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Evolution of Vertebrate Transient Receptor Potential Vanilloid 3 Channels: Opposite Temperature Sensitivity between Mammals and Western Clawed Frogs


Transient Receptor Potential (TRP) channels serve as temperature receptors in a wide variety of animals and must have played crucial roles in thermal adaptation. The TRP vanilloid (TRPV) subfamily contains several temperature receptors with different temperature sensitivities. The TRPV3 channel is known to be highly expressed in skin, where it is activated by warm temperatures and serves as a sensor to detect ambient temperatures near the body temperature of homeothermic animals such as mammals. Here we performed comprehensive comparative analyses of the TRPV subfamily in order to understand the evolutionary process; we identified novel TRPV genes and also characterized the evolutionary flexibility of TRPV3 during vertebrate evolution. We cloned the TRPV3 channel from the western clawed frog Xenopus tropicalis to understand the functional evolution of the TRPV3 channel. The amino acid sequences of the N- and C-terminal regions of the TRPV3 channel were highly diversified from those of other terrestrial vertebrate TRPV3 channels, although central portions were well conserved. In a heterologous expression system, several mammalian TRPV3 agonists did not activate the TRPV3 channel of the western clawed frog. Moreover, the frog TRPV3 channel did not respond to heat stimuli, instead it was activated by cold temperatures. Temperature thresholds for activation were about 16 °C, slightly below the lower temperature limit for the western clawed frog. Given that the TRPV3 channel is expressed in skin, its likely role is to detect noxious cold temperatures. Thus, the western clawed frog and mammals acquired opposite temperature sensitivity of the TRPV3 channel in order to detect environmental temperatures suitable for their respective species, indicating that temperature receptors can dynamically change properties to adapt to different thermal environments during evolution.


Vyšlo v časopise: Evolution of Vertebrate Transient Receptor Potential Vanilloid 3 Channels: Opposite Temperature Sensitivity between Mammals and Western Clawed Frogs. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1002041
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002041

Souhrn

Transient Receptor Potential (TRP) channels serve as temperature receptors in a wide variety of animals and must have played crucial roles in thermal adaptation. The TRP vanilloid (TRPV) subfamily contains several temperature receptors with different temperature sensitivities. The TRPV3 channel is known to be highly expressed in skin, where it is activated by warm temperatures and serves as a sensor to detect ambient temperatures near the body temperature of homeothermic animals such as mammals. Here we performed comprehensive comparative analyses of the TRPV subfamily in order to understand the evolutionary process; we identified novel TRPV genes and also characterized the evolutionary flexibility of TRPV3 during vertebrate evolution. We cloned the TRPV3 channel from the western clawed frog Xenopus tropicalis to understand the functional evolution of the TRPV3 channel. The amino acid sequences of the N- and C-terminal regions of the TRPV3 channel were highly diversified from those of other terrestrial vertebrate TRPV3 channels, although central portions were well conserved. In a heterologous expression system, several mammalian TRPV3 agonists did not activate the TRPV3 channel of the western clawed frog. Moreover, the frog TRPV3 channel did not respond to heat stimuli, instead it was activated by cold temperatures. Temperature thresholds for activation were about 16 °C, slightly below the lower temperature limit for the western clawed frog. Given that the TRPV3 channel is expressed in skin, its likely role is to detect noxious cold temperatures. Thus, the western clawed frog and mammals acquired opposite temperature sensitivity of the TRPV3 channel in order to detect environmental temperatures suitable for their respective species, indicating that temperature receptors can dynamically change properties to adapt to different thermal environments during evolution.


Zdroje

1. BandellMMacphersonLJPatapoutianA 2007 From chills to chilis: mechanisms for thermosensation and chemesthesis via thermoTRPs. Curr Opin Neurobiol 17 490 497

2. BenhamCDGunthorpeMJDavisJB 2003 TRPV channels as temperature sensors. Cell Calcium 33 479 487

3. DhakaAViswanathVPatapoutianA 2006 TRP ion channels and temperature sensation. Annu Rev Neurosci 29 135 161

4. PatapoutianAPeierAMStoryGMViswanathV 2003 ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4 529 539

5. SaitoSShingaiR 2006 Evolution of thermoTRP ion channel homologs in vertebrates. Physiol Genomics 27 219 230

6. PeierAMReeveAJAnderssonDAMoqrichAEarleyTJ 2002 A heat-sensitive TRP channel expressed in keratinocytes. Science 296 2046 2049

7. SmithGDGunthorpeMJKelsellREHayesPDReillyP 2002 TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418 186 190

8. XuHRamseyISKotechaSAMoranMMChongJA 2002 TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418 181 186

9. MoqrichAHwangSWEarleyTJPetrusMJMurrayAN 2005 Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307 1468 1472

10. HellstenUHarlandRMGilchristMJHendrixDJurkaJ 2010 The genome of the Western clawed frog Xenopus tropicalis. Science 328 633 636

11. GrandlJHuHBandellMBursulayaBSchmidtM 2008 Pore region of TRPV3 ion channel is specifically required for heat activation. Nat Neurosci 11 1007 1013

12. HuHGrandlJBandellMPetrusMPatapoutianA 2009 Two amino acid residues determine 2-APB sensitivity of the ion channels TRPV3 and TRPV4. Proc Natl Acad Sci U S A 106 1626 1631

13. ChungMKLeeHMizunoASuzukiMCaterinaMJ 2004 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J Neurosci 24 5177 5182

14. HuHZGuQWangCColtonCKTangJ 2004 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279 35741 35748

15. FelsensteinJ 1985 Confidence-Limits on Phylogenies - an Approach Using the Bootstrap. Evolution 39 783 791

16. JonesDTTaylorWRThorntonJM 1992 The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8 275 282

17. RzhetskyANeiM 1992 A Simple Method for Estimating and Testing Minimum-Evolution Trees. Molecular Biology and Evolution 9 945 967

18. Vogt-EiseleAKWeberKSherkheliMAVielhaberGPantenJ 2007 Monoterpenoid agonists of TRPV3. Br J Pharmacol 151 530 540

19. MacphersonLJHwangSWMiyamotoTDubinAEPatapoutianA 2006 More than cool: promiscuous relationships of menthol and other sensory compounds. Mol Cell Neurosci 32 335 343

20. TaylorJSBraaschIFrickeyTMeyerAVan de PeerY 2003 Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res 13 382 390

21. GrachevaEOIngoliaNTKellyYMCordero-MoralesJFHollopeterG 2010 Molecular basis of infrared detection by snakes. Nature 464 1006 1011

22. ViswanathVStoryGMPeierAMPetrusMJLeeVM 2003 Opposite thermosensor in fruitfly and mouse. Nature 423 822 823

23. BautistaDMJordtSENikaiTTsurudaPRReadAJ 2006 TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124 1269 1282

24. JordtSEBautistaDMChuangHHMcKemyDDZygmuntPM 2004 Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 260 265

25. KarashimaYTalaveraKEveraertsWJanssensAKwanKY 2009 TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci U S A 106 1273 1278

26. KwanKYAllchorneAJVollrathMAChristensenAPZhangDS 2006 TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50 277 289

27. StoryGMPeierAMReeveAJEidSRMosbacherJ 2003 ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 819 829

28. BrauchiSOrtaGSalazarMRosenmannELatorreR 2006 A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J Neurosci 26 4835 4840

29. VlachovaVTeisingerJSusankovaKLyfenkoAEttrichR 2003 Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J Neurosci 23 1340 1350

30. NeeperMPLiuYHutchinsonTLWangYFloresCM 2007 Activation properties of heterologously expressed mammalian TRPV2: evidence for species dependence. J Biol Chem 282 15894 15902

31. MandadiSSokabeTShibasakiKKatanosakaKMizunoA 2009 TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch 458 1093 1102

32. LeeHCaterinaMJ 2005 TRPV channels as thermosensory receptors in epithelial cells. Pflugers Arch 451 160 167

33. HirschNZimmermanLBGraingerRM 2002 Xenopus, the next generation: X. tropicalis genetics and genomics. Dev Dyn 225 422 433

34. KashiwagiKKashiwagiAKurabayashiAHanadaHNakajimaK 2010 Xenopus tropicalis: an ideal experimental animal in amphibia. Exp Anim 59 395 405

35. KhokhaMKChungCBustamanteELGawLWTrottKA 2002 Techniques and probes for the study of Xenopus tropicalis development. Dev Dyn 225 499 510

36. RosenblumEBPoortenTJSettlesMMurdochGKRobertJ 2009 Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS ONE 4 e6494 doi:10.1371/journal.pone.0006494

37. MyersBRSigalYMJuliusD 2009 Evolution of thermal response properties in a cold-activated TRP channel. PLoS ONE 4 e5741 doi:10.1371/journal.pone.0005741

38. ThompsonJDHigginsDGGibsonTJ 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22 4673 4680

39. TamuraKDudleyJNeiMKumarS 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 1596 1599

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