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J Biol Chem, Vol. 274, Issue 36, 25273-25280, September 3, 1999
From the Institute for Biomedical Aging Research, Austrian Academy
of Sciences, A-6020 Innsbruck, Austria
Recently, we demonstrated that mechanical stress
results in rapid phosphorylation or activation of platelet-derived
growth factor receptors in vascular smooth muscle cells (VSMCs)
followed by activation of mitogen-activated protein kinases (MAPKs) and AP-1 transcription factors (Hu, Y., Bock, G., Wick, G., and Xu, Q. (1998) FASEB J. 12, 1135-1142). Herein, we provide
evidence that VSMC responses to mechanical stress also include
induction of MAPK phosphatase-1 (MKP-1), which may serve as a negative
regulator of MAPK signaling pathways. When rat VSMCs cultivated on a
flexible membrane were subjected to cyclic strain stress (60 cycles/min, 5-30% elongation), induction of MKP-1 proteins and
mRNA was observed in time- and strength-dependent
manners. Concomitantly, mechanical forces evoked rapid and transient
activation of all three members of MAPKs, i.e.
extracellular signal-regulated kinases (ERKs), c-Jun
NH2-terminal protein kinases (JNKs), or stress-activated protein kinases (SAPKs), and p38 MAPKs. Suramin, a growth factor receptor antagonist, completely abolished ERK activation, significantly blocked MKP-1 expression, but not JNK/SAPK and p38 MAPK activation, in
response to mechanical stress. Interestingly, VSMC lines stably expressing dominant negative Ras (Ras N17) or Rac (Rac N17) exhibited a
marked decrease in MKP-1 expression; the inhibition of ERK kinases (MEK1/2) by PD 98059 or of p38 MAPKs by SB 202190 resulted in a
down-regulation of MKP-1 induction. Furthermore, overexpressing MKP-1
in VSMCs led to the dephosphorylation and inactivation of ERKs,
JNKs/SAPKs, and p38 MAPKs and inhibition of DNA synthesis. Taken
together, our findings demonstrate that mechanical stress induces MKP-1
expression regulated by two signal pathways, including growth factor
receptor-Ras-ERK and Rac-JNK/SAPK or p38 MAPK, and that MKP-1 inhibits
VSMC proliferation via MAPK inactivation. These results suggest that
MKP-1 plays a crucial role in mechanical stress-stimulated signaling
leading to VSMC growth and differentiation.
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