Contactin associates with sodium channel Nav1.3 in native tissues and increases channel density at the cell surface

Journal of Neuroscience

Volumn 24, Issue 33, 2004, Pages 7387-7399

  Shah, Bhaval S ^a,b   Rush, Anthony M ^a,b   Liu, Shujun ^a,b   Tyrrell, Lynda ^a,b   Black, Joel A ^a,b   Dib Hajj, Sulayman D ^a,b   Waxman, Stephen G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b West Haven   (United States)

Author keywords

Axotomy; Cell adhesion molecule; GPI anchor; Neuroma; Sensory neurons; Tetrodotoxin sensitive

Indexed keywords

CELL ADHESION MOLECULE; CONTACTIN; HYBRID PROTEIN; SODIUM CHANNEL; CONTACTINS; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; PEPTIDE; SCN3A PROTEIN, RAT;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; HUMAN; HUMAN CELL; NERVE EXCITABILITY; NEUROMA; NEUROPATHIC PAIN; PRIORITY JOURNAL; PROTEIN PURIFICATION; SCIATIC NERVE; SODIUM CURRENT; SPINAL GANGLION; ANIMAL; BRAIN; CELL LINE; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; ELECTRIC CONDUCTIVITY; GENETICS; METABOLISM; NERVE FIBER; PATCH CLAMP; PRENATAL DEVELOPMENT; RAT; SENSORY NERVE CELL;

ANIMALS; AXONS; BRAIN; CELL ADHESION MOLECULES, NEURONAL; CELL LINE; CELL MEMBRANE; ELECTRIC CONDUCTIVITY; GANGLIA, SPINAL; HUMANS; NERVE TISSUE PROTEINS; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; PEPTIDES; RATS; RECOMBINANT FUSION PROTEINS; SODIUM CHANNELS;

EID: 7244255887     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0322-04.2004     Document Type: Article

References (59)

1. Beckh S, Noda M, Lübbert H, Numa S (1989) Differential regulation of three sodium channel messenger RNAs in the rat central nervous system during development. EMBO J 8:3611-3616.
2. Berglund EO, Ranscht B (1994) Molecular cloning and in situ localization of the human contactin gene (CNTN1) on chromosome 12q11-q12. Genomics 21:571-582.
3. Berglund EO, Murai KK, Fredette B, Sekerkova G, Marturano B, Weber L, Mugnaini E, Ranscht B (1999) Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. Neuron 24:739-750.
4. Bergstrom U, Berglund EO, Kazarinova-Noyes K, Peles E, Brophy PJ, Shrager PBR (2002) Contactin supports the organization of central paranode junctions. Soc Neurosci Abstr 28:819.10.
5. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W, Martin MS, Li J, Einheber S, Chesler M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axon-glia interactions and the domain organization of myelinated axons requires neurexin iv/caspr/paranodin. Neuron 30:369-383.
6. Black JA, Cummins TR, Plumpton C, Chen YH, Hormuzdiar W, Clare JJ, Waxman SG (1999) Upregulation of a silent sodium channel after peripheral, but not central, nerve injury in DRG neurons. J Neurophysiol 82:2776-2785.
7. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB (2000) Potent analgesic effects of GDNF in neuropathic pain states. Science 290:124-127.
8. Boyle ME, Berglund EO, Murai KK, Weber L, Peles E, Ranscht B (2001) Contactin orchestrates assembly of the septate-like junctions at the paranode in myelinated peripheral nerve. Neuron 30:385-397.
9. Brummendorf T, Wolff JM, Frank R, Rathjen FG (1989) Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains. Neuron 2:1351-1361.
10. Chen C, Westenbroek RE, Xu X, Edwards CA, Sorenson DR, Chen Y, McEwen DP, O'Malley HA, Bharucha V, Meadows LS, Knudsen GA, Vilaythong A, Noebels JL, Saunders TL, Scheuer T, Shrager P, Catterall WA, Isom LL (2004) Mice lacking sodium channel beta1 subunits display defects in neuronal excitability, sodium channel expression, and nodal architecture. J Neurosci 24:4030-4042.
11. Cummins TR, Waxman SG (1997) Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury. J Neurosci 17:3503-3514.
12. Cummins TR, Aglieco F, Renganathan M, Herzog RI, Dib-Hajj SD, Waxman SG (2001) Nav1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J Neurosci 21:5952-5961.
13. Devor M, Govrin-Lippmann R, Frank I, Raber P (1985) Proliferation of primary sensory neurons in adult rat dorsal root ganglion and the kinetics of retrograde cell loss after sciatic nerve section. Somatosens Res 3:139-167.
14. Dib-Hajj S, Black JA, Felts P, Waxman SG (1996) Down-regulation of transcripts for Na channel alpha-SNS in spinal sensory neurons following axotomy. Proc Natl Acad Sci USA 93:14950-14954.
15. Dib-Hajj SD, Tyrrell L, Black JA, Waxman SG (1998) NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy. Proc Natl Acad Sci USA 95:8963-8968.
16. Durbec P, Gennarini G, Goridis C, Rougon G (1992) A soluble form of the F3 neuronal cell adhesion molecule promotes neurite outgrowth. J Cell Biol 117:877-887.
17. Faivre-Sarrailh C, Gauthier F, Denisenko-Nehrbass N, Le Bivic A, Rougon G, Girault JA (2000) The glycosylphosphatidyl inositol-anchored adhesion molecule F3/contactin is required for surface transport of paranodin/contactin- associated protein (caspr). J Cell Biol 149:491-502.
18. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG (1997) Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and HNE (PN1): different expression patterns in developing rat nervous system. Mol Brain Res 45:71-82.
19. Fjell J, Hjelmstrom P, Hormuzdiar W, Milenkovic M, Aglieco F, Tyrrell L, Dib-Hajj S, Waxman SG, Black JA (2000) Localization of the tetrodotoxin- resistant sodium channel NaN in nociceptors. NeuroReport 11:199-202.
20. Gennarini G, Cibelli G, Rougon G, Mattei MG, Goridis C (1989) The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin. J Cell Biol 109:775-788.
21. Goldin A (2001) Resurgence of sodium channel research. Annu Rev Physiol 63:871-894.
22. Gollan L, Sabanay H, Poliak S, Berglund EO, Ranscht B, Peles E (2002) Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr. J Cell Biol 157:1247-1256.
23. Hains BC, Black JA, Waxman SG (2002) Primary motor neurons fail to upregulate voltage-gated sodium channel Nav1.3/brain type III following axotomy resulting from spinal cord injury. J Neurosci Res 70:546-552.
24. Hains BC, Klein JP, Saab CY, Craner MJ, Black JA, Waxman SG (2003) Upregulation of sodium channel Nav1.3 and functional involvement in neuronal hyperexcitability associated with central neuropathic pain after spinal cord injury. J Neurosci 23:8881-8892.
25. Isom LL (2001) Sodium channel beta subunits: anything but auxiliary. Neuroscientist 7:42-54.
26. Isom LL, Catterall WA (1996) Na+ channel subunits and Ig domains. Nature 383:307-308.
27. Isom LL, De Jongh KS, Patton DE, Reber BF, Offord J, Charbonneau H, Walsh K, Goldin AL, Catterall WA (1992) Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science 256:839-842.
28. Isom LL, Ragsdale DS, De Jongh KS, Westenbroek RE, Reber BF, Scheuer T, Catterall WA (1995) Structure and function of the beta 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83:433-442.
29. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
30. Kazarinova-Noyes K, Malhotra JD, McEwen DP, Mattei LN, Berglund EO, Ranscht B, Levinson SR, Schachner M, Shrager P, Isom LL, Xiao ZC (2001) Contactin associates with Na+ channels and increases their functional expression. J Neurosci 21:7517-7525.
31. Keating MT, Sanguinetti MC (2001) Molecular and cellular mechanisms of cardiac arrhythmias. Cell 104:569-580.
32. Kim CH, Oh Y, Chung JM, Chung K (2001) The changes in expression of three subtypes of TTX sensitive sodium channels in sensory neurons after spinal nerve ligation. Mol Brain Res 95:153-161.
33. Leffler A, Cummins TR, Dib-Hajj SD, Hormuzdiar WN, Black JA, Waxman SG (2002) GDNF and NGF reverse changes in repriming of TTX-sensitive Na(+) currents following axotomy of dorsal root ganglion neurons. J Neurophysiol 88:650-658.
34. Lindia JA, Abbadie C (2003) Distribution of the voltage gated sodium channel Na(v)1.3-like immunoreactivity in the adult rat central nervous system. Brain Res 960:132-141.
35. Liu C, Dib-Hajj SD, Black JA, Greenwood J, Lian Z, Waxman SG (2001) Direct interaction with contactin targets voltage-gated sodium channel Nav1.9/NaN to the cell membrane. J Biol Chem 276:46553-46561.
36. Liu X, Chung K, Chung JM (1999) Ectopic discharges and adrenergic sensitivity of sensory neurons after spinal nerve injury. Brain Res 849:244-247.
37. Liu X, Zhou JL, Chung K, Chung JM (2001) Ion channels associated with the ectopic discharges generated after segmental spinal nerve injury in the rat. Brain Res 900:119-127.
38. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George Jr AL (2002) Molecular basis of an inherited epilepsy. Neuron 34:877-884.
39. Lyu YS, Park SK, Chung K, Chung JM (2000) Low dose of tetrodotoxin reduces neuropathic pain behaviors in an animal model. Brain Res 871:98-103.
40. Matzner O, Devor M (1994) Hyperexcitability at sites of nerve injury depends on voltage-sensitive Na+ channels. J Neurophysiol 72:349-359.
41. McEwen DP, Meadows LS, Chen C, Thyagarajan V, Isom LL (2004) Sodium channel beta 1 subunit-mediated modulation of Nav1.2 currents and cell surface density is dependent on interactions with contactin and ankyrin. J Biol Chem 279:16044-16049.
42. Meadows L, Malhotra JD, Stetzer A, Isom LL, Ragsdale DS (2001) The intracellular segment of the sodium channel beta 1 subunit is required for its efficient association with the channel alpha subunit. J Neurochem 76:1871-1878.
43. Meadows LS, Chen YH, Powell AJ, Clare JJ, Ragsdale DS (2002) Functional modulation of human brain Nav1.3 sodium channels, expressed in mammalian cells, by auxiliary beta 1, beta 2 and beta 3 subunits. Neuroscience 114:745-753.
44. Meisler MH, Kearney J, Ottman R, Escayg A (2001) Identification of epilepsy genes in human and mouse. Annu Rev Genet 35:567-588.
45. Moran O, Nizzari M, Conti F (2000) Endogenous expression of the beta1A sodium channel subunit in HEK-293 cells. FEBS Lett 473:132-134.
46. Moran O, Conti F, Tammaro P (2003) Sodium channel heterologous expression in mammalian cells and the role of the endogenous beta1-subunits. Neurosci Lett 336:175-179.
47. Okuse K, Malik-Hall M, Baker MD, Poon WY, Kong H, Chao MV, Wood JN (2002) Annexin II light chain regulates sensory neuron-specific sodium channel expression. Nature 417:653-656.
48. Perrin FE, Rathjen FG, Stoeckli ET (2001) Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. Neuron 30:707-723.
49. Pierre K, Dupouy B, Allard M, Poulain DA, Theodosis DT (2001) Mobilization of the cell adhesion glycoprotein F3/contactin to axonal surfaces is activity dependent. Eur J Neurosci 14:645-656.
50. Qin N, D'Andrea MR, Lubin ML, Shafaee N, Codd EE, Correa AM (2003) Molecular cloning and functional expression of the human sodium channel beta1B subunit, a novel splicing variant of the beta1 subunit. Eur J Biochem 270:4762-4770.
51. Ranscht B (1988) Sequence of contactin, a 130-kD glycoprotein concentrated in areas of interneuronal contact, defines a new member of the immunoglobulin supergene family in the nervous system. J Cell Biol 107:1561-1573.
52. Rios JC, Melendez-Vasquez CV, Einheber S, Lustig M, Grumet M, Hemperly J, Peles E, Salzer JL (2000) Contactin-associated protein (Caspr) and contactin form a complex that is targeted to the paranodal junctions during myelination. J Neurosci 20:8354-8364.
53. Shah BS, Stevens EB, Pinnock RD, Dixon AK, Lee K (2001) Developmental expression of the novel voltage-gated sodium channel auxiliary subunit beta3, in rat CNS. J Physiol (Lond) 534:763-776.
54. Shaw G, Morse S, Ararat M, Graham FL (2002) Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 16:869-871.
55. Sleeper AA, Cummins TR, Dib-Hajj SD, Hormuzdiar W, Tyrrell L, Waxman SG, Black JA (2000) Changes in expression of two tetrodotoxin-resistant sodium channels and their currents in dorsal root ganglion neurons after sciatic nerve injury but not rhizotomy. J Neurosci 20:7279-7289.
56. Tyrrell L, Renganathan M, Dib-Hajj SD, Waxman SG (2001) Glycosylation alters steady-state inactivation of sodium channel Nav1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J Neurosci 21:9629-9637.
57. Waxman SG, Kocsis JD, Black JA (1994) Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J Neurophysiol 72:466-470.
58. Waxman SG, Dib-Hajj S, Cummins TR, Black JA (2000) Sodium channels and their genes: dynamic expression in the normal nervous system, dysregulation in disease states(1). Brain Res 886:5-14.
59. Yip HK, Rich KM, Lampe PA, Johnson Jr EM (1984) The effects of nerve growth factor and its antiserum on the postnatal development and survival after injury of sensory neurons in rat dorsal root ganglia. J Neurosci 4:2986-2992.