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Molecular characterization, tissue distribution, and expression regulation from fasting and re-feeding of two growth hormone receptors in mandarin fish Siniperca chuatsi

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  • Chemistry and Biochemistry
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Abstract

Growth hormone receptors (GHRs) are especially expressed in the muscle and liver tissues of mandarin fish Siniperca chuatsi. cDNAs of two GHR types (scGHR1 and scGHR2: 1999 and 1963 bp, encoding 638 and 578 amino acids, respectively) have been isolated and characterized in mandarin fish. Both receptors, formed through fish-specific genome duplication, have conserved FGEFS and box1 and 2 motifs. Partial compensatory growth was noted following 10-day re-feeding after 4-week fasting. After 1-week fasting, pituitary GH and muscle scGHR1 and scGHR2 mRNA levels and plasma GH concentrations increased (p < 0.05), while hepatic scGHR1 and scGHR2 mRNA expressions reduced rapidly (p < 0.05). Upon re-feeding, muscle scGHR1 and scGHR2 mRNA expressions decreased, whereas they increased rapidly in the liver, eventually normalizing. Pituitary GH mRNA expression increased to 5.1 times higher than that in the controls 3 days after re-feeding (p < 0.01), and normalized 7 days after re-feeding. The varying expression of scGHR1 and scGHR2 in different tissues suggests their distinct functions. Further, changes in GH, scGHR1, and scGHR2 mRNA expressions suggest their important roles in the growth of mandarin fish. Our results provide comparative insights into evolutionary origins and roles of GHR genes in teleost growth.

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References

  1. Walock CN, Kittilson JD, Sheridan MA (2014) Characterization of a novel growth hormone receptor-encoding cDNA in rainbow trout and regulation of its expression by nutritional state. Gene 533:286–294

    Article  PubMed  CAS  Google Scholar 

  2. Fuentes EN, Valdés JA, Molina A, Bjornsson BT (2013) Regulation of skeletal muscle growth in fish by the growth hormone-Insulin-like growth factor system. Gen Comp Endocrinol 192:136–148

    Article  PubMed  CAS  Google Scholar 

  3. Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S

    PubMed  CAS  Google Scholar 

  4. Reindl KM, Sheridan MA (2012) Peripheral regulation of the growth hormone insulin-like growth factor system in fish and other vertebrates. Comp Biochem Physiol A: Mol Integr Physiol 163:231–245

    Article  CAS  Google Scholar 

  5. Laviola L, Natalicchio A, Giorgino F (2007) The IGF-I signaling pathway. Curr Pharm Des 13:663–669

    Article  PubMed  CAS  Google Scholar 

  6. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285

    Article  PubMed  CAS  Google Scholar 

  7. LeRoith D, Bondy C, Yakar S, Liu JL, Butler A (2001) The somatomedin hypothesis. Endocr Rev 22:53–74

    Article  CAS  Google Scholar 

  8. Devlin RH, Yesaki TY, Donaldson EM, Du SJ, Hew CL (1995) Production of germline transgenic Pacific salmonids with dramatically increased growth performance. Can J Fish Aquat Sci 52:1376–1384

    Article  Google Scholar 

  9. Ahmed AS, Xiong F, Pang SC, He MD, Waters MJ, Zhu ZY, Sun YH (2011) Activation of GH signaling and GH-independent stimulation of growth in zebrafish by introduction of a constitutively activated GHR construct. Transgenic Res 20:557–567

    Article  PubMed  Google Scholar 

  10. Reinecke M, Björnsson BT, Dickhoff WW (2005) Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142:20–24

    Article  PubMed  CAS  Google Scholar 

  11. Bjornsson BT, Johansson V, Benedet S, Einarsdottir IE, Hildahl J, Agustsson T, Jonsson E (2004) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27:227–242

    Article  Google Scholar 

  12. Pérez-Sánchez J, Calduch-Giner JA, Mingarro M, Vega-Rubín de Celis S, Gómez-Requeni P, Saera-Vila A, Astola A, Valdivia MM (2002) Overview of fish growth hormone family. New insights in genomic organization and heterogeneity of growth hormone receptors. Fish Physiol Biochem 27:243–258

    Article  Google Scholar 

  13. Very NM, Kittilson JD, Norbeck LA, Sheridan MA (2005) Isolation, characterization, and distribution of two cDNAs encoding for growth hormone receptor in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol 140B:615–628

    Article  CAS  Google Scholar 

  14. Ma XL, Liu XC, Zhang Y, Zhu P, Ye W, Lin HR (2007) Two growth hormone receptors in Nile tilapia (Oreochromis niloticus): molecular characterization, tissue distribution and expression profiles in the gonad during the reproductive cycle. Comp Biochem Physiol 147B:325–339

    Article  CAS  Google Scholar 

  15. Li Y, Liu X, Zhang Y, Zhu P, Lin H (2007) Molecular cloning, characterization and distribution of two types of growth hormone receptor in orange-spotted grouper (Epinephelus coioides). Gen Comp Endocrinol 152:111–122

    Article  PubMed  CAS  Google Scholar 

  16. Jiao B, Huang X, Chan CB, Zhang L, Wang D, Cheng CH (2006) The co-existence of two growth hormone receptors in teleost fish and their differential signal transduction, tissue distribution and hormonal regulation of expression in seabream. J Mol Endocrinol 36:23–40

    Article  PubMed  CAS  Google Scholar 

  17. Saera-Vila A, Calduch-Giner JA, Pérez-Sánchez J (2007) Co-expression of IGFs and GH receptors (GHRs) in gilthead sea bream (Sparus aurata L.): sequence analysis of the GHR-flanking region. J Endocrinol 194:361–372

    Article  PubMed  CAS  Google Scholar 

  18. Saera-Vila A, Calduch-Giner JA, Pérez-Sánchez J (2005) Duplication of growth hormone receptor (GHR) in fish genome: gene organization and transcriptional regulation of GHR type I and II in gilthead sea bream (Sparus aurata). Gen Comp Endocrinol 142:193–203

    Article  PubMed  CAS  Google Scholar 

  19. Zhang P, Chi ML, Wen HS, Qian K, Ni M, Zhang YC, Huang ZJ, Song ZF, Chai SH (2015) Cloning of growth hormone receptor and salinity effects on the expression of its related genes in seabass Lateolabrax maculatus. Oceanol Limnol Sin 46:446–453

    Google Scholar 

  20. Fukamachi S, Meyer A (2007) Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J Mol Evol 65:359–372

    Article  PubMed  CAS  Google Scholar 

  21. Ellens ER, Kittilson JD, Hall JA, Sower SA, Sheridan MA (2013) Evolutionary origin and divergence of the growth hormone receptor family: insight from studies on sea lamprey. Gen Comp Endocrinol 192:222–236

    Article  PubMed  CAS  Google Scholar 

  22. Pierce AL, Fox BK, Davis LK, Visitacion N, Kitahashi T, Hirano T, Grau EG (2007) Prolactin receptor, growth hormone receptor, and putative somatolactin receptor in Mozambique tilapia: tissue specific expression and differential regulation by salinity and fasting. Gen Comp Endocrinol 154:31–40

    Article  PubMed  CAS  Google Scholar 

  23. Shimizu M, Fukada H, Hara A, Dickhoff W (2007) Response of the salmon somatotropic axis to growth hormone administration under two different salinities. Aquaculture 273:320–328

    Article  CAS  Google Scholar 

  24. Poppinga J, Kittilson J, McCormick SD, Sheridan MA (2007) Effects of somatostastin on the growth hormone insulin-like growth factors axis and seawater adaptation of rainbow trout (Oncorhynchus mykiss). Aquaculture 273:312–319

    Article  CAS  Google Scholar 

  25. Gabillard JC, Yao K, Vandeputte M, Gutierrez J, Le Bail PY (2006) Differential expression of two GH receptor mRNAs following temperature change in rainbow trout (Oncorhynchus mykiss). J Endocrinol 190:29–37

    Article  PubMed  CAS  Google Scholar 

  26. Sitjá-Bobadilla A, Calduch-Giner J, Saera-Vila A, Palenzuela O, Alvarez-Pellitero P, Pérez-Sánchez J (2008) Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol 24:610–619

    Article  PubMed  Google Scholar 

  27. Saera-Vila A, Calduch-Giner JA, Prunet P, Pérez-Sánchez J (2009) Dynamics of liver GH/IGF axis and selected stress markers in juvenile gilthead sea bream (Sparus aurata) exposed to acute confinement: differential stress response of growth hormone receptors. Comp Biochem Physiol 154A:197–203

    Article  CAS  Google Scholar 

  28. Norbeck LA, Sheridan MA (2010) Regulation of the growth hormone-insulin-like growth factor system by cortisol and thyroxine in rainbow trout. Annual Meeting of the Society for Integrative and Comparative Biology January, pp 3–7

  29. Birzniece V, Sata A, Ho KK (2009) Growth hormone receptor modulators. Rev Endocr Metab Disord 10:145–156

    Article  PubMed  CAS  Google Scholar 

  30. Pierce AL, Shimizu M, Beckman BR, Baker DM, Dickhoff WW (2005) Time course of the GH/IGF axis response to fasting and increased ration in Chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol 140:192–202

    Article  PubMed  CAS  Google Scholar 

  31. Ali M, Nicieza A, Wootton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fisheries 4:147–190

    Article  Google Scholar 

  32. Peterson BC, Bilodeau-Burgeois AL, Small BC (2009) Response of the somatotropic axis to alterations in feed intake of channel catfish (Ictalurus punctatus). Comp Biochem Physiol 153A:457–463

    Article  CAS  Google Scholar 

  33. Picha ME, Turano MJ, Tipsmark CK, Borski RJ (2008) Regulation of endocrine and paracrine sources of igfs and gh receptor during compensatory growth in hybrid striped sea bass (Morone chrysops × Morone saxatilis). J Endocrinol 199:81–94

    Article  PubMed  CAS  Google Scholar 

  34. Norbeck LA, Kittilson JD, Sheridan MA (2007) Resolving the growth-promoting and metabolic effects of growth hormone: differential regulation of GH-IGF-I system components. Gen Comp Endocrinol 151:332–341

    Article  PubMed  CAS  Google Scholar 

  35. Picha ME, Turano MJ, Beckman BR, Borski RR (2008) Endocrine biomarkers of growth and applications to aquaculture: a mini review of growth hormone, insulin-like growth factor (IGF)-I, and IGF-binding proteins and potential growth indicators in fish. N Am J Aquacult 70:196–211

    Article  Google Scholar 

  36. Liang XF, Lin XT, Li SQ, Liu JK (2008) Impact of enviromental and innate factors on the food habit of Chinese perch Siniperca chuatsi (Basilewsky) (Percichthyidae). Aquacult Res 39:150–157

    Article  Google Scholar 

  37. Chu WY, Fu GH, Chen J, Chen DG, Meng T, Zhou RX, Xia XJ, Zhang JS (2010) Gene expression profiling in muscle tissues of the commercially important teleost, Siniperca chuatsi. Aquacult Int 18:667–678

    Article  CAS  Google Scholar 

  38. Luo D, Sun JJ, Lu X, Liu LZ, Chen SJ, Li GF (2011) Comparative sperm ultrastructure of three species in Siniperca (Teleostei:Perciformes: Sinipercidae). Micron 42:884–891

    Article  PubMed  Google Scholar 

  39. Wang PF, Zeng S, Xu P, Zhou L, Zeng L, Lu X, Wang HF, Li GF (2014) Identification and expression analysis of two HSP70 isoforms in mandarin fish Siniperca chuatsi. Fish Sci 80:803–817

    Article  CAS  Google Scholar 

  40. Wang HF, Sun JJ, Lu X, Wang PF, Xu P, Zeng L, Yu DG, Li GF (2013) Identification of insulin-like growth factor I gene polymorphisms using high-resolution melting and its effect on growth traits in sinipercid species. Fish Sci 79:439–446

    Article  Google Scholar 

  41. Langenheim JF, Tan D, Walker AM, Chen WY (2006) Two wrongs can make a right: dimers of prolactin and growth hormone receptor antagonists behave as agonists. Mol Endocrinol 20:661–674

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  42. Møller N, Jørgensen JO (2009) Effects of growth hormone on glucose, lipid, and protein metabolism in human subjects. Endocr Rev 30:152–177

    Article  PubMed  Google Scholar 

  43. Nakao N, Higashimoto Y, Ohkubo T, Yoshizato H, Nakai N, Nakashima K, Tanaka M (2004) Characterization of structure and expression of the growth hormone receptor gene of the Japanese flounder (Paralichtys olivaceus). J Endocrinol 182:157–164

    Article  PubMed  CAS  Google Scholar 

  44. Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Swanson P, Dickhoff WW (2004) Salmon growth hormone receptor: molecular cloning, ligand specificity, and response to fasting. Gen Comp Endocrinol 139:67–71

    Google Scholar 

  45. Deng L, Zhang WM, Lin HR, Cheng CH (2004) Effects of food deprivation on expression of growth hormone receptor and proximate composition in liver of black seabream Acanthopagrus schlegeli. Comp Biochem Physiol 137B:421–432

    Article  CAS  Google Scholar 

  46. Small BC, Murdock CA, Waldbieser GC, Peterson BC (2006) Reduction in channel catfish hepatic growth hormone receptor expression in response to food deprivation and exogenous cortisol. Domest Anim Endocrinol 31:340–356

    Article  PubMed  CAS  Google Scholar 

  47. Fox BK, Breves JP, Davis LK, Pierce AL, Hirano T, Grau EG (2010) Tissue-specific regulation of the growth hormone/insulin-like growth factor axis during fasting and re-feeding: importance of muscle expression of IGF-I and IGF-II mRNA in the tilapia. Gen Comp Endocrinol 166:573–580

    Article  PubMed  CAS  Google Scholar 

  48. Björnsson BT, Johansson V, Benedet S, Einarsdottir IE, Hildahl J, Agustsson T (2002) Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol Biochem 27:227–242

    Article  Google Scholar 

  49. Small BC, Peterson BC (2005) Establishment of a time-resolved fluoroimmunoassay for measuring plasma insulin-like growth factor I (IGF-I) in fish: effect of fasting on plasma concentrations and tissue mRNA expression of IGF-I and growth hormone (GH) in channel catfish (Ictalurus punctatus). Domest Anim Endocrinol 28:202–215

    Article  PubMed  CAS  Google Scholar 

  50. Fox BK, Riley LG, Hirano T, Grau EG (2006) Effects of fasting on growth hormone, growth hormone receptor, and insulin-like growth factor-I axis in seawater-acclimated tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 148:340–347

    Article  PubMed  CAS  Google Scholar 

  51. Uchida K, Kajimura S, Riley LG, Hirano T, Aida K, Grau EG (2003) Effects of fasting on growth hormone/insulin-like growth factor-I axis in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol 134A:429–439

    Article  CAS  Google Scholar 

  52. Duan C, Plisetskaya EM (1993) Nutritional regulation of insulin-like growth factor-I mRNA expression in salmon tissues. J Endocrinol 139:243–252

    Article  PubMed  CAS  Google Scholar 

  53. Pedroso FL, de Jesus-Ayson EG, Cortado HH, Hyodo S, Ayson FG (2006) Changes in mRNA expression of grouper (Epinephelus coioides) growth hormone and insulin-like growth factor I in response to nutritional status. Gen Comp Endocrinol 145:237–246

    Article  PubMed  CAS  Google Scholar 

  54. Ayson FG, de Jesus-Ayson EG, Takemura A (2007) mRNA expression patterns for GH, PRL, SL, IGF-I and IGF-II during altered feeding status in rabbitfish. Gen Comp Endocrinol 150:196–204

    Article  PubMed  CAS  Google Scholar 

  55. Very NM, Sheridan MA (2007) Somatostatin regulates hepatic growth hormone sensitivity by internalizing growth hormone receptors and by decreasing transcription of growth hormone receptor mRNAs. Am J Physiol 292:R1956–R1962

    CAS  Google Scholar 

  56. An X, Wang L, Hou J, Li G, Song Y, Wang J, Yang M, Cui Y, Cao B (2011) Novel polymorphisms of goat growth hormone and growth hormone receptor genes and their effects on growth traits. Mol Biol Rep 38:4037–4043

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Educational Commission of Guangdong Province, China (No. cxzd1104), the Foshan Innovative and Entepreneurial Research Team Program (No. 2014IT100122), the Special Fund for Agro-scientific Research in the Public Interest (No. 201303048), the Science and Technology Planning Project of Guangdong Province (No. 2007A020300001-1; No. 2012A020800001; No. 2008A020100003), the Cooperative Project of Guangdong Province (No. 2011B090400179) and the Agriculture Science Technology Achievement Transformation project (No.2 012GB2E000338).

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Lu, X., Gu, Y., Hou, X. et al. Molecular characterization, tissue distribution, and expression regulation from fasting and re-feeding of two growth hormone receptors in mandarin fish Siniperca chuatsi . Fish Sci 82, 155–169 (2016). https://doi.org/10.1007/s12562-015-0941-0

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