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J Biol Chem, Vol. 274, Issue 31, 21533-21538, July 30, 1999
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From the Oxidized LDL (oxLDL) have been
implicated in diverse biological events leading to the development of
atherosclerotic lesions. We previously demonstrated that the
proliferation of cultured vascular smooth muscle cells (SMC) induced by
oxLDL is preceded by an increase in neutral sphingomyelinase activity,
sphingomyelin turnover to ceramide, and stimulation of
mitogen-activated protein kinases (Augé, N., Escargueil-Blanc,
I., Lajoie-Mazenc, I., Suc, I., Andrieu-Abadie, N., Pieraggi, M. T., Chatelut, M., Thiers, J. C., Jaffrézou, J. P.,
Laurent, G., Levade, T., Nègre-Salvayre, A., and Salvayre, R. (1998) J. Biol. Chem. 273, 12893-12900). Since
ceramide can be converted to other bioactive metabolites, such as the
well established mitogen sphingosine 1-phosphate (S1P), we investigated
whether additional ceramide metabolites are involved in the
oxLDL-induced SMC proliferation. We report here that incubation of SMC
with oxLDL increased the activities of both acidic and alkaline
ceramidases as well as sphingosine kinase, and elevated cellular
sphingosine and S1P. Furthermore, the mitogenic effect of oxLDL was
inhibited by
D-erythro-2-(N-myristoylamino)-1-phenyl-1-propanol and N,N-dimethylsphingosine which are inhibitors of
ceramidase and sphingosine kinase, respectively. These findings suggest
that S1P is a key mediator of the mitogenic effect of oxLDL. In
agreement with this conclusion, exogenous addition of sphingosine
stimulated the proliferation of cultured SMC, and this effect was
abrogated by dimethylsphingosine but not by fumonisin B1, an inhibitor
of the acylation of sphingosine to ceramide. Exogenous S1P also
promoted SMC proliferation. Altogether, these results strongly suggest that the mitogenic effect of oxLDL in SMC involves the combined activation of sphingomyelinase(s), ceramidase(s), and sphingosine kinase, resulting in the turnover of sphingomyelin to a number of
sphingolipid metabolites, of which at least S1P is critical for mitogenesis.
Laboratoire de Biochimie, INSERM
U. 466, Université Paul Sabatier, CHU Rangueil, 31403 Toulouse,
France and the Departments of § Gynecology and Obstetrics
and Biochemistry, Emory University,
Atlanta, Georgia 30322-3050
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