INTRODUCTION
Tbx1, a T-box putative transcription factor, is required for the
segmentation of the pharyngeal apparatus, and homozygous
mutation causes multiple developmental defects, including
cardiovascular, craniofacial, ear, thymic and parathyroid
defects (Jerome and Papaioannou, 2001; Lindsay et al., 2001;
Vitelli et al., 2002). Tbx1 expression has been extensively
analyzed by RNA in situ hybridization (Chapman et al., 1996;
Garg et al., 2001; Jerome and Papaioannou, 2001; Lindsay et
al., 2001; Merscher et al., 2001) and by a lacZ reporter knocked
into the endogenous locus (Vitelli et al., 2002). The expression
pattern is dynamic during development and is mainly localized
in the head mesenchyme, pharyngeal endoderm, core
mesenchyme of the cranial pharyngeal arches, outflow tract of
the heart, mesenchyme surrounding the dorsal aortae, otocyst
and sclerotome. Tbx1 haploinsufficiency causes aortic arch
patterning defects in mice (Jerome and Papaioannou, 2001;
Lindsay et al., 2001; Merscher et al., 2001) of the same type
as those observed in a mouse model, named Df1/+ of the
chromosomal deletion occurring in individuals with DiGeorge
syndrome (Lindsay et al., 1999). The mouse deletion Df1 and
the human deletion del22q11 both include Tbx1, making this
gene the most likely candidate for a pathogenetic role in this
syndrome.
Tbx1 haploinsufficiency causes early growth and remodeling
defects of the fourth pharyngeal arch arteries (PAAs), first
evident at embryonic day (E) 10.5. The caudal PAAs (third,
fourth and sixth) form sequentially as symmetric vessels
connecting the aortic sac with the dorsal aortae. From ~E11.5,
the PAAs undergo a major, asymmetric remodeling that leads
to the mature aortic arch and great vessel patterning (Srivastava
and Olson, 2000). In particular, the left fourth PAA contributes
to the section of the mature aortic arch between the origins of
the left common carotid artery and the left subclavian artery.
Developmental failure of the left fourth PAA causes
interruption of the aortic arch type B (IAA-B). The right fourth
PAA provides the connection of the right subclavian artery
with the innominate artery. Developmental failure of the right
fourth PAA causes aberrant origin of the right subclavian
artery, most commonly from the descending aorta, via a
retroesophageal vessel.
4605 Development 129, 4605-4611 (2002)
Printed in Great Britain © The Company of Biologists Limited 2002
DEV14544
Tbx1 haploinsufficiency causes aortic arch abnormalities
in mice because of early growth and remodeling defects of
the fourth pharyngeal arch arteries. The function of Tbx1
in the development of these arteries is probably cell non-
autonomous, as the gene is not expressed in structural
components of the artery but in the surrounding
pharyngeal endoderm. We hypothesized that Tbx1 may
trigger signals from the pharyngeal endoderm directed to
the underlying mesenchyme. We show that the expression
patterns of Fgf8 and Fgf10, which partially overlap with
Tbx1 expression pattern, are altered in Tbx1
–/–
mutants. In
particular, Fgf8 expression is abolished in the pharyngeal
endoderm. To understand the significance of this finding
for the pathogenesis of the mutant Tbx1 phenotype, we
crossed Tbx1 and Fgf8 mutants. Double heterozygous
Tbx1
+/–
;Fgf8
+/–
mutants present with a significantly
higher penetrance of aortic arch artery defects than do
Tbx1
+/–
;Fgf8
+/+
mutants, while Tbx1
+/+
;Fgf8
+/–
animals are
normal. We found that Fgf8 mutation increases the severity
of the primary defect caused by Tbx1 haploinsufficiency,
i.e. early hypoplasia of the fourth pharyngeal arch arteries,
consistent with the time and location of the shared
expression domain of the two genes. Hence, Tbx1 and Fgf8
interact genetically in the development of the aortic arch.
Our data provide the first evidence of a genetic link
between Tbx1 and FGF signaling, and the first example of
a modifier of the Tbx1 haploinsufficiency phenotype. We
speculate that the FGF8 locus might affect the penetrance
of cardiovascular defects in individuals with chromosome
22q11 deletions involving TBX1.
Key words: Pharyngeal endoderm, Pharyngeal arch arteries,
Phenotypic modifiers
SUMMARY
DEVELOPMENT AND DISEASE
A genetic link between Tbx1 and fibroblast growth factor signaling
Francesca Vitelli
1
, Ilaria Taddei
1
, Masae Morishima
1
, Erik N. Meyers
2
, Elizabeth A. Lindsay
1
and Antonio Baldini
1,3
1
Department of Pediatrics (Cardiology), Baylor College of Medicine, Houston TX 77030, USA
2
Department of Pediatrics and Cell Biology, Duke University Medical Center, Durham NC 27710, USA
3
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston TX 77030, USA
*Author for correspondence (e-mail: baldini@bcm.tmc.edu)
Accepted 1 July 2002