Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems

Journal of Neuroscience

Volumn 22, Issue 15, 2002, Pages 6458-6470

  Altevogt, Bruce M ^a   Kleopa, Kleopas A ^b   Postma, Friso R ^a   Scherer, Steven S ^b   Paul, David L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

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

Author keywords

Connexin; Cx29; Gap junction; Myelin; Oligodendrocyte; Schwann cell

Indexed keywords

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

ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; GAP JUNCTION; GLIA CELL; IMMUNOHISTOCHEMISTRY; MOLECULAR CLONING; MOUSE; MYELINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCHWANN CELL; SCIATIC NERVE; SPINAL CORD;

EID: 0036703632     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-15-06458.2002     Document Type: Article

References (73)

1. Altevogt BM, Paul DL, Goodenough DA (2000) Cloning and characterization of a novel central nervous system specific connexin, mouse connexin29. Mol Biol Cell [Suppl] 11:330a.
2. Anzini P, Neuberg DHH, Schachner M, Nelles E, Willecke K, Zielasek J, Toyka KV, Suter U, Martini R (1997) Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein connexin 32. J Neurosci 17:4545-4551.
3. Arroyo EJ, Scherer SS (2000) On the molecular architecture of myelinated fibers. Histochem Cell Biol 113:1-18.
4. Arroyo EJ, Xu T, Poliak S, Watson M, Peles E, Scherer SS (2001) Internodal specializations of myelinated axons in the central nervous system. Cell Tissue Res 305:53-66.
5. Baba H, Akita H, Ishibashi T, Inoue Y, Nakahira K, Ikenaka K (1999) Completion of myelin compaction, but not the attachment of oligodendroglial processes triggers K(+) channel clustering. J Neurosci Res 58:752-764.
6. Balice-Gordon RJ, Bone LJ, Scherer SS (1998) Functional gap functions in the schwann cell myelin sheath. J Cell Biol 142:1095-1104.
7. Bergoffen J, Scherer SS, Wang S, Scott MO, Bone LJ, Paul DL, Chen K, Lensch MW, Chance PF, Fischbeck KH (1993) Connexin mutations in X-linked Charcot-Marie-Tooth disease. Science 262:2039-2042.
8. Browne DL, Gancher ST, Nutt JG, Brunt ER, Smith EA, Kramer P, Litt M (1994) Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat Genet 8:136-140.
9. Bunge RP (1968) Glial cells and the central myelin sheath. Physiol Rev 48:197-251.
10. Butt AM, 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.
11. Butt AM, Ransom BR (1989) Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of lucifer yellow and horseradish peroxidase. Glia 2:470-475.
12. Chandross KJ, Kessler JA, Cohen RI, Simburger E, Spray DC, Bieri P, Dermietzel R (1996) Altered connexin expression after peripheral nerve injury. Mol Cell Neurosci 7:501-518.
13. Chiu SY (1991) Functions and distribution of voltage-gated sodium and potassium channels in mammalian Schwann cells. Glia 4:541-558.
14. Del Rio-Hortega P (1928) Tercera aportación al conocimiento morfo-lógico e interpretci6n funcional de la oligodendroglia. Mem Real Soc Esp Hist Nat 14:5-122.
15. 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 tissue. Proc Natl Acad Sci USA 86:10148-10152.
16. 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.
17. Duncan ID, Hammang JP, Trapp BD (1987) Abnormal compact myelin in the myelin-deficient rat: Absence of proteolipid protein correlates with a defect in the intraperiod line. Proc Natl Acad Sci USA 84:6287-6291.
18. Einheber S, Zanazzi G, Ching W, Scherer S, Milner TA, Peles E, Salzer JL (1997) The axonal membrane protein Caspr, a homologue of neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J Cell Biol 139:1495-1506.
19. Gabriels JE, Paul DL (1998) Connexin43 is highly localized to sites of disturbed flow in rat aortic endothelium but connexin37 and connexin40 are more uniformly distributed. Circ Res 83:636-643.
20. Haefliger J-A, Bruzzone R, Jenkins NA, Gilbert DJ, Copeland NG, Paul DL (1992) Four novel members of the connexin family of gap junction proteins. Molecular cloning, expression, and chromosome mapping. J Biol Chem 267:2057-2064.
21. Hertzberg E (1984) A detergent-independent procedure for the isolation of gap junctions from rat liver. J Biol Chem 259:9936-9943.
22. Jiang JX, White TW, Goodenough DA, Paul DL (1994) Molecular cloning and functional characterization of chick lens fiber connexin45.6. Mol Biol Cell 5:363-373.
23. Kleopa KA, Yum SW, Scherer SS (2002) Cellular mechanisms of connexin32 mutations associated with CNS manifestations. J Neurosci Res 68:522-534.
24. Konishi T (1990) Voltage-gated potassium currents in myelinating Schwann cells in the mouse. J Physiol (Lond) 431:123-139.
25. 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.
26. 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.
27. Lemke G, Axel R (1985) Isolation and sequence of a CDNA encoding the major structural protein of peripheral myelin. Cell 40:501-508.
28. 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.
29. Mambetisaeva ET, Gire V, Evans WH (1999) Multiple connexin expression in peripheral nerve, Schwann cells, and Schwannoma cells. J Neurosci Res 57:166-175.
30. Massa PT, Mugnaini E (1982) Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: A freeze-fracture study. Neuroscience 7:523-538.
31. Mi H, Deerinck TJ, Ellisman MH, Schwarz TL (1995) Differential distribution of closely related potassium channels in rat Schwann cells. J Neurosci 15:3761-3774.
32. Milner RJ, Lai C, Nave KA, Lenoir D, Ogata J, Sutcliffe JG (1985) Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell 42:931-939.
33. Mirsky R, Jessen KR (1990) Schwann cell development and the regulation of myelin. Semin Neurosci 2:423-435.
34. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
35. Nagaoka T, Oyamada M, Okajima S, Takamatsu T (1999) Differential expression of gap junction proteins connexin26, 32, and 43 in normal and crush-injured rat sciatic nerves. Close relationship between connexin43 and occludin in the perineurium. J Histochem Cytochem 47:937-948.
36. 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.
37. Nagy JI, Patel D, Ochalski PA, 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.
38. 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 colocalization with connexin30 and connexin43. J Comp Neurol 441:302-323.
39. Neuberg DH, Sancho S, Suter U (1999) Altered molecular architecture of peripheral nerves in mice lacking the peripheral myelin protein 22 or connexin32. J Neurosci Res 58:612-623.
40. Oh S, Rubin JB, Bennett MV, Verselis VK, Bargiello TA (1999) Molecular determinants of electrical rectification of single channel conductance in gap junctions formed by connexins 26 and 32. J Gen Physiol 114:339-364.
41. 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.
42. Paul DL (1986) Molecular cloning of cDNA for rat liver gap junction protein. J Cell Biol 103:123-134.
43. Paul DL, Ebihara L, Takemoto LJ, Swenson KI, Goodenough DA (1991) Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J Cell Biol 115:1077-1089.
44. Poliak S, Gollan L, Martinez R, Custer A, Einheber S, Salzer JL, Trimmer JS, Shrager P, Peles E (1999) Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K+ channels. Neuron 24:1037-1047.
45. Radeke MJ, Misko TP, Hsu C, Herzenberg LA, Shooter EM (1987) Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 325:593-597.
46. 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.
47. Robinson SR, Hampson ECGM, Munro MN, Vaney DI (1993) Unidirectional coupling of gap junctions between neuroglia. Science 262:1072-1074.
48. Rodriguez CI, Dymecki SM (2000) Origin of the precerebellar system. Neuron 27:475-486.
49. Sandri C, Van Buren JM, Akert K (1977) Membrane morphology of the vertebrate nervous system. A study with freeze-etch technique. Prog Brain Res 46:1-384.
50. Scherer SS, Salzer JL (2001) Axon-Schwann cell interactions in peripheral nerve regeneration. In: Glial Cell Development (Jessen KR, Richardson WD, eds), pp 299-330. Oxford: Oxford UP.
51. Scherer SS, Braun PE, Grinspan J, Collarini E, Wang DY, Kamholz J (1994) Differential regulation of the 2′. 3′-cyclic nucleotide 3′-phosphodiesterase gene during oligodendrocyte development. Neuron 12:1363-1375.
52. Scherer SS, Deschenes SM, Xu YT, Grinspan JB, Fischbeck KH, Paul DL (1995) Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci 15:8281-8294.
53. Scherer SS, Xu YT, Nelles E, Fischbeck K, Willecke K, Bone LJ (1998) Connexin32-null mice develop demyelinating peripheral neuropathy. Glia 24:8-20.
54. Shillito P, Molenaar PC, Vincent A, Leys K, Zheng W, van den Berg RJ, Plomp JJ, van Kempen GT, Chauplannaz G, Wintzen AR (1995) Acquired neuromyotonia: Evidence for autoantibodies directed against K+ channels of peripheral nerves. Ann Neurol 38:714-722.
55. Smart SL, Lopantsev V, Zhang CL, Robbins CA, Wang H, Chiu SY, Schwartzkroin PA, Messing A, Tempel BL (1998) Deletion of the K(V)1.1 potassium channel causes epilepsy in mice. Neuron 20:809-819.
56. Sohl G, Eiberger J, Jung YT, Kozak CA, Willecke K (2001) The mouse gap junction gene connexin29 is highly expressed in sciatic nerve and regulated during brain development. J Biol Chem 382:973-978.
57. Srinivas M, Rozental R, Kojima T, Dermietzel R, Mehler M, Condorelli DF, Kessler JA, Spray DC (1999) Functional properties of channels formed by the neuronal gap junction protein connexin36. J Neurosci 19:9848-9855.
58. 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.
59. Stolinski C, Breathnach AS, Thomas PK, Gabriel G, King RH (1985) Distribution of particle aggretates in the internodal axolemma and adaxonal Schwann cell membrane in rodent peripheral nerve. J Neurol Sci 67:213-222.
60. Swenson KI, Jordan JR, Beyer EC, Paul DL (1989) Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell 57:145-155.
61. Tetzlaff W (1982) Tight junction contact events and temporary gap junctions in the sciatic nerve fibres of the chicken during Wallerian degeneration and subsequent regeneration. J Neurocytol 11:839-858.
62. Teubner B, Odermatt B, Guldenagel M, Sohl G, Degen J, Bukauskas F, 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.
63. Trapp BD, Quarles RH (1984) Immunocytochemical localization of the myelin-associated glycoprotein. Fact or artifact? J Neuroimmunol 6:233-249.
64. Veenstra RD, Wang HZ, Westphale EM, Beyer EC (1992).Multiple connexins confer distinct regulatory and conductance properties of gap junctions in developing heart. Circ Res 71:1277-1283.
65. Venance L, Cordier J, Monge M, Zalc B, Glowinski J, Giaume C (1995) Homotypic and heterotypic coupling mediated by gap junctions during glial cell differentiation in vitro. Eur J Neurosci 7:451-461.
66. Verselis VK, Trexler EB, Bukauskas FF (2000) Connexin hemichannels and cell-cell channels: Comparison of properties. Braz J Med Biol Res 33:379-389.
67. Waxman SG, Black JA (1984) Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res 308:77-87.
68. White TW (2002) Unique and redundant connexin contributions to lens development. Science 295:319-320.
69. White TW, Paul DL (1999) Genetic diseases and gene knockouts reveal diverse connexin functions. Annu Rev Physiol 61:283-310.
70. Willecke K, Temme A, Teubner B, Ott T (1999) Characterization of targeted connexin32-deficient mice: A model for the human Charcot-Marie-Tooth (X-type) inherited disease. Ann NY Acad Sci 883:302-309.
71. Yoshimura T, Satake M, Kobayashi T (1996) Connexin43 is another gap junction protein in the peripheral nervous system. J Neurochem 67:1252-1258.
72. Zamboni L, de Martino C (1967) Buffered picric-acid formaldehyde: A new rapid fixative for electron-microscopy. J Cell Biol 35:148A.
73. Zhao S, Fort A, Spray DC (1999) Characteristics of gap junction channels in Schwann cells from wild-type and connexin-null mice. Ann NY Acad Sci 883:533-537.