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J Biol Chem, Vol. 274, Issue 51, 36293-36299, December 17, 1999
,
From the Department of Anatomy and Physiology, Medical Sciences
Institute/Wellcome Trust Biocenter Complex, University of Dundee,
Dundee DD1 5EH, United Kingdom
We have investigated the cellular mechanisms that
participate in reducing insulin sensitivity in response to increased
oxidant stress in skeletal muscle. Measurement of glucose transport and glycogen synthesis in L6 myotubes showed that insulin stimulated both
processes, by 2- and 5-fold, respectively. Acute (30 min) exposure
of muscle cells to hydrogen peroxide
(H2O2) blocked the hormonal activation of
both these processes. Immunoblot analyses of cell lysates prepared
after an acute oxidant challenge using phospho-specific antibodies
against c-Jun N-terminal kinase (JNK), p38, protein kinase B (PKB), and
p42 and p44 mitogen-activated protein (MAP) kinases established that
H2O2 induced a dose-dependent activation of all five protein kinases. In vitro kinase
analyses revealed that 1 mM H2O2
stimulated the activity of JNK by ~8-fold, MAPKAP-K2 (the downstream
target of p38 MAP kinase) by ~12-fold and that of PKB by up to
34-fold. PKB activation was associated with a concomitant inactivation
of glycogen synthase kinase-3. Stimulation of the p38 pathway, but not
that of JNK, was blocked by SB 202190 or SB203580, while that of
p42/p44 MAP kinases and PKB was inhibited by PD 98059 and wortmannin
respectively. However, of the kinases assayed, only p38 MAP kinase was
activated at H2O2 concentrations (50 µM) that caused an inhibition of insulin-stimulated glucose transport and glycogen synthesis. Strikingly, inhibiting the
activation of p38 MAP kinase using either SB 202190 or SB 203580 prevented the loss in insulin-stimulated glucose transport, but not
that of glycogen synthesis, by oxidative stress. Our data indicate that
activation of the p38 MAP kinase pathway plays a central role in the
oxidant-induced inhibition of insulin-regulated glucose transport, and
unveils an important biochemical link between the classical
stress-activated and insulin signaling pathways in skeletal muscle.
Recipient of a CASE studentship from the Medical Research Council
and SmithKline Beecham Pharmaceuticals.
§
To whom correspondence should be addressed. Fax: 44-1382-345507;
E-mail: h.s.hundal@dundee.ac.uk.
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