INTRODUCTION
Cell sites of signal transduction, after the binding of a hormone
to its receptor, have been believed to occur mainly at the
plasma membrane. However, the internalisation of ligand-
receptor complexes into the endosomal apparatus may be
consistent with intracellular signalling (Baas et al., 1995;
Bevan et al., 1996). As prolactin (PRL) is internalised in
lactating mammary epithelial cells (MEC) and transcytosed to
the lumen (Ollivier-Bousquet, 1998), these cells provide a
model to study whether, during its transport through the cell,
PRL initiates distinct signalling cascades that lead to different
biological responses. PRL exerts many biological actions
through the prolactin receptors (PRLR), such as the control of
casein gene expression (Hennighausen et al., 1997) and the in
vitro stimulation of protein secretion, which is referred to as the
secretagogue effect (Ollivier-Bousquet, 1978). Transduction of
the PRL message within the cell from the cell membrane to the
nucleus, which causes activation of the transcription of milk
protein genes, includes oligomerisation of the receptor and
activation of the self-phosphorylating Janus kinase 2 (Jak2),
which in turn phosphorylates tyrosine residues on the receptor
and the signal transducers and activators of transcription
(STATs), Stat5a and Stat5b. These factors dimerise, translocate
to the nucleus and then bind to specific promoter elements on
PRL-responsive genes (Hennighausen et al., 1997; Goffin and
Kelly, 1997). However, molecular events that lead to the
transduction of the secretagogue effect of PRL remain partly
unknown. They include a very rapid and transient release of
arachidonic acid within a few minutes of the addition of PRL,
and the metabolism of this polyunsaturated fatty acid (PUFA)
(Blachier et al., 1988). Moreover, arachidonic acid, when
added to the incubation medium of lactating MEC, stimulates
casein secretion, probably after being metabolised in products
of the lipoxygenase pathway (Ollivier-Bousquet, 1982;
Ollivier-Bousquet, 1984). Together these results strongly
suggest that prolactin stimulates casein secretion by the release
of arachidonic acid.
In contrast to hormones that are endocytosed and then
rapidly degraded in lysosomes (Burgess et al., 1992), PRL is
carried through the MEC by transcytosis and then released in
the milk in either intact or cleaved molecular forms (Sinha,
1995). PRL is transported via a vesicular pathway that includes
not only endosomes, late endosomes and multivesicular bodies,
but also vesicles located in the Golgi region and secretory
vesicles containing casein micelles (Ollivier-Bousquet, 1998).
The transcytosis of PRL can be slowed down or inhibited in
tissues incubated at low temperatures (25°C) for 1 hour
(Seddiki et al., 1991), or in mammary tissues from rats that
receive a PUFA-deficient diet (Ollivier-Bousquet et al., 1993;
Ollivier-Bousquet et al., 1997). Under these two conditions, in
which PRL accumulates in late endosomes and multivesicular
bodies, basal secretion is not affected but the secretagogue
effect of the hormone is inhibited (Seddiki et al., 1991;
Ollivier-Bousquet et al., 1993; Ollivier-Bousquet et al., 1997).
One question that arises is whether the journey of PRL or the
1883
Prolactin added to the incubation medium of lactating
mammary epithelial cells is transported from the basal to
the apical region of cells through the Golgi region and
concomitantly stimulates arachidonic acid release and
protein milk secretion. We report that when PRL is added
after disorganisation of the Golgi apparatus by brefeldin A
treatment, prolactin signalling to expression of genes for
milk proteins and prolactin endocytosis are not affected.
However, prolactin transport to the apical region of cells
(transcytosis), as well as prolactin-induced arachidonic
acid release and subsequent stimulation of the secretion of
caseins, which are located in a post-Golgi compartment, are
inhibited. This inhibition was not a consequence of damage
to the secretory machinery, as under the same conditions,
protein secretion could be stimulated by the addition of
arachidonic acid to the incubation medium. Thus, it is
possible to discriminate between prolactin-induced actions
that are dependent (signalling to milk protein secretion) or
independent (signalling to milk gene expression) on the
integrity of the Golgi apparatus. These results suggest that
these two biological actions may be transduced via distinct
intracellular pathways, and support the hypothesis that
prolactin signals may be emitted at various cellular sites.
Key words: Prolactin, Lactating mammary epithelial cells, Brefeldin
A, Golgi apparatus, Secretion, Prolactin receptor, Signal transduction
SUMMARY
Prolactin signalling to milk protein secretion but not
to gene expression depends on the integrity of the
Golgi region
Mustapha Lkhider
1
, Barbara Pétridou
2
, Alain Aubourg
2
and Michèle Ollivier-Bousquet
2,
*
1
Faculté des Sciences, UCD, El Jadida, Maroc
2
Unité de Biologie Cellulaire et Moléculaire, INRA, 78352 Jouy-en-Josas Cedex, France
*Author for correspondence (e-mail: ollivier@biotec.jouy.inra.fr)
Accepted 1 March 2001
Journal of Cell Science 114, 1883-1891 © The Company of Biologists Ltd
RESEARCH ARTICLE