Advertisement

Molecular characterization and expression profiles of two insulin-like growth factor 1 receptors during fasting and re-feeding in Siniperca chuatsi

  • Xiaoli Chen
  • Gongpei Wang
  • Xue Lu
  • Peng Xu
  • Shuang Zeng
  • Zhi Chen
  • Qiaoying Zhu
  • Guifeng LiEmail author
Original Article Biology

Abstract

Two distinct insulin-like growth factor 1 receptors of the mandarin fish Siniperca chuatsi (scIGF1R1 and scIGF1R2) were cloned and characterized in this study. The complementary DNA of scIGF1R1 [4254 base pairs (bp)] and scIGF1R2 (4248 bp) encoded 1418 and 1416 amino acids, respectively. Both receptors contained a single short transmembrane domain, two receptor L domains and a furin-like cysteine-rich domain. Phylogenetic analysis revealed that scIGF1R1 and scIGF1R2 were clustered in two different branches. Both receptors were expressed in all tissues tested, and the expression levels were relatively high in the gonad, liver and brain. During the first week of starvation, the expression levels of both receptors were increased in the muscle and liver, whereas hepatic scIGF1 expression was decreased. After re-feeding, the expression levels of both receptors were gradually restored to the pre-starvation levels in the liver and muscle. The concentration of serum scIGF1 did not exhibit regular changes compared with the control group during fasting and re-feeding. The varying expression profiles of the scIGF1Rs among tissues indicated that these receptors have distinct, tissue-specific roles. Furthermore, the changes in expression levels of scIGF1, scIGF1R1s during fasting and re-feeding provided evidence to support the link between nutritional status and gene expression related to growth and development.

Keywords

Mandarin fish Phylogenetic analysis Starvation Expression profile Nutritional status Gene expression Growth 

Notes

Acknowledgments

This project 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 (nos. 2007A020300001-1, 2012A020800001, 2008A020100003), the Cooperative Project of Guangdong Province (no. 2011B090400179) and the Agriculture Science Technology Achievement Transformation project (no. 2012GB2E000338). The authors appreciate the support of the Modern Agriculture Talents Support Program (2016-2020), and are grateful to Foshan Nanhai Bairong Aquatic Breeding for providing the breeding ground for early fish seedlings. The authors would also like to thank Linqiang Han, Guiyang Li and Xiuwen Ren for providing assistance during the breeding process.

Supplementary material

12562_2019_1290_MOESM1_ESM.pptx (1.3 mb)
Fig. S1 Multiple sequence alignment of the IGF1Rs from Siniperca chuatsi and other teleost species. The amino acid sequences are listed as standard single-letter designations, and gaps are marked by dots. Different background colours represent different conservation, as follows: white non-conserved, blue more than 50% conserved, red more than 80% conserved, and black completely conserved. Sequences used in the alignment: Paralichthys olivaceus fIGF1R1 BAB83669.1, Siniperca chuatsi IGF1R1 MF598471, Sparus aurata IGF1Ra KJ591052.1, Takifugu rubripes IGF1R XM_003967057.2, Neolamprologus brichardi IGF1R1 XP_006789448.1, Oreochromis niloticus IGF1R XP_010731390.1, Cyprinus carpio IGF1Ra AY144591.1, S. chuatsi IGF1R2 MF598472, Larimichthys crocea IGF1R XP_010731390.1, Paralichthys olivaceus fIGF1R2 BAB83670.1, Danio rerio IGF1Rb AAI63581.1 (pptx 1283 kb)

References

  1. Amaral IP, Johnston IA (2011) Insulin-like growth factor (IGF) signalling and genome-wide transcriptional regulation in fast muscle of zebrafish following a single-satiating meal. J Exp Biol 214:2125–2139CrossRefGoogle Scholar
  2. Annunziata M, Granata R, Ghigo E (2011) The IGF system. Acta Diabetol 48:1–9CrossRefGoogle Scholar
  3. Castillo J, Codina M, Martinez ML, Navarro I, Gutierrez J (2004) Metabolic and mitogenic effects of IGF1 and insulin on muscle cells of rainbow trout. Am J Physiol Regul Integr Comp Physiol 286:935–941CrossRefGoogle Scholar
  4. Cheatham B, Kahn CR (1995) Insulin action and the insulin signaling network. Endocr Rev 16:117–142Google Scholar
  5. Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314SCrossRefGoogle Scholar
  6. Duan C, Plisetskaya EM, Dickhoff WW (1995) Expression of insulin-like growth factor-1 in normally and abnormally developing coho salmon (Oncorhynchus kisutch). Endocrinology 136:446–452CrossRefGoogle Scholar
  7. Dyer AR, Barlow CG, Bransden MP, Carter CG, Glencross BD, Richardson N, Thomas PM, Williams KC, Carragher JF (2004) Correlation of plasma IGF-1 concentrations and growth rate in aquacultured finfish: a tool for assessing the potential of new diets. Aquaculture 236:583–592CrossRefGoogle Scholar
  8. Eliès G, Duval H, Bonnec G, Wolff J, Boeuf G, Boujard D (1999) Insulin and insulin-like growth factor-1 receptors in an evoluted fish, the turbot: cDNA cloning and mRNA expression. Mol Cell Endocrinol 158:173–185CrossRefGoogle Scholar
  9. Frystyk J, Delhanty PJ, Skjaerbaek C, Baxter RC (1999) Changes in the circulating IGF system during short-term fasting and refeeding in rats. Am J Physiol 277:245–252Google Scholar
  10. 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 192:136–148CrossRefGoogle Scholar
  11. Greene MW, Chen TT (1999) Characterization of teleost insulin receptor family members. II. Developmental expression of insulin-like growth factor type I receptor messenger RNAs in rainbow trout. Gen Comp Endocrinol 115:254–269CrossRefGoogle Scholar
  12. He JN, Zhang BY, Chu MX, Wang PQ, Feng T, Cao GL, Di R, Fang L, Huang DW, Tang QQ, Li N (2012) Polymorphism of insulin-like growth factor-1 gene and its association with litter size in Small Tail Han sheep. Mol Biol Rep 39:9801–9807CrossRefGoogle Scholar
  13. He S, Liang XF, Sun J, Li L, Yu Y, Huang W, Tao YX (2013) Insights into food preference in hybrid F1 of Siniperca chuatsi (♀) × Siniperca scherzeri (♂) mandarin fish through transcriptome analysis. BMC Genom 14:601–602CrossRefGoogle Scholar
  14. Jones JI, Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16:3–34Google Scholar
  15. Katie MR, Mark AS (2012) Peripheral regulation of the growth hormone-insulin-like factor system in fish and other vertebrates. Comp Biochem Physiol A Mol Integr Physiol 163:231–245CrossRefGoogle Scholar
  16. Kato H, Faria TN, Stannard B, Roberts CT Jr, LeRoith D (1993) Role of tyrosine kinase activity in signal transduction by the insulin-like growth factor-I (IGF-I) receptor. Characterization of kinase-deficient IGF-I receptors and the action of an IGF-I-mimetic antibody (alpha IR-3). J Biol Chem 268:2655–2661Google Scholar
  17. Le Roith D, Werner H, Beitner-Johnson D Jr, Roberts CT (1995) Molecular and cellular aspects of the insulin-like growth factor-1 receptor. Endocr Rev 16:143–163CrossRefGoogle Scholar
  18. Le Roith D, Bondy C, Yakar S, Liu JL, Butler A (2001) The somatomedin hypothesis. Endocr Rev 22:53–74CrossRefGoogle Scholar
  19. Liang XF (1996) Study on Mandarin fish and its culture home and abroad. Fish Sci Technol Inf 23:13–17 (in Chinese with English abstract) Google Scholar
  20. Liu D, Rutter WJ, Wang LH (1992) Enhancement of transforming potential of human insulin-like growth factor-1 receptor by N-terminal truncation and fusion to avian sarcoma virus UR2 gag sequence. J Virol 66:374–385Google Scholar
  21. Liu D, Rutter WJ, Wang LH (1993) Modulating effects of the extracellular sequence of the human insulin-like growth factor-1 receptor on its transforming and tumorigenic potential. J Virol 67:9–18Google Scholar
  22. Liu J, Zhao JL, Zhang M, Dai W (2011) Full-length cDNA cloning and tissue expression of insulin-like growth factor-I in the mandarin fish, Siniperca chuatsi. Chin J Zool 46:28–36 (in Chinese with English abstract) Google Scholar
  23. Liu J, Zhao JL, Zhang M, Dai W (2012) Cloning and expression of full-length cDNA of insulin-like growth factor-II in mandarin fish Siniperca chuatsi. J Dalian Ocean Univ 27:495–501 (in Chinese with English abstract) Google Scholar
  24. Lu SQ, Liu F, Liu Z, Zhang JS, Xie XM (2008) Comparison in cloning and sequence of growth hormone gene in three species of genus siniperca. Oceanol Limnol Sin 39:354–361 (in Chinese with English abstract) Google Scholar
  25. Lu X, Gu YM, Hou XC, Wang HF, Wang PF, Xu P, Zeng L, Zhou L, Li GF (2016) Molecular characterization, tissue distribution, and expression regulation from fasting and re-feeding of two growth hormone receptors in mandarin fish Siniperca chuatsi. Fish Sci 82:155–169CrossRefGoogle Scholar
  26. Maures T, Cha SJ, Xu B, Sun H, Ding J, Duan C (2002) Structural, biochemical, and expression analysis of two distinct insulin-like growth factor-1 receptors and their ligands in zebrafish. Endocrinology 143:1858–1871CrossRefGoogle Scholar
  27. Maxwell A, Butterwick R, Batt RM, Camacho-Hübner C (1999) Serum insulin-like growth factor (IGF)-I concentrations are reduced by short-term dietary restriction and restored by refeeding in domestic cats (Felis catus). J Nutr 129:1879–1884CrossRefGoogle Scholar
  28. Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-1 in fish. Biosci Biotechnol Biochem 64:1553–1562CrossRefGoogle Scholar
  29. Nakao N, Tanaka M, Higashimoto Y, Nakashima K (2002) Molecular cloning, identification and characterization of four distinct receptor subtypes for insulin and IGF1 in Japanese flounder, Paralichthys olivaceus. J Endocrinol 173:365–375CrossRefGoogle Scholar
  30. Norbeck LA, Kittilson JD, Sheridan MA (2007) Resolving the growth-promoting and metabolic effects of growth hormone: differential regulation of GH-IGF1 system components. Gen Comp Endocrinol 151:332–341CrossRefGoogle Scholar
  31. Nordgarden U, Fjelldal PG, Hansen T, Bjornsson BT, Wargelius A (2006) Growth hormone and insulin-like growth factor-1 act together and independently when regulating growth in vertebral and muscle tissue of Atlantic salmon postsmolts. Gen Comp Endocrinol 149:253–260CrossRefGoogle Scholar
  32. 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-1 in response to nutritional status. Gen Comp Endocrinol 145:237–246CrossRefGoogle Scholar
  33. Peterson BC, Waldbieser GC (2009) Effects of fasting on IGF1, IGF-2, and IGF-binding protein mRNA concentrations in channel catfish (Ictalurus punctatus). Domest Anim Endocrinol 37:74–83CrossRefGoogle Scholar
  34. 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 140:192–202CrossRefGoogle Scholar
  35. 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 163:231–245CrossRefGoogle Scholar
  36. Reinecke M (2006) Insulin-like growth factor I and II in fish. In: Reinecke M et al (eds) Fish endocrinology, vol 1. Science Publishers, Enfield, pp 87–130Google Scholar
  37. Reinecke M (2010) Influences of the environment on the endocrine and paracrine fish growth hormone insulin-like growth factor-I system. J Fish Biol 76:1233–1254CrossRefGoogle Scholar
  38. Reinecke M, Collet C (1998) The phylogeny of the insulin-like growth factors. Int Rev Cytol 183:1–94CrossRefGoogle Scholar
  39. Rosenfeld RG, Roberts CT Jr (1999) The IGF system: molecular biology, physiology and clinical applications, 1st edn. Humana, TotowaCrossRefGoogle Scholar
  40. Sara VR, Hall K (1990) Insulin-like growth factors and their binding proteins. Physiol Rev 70:591–614CrossRefGoogle Scholar
  41. 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 31:340–356CrossRefGoogle Scholar
  42. Wang DS, Jiao B, Hu C, Huang X, Liu Z, Cheng CH (2008) Discovery of a gonad-specific IGF subtype in teleost. Biochem Biophys Res Commun 367:336–341CrossRefGoogle Scholar
  43. Wang HF, Sun JJ, Lu X, Wang PF, Xu P, Zeng L, Yu DG, Li GF (2013) Identifcation of insulin-like growth factor-1 gene polymorphisms using high-resolution melting and its effect on growth traits in sinipercid species. Fish Sci 79:439–446CrossRefGoogle Scholar
  44. Werner H, Adamo M, Roberts CT, LeRoith D (1994) Molecular and cellular aspects of insulin-like growth factor action. Vitam Horm 48:1–58CrossRefGoogle Scholar
  45. Wilkinson RJ, Porter M, Woolcott H, Longland R, Carragher JF (2006) Effects of aquaculture related stressors and nutritional restriction on circulating growth factors (GH, IGF-I and IGF-II) in Atlantic salmon and rainbow trout. Comp Biochem Physiol A 145:214–224CrossRefGoogle Scholar
  46. Wuertz S, Nitsche A, Jastroch M, Gessner J, Klingenspor M, Kirschbaum F, Kloas W (2007) The role of the IGF1 system for vitellogenesis in maturing female sterlet, Acipenser ruthenus Linnaeus, 1758. Gen Comp Endocrinol 150:140–150CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2019

Authors and Affiliations

  • Xiaoli Chen
    • 1
  • Gongpei Wang
    • 1
  • Xue Lu
    • 1
    • 2
  • Peng Xu
    • 1
  • Shuang Zeng
    • 1
  • Zhi Chen
    • 1
  • Qiaoying Zhu
    • 1
  • Guifeng Li
    • 1
    Email author
  1. 1.Guangdong Provincial Engineering Technology Research Center for Healthy Breeding of Important Economic Fish, State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory for Aquatic Economic Animals, Institute of Aquatic Economic Animals, School of Life SciencesSun Yat-sen UniversityGuangzhouPeople’s Republic of China
  2. 2.Guangdong Haid Group Company LimitedGuangzhouPeople’s Republic of China

Personalised recommendations