Distinct cell death pathways triggered by the adenovirus early region 4 ORF 4 protein

J Cell Biol. 2002 Aug 5;158(3):519-28. doi: 10.1083/jcb.200201106. Epub 2002 Aug 5.

Abstract

In transformed cells, induction of apoptosis by adenovirus type 2 (Ad2) early region 4 ORF 4 (E4orf4) correlates with accumulation of E4orf4 in the cell membrane-cytoskeleton fraction. However, E4orf4 is largely expressed in nuclear regions before the onset of apoptosis. To determine the relative contribution of nuclear E4orf4 versus membrane-associated E4orf4 to cell death signaling, we engineered green fluorescent fusion proteins to target E4orf4 to specific cell compartments. The targeting of Ad2 E4orf4 to cell membranes through a CAAX-box or a myristylation consensus signal sufficed to mimic the fast Src-dependent apoptotic program induced by wild-type E4orf4. In marked contrast, the nuclear targeting of E4orf4 abolished the early induction of extranuclear apoptosis. However, nuclear E4orf4 still induced a delayed cell death response independent of Src-like activity and of E4orf4 tyrosine phosphorylation. The zVAD.fmk-inhibitable caspases were dispensable for execution of both cell death programs. Nevertheless, both pathways led to caspase activation in some cell types through the mitochondrial pathway. Finally, our data support a critical role for calpains upstream in the death effector pathway triggered by the Src-mediated cytoplasmic death signal. We conclude that Ad2 E4orf4 induces two distinct cell death responses, whose relative contributions to cell killing may be determined by the genetic background.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoviridae / metabolism*
  • Adenoviridae Infections / metabolism*
  • Adenoviridae Infections / physiopathology
  • Apoptosis / drug effects
  • Apoptosis / physiology*
  • Calcium-Binding Proteins / metabolism
  • Calpain / genetics
  • Calpain / metabolism
  • Caspase Inhibitors
  • Caspases / genetics
  • Caspases / metabolism
  • Cell Line, Transformed
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Membrane / ultrastructure
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism
  • Cytoplasm / ultrastructure
  • DNA Fragmentation / drug effects
  • DNA Fragmentation / physiology
  • Enzyme Inhibitors / pharmacology
  • Eukaryotic Cells / cytology
  • Eukaryotic Cells / drug effects
  • Eukaryotic Cells / metabolism*
  • Green Fluorescent Proteins
  • Humans
  • Indicators and Reagents
  • Luminescent Proteins
  • Models, Biological
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*
  • Viral Proteins / genetics
  • Viral Proteins / metabolism*
  • bcl-2-Associated X Protein
  • src-Family Kinases / drug effects
  • src-Family Kinases / metabolism

Substances

  • Calcium-Binding Proteins
  • Caspase Inhibitors
  • E4orf4 protein, adenovirus
  • Enzyme Inhibitors
  • Indicators and Reagents
  • Luminescent Proteins
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Viral Proteins
  • bcl-2-Associated X Protein
  • Green Fluorescent Proteins
  • calpastatin
  • src-Family Kinases
  • Calpain
  • Caspases