Connexins are critical for normal myelination in the CNS

Journal of Neuroscience

Volumn 23, Issue 13, 2003, Pages 5963-5973

  Menichella, Daniela M ^a,c   Goodenough, Daniel A ^a   Sirkowski, Erich ^b   Scherer, Steven S ^b   Paul, David L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

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

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Connexin; Cx32; Cx47; Gap junction; Myelin; Oligodendrocyte

Indexed keywords

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

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL VACUOLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEMYELINATING DISEASE; GAP JUNCTION; GLIA CELL; HEREDITARY MOTOR SENSORY NEUROPATHY; MOUSE; MYELIN SHEATH; MYELINATION; NERVE FIBER; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROGLIA; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; TONIC SEIZURE; TREMOR;

EID: 0038383619     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-13-05963.2003     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. Balice-Gordon RJ, Bone LJ, Scherer SS (1998) Functional gap junctions in the Schwann cell myelin sheath. J Cell Biol 142:1095-1104.
3. Bao ZZ, Cepko CL (1997) The expression and function of Notch pathway genes in the developing rat eye. J Neurosci 17:1425-1434.
4. 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.
5. Bhat RV, Axt KJ, Fosnaugh JS, Smith KJ, Johnson KA, Hill DE, Kinzler KW, Baraban JM (1996) Expression of the APC tumor suppressor protein in oligodendroglia. Glia 17:169-174.
6. 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.
7. D'Ambrosio R, Wenzel J, Schwartzkroin PA, McKhann GM, Janigro D (1998) Functional specialization and topographic segregation of hippocampal astrocytes. J Neurosci 18:4425-4438.
8. Debus E, Weber K, Osborn M (1983) Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25:193-203.
9. 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.
10. 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.
11. + channels. J Neurophysiol 87:1376-1385.
12. Evans WH, Martin PE (2002) Gap junctions: structure and function. Mol Membr Biol 19:121-136.
13. Fort P, Marty L, Piechaczyk M, el Sabrouty S, Dani C, Jeanteur P, Blanchard JM (1985) Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res 13:1431-1442.
14. Garbern JY, Yool DA, Moore GJ, Wilds IB, Faulk MW, Klugmann M, Nave KA, Sistermans EA, Van Der Knaap MS, Bird TD, Shy ME, Kamholz JA, Griffiths IR (2002) Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain 125:551-561.
15. Giaume C, McCarthy KD (1996) Control of gap-junctional communication in astrocytic networks. Trends Neurosci 19:319-325.
16. Gow A, Southwood CM, Lazzarini PA (1998) Disrupted proteolipid protein trafficking results in oligodendrocyte apoptosis in an animal model of Pelizaeus-Merzbacher disease. J Cell Biol 140:925-934.
17. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave KA (1998) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin 3. Science 280:1610-1613.
18. Grinspan JB, Coulalaglou M, Beesley JS, Carpio DF, Scherer SS (1998) Maturation-dependent apoptotic cell death of oligodendrocytes in myelin-deficient rats. J Neurosci Res 54:623-634.
19. Hertzberg E (1984) A detergent-independent procedure for the isolation of gap junctions from rat liver. J Biol Chem 259:9936-9943.
20. 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.
21. Kettenmann H, Orkand RK, Schachner M (1983) Coupling among identified cells in mammalian nervous system cultures. J Neurosci 3:506-516.
22. Kleopa KA, Scherer SS (2002) Inherited neuropathies. Neurol Clin 20:679-709.
23. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA (2000) Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: phenotypic impact in retina. J Neurosci 20:5733-5740.
24. Kruger O, Plum A, Kim J, Winterhager E, Maxeiner S, Hallas G, Kirchhoff S, Traub O, Lamers WH, Willecke K (2000) Defective vascular development in connexin 45-deficient mice. Development 127:4179-4193.
25. 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.
26. Kunzelmann P, Blumcke I, Traub O, Dermietzel R, Willecke K (1997) Co-expression of connexin45 and -32 in oligodendrocytes of rat brain. J Neurocytol 26:17-22.
27. 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.
28. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA (2003) Disruption of Cnpl uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33:366-374.
29. Levin M (2002) Isolation and community: a review of the role of gap-junctional communication in embryonic patterning. J Membr Biol 185:177-192.
30. 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.
31. 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.
32. Martini R (2000) Animal models for inherited peripheral neuropathies. J Neurosci Res 61:244-250.
33. Massa PT, Mugnaini E (1982) Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 7:523-538.
34. Massa PT, Szuchet S, Mugnaini E (1984) Cell-cell interactions of isolated and cultured oligodendrocytes: formation of linear occluding junctions and expression of peculiar intramembrane particles. J Neurosci 4:3128-3139.
35. Matheson DF (1970) Some quantitative aspects of myelination of the optic nerve in rat. Brain Res 24:257-269.
36. 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.
37. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
38. Nagy JI, Ochalski PAY, Li J, Hertzberg EL (1997) Evidence for the colocalization of another connexin with connexin-43 at astrocytic gap junctions in rat brain. Neuroscience 78:533-548.
39. Nagy JI, Patel D, Ochalski PA, Stelmack GL (1999) Connexin30 in rodent, cat and human brain: selective expression in gray matter astrocytes, colocalization with connexin43 at gap junctions and late developmental appearance. Neuroscience 88:447-468.
40. 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.
41. Nelles E, Bützler C, Jung D, Temme A, Gabriel H-D, Dahl U, Traub O, Stümpel F, Jungermann K, Zielasek J, Toyka KV, Dermietzel R, Willecke K (1996) Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc Natl Acad Sci USA 93:9565-9570.
42. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P (2001) Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 21:5429-5438.
43. Orkand RK, Nicholls JG, Kuffler SW (1966) Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29:788-806.
44. 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.
45. Paul DL (1986) Molecular cloning of CDNA for rat liver gap junction protein. J Cell Biol 103:123-134.
46. Rash JE, Dillman RK, Bilhartz BL, Duffy HS, Whalen LR, Yasumura T (1996) Mixed synapses discovered and mapped throughout mammalian spinal cord. Proc Natl Acad Sci USA 93:4235-4239.
47. 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.
48. 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.
49. Robinson SR, Hampson ECGM, Munro MN, Vaney DI (1993) Unidirectional coupling of gap junctions between neuroglia. Science 262:1072-1074.
50. 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.
51. Scherer SS (1997) Molecular genetics of demyelination: new wrinkles on an old membrane. Neuron 18:13-16.
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. Tennekoon GI, Cohen SR, Price DL, McKhann GM (1977) Myelinogenesisin optic nerve: a morphological, autoradiographic, and biochemical analysis. J Cell Biol 72:604-616.
55. 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.
56. 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.
57. 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.
58. Waxman SG, Black JA (1984) Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions. Brain Res 308:77-87.
59. White TW, Paul DL (1999) Genetic diseases and gene knockouts reveal diverse connexin functions. Annu Rev Physiol 61:283-310.
60. White TW, Goodenough DA, Paul DL (1998) Targeted ablation of connexin50 in mice results in microphthalmia and zonular pulverulent cataracts. J Cell Biol 143:815-825.
61. Wujek JR, Bjartmar C, Richer E, Ransohoff RM, Yu M, Tuohy VK, Trapp BD (2002) Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J Neuropathol Exp Neurol 61:23-32.
62. Zahs KR, Newman EA (1997) Asymmetric gap junctional coupling between glial cells in the rat retina. Glia 20:10-22.