Novel mRNA isoforms of the sodium channels Nav1.2, Nav1.3 and Nav1.7 encode predicted two-domain, truncated proteins

Neuroscience

Volumn 155, Issue 3, 2008, Pages 797-808

  Kerr, N C H ^a   Holmes, F E ^a   Wynick, D ^a  

^a Dept Anat Sch Med Sci U   (United Kingdom)

Author keywords

alternative splicing; brain; DRG; Scn2a; Scn3a; Scn9a

Indexed keywords

ISOPROTEIN; MESSENGER RNA; VOLTAGE GATED SODIUM CHANNEL;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DOWN REGULATION; EXON; GENE CONTROL; GENE EXPRESSION; GENETIC CODE; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; MALE; MOUSE; NERVE FIBER TRANSECTION; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; REGULATOR GENE; RNA ISOLATION; SCN2A GENE; SCN3A GENE; SCN9A GENE; SEQUENCE ANALYSIS; SPINAL GANGLION; STOP CODON; UPREGULATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; AXOTOMY; BRAIN; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; EXONS; GANGLIA, SPINAL; GENE EXPRESSION; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; RATS; RATS, WISTAR; RNA SPLICING; RNA, MESSENGER; SODIUM CHANNELS;

EID: 49249100212     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.04.060     Document Type: Article

References (84)

1. 2+ channel. Proc Natl Acad Sci U S A 98 (2001) 6935-6940
2. Amrani N., Sachs M.S., and Jacobson A. Early nonsense: mRNA decay solves a translational problem. Nat Rev Mol Cell Biol 7 (2006) 415-425
3. Baker M.D. Electrophysiology of mammalian Schwann cells. Prog Biophys Mol Biol 78 (2002) 83-103
4. Burset M., Seledtsov I.A., and Solovyev V.V. Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res 28 (2000) 4364-4375
5. Burset M., Seledtsov I.A., and Solovyev V.V. SpliceDB: database of canonical and non-canonical mammalian splice sites. Nucleic Acids Res 29 (2001) 255-259
6. Chen J., Ikeda S.R., Lang W., Isales C.M., and Wei X. Molecular cloning of a putative tetrodotoxin-resistant sodium channel from dog nodose ganglion neurons. Gene 202 (1997) 7-14
7. Clark F., and Thanaraj T.A. Categorization and characterization of transcript-confirmed constitutively and alternatively spliced introns and exons from human. Hum Mol Genet 11 (2002) 451-464
8. Cox J.J., Reimann F., Nicholas A.K., Thornton G., Roberts E., Springell K., Karbani G., Jafri H., Mannan J., Raashid Y., Al-Gazali L., Hamamy H., Valente E.M., Gorman S., Williams R., McHale D.P., Wood J.N., Gribble F.M., and Woods C.G. An SCN9A channelopathy causes congenital inability to experience pain. Nature 444 (2006) 894-898
9. Cummins T.R., Dib-Hajj S.D., and Waxman S.G. Electrophysiological properties of mutant Nav1.7 sodium channels in a painful inherited neuropathy. J Neurosci 24 (2004) 8232-8236
10. Dib-Hajj S., Black J.A., Felts P., and Waxman S.G. Down-regulation of transcripts for Na channel alpha-SNS in spinal sensory neurons following axotomy. Proc Natl Acad Sci U S A 93 (1996) 14950-14954
11. Dietrich P.S., McGivern J.G., Delgado S.G., Koch B.D., Eglen R.M., Hunter J.C., and Sangameswaran L. Functional analysis of a voltage-gated sodium channel and its splice variant from rat dorsal root ganglia. J Neurochem 70 (1998) 2262-2272
12. + channels: multiplicity of expression, plasticity, functional implications and pathophysiological aspects. Eur Biophys J 33 (2004) 180-193
13. Dreumont N., Maresca A., Boisclair-Lachance J.F., Bergeron A., and Tanguay R.M. A minor alternative transcript of the fumarylacetoacetate hydrolase gene produces a protein despite being likely subjected to nonsense-mediated mRNA decay. BMC Mol Biol 6 (2005) 1
14. Drews V.L., Lieberman A.P., and Meisler M.H. Multiple transcripts of sodium channel SCN8A (Na(V)1.6) with alternative 5′- and 3′-untranslated regions and initial characterization of the SCN8A promoter. Genomics 85 (2005) 245-257
15. Ertel E.A., Campbell K.P., Harpold M.M., Hofmann F., Mori Y., Perez-Reyes E., Schwartz A., Snutch T.P., Tanabe T., Birnbaumer L., Tsien R.W., and Catterall W.A. Nomenclature of voltage-gated calcium channels. Neuron 25 (2000) 533-535
16. Felts P.A., Yokoyama S., Dib-Hajj S., Black J.A., and Waxman S.G. Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res Mol Brain Res 45 (1997) 71-82
17. Fertleman C.R., Baker M.D., Parker K.A., Moffatt S., Elmslie F.V., Abrahamsen B., Ostman J., Klugbauer N., Wood J.N., Gardiner R.M., and Rees M. SCN9A mutations in paroxysmal extreme pain disorder: allelic variants underlie distinct channel defects and phenotypes. Neuron 52 (2006) 767-774
18. Forrest A.R., Taylor D.F., Crowe M.L., Chalk A.M., Waddell N.J., Kolle G., Faulkner G.J., Kodzius R., Katayama S., Wells C., Kai C., Kawai J., Carninci P., Hayashizaki Y., and Grimmond S.M. Genome-wide review of transcriptional complexity in mouse protein kinases and phosphatases. Genome Biol 7 (2006) R5
19. Goldberg Y.P., MacFarlane J., MacDonald M.L., Thompson J., Dube M.P., Mattice M., Fraser R., Young C., Hossain S., Pape T., Payne B., Radomski C., Donaldson G., Ives E., Cox J., Younghusband H.B., Green R., Duff A., Boltshauser E., Grinspan G.A., Dimon J.H., Sibley B.G., Andria G., Toscano E., Kerdraon J., Bowsher D., Pimstone S.N., Samuels M.E., Sherrington R., and Hayden M.R. Loss-of-function mutations in the Nav1.7 gene underlie congenital indifference to pain in multiple human populations. Clin Genet 71 (2007) 311-319
20. Goldin A.L., Barchi R.L., Caldwell J.H., Hofmann F., Howe J.R., Hunter J.C., Kallen R.G., Mandel G., Meisler M.H., Netter Y.B., Noda M., Tamkun M.M., Waxman S.G., Wood J.N., and Catterall W.A. Nomenclature of voltage-gated sodium channels. Neuron 28 (2000) 365-368
21. Gustafson T.A., Clevinger E.C., O'Neill T.J., Yarowsky P.J., and Krueger B.K. Mutually exclusive exon splicing of type III brain sodium channel alpha subunit RNA generates developmentally regulated isoforms in rat brain. J Biol Chem 268 (1993) 18648-18653
22. Hains B.C., Saab C.Y., Klein J.P., Craner M.J., and Waxman S.G. Altered sodium channel expression in second-order spinal sensory neurons contributes to pain after peripheral nerve injury. J Neurosci 24 (2004) 4832-4839
23. Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev 48 (2005) 457-476
24. Harkin L.A., McMahon J.M., Iona X., Dibbens L., Pelekanos J.T., Zuberi S.M., Sadleir L.G., Andermann E., Gill D., Farrell K., Connolly M., Stanley T., Harbord M., Andermann F., Wang J., Batish S.D., Jones J.G., Seltzer W.K., Gardner A., Sutherland G., Berkovic S.F., Mulley J.C., and Scheffer I.E. The spectrum of SCN1A-related infantile epileptic encephalopathies. Brain 130 (2007) 843-852
25. + channels in the developing mouse heart. J Physiol 564 (2005) 683-696
26. Heinzen E.L., Yoon W., Tate S.K., Sen A., Wood N.W., Sisodiya S.M., and Goldstein D.B. Nova2 interacts with a cis-acting polymorphism to influence the proportions of drug-responsive splice variants of SCN1A. Am J Hum Genet 80 (2007) 876-883
27. Herlenius E., Heron S.E., Grinton B.E., Keay D., Scheffer I.E., Mulley J.C., and Berkovic S.F. SCN2A mutations and benign familial neonatal-infantile seizures: the phenotypic spectrum. Epilepsia 48 (2007) 1138-1142
28. Holbrook J.A., Neu-Yilik G., Hentze M.W., and Kulozik A.E. Nonsense-mediated decay approaches the clinic. Nat Genet 36 (2004) 801-808
29. International Chicken Genome Sequencing Consortium. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432 (2004) 695-716
30. 2+ channel mutations associated with episodic ataxia type 2. Am J Physiol Cell Physiol 290 (2006) C1209-C1220
31. Kasai N., Fukushima K., Ueki Y., Prasad S., Nosakowski J., Sugata K., Sugata A., Nishizaki K., Meyer N.C., and Smith R.J. Genomic structures of SCN2A and SCN3A: candidate genes for deafness at the DFNA16 locus. Gene 264 (2001) 113-122
32. Katyal S., Gao Z., Liu R.Z., and Godbout R. Evolutionary conservation of alternative splicing in chicken. Cytogenet Genome Res 117 (2007) 146-157
33. Kayano T., Noda M., Flockerzi V., Takahashi H., and Numa S. Primary structure of rat brain sodium channel III deduced from the cDNA sequence. FEBS Lett 228 (1988) 187-194
34. Kerr N.C., Gao Z., Holmes F.E., Hobson S.A., Hancox J.C., Wynick D., and James A.F. The sodium channel Na(v)1.5a is the predominant isoform expressed in adult mouse dorsal root ganglia and exhibits distinct inactivation properties from the full-length Na(v)1.5 channel. Mol Cell Neurosci 35 (2007) 283-291
35. Kerr N.C., Holmes F.E., and Wynick D. Novel isoforms of the sodium channels Nav1.8 and Nav1.5 are produced by a conserved mechanism in mouse and rat. J Biol Chem 279 (2004) 24826-24833
36. Kim C.H., Oh Y., Chung J.M., and Chung K. The changes in expression of three subtypes of TTX sensitive sodium channels in sensory neurons after spinal nerve ligation. Brain Res Mol Brain Res 95 (2001) 153-161
37. Kim C.H., Oh Y., Chung J.M., and Chung K. Changes in three subtypes of tetrodotoxin sensitive sodium channel expression in the axotomized dorsal root ganglion in the rat. Neurosci Lett 323 (2002) 125-128
38. Kryukov G.V., Castellano S., Novoselov S.V., Lobanov A.V., Zehtab O., Guigo R., and Gladyshev V.N. Characterization of mammalian selenoproteomes. Science 300 (2003) 1439-1443
39. Lemaillet G., Walker B., and Lambert S. Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem 278 (2003) 27333-27339
40. Lewis B.P., Green R.E., and Brenner S.E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci U S A 100 (2003) 189-192
41. Li R. Culture methods for selective growth of normal rat and human Schwann cells. Methods Cell Biol 57 (1998) 167-186
42. Lopreato G.F., Lu Y., Southwell A., Atkinson N.S., Hillis D.M., Wilcox T.P., and Zakon H.H. Evolution and divergence of sodium channel genes in vertebrates. Proc Natl Acad Sci U S A 98 (2001) 7588-7592
43. Macdonald R., Bingham S., Bond B.C., Parsons A.A., and Philpott K.L. Determination of changes in mRNA expression in a rat model of neuropathic pain by Taqman quantitative RT-PCR. Brain Res Mol Brain Res 90 (2001) 48-56
44. Marionneau C., Couette B., Liu J., Li H., Mangoni M.E., Nargeot J., Lei M., Escande D., and Demolombe S. Specific pattern of ionic channel gene expression associated with pacemaker activity in the mouse heart. J Physiol 562 (2005) 223-234
45. Martin M.S., Tang B., Ta N., and Escayg A. Characterization of 5′ untranslated regions of the voltage-gated sodium channels SCN1A, SCN2A, and SCN3A and identification of cis-conserved noncoding sequences. Genomics 90 (2007) 225-235
46. Modrek B., and Lee C.J. Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 34 (2003) 177-180
47. Mohler P.J., Rivolta I., Napolitano C., Lemaillet G., Lambert S., Priori S.G., and Bennett V. Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc Natl Acad Sci U S A 101 (2004) 17533-17538
48. Moric E., Herbert E., Trusz-Gluza M., Filipecki A., Mazurek U., and Wilczok T. The implications of genetic mutations in the sodium channel gene (SCN5A). Europace 5 (2003) 325-334
49. Mulley J.C., Scheffer I.E., Petrou S., Dibbens L.M., Berkovic S.F., and Harkin L.A. SCN1A mutations and epilepsy. Hum Mutat 25 (2005) 535-542
50. Nassar M.A., Stirling L.C., Forlani G., Baker M.D., Matthews E.A., Dickenson A.H., and Wood J.N. Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci U S A 101 (2004) 12706-12711
51. Neu-Yilik G., Gehring N.H., Hentze M.W., and Kulozik A.E. Nonsense-mediated mRNA decay: from vacuum cleaner to Swiss army knife. Genome Biol 5 (2004) 218
52. Noda M., Ikeda T., Kayano T., Suzuki H., Takeshima H., Kurasaki M., Takahashi H., and Numa S. Existence of distinct sodium channel messenger RNAs in rat brain. Nature 320 (1986) 188-192
53. Novak A.E., Jost M.C., Lu Y., Taylor A.D., Zakon H.H., and Ribera A.B. Gene duplications and evolution of vertebrate voltage-gated sodium channels. J Mol Evol 63 (2006) 208-221
54. Novak A.E., Taylor A.D., Pineda R.H., Lasda E.L., Wright M.A., and Ribera A.B. Embryonic and larval expression of zebrafish voltage-gated sodium channel alpha-subunit genes. Dev Dyn 235 (2006) 1962-1973
55. Okamura K., Feuk L., Marques-Bonet T., Navarro A., and Scherer S.W. Frequent appearance of novel protein-coding sequences by frameshift translation. Genomics 88 (2006) 690-697
56. Plummer N.W., Galt J., Jones J.M., Burgess D.L., Sprunger L.K., Kohrman D.C., and Meisler M.H. Exon organization, coding sequence, physical mapping, and polymorphic intragenic markers for the human neuronal sodium channel gene SCN8A. Genomics 54 (1998) 287-296
57. Plummer N.W., McBurney M.W., and Meisler M.H. Alternative splicing of the sodium channel SCN8A predicts a truncated two-domain protein in fetal brain and non-neuronal cells. J Biol Chem 272 (1997) 24008-24015
58. Plummer N.W., and Meisler M.H. Evolution and diversity of mammalian sodium channel genes. Genomics 57 (1999) 323-331
59. Raghib A., Bertaso F., Davies A., Page K.M., Meir A., Bogdanov Y., and Dolphin A.C. Dominant-negative synthesis suppression of voltage-gated calcium channel Cav2.2 induced by truncated constructs. J Neurosci 21 (2001) 8495-8504
60. Raike R.S., Kordasiewicz H.B., Thompson R.M., and Gomez C.M. Dominant-negative suppression of Cav2.1 currents by alpha(1)2.1 truncations requires the conserved interaction domain for beta subunits. Mol Cell Neurosci 34 (2007) 168-177
61. Raymond C.K., Castle J., Garrett-Engele P., Armour C.D., Kan Z., Tsinoremas N., and Johnson J.M. Expression of alternatively spliced sodium channel alpha-subunit genes. Unique splicing patterns are observed in dorsal root ganglia. J Biol Chem 279 (2004) 46234-46241
62. Rossenbacker T., Schollen E., Kuiperi C., de Ravel T.J., Devriendt K., Matthijs G., Collen D., Heidbuchel H., and Carmeliet P. Unconventional intronic splice site mutation in SCN5A associates with cardiac sodium channelopathy. J Med Genet 42 (2005) e29
63. Sangameswaran L., Fish L.M., Koch B.D., Rabert D.K., Delgado S.G., Ilnicka M., Jakeman L.B., Novakovic S., Wong K., Sze P., Tzoumaka E., Stewart G.R., Herman R.C., Chan H., Eglen R.M., and Hunter J.C. A novel tetrodotoxin-sensitive, voltage-gated sodium channel expressed in rat and human dorsal root ganglia. J Biol Chem 272 (1997) 14805-14809
64. Sarao R., Gupta S.K., Auld V.J., and Dunn R.J. Developmentally regulated alternative RNA splicing of rat brain sodium channel mRNAs. Nucleic Acids Res 19 (1991) 5673-5679
65. + channel causing benign familial neonatal-infantile seizures. J Neurosci 26 (2006) 10100-10109
66. Schaller K.L., Krzemien D.M., Yarowsky P.J., Krueger B.K., and Caldwell J.H. A novel, abundant sodium channel expressed in neurons and glia. J Neurosci 15 (1995) 3231-3242
67. 2+ channels. J Neurosci 18 (1998) 641-647
68. Shang L.L., and Dudley Jr. S.C. Tandem promoters and developmentally regulated 5′- and 3′-mRNA untranslated regions of the mouse Scn5a cardiac sodium channel. J Biol Chem 280 (2005) 933-940
69. Smith M.R., Smith R.D., Plummer N.W., Meisler M.H., and Goldin A.L. Functional analysis of the mouse Scn8a sodium channel. J Neurosci 18 (1998) 6093-6102
70. 2+ channel. Genomics 22 (1994) 77-87
71. Sorek R., and Ast G. Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Res 13 (2003) 1631-1637
72. Sorek R., Shemesh R., Cohen Y., Basechess O., Ast G., and Shamir R. A non-EST-based method for exon-skipping prediction. Genome Res 14 (2004) 1617-1623
73. Stamm S., Zhu J., Nakai K., Stoilov P., Stoss O., and Zhang M.Q. An alternative-exon database and its statistical analysis. DNA Cell Biol 19 (2000) 739-756
74. Stojic J., Stohr H., and Weber B.H. Three novel ABCC5 splice variants in human retina and their role as regulators of ABCC5 gene expression. BMC Mol Biol 8 (2007) 42
75. Striano P., Bordo L., Lispi M.L., Specchio N., Minetti C., Vigevano F., and Zara F. A novel SCN2A mutation in family with benign familial infantile seizures. Epilepsia 47 (2006) 218-220
76. Tan J., Liu Z., Nomura Y., Goldin A.L., and Dong K. Alternative splicing of an insect sodium channel gene generates pharmacologically distinct sodium channels. J Neurosci 22 (2002) 5300-5309
77. Tang H., Heeley T., Morlec R., and Hubbard S.J. Characterising alternate splicing and tissue specific expression in the chicken from ESTs. Cytogenet Genome Res 117 (2007) 268-277
78. Tang Z.Z., Liang M.C., Lu S., Yu D., Yu C.Y., Yue D.T., and Soong T.W. Transcript scanning reveals novel and extensive splice variations in human l-type voltage-gated calcium channel, Cav1.2 alpha1 subunit. J Biol Chem 279 (2004) 44335-44343
79. Thimmapaya R., Neelands T., Niforatos W., vis-Taber R.A., Choi W., Putman C.B., Kroeger P.E., Packer J., Gopalakrishnan M., Faltynek C.R., Surowy C.S., and Scott V.E. Distribution and functional characterization of human Nav1.3 splice variants. Eur J Neurosci 22 (2005) 1-9
80. Waxman S.G., Kocsis J.D., and Black J.A. Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J Neurophysiol 72 (1994) 466-470
81. Weiss L.A., Escayg A., Kearney J.A., Trudeau M., MacDonald B.T., Mori M., Reichert J., Buxbaum J.D., and Meisler M.H. Sodium channels SCN1A, SCN2A and SCN3A in familial autism. Mol Psychiatry 8 (2003) 186-194
82. Wu Q., and Krainer A.R. AT-AC pre-mRNA splicing mechanisms and conservation of minor introns in voltage-gated ion channel genes. Mol Cell Biol 19 (1999) 3225-3236
83. Xu R., Thomas E.A., Jenkins M., Gazina E.V., Chiu C., Heron S.E., Mulley J.C., Scheffer I.E., Berkovic S.F., and Petrou S. A childhood epilepsy mutation reveals a role for developmentally regulated splicing of a sodium channel. Mol Cell Neurosci 35 (2007) 292-301
84. Yang Y., Wang Y., Li S., Xu Z., Li H., Ma L., Fan J., Bu D., Liu B., Fan Z., Wu G., Jin J., Ding B., Zhu X., and Shen Y. Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J Med Genet 41 (2004) 171-174