Gene duplication and functional divergence of the zebrafish insulin-like growth factor 1 receptors
Abstract
Insulin-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 ig f1r genes in zebrafish, termed ig f1ra and ig f1rb. In this study, we tested the hypothesis that zebrafish ig f1ra and ig f1rb resulted from a gene duplication event at the ig f1r locus and that this has led to their functional divergence. The genomic structures of zebrafish ig f1ra and ig f1rb were determined and their loci mapped. While zebrafish ig f1ra has 21 exons and is located on linkage group (LG) 18, zebrafish ig f1rb has 22 exons and mapped to LG 7. There is a strong syntenic relationship between the two zebrafish genes and the human IG F1R 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 ig f1r 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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Zebrafish have two igf1r genes, igf1ra and igf1rb, that often play overlapping roles.
“Zebrafish harbor 2 igf1r genes, igf1ra and igf1rb that often play overlapping roles (Schlueter et al., 2006).”
From Retinal injury, growth factors, and cytokines converge on β-catenin and pStat3 signaling to stimulate retina regeneration (2014) · cites this paper as Schlueter et al., 2006
Cites
Stages of embryonic development of the zebrafish
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030302 · Cited by 12,037 · see citing works
Ohno, S. (1970) · doi:10.1007/978-3-642-86659-3 · Cited by 7,833 · see citing works
Insulin-Like Growth Factors and Their Binding Proteins: Biological Actions*
Jones, J. I. W., & Clemmons, D. R. (1995) · Endocrine Reviews · doi:10.1210/edrv-16-1-3 · Cited by 4,488 · see citing works
Preservation of Duplicate Genes by Complementary, Degenerative Mutations
Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y.-L., & Postlethwait, J. (1999) · Genetics · doi:10.1093/genetics/151.4.1531 · Cited by 3,529 · see citing works
Liu, J.-P., Baker, J. C., Perkins, A. S., Robertson, E. J., & Efstratiadis, A. (1993) · Cell · doi:10.1016/s0092-8674(05)80084-4 · Cited by 2,854 · see citing works
Role of insulin-like growth factors in embryonic and postnatal growth
Baker, J., Liu, J.-P., Robertson, E. J., & Efstratiadis, A. (1993) · Cell · doi:10.1016/s0092-8674(05)80085-6 · Cited by 2,463 · see citing works
Evolution by gene duplication: An update
Zhang, J. (2003) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(03)00033-8 · Cited by 2,201 · see citing works
Insulin-like growth factors and their binding proteins: biological actions
Jones, J. I. (1995) · Endocrine Reviews · doi:10.1210/er.16.1.3 · Cited by 2,060 · see citing works
Zebrafish hox Clusters and Vertebrate Genome Evolution
Amores, A., Force, A. G., Yan, Y., Joly, L., Amemiya, C. T., Fritz, A., Ho, R. K., Langeland, J. A., Prince, V., Wang, Y.-L., et al. (1998) · Science · doi:10.1126/science.282.5394.1711 · Cited by 1,737 · see citing works
The Somatomedin Hypothesis: 2001
Roith, D. L., Bondy, C. A., Yakar, S., Liu, J., & Butler, A. A. (2001) · Endocrine Reviews · doi:10.1210/edrv.22.1.0419 · Cited by 1,258 · see citing works
Woods, K. A., Camacho‐Hübner, C., Savage, M. O., & Clark, A. (1996) · New England Journal of Medicine · doi:10.1056/nejm199610313351805 · Cited by 1,083 · see citing works
Signal transduction via platelet-derived growth factor receptors
Heldin, C., Östman, A., & Rönnstrand, L. (1998) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/s0304-419x(98)00015-8 · Cited by 740 · see citing works
He, X., & Zhang, J. (2005) · Genetics · doi:10.1534/genetics.104.037051 · Cited by 694 · see citing works
Insulin-like growth factor signaling in fish
Wood, A. W., Duan, C., & Bern, H. A. (2005) · International Review of Cytology · doi:10.1016/s0074-7696(05)43004-1 · Cited by 657 · see citing works
Self-citationThe Syntenic Relationship of the Zebrafish and Human GenomesPreprint
Barbazuk, W. B., Korf, I. F., Kadavi, C., Heyen, J. W., Tate, S., Wun, E., Bedell, J. A., McPherson, J. D., & Johnson, S. L. (2000) · Genome Research · doi:10.1101/gr.144700 · Cited by 650 · see citing works
IGF-I Receptor Mutations Resulting in Intrauterine and Postnatal Growth Retardation
Abuzzahab, M. J., Schneider, A., Goddard, A. D., Grigorescu, F., Lautier, C., Keller, E., Kieß, W., Klammt, J., Kratzsch, J., Osgood, D. P., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa010107 · Cited by 624 · see citing works
Structural biology of insulin and IGF1 receptors: implications for drug design
MEYTS, P. D., & Whittaker, J. (2002) · Nature Reviews Drug Discovery · doi:10.1038/nrd917 · Cited by 584 · see citing works
Distinct and Overlapping Functions of Insulin and IGF-I Receptors
Nakae, J., Kido, Y., & Accili, D. (2001) · Endocrine Reviews · doi:10.1210/edrv.22.6.0452 · Cited by 556 · see citing works
Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural inductionPreprint
Pera, E. M., Ikeda, A., Eivers, E., & Robertis, E. M. D. (2003) · Genes & Development · doi:10.1101/gad.1153603 · Cited by 421 · see citing works
A Comparative Map of the Zebrafish GenomePreprint
Woods, I. G. (2000) · Genome Research · doi:10.1101/gr.10.12.1903 · Cited by 399 · see citing works
Patterning of the Zebrafish Retina by a Wave of Sonic Hedgehog Activity
Neumann, C. J., & Nuesslein-Volhard, C. (2000) · Science · doi:10.1126/science.289.5487.2137 · Cited by 385 · see citing works
Development of the locomotor network in zebrafish
Drapeau, P., Saint-Amant, L., Buss, R. R., Chong, M., McDearmid, J. R., & Brustein, E. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00075-8 · Cited by 376 · see citing works
Retinal Neurogenesis: The Formation of the Initial Central Patch of Postmitotic Cells
Hu, M., & Easter, S. S. (1999) · Developmental Biology · doi:10.1006/dbio.1998.9031 · Cited by 364 · see citing works
Efstratiadis, A. (1998) · The International Journal of Developmental Biology · doi:10.1387/ijdb.9853827 · Cited by 349 · see citing works
The Drosophila insulin receptor is required for normal growth.
Chen, C., Jack, J., & Garofalo, R. S. (1996) · Endocrinology · doi:10.1210/endo.137.3.8603594 · Cited by 338 · see citing works
Homozygous and Heterozygous Expression of a Novel Insulin-Like Growth Factor-I Mutation
Walenkamp, M. J. E., Karperien, M., Pereira, A. M., Hilhorst‐Hofstee, Y., van Doorn, J., Chen, J. W., Mohan, S., Denley, A., Forbes, B. E., van Duyvenvoorde, H. A., et al. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1254 · Cited by 314 · see citing works
Radiation hybrid mapping of the zebrafish genome
Hukriede, N. A., Joly, L., Tsang, M., Miles, J., Tellis, P. A., Epstein, J. A., Barbazuk, W. B., Li, F. N., Paw, B. H., Postlethwait, J. H., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9745 · Cited by 283 · see citing works
Morphant technology in model developmental systems
Ekker, S. C., & Larson, J. D. (2001) · genesis · doi:10.1002/gene.1038 · Cited by 254 · see citing works
A radiation hybrid map of the zebrafish genome
Geisler, R., Rauch, G.-J., Baier, H., van Bebber, F., Broβ, L., Dekens, M. P. S., Finger‐Baier, K., Fricke, C., Gates, M. A., Geiger, H., et al. (1999) · Nature Genetics · doi:10.1038/12692 · Cited by 251 · see citing works
Development of the zebrafish inner ear
Whitfield, T. T., Riley, B. B., Chiang, M., & Phillips, B. T. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10073 · Cited by 232 · see citing works
Neural and Head Induction by Insulin-like Growth Factor Signals
Pera, E. M., Wessely, O., Li, S.-Y., & Robertis, E. M. D. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00069-7 · Cited by 229 · see citing works
Gates, M. A., Kim, L., Egan, E. S., Cardozo, T. J., Sirotkin, H. I., Dougan, S. T., Lashkari, D. A., Abagyan, R. A., Schier, A. F., & Talbot, W. S. (1999) · Genome Research · doi:10.1101/gr.9.4.334 · Cited by 205 · see citing works
Klinghoffer, R. A., Hamilton, T., Hoch, R. V., & Soriano, P. M. (2002) · Developmental Cell · doi:10.1016/s1534-5807(01)00103-4 · Cited by 196 · see citing works
Signalling through IGF-I and insulin receptors: where is the specificity?
Kim, J. J., & Accili, D. (2002) · Growth Hormone & IGF Research · doi:10.1054/ghir.2002.0265 · Cited by 163 · see citing works
Maures, T. J., Chan, S. J., Xu, B., Sun, H., Ding, J., & Duan, C. (2002) · Endocrinology · doi:10.1210/endo.143.5.8768 · Cited by 162 · see citing works
Self-citationMorphants: A New Systematic Vertebrate Functional Genomics Approach
Ekker, S. C. (2000) · Yeast · doi:10.1002/1097-0061(200012)17:4 · Cited by 159 · see citing works
Klinghoffer, R. A., Mueting-Nelsen, P. F., Faerman, A., Shani, M., & Soriano, P. M. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00182-4 · Cited by 148 · see citing works
Pozios, K. C., Ding, J., Degger, B. G., et al. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.4.r1230 · Cited by 140 · see citing works
Kawashima, Y., Kanzaki, S., Yang, F., Kinoshita, T., Hanaki, K., Nagaishi, J.-I., Ohtsuka, Y., Hisatome, I., Ninomoya, H., Nanba, E., et al. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1947 · Cited by 133 · see citing works
Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish
Duan, C., Ding, J., Li, Q., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.15274 · Cited by 128 · see citing works
Self-citationThe IGF Pathway Regulates Head Formation by Inhibiting Wnt Signaling in Xenopus
Richard‐Parpaillon, L., Héligon, C., Chesnel, F., Boujard, D., & Philpott, A. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0605 · Cited by 109 · see citing works
Eivers, E., McCarthy, K., Glynn, C., Nolan, C. M., & Byrnes, L. (2004) · The International Journal of Developmental Biology · doi:10.1387/ijdb.041913ee · Cited by 87 · see citing works
Wood, A. W., Schlueter, P. J., & Duan, C. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0392 · Cited by 80 · see citing works
Self-citationDenley, A., Wang, C. C., McNeil, K. A., et al. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0409 · Cited by 71 · see citing works
Chan, S. J., Plisetskaya, E. M., Urbinati, E. C., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12446 · Cited by 70 · see citing works
Self-citationThe Zebrafish Eye: Developmental and Genetic Analysis
Easter, S. S., & Malicki, J. J. (2002) · Results and problems in cell differentiation · doi:10.1007/978-3-540-46041-1_17 · Cited by 63 · see citing works
Zebrafish insulin-like growth factor-I receptor: molecular cloning and developmental expression
Ayaso, E., Nolan, C. M., & Byrnes, L. (2002) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(02)00083-7 · Cited by 41 · see citing works
Pattern formation in the zebrafish retina
Neumann, C. J. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2001.0272 · Cited by 40 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Wan, J., Zhao, X.-F., Vojtek, A., & Goldman, D. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.048 · Cited by 143 · see citing works
“Zebrafish harbor 2 igf1r genes, igf1ra and igf1rb that often play overlapping roles (Schlueter et al., 2006).”
BackgroundZou, S., Kamei, H., Modi, Z., & Duan, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007026 · Cited by 122 · see citing works
Self-citationThe role of insulin receptor signaling in zebrafish embryogenesis
Toyoshima, Y., Monson, C., Duan, C., Wu, Y., Gao, C., Yakar, S., Sadler, K. C., & LeRoith, D. (2008) · Endocrinology · doi:10.1210/en.2008-0329 · Cited by 72 · see citing works
Self-citationYang, S.-A., Wang, W.-D., Chen, C.-T., Tseng, C.-Y., Chen, Y.-N., & Hsu, H.-J. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.07.018 · Cited by 37 · see citing works
- Authors
- Schlueter, P. J., Royer, T., Farah, M. H., Laser, B., Chan, S. J., Steiner, D. F., Duan, C., Schlueter, P. J., Royer, T., Farah, M. H., Laser, B., Chan, S. J., Steiner, D. F., & Duan, C.
- Venue
- The FASEB Journal
- Publisher
- Wiley
- Published
- 2006-05-16
- Volume
- 20
- Issue
- 8
- Pages
- 1230-1232
- ISSN
- 0892-6638 (ISSN-L)
- 1530-6860
- OpenAlex
- W2155475600
- Cited by
- 71
- References
- 48
- Citations by year
- 2026: 4 · 2024: 1 · 2022: 2 · 2021: 1 · 2020: 1 · 2019: 4 · 2018: 7 · 2017: 3 · 2016: 2 · 2015: 3 · 2014: 3 · 2013: 6 · 2012: 4
- FWCI
- 3.18
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- The FASEB Journal (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Science Foundation (0110864)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Keywords
- IGF-1 receptor, functional divergence, zebrafish, gene family evolution, embryonic development, muscle contractility, syntenic relationships, eye development, inner ear development, heart development, myogenesis
- MeSH terms
- Animals, Cell Survival, Chromosome Mapping, Exons, Eye, Heart, Humans, Insulin-Like Growth Factor I, Introns, Ear, Inner, Motor Neurons, Muscle Contraction, Somatomedins, Zebrafish, Signal Transduction, Receptor, IGF Type 1, Gene Targeting, Gene Duplication, Zebrafish Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
