Unique distributions of the gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes

GLIA

Volumn 47, Issue 4, 2004, Pages 346-357

  Kleopa, Kleopas A ^a,b   Orthmann, Jennifer L ^a   Enriquez, Alan ^a   Paul, David L ^c   Scherer, Steven S ^a  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Charcot Marie Tooth disease; Myelin; Neuropathy

Indexed keywords

CONNEXIN 29; CONNEXIN 32; CONNEXIN 47; GAP JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GAP JUNCTION; GRAY MATTER; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MOUSE; MYELIN SHEATH; NONHUMAN; OLIGODENDROGLIA; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; WILD TYPE;

ANIMALS; ANTIBODY SPECIFICITY; CHARCOT-MARIE-TOOTH DISEASE; CONNEXINS; GAP JUNCTIONS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICE; MICE, KNOCKOUT; MYELIN SHEATH; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; RATS; SPINAL CORD;

EID: 4644307412     PISSN: 08941491     EISSN: None     Source Type: Journal    
DOI: 10.1002/glia.20043     Document Type: Article

References (70)

1. Abel A, Bone LJ, Messing A, Scherer SS, Fischbeck KF. 1999. Studies in transgenic mice indicate a loss of connexin32 function in X-linked Charcot-Marie-Tooth disease. J Neuropathol Exp Neurol 58:702-710.
2. Abrams C, Bennett M, Verselis V, Bargiello T. 2002. Voltage opens unopposed gap junction hemichannels formed by a connexin 32 mutant associated with X-linked Charcot-Marie-Tooth disease. Proc Natl Acad Sci USA 99:3980-3984.
3. Altevogt B, Kleopa K, Postma F, Scherer S, Paul D. 2002. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J Neurosci 22:6458-6470.
4. Arroyo EJ, Xu T, Poliak S, Watson M, Peles E, Scherer SS. 2001. Internodal specializations of myelinated axons in the CNS. Cell Tiss Res 305:53-66.
5. Bahr M, Andres F, Timmerman V, Nelis E, Van Broeckhoven C, Dichgans J. 1999. Central visual, acoustic, and motor pathway involvement in a Charcot-Marie-Tooth family with an Asn205Ser mutation in the connexin32 gene. J Neurol Neurosurg Psychiat 66:202-206.
6. Balice-Gordon RJ, Bone LJ, Scherer SS. 1998. Functional gap junctions in the Schwann cell myelin sheath. J Cell Biol 142:1095-1104.
7. Bell C, Willison H, Clark C, Haites N. 1996. CNS abnormalities in a family with a connexin32 mutation and peripheral neuropathy. Eur J Hum Genet 4:S136.
8. Bergoffen J, Scherer SS, Wang S, Oronzi-Scott M, Bone L, Paul DL, Chen K, Lensch MW, Chance P, Fischbeck K. 1993. Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science 262: 2039-2042.
9. Berry M, Ibrahim M, Carlile J, Fuge F, Duncan A, Butt A. 1995. Axon-glial relationships in the anterior medullary velum of the adult rat. J Neurocytol 24:965-983.
10. Bort S, Nelis E, Timmerman V, Sevilla T, Cruz-Martinez A, Martinez F, Millan JM, Arpa J, Vilchez JJ, Prieto F, Van Broeckhoven C, Palau F. 1997. Mutational analysis of the MPZ, PMP22 and Cx32 genes in patients of Spanish ancestry with Charcot-Marie-Tooth disease and hereditary neuropathy with liability to pressure palsies. Hum Genet 99:746-754.
11. Bruzzone R, White TW, Paul DL. 1996. Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27.
12. Bunge R. 1968. Glial cells and the central myelin sheath. Physiol Rev 48:197-251.
13. Butt AM, Ibrahim M, Berry M. 1998. Axon-myelin sheath relations of oligodendrocyte unit phenotypes in the adult rat anterior medullary velum. J Neurocytol 27:259-269.
14. Butt A, Berry M. 2000. Oligodendrocytes and the control of myelination in vivo: new insights from the rat anterior medullary velum. J Neurosci Res 59:477-488.
15. Del Rio-Hortega P. 1928. Tercera aportacion al conocimiento morfologico e interpretacion functional de la oligodendroglia. Mem Real Soc Esp Hist Nat 14:5-122.
16. Dermietzel R, Traub O, Hwang TK, Beyer E, Bennett MVL, Spray DC, Willecke K. 1989. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc Natl Acad Sci USA 86:10148-10152.
17. Dermietzel R, Hwang TK, Spray DS. 1990. The gap junction family: structure, function and chemistry. Anat Embryol 182:517-528.
18. Dermietzel R, Farooq M, Kessler JA, Althaus H, Hertzberg EL, Spray DC. 1997. Oligodendrocytes express gap junction proteins connexin32 and connexin45. Glia 20:101-114.
19. Deschênes SM, Walcott JL, Wexler TL, Scherer SS, Fischbeck KH. 1997. Altered trafficking of mutant connexin32. J Neurosci 17: 9077-9084.
20. Fanarraga ML, Griffiths IR, Zhao M, Duncan ID. 1998. Oligodendrocytes are not inherently programmed to myelinate a specific size of axon. J Comp Neurol 399:94-100.
21. Friedman B, Hockfield S, Black JA, Woodruff KA, Waxman SG. 1989. In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, Rip. Glia 2:380-390.
22. Hanemann CO, Bergmann C, Senderek J, Zerres K, Sperfeld AD. 2003. Transient, recurrent, white matter lesions in X-linked Charcot-Marie-Tooth disease with novel connexin 32 mutation. Arch Neurol 60:605-609.
23. Hildebrand C, Remahl S, Persson H, Bjartmar C. 1993. Myelinated nerve fibres in the CNS. Prog Brain Res 40:319-384.
24. Ibrahim M, Butt A, Berry M. 1995. Relationship between myelin sheath diameter and internodal length in axons of the anterior medullary velum of the adult rat. J Neurol Sci 133:119-127.
25. Kawakami H, Inoue K, Sakakihara I, Nakamura S. 2002. Novel mutation in X-linked Charcot-Marie-Tooth disease associated with CNS impairment. Neurology 59:923-926.
26. Kleopa K, Yum S, Scherer S. 2002. Cellular mechanisms of connexin32 mutations associated with CNS manifestations. J Neurosci Res 68:522-534.
27. Kumai M, Nishii K, Nakamura K, Takeda N, Suzuki M, Shibata Y. 2000. Loss of connexin45 causes a cushion defect in early cardiogenesis. Development 127:3501-3512.
28. Kunzelmann P, Blumcke I, Traub O, Dermietzel R, Willecke K. 1997. Coexpression of connexin45 and -32 in oligodendrocytes of rat brain. J Neurocytol 26:17-22.
29. 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.
30. Lee M-J, Nelson I, Houlden H, Sweeney M, Hilton-Jones D, Blake J, Wood N, Reilly M. 2002. Six novel connexin32 (GJB1) mutations in X-linked Charcot-Marie-Tooth disease. J Neurol Neurosurg Psychiatry 73:304-306.
31. Li J, Hertzberg EL, Nagy JI. 1997. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J Comp Neurol 379:571-591.
32. Li X, Simard J. 2001. Connexin45 gap junction channels in rat cerebral vascular smooth muscle cells. Amer J Physiol Health Circ Physiol 281:H1890-H1898.
33. Li X, Lynn B, Olson C, Meier C, Davidson K, Yasumura T, Rash J, Nagy J. 2002. Connexin29 expression, immunocytochemistry and freeze-fracture replica immunogold labelling (FRIL) in sciatic nerve. Eur J Neurosci 16:795-806.
34. Marques W, Sweeney MG, Wood NW, Wroe SJ, Marques W. 1999. Central nervous system involvement in a novel connexin 32 mutation affecting identical twins. J Neurol Neurosurg Psychiat 66:803-804.
35. Massa PT, Mugnaini E. 1982. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 7:523-538.
36. Menichella D, Goodenough D, Sirkowski E, Scherer S, Paul D. 2003. Connexins are critical for normal myelination in the CNS. J Neurosci 23:5963-5973.
37. Musil LS, Goodenough DA. 1993. Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell 74:1075-1077.
38. Nagy JI, Ochalski PAY, Li J, Hertzberg EL. 1997. Evidence for the co-localization of another connexin with connexin-43 at astrocytic gap junctions in rat brain. Neuroscience 78:533-548.
39. Nagy JI, Patel D, Ochalski PAY, Stelmack GL. 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.
40. Nagy J, Ionescu A, Lynn B, Rash J. 2003a. Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system. J Comp Neurol 22:356-370.
41. Nagy J, Ionescu A, Lynn B, Rash J. 2003b. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: implications from normal and connexin32 knockout mice. Glia 44: 205-218.
42. Nicholson GA, Yeung L, Corbett A. 1998. Efficient neurophysiological selection of X-linked Charcot-Marie-Tooth families. Neurology 51: 1412-1416.
43. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Bussow H, Schilling K, Steinhauser 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.
44. Oh S, Ri Y, Bennett MVL, Trexler EB, Verselis VK, Bargiello TA. 1997. Changes in permeability caused by connexin 32 mutations underlie X-linked Charcot-Marie-Tooth disease. Neuron 19:927-938.
45. Omori Y, Mesnil M, Yamasaki H. 1996. Connexin 32 mutations from X-linked Charcot-Marie-Tooth disease patients: functional defects and dominant negative effects. Mol Biol Cell 7:907-916.
46. Panas M, Karadimas C, Avramopoulos D, Vassilopoulos D. 1998. Central nervous system involvement in four patients with Charcot-Marie-Tooth disease with connexin 32 extracellular mutations. J Neurol Neurosurg Psychiat 65:947-948.
47. Panas M, Kalfakis N, Karadimas C, Vassilopoulos D. 2001. Episodes of generalized weakness in two sibs with the C164T mutation of the connexin 32 gene. Neurology 57:1906-1908.
48. 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.
49. Paulson H, Garbern J, Hoban T, Krajewski K, Lewis R, Fischbeck K, Grossman R, Lenkinski R, Kamholz J, Shy M. 2002. Transient central nervous system white matter abnormality in X-linked Charcot-Marie-Tooth disease. Ann Neurol 52:429-434.
50. + channels. Neuron 24:1037-1047.
51. Rash JE, Duffy HS, Dudek FE, Bilhartz BL, Whalen LR, 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. J Comp Neurol 388:265-292.
52. Rash JE, Yasumura T, Dudek FE, Nagy JI. 2001. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J Neurosci 21:1983-2000.
53. Remahl S, Hildebrand C. 1990. Relation between axons and oligodendroglial cells during initial myelination: 1, the glial unit. J Neuro-cytol 19:313-328.
54. Rouan F, White T, Brown N, Taylor A, Lucke T, Paul D, Munro C, Uitto J, Hodgins M, Richard G. 2001. Trans-dominant inhibition of connexin-43 by mutant connexin-26: implications for dominant connexin disorders affecting epidermal differentiation. J Cell Sci 114: 2105-2113.
55. Sandri C, Van Buren J, Akert K. 1977. Membrane morphology of the vertebrate nervous system: a study with freeze-etch technique. Prog Brain Res 46:1-384.
56. Schelhaas H, Van Engelen B, Gabreels-Festen A, Hageman G, Vliegen J, Van Der Knaap M, Zwarts M. 2002. Transient cerebral white matter lesions in a patient with connexin 32 missense mutation. Neurology 59:2007-2008.
57. Scherer SS, Deschênes SM, Xu Y-T, Grinspan JB, Fischbeck KH, Paul DL. 1995. Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci 15:8281-8294.
58. Scherer SS, Xu Y-T, Nelles E, Fischbeck K, Willecke K, Bone LJ. 1998. Connexin32-null mice develop a demyelinating peripheral neuropathy. Glia 24:8-20.
59. Scherer SS, Bone LJ, Abel A, Deschênes SM, Balice-Gordon R, Fischbeck K. 1999. The role of the gap junction protein connexin32 in the pathogenesis of X-linked Charcot-Marie-Tooth disease. In: Cardew G, editor. Gap junction-mediated intercellular signaling in health and disease. New York: John Wiley and Sons. p 175-185.
60. Schwab ME, Schnell L. 1989. Region-specific appearance of myelin constituents in the developing rat spinal cord. J Neurocytol 18:161-164.
61. Sperber BR, Boyle-Walsh EA, Engleka MJ, Gadue P, Peterson AC, Stein PL, Scherer SS, McMorris FA. 2001. A unique role for fyn in CNS myelination. J Neurosci 21:2039-2047.
62. 2-connexin (connexin-26) can form heteromeric hemichannels. J Biol Chem 270:6768-6772.
63. Sternberger NH, Quarles RH, Itoyama Y, Webster HD. 1979. Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rat. Proc Natl Acad Sci USA 76:1510-1514.
64. Taylor RA, Simon EM, Marks HG, Scherer SS. 2003. The CNS phenotype of X-linked Charcot-Marie-Tooth disease: more than a peripheral problem. Neurology 61:1475-1478.
65. Teubner B, Odermatt B, Guldenagel M, Sohl G, Degen J, Bukauskas FF, Kronengold J, Verselis VK, Jung YT, Kozak CA, Schilling K, Willecke K. 2001. Functional expression of the new gap junction gene connexin47 transcribed in mouse brain and spinal cord neurons. J Neurosci 21:1117-1126.
66. VanSlyke JK, Deschênes SM, Musil LS. 2000. Intracellular transport, assembly, and degradation of wild-type and disease-linked mutant gap junction proteins. Mol Biol Cell 11:1933-1946.
67. Waxman SG, Black JA. 1984. Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res 308: 77-87.
68. Weruaga-Prieto E, Eggli P, Celio MR. 1996. Topographic variations in rat brain oligodendrocyte morphology elucidated by injection of lucifer yellow in fixed tissue slices. J Neurocytol 25:19-31.
69. Yum S, Kleopa K, Shumas S, Scherer SS. 2002. Diverse trafficking abnormalities of Connexin32 mutants causing CMTX. Neurobiol Dis 11:43-52.
70. Zamboni L, de Martino C. 1967. Buffered picric-acid formaldehyde: a new rapid fixative for electron-microscopy. J Cell Biol 35:148A.