INTRODUCTION
The developmental roles of the T-box genes have been an area
of intense research for many years (Papaioannou and Silver,
1998; Tada and Smith, 2001). Much of our current
understanding of the critical role of T-box genes comes from
the analysis of phenotypes produced by genetic mutations.
Importantly, several TBX genes are causally implicated
in human congenital malformations. For example, the
cardiovascular defects in DiGeorge syndrome are caused by
haploinsufficiency of TBX1 (Merscher et al., 2001); the ulnar-
mammary syndrome is a pleiotropic disorder characterized by
defects in limb, apocrine gland, tooth and genital development
because of haploinsufficiency of TBX3 (Bamshad et al., 1997);
and Holt-Oram syndrome, a developmental disorder of upper
limb malformation and cardiac septation defects, is associated
with haploinsufficiency of TBX5 (Li et al., 1997; Bruneau et
al., 2001).
The family of T-box transcription factors shares a
phylogenetically conserved DNA-binding domain, which
is required for specific DNA sequence recognition. The
functional activity of these genes are mediated by binding to
their cognate regulatory sites within the promoter and enhancer
regions of genes, leading to the activation or repression of gene
expression depending upon the type of T-box gene and the
context within the promoter (Carreira et al., 1998; He et al.,
1999; Sinha et al., 2000; Tada and Smith, 2001). Members of
this gene family have been shown to have selective patterns
of expression and play many key roles in patterning and
specifying the development of a variety of tissues (Basson et
al., 1999; Merscher et al., 2001; Lamolet et al., 2001; Bruneau
et al., 2001; Tada and Smith, 2001).
We recently described a novel zebrafish T-box gene, hrT
(tbx20 – Zebrafish Information Network), which is expressed
in the developing heart and dorsal aorta (Griffin et al., 2000;
Ahn et al., 2000). hrT is expressed in the cardiogenic
mesoderm of the anterior lateral plate from the beginning of
segmentation, and continues to be expressed in the heart field
until at least 72 hours (Griffin et al., 2000; Ahn et al., 2000).
The onset of hrT expression in the lateral plate is earlier than
the first expression of nkx2.5 or tbx5, and coincident with the
start of nkx2.7 expression (Lee et al., 1996; Begemann and
Ingham, 2000). hrT is thus expressed during all the key stages
of cardiac development, which include cardiac cell fate
specification, morphogenesis, looping of the heart tube and
chamber formation (Srivastavia and Olson, 2000; Yelon et al.,
1999; Stainier, 2001). In addition, hrT begins to be expressed
in the dorsal aorta at the 15-somite stage, in addition to sites
of expression in the hindbrain, eye and at the anal opening
(Griffin et al., 2000; Ahn et al., 2000).
5093 Development 129, 5093-5101 (2002)
Printed in Great Britain © The Company of Biologists Limited 2002
DEV5029
The recently identified zebrafish T-box gene hrT is
expressed in the developing heart and in the endothelial
cells forming the dorsal aorta. Orthologs of hrT are
expressed in cardiovascular cells from Drosophila to mouse,
suggesting that the function of hrT is evolutionarily
conserved. The role of hrT in cardiovascular development,
however, has not thus far been determined in any animal
model. Using morpholino antisense oligonucleotides, we
show that zebrafish embryos lacking hrT function have
dysmorphic hearts and an absence of blood circulation.
Although the early events in heart formation were normal
in hrT morphant embryos, subsequently the hearts failed
to undergo looping, and late onset defects in chamber
morphology and gene expression were observed. In
particular, we found that the loss of hrT function led to
a dramatic upregulation of tbx5, a gene required for
normal heart morphogenesis. Conversely, we show that
overexpression of hrT causes a significant downregulation
of tbx5, indicating that one key role of hrT is to regulate the
levels of tbx5. Secondly, we found that HrT is required to
inhibit the expression of the blood lineage markers gata1
and gata2 in the most posterior lateral plate mesoderm.
Finally, we show that HrT is required for vasculogenesis in
the trunk, leading to similar vascular defects to those
observed in midline mutants such as floating head. hrT
expression in the vascular progenitors depends upon
midline mesoderm, indicating that this expression is one
important component of the response to a midline-derived
signal during vascular morphogenesis.
Key words: Zebrafish, hrT, Cardiogenesis, Dorsal aorta, tbx5, fli1,
floating head
SUMMARY
DEVELOPMENT AND DISEASE
hrT is required for cardiovascular development in zebrafish
Daniel P. Szeto, Kevin J. P. Griffin and David Kimelman*
Department of Biochemistry, Box 357350, University of Washington, Seattle, WA 98195-7530, USA
*Author for correspondence (e-mail: kimelman@u.washington.edu)
Accepted 30 July 2002