Insulin-like growth factor-2 regulates early neural and
cardiovascular system development in zebrafish embryos
LORI HARTNETT
1
, CATHERINE GLYNN
1
, CATHERINE M. NOLAN
2
, MAURA GREALY
3
and LUCY BYRNES*
,1
1
Department of Biochemistry, National University of Ireland, Galway, Ireland,
2
School of Biology and Environmental Science, University College Dublin, Ireland and
3
Department of Pharmacology and Therapeutics, National University of Ireland, Galway, Ireland
ABSTRACT The insulin-like growth factor (IGF) family is essential for normal embryonic growth
and development and it is highly conserved through vertebrate evolution. However, the roles that
the individual members of the IGF family play in embryonic development have not been fully
elucidated. This study focuses on the role of IGF-2 in zebrafish embryonic development. Two igf-
2 genes, igf-2a and igf-2b, are present in the zebrafish genome. Antisense morpholinos were
designed to knock down both igf-2 genes. The neural and cardiovascular defects in IGF-2
morphant embryos were then examined further using wholemount in situ hybridisation, TUNEL
analysis and O-dianisidine staining. Knockdown of igf-2a or igf-2b resulted in ventralised embryos
with reduced growth, reduced eyes, disrupted brain structures and a disrupted cardiovascular
system, with igf-2b playing a more significant role in development. During gastrulation, igf-2a and
igf-2b are required for development of anterior neural structures and for regulation of genes
critical to dorsal-ventral patterning. As development proceeds, igf-2a and igf-2b play anti-
apoptotic roles. Gene expression analysis demonstrates that igf-2a and igf-2b play overlapping
roles in angiogenesis and cardiac outflow tract development. Igf-2b is specifically required for
cardiac valve development and cardiac looping. Injection of a dominant negative IGF-1 receptor
led to similar defects in angiogenesis and cardiac valve development, indicating IGF-2 signals
through this receptor to regulate cardiovascular development. This is the first study describing
two functional igf-2 genes in zebrafish. This work demonstrates that igf-2a and igf-2b are critical
to neural and cardiovascular development in zebrafish embryos. The finding that igf-2a and igf-
2b do not act exclusively in a redundant manner may explain why both genes have been stably
maintained in the genome.
KEY WORDS: zebrafish, IGF-2, neural, cardiovascular, development
Introduction
Insulin-like growth factor-2 (IGF-2) is a single chain polypep-
tide that acts as a foetal promoter of cell growth, survival and
differentiation. In mammals, IGF-2 can bind to two receptors: the
IGF-1 receptor (IGF-1R) and the IGF-2 receptor (IGF-2R). The
IGF-1R belongs to the tyrosine kinase receptor superfamily. It is
a heterotetrameric transmembrane protein, which mediates most
of the effects of IGF-1 and IGF-2. The IGF-2R is a single-chain
transmembrane protein and there is no evidence of a role for the
IGF-2R in transducing IGF-2 signals. The IGF family is made
more complex by the presence of IGF binding proteins (IGFBPs).
Int. J. Dev. Biol. 54: 573-583 (2010)
doi: 10.1387/ijdb.092922lh
THE INTERNATIONAL JOURNAL OF
DEVELOPMENTAL
BIOLOGY
www.intjdevbiol.com
*Address correspondence to: Dr. Lucy Byrnes. Department of Biochemistry, National University of Ireland, Galway, Ireland. Fax: +353-91-525700.
e-mail: lucy.byrnes@nuigalway.ie - Web: http://www.nuigalway.ie/biochemistry/staff/byrnes/index.html
Supplementary Material for this paper (tables, figures and 3 movies) is available at: http://dx.doi.org/10.1387/ijdb.092922lh
Accepted: 20 April 2009. Final author-corrected PDF published online: 4 September 2009. Edited by: Edward de Robertis
ISSN: Online 1696-3547, Print 0214-6282
© 2009 UBC Press
Printed in Spain
Abbreviations used in this paper: BMP, bone morphogenetic protein; DN-IGF-
1R, dominant negative insulin-like growth factor-1 receptor; eln2, tropoelastin
2; GSK3, glycogen synthase kinase 3; hpf, hours post fertilisation; IGF,
insulin-like growth factor; IGFBP, IGF binding protein; IGF-1R, IGF-1
receptor; MAPK, mitogen activated protein kinase; PI3K, phosphatidylinositol-
3 kinase; TUNEL, terminal deoxynucleotidyl transferase dUTP nick end
labelling.
These act to modulate the actions of IGFs by either inhibiting or
augmenting their availability. The majority of IGF signals are
transduced by ligand binding to the IGF-1R. This triggers
autophosphorylation of the receptor, which ultimately leads to the