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Cloning, molecular characterization and expression analysis of insulin-like growth factor binding protein-2 (IGFBP-2) cDNA in goldfish, Carassius auratus

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Abstract

In the present study, a full-length cDNA encoding the insulin-like growth factor binding protein-2 (IGFBP-2) was cloned from the liver of goldfish (Carassius auratus) by rapid amplification of cDNA ends technique. The goldfish IGFBP-2 cDNA sequence was 1,513 bp long and had an open reading frame of 825 bp encoding a predicted polypeptide of 274 amino acid residues. Semi-quantitative RT-PCR results revealed that goldfish IGFBP-2 mRNA was expressed in all detected tissues. In liver, central nervous system and pituitary gland, goldfish IGFBP-2 expressed at high levels, followed by anterior intestine, middle intestine and kidney. In posterior intestine, ovary, skin, fat, spleen, muscle and gill, the goldfish IGFBP-2 expression levels were very low. Fasting and refeeding experiment showed that the mRNA expression of goldfish IGFBP-2 was up-regulated significantly in liver compared to the fed group and restored rapidly to normal level after refed. However, the mRNA expressions of IGFBP-2 in hypothalamus and pituitary of goldfish were insensitive to fasting. Furthermore, the mRNA expressions of IGFBP-2 in hypothalamus, pituitary and liver were varied in periprandial changes and significantly down-regulated at 2 and 4 h after meal. These results imply that the IGFBP-2 mRNA expression may be associated with anabolic and catabolic metabolism and regulated by metabolic factors in goldfish.

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References

  • Armstrong DG, Baxter G, Gutierrez CG, Hogg CO, Glazyrin AL, Campbell BK, Bramley TA, Webb R (1998) Insulin-like growth factor binding protein -2 and -4 messenger ribonucleic acid expression in bovine ovarian follicles: effect of gonadotropins and developmental status. Endocrinology 139(4):2146–2154

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Binkert C, Landwehr J, Mary JL, Schwander J, Heinrich G (1989) Cloning, sequence analysis and expression of a cDNA encoding a novel insulin-like growth factor binding protein (IGFBP-2). EMBO J 8(9):2497–2502

    CAS  PubMed Central  PubMed  Google Scholar 

  • Böni-Schnetzler M, Schmid C, Mary JL, Zimmerli B, Meier PJ, Zapf J, Schwander J, Froesch ER (1990) Insulin regulates the expression of the insulin-like growth factor binding protein 2 mRNA in rat hepatocytes. Mol Endocrinol 4(9):1320–1326

    Article  PubMed  Google Scholar 

  • Chen W, Li W, Lin H (2009) Common carp (Cyprinus carpio) insulin-like growth factor binding protein-2 (IGFBP-2): molecular cloning, expression profiles, and hormonal regulation in hepatocytes. Gen Comp Endocrinol 161(3):390–399

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Wang Y, Li W, Lin H (2010) Insulin-like growth factor binding protein-2 (IGFBP-2) in orange-spotted grouper, Epinephelus coioides: molecular characterization, expression profiles and regulation by 17β-estradiol in ovary. Comp Biochem Physiol B Biochem Mol Biol 157(4):336–342

    Article  PubMed  Google Scholar 

  • Clemmons DR (1997) Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev 8(1):45–62

    Article  CAS  PubMed  Google Scholar 

  • Cwyfan Hughes S, Mason HD, Franks S, Holly JM (1997) Modulation of the insulin-like growth factor-binding proteins by follicle size in the human ovary. J Endocrinol 154(1):35–43

    Article  CAS  PubMed  Google Scholar 

  • Dai W, Kamei H, Zhao Y, Ding J, Du Z, Duan C (2010) Duplicated zebrafish insulin-like growth factor binding protein-5 genes with split functional domains: evidence for evolutionarily conserved IGF binding, nuclear localization, and transactivation activity. FASEB J 24(6):2020–2029

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Daza DO, Sundström G, Bergqvist CA, Duan C, Larhammar D (2011) Evolution of the insulin-like growth factor binding protein(IGFBP) family. Endocrinology 152(6):2278–2289

    Article  CAS  PubMed  Google Scholar 

  • Duan C, Clemmons DR (1998) Differential expression and biological effects of insulin-like growth factor-binding protein-4 and -5 in vascular smooth muscle cells. J Biol Chem 273:16836–16842

    Article  CAS  PubMed  Google Scholar 

  • Duan C, Xu Q (2005) Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen Comp Endocrinol 142(1–2):44–52

    Article  CAS  PubMed  Google Scholar 

  • Duan C, Ding J, Li Q, Tsai W, Pozios K (1999) Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish. Proc Natl Acad Sci USA 96(26):15274–15279

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Firth SM, Baxter RC (1999) Characterisation of recombinant glycosylation variants of insulin-like growth factor binding protein-3. J Endocrinol 160(3):379–387

    Article  CAS  PubMed  Google Scholar 

  • Firth SM, Baxter RC (2002) Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 23(6):824–854

    Article  CAS  PubMed  Google Scholar 

  • Funkenstein B, Tsai W, Maures T, Duan C (2002) Ontogeny, tissue distribution, and hormonal regulation of insulin-like growth factor binding protein-2 (IGFBP-2) in a marine fish, Sparus aurata. Gen Comp Endocrinol 128(2):112–122

    Article  CAS  PubMed  Google Scholar 

  • Gabillard JC, Kamangar BB, Montserrat N (2006) Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J Endocrinol 191(1):15–24

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hoeflich A, Reisinger R, Vargas GA, Elmlinger MW, Schuett B, Jehle PM, Renner-Müller I, Lahm H, Russo VC, Wolf E (2002) Mutation of the RGD sequence does not affect plasma membrane association and growth inhibitory effects of elevated IGFBP-2 in vivo. FEBS Lett 523(1–3):63–67

    Article  CAS  PubMed  Google Scholar 

  • Hwa V, Oh Y, Rosenfeld RG (1999) The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr Rev 20(6):761–787

    CAS  PubMed  Google Scholar 

  • Jones JI, Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16(1):3–34

    CAS  PubMed  Google Scholar 

  • 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 alpha 5 beta 1 integrin by means of its Arg–Gly–Asp sequence. Proc Natl Acad Sci USA 90(22):10553–10557

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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(8):e3091

    Article  PubMed Central  PubMed  Google Scholar 

  • Miller BS, Khosravi MJ, Patterson MC, Conover CA (2009) IGF system in children with congenital disorders of glycosylation. Clin Endocrinol (Oxf) 70(6):892–897

    Article  CAS  Google Scholar 

  • Nagao K, Aman Yaman M, Murai A, Sasaki T, Saito N, Okumura J, Kita K (2001) Insulin administration suppresses an increase in insulin-like growth factor binding protein-2 gene expression stimulated by fasting in the chicken. Br Poult Sci 42(4):501–504

    Article  CAS  PubMed  Google Scholar 

  • Onagbesan OM, Vleugels B, Buys N, Bruggeman V, Safi M, Decuypere E (1999) Insulin-like growth factors in the regulation of avian ovarian functions. Domest Anim Endocrinol 17(2–3):299–313

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Rajaram S, Baylink DJ, Mohan S (1997) Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr Rev 18(6):801–831

    CAS  PubMed  Google Scholar 

  • Rodgers BD, Roalson ER, Thompson T (2008) Phylogenetic analysis of the insulin-like growth factor binding protein (IGFBP) and IGFBP-related protein gene families. Gen Comp Endocrinol 155(1):201–207

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Russo VC, Schütt BS, Andaloro E, Ymer SI, Hoeflich A, Ranke MB, Bach LA, Werther GA (2005) Insulin-like growth factor binding protein-2 binding to extracellular matrix plays a critical role in neuroblastoma cell proliferation, migration, and invasion. Endocrinology 146(10):4445–4455

    Article  CAS  PubMed  Google Scholar 

  • Safian D, Fuentes EN, Valdés JA, Molina A (2012) Dynamic transcriptional regulation of autocrine/paracrine igfbp1, 2, 3, 4, 5, and 6 in the skeletal muscle of the fine flounder during different nutritional statuses. J Endocrinol 214(1):95–108

    Article  CAS  PubMed  Google Scholar 

  • Schams D, Berisha B, Kosmann M, Einspanier R, Amselgruber WM (1999) Possible role of growth hormone, IGFs, and IGF-binding proteins in the regulation of ovarian function in large farm animals. Domest Anim Endocrinol 17(2–3):279–285

    Article  CAS  PubMed  Google Scholar 

  • Schmid C, Schläpfer I, Waldvogel M, Meier PJ, Schwander J, Böni-Schnetzler M, Zapf J, Froesch ER (1992) Differential regulation of insulin-like growth factor binding protein (IGFBP)-2 mRNA in liver and bone cells by insulin and retinoic acid in vitro. FEBS Lett 303(2–3):205–209

    Article  CAS  PubMed  Google Scholar 

  • Schneider MR, Wolf E, Hoeflich A, Lahm H (2002) IGF-binding protein-5: flexible player in the IGF system and effector on its own. J Endocrinol 172(3):423–440

    Article  CAS  PubMed  Google Scholar 

  • Shi FT, Li WS, Bai CH, Lin HR (2002) IGF-I of orange spotted grouper Epinephelus coioides: cDNA cloning, sequencing and expression in Escherichia coli. Fish Physiol Biochem 27(3–4):147–156

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stewart CE, Rotwein P (1996) Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol Rev 76(4):1005–1026

    CAS  PubMed  Google Scholar 

  • 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(3):513–521

  • Wang GK, Hu L, Fuller GN, Zhang W (2006) An interaction between insulinlike growth factor-binding protein 2 (IGFBP2) and integrin alpha5 is essential for IGFBP2-induced cell mobility. J Biol Chem 281(20):14085–14091

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Lu L, Li Y, Li M, Chen C, Feng Q, Zhang C, Duan C (2009) Molecular and functional characterization of two distinct IGF binding protein-6 genes in zebrafish. Am J Physiol Regul Integr Comp Physiol 296(5):R1348–R1357

    Article  CAS  PubMed  Google Scholar 

  • Werner H, LeRoith D (1996) The role of the insulin-like growth factor system in human cancer. Adv Cancer Res 68:183–223

    Article  CAS  PubMed  Google Scholar 

  • Wood AW, Schlueter PJ, Duan C (2005) Targeted knockdown of insulin-like growth factor binding protein-2 disrupts cardiovascular development in zebrafish embryos. Mol Endocrinol 19(4):1024–1034

    Article  CAS  PubMed  Google Scholar 

  • Yuan W, Bao B, Garverick HA, Youngquist RS, Lucy MC (1998) Follicular dominance in cattle is associated with divergent patterns of ovarian gene expression for insulin-like growth factor (IGF)-I, IGF-II, and IGF binding protein-2 in dominant and subordinate follicles. Domest Anim Endocrinol 15(1):55–63

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang J, Shi Z, Zhai W, Wang X (2013) Insulin-like growth factor binding protein-2 (IGFBP-2) in Japanese flounder, Paralichthys olivaceus: molecular cloning, expression patterns and hormonal regulation during metamorphosis. Fish Physiol Biochem 39(6):1541–1554

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Li W, Kamei H, Duan C (2008) Duplication of the IGFBP-2 gene in teleost fish: protein structure and functionality conservation and gene expression divergence. PLoS One 3(12):e3926

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 31101878); the Hydrobiological Project of Shanghai Leading Academic Discipline (III) (S30701); the Excellent Youth Foundation (No. J2014-02) of Henan Polytechnic University and the Dr. Foundation (No. B2010-07) of Henan Polytechnic University to Dr. Wenbo Chen.

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Chen, W., Li, W., Zhang, Z. et al. Cloning, molecular characterization and expression analysis of insulin-like growth factor binding protein-2 (IGFBP-2) cDNA in goldfish, Carassius auratus . Fish Physiol Biochem 40, 1669–1681 (2014). https://doi.org/10.1007/s10695-014-9958-z

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