INTRODUCTION
The vertebrate hindbrain became a focus of attention for devel-
opmental biologists when studies of HOM/Hox gene
expression revealed startling similarities between its antero-
posterior patterning and that of the insect body axis (Graham
et al., 1989; Duboule and Dollé et al., 1989; Lumsden and
Keynes, 1989; Wilkinson et al., 1989b; McGinnis and
Krumlauf, 1992). A number of other genes are now known to
be expressed in the hindbrain in patterns suggesting that they
act in conjunction with the Hox genes as part of a control
system that organises the development of this part of the body.
The task now is to understand how the control system operates:
which genes regulate which others, and how do they govern
the anatomical development? For this, we need to identify as
many as possible of the genes involved and to analyse their
mutant phenotypes both in terms of effects on the expression
patterns and activities of other genes and in terms of effects on
body structure. In this paper, we examine the role of the
kreisler gene.
kreisler, an X-ray-induced recessive mutation, was first
described by Hertwig (1944). The homozygous adult is normal
in outward appearance, but easily identified by its deafness and
abnormal circling behaviour, a consequence of gross malfor-
mation of its inner ears. There have been several subsequent
studies of kreisler development (Ruben, 1973; Van De Water
and Ruben, 1974; Li, 1979). In particular, Deol (1964) reported
that in the kreisler embryo the earliest abnormalities are to be
seen, concurrently, in the positioning of the otic placodes and
in the segmentation of the hindbrain. In this paper, it is the
abnormalities of the hindbrain that particularly concern us; for
Deol’s detailed description suggested that these might reflect
a fundamental disturbance of the mechanisms controlling
anteroposterior specification.
This hypothesis has been investigated by Frohman et al.
(1993), who have analysed the kreisler hindbrain in terms of
the expression of five genes – Hoxb-1, Hoxb-3, Hoxb-4, Krox-
20 and FGF-3. They report a complex pattern of abnormali-
ties, in which certain regions of the hindbrain express combi-
nations of genes that are never normally encountered. We have
independently analysed kreisler using some of the same
markers and also several others, including neuroanatomical
features not studied by Frohman et al. (1993), and have come
to a different and simpler view of the homozygous kreisler
phenotype. We find that the major abnormalities are co-
ordinated in a simple way and can be summed up by saying
that two rhombomeres, r5 and r6, are missing. We have looked
for cell death in the kreisler hindbrain that might explain their
2199
Development 120, 2199-2211 (1994)
Printed in Great Britain © The Company of Biologists Limited 1994
kreisler is a recessive mutation resulting in gross malfor-
mation of the inner ear of homozygous mice. The defects in
the inner ear are related to abnormalities in the hindbrain
of the embryo, adjacent to the ear rudiments. At E9.5, the
neural tube posterior to the boundary between the third
and fourth rhombomeres, r3 and r4, appears unsegmented,
and the region that would normally correspond to r4 is
unusually thick-walled and contains many dying cells. The
absence of morphological segmentation in the posterior
hindbrain corresponds to an altered pattern of gene
expression in that region, with major abnormalities
posterior to the r4/5 boundary and minor abnormalities
anterior to it. From the expression patterns at E9.5 of Krox-
20, Hoxb-1 (Hox 2.9), Hoxb-2 (Hox 2.8), Hoxa-3 (Hox 1.5),
Hoxd-4 (Hox 4.2) and cellular retinoic-acid binding protein
I (CRABP I), it appears that the fundamental defect is a
loss of r5 and r6. Correspondingly, the glossopharyngeal
ganglion and nerve, associated with r6 are missing and the
abducens nerve, which originates from r5 and r6, is also
absent. Examination of Krox-20 expression at stages as
early as E8.5 indicates that Krox-20 fails ever to be
expressed in its r5 domain in the homozygous kreisler
mutant. The abnormal amount of cell death is seen only
later. An interpretation is that the cells that would
normally become specified at an early stage as r5 and r6
adopt an r4 character instead, producing an excess of r4
cells that is disposed of subsequently by cell death.
Key words: kreisler, mouse mutant, rhombomere, cranial nerves,
Hox genes, Krox-20, CRABP I
SUMMARY
The kreisler mouse: a hindbrain segmentation mutant that lacks two
rhombomeres
Ian J. McKay
1,2
, Ian Muchamore
3
, Robb Krumlauf
3
, Malcolm Maden
4
, Andrew Lumsden
2
and Julian Lewis
1
1
Imperial Cancer Research Fund Developmental Biology Unit, Department of Zoology, Oxford University, Oxford, OX1 3PS, UK
2
Division of Anatomy and Cell Biology, United Medical and Dental School, Guy’s Hospital, London SE1 9RT, UK
3
National Institute for Medical Research, The Ridgeway, Mill Hill, London NW7 1AA, UK
4
Developmental Biology Research Centre, King’s College London, 26-29 Drury Lane, London WC2B 5RL, UK