Early developmental expression of two insulins in zebrafish (Danio rerio)
Abstract
We have cloned a second insulin gene in zebrafish and studied temporal and spatial expression of two zebrafish insulin genes. Zebrafish insulin-a ( insa) and -b ( insb) mRNAs are derived from two different DNA contigs on chromosomes 5 and 14, respectively, representing two different insulin genes. Real-time PCR studies suggest that insa is a maternal and also a postzygotic transcript. insa was observed at 1 h postfertilization (hpf) and was rapidly degraded by 6 and 12 hpf but induced at 24 hpf (i.e., after pancreas formation). Expression levels at 24 hpf were ∼220-fold higher than at 6 hpf and were significantly different from earlier time points. At 72 hpf (at time of hatching), zebrafish insa mRNA levels tended to be higher than at 24 hpf and were ∼727-fold higher compared with 6 hpf. This further increase in insa expression may be one of the many rapid physiological changes associated with hatching. insb expression was observed from 1 hpf and was significantly decreased from 12 hpf onward. Its expression levels at 12 and 24 hpf were approximately twofold and sixfold lower, respectively, compared with expression at 6 hpf. insb expression levels at 48 hpf were significantly lower than at 24 hpf but not different from 72 hpf. Expression levels at 72 hpf were ∼61-fold lower than at 6 hpf. In situ hybridization studies showed insb expression in proliferating blastomeres at 3 and 4 hpf. At later time points, insb expression was restricted to the brain and pancreas (24 and 48 hpf). insa expression was observed in the pancreas at 24 and 48 hpf. Expression of insb in blastomeres and head suggests that insb could be acting as a pro-growth, survival, and neurotrophic factor during development. Pancreatic insa and insb may both be involved in regulation of glucose homeostasis as in mammals.
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Human Insulin is active in zebrafish because its mature form shares extensive amino acid identity with zebrafish Insulin and was previously shown to activate zebrafish Insulin receptors.
“We suspected that human Insulin would be active in zebrafish because its mature form exhibits extensive amino acid identity (~77%) with that of zebrafish and it was previously shown to activate zebrafish Insulin receptors (Papasani et al., 2006; Toyoshima et al., 2008).”
From Retinal injury, growth factors, and cytokines converge on β-catenin and pStat3 signaling to stimulate retina regeneration (2014) · cites this paper as Papasani et al., 2006
Cites
The zebrafish book : a guide for the laboratory use of zebrafish (Danio rerio)
Westerfield, M. (1995) · Medical Entomology and Zoology · Cited by 6,813 · see citing works
Fetal and infant growth and impaired glucose tolerance at age 64
Hales, C. N., Barker, D. J., Clark, P. M., Cox, L. J., Fall, C., Osmond, C., & Winter, P. D. (1991) · BMJ · doi:10.1136/bmj.303.6809.1019 · Cited by 2,708 · 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
Gene Activity in Early Development
Davidson, E. H. (1968) · Elsevier eBooks · doi:10.1016/c2013-0-12432-4 · Cited by 1,704 · see citing works
Steen, E., Terry, B. M., J. Rivera, E., Cannon, J. L., Neely, T. R., Tavares, R., Xu, X. J., Wands, J. R., & de la Monte, S. M. (2005) · Journal of Alzheimer's Disease · doi:10.3233/jad-2005-7107 · Cited by 1,703 · see citing works
Zebrafish Comparative Genomics and the Origins of Vertebrate Chromosomes
Postlethwait, J. H., Woods, I. G., Ngo-Hazelett, P., Yan, Y.-L., Kelly, P. D., Chu, F., Huang, H., Hill-Force, A., & Talbot, W. S. (2000) · Genome Research · doi:10.1101/gr.164800 · Cited by 688 · see citing works
The new enzymology of precursor processing endoproteases.
Steiner, D. F., Smeekens, S. P., Ohagi, S., & Chan, S. J. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)35852-6 · Cited by 612 · see citing works
Early neonatal death in mice homozygous for a null allele of the insulin receptor gene
Accili, D., Drago, J., Lee, E. J., Johnson, M. D., Cool, M. H., Salvatore, P., Asico, L. D., José, P. A., Taylor, S. I., & Westphal, H. (1996) · Nature Genetics · doi:10.1038/ng0196-106 · Cited by 594 · see citing works
de la Monte, S. M., & Wands, J. R. (2005) · Journal of Alzheimer s Disease · doi:10.3233/jad-2005-7106 · Cited by 552 · see citing works
Insulin and Insulin-like Growth Factor-1 Regulate Tau Phosphorylation in Cultured Human Neurons*
Hong, M., & Lee, V. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.31.19547 · Cited by 533 · see citing works
The structure and evolution of the two nonallelic rat preproinsulin genes
Lomedico, P. T., Rosenthal, N. A., Efstratiadis, A., et al. (1979) · Cell · doi:10.1016/0092-8674(79)90071-0 · Cited by 498 · see citing works
Insulin Receptor Substrate-2 Deficiency Impairs Brain Growth and Promotes Tau Phosphorylation
Schubert, M., Brazil, D. P., Burks, D. J., Kushner, J. A., Ye, J., Flint, C. L., Farhang-Fallah, J., Dikkes, P., Warot, X. M., Rio, C., et al. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-18-07084.2003 · Cited by 488 · see citing works
Subfunction partitioning, the teleost radiation and the annotation of the human genome
Postlethwait, J. H., Amores, A., Cresko, W. A., Singer, A., & Yan, Y. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.08.001 · Cited by 395 · see citing works
Role for neuronal insulin resistance in neurodegenerative diseases
Schubert, M., Gautam, D., Surjo, D., Ueki, K., Baudler, S., Schubert, D., Kondo, T., Alber, J., Galldiks, N., Kustermann, E., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308724101 · Cited by 339 · see citing works
Barber, A. J., Nakamura, M., Wolpert, E. B., Reiter, C. E. N., Seigel, G. M., Antonetti, D. A., & Gardner, T. W. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104738200 · Cited by 288 · see citing works
Phenotypic alterations in insulin-deficient mutant mice
Duvillié, B., Cordonnier, N., Deltour, L., Dandoy‐Dron, F., Itier, J., Monthioux, E., Jami, J., Joshi, R. L., & Bucchini, D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5137 · Cited by 272 · see citing works
STRUCTURE AND EVOLUTION OF THE INSULIN GENE
Steiner, D. F., Chan, S. J., Welsh, M., & Kwok, S. C. M. (1985) · Annual Review of Genetics · doi:10.1146/annurev.ge.19.120185.002335 · Cited by 260 · see citing works
Biemar, F., Argenton, F., Schmidtke, R., Epperlein, S., Peers, B., & Driever, W. (2001) · Developmental Biology · doi:10.1006/dbio.2000.0103 · Cited by 224 · see citing works
Differential expression of the two nonallelic proinsulin genes in the developing mouse embryo.
Deltour, L., Leduque, P., Blume, N., Madsen, O., Dubois, P. M., Jami, J., & Bucchini, D. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.2.527 · Cited by 193 · see citing works
Insulin II gene expression in rat central nervous system
Devaskar, S. U., Singh, B. S., Carnaghi, L. R., Rajakumar, P. A., & Giddings, S. J. (1993) · Regulatory Peptides · doi:10.1016/0167-0115(93)90335-6 · Cited by 137 · see citing works
Conservation of PDX-1 Structure, Function, and Expression in Zebrafish*
Milewski, W. M., Duguay, S. J., Chan, S. J., et al. (1998) · Endocrinology · doi:10.1210/endo.139.3.5768 · Cited by 134 · see citing works
Schechter, R., Beju, D., Gaffney, T. J., Schaefer, F., & Whetsell, L. H. (1996) · Brain Research · doi:10.1016/0006-8993(96)00664-6 · Cited by 92 · see citing works
Insulin in Brain and Other Extrapancreatic Tissues of Vertebrates and Nonvertebrates
Roith, D. L., HENDRICKS, S. A., Lesniak, M. A., Rishi, S., Becker, K. L., Havránková, J., Rosenzweig, J. L., Brownstein, M., & Roth, J. (1983) · Advances in metabolic disorders · doi:10.1016/b978-0-12-027310-2.50017-7 · Cited by 56 · see citing works
Girbau, M. M., Bassas, L., Alemany, J., et al. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.15.5868 · Cited by 55 · see citing works
Effects of brain endogenous insulin on neurofilament and MAPK in fetal rat neuron cell cultures
Schechter, R., Yanovitch, T. L., Abboud, M., Johnson, G., & Gaskins, J. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00842-7 · Cited by 51 · see citing works
Shuldiner, A. R., de Pablo, F., Moore, C. A., et al. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7679 · Cited by 50 · see citing works
Role of Prepancreatic (Pro)Insulin and the Insulin Receptor in Prevention of Embryonic Apoptosis1
Morales, A. V., Serna, J., Alarcón, C., et al. (1997) · Endocrinology · doi:10.1210/endo.138.9.5396 · Cited by 50 · see citing works
Planas, J. V., Méndez, E., Baños, N., et al. (2000) · Journal of Experimental Biology · doi:10.1242/jeb.203.7.1153 · Cited by 47 · see citing works
Xenopus laevis Contains Two Nonallelic Preproinsulin Genes
Shuldiner, A. R., Phillips, S., Roberts, C. T., et al. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)60549-6 · Cited by 46 · see citing works
Schechter, R., Whitmire, J., Wheet, G. S., Beju, D., Jackson, K. W., Harlow, R. D., & Gavin, J. R. (1994) · Brain Research · doi:10.1016/0006-8993(94)90170-8 · Cited by 45 · see citing works
A second insulin gene in fish genomes
Irwin, D. M. (2003) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2003.08.004 · Cited by 43 · see citing works
Pérez‐Villamil, B., de la Rosa, E. J., Morales, A. V., et al. (1994) · Endocrinology · doi:10.1210/endo.135.6.7988416 · Cited by 42 · see citing works
Insulin and insulin-like growth factor I (IGF I) in early mouse embryogenesis
Spaventi, R., Antica, M., & Pavelić, K. (1990) · Development · doi:10.1242/dev.108.3.491 · Cited by 41 · see citing works
Wanda: a database of duplicated fish genes
de Peer, Y. V. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.109 · Cited by 40 · see citing works
Unprocessed Proinsulin Promotes Cell Survival During Neurulation in the Chick Embryo
Hernández‐Sánchez, C., Rubio, E., Serna, J., et al. (2002) · Diabetes · doi:10.2337/diabetes.51.3.770 · Cited by 40 · see citing works
Does Salmon Brain Produce Insulin?
Plisetskaya, E. M., Бондарева, В. М., Duan, C., et al. (1993) · General and Comparative Endocrinology · doi:10.1006/gcen.1993.1106 · Cited by 30 · see citing works
Amino Acid Sequence of the two Insulins from Mouse(Mus musculus)
Bünzli, H. F., Glatthaar, B. E., Kunz, P. A., et al. (1972) · Hoppe-Seyler´s Zeitschrift für physiologische Chemie · doi:10.1515/bchm2.1972.353.1.451 · Cited by 30 · see citing works
Genetic Analysis of Early Endocrine Pancreas Formation in Zebrafish
Kim, H. J., Sumanas, S., Desai, S. P., Dong, Y., Chen, J., & Lin, S. (2005) · Molecular Endocrinology · doi:10.1210/me.2005-0189 · Cited by 28 · see citing works
Two insulins from channel catfish: purification, structures, receptor-binding and cDNA sequences
Mommsen, T. P., Silverstein, J. T., Plisetskaya, E. M., et al. (2001) · Fish Physiology and Biochemistry · doi:10.1023/a:1019708017696 · Cited by 18 · see citing works
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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
“We suspected that human Insulin would be active in zebrafish because its mature form exhibits extensive amino acid identity (~77%) with that of zebrafish and it was previously shown to activate zebrafish Insulin receptors (Papasani et al., 2006; Toyoshima et al., 2008).”
BackgroundZou, S., Kamei, H., Modi, Z., & Duan, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007026 · Cited by 122 · see citing works
The 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
- Authors
- Papasani, M. R., Robison, B. D., Hardy, R. W., & Hill, R. A.
- Affiliations
- University of Idaho (US)
- Venue
- Physiological Genomics
- Publisher
- American Physiological Society
- Published
- 2006-09
- Volume
- 27
- Issue
- 1
- Pages
- 79-85
- ISSN
- 1094-8341 (ISSN-L)
- 1531-2267
- OpenAlex
- W2116317329
- Cited by
- 66
- References
- 39
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 7 · 2022: 3 · 2021: 1 · 2020: 5 · 2019: 2 · 2018: 5 · 2017: 3 · 2016: 5 · 2015: 4 · 2014: 2 · 2013: 2 · 2012: 2
- FWCI
- 4.04
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiological Genomics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- 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
- insulin, zebrafish, gene expression, embryonic development, pancreatic development, maternal mRNA, blastomeres, hatching, glucose homeostasis, neurotrophic factors
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Chromosome Mapping, Cloning, Molecular, Insulin, Molecular Sequence Data, RNA, Messenger, Zebrafish, Gene Expression, Sequence Alignment, In Situ Hybridization, Zebrafish Proteins
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