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J Biol Chem, Vol. 275, Issue 19, 14760-14766, May 12, 2000

Differential Effects of Sphingomyelin Hydrolysis and Resynthesis on the Activation of NF-kappa B in Normal and SV40-transformed Human Fibroblasts*

Chiara LubertoDagger §, David S. Yoo§, Hana S. SuidanDagger , Gianna M. Bartoli||, and Yusuf A. HannunDagger **

From the Departments of Dagger  Biochemistry and Molecular Biology, Medical University of South Carolina, Charleston, South Carolina 29425,  Medicine, Division of Gastroenterology, Duke University Medical Center, Durham, North Carolina 27710, || Institute of General Pathology, Catholic University, 00168 Rome, Italy, and the Department of Biology, Tor Vergata University, 00133 Rome, Italy

The precise role of ceramide in NF-kappa B signaling remains unclear. The recent observation of differential sphingomyelin synthase (SMS) activity in normal (low SMS) versus SV40-transformed (high SMS) WI38 human lung fibroblasts provides an opportunity to assess the involvement of ceramide and SMS in NF-kappa B activation. Treatment of normal WI38 fibroblasts with bacterial sphingomyelinase resulted in a 4-fold elevation of ceramide and blocked NF-kappa B activation by serum stimulation. Such inhibition was not observed in SV40-transformed fibroblasts. Under regular growth conditions, after sphingomyelinase was washed out, normal WI38 did not show SM re-synthesis nor NF-kappa B activation. In SV40-WI38, on the other hand, sphingomyelinase washout induced resynthesis of SM due to the action of SMS on ceramide generated at the plasma membrane. NF-kappa B activation correlated with SM resynthesis. This activation was abrogated by D609, which inhibited SM resynthesis but not the initial formation of ceramide. The differential activity of SMS may explain the effects of ceramide in NF-kappa B signaling: in the absence of significant SMS activity, ceramide inhibits NF-kappa B, whereas with high SMS, the conversion of the ceramide signal to a diacylglycerol signal by the action of SMS stimulates NF-kappa B. These results also suggest a role for SMS in regulating NF-kappa B.

* This work was supported in part by National Institutes of Health Grants GM 43825 and HL-43707.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ These authors contributed equally.

** To whom correspondence should be addressed: Biochemistry and Molecular Biology, MUSC, P. O. Box 250780, 114 Doughty St., Charleston, SC 29425. Tel.: 843-792-4321; Fax: 843-953-0843; E-mail: hannun@musc.edu.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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