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Isolation, characterization and expression analysis of TRPV4 in half-smooth tongue sole Cynoglossus semilaevis

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Abstract

The transient receptor potential vanilloid 4 (TRPV4), another Ca2+ entry channel, belongs to the vanilloid subfamily and responds to a number of different physical and chemical stimuli and exists widely in mammals. However, our understanding of the TRPV4 in fish remains poor. Therefore, we studied the TRPV4 gene from Cynoglossus semilaevis, named CsTRPV4 that encodes a putative protein of 870 amino acids common in structure and characteristic of mammalian TRPV4, including the domains of ANK repeats, six TM, TRP domain, and CaMBD. The CsTRPV4 was expressed ubiquitously in examined tissues: higher expression in the heart, spleen, testis, and eye, but lower expression in kidney and liver. Surprisingly, the expression of CsTRPV4 in lateral line was significantly higher than in many other tissues as the CsTRPV4 was expressed significantly in the free neuromasts. In addition, CsTRPV4 in the free neuromast from the larval fish was significantly expressed in the hair cells of the free neuromasts. Therefore, the free neuromasts can act as a mechano-sensor to the mechanical stimulation in molecular level in C. semilaevis, which lays a foundation for further study of the functions of the free neuromasts.

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References

  • Amato V, Viña E, Calavia M G, Guerrera M C, Laurà R, Navarro M, De Carlos F, Cobo J, Germanà A, Vega J A. 2011. Trpv4 in the sensory organs of adult zebrafish, Microscopy Research & Technique, 75(1): 89–96.

    Google Scholar 

  • Bossus M, Charmantier G, Lorin-Nebel C. 2011. Transient receptor potential vanilloid 4 in the European sea bass Dicentrarchuslabrax: a candidate protein for osmosensing, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160(1): 43–51.

    Google Scholar 

  • Carton A G, Montgomery J C. 2002. Responses of lateral line receptors to water flow in the Antarcticnotothenioid, Trematomusbernacchii, Polar Biology, 25(10): 789–793.

    Google Scholar 

  • Caterina M J, Leffler A, Malmberg A B, Martin W J, Trafton J, Petersen-Zeitz K R, Koltzenburg M, Basbaum A I, Julius D. 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor, Science, 288(5464): 306–313.

    Google Scholar 

  • Caterina M J, Rosen T A, Tominaga M, Brake A J, Julius D. 1999. A capsaicin-receptor homologue with a high threshold for noxious heat, Nature, 1999, 398(6726): 436–441.

    Google Scholar 

  • Clapham D E. 2003. TRP channels as cellular sensors, Nature, 426(6966): 517–524.

    Google Scholar 

  • Colbert H A, Smith T L, Bargmann C I. 1997. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. The Journal of Neuroscience, 17(21): 8 259–8 269.

    Google Scholar 

  • Cuajungco M P, Grimm C, Oshima K, D’hoedt D, Nilius B, Mensenkamp AR, Bindels RJM, Plomann M, Heller S. 2006. PACSINs bind to the TRPV4 cation channel PACSIN 3 modulates the subcellular localization of TRPV4, Journal of Biological Chemistry, 281(27): 18 753–18 762.

    Google Scholar 

  • D’Hoedt D, Owsianik G, Prenen J, Cuajungco MP, Grimm C, Heller S, Voets T, Nilius B. 2008. Stimulus-specific modulation of the cation channel TRPV4 by PACSIN 3, Journal of Biological Chemistry, 283(10): 6 272–6 280.

    Google Scholar 

  • Dambly-Chaudière C, Sapède D, Soubiran F, Decorde K, Gompel N, Ghysen A. 2003. The lateral line of zebrafish: a model system for the analysis of morphogenesis and neural development in vertebrates, Biology of the Cell, 95(9): 579–587.

    Google Scholar 

  • Dijkgraaf S. 1963. The functioning and significance of the lateral-line organs, Biological Reviews, 38(1): 51–105.

    Google Scholar 

  • Eid S R, Cortright D N. 2009. Transient receptor potential channels on sensory nerves. In: Canning B, Spina D eds. Sensory Nerves. Springer, Berlin, Heidelberg.

    Google Scholar 

  • Engelmann J, Hanke W, Mogdans J, Bleckmann H. 2000. Hydrodynamic stimuli and the fish lateral line, Nature, 408(6808): 51–52.

    Google Scholar 

  • Everaerts W, Nilius B, Owsianik G. 2010. The vanilloid transient receptor potential channel TRPV4: From structure to disease, Progress in Biophysics and Molecular Biology, 103(1): 2–17.

    Google Scholar 

  • Galindo-Villegas J, Montalban-Arques A, Liarte S, De Oliveira S, Pardo-Pastor C, Rubio-Moscardo F, Meseguer J, Valverde M A, Mulero V. 2016. Correction: cutting edge: trpv4—mediated detection of hyposmotic stress by skin keratinocytes activates developmental immunity, Journal of Immunology, 196(8): 3 494.

    Google Scholar 

  • Garcia-Elias A, Mrkonjić S, Jung C, Pardo-Pastor C, Vicente R, Valverde M A. 2014. The trpv4 channel. In: Nilius B, Flockerzi V eds. Mammalian Transient Receptor Potential (TRP) Cation Channels. Springer, Berlin, Heidelberg.

    Google Scholar 

  • Gaudet R. 2008. A primer on ankyrin repeat function in TRP channels and beyond, Molecular BioSystems, 4(5): 372–379.

    Google Scholar 

  • Kawamura G, Masuma S, Tezuka N, Koiso M, Jinbo T, Namba K. 2003. Morphogenesis of sense organs in the bluefin tuna Thunnus orientalis: The big fish bang. In: Proceedings of the 26th Annual Larval Fish Conference. Norwegian Institute of Marine Research, Bergen, Norway. p.123–135.

  • Koyama H, Kishida R, Goris R C, Kusunoki T. 1990. Organization of the primary projections of the lateral line nerves in the lamprey Lampetra japonica. The Journal of Comparative Neurology, 295(2): 277–289.

    Google Scholar 

  • Kwan K Y, Glazer J M, Corey D P, Rice F L, Stucky C L. 2009. TRPA1 modulates mechanotransduction in cutaneous sensory neurons, Journal of Neuroscience, 29(15): 4 808–4 819.

    Google Scholar 

  • Liedtke W, Choe Y, Martí-Renom M A, Bell A M, Denis C S, Šali A, Hudspeth A J, Friedman J M, Heller S. 2000. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor, Cell, 103(3): 525–535.

    Google Scholar 

  • Liedtke W, Tobin D M, Bargmann C I, Friedman J M. 2003. Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 100(Suppl. 2): 14 531–14 536.

    Google Scholar 

  • Liedtke W. 2007. Role of TRPV ion channels in sensory transduction of osmotic stimuli in mammals, Experimental Physiology, 92(3): 507–512.

    Google Scholar 

  • Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method, Methods, 25(4): 402–408.

    Google Scholar 

  • Ma A J, Liu X Z, Xu Y J, Liang Y, Zhuang Z M. 2006. Feeding rhythm and growth of the tongue sole, Cynoglossus semilaevis Günther, during its early life stages, Aquaculture Research, 37(6): 586–593.

    Google Scholar 

  • Ma A J, Wang X A, Zhuang Z M, Zhang X M, Zhang L J. 2007b. Structure of retina and visual characteristics of the half-smooth tongue-sole Cynoglossus semilaevis Günter, Acta Zoologica Sinica, 53(2): 354–363. (in Chinese with English abstract)

    Google Scholar 

  • Ma A J, Wang X A, Zhuang Z M. 2007a. Lateral-line sense organs and dermal surface structures of the tongue sole Cynoglossus semilaevis. Acta Zoologica Sinica, 53(6): 1 113–1 120. (in Chinese with English abstract)

  • Mangos S, Liu Y, Drummond I A. 2007. Dynamic expression of the osmosensory channel trpv4 in multiple developing organs in zebrafish, Gene Expression Patterns, 7(4): 480–484.

    Google Scholar 

  • Marshall N J. 1996. Vision and sensory physiology the lateral line systems of three deep-sea fish, Journal of Fish Biology, 49(SA): 239–258.

    Google Scholar 

  • O’Neil R G, Heller S. 2005. The mechanosensitive nature of TRPV channels, Pflügers Archiv., 451(1): 193–203.

    Google Scholar 

  • Pedersen S F, Owsianik G, Nilius B. 2005. TRP channels: an overview, Cell Calcium, 38(3–4): 233–252.

    Google Scholar 

  • Rui X, Xu X Z S. 2010. Mechanosensitive channels: in touch with Piezo, Current Biology, 20(21): R936–R938.

    Google Scholar 

  • Ryskamp D A, Witkovsky P, Barabas P, Huang W, Koehler C, Akimov N P, Lee S H, Chauhan S, Xing W, Rentería R C, Liedtke W, Krizaj D. 2014. The polymodal ion channel trpv4 modulates calcium flux, spiking rate and apoptosis of mouse retinal ganglion cells, Journal of Neuroscience, 31(19): 7 089–7 101.

    Google Scholar 

  • Sha Z X, Luo X H, Liao X L, Wang SL, Wang Q L, Chen S L. 2011. Development and characterization of 60 novel EST-SSR markers in half-smooth tongue sole Cynoglossus semilaevis. Journal of Fish Biology, 78(1): 322–331.

    Google Scholar 

  • Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant T D. 2000. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity, Nature Cell Biology, 2(10): 695–702.

    Google Scholar 

  • Suzuki M, Mizuno A. 2012. The molecular mechanism of multifunctional mechano-gated channel TRPV4. In: Amkin A, Lozinsky I eds. Mechanically Gated Channels and their Regulation. Springer, Dordrecht.

    Google Scholar 

  • Thisse C, Thisse B. 2008. High-resolution in situ hybridization to whole-mount zebrafish embryos, Nature Protocols, 3(1): 59–69.

    Google Scholar 

  • Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, Bödding M, Droogmans G, Nilius B. 2002. Molecular determinants of permeation through the cation channel TRPV4, Journal of Biological Chemistry, 277(37): 33 704–33 710.

    Google Scholar 

  • Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B. 2004. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel trpv4, Proceedings of the National Academy of Sciences of the United States of America, 101(1): 396–401.

    Google Scholar 

  • Watanabe S, Seale A P, Grau E G, Kaneko T. 2012. Stretch-activated cation channel TRPV4 mediates hyposmotically induced prolactin release from prolactin cells of Mozambique tilapia Oreochromismossambicus. American Journal of Physiology Regulatory Integrative & Comparative Physiology, 302(8): R1 004–R1 011.

    Google Scholar 

  • Wissenbach U, Bödding M, Freichel M, Flockerzi V. 2000. Trp12, a novel Trp related protein from kidney, FEBS Letters, 485(2–3): 127–134.

    Google Scholar 

  • Zhang Y A, Okada A, Lew C H, Mcconnell S K. 2002. Regulated nuclear trafficking of the homeodomain protein otx1 in cortical neurons, Molecular and Cellular Neuroscience, 19(3): 430–446.

    Google Scholar 

  • Zhang Z, Zhao Z, Margolskee R F, Liman E. 2007. The transduction channel TRPM5 is gated by intracellular calcium in taste cells, Neuroscience, 27(21): 5 777–5 786.

    Google Scholar 

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Correspondence to Aijun Ma.

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Supported by the Earmarked Fund for Modern Agro-Industry Technology Research System (No. CARS-47-G01), the AoShan Talents Cultivation Program supported by Qingdao National Laboratory for Marine Science and Technology (No. 2017ASTCP-OS04), and the Qingdao Natural Science Foundation (No. 12-1-4-12-(1)-jch)

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Shang, X., Ma, A., Wang, X. et al. Isolation, characterization and expression analysis of TRPV4 in half-smooth tongue sole Cynoglossus semilaevis. J. Ocean. Limnol. 38, 294–305 (2020). https://doi.org/10.1007/s00343-019-8316-5

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