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J. Biol. Chem., Vol. 279, Issue 35, 36778-36787, August 27, 2004

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Cell Surface Ceramide Generation Precedes and Controls FcRII Clustering and Phosphorylation in Rafts^*

Abo Bakr Abdel Shakor, Katarzyna Kwiatkowska, and Andrzej Sobota

From the Nencki Institute of Experimental Biology, the Department of Cell Biology, 3 Pasteur St., 02-093 Warsaw, Poland

Despite the role of sphingolipid/cholesterol rafts as signaling platforms for Fc receptor II (FcRII), the mechanism governing translocation of an activated receptor toward the rafts is unknown. We show that at the onset of FcRII cross-linking acid sphingomyelinase is rapidly activated. This enzyme is extruded from intracellular compartments to the cell surface, and concomitantly, exofacially oriented ceramide is produced. Both non-raft and, to a lesser extent, raft sphingomyelin pools were hydrolyzed at the onset of FcRII cross-linking. The time course of ceramide production preceded the recruitment of FcRII to rafts and the receptor phosphorylation. Exogenous C₁₆-ceramide facilitated clustering of FcRII and its association with rafts. In contrast, inhibition of acid sphingomyelinase diminished both the ceramide generation and clustering of cross-linked FcRII. Under these conditions, tyrosine phosphorylation of FcRII and receptor-accompanying proteins was also reduced. All the inhibitory effects were bypassed by treatment of cells with exogenous ceramide. These data provide evidence that the generation of cell surface ceramide is a prerequisite for fusion of cross-linked FcRII and rafts, which triggers the receptor tyrosine phosphorylation and signaling.

Received for publication, February 26, 2004 , and in revised form, June 9, 2004.

^* This work was supported by the State Committee for Scientific Research, Poland, Grant KBN 3 P04C 036 23. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed. E-mail: a.sobota{at}nencki.gov.pl.

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