TIM-mediated inhibition of HIV-1 release is antagonized by Nef but potentiated by SERINC proteins

Proc Natl Acad Sci U S A. 2019 Mar 19;116(12):5705-5714. doi: 10.1073/pnas.1819475116. Epub 2019 Mar 6.

Abstract

The T cell Ig and mucin domain (TIM) proteins inhibit release of HIV-1 and other enveloped viruses by interacting with cell- and virion-associated phosphatidylserine (PS). Here, we show that the Nef proteins of HIV-1 and other lentiviruses antagonize TIM-mediated restriction. TIM-1 more potently inhibits the release of Nef-deficient relative to Nef-expressing HIV-1, and ectopic expression of Nef relieves restriction. HIV-1 Nef does not down-regulate the overall level of TIM-1 expression, but promotes its internalization from the plasma membrane and sequesters its expression in intracellular compartments. Notably, Nef mutants defective in modulating membrane protein endocytic trafficking are incapable of antagonizing TIM-mediated inhibition of HIV-1 release. Intriguingly, depletion of SERINC3 or SERINC5 proteins in human peripheral blood mononuclear cells (PBMCs) attenuates TIM-1 restriction of HIV-1 release, in particular that of Nef-deficient viruses. In contrast, coexpression of SERINC3 or SERINC5 increases the expression of TIM-1 on the plasma membrane and potentiates TIM-mediated inhibition of HIV-1 production. Pulse-chase metabolic labeling reveals that the half-life of TIM-1 is extended by SERINC5 from <2 to ∼6 hours, suggesting that SERINC5 stabilizes the expression of TIM-1. Consistent with a role for SERINC protein in potentiating TIM-1 restriction, we find that MLV glycoGag and EIAV S2 proteins, which, like Nef, antagonize SERINC-mediated diminishment of HIV-1 infectivity, also effectively counteract TIM-mediated inhibition of HIV-1 release. Collectively, our work reveals a role of Nef in antagonizing TIM-1 and highlights the complex interplay between Nef and HIV-1 restriction by TIMs and SERINCs.

Keywords: HIV; Nef; SERINC; TIM.

Publication types

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

MeSH terms

  • Cell Membrane / metabolism
  • Down-Regulation
  • HEK293 Cells
  • HIV Infections / metabolism*
  • HIV Seropositivity
  • HIV-1 / metabolism
  • HIV-1 / pathogenicity
  • Hepatitis A Virus Cellular Receptor 1 / antagonists & inhibitors
  • Hepatitis A Virus Cellular Receptor 1 / metabolism
  • Hepatitis A Virus Cellular Receptor 1 / physiology*
  • Host-Pathogen Interactions / physiology
  • Humans
  • Leukocytes, Mononuclear / metabolism
  • Membrane Glycoproteins
  • Membrane Proteins / metabolism
  • Neoplasm Proteins / metabolism
  • Protein Transport
  • Receptors, Cell Surface / metabolism
  • Virion / metabolism
  • Virus Replication / drug effects
  • nef Gene Products, Human Immunodeficiency Virus / metabolism
  • nef Gene Products, Human Immunodeficiency Virus / physiology*

Substances

  • HAVCR1 protein, human
  • Hepatitis A Virus Cellular Receptor 1
  • Membrane Glycoproteins
  • Membrane Proteins
  • Neoplasm Proteins
  • Receptors, Cell Surface
  • SERINC3 protein, human
  • SERINC5 protein, human
  • nef Gene Products, Human Immunodeficiency Virus