160 Biochimica et Biophysica Acta, 1177 (1993) 160-166
© 1993 Elsevier Science Publishers B.V. All rights reserved 0167-4889/93/$06.00
BBAMCR 13392
Epidermal growth factor stimulates phosphorylation of eukaryotic
initiation factor 4B, independently of protein kinase C
Rob M.F. Wolthuis, Alfons F.M. Cremers, Marcell6 A.M. Kasperaitis,
Cor van der Mast, Harry O. Voorma and Johannes Boonstra
Department of Molecular Cell Biology, University of Utrecht, Utrecht (The Netherlands)
(Received 24 November 1992)
Key words: Epidermal growth factor; Protein kinase C; Phosphorylation; Eukaryotic initiation factor; Epidermoid carcinoma;
(A431 cell); (Human)
We demonstrate that exposure of human epidermoid carcinoma A431 cells to epidermal growth factor (EGF) results in
phosphorylation of elF-4B within minutes after addition of EGF. The EGF-induced phosphorylation of elF-4B is not caused by
the EGF receptor tyrosine kinase itself, since no tyrosine-phosphorylated elF-4B could be detected upon immunoprecipitation
using an anti-phosphotyrosine antibody. Enhanced phosphorylation of elF-4B was also detected upon exposure of the cells to
phorbol 12-myristate 13-acetate (PMA), an activator of protein kinase C (PKC), suggesting that elF-4B may be a substrate of
PKC. However, down-regulation of PKC did not influence the EGF-induced elF-4B phosphorylation, which indicates that
elF-4B is phosphorylated by an as yet unknown kinase, activated early in the EGF-induced signal transduction cascade.
Introduction
Polypeptide growth factors play an important role in
the regulation of cell proliferation [1]. EGF, one of the
best-characterized growth factors, exerts its effects in
the target cells by binding to and activation of the
EGF-receptor. Following tyrosine kinase activation, the
receptor phosphorylates a number of proteins, includ-
ing the receptor itself, which results in the activation of
the signal transduction pathway. Ultimately these
events lead to enhanced DNA synthesis and cell divi-
sion in most cells [2-5].
Cell division requires DNA synthesis, enhanced rates
of RNA- and protein synthesis, and therefore it is
attractive to suggest that these cellular processes are
under direct control of the receptor kinase in order to
realize the specific adaptation of the cell. With respect
to protein synthesis, the targets of the growth factor
induced signal transduction cascade are most likely the
eukaryotic initiation factors (elFs), since regulation of
protein synthesis is realized at the level of these fac-
Correspondence to: J. Boonstra, Department of Molecular Cell
Biology, Padualaan 8, 3584 CH Utrecht, The Netherlands.
Abbreviations: EGF, epidermal growth factor; elF, eukaryotic initia-
tion factor; PMA, phorbol 12-myristate 13-acetate; PKC, protein
kinase C; NBT, nitroblue tetrazolium salt; BCIP, 5-bromo-4-chloro-
3-indolyl phosphate; DMEM, Dulbecco's modified Eagle's medium;
PBS, phosphate-buffered saline; BSA, bovine serum albumin; DTT,
dithiothreitol.
tors. The initiation factors are involved in modulating
rate limiting steps such as the recognition of the 5' cap
structure, unwinding of the 5' untranslated region of
mRNA and in promoting binding of the 40S ribosomal
subunit to the mRNA [6]. Of particular interest are the
observations that the eukaryotic initiation factors 3, 4B
and 4F as well as the ribosomal protein $6 may be
phosphorylated in vivo [7-11] and in vitro [12,13]. Fur-
thermore it has been shown that processes leading to a
stimulation of overall translational initiation rates cor-
relate with enhanced phosphorylation of elF-3, elF-4B,
elF-4F and $6, suggesting that the phosphorylation of
these translation factors is involved in the regulation of
protein synthesis [13,14]. In view of the above men-
tioned possible regulation of protein synthesis by
growth factor-induced signal tl'ansduction, it is of inter-
est that one of the initiation factors, elF-4B, is phos-
phorylated upon treatment of cells with the phorbol
ester PMA, an activator of protein kinase C [10,15], or
insulin [15,16]. Furthermore stimulation of protein syn-
thesis during recovery of heat-shocked cells or by addi-
tion of serum to serum-starved cells, is accompanied by
increased phosphorylation of elF-4B [7-10]. elF-4B is
an 80-kDa phosphoprotein containing at least 8 serine
residues that may be modified by phosphorylation
[14,15]. The protein can be phosphorylated in vitro by
at least five different protein kinases [12]. Sequence
analysis revealed a consensus RNA recognition motive
unique for initiation factors, but which is found in
several different RNA binding proteins [17]. elF-4B