c-Jun-dependent CD95-L expression is a rate-limiting step in the induction of apoptosis by alkylating agents

Mol Cell Biol. 2000 Jan;20(2):575-82. doi: 10.1128/MCB.20.2.575-582.2000.

Abstract

Mouse 3T3 fibroblasts derived from fetuses lacking c-Jun were used to define an essential role of c-Jun, a main component of the transcription factor AP-1, in the cellular response to the alkylating agent methyl methanesulfonate (MMS). MMS represents the most potent and selective activator of the stress-induced kinases JNK/SAPK and p38, resulting in very efficient induction of c-Jun hyperphosphorylation and c-jun transcription. This agent induced apoptosis with high efficiency in wild-type cells but not in c-jun(-/-) cells. Resistance to apoptosis was accompanied by impaired expression of CD95 ligand (CD95-L), a well-known inducer of apoptosis. The addition of recombinant CD95-L restored apoptosis sensitivity in c-jun(-/-) fibroblasts. MMS-induced apoptosis in wild-type fibroblasts or human lymphocytes was strongly reduced by neutralizing CD95-L antibodies or transdominant negative FADD, confirming the importance of CD95 signalling in MMS-induced apoptosis. The loss-of-function approach in fibroblasts allowed the identification and dissection of c-Jun-dependent and -independent processes upstream or downstream of CD95 activation. We have found that c-Jun can act as a proapoptotic regulator in cells exposed to DNA damage via induction of CD95-L. Once activated, CD95-induced death signalling is not affected by the loss of c-Jun, demonstrating that only the initiation and not the execution of stress-induced apoptosis depends on c-Jun.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 2
  • Adaptor Proteins, Signal Transducing*
  • Alkylating Agents / pharmacology*
  • Animals
  • Antibodies / pharmacology
  • Apoptosis / drug effects*
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology
  • Cell Line
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Fas Ligand Protein
  • Fas-Associated Death Domain Protein
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Gene Deletion
  • Gene Expression / drug effects
  • Humans
  • Kinetics
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Membrane Glycoproteins / pharmacology
  • Methyl Methanesulfonate / pharmacology
  • Mice
  • Proto-Oncogene Proteins c-jun / deficiency
  • Proto-Oncogene Proteins c-jun / genetics
  • Proto-Oncogene Proteins c-jun / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Recombinant Proteins / metabolism
  • Recombinant Proteins / pharmacology
  • Signal Transduction / drug effects
  • Transcription Factor AP-1 / physiology
  • Transcription Factors / metabolism
  • Transcriptional Activation / drug effects*

Substances

  • Activating Transcription Factor 2
  • Adaptor Proteins, Signal Transducing
  • Alkylating Agents
  • Antibodies
  • Carrier Proteins
  • Cyclic AMP Response Element-Binding Protein
  • FADD protein, human
  • FASLG protein, human
  • Fadd protein, mouse
  • Fas Ligand Protein
  • Fas-Associated Death Domain Protein
  • Fasl protein, mouse
  • Membrane Glycoproteins
  • Proto-Oncogene Proteins c-jun
  • RNA, Messenger
  • Recombinant Proteins
  • Transcription Factor AP-1
  • Transcription Factors
  • Methyl Methanesulfonate