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Originally published In Press as doi:10.1074/jbc.M211278200 on December 19, 2002

J. Biol. Chem., Vol. 278, Issue 9, 7043-7050, February 28, 2003
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Calcium/Calmodulin-dependent Protein Kinase II Regulation of c-FLIP Expression and Phosphorylation in Modulation of Fas-mediated Signaling in Malignant Glioma Cells*

Bao Feng YangDagger §, Chang XiaoDagger §, Wilson H. Roa, Peter H. Krammer||, and Chunhai HaoDagger **

From the Dagger  Department of Laboratory Medicine and Pathology and  Oncology, University of Alberta, Edmonton, Alberta T6G 2S2, Canada and || Tumorimmunology Program, German Cancer Research Center, Im Neuenheimer Feld 280, D-69120 Heidelberg, Germany

Fas, upon cross-linking with Fas ligand (FasL) or Fas agonistic antibody, transduces apoptotic yet also proliferative signals, which have been implicated in tumor pathogenesis. In this study, we investigated the molecular mechanisms that control Fas-mediated signaling in glioma cells. Fas agonistic antibody, CH-11, induced apoptosis in sensitive glioma cells through caspase-8 recruitment to the Fas-mediated death-inducing signaling complex (DISC) where caspase-8 was cleaved to initiate apoptosis through a systematic cleavage of downstream substrates. In contrast, CH-11 stimulated cell growth in resistant glioma cells through recruitment of c-FLIP (cellular Fas-associated death domain (FADD)-like interleukin-1beta -converting enzyme (FLICE)-inhibitory protein) to the Fas-mediated DISC. Three isoforms of long form c-FLIP were detected in glioma cells, but only the phosphorylated isoform was recruited to and cleaved into a p43 intermediate form in the Fas-mediated DISC in resistant cells. Calcium/calmodulin-dependent protein kinase II (CaMK II) activity was up-regulated in resistant cells. Treatment of resistant cells with the CaMK II inhibitor KN-93 inhibited CaMK II activity, reduced c-FLIP expression, inhibited c-FLIP phosphorylation, and rescued CH-11 sensitivity. Transfection of CaMK II cDNA in sensitive cells rendered them resistant to CH-11. These results indicated that CaMK II regulates c-FLIP expression and phosphorylation, thus modulating Fas-mediated signaling in glioma cells.

* This work was supported by grants from the Canadian Institutes of Health Research and the Alberta Heritage Foundation for Medical Research (to C. H.).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 the work.

** An Alberta Heritage Foundation for Medical Research Clinical Investigator. To whom correspondence should be addressed: Dept. of Laboratory Medicine and Pathology, University of Alberta Edmonton, Alberta T6G 2S2, Canada. Tel.: 780-492-4985; Fax: 780-492-9249; E-mail: chao@ualberta.ca.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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