Abstract
In euryhaline teleosts, the hypothalamus-pituitary-thyroid and hypothalamus-pituitary-interrenal axes (HPT and HPI, respectively) are regulated in response to environmental stimuli such as salinity changes. However, the molecular players participating in this physiological process in the gilthead seabream (Sparus aurata), a species of high value for aquaculture, are still not identified and/or fully characterized in terms of gene expression regulation. In this sense, this study identifies and isolates the thyrotropin-releasing hormone (trh) mRNA sequence from S. aurata, encoding prepro-Trh, the putative factor initiating the HPT cascade. In addition, the regulation of trh expression and of key brain genes in the HPI axis, i.e., corticotrophin-releasing hormone (crh) and corticotrophin-releasing hormone-binding protein (crhbp), was studied when the osmoregulatory status of S. aurata was challenged by exposure to different salinities. The deduced amino acid structure of trh showed 65–81% identity with its teleostean orthologs. Analysis of the tissue distribution of gene expression showed that trh mRNA is, though ubiquitously expressed, mainly found in brain. Subsequently, regulation of gene expression of trh, crh, and crhbp was characterized in fish acclimated to 5-, 15-, 40-, and 55-ppt salinities. In this regard, the brain gene expression pattern of trh mRNA was similar to that found for the crh gene, showing an upregulation of gene expression in seabream acclimated to the highest salinity tested. Conversely, crhbp did not change in any of the groups tested. Our results suggest that Trh and Crh play an important role in the acclimation of S. aurata to hypersaline environments.
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References
Aoki Y, Takahashi M, Masuda T, Tsukamoto T, Iigo M, Yanagisawa T (2005) Molecular cloning of prepro-thyrotropin-releasing hormone cDNAs from the common carp Cyprinus carpio and goldfish Carassius auratus. Gen Comp Endocrinol 141(1):84–92. https://doi.org/10.1016/j.ygcen.2004.11.011
Aoki Y, Masuda T, Iigo M, Yanagisawa T (2007) Molecular cloning of prepro-thyrotropin-releasing hormone cDNA from medaka (Oryzias latipes). Comp Endocrinol 150(2):364–370. https://doi.org/10.1016/j.ygcen.2006.09.009
Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Martin del Rio MP, Mancera JM (2007) Osmoregulatory response of Senegalese sole (Solea senegalensis) to changes in environmental salinity. Comp Biochem Physiol A Mol Integr Physiol 148(2):413–421. https://doi.org/10.1016/j.cbpa.2007.05.026
Arjona FJ, Vargas-Chacoff L, Martin Del Rio MP, Flik G, Mancera JM, Klaren PHM (2011) Effects of cortisol and thyroid hormone on peripheral outer ring deiodination and osmoregulatory parameters in the Senegalese sole (Solea senegalensis). J Endocrinol 208:323–330. https://doi.org/10.1530/JOE-10-0416
Barry TP, Grau EG (1986) Estradiol-17 beta and thyrotropin-releasing hormone stimulate prolactin release from the pituitary gland of a teleost fish in vitro. Gen Comp Endocrinol 62(2):306–314. https://doi.org/10.1016/0016-6480(86)90121-8
Bernier NJ, Peter RE (2001) Appetite-suppressing effects of urotensin I and corticotropin-releasing hormone in goldfish (Carassius auratus). Neuroendocrinology 73(4):248–260. https://doi.org/10.1159/000054642
Bernier NJ, Flik G, Klaren PHM (2009) Regulation and contribution of the corticotropic, melanotropic and thyrotropic axes to the stress response in fishes. In: Bernier NJ, van der Kraak G, Farrell AP, Brauner CJ (eds) Fish Physiology, vol 28. vol Fish Neuroendocrinology. Academic Press, Cambridge, pp 235–311
Bernier NJ, Gorissen M, Flik G (2012) Differential effects of chronic hypoxia and feed restriction on the expression of leptin and its receptor, food intake regulation and the endocrine stress response in common carp. J Exp Biol 215(13):2273–2282. https://doi.org/10.1242/jeb.066183
Blanton ML, Specker JL (2007) The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol 37(1-2):97–115. https://doi.org/10.1080/10408440601123529
Buckley C, MacDonald EE, Tuziak SM, Volkoff H (2010) Molecular cloning and characterization of two putative appetite regulators in winter flounder (Pleuronectes americanus): preprothyrotropin-releasing hormone (TRH) and preproorexin (OX). Peptides 31(9):1737–1747. https://doi.org/10.1016/j.peptides.2010.05.017
Carr JA, Patino R (2011) The hypothalamus-pituitary-thyroid axis in teleosts and amphibians: endocrine disruption and its consequences to natural populations. Gen Comp Endocrinol 170(2):299–312. https://doi.org/10.1016/j.ygcen.2010.06.001
Chatterjee A, Hsieh YL, Yu JYL (2001) Molecular cloning of cDNA encoding thyroid stimulating hormone beta subunit of bighead carp Aristichthys nobilis and regulation of its gene expression. Mol Cell Endocrinol 174(1-2):1–9. https://doi.org/10.1016/S0303-7207(01)00392-6
Clements S, Schreck CB, Larsen DA, Dickhoff WW (2002) Central administration of corticotropin-releasing hormone stimulates locomotor activity in juvenile chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol 125(3):319–327. https://doi.org/10.1006/gcen.2001.7707
de Groef B, Van der Geyten S, Darras VM, Kuhn ER (2006) Role of corticotropin-releasing hormone as a thyrotropin-releasing factor in non-mammalian vertebrates. Gen Comp Endocrinol 146(1):62–68. https://doi.org/10.1016/j.ygcen.2005.10.014
Eales JG, Himick BA (1988) The effects of TRH on plasma thyroid hormone levels of rainbow trout (Salmo gairdneri) and Arctic charr (Salvelinus alpinus). Gen Comp Endocrinol 72(3):333–339. https://doi.org/10.1016/0016-6480(88)90155-4
Flik G, Klaren PHM, Van den Burg EH, Metz JR, Huising MO (2006) CRF and stress in fish. Gen Comp Endocrinol 146(1):36–44. https://doi.org/10.1016/j.ygcen.2005.11.005
Galas L, Raoult E, Tonon MC, Okada R, Jenks BG, Castaño JP, Kikuyama S, Malagon M, Roubos EW, Vaudry H (2009) TRH acts as a multifunctional hypophysiotropic factor in vertebrates. Gen Comp Endocrinol 164(1):40–50. https://doi.org/10.1016/j.ygcen.2009.05.003
Geven EJW, Verkaar F, Flik G, Klaren PHM (2006) Experimental hyperthyroidism and central mediators of stress axis and thyroid axis activity in common carp (Cyprinus carpio L.) J Mol Endocrinol 37(3):443–452. https://doi.org/10.1677/jme.1.02144
Geven EJW, Flik G, Klaren PHM (2009) Central and peripheral integration of interrenal and thyroid axes signals in common carp (Cyprinus carpio L.) J Endocrinol 200(1):117–123. https://doi.org/10.1677/JOE-08-0410
Giraud P, Gillioz P, Conte-Devolx B, Oliver C (1979) Distribution of thyrotropin releasing hormone (TRH), alpha-melanocyte-stimulating hormone (alpha-MSH) and somatostatin in the skin of the green frog (Rana esculenta). C R Seances Acad Sci D 288(1):127–129
Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235. https://doi.org/10.1093/molbev/mst012
Han YS, Liao IC, Tzeng WN, Yu JYL (2004) Cloning of the cDNA for thyroid stimulating hormone beta subunit and changes in activity of the pituitary-thyroid axis during silvering of the Japanese eel, Anguilla japonica. J Mol Endocrinol 32(1):179–194. https://doi.org/10.1677/jme.0.0320179
Harder S, Dammann O, Buck F, Zwiers H, Lederis K, Richter D, Bruhn TO (2001) Cloning of two thyrotropin-releasing hormone receptor subtypes from a lower vertebrate (Catostomus commersoni): functional expression, gene structure, and evolution. Gen Comp Endocrinol 124(2):236–245. https://doi.org/10.1006/gcen.2001.7709
Huising MO, Metz JR, van Schooten C, Taverne-Thiele AJ, Hermsen T, Verburg-van Kemenade BM, Flik G (2004) Structural characterisation of a cyprinid (Cyprinus carpio L.) CRH, CRH-BP and CRH-R1, and the role of these proteins in the acute stress response. J Mol Endocrinol 32(3):627–648. https://doi.org/10.1677/jme.0.0320627
Huising MO, Geven EJW, Kruiswijk CP, Nabuurs SB, Stolte EH, Spanings FAT, Verburg-van Kemenade BML, Flik G (2006) Increased leptin expression in common carp (Cyprinus carpio) after food intake but not after fasting or feeding to satiation. Endocrinology 147(12):5786–5797. https://doi.org/10.1210/en.2006-0824
Huising MO, van der Aa LM, Metz JR, de Fatima Mazon A, Kemenade BM, Flik G (2007) Corticotropin-releasing factor (CRF) and CRF-binding protein expression in and release from the head kidney of common carp: evolutionary conservation of the adrenal CRF system. J Endocrinol 193(3):349–357. https://doi.org/10.1677/JOE-07-0070
Iziga R, Ponce M, Infante C, Rebordinos L, Canavate JP, Manchado M (2010) Molecular characterization and gene expression of thyrotropin-releasing hormone in Senegalese sole (Solea senegalensis). Comp Biochem Physiol B Biochem Mol Biol 157(2):167–174. https://doi.org/10.1016/j.cbpb.2010.05.013
Kagabu Y, Mishiba T, Okino T, Yanagisawa T (1998) Effects of thyrotropin-releasing hormone and its metabolites, Cyclo(His-Pro) and TRH-OH, on growth hormone and prolactin synthesis in primary cultured pituitary cells of the common carp, Cyprinus carpio. Gen Comp Endocrinol 111(3):395–403. https://doi.org/10.1006/gcen.1998.7124
Klaren PHM, Guzman JM, Reutelingsperger SJ, Mancera JM, Flik G (2007) Low salinity acclimation and thyroid hormone metabolizing enzymes in gilthead seabream (Sparus auratus). Gen Comp Endocrinol 152(2-3):215–222. https://doi.org/10.1016/j.ygcen.2007.02.010
Klaren PHM, Wunderink YS, Yufera M, Mancera JM, Flik G (2008) The thyroid gland and thyroid hormones in Senegalese sole (Solea senegalensis) during early development and metamorphosis. Gen Comp Endocrinol 155(3):686–694. https://doi.org/10.1016/j.ygcen.2007.09.014
Krayushkina LS, Semenova OG, Vyushina AV, Gerasimov AA (2015) Morphofunctional remodelling of the osmoregulatory system in starred sturgeon Acipenser stellatus (Acipenseridae) during transition from hyperosmotic to hypoosmotic regulation. J Ichthyol 55(2):259–272. https://doi.org/10.1134/S0032945215020101
Kuchler K, Richter K, Trnovsky J, Egger R, Kreil G (1990) Two precursors of thyrotropin-releasing hormone from skin of Xenopus laevis. Each contains seven copies of the end product. J Biol Chem 265(20):11731–11733
Laiz-Carrion R, Guerreiro PM, Fuentes J, Canario AVM, Martin Del Rio MP, Mancera JM (2005) Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus. J Exp Zool Part A Comp Exp Biol 303A:563–576
Laiz-Carrion R, Fuentes J, Redruello B, Guzman JM, Martin del Rio MP, Power D, Mancera JM (2009) Expression of pituitary prolactin, growth hormone and somatolactin is modified in response to different stressors (salinity, crowding and food-deprivation) in gilthead sea bream Sparus auratus. Gen Comp Endocrinol 162(3):293–300. https://doi.org/10.1016/j.ygcen.2009.03.026
Larsen DA, Swanson P, Dickey JT, Rivier J, Dickhoff WW (1998) In vitro thyrotropin-releasing activity of corticotropin-releasing hormone-family peptides in coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 109(2):276–285. https://doi.org/10.1006/gcen.1997.7031
Lechan RM, Wu P, Jackson IM, Wolf H, Cooperman S, Mandel G, Goodman RH (1986) Thyrotropin-releasing hormone precursor: characterization in rat brain. Science 231(4734):159–161. https://doi.org/10.1126/science.3079917
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
López-Bojórquez L, Villalobos P, Garcia-G C, Orozco A, Valverde-R C (2007) Functional identification of an osmotic response element (ORE) in the promoter region of the killifish deiodinase 2 gene (FhDio2). J Exp Biol 210(17):3126–3132. https://doi.org/10.1242/jeb.004150
Lorgen M, Casadei E, Król E, Douglas A, Birnie MJ, Ebbesson LOE, Nilsen TO, Jordan WC, Jørgensen EH, Dardente H, Hazlerigg DG, Martin SAM (2015) Functional divergence of type 2 deiodinase paralogs in the Atlantic salmon. Curr Biol 25(7):936–941. https://doi.org/10.1016/j.cub.2015.01.074
Martos-Sitcha JA, Wunderink YS, Straatjes J, Skrzynska AK, Mancera JM, Martinez-Rodriguez G (2014) Different stressors induce differential responses of the CRH-stress system in the gilthead sea bream (Sparus aurata). Comp Biochem Physiol A Mol Integr Physiol 177:49–61. https://doi.org/10.1016/j.cbpa.2014.07.021
McCormick SD, Farrell AP, Brauner CJ (2013) Euryhaline fishes vol 32. Fish physiology. Academic Press, Oxford
Nugegoda D, Kibria G (2016) Effects of environmental chemicals on fish thyroid function: implications for fisheries and aquaculture in Australia. Gen Comp Endocrinol 244:40–53. https://doi.org/10.1016/j.ygcen.2016.02.021
Potter E, Behan DP, Fischer WH, Linton EA, Lowry PJ, Vale WW (1991) Cloning and characterization of the cDNAs for human and rat corticotropin releasing factor-binding proteins. Nature 349(6308):423–426. https://doi.org/10.1038/349423a0
Prasad C, Wilber JF, Amborski RL (1982) Thyrotropin-releasing hormone: its distribution and metabolism during development in bullfrog (Rana catesbeiana). Dev Neurosci 5(4):293–297. https://doi.org/10.1159/000112688
Rotllant J, Balm PH, Ruane NM, Perez-Sanchez J, Wendelaar-Bonga SE, Tort L (2000) Pituitary proopiomelanocortin-derived peptides and hypothalamus-pituitary-interrenal axis activity in gilthead sea bream (Sparus aurata) during prolonged crowding stress: differential regulation of adrenocorticotropin hormone and alpha-melanocyte-stimulating hormone release by corticotropin-releasing hormone and thyrotropin-releasing hormone. Gen Comp Endocrinol 119(2):152–163. https://doi.org/10.1006/gcen.2000.7508
Rousseau K, Le Belle N, Marchelidon J, Dufour S (1999) Evidence that corticotropin-releasing hormone acts as a growth hormone-releasing factor in a primitive teleost, the European eel (Anguilla anguilla). J Neuroendocrinol 11(5):385–392
Ruiz-Jarabo I, Klaren PHM, Louro B, Martos-Sitcha JA, Pinto PIS, Vargas-Chacoff L, Flik G, Martínez-Rodríguez G, Power DM, Mancera JM, Arjona FJ (2017) Characterization of the peripheral thyroid system of gilthead seabream acclimated to different ambient salinities. Comp Biochem Physiol A 203:24–31. https://doi.org/10.1016/j.cbpa.2016.08.013
Sangiao-Alvarellos S, Arjona FJ, Miguez JM, del Rio MPM, Soengas JL, Mancera JM (2006) Growth hormone and prolactin actions on osmoregulation and energy metabolism of gilthead sea bream (Sparus auratus). Comp Biochem Phys A 144(4):491–500. https://doi.org/10.1016/j.cbpa.2006.04.015
Satoh T, Yamada M, Monden T, Iizuka M, Mori M (1992) Cloning of the mouse hypothalamic preprothyrotropin-releasing hormone (TRH) cDNA and tissue distribution of its mRNA. Brain Res Mol Brain Res 14(1-2):131–135. https://doi.org/10.1016/0169-328X(92)90020-C
Schally AV, Redding TW, Bowers CY, Barrett JF (1969) Isolation and properties of porcine thyrotropin-releasing hormone. J Biol Chem 244(15):4077–4088
Shapiro MD, Kronenberg Z, Li C, Domyan ET, Pan H, Campbell M, Tan H, Huff CD, Hu H, Vickrey AI, Nielsen SCA, Stringham SA, Hu H, Willerslev E, Gilbert MTP, Yandell M, Zhang G, Wang J (2013) Genomic diversity and evolution of the head crest in the rock pigeon. Science 339(6123):1063–1067. https://doi.org/10.1126/science.1230422
Takei Y, McCormick SD (2013) Hormonal control of fish euryhalinity. In: McCormick SD, Brauner CJ, Farrell AP (eds) Fish physiology, vol 32. vol Euryhaline Fishes. Academic Press, Amsterdam, pp 69–124
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Tran TN, Fryer JN, Bennett HP, Tonon MC, Vaudry H (1989) TRH stimulates the release of POMC-derived peptides from goldfish melanotropes. Peptides 10(4):835–841. https://doi.org/10.1016/0196-9781(89)90122-8
Vandenborne K, Roelens SA, Darras VM, Kuhn ER, Van der Geyten S (2005) Cloning and hypothalamic distribution of the chicken thyrotropin-releasing hormone precursor cDNA. J Endocrinol 186(2):387–396. https://doi.org/10.1677/joe.1.06161
Vargas-Chacoff L, Astola A, Arjona FJ, Martin del Rio MP, Garcia-Cozar F, Mancera JM, Martinez-Rodriguez G (2009) Pituitary gene and protein expression under experimental variation on salinity and temperature in gilthead sea bream Sparus aurata. Comp Biochem Physiol B Biochem Mol Biol 154(3):303–308. https://doi.org/10.1016/j.cbpb.2009.07.004
Vargas-Chacoff L, Ruiz-Jarabo I, Arjona FJ, Laiz-Carrion R, Flik G, Klaren PHM, Mancera JM (2016) Energy metabolism of hyperthiroid gilthead sea bream Sparus aurata L. Comp Biochem Physiol A Mol Integr Physiol 191:25–34. https://doi.org/10.1016/j.cbpa.2015.09.014
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77(3):591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Wilber JF, Yamada M, Kim UJ, Feng P, Carnell NE (1992) The human prepro thyrotropin-releasing hormone (TRH) gene: cloning, characterization, hormonal regulation, and gene localization. Trans Am Clin Climatol Assoc 103:111–119
Wunderink YS, Engels S, Halm S, Yúfera M, Martínez-Rodríguez G, Flik G, Klaren PHM, Mancera JM (2011) Chronic and acute stress responses in Senegalese sole (Solea senegalensis): the involvement of cortisol, CRH and CRH-BP. Gen Comp Endocrinol 171(2):203–210. https://doi.org/10.1016/j.ygcen.2011.01.010
Wunderink YS, Martinez-Rodriguez G, Yufera M, Montero IM, Flik G, Mancera JM, Klaren PHM (2012) Food deprivation induces chronic stress and affects thyroid hormone metabolism in Senegalese sole (Solea senegalensis) post-larvae. Comp Biochem Physiol A Mol Integr Physiol 162(4):317–322. https://doi.org/10.1016/j.cbpa.2012.03.023
Yamada M, Radovick S, Wondisford FE, Nakayama Y, Weintraub BD, Wilber JF (1990) Cloning and structure of human genomic DNA andhypothalamic cDNA encoding human prepro thyrotropin-releasing hormone. Mol Endocrinol 4: 551-556. https://doi.org/ 10.1210/mend-4-4-551
Acknowledgements
J. A. M. S. is currently supported by a postdoctoral research fellowship (Juan de la Cierva-Formación, reference FJCI-2014-20161) from MINECO.
Funding
This study was funded by project AGL2010-14876 from Ministerio de Ciencia e Innovación awarded to J. M. M. (Spain). This work was partially supported by Ph.D. scholarship from the University of Cadiz (UCA 2009-074-FPI) awarded to I. R-J.
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Ruiz-Jarabo, I., Martos-Sitcha, J.A., Barragán-Méndez, C. et al. Gene expression of thyrotropin- and corticotrophin-releasing hormones is regulated by environmental salinity in the euryhaline teleost Sparus aurata . Fish Physiol Biochem 44, 615–628 (2018). https://doi.org/10.1007/s10695-017-0457-x
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DOI: https://doi.org/10.1007/s10695-017-0457-x