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TRPA1 expression provides new insights into thermal perception by the sea urchin Strongylocentrotus intermedius

Published online by Cambridge University Press:  21 October 2019

Jingyun Ding ,
Yushi Yu ,
Mingfang Yang ,
Dongtao Shi ,
Zequn Li ,
Xiaomei Chi ,
Yaqing Chang ,
Qingzhi Wang  and
Chong Zhao Open the ORCID record for Chong Zhao [Opens in a new window]
Jingyun Ding
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Yushi Yu
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Mingfang Yang
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Dongtao Shi
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Zequn Li
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Xiaomei Chi
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Yaqing Chang
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
Qingzhi Wang*
Affiliation:
Liaoning Ocean and Fisheries Science Research Institute, Dalian, 116023, China
Chong Zhao*
Affiliation:
Key Laboratory of Mariculture & Stock Enhancement in North China's Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian, 116023, China
*
Author for correspondence: Chong Zhao, E-mail: [email protected] and Qingzhi Wang, E-mail: [email protected]
Author for correspondence: Chong Zhao, E-mail: [email protected] and Qingzhi Wang, E-mail: [email protected]
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Abstract

Thermal perception is crucial for the fitness of marine invertebrates in intertidal and shallow waters. TRPA1 is a non-selective cation channel that belongs to the TRP family with pivotal roles in initiating signal transduction of thermal perception. We investigated expression patterns of SiTRPA1 in different tissues (tube feet, coelomocytes, gonads and gut) of the sea urchin Strongylocentrotus intermedius. SiTRPA1 expression patterns under acute and long-term temperature stimuli were investigated in tube feet of sea urchins. In the present study, the highest expression of SiTRPA1 was detected in tube feet of S. intermedius. The SiTRPA1 expression level in tube feet were significantly 235.7-fold, 450.0-fold and 3299.7-fold higher than those in the coelomocytes, gonads and gut (df = 3, F = 47.382, P < 0.001). Expression levels of SiTRPA1 in the other tissues (coelomocytes, gonads and gut) were not significantly different (df = 3, F = 47.382, P = 0.972). There was no significant difference of SiTRPA1 expression among all groups in the acute temperature increase experiment (df = 4, F = 0.25, P = 0.902). In the acute temperature decrease experiment, the expression of SiTRPA1 showed no significant difference among all groups (df = 4, F = 1.802, P = 0.205). With long-term exposure (6 weeks) to different temperatures, SiTRPA1 expression in the low temperature group (10°C) was significantly higher than those in the high temperature (20°C) and the control groups (15°C) (df = 2, F = 9.57, P = 0.014). There was no significant difference of SiTRPA1 expression between the high temperature (20°C) and the control temperature (15°C) groups (df = 2, F = 9.57, P = 0.808). These results indicate that SiTRPA1 expression significantly responds to long-term low temperature but not to acute temperature decrease. The present study provides new insights on the distribution and temporal expression of TRPA1 in marine invertebrates after acute and long-term temperature stimuli.

Keywords

Gene expressionStrongylocentrotus intermediustemperatureTRPA1
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 8 , December 2019 , pp. 1825 - 1829
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

Agatsuma, Y (2013) Strongylocentrotus intermedius. In Lawrence, JM (ed.), Edible Sea Urchins: Biology and Ecology, 3rd Edn. San Diego, CA: Academic Press, pp. 437–447.Google Scholar
Bandell, M, Story, GM, Hwang, SW, Viswanath, V, Eid, SR, Petrus, MJ, Earley, TJ and Patapoutian, A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849–857.Google Scholar
Bodmer, MDV, Wheeler, PM, Hendrix, AM, Cesarano, DN, East, AS and Exton, DA (2017) Interacting effects of temperature, habitat and phenotype on predator avoidance behaviour in Diadema antillarum: implications for restorative conservation. Marine Ecology: Progress Series 566, 105–115.Google Scholar
Caspani, O and Heppenstall, PA (2009) TRPA1 and cold transduction: an unresolved issue? Journal of General Physiology 133, 245–249.Google Scholar
Caterina, MJ (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. American Journal of Physiology 292, R64–R76.Google Scholar
Caterina, MJ, Schumacher, MA, Tominaga, M, Rosen, TA, Levine, JD and Julius, D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389, 816–824.Google Scholar
Chang, YQ, Wang, ZC and Wang, GJ (1999) Effect of temperature and algae on feeding and growth in sea urchin, Strongylocentrotus intermedius. Journal of Fisheries of China 23, 69–76. (In Chinese with English Abstract.)Google Scholar
Chen, J (2015) The evolutionary divergence of TRPA1 channel: heat-sensitive, cold-sensitive and temperature-insensitive. Temperature 2, 158–159.Google Scholar
Chen, J, Kang, D, Xu, J, Lake, M, Hogan, JO, Sun, C, Walter, K, Yao, B and Kim, D (2013) Species differences and molecular determinant of TRPA1 cold sensitivity. Nature Communications 4, 2501.Google Scholar
Cheng, W, Yang, F, Takanishi, C and Zheng, J (2007) Thermosensitive TRPV channel subunits coassemble into heteromeric channels with intermediate conductance and gating properties. Journal of General Physiology 129, 191–207.Google Scholar
Florey, E and Cahill, MA (1977) Ultrastructure of sea urchin tube feet. Cell & Tissue Research 177, 195–214.Google Scholar
Fu, T, Yang, T, Liu, Y and Wang, GR (2015) Identification and functional characterization of TRPA1 in Apolygus lucorum (Meyer-Dür). Scientia Agricultura Sinica 25, 370–384. (In Chinese with English Abstract.)Google Scholar
Gavva, NR, Treanor, J, Garami, A, Fang, L, Surapaneni, S, Akrami, A, Alvarez, F, Bak, A, Darling, M, Gore, A, Jang, G, Kesslak, J, Ni, L, Norman, HM, Palluconi, GJ, Rose, M, Salfi, M, Tan, E, Romanovsky, A and Davar, G (2008) Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 136, 202–210.Google Scholar
Han, LS, Ding, J, Wang, H, Zuo, RT, Quan, ZJ, Fan, ZH, Liu, QD and Chang, YQ (2019) Molecular characterization and expression of SiFad1 in the sea urchin (Strongylocentrotus intermedius). Gene 705, 133–141.Google Scholar
Jordt, SE, Bautista, DM, Chuang, HH, McKemy, DD, Zygmunt, PM, Högestätt, ED, Meng, ID and Julius, D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260–265.Google Scholar
Lee, Y (2013) Contribution of Drosophila TRPA1-expressing neurons to circadian locomotor activity patterns. PLoS ONE 8, e85189.Google Scholar
Lesser, MP, Carleton, KL, Böttger, SA, Barry, TM and Walker, CW (2011) Sea urchin tube feet are photosensory organs that express a rhabdomeric-like opsin and PAX6. Proceedings of the Royal Society B: Biological Sciences 278, 3371–3379.Google Scholar
Li, KQ, Liu, L, Shang, SN, Wang, Y, Zhan, YY, Song, J, Zhang, XX and Chang, YQ (2017) cDNA cloning, expression and immune function analysis of a novel Rac1 gene (AjRac1) in the sea cucumber Apostichopus japonicas. Fish & Shellfish Immunology 69, 218e226.Google Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.Google Scholar
Luo, J, Shen, WL and Montell, C (2016) TRPA1 mediates sensing the rate of temperature change in Drosophila larvae. Nature Neuroscience 20, 34–41.Google Scholar
Murren, CJ, Auld, JR, Callahan, H, Ghalambor, CK, Handelsman, CA, Heskel, MA, Kingsolver, JG, Maclean, HJ, Masel, J, Maughan, H, Pfennig, DW, Relyea, RA, Seiter, S, Snell-Rood, E, Steiner, UK and Schlichting, CD (2015) Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115, 293–301.Google Scholar
Patapoutian, A, Peier, AM, Story, GM and Viswanath, V (2003) ThermoTRP channels and beyond: mechanisms of temperature sensation. Nature Reviews Neuroscience 4, 529–539.Google Scholar
Pearse, JS (2006) Ecological role of purple sea urchins. Science 314, 940–941.Google Scholar
Pinsky, ML, Eikeset, AM, McCauley, DJ, Payne, JL and Sunday, JM (2019) Greater vulnerability to warming of marine vs terrestrial ectotherms. Nature 569, 108–111.Google Scholar
Roessingh, S and Stanewsky, R (2017) The drosophila TRPA1 channel and neuronal circuits controlling rhythmic behaviours and sleep in response to environmental temperature. International Journal of Molecular Sciences 18, 2028.Google Scholar
Saito, S, Hamanaka, G, Kawai, N, Furukawa, R, Gojobori, J, Tominaga, M, Kaneko, H and Satta, Y (2017) Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae. Scientific Reports 7, 2173.Google Scholar
Sharp, DT and Gray, IE (1962) Studies on factors affecting the local distribution of two sea urchins, Arbacia punctulata and Lytechinus variegatus. Ecology 43, 309–313.Google Scholar
Stillman, JH and Armstrong, E (2015) Genomics are transforming our understanding of responses to climate change. Bioscience 65, 237–246.Google Scholar
Story, GM, Peier, AM, Reeve, AJ, Eid, SR, Mosbacher, J, Hricik, TR, Earley, TJ, Hergarden, AC, Andersson, DA and Hwang, SW (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819–829.Google Scholar
Tominaga, M and Caterina, MJ (2004) Thermosensation and pain. Journal of Neurobiology 61, 3–12.Google Scholar
Ullrich-Lüter, E, Dupont, S, Arboleda, E, Hausen, H and Arnone, M (2011) Unique system of photoreceptors in sea urchin tube feet. Proceedings of the National Academy of Sciences USA 108, 8367–8372.Google Scholar
Uthicke, S, Liddy, M, Nguyen, HD and Byrne, M (2014) Interactive effects of near-future temperature increase and ocean acidification on physiology and gonad development in adult Pacific sea urchin, Echinometra sp. A. Coral Reefs 33, 831–845.Google Scholar
Vandewauw, I, De Clercq, K, Mulier, M, Held, K, Pinto, S, Van Ranst, N, Segal, A, Voet, T, Vennekens, R, Zimmermann, K, Vriens, J and Voets, T (2018) A TRP channel trio mediates acute noxious heat sensing. Nature 555, 662–666.Google Scholar
Veilleux, HD, Ryu, T, Donelson, JM, Herwerden, LV, Seridi, L, Ghosheh, Y, Berumen, ML, Leggat, W, Ravasi, T and Munday, PL (2015) Molecular processes of transgenerational acclimation to a warming ocean. Nature Climate Change 5, 1074–1078.Google Scholar
Wolfe, K, Dworjanyn, SA and Byrne, M (2013) Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma). Global Change Biology 19, 2698–2707.Google Scholar
Yonemitsu, T, Kuroki, C, Takahashi, N, Mori, Y, Kanmura, Y, Kashiwadani, H, Ootsuka, Y and Kuwaki, T (2013) TRPA1 detects environmental chemicals and induces avoidance behavior and arousal from sleep. Scientific Reports 3, 3100.Google Scholar
Yun, SK, Son, JY, Kim, TH, Sang, KP, Yi, D, Noguchi, K, Dong, KA and Yong, CB (2010) Expression of transient receptor potential ankyrin 1 (TRPA1) in the rat trigeminal sensory afferents and spinal dorsal horn. Journal of Comparative Neurology 518, 687–698.Google Scholar
Zhou, ZC, Bao, ZM, Dong, Y, Wang, LM, He, CB and Liu, WD (2008) MYP gene expressions at transcription level in different stages of gonads of sea urchin Strongylocentrotus intermedius and hybrids. Hereditas 30, 1453–1458. (In Chinese with English Abstract.)Google Scholar