Immunoproteasome activation enables human TRIM5α restriction of HIV-1

Nat Microbiol. 2019 Jun;4(6):933-940. doi: 10.1038/s41564-019-0402-0. Epub 2019 Mar 18.

Abstract

Type 1 interferon suppresses viral replication by upregulating the expression of interferon-stimulated genes with diverse antiviral properties1. The replication of human immunodeficiency virus type 1 (HIV-1) is naturally inhibited by interferon, with the steps between viral entry and chromosomal integration of viral DNA being notably susceptible2-5. The interferon-stimulated gene myxovirus resistance 2 has been defined as an effective postentry inhibitor of HIV-1, but is only partially responsible for interferon's suppressive effect6-8. Using small interfering RNA-based library screening in interferon-α-treated cells, we sought to characterize further interferon-stimulated genes that target the pre-integration phases of HIV-1 infection, and identified human tripartite-containing motif 5α (TRIM5α) as a potent anti-HIV-1 restriction factor. Human TRIM5α, in contrast with many nonhuman orthologues, has not generally been ascribed substantial HIV-1 inhibitory function, a finding attributed to ineffective recognition of cytoplasmic viral capsids by TRIM5α2,9,10. Here, we demonstrate that interferon-α-mediated stimulation of the immunoproteasome, a proteasome isoform mainly present in immune cells and distinguished from the constitutive proteasome by virtue of its different catalytic β-subunits, as well as the proteasome activator 28 regulatory complex11-13, and the associated accelerated turnover of TRIM5α underpin the reprogramming of human TRIM5α for effective capsid-dependent inhibition of HIV-1 DNA synthesis and infection. These observations identify a mechanism for regulating human TRIM5α antiviral function in human cells and rationalize how TRIM5α participates in the immune control of HIV-1 infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antiviral Agents / antagonists & inhibitors*
  • Antiviral Restriction Factors
  • Capsid / drug effects
  • Capsid Proteins / drug effects
  • Carrier Proteins / antagonists & inhibitors*
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology*
  • Carrier Proteins / metabolism*
  • Cell Line
  • Gene Silencing
  • HEK293 Cells
  • HIV Infections / immunology*
  • HIV-1 / drug effects*
  • Humans
  • Interferon-alpha / immunology
  • Interferon-alpha / metabolism
  • Myxovirus Resistance Proteins / genetics
  • Proteasome Endopeptidase Complex / metabolism*
  • Tripartite Motif Proteins
  • Ubiquitin-Protein Ligases
  • Virus Replication

Substances

  • Antiviral Agents
  • Antiviral Restriction Factors
  • Capsid Proteins
  • Carrier Proteins
  • Interferon-alpha
  • Myxovirus Resistance Proteins
  • Tripartite Motif Proteins
  • TRIM5 protein, human
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex