Advertisement

Fish Physiology and Biochemistry

, Volume 44, Issue 2, pp 615–628 | Cite as

Gene expression of thyrotropin- and corticotrophin-releasing hormones is regulated by environmental salinity in the euryhaline teleost Sparus aurata

  • Ignacio Ruiz-Jarabo
  • J. A. Martos-Sitcha
  • C. Barragán-Méndez
  • G. Martínez-Rodríguez
  • J. M. Mancera
  • F. J. Arjona
Article

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.

Keywords

Corticotrophin-releasing hormone Environmental salinity Gene expression Sparus aurata Thyrotropin-releasing hormone 

Notes

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 information

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.

References

  1. 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
  2. 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 CrossRefGoogle Scholar
  3. 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
  4. 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
  5. 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 CrossRefPubMedGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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
  8. 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
  9. 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 CrossRefPubMedGoogle Scholar
  10. 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
  11. 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 CrossRefPubMedGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. 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
  14. 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 CrossRefPubMedGoogle Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. 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 CrossRefPubMedGoogle Scholar
  17. 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 CrossRefPubMedGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. 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):127–129PubMedGoogle Scholar
  21. Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235.  https://doi.org/10.1093/molbev/mst012 CrossRefPubMedGoogle Scholar
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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 CrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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
  32. 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):11731–11733PubMedGoogle Scholar
  33. 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:563–576CrossRefGoogle Scholar
  34. 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
  35. 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 CrossRefPubMedGoogle Scholar
  36. 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 CrossRefPubMedGoogle Scholar
  37. 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 CrossRefPubMedGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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
  40. 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
  41. McCormick SD, Farrell AP, Brauner CJ (2013) Euryhaline fishes vol 32. Fish physiology. Academic Press, OxfordGoogle Scholar
  42. 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 CrossRefPubMedGoogle Scholar
  43. 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 CrossRefPubMedGoogle Scholar
  44. 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 CrossRefPubMedGoogle Scholar
  45. 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
  46. 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):385–392CrossRefPubMedGoogle Scholar
  47. 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
  48. 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
  49. 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 CrossRefPubMedGoogle Scholar
  50. Schally AV, Redding TW, Bowers CY, Barrett JF (1969) Isolation and properties of porcine thyrotropin-releasing hormone. J Biol Chem 244(15):4077–4088PubMedGoogle Scholar
  51. 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
  52. 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
  53. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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 CrossRefPubMedGoogle Scholar
  55. 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 CrossRefPubMedGoogle Scholar
  56. 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
  57. 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 CrossRefPubMedGoogle Scholar
  58. 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 CrossRefPubMedGoogle Scholar
  59. 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 103:111–119PubMedPubMedCentralGoogle Scholar
  60. 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
  61. 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
  62. 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

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  1. 1.Departamento de Biología, Facultad de Ciencias del Mar y AmbientalesUniversidad de CádizPuerto RealSpain
  2. 2.Instituto de Ciencias Marinas y Limnológicas, Facultad de CienciasUniversidad Austral de ChileValdiviaChile
  3. 3.Instituto de Ciencias Marinas de Andalucía (ICMAN-CSIC)Spanish National Research CouncilPuerto RealSpain
  4. 4.Nutrigenomics and Fish Growth Endocrinology Group, Institute of Aquaculture Torre de la SalConsejo Superior de Investigaciones Científicas (IATS-CSIC)Ribera de CabanesSpain
  5. 5.Department of Physiology, Radboud Institute for Molecular Life SciencesRadboud University Medical CenterNijmegenThe Netherlands

Personalised recommendations