Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (<em>Megalobrama amblycephala</em>)

Yu-Mei TIAN; Jie CHEN; Yang TAO; Xia-Yun JIANG; Shu-Ming ZOU

doi:10.13918/j.issn.2095-8137.2014.4.300

Volume 35 Issue 4

Jul. 2014

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Yu-Mei TIAN, Jie CHEN, Yang TAO, Xia-Yun JIANG, Shu-Ming ZOU. Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala). Zoological Research, 2014, 35(4): 300-306. doi: 10.13918/j.issn.2095-8137.2014.4.300

Citation:

Yu-Mei TIAN, Jie CHEN, Yang TAO, Xia-Yun JIANG, Shu-Ming ZOU. Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala). Zoological Research, 2014, 35(4): 300-306. doi: 10.13918/j.issn.2095-8137.2014.4.300

Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala)

doi: 10.13918/j.issn.2095-8137.2014.4.300

Key Laboratory of Freshwater Aquatic Genetic Resources, Shanghai Ocean University, Shanghai 201306, China

Received Date: 2013-09-29
Rev Recd Date: 2013-12-26
Publish Date: 2014-07-08

Abstract

Insulin-like growth factor-binding protein 1 (IGFBP-1), a hypoxia-induced protein, is a member of the IGFBP family that regulates vertebrate growth and development. In this study, full-length IGFBP-1a cDNA was cloned from a hypoxia-sensitive Cyprinidae fish species, the blunt snout bream (Megalobrama amblycephala). IGFBP-1a was expressed in various organs of adult blunt snout bream, including strongly in the liver and weakly in the gonads. Under hypoxia, IGFBP-1a mRNA levels increased sharply in the skin, liver, kidney, spleen, intestine and heart tissues of juvenile blunt snout bream, but recovered to normal levels after 24-hour exposure to normal dissolved oxygen. In blunt snout bream embryos, IGFBP-1a mRNA was expressed at very low levels at both four and eight hours post-fertilization, and strongly at later stages. Embryonic growth and development rates decreased significantly in embryos injected with IGFBP-1a mRNA. The average body length of IGFBP-1a-overexpressed embryos was 82.4% of that of the control group, and somite numbers decreased to 85.2%. These findings suggest that hypoxia-induced IGFBP-1a may inhibit growth in this species under hypoxic conditions.
- Megalobrama amblycephala,
- IGFBP-1a,
- Hypoxia,
- Overexpression

References

[1]	Baker J, Liu JP, Robertson EJ, Efstratiadis A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell, 75(1): 73-82.
[2]	Crow KD, Stadler PF, Lynch V, Amemiya C, Wagner GP. 2006. The "fishspecific" Hox cluster duplication is coincident with the origin of teleosts. Molecular Biology and Evolution, 23(1): 121-136.
[3]	Duan C, Xu Q. 2005. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. General and Comparative Endocrinology, 142(1-2): 44-52.
[4]	Firth SM, Baxter RC. 2002. Cellular actions of the insulin-like growth factor binding proteins. Endocrine Reviews, 23(6): 824-854.
[5]	Hwa V, Oh Y, Rosenfeld RG. 1999. The Insulin-like growth factor-binding proteins (IGFBPs) super family. Endocrine Reviews, 20(6): 761-787.
[6]	Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, et al. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature, 431(7011): 946-957.
[7]	Jiang XY, Du XD, Tian YM, Shen RJ, Sun CF, Zou SM. 2012. Goldfish transposase Tgf2 presumably from recent horizontal transfer is active. FASEB Journal, 26(7): 2743-2752.
[8]	Kajimura S, Aida K, Duan C. 2005. Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proceedings of the National Academy of Sciences of the United States of America, 102(4): 1240-1245.
[9]	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 zebrafish insulin-like growth factor binding protein 1 gene expression. Molecular and Cellular Biology, 26(3): 1142-1155.
[10]	Kajimura S, Duan C. 2007. Insulin-like growth factor (IGF) binding protein-1: An evolutionarily conserved fine tuner of IGF actions under catabolic conditions. Journal of Fish Biology, 71: 309-325.
[11]	Kamei H, Lu L, Jiao S, Li Y, Gyrup C, Laursen LS, Duan C. 2008. Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS ONE, 3: e3091.
[12]	Kane DA, Kimmel CB. 1993. The zebrafish midblastula transition. Development, 119(2): 447-456.
[13]	Macqueen DJ, Garcia de la Serrana D, Johnston IA. 2013. Evolution of ancient functions in the vertebrate insulin-like growth factor system uncovered by study of duplicated salmonid fish genomes. Molecular Biology and Evolution, 30(5): 1060-1076.
[14]	Maures TJ, Duan C. 2002. Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1.
[15]	Endocrinology, 143(7): 2722-2731.
[16]	Ocampo Daza DO, Sundstrom G, Bergqvist CA, Duan C, Larhammar D. 2011. Evolution of the insulin-like growth factor binding protein (IGFBP) family. Endocrinology, 152(6): 2278-2289.
[17]	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. American Journal of Physiology: Endocrinology and Metabolism, 301(4): E637-E648.
[18]	Reindl KM, Sheridan MA. 2012. Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comparative Biochemistry and Physiology-Part A: Molecular & Integrative Physiology, 163(3-4): 231-245.
[19]	Shen RJ, Jiang XY, Pu JW, Zou SM. 2010. HIF-1α and-2α genes in a hypoxia-sensitive teleost species Megalobrama amblycephala: cDNA cloning, expression and different responses to hypoxia. Comparative Biochemistry and Physiology-Part B: Biochemistry & Molecular Biology, 157(3): 273-280.
[20]	Shen WY, Ren G, Zhu YR. 2012. Effects of compensatory growth on the levels of IGF-1, IGFBP-1 and expressions of IGF-1 mRNA, IGF-1R mRNA in Carassius auratus gibelio.Zoological Research, 33(3): 298-303. (in Chinese)
[21]	Shimizu M, Dickey JT, Fukada H, Dickhoff WW. 2005. Salmon serum 22 kDa insulin-like growth factor-binding protein(IGFBP) is IGFBP-1. Journal of Endocrinology, 184(1): 267-276.
[22]	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. General and Comparative Endocrinology, 172(3): 409-415.
[23]	Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731-2739.
[24]	Tao Y, Zou SM. 2011. cDNA cloning and expression of insulin-like growth factor binding protein gene IGFBP-1 in Ctenopharyngodon idellus.Journal of Shanghai Ocean University, 20(1): 11-19. (in Chinese)
[25]	Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y. 2003. Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Research, 13(3): 382-390.
[26]	Zhang Z, Wu RSS, Mok HOL, Wang Y, Poon WWL, Cheng SH, Kong RYC. 2003. Isolation, characterization and expression analysis of a hypoxia-responsive glucose transporter gene from the grass carp, Ctenopharyngodon idellus.European Journal of Biochemistry, 270(14): 3010-3017.

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通讯作者: 陈斌, bchen63@163.com

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Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala)

Key Laboratory of Freshwater Aquatic Genetic Resources, Shanghai Ocean University, Shanghai 201306, China

Received Date: 2013-09-29

Rev Recd Date: 2013-12-26

Publish Date: 2014-07-08

Key words:

Abstract: Insulin-like growth factor-binding protein 1 (IGFBP-1), a hypoxia-induced protein, is a member of the IGFBP family that regulates vertebrate growth and development. In this study, full-length IGFBP-1a cDNA was cloned from a hypoxia-sensitive Cyprinidae fish species, the blunt snout bream (Megalobrama amblycephala). IGFBP-1a was expressed in various organs of adult blunt snout bream, including strongly in the liver and weakly in the gonads. Under hypoxia, IGFBP-1a mRNA levels increased sharply in the skin, liver, kidney, spleen, intestine and heart tissues of juvenile blunt snout bream, but recovered to normal levels after 24-hour exposure to normal dissolved oxygen. In blunt snout bream embryos, IGFBP-1a mRNA was expressed at very low levels at both four and eight hours post-fertilization, and strongly at later stages. Embryonic growth and development rates decreased significantly in embryos injected with IGFBP-1a mRNA. The average body length of IGFBP-1a-overexpressed embryos was 82.4% of that of the control group, and somite numbers decreased to 85.2%. These findings suggest that hypoxia-induced IGFBP-1a may inhibit growth in this species under hypoxic conditions.

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Reference (26)

[1]	Baker J, Liu JP, Robertson EJ, Efstratiadis A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell, 75(1): 73-82.
[2]	Crow KD, Stadler PF, Lynch V, Amemiya C, Wagner GP. 2006. The "fishspecific" Hox cluster duplication is coincident with the origin of teleosts. Molecular Biology and Evolution, 23(1): 121-136.
[3]	Duan C, Xu Q. 2005. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. General and Comparative Endocrinology, 142(1-2): 44-52.
[4]	Firth SM, Baxter RC. 2002. Cellular actions of the insulin-like growth factor binding proteins. Endocrine Reviews, 23(6): 824-854.
[5]	Hwa V, Oh Y, Rosenfeld RG. 1999. The Insulin-like growth factor-binding proteins (IGFBPs) super family. Endocrine Reviews, 20(6): 761-787.
[6]	Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, et al. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature, 431(7011): 946-957.
[7]	Jiang XY, Du XD, Tian YM, Shen RJ, Sun CF, Zou SM. 2012. Goldfish transposase Tgf2 presumably from recent horizontal transfer is active. FASEB Journal, 26(7): 2743-2752.
[8]	Kajimura S, Aida K, Duan C. 2005. Insulin-like growth factor-binding protein-1 (IGFBP-1) mediates hypoxia-induced embryonic growth and developmental retardation. Proceedings of the National Academy of Sciences of the United States of America, 102(4): 1240-1245.
[9]	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 zebrafish insulin-like growth factor binding protein 1 gene expression. Molecular and Cellular Biology, 26(3): 1142-1155.
[10]	Kajimura S, Duan C. 2007. Insulin-like growth factor (IGF) binding protein-1: An evolutionarily conserved fine tuner of IGF actions under catabolic conditions. Journal of Fish Biology, 71: 309-325.
[11]	Kamei H, Lu L, Jiao S, Li Y, Gyrup C, Laursen LS, Duan C. 2008. Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS ONE, 3: e3091.
[12]	Kane DA, Kimmel CB. 1993. The zebrafish midblastula transition. Development, 119(2): 447-456.
[13]	Macqueen DJ, Garcia de la Serrana D, Johnston IA. 2013. Evolution of ancient functions in the vertebrate insulin-like growth factor system uncovered by study of duplicated salmonid fish genomes. Molecular Biology and Evolution, 30(5): 1060-1076.
[14]	Maures TJ, Duan C. 2002. Structure, developmental expression, and physiological regulation of zebrafish IGF binding protein-1.
[15]	Endocrinology, 143(7): 2722-2731.
[16]	Ocampo Daza DO, Sundstrom G, Bergqvist CA, Duan C, Larhammar D. 2011. Evolution of the insulin-like growth factor binding protein (IGFBP) family. Endocrinology, 152(6): 2278-2289.
[17]	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. American Journal of Physiology: Endocrinology and Metabolism, 301(4): E637-E648.
[18]	Reindl KM, Sheridan MA. 2012. Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comparative Biochemistry and Physiology-Part A: Molecular & Integrative Physiology, 163(3-4): 231-245.
[19]	Shen RJ, Jiang XY, Pu JW, Zou SM. 2010. HIF-1α and-2α genes in a hypoxia-sensitive teleost species Megalobrama amblycephala: cDNA cloning, expression and different responses to hypoxia. Comparative Biochemistry and Physiology-Part B: Biochemistry & Molecular Biology, 157(3): 273-280.
[20]	Shen WY, Ren G, Zhu YR. 2012. Effects of compensatory growth on the levels of IGF-1, IGFBP-1 and expressions of IGF-1 mRNA, IGF-1R mRNA in Carassius auratus gibelio.Zoological Research, 33(3): 298-303. (in Chinese)
[21]	Shimizu M, Dickey JT, Fukada H, Dickhoff WW. 2005. Salmon serum 22 kDa insulin-like growth factor-binding protein(IGFBP) is IGFBP-1. Journal of Endocrinology, 184(1): 267-276.
[22]	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. General and Comparative Endocrinology, 172(3): 409-415.
[23]	Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731-2739.
[24]	Tao Y, Zou SM. 2011. cDNA cloning and expression of insulin-like growth factor binding protein gene IGFBP-1 in Ctenopharyngodon idellus.Journal of Shanghai Ocean University, 20(1): 11-19. (in Chinese)
[25]	Taylor JS, Braasch I, Frickey T, Meyer A, Van de Peer Y. 2003. Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Research, 13(3): 382-390.
[26]	Zhang Z, Wu RSS, Mok HOL, Wang Y, Poon WWL, Cheng SH, Kong RYC. 2003. Isolation, characterization and expression analysis of a hypoxia-responsive glucose transporter gene from the grass carp, Ctenopharyngodon idellus.European Journal of Biochemistry, 270(14): 3010-3017.

Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala)

doi: 10.13918/j.issn.2095-8137.2014.4.300

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References

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Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala)

doi: 10.13918/j.issn.2095-8137.2014.4.300

Key Laboratory of Freshwater Aquatic Genetic Resources, Shanghai Ocean University, Shanghai 201306, China

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Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala)

doi: 10.13918/j.issn.2095-8137.2014.4.300

Abstract

References

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Molecular cloning and function analysis of insulin-like growth factor-binding protein 1a in blunt snout bream (Megalobrama amblycephala)

doi: 10.13918/j.issn.2095-8137.2014.4.300

Key Laboratory of Freshwater Aquatic Genetic Resources, Shanghai Ocean University, Shanghai 201306, China

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