Caspase-1 protein induces apoptosis-associated speck-like protein containing a caspase recruitment domain (ASC)-mediated necrosis independently of its catalytic activity

J Biol Chem. 2011 Sep 30;286(39):33963-72. doi: 10.1074/jbc.M111.286823. Epub 2011 Aug 8.

Abstract

The adaptor protein, apoptosis-associated speck-like protein containing a caspase recruitment domain (ASC), connects pathogen/danger sensors such as NLRP3 and NLRC4 with caspases and is involved in inflammation and cell death. We have found that ASC activation induced caspase-8-dependent apoptosis or CA-074Me (cathepsin B inhibitor)-inhibitable necrosis depending on the cell type. Unlike necroptosis, another necrotic cell death, ASC-mediated necrosis, was neither RIP3-dependent nor necrostatin-1-inhibitable. Although acetyl-YVAD-chloromethylketone (Ac-YVAD-CMK) (caspase-1 inhibitor) did not inhibit ASC-mediated necrosis, comprehensive gene expression analyses indicated that caspase-1 expression coincided with the necrosis type. Furthermore, caspase-1 knockdown converted necrosis-type cells to apoptosis-type cells, whereas exogenous expression of either wild-type or catalytically inactive caspase-1 did the opposite. Knockdown of caspase-1, but not Ac-YVAD-CMK, suppressed the monocyte necrosis induced by Staphylococcus and Pseudomonas infection. Thus, the catalytic activity of caspase-1 is dispensable for necrosis induction. Intriguingly, a short period of caspase-1 knockdown inhibited IL-1β production but not necrosis, although longer knockdown suppressed both responses. Possible explanations of this phenomenon are discussed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Amino Acid Chloromethyl Ketones / pharmacology
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Caspase 1 / genetics
  • Caspase 1 / metabolism*
  • Caspase 8 / genetics
  • Caspase 8 / metabolism
  • Caspase Inhibitors
  • Cell Line, Tumor
  • Cysteine Proteinase Inhibitors / pharmacology
  • Cytoskeletal Proteins / biosynthesis*
  • Cytoskeletal Proteins / genetics
  • Dipeptides / pharmacology
  • Gene Expression Regulation*
  • Gene Knockdown Techniques
  • Humans
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Necrosis / genetics
  • Necrosis / metabolism
  • Pseudomonas Infections / genetics
  • Pseudomonas Infections / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Staphylococcal Infections / genetics
  • Staphylococcal Infections / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Amino Acid Chloromethyl Ketones
  • CA 074 methyl ester
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins
  • Caspase Inhibitors
  • Cysteine Proteinase Inhibitors
  • Cytoskeletal Proteins
  • Dipeptides
  • IL1B protein, human
  • Interleukin-1beta
  • N-acetyl-tyrosyl-valyl-alanyl-aspartyl chloromethyl ketone
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • NLRP4 protein, human
  • PYCARD protein, human
  • Repressor Proteins
  • CASP8 protein, human
  • Caspase 8
  • Caspase 1