Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish.
Gene duplication is the primary force of new gene evolution. Deciphering whether a pair of duplicated genes has evolved divergent functions is often challenging. The zebrafish is uniquely positioned to provide insight into the process of functional gene evolution due to its amenability to genetic an...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2008-08-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC2518108?pdf=render |
| _version_ | 1819327012195532800 |
|---|---|
| author | Hiroyasu Kamei Ling Lu Shuang Jiao Yun Li Claus Gyrup Lisbeth S Laursen Claus Oxvig Jianfeng Zhou Cunming Duan |
| author_facet | Hiroyasu Kamei Ling Lu Shuang Jiao Yun Li Claus Gyrup Lisbeth S Laursen Claus Oxvig Jianfeng Zhou Cunming Duan |
| author_sort | Hiroyasu Kamei |
| collection | DOAJ |
| description | Gene duplication is the primary force of new gene evolution. Deciphering whether a pair of duplicated genes has evolved divergent functions is often challenging. The zebrafish is uniquely positioned to provide insight into the process of functional gene evolution due to its amenability to genetic and experimental manipulation and because it possess a large number of duplicated genes.We report the identification and characterization of two hypoxia-inducible genes in zebrafish that are co-ortholgs of human IGF binding protein-1 (IGFBP-1). IGFBP-1 is a secreted protein that binds to IGF and modulates IGF actions in somatic growth, development, and aging. Like their human and mouse counterparts, in adult zebrafish igfbp-1a and igfbp-1b are exclusively expressed in the liver. During embryogenesis, the two genes are expressed in overlapping spatial domains but with distinct temporal patterns. While zebrafish IGFBP-1a mRNA was easily detected throughout embryogenesis, IGFBP-1b mRNA was detectable only in advanced stages. Hypoxia induces igfbp-1a expression in early embryogenesis, but induces the igfbp-1b expression later in embryogenesis. Both IGFBP-1a and -b are capable of IGF binding, but IGFBP-1b has much lower affinities for IGF-I and -II because of greater dissociation rates. Overexpression of IGFBP-1a and -1b in zebrafish embryos caused significant decreases in growth and developmental rates. When tested in cultured zebrafish embryonic cells, IGFBP-1a and -1b both inhibited IGF-1-induced cell proliferation but the activity of IGFBP-1b was significantly weaker.These results indicate subfunction partitioning of the duplicated IGFBP-1 genes at the levels of gene expression, physiological regulation, protein structure, and biological actions. The duplicated IGFBP-1 may provide additional flexibility in fine-tuning IGF signaling activities under hypoxia and other catabolic conditions. |
| first_indexed | 2024-12-24T13:04:04Z |
| format | Article |
| id | doaj.art-15384b34a364491eb9f46b0f32550dd4 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-24T13:04:04Z |
| publishDate | 2008-08-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-15384b34a364491eb9f46b0f32550dd42022-12-21T16:54:04ZengPublic Library of Science (PLoS)PLoS ONE1932-62032008-08-0138e309110.1371/journal.pone.0003091Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish.Hiroyasu KameiLing LuShuang JiaoYun LiClaus GyrupLisbeth S LaursenClaus OxvigJianfeng ZhouCunming DuanGene duplication is the primary force of new gene evolution. Deciphering whether a pair of duplicated genes has evolved divergent functions is often challenging. The zebrafish is uniquely positioned to provide insight into the process of functional gene evolution due to its amenability to genetic and experimental manipulation and because it possess a large number of duplicated genes.We report the identification and characterization of two hypoxia-inducible genes in zebrafish that are co-ortholgs of human IGF binding protein-1 (IGFBP-1). IGFBP-1 is a secreted protein that binds to IGF and modulates IGF actions in somatic growth, development, and aging. Like their human and mouse counterparts, in adult zebrafish igfbp-1a and igfbp-1b are exclusively expressed in the liver. During embryogenesis, the two genes are expressed in overlapping spatial domains but with distinct temporal patterns. While zebrafish IGFBP-1a mRNA was easily detected throughout embryogenesis, IGFBP-1b mRNA was detectable only in advanced stages. Hypoxia induces igfbp-1a expression in early embryogenesis, but induces the igfbp-1b expression later in embryogenesis. Both IGFBP-1a and -b are capable of IGF binding, but IGFBP-1b has much lower affinities for IGF-I and -II because of greater dissociation rates. Overexpression of IGFBP-1a and -1b in zebrafish embryos caused significant decreases in growth and developmental rates. When tested in cultured zebrafish embryonic cells, IGFBP-1a and -1b both inhibited IGF-1-induced cell proliferation but the activity of IGFBP-1b was significantly weaker.These results indicate subfunction partitioning of the duplicated IGFBP-1 genes at the levels of gene expression, physiological regulation, protein structure, and biological actions. The duplicated IGFBP-1 may provide additional flexibility in fine-tuning IGF signaling activities under hypoxia and other catabolic conditions.http://europepmc.org/articles/PMC2518108?pdf=render |
| spellingShingle | Hiroyasu Kamei Ling Lu Shuang Jiao Yun Li Claus Gyrup Lisbeth S Laursen Claus Oxvig Jianfeng Zhou Cunming Duan Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. PLoS ONE |
| title | Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. |
| title_full | Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. |
| title_fullStr | Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. |
| title_full_unstemmed | Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. |
| title_short | Duplication and diversification of the hypoxia-inducible IGFBP-1 gene in zebrafish. |
| title_sort | duplication and diversification of the hypoxia inducible igfbp 1 gene in zebrafish |
| url | http://europepmc.org/articles/PMC2518108?pdf=render |
| work_keys_str_mv | AT hiroyasukamei duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT linglu duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT shuangjiao duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT yunli duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT clausgyrup duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT lisbethslaursen duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT clausoxvig duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT jianfengzhou duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish AT cunmingduan duplicationanddiversificationofthehypoxiainducibleigfbp1geneinzebrafish |