Abstract
In this study, the cDNA encoding insulin-like growth factor-binding protein-1 (IGFBP-1) was cloned from the liver of goldfish (Carassius auratus). The obtained goldfish IGFBP-1 cDNA sequence was 1037 bp in length and had an open reading frame of 789 bp encoding a predicted polypeptide of 262 amino acid residues. IGFBP-1 transcript was detected in all tested central nervous and peripheral tissues. The relatively higher levels of IGFBP-1 mRNA were observed in the liver, gill, kidney, heart, spleen, fat and testis, while the lower levels were found in all different regions of brain, muscle and intestine. In the skin, IGFBP-1 mRNA expression level was extremely low. The IGFBP-1 mRNA expression level in liver was significantly elevated after feeding. With cadmium exposure for 24 h, IGFBP-1 mRNA expression levels in spleen and liver were significantly increased at different cadmium concentrations ranging from 0.5 to 10 ppm. The results in this study provided the data regarding molecular characteristics and expression patterns of IGFBP-1 in goldfish and showed that the expression of IGFBP-1 mRNA might be associated with metabolic status and heavy metal stress and regulated by metabolic factors and cadmium in fish.
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References
Alvarez SM, Gómez NN, Scardapane L, Zirulnik F, Martínez D, Giménez MS (2004) Morphological changes and oxidative stress in rat prostate exposed to a non-carcinogenic dose of cadmium. Toxicol Lett 153(3):365–376
Ayres RU (1992) Toxic heavy metals: materials cycle optimization. Proc Natl Acad Sci USA 89(3):815–820
Bartosiewicz MJ, JenkinsD Penn S, Emery J, Buckpitt A (2001) Unique gene expression patterns in liver and kidney associated with exposure to chemical toxicants. J Pharmacol Exp Ther 297(3):895–905
Baxter RC (2000) Insulin-like growth factor (IGF)-binding proteins: interactions with IGFs and intrinsic bioactivities. Am J Physiol Endocrinol Metab 278(6):E967–E976
Chen L, Liu L, Luo Y, Huang S (2008) MAPK and mTOR pathways are involved in cadmium-induced neuronal apoptosis. J Neurochem 105(1):251–261
Choi CY, An KW, Nelson ER, Habibi HR (2007) Cadmium affects the expression of metallothionein (MT) and glutathione peroxidase (GPX) mRNA in goldfish, Carassius auratus. Comp Biochem Physiol C: Toxicol Pharmacol 145(4):595–600
Clemmons DR (1997) Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev 8(1):45–62
Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23(6):824–854
Frystyk J (2004) Free insulin-like growth factors—measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res 14(5):337–375
Fujiki K, Inamura H, Matsuoka M (2013) Phosphorylation of FOXO3a by PI3K/Akt pathway in HK-2 renal proximal tubular epithelial cells exposed to cadmium. Arch Toxicol 87(12):2119–2127
Gracey AY, Troll JV, Somero GN (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci USA 98(4):1993–1998
Hermesz E, Abrahám M, Nemcsók J (2001) Tissue-specific expression of two metallothionein genes in common carp during cadmium exposure and temperature shock. Comp Biochem Physiol C: Toxicol Pharmacol 128(3):457–465
Hwa V, Oh Y, Rosenfeld RG (1999) The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev 20(6):761–787
Jones JI, Gockerman A, Busby WH Jr, Wright G, Clemmons DR (1993) Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha5 beta 1 integrin by means of its Arg–Gly–Asp sequence. Proc Natl Acad Sci USA 90(22):10553–10557
Kajimura S, Aida K, Duan C (2005) Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proc Natl Acad Sci USA 102(4):1240–1245
Kajimura S, Aida K, Duan C (2006) Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxia-inducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1 gene expression. Mol Cell Biol 26(3):1142–1155
Kamangar BB, Gabillard JC, Bobe J (2006) Insulin-like growth factor-binding protein (IGFBP)-1, -2, -3, -4, -5, and -6 and IGFBP-related protein 1 during rainbow trout postvitellogenesis and oocyte maturation: molecular characterization, expression profiles, and hormonal regulation. Endocrinology 147(5):2399–2410
Kamei H, Lu L, Jiao S, Li Y, Gyrup C, Laursen LS, Oxvig C, Zhou J, Duan C (2008) Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS ONE 3:e3091
Kumar SV, Bhattacharya S (2000) In vitro toxicity of mercury, cadmium, and arsenic to platelet aggregation: influence of adenylate cyclase and phosphodiesterase activity. In Vitr Mol Toxicol 13(2):137–144
Lee PD, Conover CA, Powell DR (1993) Regulation and function of insulin-like growth factor-binding protein-1. Proc Soc Exp Bio Med 204(1):4–29
Lee PD, Giudice LC, Conover CA, Powell DR (1997) Insulin-like growth factor binding protein-1: recent findings and new directions. Proc Soc Exp Biol Med 216(3):319–357
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Maures TJ, Duan C (2002) Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1. Endocrinology 143(7):2722–2731
Oishi Y, Ohnishi M, Kobayashi-Hattori K, Takita T, Noguchi T (2007) Cadmium cation increases the production and mRNA levels of insulin-like growth factor-binding protein-1 in HepG2. Biosci Biotechnol Biochem 71(5):1334–1337
Orlowski CC, Ooi GT, Brown DR, Yang YW, Tseng LY, Rechler MM (1991) Insulin rapidly inhibits insulin-like growth factor-binding protein-1 gene expression in H4-II-E rat hepatoma cells. Mol Endocrinol 5(8):1180–1187
Park SY, Gomes C, Oh SD, Soh J (2015) Cadmium up-regulates transcription of the steroidogenic acute regulatory protein (StAR) gene through phosphorylated CREB rather than SF-1 in K28 cells. J Toxicol Sci 40(2):151–161
Pedroso FL, Fukada H, Masumoto T (2009) Molecular characterization, tissue distribution patterns and nutritional regulation of IGFBP-1, -2, -3 and -5 in yellowtail, Seriola quinqueradiata. Gen Comp Endocrinol 161(3):344–353
Pierce AL, Shimizu M, Felli L, Swanson P, Dickhoff WW (2006) Metabolic hormones regulate insulin-like growth factor binding protein-1 mRNA levels in primary cultured salmon hepatocytes; lack of inhibition by insulin. J Endocrinol 191(2):379–386
Powell DR, Suwanichkul A, Cubbage ML, DePaolis LA, Snuggs MB, Lee PD (1991) Insulin inhibits transcription of the human gene for insulin-like growth factor-binding protein-1. J Biol Chem 266(28):18868–18876
Rahman MS, Thomas P (2011) Characterization of three IGFBP mRNAs in Atlantic croaker and their regulation during hypoxic stress: potential mechanisms of their upregulation by hypoxia. Am J Physiol Endocrinol Metab 301(4):E637–E648
Sackett RL, McCusker RH (1998) Multivalent cations depress ligand binding to cell-associated insulin-like growth factor binding protein-5 on human glioblastoma cells. Endocrinology 139(4):1943–1951
Shimizu M, Dickey JT, Fukada H, Dickhoff WW (2005) Salmon serum 22 kDa insulin-like growth factor-binding protein (IGFBP) is IGFBP-1. J Endocrinol 184(1):267–276
Shimizu M, Kishimoto K, Yamaguchi T, Nakano Y, Hara A, Dickhoff WW (2011) Circulating salmon 28- and 22-kDa insulin-like growth factor binding proteins (IGFBPs) are co-orthologs of IGFBP-1. Gen Comp Endocrinol 174(2):97–106
Sun CF, Tao Y, Jiang XY, Zou SM (2011) IGF binding protein 1 is correlated with hypoxia-induced growth reduce and developmental defects in grass carp (Ctenopharyngodon idellus) embryos. Gen Comp Endocrinol 172(3):409–415
Turgut S, Kaptanoglu B, Turgut G, Emmungil G, Genç O (2005) Effects of cadmium and zinc on plasma levels of growth hormone, insulin-like growth factor I, and insulin-like growth factor-binding protein 3. Biol Trace Elem Res 108(1–3):197–204
Unterman TG, Oehler DT, Murphy LJ, Lacson RG (1991) Multihormonal regulation of insulin-like growth factor-binding protein-1 in rat H4IIE hepatoma cells: the dominant role of insulin. Endocrinology 128(6):2693–2701
Villafuerte BC, Goldstein S, Robertson DG, Pao CI, Murphy LJ, Phillips LS (1992) Nutrition and somatomedin XXIX. Molecular regulation of IGFBP-1 in hepatocyte primary culture. Diabetes 41(7):835–842
Zhai W, Zhang J, Shi Z, Fu Y (2012) Identification and expression analysis of IGFBP-1 gene from Japanese flounder (Paralichthys olivaceus). Comp Biochem Physiol B: Biochem Mol Biol 161(4):413–420
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This work was supported by the National Natural Science Foundation of China (No. 31101878), the Excellent Youth Foundation of Henan Polytechnic University (No. J2014-02), the Dr. Foundation of Henan Polytechnic University (No. B2010-07) and the Youth Backbone Teacher Foundation of Henan Polytechnic University to Dr. Wenbo Chen.
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Chen, W., Zhang, Z., Dong, H. et al. Insulin-like growth factor-binding protein-1 (IGFBP-1) in goldfish, Carassius auratus: molecular cloning, tissue expression, and mRNA expression responses to periprandial changes and cadmium exposure. Fish Physiol Biochem 42, 1043–1052 (2016). https://doi.org/10.1007/s10695-015-0195-x
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DOI: https://doi.org/10.1007/s10695-015-0195-x