OTUD7B deubiquitinates SQSTM1/p62 and promotes IRF3 degradation to regulate antiviral immunity

Autophagy. 2022 Oct;18(10):2288-2302. doi: 10.1080/15548627.2022.2026098. Epub 2022 Jan 31.

Abstract

Deubiquitination plays an important role in the regulation of the crosstalk between macroautophagy/autophagy and innate immune signaling, yet its regulatory mechanisms are not fully understood. Here we identify the deubiquitinase OTUD7B as a negative regulator of antiviral immunity by targeting IRF3 (interferon regulatory factor 3) for selective autophagic degradation. Mechanistically, OTUD7B interacts with IRF3, and activates IRF3-associated cargo receptor SQSTM1/p62 (sequestosome 1) by removing its K63-linked poly-ubiquitin chains at lysine 7 (K7) to enhance SQSTM1 oligomerization. Moreover, viral infection increased the expression of OTUD7B, which forms a negative feedback loop by promoting IRF3 degradation to balance type I interferon (IFN) signaling. Taken together, our study reveals a specific role of OTUD7B in mediating the activation of cargo receptors in a substrate-dependent manner, which could be a potential target against excessive immune responses.Abbreviations: Baf A1: bafilomycin A1; CGAS: cyclic GMP-AMP synthase; DDX58/RIG-I: DExD/H-box helicase 58; DSS: dextran sodium sulfate; DUBs: deubiquitinating enzymes; GFP: green fluorescent protein; IFN: interferon; IKKi: IKBKB/IkappaB kinase inhibitor; IRF3: interferon regulatory factor 3; ISGs: interferon-stimulated genes; MAVS: mitochondrial antiviral signaling protein; MOI: multiplicity of infection; PAMPs: pathogen-associated molecular patterns; SeV: Sendai virus; siRNA: small interfering RNA; SQSTM1/p62: sequestosome 1; STING1: stimulator of interferon response cGAMP interactor 1; TBK1: TANK binding kinase 1; Ub: ubiquitin; WT: wild-type; VSV: vesicular stomatitis virus.

Keywords: Antiviral immunity; cargo receptor; deubiquitination; selective autophagy; type I interferon signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antiviral Agents
  • Autophagy
  • Deubiquitinating Enzymes / metabolism
  • Dextrans / metabolism
  • Green Fluorescent Proteins / metabolism
  • I-kappa B Kinase
  • Immunity, Innate / genetics
  • Interferon Regulatory Factor-3* / metabolism
  • Interferon Type I* / metabolism
  • Lysine
  • Nucleotidyltransferases / metabolism
  • Pathogen-Associated Molecular Pattern Molecules
  • RNA, Small Interfering
  • Sequestosome-1 Protein / metabolism
  • Ubiquitins / metabolism

Substances

  • Antiviral Agents
  • Dextrans
  • Interferon Regulatory Factor-3
  • Interferon Type I
  • Pathogen-Associated Molecular Pattern Molecules
  • RNA, Small Interfering
  • Sequestosome-1 Protein
  • Ubiquitins
  • Green Fluorescent Proteins
  • I-kappa B Kinase
  • Nucleotidyltransferases
  • Deubiquitinating Enzymes
  • Lysine

Grants and funding

This work was supported by the National Natural Science Foundation of China [92042303, 31870862, 31970700 and 32170876], Science and Technology Planning Project of Guangzhou, China [201907010038], Guangdong Basic and Applied Basic Research Foundation [2020B1515120090], and China Postdoctoral Science Foundation [2020TQ0388 and 2020M683036].