Eur. J. Entomol. 113: 315-319, 2016 | 10.14411/eje.2016.040

Capsazepine affects thermal preferences of the American cockroach (Blattodea: Blattidae)

Justyna MALISZEWSKA, Eugenia T╩GOWSKA
Department of Animal Toxicology, Faculty of Biology and Environment Protection, Nicolaus Copernicus University, ul. Lwowska 1, 87-100 Toru˝, Poland; e-mails: ojustyna@umk.pl, tegowska@umk.pl

Capsazepine is a competitive antagonist of capsaicin, a TRPV1 agonist responsible for the spicy taste of pepper. TRPV1 agonists and antagonists are known to affect mammalian body temperature, but their action on thermoregulation in insects is poorly known. In this study we evaluated the effect of capsazepine on the thermal preference of the American cockroach, Periplaneta americana using a thermal gradient. Our results revealed that capsazepine in submicromolar concentrations induces a preference for higher ambient temperatures when compared to the control insects. To assess whether capsazepine may act also as an antagonist of capsaicin in insects, we determined this insects' thermal behaviour when capsazepine was applied before capsaicin. The hypothermic response to capsaicin was clearly blocked by pre-treatment with capsazepine only in female American cockroaches. Our results indicate the involvement of structures functionally similar to TRPV1 in insect thermosensation.

Keywords: Blattodea, Blattidae, American cockroach, behavioural thermoregulation, capsaicin, capsazepine, TRPV

Received: February 1, 2016; Accepted: March 14, 2016; Published online: April 21, 2016

Download citation

References

  1. Al-Anzi B., Tracey W.D. Jr & Benzer S. 2006: Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANTKM. - Curr. Biol. 16: 1034-1040. Go to original source...
  2. Bell W.J., Roth L.M. & Nalepa C.A. 2007: Cockroaches: Ecology, Behavior, and Natural History. The Johns Hopkins University Press, Baltimore, 230 pp.
  3. Bevan S., Hothi S., Hughes G., James I.F., Rang H.P., Shah K., Walpole C.S.J. & Yeats J.C. 1992: Capsazepine: a competitive antagonist of the sensory neurone excitant capsaicin. - Br. J. Pharmacol. 107: 544-552. Go to original source...
  4. Caterina M.J. 2007: Transient receptor potential ion channels as participants in thermosensation and thermoregulation. - Am. J. Physiol. Regul. Integr. Comp. Physiol. 292: 64-76. Go to original source...
  5. 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. Go to original source...
  6. Dillon M.E., Wang G., Garrity P.A. & Huey R.B. 2009: Review: thermal preference in Drosophila. - J. Therm. Biol. 34: 109-119. Go to original source...
  7. Docherty R.J., Yeats J.C. & Piper A.S. 1997: Capsazepine block of voltage-activated calcium channels in adult rat dorsal root ganglion neurones in culture. - Br. J. Pharmacol. 121: 1461-1467. Go to original source...
  8. Dogan M.D., Patel S., Rudaya A.Y., Steiner A.A., SzÚkely M. & Romanovsky A.A. 2004: Lipopolysaccharide fever is initiated via a capsaicin-sensitive mechanism independent of the subtype-1 vanilloid receptor. - Br. J. Pharmacol. 143: 1023-1032. Go to original source...
  9. Forsman A. 2000: Some like it hot: intra-population variation in behavioral thermoregulation in color-polymorphic pygmy grasshoppers. - Evol. Ecol. 14: 25-38. Go to original source...
  10. French A.S., Meisner S., Liu H., Weckstr÷m M. & Torkkeli P.H. 2015: Transcriptome analysis and RNA interference of cockroach phototransduction indicate three opsins and suggest a major role for TRPL channels. - Front. Physiol. 6: 207. Go to original source...
  11. Gallio M., Ofstad T.A., Macpherson L.J., Wang J.W. & Zuker C.S. 2011: The coding of temperature in the Drosophila brain. - Cell 144: 614-624. Go to original source...
  12. Gau P., Poon J., Ufret-Vincenty C., Snelson C.D., Gordon S.E., Raible D.W. & Dhaka A. 2013: The zebrafish ortholog of TRPV1 is required for heat-induced locomotion. - J. Neurosci. 33: 5249-5260. Go to original source...
  13. Gavva N.R., Bannon A.W., Surapaneni S., Hovland D.N., Lehto S.G., Gore A., Juan T., Deng H., Han B., Klionsky L., Kuang R., Le A., Tamir R., Wang J., Youngblood B., Zhu D., Norman M.H., Magal E., Treanor J.J. & Louis J.C. 2007: The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. - J. Neurosci. 27: 3366-3374. Go to original source...
  14. Gong Z., Son W., Chung Y.D., Kim J., Shin D.W., McClung C.A., Lee Y., Lee H., Chung D.J., Kaang B.K., Cho H., Oh U., Hirsh J., Kernan M.J. & Kim C. 2004: Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. - J. Neurosci. 24: 9059-9066. Go to original source...
  15. Jordt S.E. & Julius D. 2000: Molecular basis for species-species sensitivity to "hot" chili peppers. - Cell 108: 421-430. Go to original source...
  16. Kim J., Chung Y.D., Park D., Choi S., Shin D.W., Soh H., Lee H.W., Son W., Yim J., Park C.S., Kernan M.J. & Kim C. 2003: A TRPV family ion channel required for hearing in Drosophila. - Nature 424: 81-84. Go to original source...
  17. Kwon Y., Shen W.L., Shim H.S. & Montell C. 2010. Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. - J. Neurosci. 30: 10465-10471. Go to original source...
  18. Lee Y., Lee Y., Lee J., Bang S., Hyun S., Kang J., Hong S.T., Bae E., Kaang B.K. & Kim J. 2005: Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. - Nature Gen. 37: 305-310. Go to original source...
  19. Lundbæk J.A., Birn P., Tape S.E., Toombes G.E.S., Søgaard R., Koeppe II R.E., Gruner S.M., Hansen A.J. & Andersen O.S. 2005: Capsaicin regulates voltage-dependent sodium channels by altering lipid bilayer elasticity. - Mol. Pharmacol. 68: 680-689. Go to original source...
  20. McCllelan-Green P., Romano J. & Oberd÷rster E. 2007: Does gender really matter in contaminant exposure? A case study using invertebrate models. - Environ. Res. 104: 183-191. Go to original source...
  21. McIntyre P., McLatchie L.M., Chambers A., Phillips E., Clarke M., Savidge J., Toms C., Paecock M., Shah K., Winter J., Weerasakera N., Webb N., 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. Go to original source...
  22. Ohkita M., Saito S., Imigawa 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. Go to original source...
  23. Olszewska J. & Tŕgowska E. 2011: Opposite effect of capsaicin and capsazepine on behavioral thermoregulation in insects. - J. Comp. Physiol. (A) 197: 1021-1026. Go to original source...
  24. Romanovsky A.A., Almeida M.C., Garami A., Steiner A.A., Norman M.H., Morrison S.F., Nakamura K., Burmeister J.J. & Nucci T.B. 2009: The transient receptor potential vanilloid-1 channel in thermoregulation: a thermosensor it is not. - Pharmacol. Rev. 61: 228-261. Go to original source...
  25. Rosenzweig M., Kang K. & Garrity P.A. 2008: Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. - Proc. Natl. Acad. Sci. U.S.A. 105: 14668-14673. Go to original source...
  26. Seelinger G. 1984: Sex-specific activity patterns in Periplaneta americana and their relation to mate-finding. - Z. Tierpsychol. 65: 309-326. Go to original source...
  27. 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. Go to original source...
  28. Spurr E.B. & McGregor P.G. 2003: Potential invertebrate antifeedants for toxic baits used for vertebrate pest control. - Sci. Conserv. 232: 13.
  29. Tracey D.W. Jr, Wilson R.I., Laurent G. & Benzer S. 2003: painless, a Drosophila gene essential for nociception. - Cell 113: 261-273. Go to original source...
  30. Wicher D., Agricola H.J., Sch÷ner R., Heinemann S.H. & Derst C. 2006: TRPγ channels are inhibited by cAMP and contribute to pacemaking in neurosecretory insect neurons. - J. Biol. Chem. 281: 322-326. Go to original source...
  31. Zermoglio P.F., Latorre-Estivalis J.M., Crespo J.E., Lorenzo M.G. & Lazzari C.R. 2015: Thermosensation and TRPV channel in Rhodnius prolixus. - J. Insect Physiol. 81: 145-156. Go to original source...