Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system

Journal of Comparative Neurology

Volumn 464, Issue 3, 2003, Pages 356-370

  Nagy, James I ^a   Ionescu, Andrei V ^a   Lynn, Bruce D ^a   Rash, John E ^b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Brain; Confocal microscopy, Schmidt Lanterman incisures; Glia, antibodies, intercellular communication

Indexed keywords

CONNEXIN 29; CONNEXIN 30; CONNEXIN 32; CONNEXIN 43; GAP JUNCTION PROTEIN; MYELIN; UNCLASSIFIED DRUG;

ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CELL COMMUNICATION; CENTRAL NERVOUS SYSTEM; GAP JUNCTION; IMMUNOFLUORESCENCE; KNOCKOUT MOUSE; MOUSE; MYELINATED NERVE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; SPINAL CORD;

2',3'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASES; ANIMALS; ASTROCYTES; BRAIN; CONNEXIN 43; CONNEXINS; FLUORESCENT ANTIBODY TECHNIQUE; GAP JUNCTIONS; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MYELIN SHEATH; MYELIN-ASSOCIATED GLYCOPROTEIN; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; TISSUE DISTRIBUTION;

EID: 0042731782     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10797     Document Type: Article

References (62)

1. Altevogt BM, Kleopa KA, Postma FR, Scherer SS, Paul DL. 2002. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J Neurosci 22:6458-6470.
2. Arroyo EJ, Scherer SS. 2000. On the molecular architecture of myelinated fibres. Histochem Cell Biol 113:1-18.
3. Balice-Gordon RJ, Bone LJ, Scherer SS. 1998. Functional gap junctions in the Schwann cell myelin sheath. J Cell Biol 142:1095-1104.
4. 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.
5. Bone LJ, Deschênes SM, Balice-Gordon RJ, Fischbeck KH, Scherer SS. 1997. Connexin 32 and X-linked Charcot-Marie-Tooth disease. Neurobiol Dis 4:221-230.
6. Blakemore WF. 1969. Schmidt-Lanterman incisures in the central nervous system. J Ultrastruct Res 29:496-498.
7. Bruzzone R, White TW, Paul DL. 1996. Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27.
8. Bunge RP, Bunge MB, Ris R. 1960. Electron microscopic study of demyelination in an experimentally induced lesion in adult cat spinal cord. J Biophys Biochem Cytol 7:685-696.
9. Conradi S. 1969. Observations on the ultrastructure of the axon hillock and initial axon segment of lumbosacral motoneurons in the cat. Acta Physiol Scand Suppl 332:65-84.
10. Dahl E, Manthey D, Chen Y, Schwarz H-J, Chang S, Lalley PA, Nicholson BJ, Willecke K. 1996. Molecular cloning and functional expression of mouse connexin30, a gap junction gene highly expressed in adult brain and skin. J Biol Chem 271:17903-17910.
11. Dermietzel R, Traub O, Hwang TK, Beyer E, Bennett MVL, Spray DC, Willecke K. 1989. Differential expression ofthree gap junction proteins in developing and mature brain tissues. Proc Nat Acad Sci USA 86: 10148-10152.
12. Dermietzel R, Farooq M, Kessler JA, Hertzberg EL, Spray DC. 1997. Oligodendrocytes express gap junction proteins connexin32 and connexin45. Glia 20:101-114.
13. Friede R, Samorajski T. 1969. The clefts of Schmidt-Lanterman: a quantitative electron microscopic study of their structure in developing and adult sciatic nerves of the rat. Anat Rec 165:89-102.
14. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. 2002. Multicolor and electron microscopic imaging of connexin trafficking. Science 296:503-507.
15. George CH, Kendall JM, Evans WH. 1999. Intracellular trafficking pathways in the assembly of connexins into gap junctions. J Biol Chem 274:8678-8685.
16. Ghabriel MN, Allt G. 1981. Incisures of Schmidt-Lanterman. Prog Neurobiol 17:25-58.
17. Hall SM, Williams PL. 1970. Studies of the incisures of Schmidt and Lanterman. J Cell Sci 6:767-791.
18. Hildebrand C. 1971. Ultrastructural and light-microscopic studies of the nodal region in large myelinated fibers of the adult feline spinal cord white matter. Acta Physiol Scand Suppl 364:43-79.
19. Hildebrand C, Remahl S, Persson H, Bjartmar C. 1993. Myelinated nerve fibers in the CNS. Prog Neurobiol 40:319-384.
20. Hirano A, Dembitzer HM. 1967. A structural analysis of the myelin sheath in the central nervous system. J Cell Biol 34:555-567.
21. Jordan K, Salan JL, Dominquez M, Sia M, Hand A, Lampe PD, Laird DW. 1999. Trafficking, assembly, and function of a connexin Cx43-green fluorescent protein chimera in live mammalian cells. Mol Biol Cell 10:2033-2050.
22. 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.
23. Kunzelmann P, Schröder W, Traub O, Steinhäuser 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.
24. Lauf U, Giepmans BNG, Lopez P, Braconnot S, Chen S-S, Falk MM. 2002. Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc Natl Acad Sci USA 99:10446-10451.
25. 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.
26. Li WEI, Ochalski PAY, Hertzberg EL, Nagy JI. 1998. Immunorecognition, ultrastructure and phosphorylation of astrocytic gap junctions and connexin43 in rat brain after cerebral focal ischemia. Eur J Neurosci 10:2444-2463.
27. Li X, Lynn BD, Olson C, Meier C, Davidson KG, Yasumura T, Rash JE, Nagy JI. 2002. Connexin29 expression, immunocytochemistry and freeze-fracture replica immunogold labelling (FRIL) in sciatic nerve. Eur J Neurosci 16:795-806.
28. Luizzi FJ, Miller RH. 1987. Radially oriented astrocytes in the normal adult rat spinal cord. Brain Res 403:385-388.
29. Lynn BD, Rempel JL, Nagy JI. 2001. Enrichment of neuronal and glial connexins in the postsynaptic density subcellular fraction of rat brain. Brain Res 898:1-8.
30. Martin PE, Blundell G, Ahmad S, Errington RJ, Evans WH. 2001. Multiple pathways in the trafficking and assembly of connexin 26, 32 and 43 into gap junction intercelluar communication channels. J Cell Sci 114: 3845-3855.
31. Massa PT, Mugnaini E. 1982. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 7:523-538.
32. Mugnaini E. 1986. Cell junctions of astrocytes, ependyma, and related cells in the mammalian central nervous system, with emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In: Fedoroff S, Vernadakis A, editors. Astrocytes. Volume 1. New York: Academic Press. p 329-371.
33. Nagy JI, Dermietzel R. 2000. Gap junctions and connexins in the mammalian central nervous system. In: Hertzberg EL, editor. Advances in molecular and cell biology. Volume 30. Greenwich: JAI Press. p 323-396.
34. Nagy JI, Rash JE. 2000. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res Rev 32:29-44.
35. Nagy JI, Ochalski PAY, Li J, Hertzberg EL. 1997. Evidence for co-localization of another connexin with connexin43 at astrocytic gap junctions in rat brain. Neuroscience 78:533-548.
36. 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.
37. Nagy JI, Li X, Rempel J, Stelmack G, Patel D, Staines WA Yasumura T, Rash JE. 2001. Connexin26 in adult rodent CNS: demonstration at astrocytic gap junctions and co-localization with connexin30 and connexin43. J Comp Neurol 441:302-323.
38. Nagy JI, Dudek FE, Rash JE. 2003a. Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Rev, In press.
39. Nagy JI, Ionescu AV, Lynn BD, Rash JE. 2003b. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: Implications from normal and Cx32 knockout mice. Glia, In press.
40. Ochalski PAY, Frankenstein UN, Hertzberg EL, Nagy JI. 1997. Connexin43 in rat spinal cord: localization in astrocytes and identification of heterotypic astro-oligodendrocytic gap junctions. Neuroscience 76: 931-945.
41. Prime G, Horn G, Sutor B. 2000. Time-related changes in connexin mRNA abundance in the rat neocortex during postnatal development. Dev Brain Res 119:111-125.
42. Rash JE, Yasumura T. 1999. Direct immunogold labeling of connexins and aquaporin4 in freeze-fracture replicas of liver, brain and spinal cord: factors limiting quantitative analysis. Cell Tissue Res 296:307-321.
43. 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.
44. Rash JE, Staines WA, Yasumura T, Patel D, Hudson CS, Stelmack GL, Nagy JI. 2000. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin36 but not Cx32 or Cx43. Proc Natl Acad Sci USA 97:7573-7578.
45. 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.
46. Scadding JW. 1981. Development of ongoing activity, mechanosensitivity, and adrenaline sensitivity in severed peripheral nerve axons. Exp Neurol 73:345-364.
47. Scherer SS. 1996. Molecular specializations at nodes and paranodes in peripheral nerve. Microsc Res Tech 34:452-461.
48. Scherer SS, Deschennes SM, Xu Y-T, Grinspan JP, Fischbeck KH, Paul DL. 1995. Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci 15:8281-8294.
49. Severs NJ. 1999. Cardiovascular disease. Novartis Found Symp 219:188-206.
50. 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. Biol Chem 382:973-978.
51. Trapp BD, Andrews SB, Cootauco C, Quarles R. 1989. The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J Cell Biol 109:2417-2426.
52. Veenstra RD. 1996. Size and selectivity of gap junction channels formed from different connexins. J Bioenerg Biomembr 28:327-337.
53. Verity AN, Campagnoni AT. 1988. Regional expression of myelin protein genes in the developing mouse brain: in situ hybridization studies. J Neurosci Res 21:238-248.
54. Waxman SG, Black JA. 1984. Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res 308:77-87.
55. Webster HF. 1965. The relationship between Schmidt-Lanterman incisures and myelin segmentation during Wallerian degeneration. Ann NY Acad Sci 122:29-38.
56. White TW, Bruzzone R. 1996. Multiple connexin proteins in single intercellular channels: connexin compatibility and functional consequences. J Bioenerg Biomembr 28:339-350.
57. Williams PL, Hall SM. 1970. In vivo observations on mature myelinated nerve fibers of the mouse. J Anat 107:31-38.
58. Williams PL, Hall SM. 1971a. Prolonged in vivo observations of normal peripheral nerve fibers and their acute reactions to crush and deliberate trauma. J Anat 108:397-408.
59. Williams PL, Hall SM. 1971b. Chronic Wallerian degeneration - an in vivo and ultrastructural study. J Anat 109:487-503.
60. Wolburg H, Rohlmann A. 1995. Structure-function relationships in gap junctions. Int Rev Cytol 157:315-373.
61. Yamamoto T, Ochalski PAY, Hertzberg EL, Nagy JI. 1990a. LM and EM immunolocalization of the gap junctions protein connexin43 in rat brain. Brain Res 508:313-319.
62. Yamamoto T, Ochalski PAY, Hertzberg EL, Nagy JI. 1990b. On the organization of astrocytic gap junctions in the brain as suggested by LM and EM immunocytochemistry of connexin43 expression. J Comp Neurol 302:853-883.