Insulin-like growth factor-2 regulates early neural and cardiovascular system development in zebrafish embryos

International Journal of Developmental Biology

Volumn 54, Issue 4, 2010, Pages 573-583

  Hartnett, Lori ^a   Glynn, Catherine ^a   Nolan, Catherine M ^b   Grealy, Maura ^a   Byrnes, Lucy ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cardiovascular; Development; IGF 2; Neural; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; INSULIN LIKE GROWTH FACTOR 2A; INSULIN LIKE GROWTH FACTOR 2B; NOTCH1 RECEPTOR; SOMATOMEDIN B; TRANSCRIPTION FACTOR GATA 2; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYO SEGMENTATION; GASTRULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME; HEART DEVELOPMENT; HEART LEFT VENTRICLE OUTFLOW TRACT; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VALVE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TISSUE SPECIFICITY; ZEBRA FISH;

ANIMALS; CARDIOVASCULAR SYSTEM; DIANISIDINE; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; NERVOUS SYSTEM; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; SOMATOMEDINS; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 77950536101     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.092922lh     Document Type: Article

References (58)

1. AMORES, A., FORCE, A., YAN, Y.L., JOLY, L., AMEMIYA, C., FRITZ, A., HO, R.K., LANGELAND, J., PRINCE, V., WANG, Y.L. et al. (1998). Zebrafish hox clusters and vertebrate genome evolution. Science 282: 1711-1714.
2. ARCINIEGAS, E., NEVES, Y.C. and CARRILLO, L.M. (2006). Potential role for insulin-like growth factor II and vitronectin in the endothelial-mesenchymal transition process. Differentiation 74: 277-292.
3. ARMSTRONG, E.J. and BISCHOFF, J. (2004). Heart valve development: endothelial cell signaling and differentiation. Circ Res 95: 459-470.
4. BROWN, L.A., RODAWAY, A.R., SCHILLING, T.F., JOWETT, T., INGHAM, P.W., PATIENT, R.K. and SHARROCKS, A.D. (2000). Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos. Mech Dev 90: 237-252.
5. CHUANG, J.C., MATHERS, P.H. and RAYMOND, P.A. (1999). Expression of three Rx homeobox genes in embryonic and adult zebrafish. Mech Dev 84: 195-198.
6. CROSIER, P.S., KALEV-ZYLINSKA, M.L., HALL, C.J., FLORES, M.V., HORSFIELD, J.A. and CROSIER, K.E. (2002). Pathways in blood and vessel development revealed through zebrafish genetics. Int J Dev Biol 46: 493-502.
7. DE ROBERTIS, E.M. and KURODA, H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20: 285-308.
8. DECHIARA, T.M., EFSTRATIADIS, A. and ROBERTSON, E.J. (1990). A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345: 78-80.
9. DETRICH, H.W., 3 RD, KIERAN, M.W., CHAN, F.Y., BARONE, L.M., YEE, K., RUNDSTADLER, J.A., PRATT, S., RANSOM, D. and ZON, L.I. (1995). Intraembryonic hematopoietic cell migration during vertebrate development. Proc Natl Acad Sci USA 92: 10713-10717.
10. EIVERS, 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.
11. FEKANY, K., YAMANAKA, Y., LEUNG, T., SIROTKIN, H.I., TOPCZEWSKI, J., GATES, M.A., HIBI, M., RENUCCI, A., STEMPLE, D., RADBILL, A. et al. (1999). The zebrafish bozozok locus encodes Dharma, a homeodomain protein essential for induction of gastrula organizer and dorsoanterior embryonic structures. Development 126: 1427-1438.
12. FUENTEALBA, L.C., EIVERS, E., IKEDA, A., HURTADO, C., KURODA, H., PERA, E.M. and DE ROBERTIS, E.M. (2007). Integrating patterning signals: Wnt/ GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131: 980-993.
13. FURTHAUER, M., THISSE, C. and THISSE, B. (1997). A role for FGF-8 in the dorsoventral patterning of the zebrafish gastrula. Development 124: 4253-4264.
14. GERING, M., RODAWAY, A.R., GÖTTGENS, B., PATIENT, R.K. and GREEN, A.R. (1998). The SCL gene specifies haemangioblast development from early mesoderm. EMBO J 17: 4029-4045.
15. GONZALEZ, E.M., FEKANY-LEE, K., CARMANY-RAMPEY, A., ERTER, C., TOPCZEWSKI, J., WRIGHT, C.V. and SOLNICA-KREZEL, L. (2000). Head and trunk in zebrafish arise via coinhibition of BMP signaling by bozozok and chordino. Genes Dev 14: 3087-3092.
16. HAMMERSCHMIDT, M., PELEGRI, F., MULLINS, M.C., KANE, D.A., VAN EEDEN, F.J., GRANATO, M., BRAND, M., FURUTANI-SEIKI, M., HAFFTER, P., HEISENBERG, C.P. et al. (1996). dino and mercedes, two genes regulating dorsal development in the zebrafish embryo. Development 123: 95-102.
17. HE, X. and ZHANG, J. (2005). Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169: 1157-1164.
18. HERR, F., LIANG, O.D., HERRERO, J., LANG, U., PREISSNER, K.T., HAN, V.K. and ZYGMUNT, M. (2003). Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy. J Clin Endocrinol Metab 88: 4811-4817.
19. HOLZENBERGER, M., LAPOINTE, F. and AYER-LELIEVRE, C. (2000). Expression of insulin-like growth factor-I (IGF-I) and IGF-II in the avian brain: relationship of in situ hybridization patterns with IGF type 1 receptor expression. Int J Dev Neurosci 18: 69-82.
20. IUCHI, I. and YAMAMOTO, M. (1983). Erythropoiesis in the developing rainbow trout, Salmo gairdneri irideus: histochemical and immunochemical detection of erythropoietic organs. J Exp Zool 226: 409-417.
21. KRETZSCHMAR, M., DOODY, J. and MASSAGUÉ, J. (1997). Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389: 618-622.
22. LAU, M.M., STEWART, C.E., LIU, Z., BHATT, H., ROTWEIN, P. and STEWART, C.L. (1994). Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 8: 2953-2963.
23. LAUSTSEN, P.G., RUSSELL, S.J., CUI, L., ENTINGH-PEARSALL, A., HOLZENBERGER, M., LIAO, R. and KAHN, C.R. (2007). Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol Cell Biol 27: 1649-1664.
24. LAWSON, N.D. and WEINSTEIN, B.M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318.
25. LEE, J.E., PINTAR, J. and EFSTRATIADIS, A. (1990). Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis. Development 110: 151-159.
26. LEMBO, G., ROCKMAN, H.A., HUNTER, J.J., STEINMETZ, H., KOCH, W.J., MA, L., PRINZ, M.P., ROSS, J., JR., CHIEN, K.R. and POWELL-BRAXTON, L. (1996). Elevated blood pressure and enhanced myocardial contractility in mice with severe IGF-1 deficiency. J Clin Invest 98: 2648-2655.
27. LEVIN, M. (2005). Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 122: 3-25.
28. LI, Y.X., ZDANOWICZ, M., YOUNG, L., KUMISKI, D., LEATHERBURY, L. and KIRBY, M.L. (2003). Cardiac neural crest in zebrafish embryos contributes to myocardial cell lineage and early heart function. Dev Dyn 226: 540-550.
29. LIEN, C.L., SCHEBESTA, M., MAKINO, S., WEBER, G.J. and KEATING, M.T. (2006). Gene expression analysis of zebrafish heart regeneration. PLoS Biol 4: e260.
30. LIU, 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.
31. LIU, Q., YAN, H., DAWES, N.J., MOTTINO, G.A., FRANK, J.S. and ZHU, H. (1996). Insulin-like growth factor II induces DNA synthesis in fetal ventricular myocytes in vitro. Circ Res 79: 716-726.
32. MARTINEZ-BARBERÁ, J.P., TORESSON, H., DA ROCHA, S. and KRAUSS, S. (1997). Cloning and expression of three members of the zebrafish Bmp family: Bmp2a, Bmp2b and Bmp4. Gene 198: 53-59.
33. MAURES, 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 ligands in zebrafish. Endocrinology 143: 1858-1871.
34. MCMULLEN, J.R., SHIOI, T., HUANG, W.Y., ZHANG, L., TARNAVSKI, O., BISPING, E., SCHINKE, M., KONG, S., SHERWOOD, M.C., BROWN, J. et al. (2004). The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway. J Biol Chem 279: 4782-4793.
35. MIAO, M., BRUCE, A.E., BHANJI, T., DAVIS, E.C. and KEELEY, F.W. (2007). Differential expression of two tropoelastin genes in zebrafish. Matrix Biol 26: 115-124.
36. MILLER-BERTOGLIO, V.E., FISHER, S., SÁNCHEZ, A., MULLINS, M.C. and HALPERN, M.E. (1997). Differential regulation of chordin expression domains in mutant zebrafish. Dev Biol 192: 537-550.
37. MORALI, O.G., DELMAS, V., MOORE, R., JEANNEY, C., THIERY, J.P. and LARUE, L. (2001). IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 20: 4942-4950.
38. NIKAIDO, M., TADA, M., SAJI, T. and UENO, N. (1997). Conservation of BMP signaling in zebrafish mesoderm patterning. Mech Dev 61: 75-88.
39. NORNES, S., CLARKSON, M., MIKKOLA, I., PEDERSEN, M., BARDSLEY, A., MARTINEZ, J.P., KRAUSS, S. and JOHANSEN, T. (1998). Zebrafish contains two pax6 genes involved in eye development. Mech Dev 77: 185-196.
40. PERA, 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.
41. PERA, 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.
42. POZIOS, K.C., DING, J., DEGGER, B., UPTON, Z. and DUAN, C. (2001). IGFs stimulate zebrafish cell proliferation by activating MAP kinase and PI3-kinase-signaling pathways. Am J Physiol Regul Integr Comp Physiol 280: R1230-1239.
43. RICHARD-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.
44. RISAU, W. (1997). Mechanisms of angiogenesis. Nature 386: 671-674.
45. SANG, X., CURRAN, M.S. and WOOD, A.W. (2008). Paracrine insulin-like growth factor signaling influences primordial germ cell migration: in vivo evidence from the zebrafish model. Endocrinology 149: 5035-5042.
46. SAPKOTA, G., ALARCON, C., SPAGNOLI, F.M., BRIVANLOU, A.H. and MASSAGUE, J. (2007). Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25: 441-454.
47. SCHERZ, P.J., HUISKEN, J., SAHAI-HERNANDEZ, P. and STAINIER, D.Y. (2008). High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development 135: 1179-1187.
48. SCHLUETER, P.J., PENG, G., WESTERFIELD, M. and DUAN, C. (2007). Insulin-like growth factor signaling regulates zebrafish embryonic growth and development by promoting cell survival and cell cycle progression. Cell Death Differ 14: 1095-1105.
49. STAINIER, D.Y. (2001). Zebrafish genetics and vertebrate heart formation. Nat Rev Genet 2: 39-48.
50. THISSE, C., THISSE, B., HALPERN, M. E. and POSTLETHWAIT, J. H. (1994). Goosecoid expression in neuroectoderm and mesendoderm is disrupted in zebrafish cyclops gastrulas. Dev. Biol. 164: 420-429.
51. THOMPSON, M.A., RANSOM, D.G., PRATT, S.J., MACLENNAN, H., KIERAN, M.W., DETRICH, H.W., 3RD, VAIL, B., HUBER, T.L., PAW, B., BROWNLIE, A.J. et al. (1998). The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev Biol 197: 248-269.
52. VALENTINIS, B., ROMANO, G., PERUZZI, F., MORRIONE, A., PRISCO, M., SODDU, S., CRISTOFANELLI, B., SACCHI, A. and BASERGA, R. (1999). Growth and differentiation signals by the insulin-like growth factor 1 receptor in hemopoietic cells are mediated through different pathways. J Biol Chem 274: 12423-12430.
53. WESTERFIELD, M. (1995). The Zebrafish book. University of Oregon Press, Eugene.
54. WESTIN, J., LARDELLI, M. (1997). Three novel Notch genes in zebrafish: implications for vertebrate Notch gene evolution and function. Dev Genes Evol 207: 51-63.
55. WOOD, A.W., DUAN, C. and BERN, H.A. (2005a). Insulin-like growth factor signaling in fish. Int Rev Cytol 243: 215-285.
56. WOOD, A.W., SCHLUETER, P.J. and DUAN, C. (2005b). Targeted knockdown of insulin-like growth factor binding protein-2 disrupts cardiovascular development in zebrafish embryos. Mol Endocrinol 19: 1024-1034.
57. YELON, D., HORNE, S.A. and STAINIER, D.Y. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev Biol 214: 23-37.
58. ZAINA, S., PETTERSSON, L., THOMSEN, A.B., CHAI, C.M., QI, Z., THYBERG, J. and NILSSON, J. (2003). Shortened life span, bradycardia, and hypotension in mice with targeted expression of an igf2 transgene in smooth muscle cells. Endocrinology 144: 2695-2703.