Human oligodendrocytes express Cx31.3: Function and interactions with Cx32 mutants

Neurobiology of Disease

Volumn 30, Issue 2, 2008, Pages 221-233

  Sargiannidou, Irene ^a   Ahn, Meejin ^b   Enriquez, Alan D ^b   Peinado, Alejandro ^c   Reynolds, Richard ^d   Abrams, Charles ^c   Scherer, Steven S ^b   Kleopa, Kleopas A ^a  

^a CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c SUNY DOWNSTATE MEDICAL CENTER   (United States)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

CMT1X; Connexin29; Gap junctions; Protein trafficking, Hemichannels

Indexed keywords

CX31 3 PROTEIN; CX32 PROTEIN; CX47 PROTEIN; GENE PRODUCT; GJ PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GRAY MATTER; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MUTANT; MYELINATED NERVE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RODENT;

AMINO ACID SEQUENCE; CELL COMMUNICATION; CONNEXINS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NERVE TISSUE PROTEINS; OLIGODENDROGLIA;

EID: 42649116417     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2008.01.009     Document Type: Article

References (49)

1. Abrams C., Freidin M., Bukauskas F., Dobrenis K., Bargiello T., Verselis V., Bennett M., Chen L., and Sahenk Z. Pathogenesis of X-linked Charcot-Marie-Tooth disease: differential effects of two mutations in connexin 32. J. Neurosci. 23 (2003) 10548-10558
2. Ahn M., Lee J., Gustafsson A., Enriquez A., Lancaster E., Sul J.-Y., Haydon P.G., Paul D.L., Huang Y., Abrams C.K., et al. Cx29 and Cx32, two connexins expressed by myelinating glia, do not interact and are functionally distinct. J. Neurosci. Res. (2007) Oct 30; [Electronic publication ahead of print]
3. Altevogt B.M., and Paul D.L. Four classes of intercellular channels between glial cells in the CNS. J. Neurosci. 24 (2004) 4313-4323
4. Altevogt B.M., Kleopa K.A., Postma F.R., Scherer S.S., and Paul D.L. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J. Neurosci. 22 (2002) 6458-6470
5. Bergoffen J., Scherer S.S., Wang S., Oronzi-Scott M., Bone L., Paul D.L., Chen K., Lensch M.W., Chance P., and Fischbeck K. Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science 262 (1993) 2039-2042
6. Butt A.M., Ibrahim M., and Berry M. Axon-myelin sheath relations of oligodendrocyte unit phenotypes in the adult rat anterior medullary velum. J. Neurocytol. 27 4 (1998) 259-269
7. Contreras J.E., Sáez J.C., Bukauskas F.F., and Bennett M.V. Gating and regulation of connexin 43 (Cx43) hemichannels. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 11388-11393
8. Cruciani V., and Mikalsen S.O. The vertebrate connexin family. Cell. Mol. Life Sci. 63 (2006) 1125-1140
9. Deschênes S.M., Walcott J.L., Wexler T.L., Scherer S.S., and Fischbeck K.H. Altered trafficking of mutant connexin32. J. Neurosci. 17 (1997) 9077-9084
10. Eastman S.D., Chen T.H., Falk M.M., Mendelson T.C., and Iovine M.K. Phylogenetic analysis of three complete gap junction gene families reveals lineage-specific duplications and highly supported gene classes. Genomics 87 (2006) 265-274
11. el-Fouly M.H., Trosko J.E., and Chang C.C. Scrape-loading and dye transfer. A rapid and simple technique to study gap junctional intercellular communication. Exp. Cell Res. 168 (1987) 422-430
12. González D., Gómez-Hernández J.M., and Barrio L.C. Species specificity of mammalian connexin-26 to form open voltage-gated hemichannels. FASEB J. 20 (2006) 2329-2338
13. Hahn A.F., Ainsworth P.J., Naus C.C.G., Mao J., and Bolton C.F. Clinical and pathological observations in men lacking the gap junction protein connexin 32. Muscle Nerve (2000) S39-S48
14. Hanemann C.O., Bergmann C., Senderek J., Zerres K., and Sperfeld A. Transient, recurrent, white matter lesions in X-linked Charcot-Marie-Tooth disease with novel connexin 32 mutation. Arch. Neurol. 60 (2003) 605-609
15. Iacobas D.A., Iacobas S., Urban-Maldonado M., and Spray D.C. Sensitivity of the brain transcriptome to connexin ablation. Biochim. Biophys. Acta 1711 (2005) 183-196
16. Jeng L.J., Balice-Gordon R.J., Messing A., Fischbeck K.H., and Scherer S.S. The effects of a dominant connexin32 mutant in myelinating Schwann cells. Mol. Cell. Neurosci. 32 (2006) 283-298
17. Kamasawa N., Sik A., Morita M., Yasumura T., Davidson K., Nagy J., and Rash J. 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
18. Kassubek J., Bretschneider V., and Sperfeld A.D. Corticospinal tract MRI hyperintensity in X-linked Charcot-Marie-Tooth Disease. J. Clin. Neurosci. 12 (2005) 588-589
19. Kleopa K.A., and Scherer S.S. Molecular genetics of X-linked Charcot-Marie-Tooth disease. Neuromolecular Med. 8 (2006) 107-122
20. Kleopa K.A., Yum S.W., and Scherer S.S. Cellular mechanisms of connexin32 mutations associated with CNS manifestations. J. Neurosci. Res. 68 (2002) 522-534
21. Kleopa K.A., Orthmann J.L., Enriquez A., Paul D.L., and Scherer S.S. Unique distribution of gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia 47 (2004) 346-357
22. Kleopa K.A., Zamba-Papanicolaou E., Alevra X., Nicolaou P., Georgiou D.M., Hadjisavvas A., Kyriakides T., and Christodoulou K. Phenotypic and cellular expression of two novel connexin32 mutations causing CMT1X. Neurology 66 (2006) 396-402
23. Li J., Hertzberg E.L., and Nagy J.I. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J. Comp. Neurol. 379 4 (1997) 571-591
24. Li X., Ionescu A.V., Lynn B.D., Lu S., Kamasawa N., Morita M., Davidson K.G.V., Yasumura T., Rash J.E., and Nagy J.I. Connexin47, connexin29 and connexin32 co-expression in oligodendrocytes and Cx47 association with zonula occludens-1 (ZO-1) in mouse brain. Neuroscience 126 (2004) 611-630
25. Madhavarao C.N., Arun P., Moffett J.R., Szucs S., Surendran S., Matalon R., Garbern J., Hristova D., Johnson A., Jiang W.a., et al. Defective N-acetylaspartate catabolism reduces brain acetate levels and myelin lipid synthesis in Canavan's disease. Proc. Nat. Acad. Sci. U. S. A. 102 (2005) 5221-5226
26. Menichella D.M., Goodenough D.A., Sirkowski E., Scherer S.S., and Paul D.L. Connexins are critical for normal myelination in the CNS. J. Neurosci. 23 (2003) 5963-5973
27. Menichella D.M., Majdan M., Awatramani R., Goodenough D.A., Sirkowski E., Scherer S.S., and Paul D.L. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J. Neurosci. 26 48 (2006) 10984-10991
28. Nagy J.I., Ionescu A.V., Lynn B.D., and Rash J.E. Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system. J. Comp. Neurol. 22 (2003) 356-370
29. Nagy J.I., Ionescu A.V., Lynn B.D., and Rash J.E. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: implications from normal and connexin32 knockout mice. Glia 44 (2003) 205-218
30. Odermatt B., Wellershaus K., Wallraff A., Seifert G., Degen J., Euwens C., Fuss B., Bussow H., Schilling K., Steinhauser C., et al. 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
31. Oh S., Ri Y., Bennett M.V.L., Trexler E.B., Verselis V.K., and Bargiello T.A. Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron 19 4 (1997) 927-938
32. Omori Y., Mesnil M., and Yamasaki H. Connexin 32 mutations from X-linked Charcot-Marie-Tooth disease patients: functional defects and dominant negative effects. Mol. Biol. Cell 7 6 (1996) 907-916
33. Orthmann-Murphy J.L., Enriquez A.D., Abrams C.K., and Scherer S.S. Loss-of-function connexin47 mutations cause Pelizaeus-Merzbacher-like disease. Mol. Cell. Neurosci. 34 (2007) 629-641
34. 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., and Shy M.E. Transient central nervous system white matter abnormality in X-linked Charcot-Marie-Tooth disease. Ann. Neurol. 52 (2002) 429-434
35. Rash J.E., Yasumura T., Dudek F.E., and Nagy J.I. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci. 21 6 (2001) 1983-2000
36. Remahl S., and Hildebrand C. Relation between axons and oligodendroglial cells during initial myelination. I. The glial unit. J. Neurocytol. 19 (1990) 313-328
37. Richard G., White T.W., Smith L.E., Bailey R.A., Compton J.G., Paul D.L., and Bale S.J. Functional defects of Cx26 resulting from a heterozygous missense mutation in a family with dominant deaf-mutism and palmoplantar keratoderma. Hum. Genet. 103 4 (1998) 393-399
38. Rouan F., White T., Brown N., Taylor A., Lucke T., Paul D., Munro C., Uitto J., Hodgins M., and Richard G. Trans-dominant inhibition of connexin-43 by mutant connexin-26: implications for dominant connexin disorders affecting epidermal differentiation. J. Cell Sci. 114 (2001) 2105-2113
39. Sáez J.C., Retamal M.A., Basilio D., Bukauskas F.F., and Bennett M.V. Connexin-based gap junction hemichannels: gating mechanisms. Biochim. Biophys. Acta 1711 (2005) 215-224
40. Scherer S.S., Deschênes S.M., Xu Y.-T., Grinspan J.B., Fischbeck K.H., and Paul D.L. Connexin32 is a myelin-related protein in the PNS and CNS. J. Neurosci. 15 (1995) 8281-8294
41. Scherer S.S., Xu Y.-T., Nelles E., Fischbeck K., Willecke K., and Bone L.J. Connexin32-null mice develop a demyelinating peripheral neuropathy. Glia 24 (1998) 8-20
42. Sohl G., Eiberger J., Jung Y.T., Kozak C.A., and Willecke K. The mouse gap junction gene connexin29 is highly expressed in sciatic nerve and regulated during brain development. Biol. Chem. 382 (2001) 973-978
43. Taylor R.A., Simon E.M., Marks H.G., and Scherer S.S. The CNS phenotype of X-linked Charcot-Marie-Tooth disease: more than a peripheral problem. Neurology 61 (2003) 1475-1478
44. Trexler E.B., Bennett M.V., Bargiello T.A., and Verselis V.K. Voltage gating and permeation in a gap junction hemichannel. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 5836-5841
45. Valiunas V. Biophysical properties of connexin-45 gap junction hemichannels studied in vertebrate cells. J. Gen. Physiol. 119 (2002) 147-164
46. Valiunas V., and Weingart R. Electrical properties of gap junction hemichannels identified in transfected HeLa cells. Pflugers. Arch. 440 (2000) 366-379
47. VanSlyke J.K., Deschênes S.M., and Musil L.S. Intracellular transport, assembly, and degradation of wild-type and disease-linked mutant gap junction proteins. Mol. Biol. Cell 11 (2000) 1933-1946
48. Willecke K., Eiberger J., Degen J., Eckardt D., Romualdi A., Guldenagel M., Deutsch U., and Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol. Chem. 383 (2002) 725-737
49. Yum S.W., Kleopa K.A., Shumas S., and Scherer S.S. Diverse trafficking abnormalities of Connexin32 mutants causing CMTX. Neurobiol. Dis. 11 (2002) 43-52