Altered expression of ion channel isoforms at the node of Ranvier in P0-deficient myelin mutants

Molecular and Cellular Neuroscience

Volumn 25, Issue 1, 2004, Pages 83-94

  Ulzheimer, Jochen C ^a   Peles, Elior ^b   Levinson, S Rock ^c   Martini, Rudolf ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; MYELIN; POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE CLUSTER; MOTOR NERVE; MOUSE; MYELINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANVIER NODE; SCHWANN CELL;

EID: 1242316261     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.09.015     Document Type: Article

References (68)

1. Akopian A.N., Sivilotti L., Wood J.N. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature. 379:1996;257-262.
2. Akopian A.N., Souslova V., England S., Okuse K., Ogata N., Ure J., Smith A., Kerr B.J., McMahon S.B., Boyce S., Hill R., Stanfa L.C., Dickenson A.H., Wood J.N. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat. Neurosci. 2:1999;541-548.
3. Arroyo E.J., Scherer S.S. On the molecular architecture of myelinated fibers. Histochem. Cell Biol. 113:2000;1-18.
4. Arroyo E.J., Xu T., Grinspan J., Lambert S., Levinson S.R., Brophy P.J., Peles E., Scherer S.S. Genetic dysmyelination alters the molecular architecture of the nodal region. J. Neurosci. 22:2002;1726-1737.
5. Baker M.D., Wood J.N. Involvement of Na+ channels in pain pathways. Trends Pharmacol. Sci. 22:2001;27-31.
6. Bennett V., Lambert S. Physiological roles of axonal ankyrins in survival of premyelinated axons and localization of voltage-gated sodium channels. J. Neurocytol. 28:1999;303-318.
7. Bhat M., Rios J., Lu Y., Garcia-Fresco G., Ching W., St Martin M., Li J., Einheber S., Chesler M., Rosenbluth J., Salzer J.L., Bellen H. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron. 30:2001;369-383.
8. Black J.A., Fjell J., Dib-Hajj S., Duncan I.D., O'Connor L.T., Fried K., Gladwell Z., Tate S., Waxman S.G. Abnormal expression of SNS/PN3 sodium channel in cerebellar Purkinje cells following loss of myelin in the taiep rat. NeuroReport. 10:1999;913-918.
9. Black J.A., Dib-Hajj S., Baker D., Newcombe J., Cuzner M.L., Waxman S.G. Sensory neuron-specific sodium channel SNS is abnormally expressed in the brains of mice with experimental allergic encephalomyelitis and humans with multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 97:2000;11598-11602.
10. Black J.A., Dusart I., Sotelo C., Waxman S.G. Axotomy does not up-regulate expression of sodium channel Nav1.8 in Purkinje cells. Mol. Brain Res. 101:2002;126-131.
11. Boiko T., Rasband M.N., Levinson S.R., Caldwell J.H., Mandel G., Trimmer J.S., Matthews G. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon. Neuron. 30:2001;91-104.
12. Boyle M.E., Berglund E.O., Murai K.K., Weber L., Peles E., Ranscht B. Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron. 30:2001;385-397.
13. Caldwell J.H., Schaller K.L., Lasher R.S., Peles E., Levinson S.R. Sodium channel Nav1.6 is localized at nodes of Ranvier, dendrites, and synapses. Proc. Natl. Acad. Sci. U. S. A. 97:2000;5616-5620.
14. Carenini S., Montag D., Schachner M., Martini R. Subtle roles of neural cell adhesion molecule and myelin-associated glycoprotein during Schwann cell spiralling in P0-deficient mice. Glia. 27:1999;203-212.
15. Carenini S., Maurer M., Werner A., Blazyca H., Toyka K.V., Schmid C.D., Raivich G., Martini R. The role of macrophages in demyelinating peripheral nervous system of mice heterozygously deficient in P0. J. Cell Biol. 152:2001;301-308.
16. Charles P., Tait S., Faivre-Sarrailh C., Barbin G., Gunn-Moore F., Denisenko-Nehrbass N., Guennoc A.M., Girault J.A., Brophy P.J., Lubetzki C. Neurofascin is a glial receptor for the Paranodin/Caspr-Contactin axonal complex at the axoglial junction. Curr. Biol. 12:2002;217-220.
17. Ching W., Zanazzi G., Levinson S.R., Salzer J.L. Clustering of neuronal sodium channels requires contact with myelinating Schwann cells. J. Neurocytol. 28:1999;295-301.
18. + channels. Ann. N. Y. Acad. Sci. 868:1999;233-255.
19. Dugandzija-Novakovic S., Koszowski A.G., Levinson S.R., Shrager P. Clustering of Na+ channels and node of Ranvier formation in remyelinating axons. J. Neurosci. 15:1995;492-503.
20. Dupree J.L., Girault J.A., Popko B. Axo-glial interactions regulate the localization of axonal paranodal proteins. J. Cell Biol. 147:1999;1145-1152.
21. Frei R., Motzing S., Kinkelin I., Schachner M., Koltzenburg M., Martini R. Loss of distal axons and sensory Merkel cells and features indicative of muscle denervation in hindlimbs of P0-deficient mice. J. Neurosci. 19:1999;6058-6067.
22. Giese K., Martini R., Lemke G., Soriano P., Schachner M. Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell. 71:1992;565-576.
23. Girault J.A., Peles E. Development of nodes of Ranvier. Curr. Opin. Neurobiol. 12:2002;476-485.
24. Goldin A.L. Diversity of mammalian voltage-gated sodium channels. Ann. N. Y. Acad. Sci. 868:1999;38-50.
25. Gould H.J. III, Gould T.N., England J.D., Paul D., Liu Z.P., Levinson S.R. A possible role for nerve growth factor in the augmentation of sodium channels in models of chronic pain. Brain Res. 854:2000;19-29.
26. Hinson A.W., Gu X.Q., Dib-Hajj S., Black J.A., Waxman S.G. Schwann cells modulate sodium channel expression in spinal sensory neurons in vitro. Glia. 21:1997;339-349.
27. Ishibashi T., Dupree J.L., Ikenaka K., Hirahara Y., Honke K., Peles E., Popko B., Suzuki K., Nishino H., Baba H. A myelin galactolipid, sulfatide, is essential for maintenance of ion channels on myelinated axon but not essential for initial cluster formation. J. Neurosci. 22:2002;6507-6514.
28. Isom L.L. Sodium channel beta subunits: anything but auxiliary. Neuroscientist. 7:2001;42-54.
29. Jenkins S.M., Bennett V. Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155:2001;739-746.
30. Jenkins S.M., Bennett V. Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion. Proc. Natl. Acad. Sci. U. S. A. 99:2002;2303-2308.
31. Kobsar I., Berghoff M., Samsam M., Wessig C., Mäurer M., Toyka K.V., Martini R. Preserved myelin integrity and reduced axonopathy in connexin32-deficient mice lacking the recombination activating gene-1. Brain. 126:2003;804-813.
32. Kordeli E., Lambert S., Bennett V. AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem. 270:1995;2352-2359.
33. Kozak C.A., Sangameswaran L. Genetic mapping of the peripheral sodium channel genes, Scn9a and Scn10a, in the mouse. Mamm. Genome. 7:1996;787-788.
34. Krzemien D.M., Schaller K.L., Levinson S.R., Caldwell J.H. Immunolocalization of sodium channel isoform NaCh6 in the nervous system. J. Comp. Neurol. 420:2000;70-83.
35. Lambert S., Davis J.Q., Bennett V. Morphogenesis of the node of Ranvier: co-clusters of ankyrin and ankyrin-binding integral proteins define early developmental intermediates. J. Neurosci. 17:1997;7025-7036.
36. Malhotra J.D., Kazen-Gillespie K., Hortsch M., Isom L.L. Sodium channel beta subunits mediate homophilic cell adhesion and recruit ankyrin to points of cell-cell contact. J. Biol. Chem. 275:2000;11383-11388.
37. Martini R., Mohajeri M.H., Kasper S., Giese K.P., Schachner M. Mice doubly deficient in the genes for P0 and myelin basic protein show that both proteins contribute to the formation of the major dense line in peripheral nerve myelin. J. Neurosci. 15:1995;4488-4495.
38. Martini R., Zielasek J., Toyka K.V., Giese K., Schachner M. Protein zero (P0)deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nat. Genet. 11:1995;281-286.
39. Melendez-Vasquez C.V., Rios J.C., Zanazzi G., Lambert S., Bretscher A., Salzer J.L. Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes. Proc. Natl. Acad. Sci. U. S. A. 98:2001;1235-1240.
40. Menichella D.M., Awatramani R., Xu T., Baron P., Vallat J.M., Balsamo J., Lilien J., Scarlato G., Kamholz J., Scherer S.S., Shy M.E. Protein zero is necessary for E-cadherin-mediated adherens junction formation in Schwann cells. Mol. Cell. Neurosci. 18:2001;606-618.
41. Mirsky R., Jessen K.R., Brennan A., Parkinson D., Dong Z., Meier C., Parmantier E., Lawson D. Schwann cells as regulators of nerve development. J. Physiol. (Paris). 96:2002;17-24.
42. Novakovic S.D., Tzoumaka E., McGivern J.G., Haraguchi M., Sangameswaran L., Gogas K.R., Eglen R.M., Hunter J.C. Distribution of the tetrodotoxin- resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. J. Neurosci. 18:1998;2174-2187.
43. Novakovic S.D., Eglen R.M., Hunter J.C. Regulation of Na+ channel distribution in the nervous system. Trends Neurosci. 24:2001;473-478.
44. Peles E., Salzer J.L. Molecular domains of myelinated axons. Curr. Opin. Neurobiol. 10:2000;558-565.
45. Peles E., Nativ M., Lustig M., Grumet M., Schilling J., Martinez R., Plowman G.D., Schlessinger J. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interaction. EMBO J. 16:1997;978-988.
46. Poliak S., Gollan L., Martinez R., Custer A., Einheber S., Salzer J.L., Trimmer J.S., Shrager P., Peles E. Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K+ channels. Neuron. 24:1999;1037-1047.
47. Poliak S., Gollan L., Salomon D., Berglund E.O., Ohara R., Ranscht B., Peles E. Localization of Caspr2 in myelinated nerves depends on axon-glia interactions and the generation of barriers along the axon. J. Neurosci. 21:2001;7568-7575.
48. Rasband M.N., Trimmer J.S. Developmental clustering of ion channels at and near the node of Ranvier. Dev. Biol. 236:2001;5-16.
49. Rasband M.N., Peles E., Trimmer J.S., Levinson S.R., Lux S.E., Shrager P. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J. Neurosci. 19:1999;7516-7528.
50. Rasband M.N., Kagawa T., Park E.W., Ikenaka K., Trimmer J.S. Dysregulation of axonal sodium channel isoforms after adult-onset chronic demyelination. J. Neurosci. Res. 73:2003;465-470.
51. Renganathan M., Cummins T.R., Waxman S.G. Contribution of Nav1.8 sodium channels to action potential electrogenesis in DRG neurons. J. Neurophysiol. 86:2001;629-640.
52. Rios K.C., Rubin M., St. Martin M., Downey R.T., Einheber S., Rosenbluth J., Levinson S.R., Bhat M., Salzer J.L. Paranodal interactions regulate expression of sodium channel subtypes and provide a diffusion barrier for the node of Ranvier. J. Neurosci. 23:2003;7001-7011.
53. Rizzo M.A., Kocsis J.D., Waxman S.G. Mechanisms of paresthesiae, dysesthesiae and hyperesthesiae: role of Na+ channel heterogeneity. Eur. Neurol. 36:1996;3-12.
54. Saito F., Moore S.A., Barresi R., Henry M.D., Messing A., Ross-Barta S., Cohn R.D., Willamson R.A., Sluka K.A., Sherman D.L., Brophy P.J., Schmelzer J.D., Low P.A., Wrabetz L., Feltri M.L., Campbell K.P. Unique role of dystroglycan in peripheral nerve myelination, nodal structure, and sodium channel stabilization. Neuron. 38:2003;747-758.
55. Sangameswaran L., Delgado S.G., Fish L.M., Koch B.D., Jakeman L.B., Stewart G.R., Sze P., Hunter J.C., Eglen R.M., Herman R.C. Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons. J. Biol. Chem. 271:1996;5953-5956.
56. Scherer S.S., Arroyo E.J. Recent progress on the molecular organization of myelinated axons. J. Peripher. Nerv. Syst. 7:2002;1-12.
57. Schmid C.D., Stienekemeier M., Oehen S., Bootz F., Zielasek J., Gold R., Toyka K.V., Schachner M., Martini R. Immune deficiency in mouse models for inherited peripheral neuropathies leads to improved myelin maintenance. J. Neurosci. 20:2000;729-735.
58. Tanaka M., Cummins T.R., Ishikawa K., Dib-Hajj S.D., Black J.A., Waxman S.G. SNS Na+ channel expression increases in dorsal root ganglion neurons in the carrageenan inflammatory pain model. NeuroReport. 9:1998;967-972.
59. Traka M., Dupree J.L., Popko B., Karagogeos D. The neuronal adhesion protein TAG-1 is expressed by Schwann cells and oligodendrocytes and is localized to the juxtaparanodal region of myelinated fibers. J. Neurosci. 22:2002;3016-3024.
60. Tzoumaka E., Tischler A.C., Sangameswaran L., Eglen R.M., Hunter J.C., Novakovic S.D. Differential distribution of the tetrodotoxin-sensitive rPN4/NaCh6/Scn8a sodium channel in the nervous system. J. Neurosci. Res. 60:2000;37-44.
61. Vabnick I., Novakovic S.D., Levinson S.R., Schachner M., Shrager P. The clustering of axonal sodium channels during development of the peripheral nervous system. J. Neurosci. 16:1996;4914-4922.
62. Vabnick I., Trimmer J.S., Schwarz T.L., Levinson S.R., Risal D., Shrager P. Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J. Neurosci. 19:1999;747-758.
63. Vincent A. Understanding neuromyotonia. Muscle Nerve. 23:2000;655-657.
64. Waxman S.G. The molecular pathophysiology of pain: abnormal expression of sodium channel genes and its contributions to hyperexcitability of primary sensory neurons. Pain. 82:1999;S133-S140.
65. Waxman S.G. Acquired channelopathies in nerve injury and MS. Neurology. 56:2001;1621-1627.
66. Waxman S.G. Transcriptional channelopathies: an emerging class of disorders. Nat. Rev. Neurosci. 2:2001;652-659.
67. Zielasek J., Martini R., Toyka K.V. Functional abnormalities in P0-deficient mice resemble human hereditary neuropathies linked to P0 gene mutations. Muscle Nerve. 19:1996;946-952.
68. Zielasek J., Martini R., Suter U., Toyka K.V. Neuromyotonia in mice with hereditary myelinopathies. Muscle Nerve. 23:2000;696-701.