X. Neurology 2006, 66:396-402.
24. Kumar N.M., Gilula N.B. The gap junction communication channel. Cell 1996, 84:381-388.
25. Li J., Hertzberg E.L., Nagy J.I. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J. Comp. Neurol. 1997, 379:571-591.
26. Li X., Ionescu A.V., Lynn B.D., Lu S., Kamasawa N., Morita M., Davidson K.G., Yasumura T., Rash J.E., Nagy J.I. Connexin47, connexin29 and connexin32 co-expression in oligodendrocytes and Cx47 association with zonula occludens-1 (ZO-1) in mouse brain. Neuroscience 2004, 126:611-630.
27. Li X., Penes M., Odermatt B., Willecke K., Nagy J.I. Ablation of Cx47 in transgenic mice leads to the loss of MUPP1, ZONAB and multiple connexins at oligodendrocyte-astrocyte gap junctions. Eur. J. Neurosci. 2008, 28:1503-1517.
28. Maglione M., Tress O., Haas B., Karram K., Trotter J., Willecke K., Kettenmann H. Oligodendrocytes in mouse corpus callosum are coupled via gap junction channels formed by connexin47 and connexin32. Glia 2010, 58:1104-1117.
29. Magnotti L.M., Goodenough D.A., Paul D.L. Functional heterotypic interactions between astrocyte and oligodendrocyte connexins. Glia 2011, 59:26-34.
30. Massa P.T., Mugnaini E. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 1982, 7:523-538.
31. Matyash V., Kettenmann H. Heterogeneity in astrocyte morphology and physiology. Brain Res. Rev. 2010, 63:2-10.
32. Menichella D.M., Goodenough D.A., Sirkowski E., Scherer S.S., Paul D.L. Connexins are critical for normal myelination in the CNS. J. Neurosci. 2003, 23:5963-5973.
33. Menichella D.M., Majdan M., Awatramani R., Goodenough D.A., Sirkowski E., Scherer S.S., Paul D.L. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J. Neurosci. 2006, 26:10984-10991.
34. Mugnaini E. Astrocytes 1986, 329-371. Academic Press, Orlanodo Florida. S. Fedoroff, A. Vernadakis (Eds.).
35. Nagy J.I., Rash J.E. Astrocyte and oligodendrocyte connexins of the glial syncytium in relation to astrocyte anatomical domains and spatial buffering. Cell Commun. Adhes. 2003, 10:401-406.
36. Nagy J.I., Ionescu A.V., Lynn B.D., Rash J.E. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: implications from normal and connexin32 knockout mice. Glia 2003, 44:205-218.
37. Nagy J.I., Ionescu A.V., Lynn B.D., Rash J.E. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: implications from normal and connexin32 knockout mice. Glia 2003, 44:205-218.
38. Nelles E., Butzler C., Jung D., Temme A., Gabriel H.D., Dahl U., Traub O., Stumpel F., Jungermann K., Zielasek J., Toyka K.V., Dermietzel R., Willecke K. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA 1996, 93:9565-9570.
39. Nicholson G., Corbett A. Slowing of central conduction in X-linked Charcot-Marie-Tooth neuropathy shown by brain stem auditory evoked responses. J. Neurol. Neurosurg. Psychiatry 1996, 61:43-46.
40. Nicholson G.A., Yeung L., Corbett A. Efficient neurophysiologic selection of X-linked Charcot-Marie-Tooth families: ten novel mutations. Neurology 1998, 51:1412-1416.
41. Nimmerjahn A., Kirchhoff F., Kerr J.N., Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 2004, 1:31-37.
42. Odermatt B., Wellershaus K., Wallraff A., Seifert G., Degen J., Euwens C., Fuss B., Bussow H., Schilling K., Steinhauser C., Willecke K. 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. J. Neurosci. 2003, 23:4549-4559.
43. Oh S., Rubin J.B., Bennett M.V., Verselis V.K., Bargiello T.A. Molecular determinants of electrical rectification of single channel conductance in gap junctions formed by connexins 26 and 32. J. Gen. Physiol. 1999, 114:339-364.
44. Orkand R.K., Nicholls J.G., Kuffler S.W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 1966, 29:788-806.
45. Orthmann-Murphy J.L., Enriquez A.D., Abrams C.K., Scherer S.S. Loss-of-function GJA12/Connexin47 mutations cause Pelizaeus-Merzbacher-like disease. Mol. Cell. Neurosci. 2007, 34:629-641.
46. Orthmann-Murphy J.L., Freidin M., Fischer E., Scherer S.S., Abrams C.K. Two distinct heterotypic channels mediate gap junction coupling between astrocyte and oligodendrocyte connexins. J. Neurosci. 2007, 27:13949-13957.
47. Orthmann-Murphy J.L., Abrams C.K., Scherer S.S. Gap junctions couple astrocytes and oligodendrocytes. J. Mol. Neurosci. 2008, 35:101-116.
48. Panas M., Kalfakis N., Karadimas C., Vassilopoulos D. Episodes of generalized weakness in two sibs with the C164T mutation of the connexin 32 gene. Neurology 2001, 57:1906-1908.
49. Pastor A., Kremer M., Moller T., Kettenmann H., Dermietzel R. Dye coupling between spinal cord oligodendrocytes: differences in coupling efficiency between gray and white matter. Glia 1998, 24:108-120.
50. Paulson H.L., Garbern J.Y., Hoban T.F., Krajewski K.M., Lewis R.A., Fischbeck K.H., Grossman R.I., Lenkinski R., Kamholz J.A., Shy M.E. Transient central nervous system white matter abnormality in X-linked Charcot-Marie-Tooth disease. Ann. Neurol. 2002, 52:429-434.
51. Peters A., Palay S., Webster H. Fine Structure of the Nervous System: Neurons and Their Supporting Cells 1991, Oxford University Press, NewYork, NY.
52. Ransom B.R., Kettenmann H. Electrical coupling, without dye coupling, between mammalian astrocytes and oligodendrocytes in cell culture. Glia 1990, 3:258-266.
53. Rash J.E., Duffy H.S., Dudek F.E., Bilhartz B.L., Whalen L.R., Yasumura T. 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. J. Comp. Neurol. 1997, 388:265-292.
54. Rash J.E., Yasumura T., Davidson K.G., Furman C.S., Dudek F.E., Nagy J.I. Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord. Cell Commun. Adhes. 2001, 8:315-320.
55. Rash J.E., Yasumura T., Dudek F.E., Nagy J.I. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci. 2001, 21:1983-2000.
56. Rouach N., Koulakoff A., Abudara V., Willecke K., Giaume C. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 2008, 322:1551-1555.
57. Sandri C., Van Buren J.M., Akert K. Membrane morphology of the vertebrate nervous system. Prog. Brain Res. 1982, 46:201-265.
58. Siskind C., Feely S.M., Bernes S., Shy M.E., Garbern J.Y. Persistent CNS dysfunction in a boy with CMT1X. J. Neurol. Sci. 2009, 279:109-113.
59. Sohl G., Willecke K. Gap junctions and the connexin protein family. Cardiovasc. Res. 2004, 62:228-232.
60. Sohl G., Eiberger J., Jung Y.T., Kozak C.A., Willecke K. The mouse gap junction gene connexin29 is highly expressed in sciatic nerve and regulated during brain development. Biol. Chem. 2001, 382:973-978.
61. Sotelo C., Angaut P. The fine structure of the cerebellar central nuclei in the cat. I. Neurons and neuroglial cells. Exp. Brain Res. 1973, 16:410-430.
62. Takashima H., Nakagawa M., Umehara F., Hirata K., Suehara M., Mayumi H., Yoshishige K., Matsuyama W., Saito M., Jonosono M., Arimura K., Osame M. Gap junction protein beta 1 (GJB1) mutations and central nervous system symptoms in X-linked Charcot-Marie-Tooth disease. Acta Neurol. Scand. 2003, 107:31-37.
63. Taylor R.A., Simon E.M., Marks H.G., Scherer S.S. The CNS phenotype of X-linked Charcot-Marie-Tooth disease: more than a peripheral problem. Neurology 2003, 61:1475-1478.
64. Uhlenberg B., Schuelke M., Ruschendorf F., Ruf N., Kaindl A.M., Henneke M., Thiele H., Stoltenburg-Didinger G., Aksu F., Topaloglu H., Nurnberg P., Hubner C., Weschke B., Gartner J. Mutations in the gene encoding gap junction protein alpha 12 (connexin 46.6) cause Pelizaeus-Merzbacher-like disease. Am. J. Hum. Genet. 2004, 75:251-260.
65. Wallraff A., Kohling R., Heinemann U., Theis M., Willecke K., Steinhauser C. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J. Neurosci. 2006, 26:5438-5447.
66. Yum S.W., Zhang J., Valiunas V., Kanaporis G., Brink P.R., White T.W., Scherer S.S. Human connexin26 and connexin30 form functional heteromeric and heterotypic channels. Am. J. Physiol. Cell Physiol. 2007, 293:C1032-C1048.
67. Zambelis T., Panas M., Kokotis P., Karadima G., Kararizou E., Karandreas N. Central motor and sensory pathway involvement in an X-linked Charcot-Marie-Tooth family. Acta Neurol. Belg. 2008, 108:44-47.