Molecular cloning and functional characterization of Xenopus tropicalis frog transient receptor potential vanilloid 1 reveal its functional evolution for heat, acid, and capsaicin sensitivities in terrestrial vertebrates

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2388-2397

  Ohkita, Masashi ^a   Saito, Shigeru ^b   Imagawa, Toshiaki ^c   Takahashi, Kenji ^a   Tominaga, Makoto ^b   Ohta, Toshio ^a  

^a TOTTORI UNIVERSITY   (Japan)

^b OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CLONE CELLS; CLONING; LANTHANUM COMPOUNDS; MAMMALS; NEURONS; PLANTS (BOTANY);

DORSAL ROOT GANGLION NEURONS; FUNCTIONAL CHARACTERIZATION; INTRACELLULAR CALCIUM CONCENTRATION; MOLECULAR CLONING; SEQUENCE IDENTITY; TRANSIENT RECEPTOR POTENTIAL VANILLOID; TRANSIENT RECEPTOR POTENTIALS; XENOPUS TROPICALIS;

TRANSIENTS;

CALCIUM ION; CAPSAICIN; VANILLOID RECEPTOR 1;

ACIDITY; AMINO ACID SEQUENCE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CHEMOSENSITIVITY; CONTROLLED STUDY; HEAT SENSITIVITY; HELA CELL; HUMAN; HUMAN CELL; ION TRANSPORT; MOLECULAR CLONING; MOLECULAR EVOLUTION; MUTAGENESIS; NOCICEPTIVE STIMULATION; NONHUMAN; OOCYTE; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL GANGLION; STIMULUS RESPONSE; TERRESTRIAL SPECIES; VERTEBRATE; XENOPUS; XENOPUS TROPICALIS;

AMPHIBIA; ANIMALIA; ANURA; MAMMALIA; VERTEBRATA; XENOPUS TROPICALIS;

EID: 84862929579     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.305698     Document Type: Article

References (40)

1. Saito, S., and Shingai, R. (2006) Evolution of thermo-TRP ion channel homologs in vertebrates. Physiol. Genomics 27, 219-230 (Pubitemid 46708775)
2. Hayes, P., Meadows, H. J., Gunthorpe, M. J., Harries, M. H., Duckworth, D. M., Cairns, W., Harrison, D. C., Clarke, C. E., Ellington, K., Prinjha, R. K., Barton, A. J., Medhurst, A. D., Smith, G. D., Topp, S., Murdock, P., Sanger, G. J., Terrett, J., Jenkins, O., Benham, C. D., Randall, A. D., Gloger, I. S., Davis, J. B. (2000) Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain 88, 205-215
3. Jordt, S. E., and Julius, D. (2002) Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108, 421-430
4. Savidge, J., Davis, C., Shah, K., Colley, S., Phillips, E., Ranasinghe, S., Winter, J., Kotsonis, P., Rang, H., McIntyre, P. (2002) Cloning and functional characterization of the guinea pig vanilloid receptor 1. Neuropharmacology 43, 450-456 (Pubitemid 35257937)
5. Correll, C. C., Phelps, P. T., Anthes, J. C., Umland, S., Greenfeder, S. (2004) Cloning and pharmacological characterization of mouse TRPV1. Neurosci. Lett. 370, 55-60 (Pubitemid 39369856)
6. Gavva, N. R., Klionsky, L., Qu, Y., Shi, L., Tamir, R., Edenson, S., Zhang, T. J., Viswanadhan, V. N., Toth, A., Pearce, L. V., Vanderah, T. W., Porreca, F., Blumberg, P. M., Lile, J., Sun, Y., Wild, K., Louis, J. C., Treanor, J. J. (2004) Molecular determinants of vanilloid sensitivity in TRPV1. J. Biol. Chem. 279, 20283-20295 (Pubitemid 38623474)
7. Phelps, P. T., Anthes, J. C., Correll, C. C. (2005) Cloning and functional characterization of dog transient receptor potential vanilloid receptor-1 (TRPV1). Eur. J. Pharmacol. 513, 57-66 (Pubitemid 40692246)
8. Seebacher, F., and Murray, S. A. (2007) Transient receptor potential ion channels control thermoregulatory behaviour in reptiles. PLoS One 2, e281
9. Gracheva, E. O., Ingolia, N. T., Kelly, Y. M., Cordero-Morales, J. F., Hollopeter, G., Chesler, A. T., Sánchez, E. E., Perez, J. C., Weissman, J. S., Julius, D. (2010) Molecular basis of infrared detection by snakes. Nature 464, 1006-1011
10. Chéry-Croze, S., Godinot, F., Jourdan, G., Bernard, C., Chayvialle, J. A. (1985) Capsaicin in adult frogs. Effects on nociceptive responses to cutaneous stimuli and on nervous tissue concentrations of immunoreactive substance P, somatostatin, and cholecystokinin. Naunyn. Schmiedebergs. Arch. Pharmacol. 331, 159-165 (Pubitemid 16211035)
11. Szolcsányi, J. (2004) Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptides 38, 377-384
12. Kuffler, D. P., Lyfenko, A., Vyklický, L., Vlachová, V. (2002) Cellular mechanisms of nociception in the frog. J. Neurophysiol. 88, 1843-1850 (Pubitemid 35191185)
13. Saito, S., Fukuta, N., Shingai, R., Tominaga, M. (2011) Evolution of vertebrate transient receptor potential vanilloid 3 channels. Opposite temperature sensitivity between mammals and western clawed frogs. PLoS Genet. 7, e1002041
14. Philippi, M., Vyklický, L., Kuffler, D. P., Orkand, R. K. (1995) Serotonin- and proton-induced and modified ionic currents in frog sensory neurons. J. Neurosci. Res. 40, 387-395
15. Dowland, L. K., Luyckx, V. A., Enck, A. H., Leclercq, B., Yu, A. S. (2000) Molecular cloning and characterization of an intracellular chloride channel in the proximal tubule cell line, LLC-PK1. J. Biol. Chem. 275, 37765-37773 (Pubitemid 32004892)
16. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., Miyawaki, A. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90 (Pubitemid 34044921)
17. Kalderon, D., Roberts, B. L., Richardson, W. D., Smith, A. E. (1984) A short amino acid sequence able to specify nuclear location. Cell 39, 499-509 (Pubitemid 15198589)
18. Ohta, T., Imagawa, T., Ito, S. (2008) Novel gating and sensitizing mechanism of capsaicin receptor (TRPV1). Tonic inhibitory regulation of extracellular sodium through the external protonation sites on TRPV1. J. Biol. Chem. 283, 9377-9387
19. Caterina, M. J., and Julius, D. (2001) The vanilloid receptor. A molecular gateway to the pain pathway. Annu. Rev. Neurosci. 24, 487-517 (Pubitemid 32695237)
20. Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., Julius, D. (1997) The capsaicin receptor. A heat-activated ion channel in the pain pathway. Nature 389, 816-824 (Pubitemid 27462969)
21. Jordt, S. E., Tominaga, M., Julius, D. (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc. Natl. Acad. Sci. U.S.A. 97, 8134-8139 (Pubitemid 30460785)
22. Ohta, T., Ikemi, Y., Murakami, M., Imagawa, T., Otsuguro, K., Ito, S. (2006) Potentiation of transient receptor potential V1 functions by the activation of metabotropic 5-HT receptors in rat primary sensory neurons. J. Physiol. 576, 809-822 (Pubitemid 44637885)
23. Kajihara, Y., Murakami, M., Imagawa, T., Otsuguro, K., Ito, S., Ohta, T. (2010) Histamine potentiates acid-induced responses mediating transient receptor potential V1 in mouse primary sensory neurons. Neuroscience 166, 292-304
24. McIntyre, P., McLatchie, L. M., Chambers, A., Phillips, E., Clarke, M., Savidge, J., Toms, C., Peacock, M., Shah, K., Winter, J., Weerasakera, N., Webb, M., Rang, H. P., Bevan, S., James, I. F. (2001) Pharmacological differences between the human and rat vanilloid receptor 1 (VR1). Br. J. Pharmacol. 132, 1084-1094 (Pubitemid 32238914)
25. Tominaga, M., and Tominaga, T. (2005) Structure and function of TRPV1. Pflugers. Arch. 451, 143-150 (Pubitemid 41424917)
26. Xu, H., Ramsey, I. S., Kotecha, S. A., Moran, M. M., Chong, J. A., Lawson, D., Ge, P., Lilly, J., Silos-Santiago, I., Xie, Y., DiStefano, P. S., Curtis, R., Clapham, D. E. (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418, 181-186 (Pubitemid 34773772)
27. Güler, A. D., Lee, H., Iida, T., Shimizu, I., Tominaga, M., Caterina, M. (2002) Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 22, 6408-6414 (Pubitemid 35386397)
28. Bianchi, B. R., Lee, C. H., Jarvis, M. F., El Kouhen, R., Moreland, R. B., Faltynek, C. R., Puttfarcken, P. S. (2006) Modulation of human TRPV1 receptor activity by extracellular protons and host cell expression system. Eur. J. Pharmacol. 537, 20-30
29. Wood, J. N., Winter, J., James, I. F., Rang, H. P., Yeats, J., Bevan, S. (1988) Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J. Neurosci. 8, 3208-3220
30. 3H]Resiniferatoxin binding by the vanilloid receptor. Species-related differences, effects of temperature, and sulfhydryl reagents. Naunyn. Schmiedebergs. Arch. Pharmacol. 347, 84-91
31. Tewksbury, J. J., and Nabhan, G. P. (2001) Seed dispersal. Directed deterrence by capsaicin in chilies. Nature 412, 403-404 (Pubitemid 32702696)
32. Khokha, M. K., Chung, C., Bustamante, E. L., Gaw, L. W., Trott, K. A., Yeh, J., Lim, N., Lin, J. C., Taverner, N., Amaya, E., Papalopulu, N., Smith, J. C., Zorn, A. M., Harland, R. M., Grammer, T. C. (2002) Techniques and probes for the study of Xenopus tropicalis development. Dev. Dyn. 225, 499-510 (Pubitemid 35429732)
33. Rosenblum, E. B., Poorten, T. J., Settles, M., Murdoch, G. K., Robert, J., Maddox, N., Eisen, M. B. (2009) Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS One 4, e6494
34. Myers, B. R., Sigal, Y. M., Julius, D. (2009) Evolution of thermal response properties in a cold-activated TRP channel. PLoS One 4, e5741
35. Benton, M. J., and Donoghue, P. C. (2007) Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26-53 (Pubitemid 46026279)
36. Kashiwagi, K., Kashiwagi, A., Kurabayashi, A., Hanada, H., Nakajima, K., Okada, M., Takase, M., Yaoita, Y. (2010) Xenopus tropicalis. An ideal experimental animal in amphibia. Exp. Anim. 59, 395-405
37. Hellsten, U., Harland, R. M., Gilchrist, M. J., Hendrix, D., Jurka, J., Kapitonov, V., Ovcharenko, I., Putnam, N. H., Shu, S., Taher, L., Blitz, I. L., Blumberg, B., Dichmann, D. S., Dubchak, I., Amaya, E., Detter, J. C., Fletcher, R., Gerhard, D. S., Goodstein, D., Graves, T., Grigoriev, I. V., Grimwood, J., Kawashima, T., Lindquist, E., Lucas, S. M., Mead, P. E., Mitros, T., Ogino, H., Ohta, Y., Poliakov, A. V., Pollet, N., Robert, J., Salamov, A., Sater, A. K., Schmutz, J., Terry, A., Vize, P. D., Warren, W. C., Wells, D., Wills, A., Wilson, R. K., Zimmerman, L. B., Zorn, A. M., Grainger, R., Grammer, T., Khokha, M. K., Richardson, P. M., Rokhsar, D. S. (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328, 633-636
38. Jones, D. T., Taylor, W. R., Thornton, J. M. (1992) The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282
39. Rzhetsky, A., and Nei, M. (1992) Mol. Biol. Evol. 9, 945-967
40. Felsenstein, J. (1985) Evolution 39, 783-791