in

TRPM8 thermosensation in poikilotherms mediates both skin colour and locomotor performance responses to cold temperature

  • Lovegrove, B. G. A phenology of the evolution of endothermy in birds and mammals. Biol. Rev. 92, 1213–1240 (2017).

    Google Scholar 

  • Cuthill, I. C. et al. The biology of color. Science 357, 1–7 (2017).

    Google Scholar 

  • Stuart-Fox, D., Newton, E. & Clusella-Trullas, S. Thermal consequences of colour and near-infrared reflectance. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160345 (2017).

    Google Scholar 

  • Smith, K. R. et al. Color change for thermoregulation versus camouflage in free-ranging lizards. Am. Nat. 188, 668–678 (2016).

    Google Scholar 

  • Rudh, A. & Qvarnström, A. Adaptive colouration in amphibians. Semin. Cell Dev. Biol. 24, 553–561 (2013).

    Google Scholar 

  • Geen, M. R. S. & Johnston, G. R. Coloration affects heating and cooling in three color morphs of the Australian bluetongue lizard, Tiliqua scincoides. J. Therm. Biol. 43, 54–60 (2014).

    Google Scholar 

  • Tattersall, G. J., Eterovick, P. C. & de Andrade, D. V. Tribute to R. G. Boutilier: skin colour and body temperature changes in basking Bokermannohyla alvarengai (Bokermann 1956). J. Exp. Biol. 209, 1185–1196 (2006).

    Google Scholar 

  • Tattersall, G. J., Hillman, S. S., Drewes, R. C. & Sokol, O. M. The thermogenesis of digestion in rattlesnakes. J. Exp. Biol. 207, 579–585 (2004).

    Google Scholar 

  • Seebacher, F. & Murray, S. A. Transient receptor potential ion channels control thermoregulatory behaviour in reptiles. PLoS One 2, e281, 1–7 (2007).

  • Forget-Klein, É. & Green, D. M. Toads use the subsurface thermal gradient for temperature regulation underground. J. Therm. Biol. 99, 1–9 (2021).

    Google Scholar 

  • Kiefer, M. C., Van Sluys, M. & Rocha, C. F. D. Thermoregulatory behaviour in Tropidurus torquatus (Squamata, Tropiduridae) from Brazilian coastal populations: an estimate of passive and active thermoregulation in lizards. Acta Zool. 88, 81–87 (2007).

    Google Scholar 

  • Spencer, K. et al. Growth at cold temperature increases the number of motor neurons to optimize locomotor function. Curr. Biol. 29, 1787–1799.e5 (2019).

    CAS 

    Google Scholar 

  • Herrel, A. & Bonneaud, C. Temperature dependence of locomotor performance in the tropical clawed frog, Xenopus tropicalis. J. Exp. Biol. 215, 2465–2470 (2012).

    Google Scholar 

  • Casterlin, M. E. & Reynolds, W. W. Diel activity and thermoregulatory behavior of a fully aquatic frog: Xenopus laevis. Hydrobiologia 75, 189–191 (1980).

    Google Scholar 

  • Guo, K. et al. The thermal dependence and molecular basis of physiological color change in Takydromus septentrionalis (Lacertidae). Biol. Open 10, 1–9 (2021).

    Google Scholar 

  • De Velasco, J. B. & Tattersall, G. J. The influence of hypoxia on the thermal sensitivity of skin colouration in the bearded dragon, Pogona vitticeps. J. Comp. Physiol. B. 178, 867–875 (2008).

    CAS 

    Google Scholar 

  • Stuart-Fox, D. & Moussalli, A. Camouflage, communication and thermoregulation: lessons from colour changing organisms. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 463–470 (2009).

    Google Scholar 

  • Sanabria, E. A., Vaira, M., Quiroga, L. B., Akmentins, M. S. & Pereyra, L. C. Variation of thermal parameters in two different color morphs of a diurnal poison toad, Melanophryniscus rubriventris (Anura: Bufonidae). J. Therm. Biol. 41, 1–5 (2014).

    Google Scholar 

  • Clusella-Trullas, S., van Wyk, J. H. & Spotila, J. R. Thermal benefits of melanism in cordylid lizards: a theoretical and field test. Ecology 90, 2297–2312 (2009).

    Google Scholar 

  • Duarte, R. C., Flores, A. A. V. & Stevens, M. Camouflage through colour change: mechanisms, adaptive value and ecological significance. Philos. Trans. R. Soc. B: Biol. Sci. 372, 1–7 (2017).

  • Bertolesi, G. E. & McFarlane, S. Seeing the light to change colour: an evolutionary perspective on the role of melanopsin in neuroendocrine circuits regulating light-mediated skin pigmentation. Pigment Cell Melanoma Res. 31, 354–373 (2018).

    CAS 

    Google Scholar 

  • Bertolesi, G. E. et al. The regulation of skin pigmentation in response to environmental light by pineal type II opsins and skin melanophore melatonin receptors. J. Photochem. Photobiol. B Biol. 212, 112024 (2020).

    CAS 

    Google Scholar 

  • Bagnara, J. T. Pineal regulation of the body lightening reaction in amphibian larvae. Sci. (80-.). 132, 1481–1483 (1960).

    CAS 

    Google Scholar 

  • Bertolesi, G. E., Song, Y. N., Atkinson-Leadbeater, K., Yang, J.-L. J. & McFarlane, S. Interaction and developmental activation of two neuroendocrine systems that regulate light-mediated skin pigmentation. Pigment Cell Melanoma Res. 30, 413–423 (2017).

    CAS 

    Google Scholar 

  • Wang, H. & Siemens, J. TRP ion channels in thermosensation, thermoregulation and metabolism. Temp. (Austin, Tex.) 2, 178–187 (2015).

    Google Scholar 

  • Hoffstaetter, L. J., Bagriantsev, S. N. & Gracheva, E. O. TRPs et al.: a molecular toolkit for thermosensory adaptations. Pflug. Arch. Eur. J. Physiol. 470, 745–759 (2018).

    CAS 

    Google Scholar 

  • Kashio, M. Thermosensation involving thermo-TRPs. Mol. Cell. Endocrinol. 520, 1–8 (2021).

    Google Scholar 

  • Señarís, R., Ordás, P., Reimúndez, A. & Viana, F. Mammalian cold TRP channels: impact on thermoregulation and energy homeostasis. Pflug. Arch. 470, 761–777 (2018).

    Google Scholar 

  • Guo, H., Carlson, J. A. & Slominski, A. Role of TRPM in melanocytes and melanoma. Exp. Dermatol. 21, 650–654 (2012).

    CAS 

    Google Scholar 

  • Kadowaki, T. Evolutionary dynamics of metazoan TRP channels. Pflug. Arch. 467, 2043–2053 (2015).

    CAS 

    Google Scholar 

  • Saito, S. & Tominaga, M. Evolutionary tuning of TRPA1 and TRPV1 thermal and chemical sensitivity in vertebrates. Temp. (Austin, Tex.) 4, 141–152 (2017).

    Google Scholar 

  • Saito, S. et al. 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).

    CAS 

    Google Scholar 

  • Saito, S. et al. Evolution of heat sensors drove shifts in thermosensation between xenopus species adapted to different thermal niches. J. Biol. Chem. 291, 11446–11459 (2016).

    CAS 

    Google Scholar 

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

    CAS 

    Google Scholar 

  • Laursen, W. J., Anderson, E. O., Hoffstaetter, L. J., Bagriantsev, S. N. & Gracheva, E. O. Species-specific temperature sensitivity of TRPA1. Temp. (Austin, Tex.) 2, 214–226 (2015).

    Google Scholar 

  • Bertolesi, G. E., Hehr, C. L. & McFarlane, S. Melanopsin photoreception in the eye regulates light-induced skin colour changes through the production of α-MSH in the pituitary gland. Pigment Cell Melanoma Res. 28, 559–571 (2015).

    CAS 

    Google Scholar 

  • Bagnara, J. T. The pineal and the body lightening reaction of larval amphibians. Gen. Comp. Endocrinol. 3, 86–100 (1963).

    CAS 

    Google Scholar 

  • Nisembaum, L. et al. In the heat of the night: thermo-TRPV channels in the salmonid pineal photoreceptors and modulation of melatonin secretion. Endocrinology 156, 4629–4638 (2015).

    CAS 

    Google Scholar 

  • Schartl, M. et al. What is a vertebrate pigment cell? Pigment Cell Melanoma Res. 29, 8–14 (2016).

    Google Scholar 

  • Slominski, A. Cooling skin cancer: menthol inhibits melanoma growth. Focus on ‘TRPM8 activation suppresses cellular viability in human melanoma’. Am. J. Physiol. – Cell Physiol. 295, C293–C295 (2008).

    CAS 

    Google Scholar 

  • Yamamura, H., Ugawa, S., Ueda, T., Morita, A. & Shimada, S. TRPM8 activation suppresses cellular viability in human melanoma. Am. J. Physiol. Cell Physiol. 295, C296–C301 (2008).

    CAS 

    Google Scholar 

  • Knowlton, W. M. et al. A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. J. Neurosci. 33, 2837–2848 (2013).

    CAS 

    Google Scholar 

  • Weyer-Menkhoff, I., Pinter, A., Schlierbach, H., Schänzer, A. & Lötsch, J. Epidermal expression of human TRPM8, but not of TRPA1 ion channels, is associated with sensory responses to local skin cooling. Pain 160, 2699–2709 (2019).

  • Kumasaka, M., Sato, S., Yajima, I. & Yamamoto, H. Isolation and developmental expression of tyrosinase family genes in Xenopus laevis. Pigment Cell Res. 16, 455–462 (2003).

    CAS 

    Google Scholar 

  • Rodionov, V. I., Hope, A. J., Svitkina, T. M. & Borisy, G. G. Functional coordination of microtubule-based and actin-based motility in melanophores. Curr. Biol. 8, 165–169 (1998).

    CAS 

    Google Scholar 

  • Session, A. M. et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature 538, 336–343 (2016).

    CAS 

    Google Scholar 

  • Gosset, J. R. et al. A cross-species translational pharmacokinetic-pharmacodynamic evaluation of core body temperature reduction by the TRPM8 blocker PF-05105679. Eur. J. Pharm. Sci. 109S, S161–S167 (2017).

    Google Scholar 

  • Winchester, W. J. et al. Inhibition of TRPM8 channels reduces pain in the cold pressor test in humans. J. Pharmacol. Exp. Ther. 351, 259–269 (2014).

    Google Scholar 

  • Bianchi, B., Smith, P. A. & Abriel, H. The ion channel TRPM4 in murine experimental autoimmune encephalomyelitis and in a model of glutamate-induced neuronal degeneration. Mol. Brain 11, 1–10 (2018).

    Google Scholar 

  • Li, K., Shi, Y., Gonye, E. C. & Bayliss, D. A. TRPM4 contributes to subthreshold membrane potential oscillations in multiple mouse pacemaker neurons. eNeuro 8, 1–13 (2021).

    Google Scholar 

  • Dong, W. et al. Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum. J. Neurophysiol. 101, 803–815 (2009).

    Google Scholar 

  • Bertolesi, G. E., Debnath, N., Atkinson-Leadbeater, K., Niedzwiecka, A. & McFarlane, S. Distinct type II opsins in the eye decode light properties for background adaptation and behavioural background preference. Mol. Ecol. 30, 6659–6676 (2021).

    CAS 

    Google Scholar 

  • Viczian, A. S. & Zuber, M. E. A simple behavioral assay for testing visual function in xenopus laevis. J. Vis. Exp. 12, 51726 (2014).

    Google Scholar 

  • Myers, B. R., Sigal, Y. M. & Julius, D. Evolution of thermal response properties in a cold-activated TRP channel. PLoS One 4, e5741 (2009).

    Google Scholar 

  • Furman, B. L. S. et al. Pan-African phylogeography of a model organism, the African clawed frog ‘Xenopus laevis’. Mol. Ecol. 24, 909–925 (2015).

    CAS 

    Google Scholar 

  • Wilson, R. S., James, R. S. & Johnston, I. A. Thermal acclimation of locomotor performance in tadpoles and adults of the aquatic frog Xenopus laevis. J. Comp. Physiol. B. 170, 117–124 (2000).

    CAS 

    Google Scholar 

  • Kashiwagi, K. et al. Xenopus tropicalis: an ideal experimental animal in amphibia. Exp. Anim. 59, 395–405 (2010).

    CAS 

    Google Scholar 

  • Martínez-Freiría, F., Toyama, K. S., Freitas, I. & Kaliontzopoulou, A. Thermal melanism explains macroevolutionary variation of dorsal pigmentation in Eurasian vipers. Sci. Rep. 10, 72871–1 (2020).

  • Tanaka, K. Does the thermal advantage of melanism produce size differences in color-dimorphic snakes? Zool. Sci. 26, 698–703 (2009).

    Google Scholar 

  • Moreno Azócar, D. L., Nayan, A. A., Perotti, M. G. & Cruz, F. B. How and when melanic coloration is an advantage for lizards: the case of three closely-related species of Liolaemus. Zool. (Jena.) 141, 125774 (2020).

    Google Scholar 

  • Azócar, D. L. M. et al. Effect of body mass and melanism on heat balance in Liolaemus lizards of the goetschi clade. J. Exp. Biol. 219, 1162–1171 (2016).

    Google Scholar 

  • Smith, K. R. et al. Colour change on different body regions provides thermal and signalling advantages in bearded dragon lizards. Proc. R. Soc. B Biol. Sci. 283, 20160626 (2016).

    Google Scholar 

  • Rowe, J. W. et al. Thermal and substrate color-induced melanization in laboratory reared red-eared sliders (Trachemys scripta elegans). J. Therm. Biol. 61, 125–132 (2016).

    Google Scholar 

  • Larsen, E. H. Dual skin functions in amphibian osmoregulation. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 253, 110869 (2021).

    CAS 

    Google Scholar 

  • Franco-Belussi, L., Sköld, H. N. & De Oliveira, C. Internal pigment cells respond to external UV radiation in frogs. J. Exp. Biol. 219, 1378–1383 (2016).

    Google Scholar 

  • Langhelle, A., Lindell, M. J. & Nyström, P. Effects of ultraviolet radiation on amphibian embryonic and larval development. J. Herpetol. 33, 449–456 (1999).

    Google Scholar 

  • Mueller, K. P. & Neuhauss, S. C. F. Sunscreen for fish: co-option of UV light protection for camouflage. PLoS One 9, e87372 (2014).

    Google Scholar 

  • Perotti, M. G., Diéguez, M. & Del, C. Effect of UV-B exposure on eggs and embryos of patagonian anurans and evidence of photoprotection. Chemosphere 65, 2063–2070 (2006).

    CAS 

    Google Scholar 

  • Nilsson Sköld, H., Aspengren, S. & Wallin, M. Rapid color change in fish and amphibians – function, regulation, and emerging applications. Pigment Cell Melanoma Res. 26, 29–38 (2013).

    Google Scholar 

  • Vences, M. et al. Field body temperatures and heating rates in a montane frog population: the importance of black dorsal pattern for thermoregulation on JSTOR. Ann. Zool. Fennici 39, 209–220 (2002).

    Google Scholar 

  • Lindgren, J. et al. Skin pigmentation provides evidence of convergent melanism in extinct marine reptiles. Nature 506, 484–488 (2014).

    CAS 

    Google Scholar 

  • Bonino, M. F., Cruz, F. B. & Perotti, M. G. Does temperature at local scale explain thermal biology patterns of temperate tadpoles? J. Therm. Biol. 94, 102744 (2020).

    Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).

    CAS 

    Google Scholar 

  • Liu, T. et al. RNA interference-mediated depletion of TRPM8 enhances the efficacy of epirubicin chemotherapy in prostate cancer LNCaP and PC3 cells. Oncol. Lett. 15, 4129–4136 (2018).

    Google Scholar 

  • Kashina, A. S. et al. Protein Kinase A, which regulates intracellular transport, forms complexes with molecular motors on organelles. Curr. Biol. 14, 1877–1881 (2004).

    CAS 

    Google Scholar 


  • Source: Ecology - nature.com

    Chess players face a tough foe: air pollution

    To decarbonize the chemical industry, electrify it