Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity

Molecular Biology and Evolution

Volumn 28, Issue 4, 2011, Pages 1415-1424

  Zakon, Harold H ^a,b   Jost, Manda C ^c   Lu, Ying ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c WESTERN NEW MEXICO UNIVERSITY   (United States)

Author keywords

amniotes; brain; gene duplication; sodium channel; terrestriality; tetrapods

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

AMPHIBIA; ARTICLE; BRAIN; CARBONIFEROUS; CELLULAR DISTRIBUTION; CHROMOSOME; DEVONIAN; ELASMOBRANCHII; FOWL; GENE DUPLICATION; GENETIC VARIABILITY; LAND BIOME; LIZARD; MAMMAL; NONHUMAN; NULL HYPOTHESIS; PHYLOGENY; PROTEIN EXPRESSION; SOMATOSENSORY SYSTEM; SYNTENY; TELEOST; TETRAPOD; VERTEBRATE;

ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; BRAIN; EVOLUTION, MOLECULAR; GENE DUPLICATION; HUMANS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHYLOGENY; SODIUM CHANNELS;

AMNIOTA; AMPHIBIA; AVES; MAMMALIA; SQUAMATA; TELEOSTEI; TETRAPODA;

EID: 79952849568     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq325     Document Type: Article

References (57)

1. Akopian A, Sivilotti L, Wood J. 1996. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379:257-262.
2. Angelino E, Brenner M. 2007. Excitability constraints on voltage-gated sodium channels. PLoS Comput Biol. 3:e177.
3. Blomme T, Vandepoele K, De Bodt S, Simillion C, Maere S, Van de Peer Y. 2006. The gain and loss of genes during 600 million years of vertebrate evolution. Genome Biol. 7:R43.
4. v1.6 is localized at nodes of Ranvier, dendrites, and synapses. Proc Natl Acad Sci USA. 97:5616-5620. (Pubitemid 30313767)
5. Clack J. 2007. Devonian climate change, breathing, and the origin of the tetrapod stem group. Integr Comp Biol. 47:510-523. (Pubitemid 351176840)
6. Cummins T, Aglieco F, Renganathan M, Herzog R, Dib-Hajj S, Waxman S. 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. (Pubitemid 32737728)
7. Cummins T, Dib-Hajj S, Black J, Akopian A, Wood J, Waxman S. 1999. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons. J Neurosci. 19:1-6.
8. Dehal P, Boore J. 2005. Two rounds of genome duplication in the ancestral vertebrate. PLoS Biol. 3:e314.
9. Dib-Hajj S, Black J, Cummins T, Waxman S. 2002. NaN/Nav1.9: a sodium channel with unique properties. Trends Neurosci. 25:253-259. (Pubitemid 34327799)
10. Dorward P, Macintyre A. 1971. Responses from vibration-sensitive receptors in the interosseous region of the duck's hind limb. J Physiol. 219:77-87.
11. Duflocq A, Le Bras B, Bullier E, Couraud F, Davenne M. 2008. Nav1.1 is predominantly expressed in nodes of Ranvier and axon initial segments. Mol Cell Neurosci. 39:180-192.
12. Farré D, Alba M. 2009. Heterogenous patterns of gene-expression diversification in mammalian gene duplicates. Mol Biol Evol. 27:325-335.
13. Glenner H, Thomsen P, Hebsgaard M, Sørensen M, Willwerslev E. 2006. The origin of insects. Science 314:1883-1884. (Pubitemid 46028498)
14. Goldin A. 2002. Evolution of voltage-gated Na(\+) channels. J Exp Biol. 205:575-584.
15. Hains B, Klein J, Saab C, Craner M, Black J, Waxman S. 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. (Pubitemid 37210901)
16. Hasenstaub A, Otte S, Callaway E, Sejnowski TJ. 2010. Metbolic cost as a unifying principle governing neuronal biophysics. Proc Natl Acad Sci USA. 107:12329-12334.
17. Hedges S. 2009. Vertebrates (Vertebrata). New York: Oxford University Press. p. 309-314.
18. Hellsten U, Harland R, Gilchrist M, et al. 2010. The genome of the Western clawed frog Xenopus tropicalis. Science 328:633-636.
19. Herzog R, Cummins T, Ghassemi F, Dib-Hajj S, Waxman S. 2003. Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons. J Physiol. 551:741-750. (Pubitemid 37221069)
20. Hill A, Nishino A, Nakajo K, Zhang G, Fineman J, Selzer M, Okamura Y, Cooper E. 2008. Ion channel clustering at the axon initial segment and node of Ranvier evolved sequentially in early chordates. PLoS Genet. 4:e1000317.
21. Hoegg S, Meyer A. 2007. Phylogenomic analyses of KCNA gene clusters in vertebrates: why do gene clusters stay intact? BMC Evol Biol. 7:139.
22. Hu W, Tian C, Li T, Yang M, Hou H, Shu Y. 2009. Distinct contributions of Nav1.6 and Nav1.2 in action potential initiation and backpropagation. Nat Neurosci. 12:996-1002.
23. Hunt C. 1961. On the nature of vibration receptors in the hind limb of the cat. J Physiol. 155:175-186.
24. Hurley I, Mueller R, Dunn K, et al. 2007. A new time-scale for ray-finned fish evolution. Proc R Soc Lond B Biol Sci. 274:489-498. (Pubitemid 47055521)
25. Jackson H, Marshall C, Accill E. 2007. Evolution and structural diversification of hyperpolarization-activated cyclic nucleotide-gated channel genes. Physiol Genomics. 29:231-245. (Pubitemid 47173295)
26. Jarnot M, Corbett A. 2006. Immunolocalization of NaV1.2 channel subtypes in rat and cat brain and spinal cord with high affinity antibodies. Brain Res. 1107:1-12. (Pubitemid 44205114)
27. Kellis M, Birren B, Lander E. 2004. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 28:617-624. (Pubitemid 38524797)
28. Kuraku S. 2008. Insights into cyclostome phylogenomics: pre-2R or post-2R. Zool Sci. 25:960-968.
29. Lopreato G, Lu Y, Southwell A, Atkinson A, Hillis D, Wilcox T, Zakon H. 2001. Evolution and divergence of sodium channel genes in vertebrates. Proc Natl Acad Sci USA. 98:7588-7592. (Pubitemid 32567992)
30. Lorincz A, Nusser Z. 2010. Molecular identity of dendritic voltage-gated sodium channels. Science 328:906-909.
31. Madsen O. 2009. Mammals (Mammalia). New York: Oxford University Press. p. 459-461.
32. Maeda N, Miyoshi S, Toh H. 1983. First observation of a muscle spindle in fish. Nature 302:61-62. (Pubitemid 13138475)
33. Maier SKG, Westenbroek RE, McCormick KA, Curtis R, Scheuer T, Catterall WA. 2004. Distinct subcellular localization of different sodium channel a and b subunits in single ventricular myocytes from mouse heart. Circulation 109:1421-1427. (Pubitemid 38387830)
34. Meyer A, Schartl M. 1999. Gene and genome duplications in vertebrates: the one-to-four (-to eight in fish) rule and the evolution of novel gene function. Curr Opin Cell Biol. 11:699-704.
35. Milinkovitch M, Helaers R, Tzika A. 2010. Historical constraints on vertebrate genome evolution. Genome Biol Evol. 2:13-18.
36. Northcutt R. 2002. Understanding brain evolution. Integr Comp Biol. 42:743-756.
37. Novak A, Jost M, Lu Y, Taylor A, Zakon H, Ribera A. 2006. Gene duplications and evolution of vertebrate voltage-gated sodium channels. J Mol Evol. 63:208-221. (Pubitemid 44126976)
38. v1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J Neurosci. 27:5903-5914. (Pubitemid 46849766)
39. Okamura Y, Ono F, Okagaki R, Chong J, Mandel G. 1994. Neural expression of a sodium channel gene requires cell-specific interactions. Neuron 13:937-948. (Pubitemid 24347306)
40. Panopoulou G, Poustka A. 2005. Timing and mechanisms of ancient vertebrate genome duplications-the adventure of a hypothesis. Trends Genet. 121:559-567. (Pubitemid 41278461)
41. Piontkivska H, Hughes A. 2003. Evolution of vertebrate voltage-gated ion channel alpha chains by sequential gene duplication. J Mol Evol. 56:277-285. (Pubitemid 36279033)
42. Plummer N, Meisler M. 1999. Evolution and diversity of mammalian sodium channel genes. Genomics 57:323-331. (Pubitemid 29205515)
43. Proske U. 1969. Vibration sensitive mechanoreceptors in snake skin. Exp Neurol. 23:187-194.
44. Ross C, Eckhardt A, Herrel A, Hylander W, Metzger K, Shaerlaeken V, Washington R, Williams S. 2007. Modulation of intra-oral processing in mammals and lepidosaurs. Integr Comp Biol. 47:118-136. (Pubitemid 351176744)
45. Saito S, Shingai R. 2006. Evolution of thermo TRP ion channel homologs in vertebrates. Physiol Genomics. 27:219-230. (Pubitemid 46708775)
46. Sallan L, Coates M. 2010. End-Devonian extinction and a bottleneck in the early evolution of modern jawed vertebrates. Proc Natl Acad Sci USA. 107:10131-10135.
47. Schmidt-Hieber C, Bischofberger J. 2010. Fast sodium channel gating supports localized and efficient axonal action potential initiation. J Neurosci. 30:10233-10242.
48. Shedlock A, Edwards S. 2009. Amniotes (Amniota). New York: Oxford University Press. p. 375-379.
49. Sneddon L. 2002. Anatomical and electrophysiological analysis of the trigeminal nerve in a teleost fish, Oncorhynchus mykiss. Neurosci Lett. 319:167-171. (Pubitemid 34143198)
50. Sneddon L, Braithwaite V, Gentle M. 2003. Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system. Proc R Soc Lond B Biol Sci. 270:1115-1121. (Pubitemid 36683454)
51. Soares D. 2002. Neurology: an ancient sensory organ in crocodilians. Nature 417:241-242. (Pubitemid 34534696)
52. Van Wart A, Trimmer J, Matthews G. 2007. Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol. 500:339-352. (Pubitemid 44937127)
53. Von Düring M, Miller M. 1979. Sensory nerve endings in the skin and deep structures. In: Gans C, Northcutt R, Ulinski P, editors. Biology of the Reptilia. New York: Academic Press. p. 407-442.
54. Watanabe E, Hiyama T, Shimizu H, Kodama R, Hayashi N, Miyata S, Yanagawa Y, Obara K, Noda M. 2006. Sodium-level-sensitive sodium channel Na(x) is expressed in glial laminate processes in the sensory circumventricular organs. Am J Physiol Regul Integr Comp Physiol. 290:R568-R576.
55. \+ channel subtypes in central neurons. Neuron. 3:695-704.
56. Whitaker W, Clare J, Powell A, Chen Y-H, Faull R, Emson P. 2000. Distribution of voltage-gated sodium channel alpha-subunit and beta-subunit mRNAs in human hippocampal formation, cortex, and cerebellum. J Comp Neurol. 422:123-139. (Pubitemid 30346568)
57. Whitaker WR, Faull RL, Waldvogel HJ, Plumpton CJ, Emson PC, Clare JJ. 2001. Comparative distribution of voltage-gated sodium channel proteins in human brain. Brain Res Mol Brain Res. 88:37-53. (Pubitemid 32274258)