E3 ubiquitin ligase NKLAM ubiquitinates STAT1 and positively regulates STAT1-mediated transcriptional activity

Cell Signal. 2016 Dec;28(12):1833-1841. doi: 10.1016/j.cellsig.2016.08.014. Epub 2016 Aug 26.

Abstract

Signal transducer and activator of transcription 1 (STAT1) is critically important for the transcription of a large number of immunologically relevant genes. In macrophages, interferon gamma (IFNγ) signal transduction occurs via the JAK/STAT pathway and ends with the transcription of a number of genes necessary for a successful host immune response. The predominant mechanism of regulation of STAT1 is phosphorylation; however, there is a growing body of evidence that demonstrates STAT1 is also regulated by ubiquitination. In this report we show that JAK1 and STAT1 in macrophages deficient in an E3 ubiquitin ligase termed Natural Killer Lytic-Associated Molecule (NKLAM) are hyperphosphorylated following IFNγ stimulation. We found NKLAM was transiently localized to the IFNγ receptor complex during stimulation with IFNγ, where it bound to and mediated K63-linked ubiquitination of STAT1. In vitro nucleofection studies demonstrated that STAT1-mediated transcription was significantly reduced in NKLAM-KO macrophages. There was no obvious defect in STAT1 nuclear translocation; however, STAT1 from NKLAM-KO macrophages had a reduced ability to bind a functional gamma activation DNA sequence. There was also less mRNA expression of STAT1-mediated genes in NKLAM-KO macrophages treated with IFNγ. Our results demonstrate for the first time that NKLAM is a positive regulator of STAT1-mediated transcriptional activity and is an important component of the innate immune response.

Keywords: Innate immunity; Interferon gamma; Macrophage; NKLAM; STAT1; Ubiquitination.

MeSH terms

  • Animals
  • Bone Marrow Cells / cytology
  • DNA / metabolism
  • HEK293 Cells
  • Humans
  • Interferon gamma Receptor
  • Interferon-gamma / pharmacology
  • Janus Kinase 1 / metabolism
  • Lysine / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Biological
  • Phosphorylation
  • Protein Binding / drug effects
  • RAW 264.7 Cells
  • Receptors, Interferon / metabolism
  • STAT1 Transcription Factor / metabolism*
  • Transcription, Genetic* / drug effects
  • Ubiquitination* / drug effects

Substances

  • Membrane Proteins
  • NK lytic-associated molecule
  • Receptors, Interferon
  • STAT1 Transcription Factor
  • Interferon-gamma
  • DNA
  • Jak1 protein, mouse
  • Janus Kinase 1
  • Lysine