Evolutionary genomics reveals the premetazoan origin of opposite gating polarity in animal-type voltage-gated ion channels

Genomics

Volumn 99, Issue 4, 2012, Pages 241-245

  Cai, Xinjiang ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Channel evolution; Choanoflagellate; Electric signaling; Genomics; HCN channel; Hyperpolarization

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL;

ARTICLE; CELL POLARITY; CHANNEL GATING; CHOANOFLAGELLATE; CONTROLLED STUDY; GENETIC CONSERVATION; METAZOON; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; SALPINGOECA ROSETTA; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; BIOPHYSICS; CALCIUM CHANNELS; CHOANOFLAGELLATA; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; EVOLUTION, MOLECULAR; GENOMICS; MOLECULAR SEQUENCE DATA; NUCLEOTIDES, CYCLIC; PHYLOGENY; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SODIUM CHANNELS;

ANIMALIA; CHOANOFLAGELLIDA; METAZOA; PROTISTA; SALPINGOECA;

EID: 84859099458     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2012.01.007     Document Type: Article

References (50)

1. Yu F.H., Yarov-Yarovoy V., Gutman G.A., Catterall W.A. Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol. Rev. 2005, 57:387-395.
2. Catterall W.A. Ion channel voltage sensors: structure, function, and pathophysiology. Neuron 2010, 67:915-928.
3. DiFrancesco D. A study of the ionic nature of the pace-maker current in calf Purkinje fibres. J. Physiol. 1981, 314:377-393.
4. Halliwell J.V., Adams P.R. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res. 1982, 250:71-92.
5. Mannikko R., Elinder F., Larsson H.P. Voltage-sensing mechanism is conserved among ion channels gated by opposite voltages. Nature 2002, 419:837-841.
6. Vemana S., Pandey S., Larsson H.P. S4 movement in a mammalian HCN channel. J. Gen. Physiol. 2004, 123:21-32.
7. Robinson R.B., Siegelbaum S.A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 2003, 65:453-480.
8. Craven K.B., Zagotta W.N. CNG and HCN channels: two peas, one pod. Annu. Rev. Physiol. 2006, 68:375-401.
9. Biel M., Wahl-Schott C., Michalakis S., Zong X. Hyperpolarization-activated cation channels: from genes to function. Physiol. Rev. 2009, 89:847-885.
10. DiFrancesco D. The role of the funny current in pacemaker activity. Circ. Res. 2010, 106:434-446.
11. Jackson H.A., Marshall C.R., Accili E.A. Evolution and structural diversification of hyperpolarization-activated cyclic nucleotide-gated channel genes. Physiol. Genomics 2007, 29:231-245.
12. Cai X. Subunit stoichiometry and channel pore structure of ion channels: all for one, or one for one?. J. Physiol. 2008, 586:925-926.
13. Arnegard M.E., Zwickl D.J., Lu Y., Zakon H.H. Old gene duplication facilitates origin and diversification of an innovative communication system-twice. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:22172-22177.
14. Zakon H.H., Jost M.C., Lu Y. Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity. Mol. Biol. Evol. 2011, 28:1415-1424.
15. Liebeskind B.J., Hillis D.M., Zakon H.H. Evolution of sodium channels predates the origin of nervous systems in animals. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9154-9159.
16. Carr M., Leadbeater B.S., Hassan R., Nelson M., Baldauf S.L. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16641-16646.
17. Strong M., Chandy K.G., Gutman G.A. Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol. Biol. Evol. 1993, 10:221-242.
18. King N., Carroll S.B. A receptor tyrosine kinase from choanoflagellates: molecular insights into early animal evolution. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:15032-15037.
19. King N., Hittinger C.T., Carroll S.B. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 2003, 301:361-363.
20. King N., Westbrook M.J., Young S.L., Kuo A., Abedin M., Chapman J., Fairclough S., Hellsten U., Isogai Y., Letunic I., et al. The genome of the choanoflagellate Monosiga brevicollis and the origins of metazoan multicellularity. Nature 2008, 451:783-788.
21. 2+ signaling 'toolkit' at the origin of Metazoa. Mol. Biol. Evol. 2008, 25:1357-1361.
22. Sebe-Pedros A., Roger A.J., Lang F.B., King N., Ruiz-Trillo I. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10142-10147.
23. 2+ signaling machinery in early animal and fungal evolution. Mol. Biol. Evol. 2012, 29:91-100.
24. X. Cai, Ancient origin of four-domain voltage-gated Na+ channels predates the divergence of animals and fungi, J. Membr. Biol. (in press) doi: doi:10.1007/s00232-012-9415-9.
25. Cavalier-Smith T., Chao E.E. Phylogeny and evolution of apusomonadida (protozoa: apusozoa): new genera and species. Protist 2010, 161:549-576.
26. Ruiz-Trillo I., Burger G., Holland P.W., King N., Lang B.F., Roger A.J., Gray M.W. The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 2007, 23:113-118.
27. Fairclough S.R., Dayel M.J., King N. Multicellular development in a choanoflagellate. Curr. Biol. 2010, 20:R875-R876.
28. Dayel M.J., Alegado R.A., Fairclough S.R., Levin T.C., Nichols S.A., McDonald K., King N. Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev. Biol. 2011, 357:73-82.
29. Heginbotham L., Abramson T., MacKinnon R. A functional connection between the pores of distantly related ion channels as revealed by mutant K+ channels. Science 1992, 258:1152-1155.
30. Eismann E., Muller F., Heinemann S.H., Kaupp U.B. A single negative charge within the pore region of a cGMP-gated channel controls rectification, Ca2+ blockage, and ionic selectivity. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:1109-1113.
31. Kaupp U.B., Seifert R. Molecular diversity of pacemaker ion channels. Annu. Rev. Physiol. 2001, 63:235-257.
32. Roncaglia P., Mistrik P., Torre V. Pore topology of the hyperpolarization-activated cyclic nucleotide-gated channel from sea urchin sperm. Biophys. J. 2002, 83:1953-1964.
33. Baruscotti M., Bottelli G., Milanesi R., DiFrancesco J.C., DiFrancesco D. HCN-related channelopathies. Pflugers Arch. 2010, 460:405-415.
34. Bell D.C., Yao H., Saenger R.C., Riley J.H., Siegelbaum S.A. Changes in local S4 environment provide a voltage-sensing mechanism for mammalian hyperpolarization-activated HCN channels. J. Gen. Physiol. 2004, 123:5-19.
35. Zagotta W.N., Olivier N.B., Black K.D., Young E.C., Olson R., Gouaux E. Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 2003, 425:200-205.
36. Flynn G.E., Black K.D., Islas L.D., Sankaran B., Zagotta W.N. Structure and rearrangements in the carboxy-terminal region of SpIH channels. Structure 2007, 15:671-682.
37. Zhou L., Siegelbaum S.A. Gating of HCN channels by cyclic nucleotides: residue contacts that underlie ligand binding, selectivity, and efficacy. Structure 2007, 15:655-670.
38. Schulze-Bahr E., Neu A., Friederich P., Kaupp U.B., Breithardt G., Pongs O., Isbrandt D. Pacemaker channel dysfunction in a patient with sinus node disease. J. Clin. Invest. 2003, 111:1537-1545.
39. Nof E., Luria D., Brass D., Marek D., Lahat H., Reznik-Wolf H., Pras E., Dascal N., Eldar M., Glikson M. Point mutation in the HCN4 cardiac ion channel pore affecting synthesis, trafficking, and functional expression is associated with familial asymptomatic sinus bradycardia. Circulation 2007, 116:463-470.
40. Milanesi R., Baruscotti M., Gnecchi-Ruscone T., DiFrancesco D. Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel. N. Engl. J. Med. 2006, 354:151-157.
41. Ueda K., Nakamura K., Hayashi T., Inagaki N., Takahashi M., Arimura T., Morita H., Higashiuesato Y., Hirano Y., Yasunami M., et al. Functional characterization of a trafficking-defective HCN4 mutation, D553N, associated with cardiac arrhythmia. J. Biol. Chem. 2004, 279:27194-27198.
42. Shemarova I.V. cAMP-dependent signal pathways in unicellular eukaryotes. Crit. Rev. Microbiol. 2009, 35:23-42.
43. Nimigean C.M., Shane T., Miller C. A cyclic nucleotide modulated prokaryotic K+ channel. J. Gen. Physiol. 2004, 124:203-210.
44. Clayton G.M., Silverman W.R., Heginbotham L., Morais-Cabral J.H. Structural basis of ligand activation in a cyclic nucleotide regulated potassium channel. Cell 2004, 119:615-627.
45. Haynes W.J., Ling K.Y., Saimi Y., Kung C. PAK paradox: paramecium appears to have more K(+)-channel genes than humans. Eukaryot. Cell 2003, 2:737-745.
46. Kaupp U.B., Kashikar N.D., Weyand I. Mechanisms of sperm chemotaxis. Annu. Rev. Physiol. 2008, 70:93-117.
47. Katoh K., Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 2008, 9:286-298.
48. Talavera G., Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 2007, 56:564-577.
49. Darriba D., Taboada G.L., Doallo R., Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011, 27:1164-1165.
50. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.