INTRODUCTION
It is still a major challenge to understand how vast numbers of
different neuronal types are generated and assigned their fates in
the vertebrate nervous system. Among the transcriptional regula-
tors implicated in vertebrate neural development, homeodomain
proteins expressed in differentiating neurons are good candidates
to control final neuronal phenotypes. Targeted gene inactivation
experiments have demonstrated that homeodomain proteins are
required for the generation of various classes of neurons (Erkman
et al., 1996; Gan et al., 1996; Xiang et al., 1996; McEvilly et al.,
1996; Pfaff et al., 1996; Morin et al., 1997). An emerging concept
from these and other studies is that structurally similar homeo-
domain proteins could insure the determination of subsets of
related neuronal phenotypes, suggesting that duplication of tran-
scription factor genes is causally linked to the appearance of new
subclasses of neurons during evolution. For example, the three
known POU-domain proteins of the Brn-3 family are expressed
in overlapping but distinct patterns (Xiang et al., 1995, 1996;
Turner et al., 1994). Each is uniquely expressed in some classes
of neurons and is necessary for their generation as shown by the
knock-out phenotypes (Erkman et al., 1996; Gan et al., 1996;
McEvilly et al., 1996; Xiang et al., 1996). They are co-expressed
in other neurons, most of which are apparently spared in the
knock-out mice. In these cells, they could be functionally
redundant with each other or, alternatively, co-operate to diversify
phenotypes on a combinatorial mode. The latter model has been
proposed for the closely homologous LIM-homeodomain
proteins expressed in motoneurons and commissural neurons of
the spinal cord (Tsuchida et al., 1994; Tanabe and Jessell, 1996).
Phox2a is a homeodomain protein specific to the nervous
system (Valarché et al., 1993; Tiveron et al., 1996). Its expression
pattern reveals two striking correlates. The first is with a neuro-
transmitter phenotype: Phox2a is expressed in all neurons that
transiently or permanently express dopamine-β-hydroxylase
(DBH), the last enzyme in the pathway of noradrenaline
synthesis, suggesting that Phox2a is a determinant of the nora-
drenergic phenotype. The second correlate is with neuronal
circuitry: Phox2a expression is largely restricted to circuits
involved in medullary control of autonomic functions (Tiveron et
al., 1996). Inactivation of the Phox2a gene leads to agenesis of
the locus coeruleus and of parasympathetic ganglia, to altered
morphology of the superior cervical ganglion and to massive
atrophy of cranial sensory ganglia (Morin et al., 1997). In the
cranial ganglia, it was possible to show the dependence of DBH
expression on Phox2a, providing the first in vivo evidence that
Phox2a may indeed regulate the noradrenergic phenotype (Morin
et al., 1997). The gene coding for the GDNF (glial cell line-
derived neurotrophic factor) receptor subunit Ret is also
regulated, directly or indirectly, by Phox2a in these ganglia, sug-
4065 Development 124, 4065-4075 (1997)
Printed in Great Britain © The Company of Biologists Limited 1997
DEV1198
Recent evidence suggests that specific families of homeo-
domain transcription factors control the generation and
survival of distinct neuronal types. We had previously char-
acterized the homeobox gene Phox2a, which is expressed in
differentiating neurons of the central and peripheral
autonomic nervous system as well as in motor nuclei of the
hindbrain. Targeted deletion of the Phox2a gene affects
part of the structures in which it is expressed: the locus
coeruleus, visceral sensory and parasympathetic ganglia
and, as we show here, the nuclei of the IIIrd and IVth
cranial nerves. We now report on the characterization of
Phox2b, a close relative of Phox2a, with an identical homeo-
domain. Phox2a and Phox2b are co-expressed at most sites,
therefore suggesting a broader role for Phox2 genes in the
specification of the autonomic nervous system and cranial
motor nuclei than revealed by the Phox2a knock-out mice.
A detailed analysis of the relative timing of Phox2a and
Phox2b expression at various sites suggests positive cross-
regulations, which are substantiated by the loss of Phox2b
expression in cranial ganglia of Phox2a-deficient mice. In
the major part of the rhombencephalon, Phox2b expression
precedes that of Phox2a and starts in the proliferative neu-
roepithelium, in a pattern strikingly restricted on the
dorsoventral axis and at rhombomeric borders. This
suggests that Phox2b links early patterning events to the
differentiation of defined neuronal populations in the
hindbrain.
Key words: Phox2a, Phox2b, neurogenesis, homeodomain, mouse,
nervous system
SUMMARY
Expression and interactions of the two closely related homeobox genes
Phox2a and Phox2b during neurogenesis
Alexandre Pattyn, Xavier Morin, Harold Cremer, Christo Goridis and Jean-François Brunet*
Laboratoire de Génétique et Physiologie du Développement, Institut de Biologie du Développement de Marseille,
CNRS/INSERM/Université de la Méditerranée, Campus de Luminy, Case 907, F-13288 Marseille Cedex 9, France
*Address for correspondence: (e-mail: brunet@ibdm.univ-mrs.fr)