Species differences and molecular determinant of TRPA1 cold sensitivity

Abstract

TRPA1 is an ion channel and has been proposed as a thermosensor across species. In invertebrate and ancestral vertebrates such as fly, mosquito, frog, lizard and snakes, TRPA1 serves as a heat receptor, a sensory input utilized for heat avoidance or infrared detection. However, in mammals, whether TRPA1 is a receptor for noxious cold is highly controversial, as channel activation by cold was observed by some groups but disputed by others. Here we attribute the discrepancy to species differences. We show that cold activates rat and mouse TRPA1 but not human or rhesus monkey TRPA1. At the molecular level, a single residue within the S5 transmembrane domain (G878 in rodent but V875 in primate) accounts for the observed difference in cold sensitivity. This residue difference also underlies the species-specific effects of menthol. Together, our findings identify the species-specific cold activation of TRPA1 and reveal a molecular determinant of cold-sensitive gating.

References 40

1. 1.

   Bandell M.. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849–857 (2004 ).

   Not in our library10.1016/s0896-6273(04)00150-3

2. 2.

   Bautista D. M.. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269–1282 (2006 ).

   Not in our library10.1016/j.cell.2006.02.023

3. 3.

   Jordt S. E.. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260–265 (2004 ).

   Not in our library10.1038/nature02282

4. 4.

   Andersson D. A., Gentry C., Moss S. & Bevan S. Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J. Neurosci. 28, 2485–2494 (2008 ).

   Not in our library10.1523/jneurosci.5369-07.2008

5. 5.

   Trevisani M.. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc. Natl Acad. Sci. USA 104, 13519–13524 (2007 ).

   Not in our library10.1073/pnas.0705923104

6. 6.
   A Gain-of-Function Mutation in TRPA1 Causes Familial Episodic Pain Syndrome · 2010

   No notice
7. 7.

   Kwan K. Y.. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50, 277–289 (2006 ).

   Not in our library10.1016/j.neuron.2006.03.042

8. 8.

   Story G. M.. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819–829 (2003 ).

   Not in our library10.1016/s0092-8674(03)00158-2

9. 9.

   Obata K.. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J. Clin. Invest. 115, 2393–2401 (2005 ).

   Not in our library10.1172/jci25437

10. 10.

    Bessac B. F.. TRPA1 is a major oxidant sensor in murine airway sensory neurons. J. Clin. Invest. 118, 1899–1910 (2008 ).

    Not in our library10.1172/jci34192

11. 11.

    Caspani O. & Heppenstall P. A. TRPA1 and cold transduction: an unresolved issue? J. Gen. Physiol. 133, 245–249 (2009 ).

    Not in our library10.1085/jgp.200810136

12. 12.

    Kwan K. Y. & Corey D. P. Burning cold: involvement of TRPA1 in noxious cold sensation. J. Gen. Physiol. 133, 251–256 (2009 ).

    Not in our library10.1085/jgp.200810146

13. 13.

    del Camino D.. TRPA1 contributes to cold hypersensitivity. J. Neurosci. 30, 15165–15174 (2010 ).

    Not in our library10.1523/jneurosci.2580-10.2010

14. 14.

    Karashima Y.. TRPA1 acts as a cold sensor in vitro and in vivo. Proc. Natl Acad. Sci. USA 106, 1273–1278 (2009 ).

    Not in our library10.1073/pnas.0808487106

15. 15.

    Sawada Y., Hosokawa H., Hori A., Matsumura K. & Kobayashi S. Cold sensitivity of recombinant TRPA1 channels. Brain Res. 1160, 39–46 (2007 ).

    Not in our library10.1016/j.brainres.2007.05.047

16. 16.

    Cordero-Morales J. F., Gracheva E. O. & Julius D. Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc. Natl Acad. Sci. USA 108, E1184–E1191 (2011 ).

    Not in our library10.1073/pnas.1114124108

17. 17.

    Zurborg S., Yurgionas B., Jira J. A., Caspani O. & Heppenstall P. A. Direct activation of the ion channel TRPA1 by Ca2+. Nat. Neurosci. 10, 277–279 (2007 ).

    Not in our library10.1038/nn1843

18. 18.

    Knowlton W. M., Bifolck-Fisher A., Bautista D. M. & McKemy D. D. TRPM8, but not TRPA1, is required for neural and behavioral responses to acute noxious cold temperatures and cold-mimetics in vivo. Pain 150, 340–350 (2010 ).

    Not in our library10.1016/j.pain.2010.05.021

19. 19.

    Gracheva E. O.. Molecular basis of infrared detection by snakes. Nature 464, 1006–1011 (2010 ).

    Not in our library10.1038/nature08943

20. 20.

    Kang K.. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481, 76–80 (2012 ).

    Not in our library10.1038/nature10715

21. 21.

    Viswanath V.. Opposite thermosensor in fruitfly and mouse. Nature 423, 822–823 (2003 ).

    Not in our library10.1038/423822a

22. 22.

    Saito S.. 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 (2012 ).

    Not in our library10.1074/jbc.m112.362194

23. 23.

    Kwon Y., Shim H. S., Wang X. & Montell C. Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat. Neurosci. 11, 871–873 (2008 ).

    Not in our library10.1038/nn.2170

24. 24.

    Chen J.. Molecular determinants of species-specific activation or blockade of TRPA1 channels. J. Neurosci. 28, 5063–5071 (2008 ).

    Not in our library10.1523/jneurosci.0047-08.2008

25. 25.

    Nagatomo K., Ishii H., Yamamoto T., Nakajo K. & Kubo Y. The Met268Pro mutation of mouse TRPA1 changes the effect of caffeine from activation to suppression. Biophys. J. 99, 3609–3618 (2010 ).

    Not in our library10.1016/j.bpj.2010.10.014

26. 26.

    Xiao B.. Identification of transmembrane domain 5 as a critical molecular determinant of menthol sensitivity in mammalian TRPA1 channels. J. Neurosci. 28, 9640–9651 (2008 ).

    Not in our library10.1523/jneurosci.2772-08.2008

27. 27.

    Grandl J.. Pore region of TRPV3 ion channel is specifically required for heat activation. Nat. Neurosci. 11, 1007–1013 (2008 ).

    Not in our library10.1038/nn.2169

28. 28.

    Chen J.. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation. Pain 152, 1165–1172 (2011 ).

    Not in our library10.1016/j.pain.2011.01.049

29. 29.

    Bianchi B. R.. Species comparison and pharmacological characterization of human, monkey, rat, and mouse TRPA1 channels. J. Pharmacol. Exp. Ther. 341, 360–368 (2012 ).

    Not in our library10.1124/jpet.111.189902

30. 30.

    Karashima Y.. Bimodal action of menthol on the transient receptor potential channel TRPA1. J. Neurosci. 27, 9874–9884 (2007 ).

    Not in our library10.1523/jneurosci.2221-07.2007

31. 31.

    Nagata K., Duggan A., Kumar G. & Garcia-Anoveros J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25, 4052–4061 (2005 ).

    Not in our library10.1523/jneurosci.0013-05.2005

32. 32.

    Kang K.. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464, 597–600 (2010 ).

    Not in our library10.1038/nature08848

33. 33.

    Kim S. H.. Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc. Natl Acad. Sci. USA 107, 8440–8445 (2010 ).

    Not in our library10.1073/pnas.1001425107

34. 34.

    Gracheva E. O.. Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 476, 88–91 (2011 ).

    Not in our library10.1038/nature10245

35. 35.

    Grandl J.. Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat. Neurosci. 13, 708–714 (2010 ).

    Not in our library10.1038/nn.2552

36. 36.

    Yang F., Cui Y., Wang K. & Zheng J. Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc. Natl Acad. Sci. USA 107, 7083–7088 (2010 ).

    Not in our library10.1073/pnas.1000357107

37. 37.

    Yao J., Liu B. & Qin F. Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. Proc. Natl Acad. Sci. USA 108, 11109–11114 (2011 ).

    Not in our library10.1073/pnas.1105196108

38. 38.

    Brauchi S., Orta G., Salazar M., Rosenmann E. & Latorre R. A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J. Neurosci. 26, 4835–4840 (2006 ).

    Not in our library10.1523/jneurosci.5080-05.2006

39. 39.

    Wang H., Schupp M., Zurborg S. & Heppenstall P. A. Residues in the pore region of Drosophila transient receptor potential A1 dictate sensitivity to thermal stimuli. J. Physiol. 591, 185–201 (2013 ).

    Not in our library10.1113/jphysiol.2012.242842

40. 40.

    Chen J. & Kym P. R. TRPA1: the species difference. J. Gen. Physiol. 133, 623–625 (2009 ).

    Not in our library10.1085/jgp.200910246

Cited by papers we hold 3

• Neural Mechanisms of Inflammation-Induced Fever · 2018
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• Human TRPA1 is a heat sensor displaying intrinsic U-shaped thermosensitivity · 2016
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• TRPA1 as a drug target—promise and challenges · 2015
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