CELL REGULATION, VOI. 1, 425-434, April 1990
Regulation of IL-4 lymphokine gene expression and
cellular proliferation in murine T helper type 11 cells
Eduardo Mufloz, Ana M. Zubiaga, Juan Mufloz
and Brigitte T. Huber
Department of Pathology
Tufts University School of Medicine
Boston, Massachusetts 02111
Activation of T cells results in the production of
lymphokines and cellular proliferation. Protein ki-
nase C (PKC) plays a key role in this process. It has
been shown that this enzyme is essential to elicit
a response to Con A or specific antigen in CD4+ T
helper type 1 (Th 1) cells that secrete IL-2. We have
now explored the signal transduction pathway that
leads to transcription of the IL-4 gene and prolif-
eration in murine CD4+ T helper type 2 (Th 2) cells.
Surprisingly, we have found in two independently
derived Th 2 clones that neither cellular prolifera-
tion nor IL-4 lymphokine production is affected by
blocking or depletion of PKC. This differential
mechanism of signal transmission leading to cel-
lular activation implies a new distinction between
murine Th 1 and Th 2 cells.
Introduction
The activation of T cells by specific antigen,
mitogen, or monoclonal antibodies directed
against certain cell surface proteins induces the
hydrolysis of phosphatidylinositol 4'5', biphos-
phate (PIP2), mediated by phospholipase C (Wil-
son etal., 1984; Bennett and Crooke, 1987). This
hydrolysis leads to the production of second
messengers such as diacylglycerol (DAG) and
inositol triphosphate (InsP3) (Berridge, 1987).
InsP3 increases the concentration of intracel-
lular calcium
([Ca2+],)
(Carafoli, 1987), whereas
DAG is an essential cofactor for the activation
of the enzyme protein kinase C (PKC) (Kikkawa
and Nishizuka, 1986). It has been postulated
that the combination of both effects leads to
production of lymphokines, expression of lym-
phokine receptors, and cellular proliferation
(Mills et al., 1985; Isakov et al., 1987).
In the murine system two types of CD4+ T
helper (Th) cells have been defined, namely Th
1 and Th 2 cells, that differ in their lymphokine
production and immune function (reviewed by
Mosmann and Coffman, 1987). Whereas Th 1
cells produce IL-2, y-IFN, and lymphotoxin on
activation, Th 2 cells secrete IL-4 and IL-5
(Cherwinsky et al., 1987). Recently, it has been
reported that in Th 1 cells PKC is essential for
IL-2 production and proliferation in response to
T cell receptor (Tcr)-mediated activation but not
for proliferation in response to exogenous IL-2
(Mills et al., 1988; Valge et aL, 1988).
The mechanism of signal transduction in Th
2 cells after Tcr-mediated stimulation has not
been elucidated yet. Using two different sys-
tems to block the function of PKC, we have
found that this enzyme plays a different regu-
latory role in Th 2 than in Th 1 cells; namely,
neither IL-4 lymphokine production nor cellular
proliferation is dependent on the presence of
PKC in Th 2 cells. These results support the
idea that the differentiation of CD4+ T cells into
Th 1 or Th 2 cells is an event that occurs at the
level of second messengers generated by the
activation of differential signaling pathways.
Results
Calcium ionophores induce IL-4 mRNA
in D10 cells
We were interested in determining what signals
lead to IL-4 mRNA expression in the prototype
Th 2 cell, D1O.G4.1 (D10). There is general
agreement that activation of T cells through the
Tcr leads to an increase in [Ca2+i as well as
activation of PKC. This physiological activation
signal can be mimicked by the use of ionophores
in conjunction with phorbol esters (Truneh et
al., 1985). We cultured resting Dl 0 cells for 6 h
with these agents and measured IL-4 mRNA
expression in a Northern blot. As shown in Fig-
ure 1, ionomycin alone (but not PMA alone) is
able to induce IL-4 message. Synergy is seen
with the combination of the two agents, result-
ing in IL-4 mRNA levels similar to those induced
by Con A stimulation. Another Ca2l ionophore,
A23187, also induced IL-4 steady-state mes-
sage in D10 cells in a dose-dependent manner,
supporting the idea that the IL-4 gene is posi-
tively regulated by a Ca2"-dependent pathway.
© 1990 by The American Society for Cell Biology 425