Brain connexins in demyelinating diseases: Therapeutic potential of glial targets

Brain Research

Volumn 1487, Issue , 2012, Pages 61-68

  Cotrina, Maria Luisa ^a   Nedergaard, Maiken ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Astrocyte; Gap junction; Glucose; Myelin; Oligodendrocyte; Potassium

Indexed keywords

AQUAPORIN 4; GAMMA INTERFERON; GAP JUNCTION PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INITIATION FACTOR 2; INTERLEUKIN 17; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MYELIN; POTASSIUM; POTASSIUM CHANNEL; TRANSCRIPTION FACTOR SOX10;

ALEXANDER DISEASE; ASTROCYTE; CELL ADHESION; CELL JUNCTION; DEMYELINATING DISEASE; GENE MUTATION; GLIA; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; INTRACELLULAR SIGNALING; LEUKODYSTROPHY; MOLECULARLY TARGETED THERAPY; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PELIZAEUS MERZBACHER DISEASE; PRIORITY JOURNAL; REVIEW; SCHWANN CELL; SPASTIC PARAPLEGIA; TH1 CELL;

ANIMALS; AQUAPORIN 4; ASTROCYTES; BRAIN CHEMISTRY; CELL ADHESION; CONNEXINS; DEMYELINATING DISEASES; HUMANS; MICE; NEUROGLIA; OLIGODENDROGLIA; POTASSIUM;

MUS MUSCULUS;

EID: 84869505523     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.07.003     Document Type: Review

References (58)

1. M. Ahn, J. Lee, A. Gustafsson, A. Enriquez, E. Lancaster, J.Y. Sul, P.G. Haydon, D.L. Paul, Y. Huang, C.K. Abrams, and S.S. Scherer Cx29 and Cx32, two connexins expressed in myelinating glia, do not interact and are functionally distinct J. Neurosci. Res. 86 2008 992 1006 (Pubitemid 351441297)
2. I. Allaman, M. Bélanger, and P.J. Magistretti Astrocyte-neuron metabolic relationships: for better and for worse Trends Neurosci. 34 2011 76 87
3. M. Brenner, J.E. Goldman, R.A. Quinlan, and A. Messing Alexander disease: A genetic disorder of astrocytes V. Parpura, P. Haydon, Astrocytes in (patho)physiology of the nervous system 2009 Springer 591 648
4. R. Bruzzone, T.W. White, and D.L. Paul Connections with connexins: the molecular basis of direct intercellular signaling Eur. J. Biochem. 238 1996 1 27 (Pubitemid 26164180)
5. M. Bugiani, I. Boor, J.M. Powers, G.C. Scheper, and M.S. Van Der Knaap Leukoencephalopathy with Vanishing White Matter: A review J. Neuropathol. Exp. Neurol. 69 2010 987 996
6. M.L. Cotrina, J.H.C. Lin, and M. Nedergaard Adhesive properties of connexin hemichannels Glia 56 2008 1791 1798
7. E. Dere, M.A. De Souza-Silva, C. Frisch, B. Teubner, G. Söhl, K. Willecke, and J.P. Huston Connexin30-deficient mice show increased emotionality and decreased rearing activity in the open-field along with neurochemical changes Eur. J. Neurosci. 18 2003 629 638 (Pubitemid 37041111)
8. J. Dietrich, M. Lacagnina, D. Gass, E. Richfield, M. Mayer-Pröschel, M. Noble, C. Torres, and C. Pröschel EIF2B5 mutations compromise GFAP+ astrocyte generatin in vanishing white matter leukodystrophy Nat. Med. 11 2005 277 283 (Pubitemid 40460555)
9. A. Duarri, M. López de Heredia, X. Capdevila-Nortes, M.C. Ridder, M. Montolio, T. López-Hernández, I. Boor, C. Lien, T. Hagermann, A. Messing, D.C. Gorecki, G.C. Scheper, A. Martínez, V. Nunes, M.S. Van Der Knaap, and R. Estévez Knockdown of MLC1 in primary astrocytes causes cell vacuolation: A MLC disease cell model Neurobiol. Dis. 43 2011 228 238
10. I.D. Duncan, Y. Kondo, and S.-C. Zhang The myelin mutants as models to study myelin repair in the leukodystrophies Neurotherapeutics 8 2011 607 624
11. F. Gankam, C. Nicaise, A. Soupart, A. Boom, J. Schiettecatte, R. Pochet, J.P. Brion, and G. Decaux Astrocytes are an early target in osmotic demyelination syndrome J. Am. Soc. Nephrol. 22 2011 1834 1845
12. S.R. Hinson, S.F. Roemer, C.F. Lucchinetti, J.P. Fryer, T.J. Kryzer, J.L. Chamberlain, C.L. Howe, S.J. Pittock, and V.A. Lennon Aquaporin-4-binding autoantibodies in patients with neuromyelitis optica impair glutamate transport by down-regulating EAAT2 J. Exp. Med. 205 2008 2473 2481
13. S.R. Hinson, A. Mckeon, and V.A. Lennon Neurological autoimmunity targeting aquaporin-4 Neuroscience 168 2010 1009 1018
14. B. Huang, and W. He Molecular characteristics of inherited congenital cataracts Eur. J. Med. Gen. 53 2010 347 357
15. C. Huang, X. Han, X. Li, E. Lam, W. Peng, N. Lou, A. Torres, M. Yang, J.M. Garre, G.-F. Tian, M.V.L. Bennett, M. Nedergaard, and T. Takano Critical role of Connexin 43 in secondary expansion of traumatic spinal cord injury J. Neurosci. 32 2012 3333 3338
16. E. Jeworutzki, T. López-Hernández, X. Capdevila-Nortes, S. Sirisi, L. Bengtsson, M. Montolio, G. Zifarelli, T. Amedo, C. Müller, U. Schulte, V. Nunes, A. Martínez, T.J. Jentsch, X. Gasull, M. Pusch, and R. Estévez GlialCAM, a protein defective in a leukodystrophy, serves as a CIC-2 Cl- channel auxiliary subunit Neuron 73 2012 951 961
17. N. Kamasawa, A. Sik, M. Morita, T. Yasumura, K.G.V. Davidson, J.I. Nagy, and J.E. Rash 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 2005 65 86 (Pubitemid 41483836)
18. J. Kira Autoimmunity in neuromyelitis optica and opticospinal multiple sclerosis: Astrocytopathy as a common denominator in demyelinating disorders J. Neurol. Sci. 311 2011 69 77
19. K.A. Kleopa The role of gap junctions in Charcot-Marie-Tooth Disease J. Neurosci. 31 2011 17753 17760
20. P.A. Leegwater, B.Q. Yuan, J. Van Der Steen, J. Mulders, A.A. Könst, P.K. Boor, V. Mejaski-Bosnjak, S.M. Van Der Maarel, R.R. Frants, C.B. Oudejans, R.B. Schutgens, J.C. Pronk, and M.S. Van Der Knaap Mutations of MLC1 (KIAA0027), encoding a putative membrane protein, cause megalencephalic leukoencephalopathy with subcortical cysts Am. J. Hum. Genet. 68 2001 831 838 (Pubitemid 32289728)
21. V.A. Lennon, D.M. Wingerchuk, T.J. Kryzer, S.J. Pittock, C.F. Lucchinetti, K. Fujihara, I. Nakashima, and B.G. Weinshenker A serum auto-antibody marker of neuromyelitis optica: distinction from multiple sclerosis Lancet 364 2004 2106 2112 (Pubitemid 39626806)
22. X. Li, A.V. Ionescu, B.D. Lynn, S. Lu, N. Kamasawa, M. Morita, K.G. Davidson, T. Yasumura, J.E. Rash, and J.I. Nagy Connexin47, connexin29 and connexin32 coexpression in oligodendrocytes and Cx47 association with zonula occludens-1 (ZO-1) in mouse brain Neuroscience 7 2004 523 538
23. X. Li, M. Penes, B. Odermatt, K. Willecke, and J.I. Nagy Ablation of Cx47 in transgenic mice leads to the loss of MUPP1, ZONAB and multiple connexins at oligodendrocyte-astrocyte gap junctions Eur. J. Neurosci. 28 2008 1503 1517
24. J.H.C. Lin, T. Takano, M.L. Cotrina, G. Arcuino, J. Kang, S. Liu, Q. Gao, L. Jiang, H. Lichtenberg-Frate, S. Hsubrich, K. Willecke, S.A. Goldman, and M. Nedergaard Connexin 43 enhances de adhesivity and mediates the invasion of malignant glioma cells J. Neurosci. 22 2002 4302 4311 (Pubitemid 37465645)
25. J. Liu, J. Xu, S. Gu, B.J. Nicholson, and J.X. Jiang Aquaporin 0 enhances gap junction coupling via its cell adhesion function and interaction with connexin 50 J. Cell Sci. 124 2011 198 206
26. T. López-Hernández, M.C. Ridder, M. Montolio, X. Capdevila-Nortes, E. Polder, S. Sirisi, A. Duarri, U. Schulte, B. Fakler, V. Nunes, G.C. Scheper, A. Martínez, R. Estévez, and M.S. Van Der Knaap Mutant GlialCAM causes megalencephalic leukoencephalopathy with subcortical cysts, benign familial macrocephaly, and macrocephaly with retardation and autism Am. J. Hum. Genet. 88 2011 422 432
27. S.E. Lutz, Y. Zhao, M. Gulinello, C.S. Lee, C.S. Raine, and C.F. Brosnan Deletion of astrocyte connexins 43 and 30 leads to a dysmyelinating phenotype and hippocampal CA1 vacuolation J. Neurosci. 29 2009 7743 7752
28. S.E. Lutz, C.S. Raine, and C.F. Brosnan Loss of astrocyte connexins 43 and 30 does not significantly alter susceptibility or severity of acute experimental autoimmune encephalomyelitis in mice J. Neuroimmunol. 245 2012 8 14
29. M. Maglione, O. Tress, B. Haas, K. Karram, J. Trotter, K. Willecke, and H. Kettenmann Oligodendrocytes in mouse corpus callosum are coupled via gap junction channels formed by connexin 47 and connexin 32 Glia 58 2010 1104 1117
30. L.M. Magnotti, D.A. Goodenough, and D.L. Paul Deletion of oligodendrocyte Cx32 and astrocyte Cx43 causes white matter vacuolation, astrocyte loss and early mortality Glia 59 2011 1064 1074
31. R. Marignier, A. Nicolle, C. Watrin, M. Touret, S. Cavagna, M. Varrin-Doyer, G. Cavillon, V. Rogemond, C. Confavreux, J. Honnorat, and P. Giraudon Oligodendrocytes are damaged by neuromyelitis optica immunoglobulin G via astrocyte injury Brain 133 2010 2578 2591
32. W. Meme, C. Calvo, N. Froger, P. Ezan, E. Amigou, A. Koulakoff, and C. Giaume Proinflammatory cytokines released from microglia inhibit gap junctions in astrocytes: potentiation by β-amyloid FASEB J. 20 2006 494 496 (Pubitemid 46671227)
33. D.M. Menichela, D.A. Goodenough, E. Sirkowski, S.S. Scherer, and D.L. Paul Connexins are critical for normal muelination in the CNS J. Neurosci. 23 2003 5963 5973 (Pubitemid 36807876)
34. J.I. Nagy, X. Li, J. Rempel, G. Stelmack, D. Patel, W.A. Staines, T. Yasumura, and J.E. Rash Connexin 26 in adult rodent central nervous system: demonstration of astrocytic gap junctions and colocalization with connexin30 and connexin 43 J. Comp. Neurol. 441 2001 302 323 (Pubitemid 33104407)
35. T. Nakase, G. Söhl, M. Theis, K. Willecke, and C.C. Naus Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin43 in astrocytes Am. J. Pathol. 164 2004 2067 2075 (Pubitemid 38669354)
36. K. Nave Myelination and support of axonal integrity by glia Nature 468 2010 244 252
37. M. Nedergaard, and A. Verkhratsky Artifact versus reality - how astrocytes contribute to synaptic events Glia 60 2012 1013 1023
38. E. Nelles, C. Butzler, D. Jung, A. Temme, H.-D. Gabriel, U. Dahl, O. Traub, F. Stumpel, K. Jungermann, J. Zielasek, K.V. Toyka, R. Dermietzel, and K. Willecke Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice Proc. Natl. Acad. Sci. USA 93 1996 9565 9670
39. G.P. Nicchia, M. Srinivas, W. Li, C.F. Brosnan, A. Frigeri, and D.C. Spray New possible roles for aquaporin-4 in astrocytes: cell cytoskeleton and functional relationship with connexin43 FASEB J. 19 2005 1674 1686
40. N.A. Oberheim, T. Takano, X. Han, W. He, J.H.C. Lin, F. Wang, Q. Xu, J.D. Wyatt, W. Pilcher, J.G. Ojemann, B.R. Ransom, S.A. Goldman, and M. Nedergaard Uniquely hominid features of adult human astrocytes J. Neurosci. 29 2009 3276 3287
41. S.J. O'Carroll, M. Alkadhi, L.F.B. Nicholson, and C.R. Green A Cx43 mimetic peptide reduces swelling, astrogliosis and neuronal cell death after spinal cord injury Cell Comm. Adhes. 15 2008 27 42
42. B. Odermatt, K. Wellershaus, A. Wallraff, G. Seifert, J. Degen, C. Euwens, B. Fuss, H. Büssow, C. Steinhäuser, and K. Willecke 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 2003 4549 4559 (Pubitemid 36706185)
43. H. Osaka, H. Hamanoue, R. Yamamoto, A. Nezu, M. Sasaki, H. Saitsu, K. Kurosawa, H. Shimbo, N. Matsumoto, and K. Inoue Disrupted SOX10 regulation on GJC2 transcription causes Pelizaeus-Merzbacher-Like disease Ann. Neurol. 68 2010 250 254
44. U. Pannasch, L. Vargová, J. Reingruber, P. Ezan, D. Holcman, C. Giaume, E. Syková, and N. Rouach Astroglial networks scale synaptic activity and plasticity Proc. Natl. Acad. Sci. USA 108 2011 8467 8472
45. V. Pingault, N. Bondurand, and K. Kuhlbrodt et al. 1998. SOX10 mutations in patients with Waardenburg-Hirschsprung disease Nat. Genet. 18 1998 171 173 (Pubitemid 28082467)
46. M.A. Retamal, N. Froger, N. Palacios-Prado, P. Ezan, P.J. Sáez, J.C. Sáez, and C. Giaume Cx43 Hemichannels and gap junction channels in astrocytes are regulated oppositely by proinflammatory cytokines released from activated microglia J. Neurosci. 27 2007 13781 13792 (Pubitemid 350278255)
47. N. Rouach, A. Koulakoff, V. Abudara, K. Willecke, and C. Giaume Astroglial metabolic networks sustain hippocampal synaptic transmission Science 322 2008 1551 1555
48. I. Sargiannidou, N. Vavlitou, S. Aristodemou, A. Hadjisavvas, K. Kyriacou, S.S. Scherer, and K.A. Kleopa Connexin 32 mutations cause loss of function in Schwann cells and oligodendrocytes leading to PNS and CNS myelination defects J. Neurosci. 29 2009 4736 4749
49. Y. Sawaishi Review of Alexander disease: beyond the classical concept of leukodystrophy Brain Dev. 31 2009 493 498
50. R. Sharma, M. Fisher, J. Bauer, P.A. Felts, K.J. Smith, T. Misu, K. Fujihara, M. Bradl, and H. Lassmann Inflammation induced by innate immunity in the central nervous system leads to primary astrocyte dysfunction followed by demyelination Acta Neuropat. 120 2010 223 236
51. D.L. Sherman, and P.J. Brophy Mechanisms of axon ensheathment and myelin growth Nat. Rev. Neurosci. 6 2005 683 690 (Pubitemid 43160317)
52. B. Uhlenberg, M. Schuelke, F. Rüschendorf, N. Ruf, A.M. Kaindl, M. Henneke, H. Thiele, G. Stoltenbug-Didinger, F. Aksu, H. Topaloglu, P. Nürnberg, C. Hübner, B. Weschke, and J. Gärtner Mutations in the gene encoding gap junction protein α12 (connexin 46.6) cause Pelizaeus-Merzbacher-Like disease Am. J. Hum. Genet. 75 2004 251 260 (Pubitemid 38943868)
53. M.S. Van Der Knaap, J. Valk, P.G. Barth, L.M. Smit, B.G. van Engelen, and P. Tortori Donati Leukoencephalopathy with swelling in children and adolescents: MRI patterns and differential diagnosis Neuroradiology 37 1995 679 686
54. M.S. Van Der Knaap, P.G. Barth, G.F. Vrensen, and J. Valk Histopathology of an infantile-onset spongiform leukoencephalopathy with a discrepantly mild clinical course Acta Neuropathol. 92 1996 206 212 (Pubitemid 26248465)
55. K. Van Haren, P. Van Der Voorn, D.R. Peterson, M.S. Van Der Knaap, and J.M. Powers The life and death of oligodendrocytes in Vanishing White Matter disease J. Neuropathol. Exp. Neurol. 63 2004 618 630 (Pubitemid 38736425)
56. A. Wallraff, R. Köhling, U. Heinemann, M. Theis, K. Willecke, and C. Steinhäuser The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus J. Neurosci. 26 2006 5438 5447 (Pubitemid 44318396)
57. S.G. Waxman Transcriptional channelopathies: An emerging class of disorders Nat. Rev. Neurosci. 2 2001 652 659 (Pubitemid 33675681)
58. Yu, X.S., Jiang, J.X. 2004. Interaction of major intrinsic protein (aquaporin-0) with fiber connexin