Abstract
The full-length cDNA coding IGF-I was cloned from the liver of Yellow catfish Pelteobagrus fulvidraco. The tissue distributions of IGF-I in adults were then analyzed by using real-time PCR. The effects of starvation (3 weeks) and subsequent refeeding (3 weeks) on the compensatory growth performance in juvenile fish weighing 3.80 ± 0.78 g and hepatic IGF-I mRNA expressions were also investigated. The cDNA obtained covered 884 bp with an open reading frame of 480 bp encoding 159 amino acids. It is composed of a signal peptide with 41 amino acids (AAs), a mature peptide comprising the B, C, A, and D domains (71 AAs) and E domain of 47 AAs. Sequence alignment and phylogenetic analysis revealed a high degree of conservation (71–87%) among the species of Siluriformes and some closely related species. In adults, the highest IGF-I expression was observed in the liver, followed by the brain, whereas relatively low expressions were detected in muscle and stomach. Both body weight and length increased significantly in fish fed to satiation continuously. Body weight, body length, condition factor, and hepatic IGF-I expressions were all decreased remarkably with increasing starvation times, but increased significantly after refeeding. The results showed that the expression of IGF-I was positively correlated with feed intakes and IGF-I may play a key regulatory role for somatic growth induced by compensatory growth in Yellow catfish.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali M, Nicieza A, Wootton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190. https://doi.org/10.1046/j.1467-2979.2003.00120.x
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Biga PR, Schelling GT, Hardy RW, Cain KD, Overturf K, Ott TL (2004) The effects of recombinant bovine somatotropin (rbST) on tissue IGF-I, IGF-I receptor, and GH mRNA levels in rainbow trout, Oncorhynchus mykis. Gen Comp Endocrinol 135:324–333. https://doi.org/10.1016/j.ygcen.2003.10.014
Caelers A, Berishvili G, Meli ML, Eppler E, Reinecke M (2004) Establishment of a real-time RT-PCR for the determination of absolute amounts of IGF-I and IGF-II gene expression in liver and extrahepatic sites of the tilapia. Gen Comp Endocrinol 137:196–204. https://doi.org/10.1016/j.ygcen.2004.03.006
Cameron C, Moccia R, Azevedo PA, Leatherland JF (2007) Effect of diet and ration on the relationship between plasma GH and IGF-1 concentrations in Arctic charr, Salvelinus alpinus (L.). Aquac Res 38:877–886
Cao QP, Duguay SJ, Plisetskaya E, Steiner DF, Chan SJ (1989) Nucleotide sequence and growth hormone-regulated expression of salmon insulin-like growth factor I mRNA. Mol Endocrinol 3(12):2005–2010
Castillo J, Codina M, Martínez ML, Navarro I, Gutiérrez J (2004) Metabolic and mitogenic effects of IGF-I and insulin on muscle cells of rainbow trout. Am J Phys Regul Integr Comp Phys 283:R647–R652
Clay LA, Wang SY, Wolters WR, Peterson BC, Waldbieser GC (2005) Molecular characterization of the insulin-like growth factor-I (IGF-I) gene in channel catfish (Ictalurus punctatus). Biochim Biophys Acta 1731:139–148. https://doi.org/10.1016/j.bbaexp.2005.10.001
Dong Z, Ge J, Li K, Xu Z, Liang D, Li J, Li J, Jia W, Li Y, Dong X, Cao S, Wang X, Pan J, Zhao Q (2011) Heritable targeted inactivation of myostatin gene in yellow catfish (Pelteobagrus fulvidraco) using engineered zinc finger nucleases. PLoS One 6(12):e28897
Duan C, Duguay SJ, Plisetskaya EM (1993) Insulin-like growth factor I (IGF-I) mRNA expression in coho salmon, Oncorhynchus kisutch: tissue distribution and effects of growth hormone/prolactin family proteins. Fish Physiol Biochem 11:371–379. https://doi.org/10.1007/BF00004587
Duguay SJ, Swanson P, Dickhoff WW (1994) Differential expression and hormonal regulation of alternatively spliced IGF-I mRNA transcripts in salmon. J Mol Endocrinol 12:25–37. https://doi.org/10.1677/jme.0.0120025
Imsland AK, Foss A, Roth B, Stefansson SO, Vikingstad E, Pedersen S, Sandvik T, Norberg B (2008) Plasma insulin-like growth factor-I concentrations and growth in juvenile halibut (Hippoglossus hippoglossus): effects of photoperiods and feeding regimes. Comp Biochem Physiol A Mol Integr Physiol 151:66–70. https://doi.org/10.1016/j.cbpa.2008.05.179
Inoue K, Iwatani H, Takei Y (2003) Growth hormone and insulin-like growth factor I of a Euryhaline fish Cottus kazika: cDNA cloning and expression after seawater acclimation. Gen Comp Endocrinol 131:77–84. https://doi.org/10.1016/S0016-6480(02)00650-0
Jia B, St-Hilaire S, Singh K, Gardner IA (2016) Farm-level returns and costs of yellow catfish (pelteobagrus fulvidraco) aquaculture in Guangdong and Zhejiang provinces, China. Aquaculture Reports 4(C):48–56
Jobling M (2010) Are compensatory growth and catch-up growth two sides of the same coin? Aquac Int 18:501–510. https://doi.org/10.1007/s10499-009-9260-8
Jobling M, Meløy OH, Santos JD, Christiansen B (1994) The compensatory growth response of the Atlantic cod: effects of nutritional history. Aquac Int 2:75–90. https://doi.org/10.1007/BF00128802
Jones JI, Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16:3–34. https://doi.org/10.1210/edrv-16-1-3
Kershaw EE, Flier JS (2004) Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 89:2548–2556. https://doi.org/10.1210/jc.2004-0395
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C T method. METHODS 25:402–408. https://doi.org/10.1006/meth.2001.1262
McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. Am Zool 41:781–794
Ministry of Agriculture of the People’s Republic of China (2016) China fishery statistical yearbook. Chinese Agricultural Press, Beijing, p 31
Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotechnol Biochem 64:1553–1562. https://doi.org/10.1271/bbb.64.1553
Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 4. Elsevier, Amsterdam, pp 393–434
Pérez-Sánchez J, Bail PYL (1999) Growth hormone axis as marker of nutritional status and growth performance in fish. Aquaculture 177:117–128. https://doi.org/10.1016/S0044-8486(99)00073-3
Pozios KC, Ding J, Degger B, Upton Z, Duan C (2001) IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinase-signaling pathways. Am J Phys Regul Integr Comp Phys 280:R1230–R1239
Sara VR, Hall K (1990) Insulin-like growth factors and their binding proteins. Phys Rev 70:591–614. https://doi.org/10.1152/physrev.1990.70.3.591
Sciara AA, Somoza GM, Arranz SE (2008) Insulin-like growth factor-I of pejerrey, Odontesthes bonariensis: cDNA characterization, tissue distribution and expression profiles after growth hormone administration. J Exp Zool 309:407–418. https://doi.org/10.1002/jez.466
Shamblott MJ, Cheng CM, Bolt D, Chen TT (1995) Appearance of insulin-like growth factor mRNA in the liver and pyloric ceca of a teleost in response to exogenous growth hormone. P NATL ACAD SCI USA 92:6943–6946. https://doi.org/10.1073/pnas.92.15.6943
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Vong QP, Chan KM, Cheng CH (2003) Quantification of common carp (Cyprinus carpio) IGF-I and IGF-II mRNA by real-time PCR: differential regulation of expression by GH. J Endocrinol 178:513–521
Wang Y, Cui Y, Yang Y, Cai F (2000) Compensatory growth in hybrid tilapia, Oreochromis mossambicus × O. niloticus, reared in seawater. AQUACULTURE 189:101–108. https://doi.org/10.1016/S0044-8486(00)00353-7
Weber G, Sullivan CV (2000) Effects of insulin-like growth factor-I on in vitro final oocyte maturation and ovarian steroidogenesis in striped bass, Morone saxatilis. Biol Reprod 63:1049–1057
Won ET, Borski RJ (2013) Endocrine regulation of compensatory growth in fish. Front Endocrinol 4:1–13
Wu S, Gao T, Zheng Y, Wang W, Cheng Y, Wang G (2010) Microbial diversityof intestinal contents and mucus in yellow catfish (Pelteobagrus fulvidraco). Aquaculture 303(1):1–7
Xu Y, Zang K, Liu X, Shi B, Li C, Shi X (2014) Insulin-like growth factors I and II in starry flounder (Platichthys stellatus): molecular cloning and differential expression during embryonic development. Fish Physiol Biochem 41:139–152. https://doi.org/10.1007/s10695-014-0012-y
Yakar S, Rosen CJ, Beamer WG, Ackert-Bicknell CL, Wu Y, Liu JL, Ooi GT, Setser J, Frystyk J, Boisclair YR, LeRoith D (2002) Circulating levels of IGF-I directly regulate bone growth and density. J Clin Invest 110:771–781. https://doi.org/10.1172/JCI15463
Funding
This study was funded by the Major Project for New Cultivar Breeding of Jiangsu Province (PZCZ201742) and the China Agriculture Research System (CARS-46). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable Institutional Animal Care and Use Committee (IACUC) of Nanjing Agricultural University were followed by the authors. All efforts were made to minimize the suffering of the animals.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Qin, Q., Chen, X., Zhu, X. et al. Insulin-like growth factor I of Yellow catfish (Pelteobagrus fulvidraco): cDNA characterization, tissue distribution, and expressions in response to starvation and refeeding. Fish Physiol Biochem 46, 177–186 (2020). https://doi.org/10.1007/s10695-019-00707-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-019-00707-5