Toll-like receptor-mediated down-regulation of the deubiquitinase cylindromatosis (CYLD) protects macrophages from necroptosis in wild-derived mice

J Biol Chem. 2014 May 16;289(20):14422-33. doi: 10.1074/jbc.M114.547547. Epub 2014 Apr 4.

Abstract

Pathogen recognition by the innate immune system initiates the production of proinflammatory cytokines but can also lead to programmed host cell death. Necroptosis, a caspase-independent cell death pathway, can contribute to the host defense against pathogens or cause damage to host tissues. Receptor-interacting protein (RIP1) is a serine/threonine kinase that integrates inflammatory and necroptotic responses. To investigate the mechanisms of RIP1-mediated activation of immune cells, we established a genetic screen on the basis of RIP1-mediated necroptosis in wild-derived MOLF/EiJ mice, which diverged from classical laboratory mice over a million years ago. When compared with C57BL/6, MOLF/EiJ macrophages were resistant to RIP1-mediated necroptosis induced by Toll-like receptors. Using a forward genetic approach in a backcross panel of mice, we identified cylindromatosis (CYLD), a deubiquitinase known to act directly on RIP1 and promote necroptosis in TNF receptor signaling, as the gene conferring the trait. We demonstrate that CYLD is required for Toll-like receptor-induced necroptosis and describe a novel mechanism by which CYLD is down-regulated at the transcriptional level in MOLF/EiJ macrophages to confer protection from necroptosis.

Keywords: Deubiquitination; Forward Genetic Mapping; Gene Regulation; Mouse Genetics; Necrosis (Necrotic Death); Toll-like Receptor (TLR); Wild-derived Mice.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Cells / cytology
  • Cysteine Endopeptidases / genetics*
  • Deubiquitinating Enzyme CYLD
  • Down-Regulation*
  • HEK293 Cells
  • Humans
  • Macrophages, Peritoneal / cytology*
  • Macrophages, Peritoneal / metabolism*
  • Mice
  • Necrosis*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Toll-Like Receptors / metabolism*

Substances

  • RNA, Messenger
  • Toll-Like Receptors
  • CYLD protein, mouse
  • Deubiquitinating Enzyme CYLD
  • Cysteine Endopeptidases