Development 110, 343-352 (1990)
Printed in Great Britain © The Company of Biologists Limited 1990
343
Localization of specific retinoid-binding sites and expression of cellular
retinoic-acid-binding protein (CRABP) in the early mouse embryo
L. DENCKER
1
*, E. ANNERWALL
1
, C. BUSCH
2
and U. ERIKSSON
3
1
Department of Toxicology, The Biomedical Centre, University of Uppsala, Box 594 S-751 24, Uppsala Sweden
2
Department of Pathology, University Hospital, University of Uppsala, S-751 85, Uppsala Sweden
3
Ludwtg Institute for Cancer Research, Stockholm Branch, Box 60202, S-104 01 Stockholm Sweden
• To whom correspondence should be addressed
Summary
Retinoids (vitamin A derivatives) are important for
normal embryogenesis and retinoic acid, an acidic
derivative of vitamin A, was recently proposed to be an
endogenous morphogen. Several retinoids are also
potent teratogens. Using an autoradiographic technique,
we have identified tissues and cells in early mouse
embryos that are able to specifically accumulate a
radiolabelled synthetic derivative of retinoic acid.
Strong accumulation of radioactivity was seen in several
neural crest derivatives and in specific areas of the CNS.
Gel filtration analyses of cytosols from embryos that
received the radiolabelled retinoid in utero suggested
that cellular retinoic acid-binding protein (CRABP) was
involved in the accumulation mechanism. Immunohisto-
chemical localization confirmed that cells accumulating
retinoids also expressed CRABP. Strong CRABP immu-
noreactivity was found in neural crest-derived mesen-
chyme of the craniofacial area, in visceral arches, in
dorsal root ganglia and in cells along the gut and the
major vessels of the trunk region. In CNS, CRABP
expression and retinoid binding was largely restricted to
the hindbrain, to a single layer of cells in the roof of the
midbrain and to cells in the mantle layer of the neural
tube. Our data suggest that cells in the embryo
expressing CRABP are target cells for exogenous
retinoids as well as endogenous retinoic acid. Retinoic
acid may thus play an essential role in normal
development of the CNS and of tissues derived from the
neural crest. We propose that the teratogenic effects of
exogenous retinoids are due to an interference with
mechanisms by which endogenous retinoic acid regulates
differentiation and pattern formation in these tissues.
Key words: retinoic acid, binding, embryo, mouse,
teratogenesis.
Introduction
Retinoic acid (RA), a biologically active form of
vitamin A, is known to support embryonic development
(Takahashi et al. 1975: Thompson et al. 1964) and to
affect differentiation and growth properties of many
cell types. (Lotan, 1980; Strickland and Mahdavi,
1978). The presence of RA in limb and its ability to
specify the anteroposterior axis during limb develop-
ment suggests that RA is an endogenous morphogen
(Thaller and Eichele, 1987). In addition, RA is a potent
teratogen, drastically affecting formation of the cranio-
facial area, brain and vascular system in exposed
humans (Rosa, 1983: Lammer et al. 1985) and
experimental animals (Durston et al. 1989; Goulding
and Pratt, 1986; Kochhar, 1967; Shenefelt, 1972; Wiley
et al. 1983; Webster et al. 1986). There is some evidence
suggesting that neural crest-derived cells and neuroepi-
thelial cells are among the primary targets for RA
during early embryonic development, since adminis-
tration of RA early in gestation or to early embryos in
vitro, predominantly induces malformations in tissues
derived from these cells (Durston et al. 1989; Goulding
and Pratt, 1986; Lammer et al. 1985: Webster et al.
1986) Furthermore, a previous study indicated that
exogenous RA accumulate in neural-crest-derived cells
and in neuroepithelium (Dencker et al. 1987).
The various biological effects caused by RA treat-
ment are likely to be mediated by specific binding
proteins. One RA-binding protein, the cellular retinoic-
acid-binding protein (CRABP) was identified almost 15
years ago. However, its role in retinoid metabolism
remains unclear (for a review see Chytil and Ong,
1984). The close structural similarities to a number of
intracellular fatty-acid-binding proteins suggest its
possible role as a transport and storage protein for RA
(Sundelin et al. 1985a,/?). It is conceivable that CRABP
may be involved in regulating the supply of RA to the
recently identified family of nuclear receptors for RA.
The three RA receptors identified in mammals (RAR,