Gene expression of thyrotropin- and corticotrophin-releasing hormones is regulated by environmental salinity in the euryhaline teleost Sparus aurata
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.
KeywordsCorticotrophin-releasing hormone Environmental salinity Gene expression Sparus aurata Thyrotropin-releasing hormone
J. A. M. S. is currently supported by a postdoctoral research fellowship (Juan de la Cierva-Formación, reference FJCI-2014-20161) from MINECO.
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.
Compliance with ethical standards
The experimental procedures complied with the Guidelines of the European Union (2010/63/UE) and the Spanish legislation (RD 1201/2005 and law 32/2007) for the use of animals for scientific purposes.
Conflict of interest
The authors declare that they have no conflict of interest.
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 PubMedGoogle Scholar
- 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 235–311CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- McCormick SD, Farrell AP, Brauner CJ (2013) Euryhaline fishes vol 32. Fish physiology. Academic Press, OxfordGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 69–124Google Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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