Panglial gap junctional communication is essential for maintenance of myelin in the CNS

Journal of Neuroscience

Volumn 32, Issue 22, 2012, Pages 7499-7518

  Tress, Oliver ^a   Maglione, Marta ^b   May, Dennis ^a   Pivneva, Tatjyana ^c   Richter, Nadine ^b   Seyfarth, Julia ^b   Binder, Sonja ^d   Zlomuzica, Armin ^d   Seifert, Gerald ^e   Theis, Martin ^e   Dere, Ekrem ^d   Kettenmann, Helmut ^b   Willecke, Klaus ^a  

^a UNIVERSITY OF BONN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 30; CONNEXIN 32; CONNEXIN 47; GLIAL FIBRILLARY ACIDIC PROTEIN; MYELIN; MYELIN BASIC PROTEIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; CELL VACUOLE; CEREBELLUM; CONTROLLED STUDY; CORPUS CALLOSUM; DEATH; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; GAP JUNCTION; GRAY MATTER; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MICROGLIA; MOTOR COORDINATION; MOTOR DYSFUNCTION; MOUSE; MYELIN SHEATH; NERVE CELL NETWORK; NONHUMAN; OLIGODENDROGLIA; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAROD TEST; WHITE MATTER;

2',3'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASES; ACTINS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOPHYSICS; CENTRAL NERVOUS SYSTEM; CONNEXINS; ELECTRIC STIMULATION; EXPLORATORY BEHAVIOR; GAP JUNCTIONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; HABITUATION, PSYCHOPHYSIOLOGIC; KAPLAN-MEIER ESTIMATE; MAZE LEARNING; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MOTOR ACTIVITY; MYELIN SHEATH; NERVE TISSUE PROTEINS; NEUROGLIA; OLIGODENDROGLIA; PATCH-CLAMP TECHNIQUES; PSYCHOMOTOR PERFORMANCE; RECOGNITION (PSYCHOLOGY); RNA, MESSENGER; SILVER STAINING; STATISTICS, NONPARAMETRIC;

EID: 84861595502     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0392-12.2012     Document Type: Article

References (36)

1. Ahn M, Lee J, Gustafsson A, Enriquez A, Lancaster E, Sul JY, Haydon PG, Paul DL, Huang Y, Abrams CK, Scherer SS (2008) Cx29 and Cx32, two con-nexins expressed by myelinating glia, do not interact and are functionally distinct. J Neurosci Res 86:992-1006.
2. Altevogt BM, Paul DL (2004) Four classes of intercellular channels between glial cells in the CNS. J Neurosci 24:4313-4323.
3. Crawley JN (2008) Behavioral phenotyping strategies for mutant mice. Neuron 57:809-818.
4. de Leonibus E, Pascucci T, Lopez S, Oliverio A, Amalric M, Mele A (2007) Spatial deficits in a mouse model of Parkinson disease. Psychopharma-cology (Berl) 194:517-525.
5. Frantseva MV, Kokarovtseva L, Naus CG, Carlen PL, MacFabe D, Perez Velazquez JL (2002) Specific gap junctions enhance the neuronal vulnerability to brain traumatic injury. J Neurosci 22:644-653.
6. Giaume C, Theis M (2010) Pharmacological and genetic approaches to study connexin-mediated channels in glial cells of the central nervous system. Brain Res Rev 63:160-176.
7. Haas S, Brockhaus J, Verkhratsky A, Kettenmann H (1996) ATP-induced membrane currents in ameboid microglia acutely isolated from mouse brain slices. Neuroscience 75:257-261.
8. Kamasawa N, Sik A, Morita M, Yasumura T, Davidson KG, Nagy JI, Rash JE (2005) Connexin-47 and connexin-32 in gap junctions of oligodendro-cyte somata, myelin sheaths, paranodal loops and Schmidt-Lanterman incisures: implications for ionic homeostasis and potassium siphoning. Neuroscience 136:65-86.
9. Kleopa KA, Scherer SS (2006) Molecular genetics of X-linked Charcot-Marie-Tooth disease. Neuromolecular Med 8:107-122.
10. Kleopa KA, Orthmann JL, Enriquez A, Paul DL, Scherer SS (2004) Unique distributions of the gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia 47:346-357.
11. Li WE, Nagy JI (2000) Connexin43 phosphorylation state and intercellular communication in cultured astrocytes following hypoxia and protein phosphatase inhibition. Eur J Neurosci 12:2644-2650.
12. Lutz SE, Zhao Y, Gulinello M, Lee SC, Raine CS, Brosnan CF (2009) Dele-tionofastrocyte connexins43and30leadstoa dysmyelinating phenotype and hippocampal CA1 vacuolation. J Neurosci 29:7743-7752.
13. Maglione M, Tress O, Haas B, Karram K, Trotter J, Willecke K, Kettenmann H (2010) Oligodendrocytes in mouse corpus callosum are coupled via gap junction channels formed by connexin47 and connexin32. Glia 58:1104-1117.
14. Magnotti LM, Goodenough DA, Paul DL (2011a) Functional heterotypic interactions between astrocyte and oligodendrocyte connexins. Glia 59:26-34.
15. Magnotti LM, Goodenough DA, Paul DL (2011b) Deletion of oligodendro-cyte Cx32 and astrocyte Cx43 causes white matter vacuolation, astrocyte loss and early mortality. Glia 59:1064-1074.
16. Menichella DM, Goodenough DA, Sirkowski E, Scherer SS, Paul DL (2003) Connexins are critical for normal myelination in the CNS. J Neurosci 23:5963-5973.
17. Menichella DM, Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS, Paul DL (2006) Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci 26:10984-10991.
18. Nagy JI, Li X, Rempel J, Stelmack G, Patel D, Staines WA, Yasumura T, Rash JE (2001) Connexin26 in adult rodent central nervous system: demonstration at astrocytic gap junctions and co localization with connexin30 and connexin43. J Comp Neurol 441:302-323.
19. Nagy JI, Ionescu AV, Lynn BD, Rash JE (2003) Coupling of astrocyte con-nexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: implications from normal and connexin32 knockout mice. Glia 44:205-218.
20. Nagy JI, Lynn BD, Tress O, Willecke K, Rash JE (2011) Connexin26 expression in brain parenchymal cells demonstrated by targeted connexin ablation in transgenic mice. Eur J Neurosci 34:263-271.
21. Norenberg MD, Leslie KO, Robertson AS (1982) Association between rise in serum sodium and central pontine myelinolysis. Ann Neurol 11:128-135.
22. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Büssow H, Schilling K, Steinhäuser C, Willecke K (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. J Neurosci 23:4549-4559.
23. Orthmann-Murphy JL, Freidin M, Fischer E, Scherer SS, Abrams CK (2007) Two distinct heterotypic channels mediate gap junction coupling between astrocyte and oligodendrocyte connexins. J Neurosci 27:13949-13957.
24. Rash JE (2010) Molecular disruptions of the panglial syncytium block potassium siphoning and axonal saltatory conduction: pertinence to neuro-myelitis optica and other demyelinating diseases of the central nervous system. Neuroscience 168:982-1008.
25. Rash JE, Davidson KG, Kamasawa N, Yasumura T, Kamasawa M, Zhang C, Michaels R, Restrepo D, Ottersen OP, Olson CO, Nagy JI (2005) Ultra-structural localization of connexins (Cx36, Cx43, Cx45), glutamate receptors and aquaporin-4 in rodent olfactory mucosa, olfactory nerve and olfactory bulb. J Neurocytol 34:307-341.
26. Requardt RP, Kaczmarczyk L, Dublin P, Wallraff-Beck A, Mikeska T, Degen J, Waha A, Steinhäuser C, Willecke K, Theis M (2009) Quality control of astrocyte directed Cre transgenic mice: the benefits of a direct link between loss of gene expression and reporter activation. Glia 57:680-692.
27. Sadile AG, Pellicano MP, Sagvolden T, Sergeant JA (1996) NMDA and non-NMDA sensitive [L-3H]glutamate receptor binding in the brain of the Naples high- and low-excitability rats: an autoradiographic study. Behav Brain Res 78:163-174.
28. Sargiannidou I, Vavlitou N, Aristodemou S, Hadjisavvas A, Kyriacou K, Scherer SS, Kleopa KA (2009) Connexin32 mutations cause loss of function in Schwann cells and oligodendrocytes leading to PNS and CNS myelination defects. J Neurosci 29:4736-4749.
29. Schmued L, Bowyer J, Cozart M, Heard D, Binienda Z, Paule M (2008) Introducing Black-Gold II, a highly soluble gold phosphate complex with several unique advantages for the histo chemical localization of myelin. Brain Res 1229:210-217.
30. Takefuji S, Murase T, Sugimura Y, Takagishi Y, Hayasaka S, Oiso Y, Murata Y (2007) Role of microglia in the pathogenesis of osmotic-induced demyelination. Exp Neurol 204:88-94.
31. Teubner B, Michel V, Pesch J, Lautermann J, Cohen-Salmon M, Söhl G, Jahnke K, Winterhager E, Herberhold C, Hardelin JP, Petit C, Willecke K (2003) Connexin30 (Gjb6)-deficiency causes severe hearing impairment and lack of endocochlear potential. Hum Mol Genet 12:13-21.
32. Tress O, Maglione M, Zlomuzica A, May D, Dicke N, Degen J, Dere E, Ketten-mann H, Hartmann D, Willecke K (2011) Pathologic and phenotypic alterations in a mouse expressing a connexin 47 missense mutation that causes pelizaeus-merzbacher-like disease in humans. PLoS Genet 7:e1002146.
33. Uhlenberg B, Schuelke M, Rüschendorf F, Ruf N, Kaindl AM, Henneke M, Thiele H, Stoltenburg-Didinger G, Aksu F, Topaloǧlu H, Nürnberg P, Hübner C, Weschke B, Gärtner J (2004) Mutations in the gene encoding gap junction protein alpha 12 (connexin 46.6) cause Pelizaeus-Merzbacher-like disease. Am J Hum Genet 75:251-260.
34. Wallraff A, Köhling R, Heinemann U, Theis M, Willecke K, Steinhäuser C (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26:5438-5447.
35. Wasseff SK, Scherer SS (2011) Cx32 and Cx47 mediate oligodendrocyte: astrocyte and oligodendrocyte:oligodendrocyte gap junction coupling. Neurobiol Dis 42:506-513.
36. Zeinieh MP, Talhouk RS, El-Sabban ME, Mikati MA (2010) Differential expression of hippocampal connexins after acute hypoxia in the developing brain. Brain Dev 32:810-817.