View Item 

Show simple item record

Gene duplication and functional divergence of the zebrafish insulin‐like growth factor 1 receptors
dc.contributor.authorSchlueter, Peter J.
dc.contributor.authorRoyer, Tricia
dc.contributor.authorFarah, Mohamed H.
dc.contributor.authorLaser, Benjamin
dc.contributor.authorChan, Shu Jin
dc.contributor.authorSteiner, Donald F.
dc.contributor.authorDuan, Cunming
dc.contributor.authorSchlueter, Peter J.
dc.contributor.authorRoyer, Tricia
dc.contributor.authorFarah, Mohamed H.
dc.contributor.authorLaser, Benjamin
dc.contributor.authorChan, Shu Jin
dc.contributor.authorSteiner, Donald F.
dc.contributor.authorDuan, Cunming
dc.date.accessioned2020-03-17T18:33:02Z
dc.date.available2020-03-17T18:33:02Z
dc.date.issued2006-06
dc.identifier.citationSchlueter, Peter J.; Royer, Tricia; Farah, Mohamed H.; Laser, Benjamin; Chan, Shu Jin; Steiner, Donald F.; Duan, Cunming; Schlueter, Peter J.; Royer, Tricia; Farah, Mohamed H.; Laser, Benjamin; Chan, Shu Jin; Steiner, Donald F.; Duan, Cunming (2006). "Gene duplication and functional divergence of the zebrafish insulin‐like growth factor 1 receptors." The FASEB Journal 20(8): 1230-1232.
dc.identifier.issn0892-6638
dc.identifier.issn1530-6860
dc.identifier.urihttps://hdl.handle.net/2027.42/154460
dc.description.abstractInsulin‐like growth factor (IGF) 1 receptor (IGF1R)‐mediated signaling plays key roles in growth, development, and physiology. Recent studies have shown that there are two distinct igf1r genes in zebrafish, termed igf1ra and igf1rb. In this study, we tested the hypothesis that zebrafish igf1ra and igf1rb resulted from a gene duplication event at the igf1r locus and that this has led to their functional divergence. The genomic structures of zebrafish igf1ra and igf1rb were determined and their loci mapped. While zebrafish igf1ra has 21 exons and is located on linkage group (LG) 18, zebrafish igf1rb has 22 exons and mapped to LG 7. There is a strong syntenic relationship between the two zebrafish genes and the human IGF1R gene. Using a MO‐based loss‐of‐function approach, we show that both Igf1ra and Igf1rb are required for zebrafish embryo viability and proper growth and development. Although Igf1ra and Igf1rb demonstrated a large degree of functional overlap with regard to cell differentiation in the developing eye, inner ear, heart, and muscle, they also exhibited functional distinction involving a greater requirement for Igf1rb in spontaneous muscle contractility. These findings suggest that the duplicated zebrafish igf1r genes play largely overlapping but not identical functional roles in early development and provide novel insight into the functional evolution of the IGF1R/insulin receptor gene family.— Schlueter, P. J., Royer, T., Mohamed, H. F., Laser, B., Chan, S. J., Steiner, D. F., Duan, C. Gene duplication and functional divergence of the zebrafish insulin‐like growth factor 1 receptors. FASEB J. 20, E462–E471 (2006)
dc.publisherWiley Periodicals, Inc.
dc.publisherFederation of American Societies for Experimental Biology
dc.subject.otherheart
dc.subject.othermuscle
dc.subject.otherIGF signaling
dc.subject.othergrowth
dc.subject.otherdevelopmental timing
dc.subject.otherretina
dc.subject.otherinner ear
dc.titleGene duplication and functional divergence of the zebrafish insulin‐like growth factor 1 receptors
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelBiology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/154460/1/fsb2fj053882fje.pdf
dc.identifier.doi10.1096/fj.05-3882fje
dc.identifier.sourceThe FASEB Journal
dc.identifier.citedreferenceNeumann, C. J., and Nuesslein-Volhard, C. ( 2000 ) Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289, 2137 – 2139
dc.identifier.citedreferenceEfstratiadis, A. ( 1998 ) Genetics of mouse growth. Int. J. Dev. Biol. 42, 955 – 976
dc.identifier.citedreferenceKim, J. J., and Accili, D. ( 2002 ) Signalling through IGF-I and insulin receptors: where is the specificity? Growth Horm. IGF Res. 12, 84 – 90
dc.identifier.citedreferencePera, E. M., Ikeda, A., Eivers, E., and De Robertis, E. M. ( 2003 ) Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev. 17, 3023 – 3028
dc.identifier.citedreferencePera, E. M., Wessely, O., Li, S. Y., and De Robertis, E. M. ( 2001 ) Neural and head induction by insulin-like growth factor signals. Dev. Cell 1, 655 – 665
dc.identifier.citedreferenceRichard-Parpaillon, L., Heligon, C., Chesnel, F., Boujard, D., and Philpott, A. ( 2002 ) The IGF pathway regulates head formation by inhibiting Wnt signaling in Xenopus. Dev. Biol. 244, 407 – 417
dc.identifier.citedreferenceEivers, E., McCarthy, K., Glynn, C., Nolan, C. M., and Byrnes, L. ( 2004 ) Insulin-like growth factor (IGF) signalling is required for early dorso-anterior development of the zebrafish embryo. Int. J. Dev. Biol. 48, 1131 – 1140
dc.identifier.citedreferenceMaures, T., Chan, S. J., Xu, B., Sun, H., Ding, J., and Duan, C. ( 2002 ) Structural, biochemical, and expression analysis of two distinct insulin-like growth factor I receptors and their lig ands in zebrafish. Endocrinology 143, 1858 – 1871
dc.identifier.citedreferenceKimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. ( 1995 ) Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253 – 310
dc.identifier.citedreferenceHukriede, N. A., Joly, L., Tsang, M., Miles, J., Tellis, P., Epstein, J. A., Barbazuk, W. B., Li, F. N., Paw, B., Postlethwait, J. H., Hudson, T. J., Zon, L. I., McPherson, J. D., Chevrette, M., Dawid, I. B., Johnson, S. L., and Ekker, M. ( 1999 ) Radiation hybrid mapping of the zebrafish genome. Proc. Natl. Acad. Sci. U. S. A. 96, 9745 – 9750
dc.identifier.citedreferenceWood, A. W., Schlueter, P. J., and Duan, C. ( 2005 ) Targeted knockdown of insulin-like growth factor binding protein-2 disrupts cardiovascular development in zebrafish embryos. Mol. Endocrinol. 19, 1024 – 1034
dc.identifier.citedreferenceDuan, C., Ding, J., Li, Q., Tsai, W., and Pozios, K. ( 1999 ) Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish. Proc. Natl. Acad. Sci. U. S. A. 96, 15274 – 15279
dc.identifier.citedreferenceHu, M., and Easter, S. S. ( 1999 ) Retinal neurogenesis: the formation of the initial central patch of postmitotic cells. Dev. Biol. 207, 309 – 321
dc.identifier.citedreferenceAyaso, E., Nolan, C. M., and Byrnes, L. ( 2002 ) Zebrafish insulin-like growth factor-I receptor: molecular cloning and developmental expression. Mol. Cell. Endocrinol. 191, 137 – 148
dc.identifier.citedreferenceGates, M. A., Kim, L., Egan, E. S., Cardozo, T., Sirotkin, H. I., Dougan, S. T., Lashkari, D., Abagyan, R., Schier, A. F., and Talbot, W. S. ( 1999 ) A genetic linkage map for zebrafish: comparative analysis and localization of genes and expressed sequences. Genome Res. 9, 334 – 347
dc.identifier.citedreferenceGeisler, R., Rauch, G. J., Baier, H., van Bebber, F., Bross, L., Dekens, M. P., Finger, K., Fricke, C., Gates, M. A., Geiger, H., Geiger-Rudolph, S., et al. ( 1999 ) A radiation hybrid map of the zebrafish genome. Nat. Genet. 23, 86 – 89
dc.identifier.citedreferenceWoods, I. G., Kelly, P. D., Chu, F., Ngo-Hazelett, P., Yan, Y. L., Huang, H., Postlethwait, J. H., and Talbot, W. S. ( 2000 ) A comparative map of the zebrafish genome. Genome Res. 10, 1903 – 1914
dc.identifier.citedreferenceBarbazuk, W. B., Korf, I., Kadavi, C., Heyen, J., Tate, S., Wun, E., Bedell, J. A., McPherson, J. D., and Johnson, S. L. ( 2000 ) The syntenic relationship of the zebrafish and human genomes. Genome Res. 10, 1351 – 1358
dc.identifier.citedreferencePozios, K.C., Ding, J., Degger, B., Upton, Z., and Duan, C. ( 2001 ) IGFs stimulate zebrafish cell proliferation through activating the MAP kinase and PI3-kinase signaling pathways. Am. J. Physiol. 280, R1230 – R1239
dc.identifier.citedreferenceEkker, S. C. ( 2000 ) Morphants: a new systematic vertebrate functional genomics approach. Yeast 17, 302 – 306
dc.identifier.citedreferenceEkker, S. C., and Larson, J. D. ( 2001 ) Morphant technology in model developmental systems. Genesis 30, 89 – 93
dc.identifier.citedreferenceEaster, S. S., Jr., and Malicki, J. J. ( 2002 ) The zebrafish eye: developmental and genetic analysis. Results Probl. Cell Differ. 40, 346 – 370
dc.identifier.citedreferenceNeumann, C. J. ( 2001 ) Pattern formation in the zebrafish retina. Semin. Cell Dev. Biol. 12, 485 – 490
dc.identifier.citedreferenceWhitfield, T. T., Riley, B. B., Chiang, M. Y., and Phillips, B. ( 2002 ) Development of the zebrafish inner ear. Dev. Dyn. 223, 427 – 458
dc.identifier.citedreferenceDrapeau, P., Saint-Amant, L., Buss, R. R., Chong, M., McDear-mid, J. R., and Brustein, E. ( 2002 ) Development of the locomotor network in zebrafish. Prog. Neurobiol. 68, 85 – 111
dc.identifier.citedreferenceWood, A. W., Duan, C., and Bern, H. A. ( 2005 ) Insulin-like growth factor signaling in fish. Int. Rev. Cytol. 243, 215 – 285
dc.identifier.citedreferenceChan, S. J., Plisetskaya, E. M., Urbinati, E., Jin, Y., and Steiner, D. F. ( 1997 ) Expression of multiple insulin and insulin-like growth factor receptor genes in salmon gill cartilage. Proc. Natl. Acad. Sci. U. S. A. 94, 12446 – 12451
dc.identifier.citedreferenceAmores, A., Force, A., Yan, Y. L., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Prince, V., Wang, Y. L., Westerfield, M., Ekker, M., and Postlethwait, J. H. ( 1998 ) Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711 – 1714
dc.identifier.citedreferenceOhno, S. ( 1970 ) Evolution by Gene Duplication. Springer-Verlag, New York
dc.identifier.citedreferenceZhang, J. ( 2003 ) Evolution by gene duplication: an update. Trends Ecol. Evol. 16, 292 – 298
dc.identifier.citedreferenceChen, C., Jack, J., and Garofalo, R. S. ( 1996 ) The Drosophila insulin receptor is required for normal growth. Endocrinology 137, 846 – 856
dc.identifier.citedreferenceForce, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., and Postlethwait, J. ( 1999 ) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531 – 1545
dc.identifier.citedreferenceHe, X., and Zhang, J. ( 2005 ) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157 – 1164
dc.identifier.citedreferenceKlinghoffer, R. A., Mueting-Nelsen, P. F., Faerman, A., Shani, M., and Soriano, P. ( 2001 ) The two PDGF receptors maintain conserved signaling in vivo despite divergent embryological functions. Mol. Cell. 7, 343 – 354
dc.identifier.citedreferenceHeldin, C. H., Ostman, A., and Ronnstrand, L. ( 1998 ) Signal transduction via platelet-derived growth factor receptors. Bio-chim. Biophys. Acta 1378, F79 – 113
dc.identifier.citedreferenceKlinghoffer, R. A., Hamilton, T. G., Hoch, R., and Soriano, P. ( 2002 ) An allelic series at the PDGFalphaR locus indicates unequal contributions of distinct signaling pathways during development. Dev. Cell 2, 103 – 113
dc.identifier.citedreferenceLe Roith, D., Bondy, C., Yakar, S., Liu, J. L., and Butler, A. ( 2001 ) The somatomedin hypothesis: 2001. Endocr. Rev. 22, 53 – 74
dc.identifier.citedreferenceJones, J. I., and Clemmons, D. R. ( 1995 ) Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16, 3 – 34
dc.identifier.citedreferenceNakae, J., Kido, Y., and Accili, D. ( 2001 ) Distinct and overlapping functions of insulin and IGF-I receptors. Endocr. Rev. 22, 818 – 835
dc.identifier.citedreferenceDe Meyts, P., and Whittaker, J. ( 2002 ) Structural biology of insulin and IGF1 receptors: implications for drug design. Nat. Rev. Drug Discov. 1, 769 – 783
dc.identifier.citedreferenceAbuzzahab, M. J., Schneider, A., Goddard, A., Grigorescu, F., Lautier, C., Keller, E., Kiess, W., Klammt, J., Kratzsch, J., Osgood, D., Pfaffle, R., Raile, K., Seidel, B., Smith, R. J., and Chernausek, S. D. ( 2003 ) IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N. Engl. J. Med. 349, 2211 – 2222
dc.identifier.citedreferenceKawashima, Y., Kanzaki, S., Yang, F., Kinoshita, T., Hanaki, K., Nagaishi, J., Ohtsuka, Y., Hisatome, I., Ninomoya, H., Nanba, E., Fukushima, T., and Takahashi, S. ( 2005 ) Mutation at cleavage site of insulin-like growth factor receptor in a short-stature child born with intrauterine growth retardation. J. Clin. Endocr. Metab. 90, 4679 – 4687
dc.identifier.citedreferenceWoods, K. A., Camacho-Hubner, C., Savage, M. O., and Clark, A. J. ( 1996 ) Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N. Engl. J. Med. 335, 1363 – 1367
dc.identifier.citedreferenceDenley, A., Wang, C. C., McNeil, K. A., Walenkamp, M. J., van Duyvenvoorde, H., Wit, J. M., Wallace, J. C., Norton, R. S., Karperien, M., and Forbes, B. E. ( 2005 ) Structural and functional characteristics of the Val44Met insulin-like growth factor I missense mutation: correlation with effects on growth and development. Mol. Endocrinol. 19, 711 – 721
dc.identifier.citedreferenceWalenkamp, M. J., Karperien, M., Pereira, A. M., Hilhorst-Hofstee, Y., van Doorn, J., Chen, J. W., Mohan, S., Denley, A., Forbes, B., van Duyvenvoorde, H. A., van Thiel, S. W., Sluimers, C. A., Bax, J. J., de Laat, J. A., Breuning, M. B., Romijn, J. A., and Wit, J. M. ( 2005 ) Homozygous and heterozygous expression of a novel insulin-like growth factor-I mutation. J. Clin. Endocrinol. Metab. 90, 2855 – 2864
dc.identifier.citedreferenceBaker, J., Liu, J. P., Robertson, E. J., and Efstratiadis, A. ( 1993 ) Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75, 73 – 82
dc.identifier.citedreferenceLiu, J. P., Baker, J., Perkins, A. S., Robertson, E. J., and Efstratiadis, A. ( 1993 ) Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75, 59 – 72
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
fsb2fj053882fje.pdf
Size:
609.7KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe its collections in a way that respects the people and communities who create, use, and are represented in them. We encourage you to Contact Us anonymously if you encounter harmful or problematic language in catalog records or finding aids. More information about our policies and practices is available at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.