Structural basis for IFN antagonism by human respiratory syncytial virus nonstructural protein 2

Proc Natl Acad Sci U S A. 2021 Mar 9;118(10):e2020587118. doi: 10.1073/pnas.2020587118.

Abstract

Human respiratory syncytial virus (RSV) nonstructural protein 2 (NS2) inhibits host interferon (IFN) responses stimulated by RSV infection by targeting early steps in the IFN-signaling pathway. But the molecular mechanisms related to how NS2 regulates these processes remain incompletely understood. To address this gap, here we solved the X-ray crystal structure of NS2. This structure revealed a unique fold that is distinct from other known viral IFN antagonists, including RSV NS1. We also show that NS2 directly interacts with an inactive conformation of the RIG-I-like receptors (RLRs) RIG-I and MDA5. NS2 binding prevents RLR ubiquitination, a process critical for prolonged activation of downstream signaling. Structural analysis, including by hydrogen-deuterium exchange coupled to mass spectrometry, revealed that the N terminus of NS2 is essential for binding to the RIG-I caspase activation and recruitment domains. N-terminal mutations significantly diminish RIG-I interactions and result in increased IFNβ messenger RNA levels. Collectively, our studies uncover a previously unappreciated regulatory mechanism by which NS2 further modulates host responses and define an approach for targeting host responses.

Keywords: IFN antagonist; NS2; RSV; nonstructural protein.

Publication types

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

MeSH terms

  • Crystallography, X-Ray
  • DEAD Box Protein 58* / chemistry
  • DEAD Box Protein 58* / metabolism
  • Deuterium Exchange Measurement
  • HEK293 Cells
  • Humans
  • Interferon-Induced Helicase, IFIH1* / chemistry
  • Interferon-Induced Helicase, IFIH1* / metabolism
  • Interferon-beta* / chemistry
  • Interferon-beta* / metabolism
  • Protein Binding
  • RNA, Messenger / chemistry
  • RNA, Messenger / metabolism
  • Receptors, Immunologic* / chemistry
  • Receptors, Immunologic* / metabolism
  • Viral Nonstructural Proteins* / chemistry
  • Viral Nonstructural Proteins* / metabolism

Substances

  • NS2 protein, human respiratory syncytial virus
  • RNA, Messenger
  • Receptors, Immunologic
  • Viral Nonstructural Proteins
  • Interferon-beta
  • RIGI protein, human
  • IFIH1 protein, human
  • DEAD Box Protein 58
  • Interferon-Induced Helicase, IFIH1