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.
Similar content being viewed by others
References
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 214:2125–2139
Annunziata M, Granata R, Ghigo E (2011) The IGF system. Acta Diabetol 48:1–9
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 286:935–941
Cheatham B, Kahn CR (1995) Insulin action and the insulin signaling network. Endocr Rev 16:117–142
Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314S
Duan C, Plisetskaya EM, Dickhoff WW (1995) Expression of insulin-like growth factor-1 in normally and abnormally developing coho salmon (Oncorhynchus kisutch). Endocrinology 136:446–452
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 236:583–592
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 158:173–185
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 277:245–252
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
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 115:254–269
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 39:9801–9807
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 14:601–602
Jones JI, Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16:3–34
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 163:231–245
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 268:2655–2661
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 16:143–163
Le Roith D, Bondy C, Yakar S, Liu JL, Butler A (2001) The somatomedin hypothesis. Endocr Rev 22:53–74
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)
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 66:374–385
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 67:9–18
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)
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)
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)
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 82:155–169
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 143:1858–1871
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 129:1879–1884
Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-1 in fish. Biosci Biotechnol Biochem 64:1553–1562
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 173:365–375
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 151:332–341
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 149:253–260
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 145:237–246
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 37:74–83
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
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
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 87–130
Reinecke M (2010) Influences of the environment on the endocrine and paracrine fish growth hormone insulin-like growth factor-I system. J Fish Biol 76:1233–1254
Reinecke M, Collet C (1998) The phylogeny of the insulin-like growth factors. Int Rev Cytol 183:1–94
Rosenfeld RG, Roberts CT Jr (1999) The IGF system: molecular biology, physiology and clinical applications, 1st edn. Humana, Totowa
Sara VR, Hall K (1990) Insulin-like growth factors and their binding proteins. Physiol Rev 70:591–614
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
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 367:336–341
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 79:439–446
Werner H, Adamo M, Roberts CT, LeRoith D (1994) Molecular and cellular aspects of insulin-like growth factor action. Vitam Horm 48:1–58
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 145:214–224
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 150:140–150
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
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)
Rights and permissions
About this article
Cite this article
Chen, X., Wang, G., Lu, X. et al. Molecular characterization and expression profiles of two insulin-like growth factor 1 receptors during fasting and re-feeding in Siniperca chuatsi. Fish Sci 85, 349–360 (2019). https://doi.org/10.1007/s12562-019-01290-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-019-01290-7