Abstract
Transient receptor potential (TRP) channels are unusual among cation channels because of their diverse cation selectivities and activation mechanisms. TRP channels thus play major roles in various sensory perceptions by functioning as multimodal signal integrators. Some TRP subfamily members are also implicated in acute and chronic pain and inflammation. So far, most TRP channel studies have been targeted to human and model organisms within a limited evolutionary context. Classification of TRP channels in various animal genomes has revealed extensive gene gain and loss events across animal species. Furthermore, the chemical activation profiles of some orthologous TRP channels were different between species such as human and mouse. Amino acid substitutions must underlie such differences, and the crucial amino acid residues have been identified in some cases. These changes represent the evolution of TRP channels at the amino acid sequence level. There is also evidence that TRP channels have obtained species-diversity through alternative splicing and possibly cis-regulatory element mutations. All of the above demonstrate the dynamic and plastic evolutionary history of metazoan TRP channels at multiple levels, possibly in conjunction with the specific habitats and life histories of individual species.
Similar content being viewed by others
References
Audo I, Kohl S, Leroy BP, Munier FL, Guillonneau X, Mohand-Said S, Bujakowska K, Nandrot EF, Lorenz B, Preising M, Kellner U, Renner AB, Bernd A, Antonio A, Moskova-Doumanova V, Lancelot M-E, Poloschek CM, Drumare I, Defoort-Dhellemmes S, Wissinger B, Leveillard T, Hamel CP, Schorderet DF, De Baere E, Berger W, Jacobson SG, Zrenner E, Sahel J-A, Bhattacharya SS, Zeitz C (2009) TRPM1 is mutated in patients with autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 85:720–729. doi:10.1016/j.ajhg.2009.10.013
Auer-Grumbach M, Olschewski A, Papic L, Kremer H, McEntagart ME, Uhrig S, Fischer C, Froehlich E, Balint Z, Tang B, Strohmaier H, Lochmueller H, Schlotter-Weigel B, Senderek J, Krebs A, Dick KJ, Petty R, Longman C, Anderson NE, Padberg GW, Schelhaas HJ, van Ravenswaaij-Arts CMA, Pieber TR, Crosby AH, Guelly C (2010) Alterations in the ankyrin domain of TRPV4 cause congenital distal SMA, scapuloperoneal SMA and HMSN2C. Nat Genet 42:160–U196. doi:10.1038/ng.508
Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, Lee LJ, Slobodeniuc V, Kutter C, Watt S, Colak R, Kim T, Misquitta-Ali CM, Wilson MD, Kim PM, Odom DT, Frey BJ, Blencowe BJ (2012) The evolutionary landscape of alternative splicing in vertebrate species. Science 338:1587–1593. doi:10.1126/science.1230612
Boenigk J, Arndt H (2002) Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Anton Leeuw Int J Gen Mol Microbiol 81:465–480. doi:10.1023/a:1020509305868
Cai X (2008) Unicellular Ca(2+) signaling 'toolkit' at the origin of Metazoa. Mol Biol Evol 25:1357–1361. doi:10.1093/molbev/msn077
Cai X, Clapham DE (2012) Ancestral Ca2+ signaling machinery in early animal and fungal evolution. Mol Biol Evol 29:91–100. doi:10.1093/molbev/msr149
Cao E, Liao M, Cheng Y, Julius D (2013) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:113. doi:10.1038/nature12823
Chen J, Kang D, Xu J, Lake M, Hogan JO, Sun C, Walter K, Yao B, Kim D (2013) Species differences and molecular determinant of TRPA1 cold sensitivity. Nat Commun 4. doi:10.1038/ncomms3501
Chen J, Zhang X-F, Kort ME, Huth JR, Sun C, Miesbauer LJ, Cassar SC, Neelands T, Scott VE, Moreland RB, Reilly RM, Hajduk PJ, Kym PR, Hutchins CW, Faltynek CR (2008) Molecular determinants of species-specific activation or blockade of TRPA1 channels. J Neurosci 28:5063–5071. doi:10.1523/jneurosci. 0047-08.2008
Colletti GA, Kiselyov K (2011) TRPML1. Transient receptor potential channels. Adv Exp Med Biol 704:209–219. doi:10.1007/978-94-007-0265-3_11
Cordero-Morales JF, Gracheva EO, Julius D (2011) Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc Natl Acad Sci U S A 108:E1184–E1191. doi:10.1073/pnas.1114124108
Damann N, Voets T, Nilius B (2008) TRPs in our senses. Curr Biol 18:R880–R889. doi:10.1016/j.cub.2008.07.063
Deng H-X, Klein CJ, Yan J, Shi Y, Wu Y, Fecto F, Yau H-J, Yang Y, Zhai H, Siddique N, Hedley-Whyte ET, DeLong R, Martina M, Dyck PJ, Siddique T (2010) Scapuloperoneal spinal muscular atrophy and CMT2C are allelic disorders caused by alterations in TRPV4. Nat Genet 42:165–U102. doi:10.1038/ng.509
Denis V, Cyert MS (2002) Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156:29–34. doi:10.1083/jcb.200111004
Effertz T, Wiek R, Goepfert MC (2011) NompC TRP channel is essential for drosophila sound receptor function. Curr Biol 21:592–597. doi:10.1016/j.cub.2011.02.048
Falardeau JL, Kennedy JC, Acierno JS, Sun M, Stahl S, Goldin E, Slaugenhaupt SA (2002) Cloning and characterization of the mouse McolnI gene reveals an alternatively spliced transcript not seen in humans. BMC Genomics 3. doi:10.1186/1471-2164-3-3
Gaudet R (2008) A primer on ankyrin repeat function in TRP channels and beyond. Mol BioSyst 4:372–379. doi:10.1039/b801481g
Gavva NR, Klionsky L, Qu YS, Shi LC, Tamir R, Edenson S, Zhang TJ, Viswanadhan VN, Toth A, Pearce LV, Vanderah TW, Porreca F, Blumberg PM, Lile J, Sun Y, Wildt K, Louis JC, Treanor JJS (2004) Molecular determinants of vanilloid sensitivity in TRPV1. J Biol Chem 279:20283–20295. doi:10.1074/jbc.M312577200
Gong ZF, Son WS, Chung YD, Kim JW, Shin DW, McClung CA, Lee Y, Lee HW, Chang DJ, Kaang BK, Cho HW, Oh U, Hirsh J, Kernan MJ, Kim CS (2004) Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 24:9059–9066. doi:10.1523/jneurosci. 1645-04.2004
Gracheva EO, Cordero-Morales JF, Gonzalez-Carcacia JA, Ingolia NT, Manno C, Aranguren CI, Weissman JS, Julius D (2011) Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 476:88. doi:10.1038/nature10245
Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sanchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–U1066. doi:10.1038/nature08943
Hinman A, H-h C, Bautista DM, Julius D (2006) TRP channel activation by reversible covalent modification. Proc Natl Acad Sci U S A 103:19564–19568. doi:10.1073/pnas.0609598103
Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278. doi:10.1016/j.cell.2014.05.010
Jabba S, Goyal R, Sosa-Pagan JO, Moldenhauer H, Wu J, Kalmeta B, Bandell M, Latorre R, Patapoutian A, Grandl J (2014) Directionality of temperature activation in mouse TRPA1 ion channel can be inverted by single-point mutations in ankyrin repeat six. Neuron 82:1017–1031. doi:10.1016/j.neuron.2014.04.016
Jang Y, Lee Y, Kim SM, Yang YD, Jung J, Oh U (2012) Quantitative analysis of TRP channel genes in mouse organs. Arch Pharm Res 35:1823–1830. doi:10.1007/s12272-012-1016-8
Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108:421–430. doi:10.1016/s0092-8674(02)00637-2
Julius D (2013) TRP channels and pain. Annu Rev Cell Dev Biol 29(29):355–384. doi:10.1146/annurev-cellbio-101011-155833
Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, Regna K, Muskavitch MAT, Garrity PA (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481:76–U82. doi:10.1038/nature10715
Kang K, Pulver SR, Panzano VC, Chang EC, Griffith LC, Theobald DL, Garrity PA (2010) Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464:597–U155. doi:10.1038/nature08848
Karashima Y, Damann N, Prenen J, Talavera K, Segal A, Voets T, Nilius B (2007) Bimodal action of menthol on the transient receptor potential channel TRPA1. J Neurosci 27:9874–9884. doi:10.1523/jneurosci. 2221-07.2007
Kim J, Chung YD, Park DY, Choi SK, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84. doi:10.1038/nature01733
Koettgen M (2007) TRPP2 and autosomal dominant polycystic kidney disease. Biochim Biophys Acta Mol basis Dis 1772:836–850. doi:10.1016/j.bbadis.2007.01.003
Kohno K, Sokabe T, Tominaga M, Kadowaki T (2010) Honey bee thermal/chemical sensor, AmHsTRPA, reveals neofunctionalization and loss of transient receptor potential channel genes. J Neurosci 30:12219–12229. doi:10.1523/jneurosci. 2001-10.2010
Kremeyer B, Lopera F, Cox JJ, Momin A, Rugiero F, Marsh S, Woods CG, Jones NG, Paterson KJ, Fricker FR, Villegas A, Acosta N, Pineda-Trujillo NG, Diego Ramirez J, Zea J, Burley M-W, Bedoya G, Bennett DLH, Wood JN, Ruiz-Linares A (2010) A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome. Neuron 66:671–680. doi:10.1016/j.neuron.2010.04.030
Kruse M, Schulze-Bahr E, Corfield V, Beckmann A, Stallmeyer B, Kurtbay G, Ohmert I, Schulze-Bahr E, Brink P, Pongs O (2009) Impaired endocytosis of the ion channel TRPM4 is associated with human progressive familial heart block type I. J Clin Investig 119:2737–2744. doi:10.1172/jci38292
Kunert-Keil C, Bisping F, Krueger J, Brinkmeier H (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7. doi:10.1186/1471-2164-7-159
Landoure G, Zdebik AA, Martinez TL, Burnett BG, Stanescu HC, Inada H, Shi Y, Taye AA, Kong L, Munns CH, Choo SS, Phelps CB, Paudel R, Houlden H, Ludlow CL, Caterina MJ, Gaudet R, Kleta R, Fischbeck KH, Sumner CJ (2010) Mutations in TRPV4 cause Charcot-Marie-Tooth disease type 2C. Nat Genet 42:170–U109. doi:10.1038/ng.512
Lee Y, Lee J, Bang S, Hyun S, Kang J, Hong ST, Bae E, Kaang BK, Kim J (2005) Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat Genet 37:305–310. doi:10.1038/ng1513
Leys SP, Degnan BM (2001) Cytological basis of photoresponsive behavior in a sponge larva. Biol Bull 201:323–338. doi:10.2307/1543611
Li Z, Sergouniotis PI, Michaelides M, Mackay DS, Wright GA, Devery S, Moore AT, Holder GE, Robson AG, Webster AR (2009) Recessive mutations of the gene TRPM1 abrogate ON bipolar cell function and cause complete congenital stationary night blindness in humans. Am J Hum Genet 85:711–719. doi:10.1016/j.ajhg.2009.10.003
Liao M, Cao E, Julius D, Cheng Y (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107. doi:10.1038/nature12822
Liu L, Li Y, Wang R, Yin C, Dong Q, Hing H, Kim C, Welsh MJ (2007) Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450:294–U214. doi:10.1038/nature06223
Ludeman DA, Farrar N, Riesgo A, Paps J, Leys SP (2014) Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges. BMC Evol Biol 14:3. doi:10.1186/1471-2148-14-3
Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, Patapoutian A (2007) Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445:541–545. doi:10.1038/nature05544
Matsuura H, Sokabe T, Kohno K, Tominaga M, Kadowaki T (2009) Evolutionary conservation and changes in insect TRP channels. BMC Evol Biol 9:228. doi:10.1186/1471-2148-9-228
Nadler MJS, Hermosura MC, Inabe K, Perraud AL, Zhu QQ, Stokes AJ, Kurosaki T, Kinet JP, Penner R, Scharenberg AM, Fleig A (2001) LTRPC7 is a Mg center dot ATP-regulated divalent cation channel required for cell viability. Nature 411:590–595. doi:10.1038/35079092
Nagatomo K, Ishii H, Yamamoto T, Nakajo K, Kubo Y (2010) The Met268Pro mutation of mouse TRPA1 changes the effect of caffeine from activation to suppression. Biophys J 99:3609–3618. doi:10.1016/j.bpj.2010.10.014
Nagatomo K, Kubol Y (2008) Caffeine activates mouse TRPA1 channels but suppresses human TRPA1 channels. Proc Natl Acad Sci U S A 105:17373–17378. doi:10.1073/pnas.0809769105
Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Arch Eur J Physiol 464:425–458. doi:10.1007/s00424-012-1158-z
Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12. doi:10.1186/gb-2011-12-3-218
Oberwinkler J, Lis A, Giehl KM, Flockerzi V, Philipp SE (2005) Alternative splicing switches the divalent cation selectivity of TRPM3 channels. J Biol Chem 280:22540–22548. doi:10.1074/jbc.M503092200
Ohkita M, Saito S, Imagawa T, Takahashi K, Tominaga M, Ohta T (2012) 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. J Biol Chem 287:2388–2397. doi:10.1074/jbc.M111.305698
Palmer CP, Zhou XL, Lin JY, Loukin SH, Kung C, Saimi Y (2001) A TRP homolog in Saccharomyces cerevisiae forms an intracellular Ca2 + -permeable channel in the yeast vacuolar membrane. Proc Natl Acad Sci U S A 98:7801–7805. doi:10.1073/pnas.141036198
Peng G, Shi X, Kadowaki T (2015) Evolution of TRP channels inferred by their classification in diverse animal species. Mol Phylogenet Evol 84:145–157. doi:10.1016/j.ympev.2014.06.016
Reiser J, Polu KR, Moller CC, Kenlan P, Altintas MM, Wei CL, Faul C, Herbert S, Villegas I, Avila-Casado C, McGee M, Sugimoto H, Brown D, Kalluri R, Mundel P, Smith PL, Clapham DE, Pollak MR (2005) TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 37:739–744. doi:10.1038/ng1592
Runnels LW, Yue LX, Capham DE (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291:1043–1047. doi:10.1126/science.1058519
Saito S, Banzawa N, Fukuta N, Saito CT, Takahashi K, Imagawa T, Ohta T, Tominaga M (2014) Heat and noxious chemical sensor, chicken TRPA1, as a target of bird repellents and identification of its structural determinants by multispecies functional comparison. Mol Biol Evol 31:708–722. doi:10.1093/molbev/msu001
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. doi:10.1371/journal.pgen.1002041
Saito S, Nakatsuka K, Takahashi K, Fukuta N, Imagawa T, Ohta T, Tominaga M (2012) Analysis of Transient Receptor Potential Ankyrin 1 (TRPA1) in frogs and lizards illuminates both nociceptive heat and chemical sensitivities and coexpression with TRP Vanilloid 1 (TRPV1) in ancestral vertebrates. J Biol Chem 287:30743–30754. doi:10.1074/jbc.M112.362194
Saito S, Tominaga M (2015) Functional diversity and evolutionary dynamics of thermoTRP channels. Cell Calcium 57:214–221. doi:10.1016/j.ceca.2014.12.001
Sakai T, Kasuya J, Kitamoto T, Aigaki T (2009) The Drosophila TRPA channel, painless, regulates sexual receptivity in virgin females. Genes Brain Behav 8:546–557. doi:10.1111/j.1601-183X.2009.00503.x
Sato A, Sokabe T, Kashio M, Yasukochi Y, Tominaga M, Shiomi K (2014) Embryonic thermosensitive TRPA1 determines transgenerational diapause phenotype of the silkworm, Bombyx mori. Proc Natl Acad Sci U S A 111:E1249–E1255. doi:10.1073/pnas.1322134111
Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99. doi:10.1126/science.1084370
Sokabe T, Tsujiuchi S, Kadowaki T, Tominaga M (2008) Drosophila Painless is a Ca2+ -requiring channel activated by noxious heat. J Neurosci 28:9929–9938. doi:10.1523/jneurosci. 2757-08.2008
Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, Kuo A, Mitros T, Salamov A, Carpenter ML, Signorovitch AY, Moreno MA, Kamm K, Grimwood J, Schmutz J, Shapiro H, Grigoriev IV, Buss LW, Schierwater B, Dellaporta SL, Rokhsar DS (2008) The Trichoplax genome and the nature of placozoans. Nature 454:955–U919. doi:10.1038/nature07191
Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–U723. doi:10.1038/nature09201
Sun Y, Liu L, Ben-Shahar Y, Jacobs JS, Eberl DF, Welsh MJ (2009) TRPA channels distinguish gravity sensing from hearing in Johnston's organ. Proc Natl Acad Sci U S A 106:13606–13611. doi:10.1073/pnas.0906377106
Tang X, Platt MD, Lagnese CM, Leslie JR, Hamada FN (2013) Temperature integration at the AC thermosensory neurons in Drosophila. J Neurosci 33:894–901. doi:10.1523/jneurosci. 1894-12.2013
Tracey WD, Wilson RI, Laurent G, Benzer S (2003) Painless, a Drosophila gene essential for nociception. Cell 113:261–273. doi:10.1016/s0092-8674(03)00272-1
van Genderen MM, Bijveld MMC, Claassen YB, Florijn RJ, Pearring JN, Meire FM, McCall MA, Riemslag FCC, Gregg RG, Bergen AAB, Kamermans M (2009) Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. Am J Hum Genet 85:730–736. doi:10.1016/j.ajhg.2009.10.012
Vazquez E, Valverde MA (2006) A review of TRP channels splicing. Semin Cell Dev Biol 17:607–617. doi:10.1016/j.semcdb.2006.11.004
Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417. doi:10.1146/annurev.biochem.75.103004.142819
Voets T, Owsianik G, Janssens A, Talavera K, Nilius B (2007) TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol 3:174–182. doi:10.1038/nchembio862
Vriens J, Appendino G, Nilius B (2009) Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol 75:1262–1279. doi:10.1124/mol.109.055624
Walder RY, Landau D, Meyer P, Shalev H, Tsolia M, Borochowitz Z, Boettger MB, Beck GE, Englehardt RK, Carmi R, Sheffield VC (2002) Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 31:171–174. doi:10.1038/ng901
Wang CB, Hu HZ, Colton CK, Wood JD, Zhu MX (2004) An alternative splicing product of the murine trpv1 gene dominant negatively modulates the activity of TRPV1 channels. J Biol Chem 279:37423–37430. doi:10.1074/jbc.M407205200
Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, Daskalakis N, Kwan SY, Ebersviller S, Burchette JL, Pericak-Vance MA, Howel DN, Vance JM, Rosenberg PB (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308:1801–1804. doi:10.1126/science.1106215
Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69. doi:10.1038/nrg3095
Wolfgang W, Simoni A, Gentile C, Stanewsky R (2013) The Pyrexia transient receptor potential channel mediates circadian clock synchronization to low temperature cycles in Drosophila melanogaster. Proc R Soc B Biol Sci 280. doi:10.1098/rspb.2013.0959
Wright DA, Li T, Yang B, Spalding MH (2014) TALEN-mediated genome editing: prospects and perspectives. Biochem J 462:15–24. doi:10.1042/bj20140295
Xiao B, Dubin AE, Bursulaya B, Viswanath V, Jegla TJ, Patapoutian A (2008) Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels. J Neurosci 28:9640–9651. doi:10.1523/jneurosci. 2772-08.2008
Xu J, Sornborger AT, Lee JK, Shen P (2008) Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat Neurosci 11:676–682. doi:10.1038/nn.2119
Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y, Cheng LE, Meltzer S, Jan LY, Jan YN (2013) Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493:221–225. doi:10.1038/nature11685
Zeevi DA, Frumkin A, Bach G (2007) TRPML and lysosomal function. Biochim Biophys Acta Mol basis Dis 1772:851–858. doi:10.1016/j.bbadis.2007.01.004
Zhong L, Bellemer A, Yan H, Honjo K, Robertson J, Hwang RY, Pitt GS, Tracey WD (2012) Thermosensory and nonthermosensory isoforms of Drosophila melanogaster TRPA1 Reveal heat-sensor domains of a ThermoTRP channel. Cell Rep 1:43–55. doi:10.1016/j.celrep.2011.11.002
Zhou Y, Suzuki Y, Uchida K, Tominaga M (2013) Identification of a splice variant of mouse TRPA1 that regulates TRPA1 activity. Nat Commun 4. doi:10.1038/ncomms3399
Acknowledgments
The study on TRP channels in my laboratory has been conducted by Seiya Tsujiuchi, Hironori Matsuura, Keigo Kohno, Tomomi Morimoto (at Nagoya University), Guangda Peng, Xiaofeng Dong, Xiao Shi, Tianbang Li (at Xi’an Jiaotong-Liverpool University) in collaboration with Takaaki Sokabe, Makiko Kashio, and Makoto Tominaga (at Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences).
Compliance with ethical standards
ᅟ
Disclosure of potential conflicts of interest
The author’s study on TRP channels has been funded by 2012 Suzhou Science and Technology Development Planning Programme (Grant no. SYN201213). The author declares that there is no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kadowaki, T. Evolutionary dynamics of metazoan TRP channels. Pflugers Arch - Eur J Physiol 467, 2043–2053 (2015). https://doi.org/10.1007/s00424-015-1705-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00424-015-1705-5