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Fish Physiology and Biochemistry

, Volume 39, Issue 2, pp 263–275 | Cite as

Characterization of genes encoding prolactin and prolactin receptors in starry flounder Platichthys stellatus and their expression upon acclimation to freshwater

  • Gyeong Eon Noh
  • Han Kyu Lim
  • Jong-Myoung KimEmail author
Article

Abstract

This study aims to investigate the genes encoding prolactin (PRL) and prolactin receptors (PRLR) and their tissue-specific expression in starry flounder Platichthys stellatus. Starry flounder PRL gene consisting of five exons encodes an ORF of 212 amino acid residue comprised of a putative signal peptide of 24 amino acids and a mature protein of 188 amino acids. It showed amino acid identities of 73 % with tuna Thunnus thynnus, 71 % with black porgy Acanthopagrus schlegelii, 69 % with Nile tilapia Oreochromis niloticus, 64 % with pufferfish Takifugu rubripes, 63 % with rainbow trout Oncorhynchus mykiss, and 60 % with mangrove rivulus Kryptolebias marmoratus. Phylogenetic analysis of piscine PRLs also demonstrated a similarity between starry flounder and other teleosts but with a broad distinction from non-teleost PRLs. PRLR gene consists of eight exons encoding a protein of 528 amino acid residues. It showed a similarity to the PRLR2 subtype as reflected by amino acid identities of 54 % with A. schlegelii, 48.1 % with K. marmoratus, 46.3 % with tilapia O. mossambicus, and 46.1 % with O. niloticus PRLR2 as compared to PRLR1 isoform having less than 30 % identities. While mRNA transcript corresponding to PRL was detected only from the pituitary, most of PRLR mRNA was detected in the gill, kidney, and intestine, with a small amount in the ovary. The level of PRL transcript progressively increased during 6 days of acclimation to freshwater and then decreased but stayed higher than that of seawater at 60 days of acclimation. An opposite pattern of changes including a decrease at the beginning of the acclimation but a slight increase in the level osmolality was found as adaptation continued. The results support the osmoregulatory role of PRL signaling in starry flounder.

Keywords

Low salinity adaptation Prolactin Prolactin receptor Starry flounder Platichthys stellatus 

Notes

Acknowledgments

This work was supported by the project (RP-2012-AQ-049) at the National Fisheries Research and Development Institute. We would like to thank Prof. MS Noh, Dept of Statistics, PKNU, for his help on statistic analysis.

References

  1. Astola A, Ortiz M, Calduch-Giner JA, Pérez-Sánchez J, Valdivia MM (2003) Isolation of Sparus auratus prolactin gene and activity of the cis-acting regulatory elements. Gen Comp Endocrinol 134:57–61PubMedCrossRefGoogle Scholar
  2. Auperin B, Rentier-Delrue F, Martial JA, Prunet P (1994) Evidence that two tilapia (Oreochromis niloticus) prolactins have different osmoregulatory functions during adaptation to a hyperosmotic environment. J Mol Endocrinol 12:13–24PubMedCrossRefGoogle Scholar
  3. Ayson FG, Kaneko T, Tagawa M, Hasegawa S, Grau EG, Nishioka RS, David SK, Bern HA, Hirano T (1993) Effects of acclimation to hypertonic environment on plasma and pituitary levels of two prolactins and growth hormone in two species of tilapia, Oreochromis mossambicus and Oreochromis niloticus. Gen Comp Endocrinol 89:138–148PubMedCrossRefGoogle Scholar
  4. Boeuf G, Marc AM, Prunet P, Le Bail PY, Smal J (1994) Stimulation of parr-smolt transformation by hormonal treatment in Atlantic salmon (Salmo salar L.). Aquaculture 121:195–208CrossRefGoogle Scholar
  5. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA (1998) Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19:225–268PubMedCrossRefGoogle Scholar
  6. Boutet I, Lorin-Nebel C, De Lorgeril J, Guinand B (2007) Molecular characterization of prolactin and analysis of extrapituitary expression in the European sea bass Dicentrarchus labrax under various salinity conditions. Comp Biochem Physiol D 2:74–83Google Scholar
  7. Chang YJ, Min BH, Choi CY (2007) Black porgy Acanthopagrus schlegeli prolactin cDNA sequence: mRNA expression and blood physiological responses during freshwater acclimation. Comp Biochem Physiol B 147:122–128PubMedCrossRefGoogle Scholar
  8. De Ruiter AJ, Wendelaar BSE, Slijkhuis H, Baggerman B (1986) The effect of prolactin on fanning behavior in the male three-spined stickleback, Gasterosteus aculeatus L. Gen Comp Endocrinol 64:273–283PubMedCrossRefGoogle Scholar
  9. Doneen BA, Bewley TA, Li CH (1979) Studies on prolactin. Selective reduction of the disulfide bonds of the ovine hormone. Biochemistry 18:4851–4860PubMedCrossRefGoogle Scholar
  10. Eckert SM, Yada T, Shepherd BS, Stetson MH, Hirano T, Grau EG (2001) Hormonal control of osmoregulation in the channel catfish Ictalurus punctatus. Gen Comp Endocrinol 122:270–286PubMedCrossRefGoogle Scholar
  11. Fiol DF, Sanmarti E, Sacchi R, Kültz D (2007) A novel tilapia prolactin receptor is functionally distinct from its paralog. J Exp Biol 212:2007–2015CrossRefGoogle Scholar
  12. Freeman ME, Kanyicska B, Lerant A, Nagy G (2000) Prolactin: structure, function, and regulation of secretion. Physiol Rev 80:1523–1631PubMedGoogle Scholar
  13. Higashimoto Y, Nakao N, Ohkubo T, Tanaka M, Nakashima K (2001) Structure and tissue distribution of prolactin receptor mRNA in Japanese flounder (Paralichtys olivaceus): conserved and preferential expression in osmoregulatory organs. Gen Com Endocrinol 123:170–179CrossRefGoogle Scholar
  14. Huang X, Jiao B, Fung CK, Zhang Y, Ho WKK, Chan CB, Lin H, Wang D, Cheng CHK (2007) The presence of two distinct prolactin receptors in seabream with different tissue distribution patterns, signal transduction pathways and regulation of gene expression by steroid hormones. J Endocrinol 194:373–392PubMedCrossRefGoogle Scholar
  15. Imaoka T, Matsuda M, Mori T (2000) Extrapituitary expression of the prolactin gene in the goldfish, African clawed frog and mouse. Zool Sci 17:791–796CrossRefGoogle Scholar
  16. Khong HK, Kuah MK, Jaya-Ram A, Shu-Chien AC (2009) Prolactin receptor mRNA is upregulated in discus fish (Symphysodon aequifasciata) skin during parental phase. Comp Biochem Physiol B 153:18–28PubMedCrossRefGoogle Scholar
  17. Laiz-Carrión R, Fuentes J, Redruello B, Guzmán JM, Martín del Río 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 162:292–300CrossRefGoogle Scholar
  18. Lee HJ, Kim JM (2010) Molecular cloning and tissue-specific expression of melanocortin 4 receptor gene from olive flounder Paralichthys olivaceus. Fish Aquat Sci 13:263–271Google Scholar
  19. Lee KM, Kaneko T, Aida K (2006) Prolactin and prolactin receptor expressions in a marine teleost, pufferfish Takifugu rubripes. Gen Comp Endocrinol 146:318–328PubMedCrossRefGoogle Scholar
  20. Leena S, Oommen OV (2000) Hormonal control on enzymes of osmoregulation in a teleost, Anabas testudineus (Bloch): an in vivo and in vitro study. Endocr Res 26:169–287PubMedCrossRefGoogle Scholar
  21. Lim HK, Byun SG, Lee JH, Park SU, Kim YC (2007) Sexual maturity and reproductive cycle of starry flounder Platichthys stellatus cultured in indoor tank. J Aquacult 20:12–218Google Scholar
  22. Madsen SS, Nishioka RS, Bern HA (1997) Prolactin antagonises seawater acclimation in the anandromous striped bass, Morone saxatilis. In: Kawashima S, Kikuyama S (eds) Advances in comparative endocrinology, vol 2. Monduzzi Editore, Italy, pp 1011–1015Google Scholar
  23. Manzon LA (2002) The role of prolactin in fish osmoregulation: a review. Gen Comp Endocrinol 125:291–310PubMedCrossRefGoogle Scholar
  24. McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttleworth TJ (eds) Fish physiology, vol XIV. Academic Press, San Diego, pp 285–315Google Scholar
  25. McCormick SD (2001) Endocrine control of osmoregulation in fish. Am Zool 282:290–300Google Scholar
  26. Min BH, Lim HK, Chang YJ, Kim YS, Myeong JI (2009) Effects of 3,5,3′-triiodothyronine (T3) on osmoregulation following freshwater acclimation in starry flounder. Dev Reprod 13:313–320Google Scholar
  27. Nishioka RS, Kelley KM, Bern HA (1988) Control of prolactin and growth hormone secretion in teleost fishes. Zool Sci 5:267–280Google Scholar
  28. Pickford GE, Phillips JG (1959) Prolactin, a factor in promoting survival of hypophysectomized killifish in fresh water. Science 21:454–455CrossRefGoogle Scholar
  29. Riley LG, Hirano T, Grau EG (2003) Effects of transfer from seawater to fresh water on the growth hormone/insulin-like growth factor-I axis and prolactin in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol B 136:647–655PubMedCrossRefGoogle Scholar
  30. Rubin DA, Specker JL (1992) In vitro effects of homologous prolactins on testosterone production by testes of tilapia (Oreochromis mossambicus). Gen Comp Endocrinol 87:187–196CrossRefGoogle Scholar
  31. Sakamoto T, Shepherd BS, Madsen SS, Nishioka RS, Siharath K, Richman NH III, Bern HA, Grau EG (1997) Osmoregulatory actions of growth hormone and prolactin in an advanced teleost. Gen Comp Endocrinol 106:95–101PubMedCrossRefGoogle Scholar
  32. Sandra O, Sohm F, Luze AD, Prunet P, Edery M, Kelly PA (1995) Expression cloning of a cDNA encoding a fish prolactin receptor. Proc Natl Acad Sci USA 92:6037–6041PubMedCrossRefGoogle Scholar
  33. Santos CRA, Ingleton PM, Cavaco JEB, Kelly PA, Edery M, Power DM (2001) Cloning, characterization, and tissue distribution of prolactin receptor in the sea bream (Sparus aurata). Gen Comp Endocrinol 121:32–47PubMedCrossRefGoogle Scholar
  34. Seale AP, Riley LG, Leedom TA, Kajimura S, Dores RM, Hirano T, Grau EG (2002) Effects of environmental osmolality on release of prolactin, growth hormone, and ACTH from tilapia pituitary. Gen Com Endocrinol 128:91–101CrossRefGoogle Scholar
  35. Shepherd BS, Sakamoto T, Hyodo S, Ball C, Nishioka RS, Bern HA, Grau EG (1999) Is the primitive regulation of pituitary prolactin (tPRL177 and tPRL188) secretion and gene expression in the euryhaline tilapia (Oreochromis mossambicus) hypothalamic or environmental? J Endocrinol 161:121–129PubMedCrossRefGoogle Scholar
  36. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  37. Tomy S, Chang YM, Chen YH, Cao JC, Wang TP, Chang CF (2009) Salinity effects on the expression of osmoregulatory genes in the euryhaline black porgy Acanthopagrus schlegeli. Gen Comp Endocrinol 161:123–132PubMedCrossRefGoogle Scholar
  38. Yada T, Hirano T, Grau EG (1994) Changes in plasma levels of the two prolactins and growth hormone during adaptation to different salinities in the euryhaline tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 93:214–223PubMedCrossRefGoogle Scholar
  39. Zhang W, Tian J, Zhang L, Zhang Y, Li X, Lin H (2004) cDNA sequence and spatio-temporal expression of prolactin in the orange-spotted grouper, Epinephelus coioides. Gen Comp Endocrinol 136:134–142PubMedCrossRefGoogle Scholar
  40. Zhang Y, Long Z, Li Y, Yi S, Shi Y, Ma X, Huang W, Lu D, Zhu P, Liu X, Meng Z, Huang X, Cheng CHK, Lin H (2010) The second prolactin receptor in Nile tilapia (Oreochromis niloticus): molecular characterization, tissue distribution and gene expression. Fish Physiol Biochem 36:283–295PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Gyeong Eon Noh
    • 1
  • Han Kyu Lim
    • 2
  • Jong-Myoung Kim
    • 1
    Email author
  1. 1.Department of Fishery BiologyPukyong National UniversityBusanRepublic of Korea
  2. 2.Aquaculture Management TeamNational Fisheries Research & Development InstituteBusanRepublic of Korea

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