Skip to main content
Log in

Characterization of the 5′ flanking region of the growth hormone gene of the marine teleost, gilthead sea bream Sparus aurata: analysis of a polymorphic microsatellite in the proximal promoter

  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

The 5′ flanking region (1712 bp) of the growth hormone (GH) gene of the gilthead sea bream Sparus aurata was cloned, sequenced and characterized. It contains a consensus sequence for TATA box and several Pit-1 binding site motifs. Consensus sequences related to cyclic AMP response element, glucocortiocoid response element, and several other transcription factors were identified by comparison to consensus sequences in fish or mammalian GH genes. The promoter contains two microsatellites (di- and tri-nucleotides repeats) with additional upstream microsatellites (tri-and tetranucleotides), 10-mer tandem repeat, and two long inverted repeats. Analysis of the proximal dinucleotide microsatellite by polymerase chain reaction revealed polymorphism among individuals from a hatchery population and an association of alleles 250 and 254 with growth performance. Segregation analysis of this marker in one family showed Mendelian inheritance. These results suggest that the microsatellite in the promoter region (termed saGHpCA) might be considered as a candidate genetic marker for broodstock management and growth selection programs of Sparus aurata.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Funkenstein B. Potential application of recombinant hormones and growth factors in fish culture. In: Fingerman M, Nagabhushanam R (eds) Recent Advances in Marine Biotechnology Vol. 4: Aquaculture, Part B: Fishes, Science Publishers Inc., Enfield, NH. 2000; 57–76.

    Google Scholar 

  2. Andersen B, Rosenfeld MG. POU domain factors in the neuroendocrine system: lessons from developmental biology provide insights into human disease. Endocr. Rev. 2001; 22: 2–35.

    Article  PubMed  CAS  Google Scholar 

  3. Theill LE, Karin M. Transcriptional control of GH expression and anterior pituitary development. Endocr. Rev. 1993; 14: 670–689.

    PubMed  CAS  Google Scholar 

  4. Cooke NE, Liebhaber SA. Regulation of growth hormone gene expression. In: Kostyo JL, Goodman HM (eds). Handbook of Physiology, Section 7: the Endocrine System, Vol. V: Hormonal Control of Growth. Oxford University Press, New York, NY. 1999; 163–185.

    Google Scholar 

  5. Argenton F, Vianello S, Bernardini S, Jacquemin P, Martial J, Belayew A, Colombo L, Bortolussi M. The transcriptional regulation of the growth hormone gene is conserved in vertebrate evolution. Biochem. Biophys. Res. Commun. 1993; 192: 1360–1366.

    Article  PubMed  CAS  Google Scholar 

  6. Argenton F, Bernardini S, Puttini S, Colombo L, Bortolussi M. A TGACG motif mediates growth-hormone-factor-1/pituitary-transcriptional-activator-1-dependent cAMP regulation of the rainbow trout growth-hormone promoter. Eur. J. Biochem. 1996; 238: 591–598.

    Article  PubMed  CAS  Google Scholar 

  7. Wong AO, Le Drean Y, Liu D, Hu ZZ, Du SJ, Hew CL. Induction of Chinook salmon growth hormone promoter activity by the adenosine 3′,5′-monophosphate (cAMP)-dependent pathway involves two cAMP-response elements with the CGTCA motif and the pituitary-specific transcription factor pit-1. Endocrinology 1996; 137: 1775–1784.

    Article  PubMed  CAS  Google Scholar 

  8. Sekkali B, Brim H, Muller M, Argenton F, Bortolussi M, Colombo L, Belayew A, Martial JA. Structure and functional analysis of a tilapia (Oreochromis mossambicus) growth hormone gene: activation and repression by pituitary transcription factor Pit-1. DNA Cell Biol. 1999; 18: 489–502.

    Article  PubMed  CAS  Google Scholar 

  9. Melamed P, Yaron Z. Endocrine regulation of gonadotropin and growth hormone gene transcription in fish. Comp. Biochem. Physiol. Part C 1998; 119: 325–338.

    CAS  Google Scholar 

  10. Sekkali B, Belayew A, Bortolussi M, Martial JA, Muller M. Pit-1 mediates cell-specific and cAMP-induced transcription of the tilapia GH gene. Mol. Cell Endocrinol. 1999; 152: 111–123.

    Article  PubMed  CAS  Google Scholar 

  11. Yowe DL, Epping RJ. Cloning of the barramundi growth-hormone encoding gene: a comparative analysis of higher and lower vertebrate growth hormone genes. Gene 1995; 162: 255–259.

    Article  PubMed  CAS  Google Scholar 

  12. Yowe DL, Epping RJ. A minisatellite polymorphism in intron III of the barramundi (Lates calcarifer) growth hormone gene. Genome 1996; 39: 934–940.

    Article  PubMed  CAS  Google Scholar 

  13. Tanaka M, Toma Y, Ohkubo T, Sudo S, Nakashima K. Sequence of the flounder (Paralichthys olivaceus) growth hormone-encoding gene and its promoter region. Gene 1995; 165: 321–322.

    Article  PubMed  CAS  Google Scholar 

  14. Kang H, Lee SJ, Park SR, Ryu HY. DNA polymorphism in the growth hormone gene and its association with weight in olive flounder Paralichtys olivaceus. Fish. Sci. 2002; 68: 494–498.

    Article  CAS  Google Scholar 

  15. Ber R, Daniel V. Structure and sequence of the growth hormone encoding gene from Tilapia nilotica. Gene 1992; 113: 245–250.

    Article  PubMed  CAS  Google Scholar 

  16. Ber R, Daniel V. Sequence analysis suggests a recent duplication of the growth hormone-encoding gene in Tilapia nilotica. Gene 1993; 125: 143–150.

    Article  PubMed  CAS  Google Scholar 

  17. Venkatesh B, Brenner S. Genomic structure and sequence of the pufferfish (Fugu rubripes) growth hormone genes. Gene 1997; 187: 211–215.

    Article  PubMed  CAS  Google Scholar 

  18. Almuly R, Cavari B, Ferstman H, Kolodny O, Funkenstein B. Genomic structure and sequence of the gilthead seabream (Sparus aurata) growth hormone-encoding gene: identification of minisatellite polymorphism in intron I. Genome 2000; 43: 836–845.

    Article  PubMed  CAS  Google Scholar 

  19. Kashi Y, King D, Soller M. Simple sequence repeats as a source of quantitative genetic variation. Trends Genet. 1997; 13: 74–78.

    Article  PubMed  CAS  Google Scholar 

  20. Williams RR, Hassan-Walker AF, Lavender FL, Morgan M, Faik P, Ragoussis J. The minisatellite of the GPI/AMF/NLK/MF gene: interspecies conservation and transcriptional activity. Gene 2001; 269: 81–92.

    Article  PubMed  CAS  Google Scholar 

  21. Iwashita S, Koyama K, Nakamura Y. VNTR sequence on human chromosome 11p15 that affects transcriptional activity. J. Hum. Genet. 2001; 46: 717–721.

    Article  PubMed  CAS  Google Scholar 

  22. Pugliese A, Miceli D. The insulin gene in diabetes. Diabet. Metab. Res. Rev. 2002; 18: 13–25.

    Article  CAS  Google Scholar 

  23. Mill J, Asherson P, Browes C, D’Souza U, Craig I. Expression of the dopamine transporter gene is regulated by the 3′ UTR VNTR. Evidence from brain and lymphocytes using quantitative RT-PCR. Am. J. Med. Genet. 2002; 114: 975–979.

    Article  PubMed  Google Scholar 

  24. Ueno S. Genetic polymorphisms of serotonin and dopamine transporters in mental disorders. J. Med. Invest. 2003; 50: 25–31.

    PubMed  Google Scholar 

  25. Rich A. DNA comes in many forms. Gene 1993; 135: 99–109.

    Article  PubMed  CAS  Google Scholar 

  26. Wittig B, Wolfl S, Dorbic T, Vahrson W, Rich A. Transcription of human c-myc in permeabilized nuclei is associated with formation of Z-DNA in three discrete regions of the gene. EMBO J. 1992; 11: 4653–4663.

    PubMed  CAS  Google Scholar 

  27. Wolfl S, Martinez C, Rich A, Majzoub JA. Transcription of the human corticotropin-releasing hormone gene in NPLC cells is correlated with Z-DNA formation. Proc. Natl. Acad. Sci. USA 1996; 93: 3664–3668.

    Article  PubMed  CAS  Google Scholar 

  28. Müller V, Takeya M, Brendel S, Wittig B, Rich A. Z-DNA-forming sites within the human β-globin gene cluster. Proc. Natl. Acad. Sci. USA 1996; 93: 780–784.

    Article  PubMed  Google Scholar 

  29. Knorr C, Moser G, Muller E, Geldermann H. Association of GH gene variants with performance traits in F2 generations of European wild boar, Pietrain and Meishan pigs. Anim. Genet. 1997; 28: 124–128.

    Article  PubMed  CAS  Google Scholar 

  30. Hoj S, Fredholm M, Larsen NJ, Nielsen VH. Growth hormone gene polymorphism associated with selection for milk fat production in lines of cattle. Anim. Genet. 1993; 24: 91–96.

    Article  PubMed  CAS  Google Scholar 

  31. Lucy MC, Hauser SD, Eppard PJ, Krivi GG, Clark JH, Bauman DE, Collier RJ. Variants of somatotropin in cattle: gene frequencies in major dairy breeds and associated milk production. Domest. Anim. Endocrinol. 1993; 10: 325–333.

    Article  PubMed  CAS  Google Scholar 

  32. Kuhnlein U, Ni L, Weigend S, Gavora JS, Fairfull W, Zandworny D. DNA polymorphisms in the chicken growth hormone gene: response to selection for disease resistance and association with egg production. Anim. Genet. 1997; 28: 116–123.

    Article  PubMed  CAS  Google Scholar 

  33. Gorshkov S, Gordin H, Gorshkova G, Knibb W. Reproductive constraints for family selection of the gilthead seabream Sparus aurata L. Isr. J. Aquacult. Bamidgeh 1997; 49: 124–134.

    Google Scholar 

  34. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory. Cold Spring Harbor, NY. 1989.

    Google Scholar 

  35. Titus DE. Promega Protocols and Application Guide. 2nd edn. Madison WI 1991.

    Google Scholar 

  36. Israel DI. A PCR-based method for high stringency screening of DNA libraries. Nucleic Acids Res. 1993; 21: 2627–2631.

    Article  PubMed  CAS  Google Scholar 

  37. Schug J, Overton GC. TESS: Transcription Element Search Software on the WWW. Technical Report CBIL-TR-1997-1001-v0.0. Computational Biology and Informatics Laboratory, School of Medicine University of Pennsylvania. PA, USA, 1997.

    Google Scholar 

  38. Nelson JS. Fishes of the World, 3rd edn. John Wiley & Sons Inc., New York, 1994.

    Google Scholar 

  39. Ohkubo T, Araki M, Tanaka M, Sudo S, Nakashima K. Molecular cloning and characterization of the yellowtail GH gene and its promoter: a consensus sequence for teleost and avian Pit-1/GHF-1 binding sites. J. Mol. Endocrinol. 1996; 16: 63–72.

    Article  PubMed  CAS  Google Scholar 

  40. Argenton F, Vianello S, Bernardini S, Lopreiato R, Colombo L, Bortolussi M. Trout GH promoter analysis reveals a modular pattern of regulation consistent with the diversification of GH gene control and function in vertebrates. Mol. Cell Endocrinol. 2002; 189: 11–23.

    Article  PubMed  CAS  Google Scholar 

  41. Harvey S, Azumaya Y, Hull KL. Pituitary and extrapituitary growth hormone: Pit-1 dependence? Can. J. Physiol. Pharmacol. 2000; 78: 1013–1028.

    Article  PubMed  CAS  Google Scholar 

  42. Harvey S, Hull K. Neural growth hormone: an update. J. Mol. Neurosci. 2003; 20: 1–14.

    Article  PubMed  CAS  Google Scholar 

  43. Mori T, Devlin RH. Transgene and host growth hormone gene expression in pituitary and nonpituitary tissues of normal and growth hormone transgenic salmon. Mol. Cell Endocrinol. 1999; 149: 129–139.

    Article  PubMed  CAS  Google Scholar 

  44. Yang BY, Greene M, Chen TT, Early embryonic expression of the growth hormone family protein genes in the developing rainbow trout, Oncorhynclus mykiss. Mol. Reprod. Dev. 1999; 53: 127–134.

    Article  PubMed  CAS  Google Scholar 

  45. Yada T, Uchida K, Kajimura S, Azuma T, Hirano T, Grau EG. Immunomodulatory effects of prolactin and growth hormone in the tilapia, Oreochromis mossambicus. J. Endocrinol. 2002; 173: 483–492.

    Article  PubMed  CAS  Google Scholar 

  46. Schreiber E, Tobler A, Malipiero U, Schaffner W, Fontana A. cDNA cloning of human N-Oct3, a nervoussystem specific POU domain transcription factor binding to the octamer DNA motif. Nucleic Acids Res. 1993; 21: 253–258.

    Article  PubMed  CAS  Google Scholar 

  47. Takeda H, Matsuzaki T, Oki T, Miyagawa T, Amanuma H. A novel POU domain gene, zebrafish pou2: expression and roles of two alternatively spliced twin products in early development. Genes Dev. 1994; 8: 45–59.

    Article  PubMed  CAS  Google Scholar 

  48. Gao N, Zhang J, Rao MA, Case TC, Mirosevich J, Wang Y, Jin R, Gupta A, Rennie PS, Matusik RJ. The role of hepatocyte nuclear factor-3 alpha (Forkhead Box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol. Endocrinol. 2003; 17: 1484–1507.

    Article  PubMed  CAS  Google Scholar 

  49. Strahle U, Blader P, Ingham PW. Expression of axial and sonic hedgehog in wildtype and midline defective zebrafish embryos. Int. J. Dev. Biol. 1996; 40: 929–940.

    PubMed  CAS  Google Scholar 

  50. Stenson-Cox C, McNair A, Curley M, Smith T, Gannon F. A role for HNF-3 in the regulation of the HNF-1 gene of the Atlantic salmon. Mol. Genet. Genomics 2002; 266: 832–837.

    Article  PubMed  CAS  Google Scholar 

  51. Mao Z, Bonni A, Xia F, Nadal-Vicens M. Greenberg ME. Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science 1999; 286: 785–790.

    Article  PubMed  CAS  Google Scholar 

  52. Blaeser F, Ho N, Prywes R, Chatila TA. Ca(2+)-dependent gene expression mediated by MEF2 transcription factors. J. Biol. Chem. 2000; 275: 197–209.

    Article  PubMed  CAS  Google Scholar 

  53. Yue G, Yang L, Orban L. Characterization of microsatellites in the IGF-2 and GH genes of Asian seabass (Lates calcarifer). Mar. Biotechnol. 2001; 3: 1–3.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bruria Funkenstein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Almuly, R., Poleg-Danin, Y., Gorshkov, S. et al. Characterization of the 5′ flanking region of the growth hormone gene of the marine teleost, gilthead sea bream Sparus aurata: analysis of a polymorphic microsatellite in the proximal promoter. Fish Sci 71, 479–490 (2005). https://doi.org/10.1111/j.1444-2906.2005.00991.x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1111/j.1444-2906.2005.00991.x

Key Words

Navigation