INTRODUCTION
The inner ears of vertebrates are responsible for the sensations
of hearing and of balance. Although the two ears are symmetric
about the midline of the organism, each individual organ in
most vertebrate species is asymmetric about all three axes
[anteroposterior/rostrocaudal (AP), dorsoventral (DV) and
mediolateral (ML)]. The zebrafish otic field (defined by the
expression of pax8) is induced at the lateral edges of the neural
plate, adjacent to several presumptive rhombomeres (r) of the
developing hindbrain. By about 14 hours post fertilisation
(hpf), condensation of cells gives rise to distinct thickenings
(the otic placodes) immediately opposite r5 (Kimmel et al.,
1995; Pfeffer et al., 1998; Phillips et al., 2001). The expression
of several genes, for example pax2a (formerly pax2.1), dlx3b
(formerly dlx3) and eya1, is now detected throughout these
placodes (Krauss et al., 1991; Akimenko et al., 1994; Sahly et
al., 1999). The only known genes with restricted patterns of
expression in the otic placode at this stage are the Delta genes.
These are expressed in anterior and posterior domains,
symmetrical about the AP and DV axes, but restricted to the
medial side of the placode (Haddon et al., 1998). It is therefore
likely that at 14 hpf only the ML axis of the otic placode has
been specified.
Asymmetric gene expression patterns about both the AP and
the DV axes are obvious by 18 hpf, when the placode begins
to cavitate to form an otic vesicle. nkx5.1 (hmx3 – Zebrafish
Information Network), which is currently the earliest known
marker of an asymmetry about the AP axis, is expressed in an
anterior domain from around 16 hpf; pax5 is detectable in the
anterior epithelium from 17.5 hpf and dacha is detected in the
dorsal otic epithelium by 17-18 hpf, suggesting that all axes of
the ear have been specified by this time (Pfeffer et al., 1998;
Adamska et al., 2000; Hammond et al., 2002). By 24 hpf,
several further otic genes are expressed asymmetrically, and
this presumably both reflects and reinforces axis specification.
pax5, nkx5.1 and fgf8 are expressed anteriorly, bmp7 and
follistatin posteriorly, dlx3b and dacha dorsally, eya1 ventrally,
and pax2a and dacha medially (Krauss et al., 1991; Akimenko
et al., 1994; Pfeffer et al., 1998; Reifers et al., 1998; Sahly et
al., 1999; Adamska et al., 2000; Mowbray et al., 2001;
Hammond et al., 2002). Sensory epithelium now thickens and
stratifies, and fingers of non-sensory epithelium protrude into
the otic lumen and fuse to form the semicircular canal system
(reviewed by Whitfield et al., 2002).
Fekete and colleagues have proposed a model in which
tissues surrounding the ear provide inductive signals for both
axis specification and further otic differentiation (Fekete, 1996;
Brigande et al., 2000a; Brigande et al., 2000b). They propose
that signals from the hindbrain have dorsalising activity, and
may also be important in providing AP information and
medialising signals to the otic vesicle. Several lines of
1403 Development 130, 1403-1417
© 2003 The Company of Biologists Ltd
doi:10.1242/dev.00360
Currently, few factors have been identified that provide the
inductive signals necessary to transform the simple otic
placode into the complex asymmetric structure of the adult
vertebrate inner ear. We provide evidence that Hedgehog
signalling from ventral midline structures acts directly on
the zebrafish otic vesicle to induce posterior otic identity.
We demonstrate that two strong Hedgehog pathway
mutants, chameleon (con
tf18b
) and slow muscle omitted
(smu
b641
) exhibit a striking partial mirror image
duplication of anterior otic structures, concomitant with
a loss of posterior otic domains. These effects can be
phenocopied by overexpression of patched1 mRNA to
reduce Hedgehog signalling. Ectopic activation of the
Hedgehog pathway, by injection of sonic hedgehog or
dominant-negative protein kinase A RNA, has the reverse
effect: ears lose anterior otic structures and show a mirror
image duplication of posterior regions. By using double
mutants and antisense morpholino analysis, we also show
that both Sonic hedgehog and Tiggy-winkle hedgehog are
involved in anteroposterior patterning of the zebrafish otic
vesicle.
Key words: Hedgehog, Sonic hedgehog, Tiggy-winkle hedgehog,
Inner ear, Zebrafish, Mirror image duplication, slow muscle omitted,
chameleon, Otic vesicle, Axis formation
SUMMARY
Hedgehog signalling is required for correct anteroposterior patterning of the
zebrafish otic vesicle
Katherine L. Hammond, Helen E. Loynes, Amos A. Folarin, Joanne Smith and Tanya T. Whitfield*
Centre for Developmental Genetics, University of Sheffield School of Medicine and Biomedical Science, Western Bank,
Sheffield S10 2TN, UK
*Author for correspondence (e-mail: t.whitfield@sheffield.ac.uk)
Accepted 18 December 2002