Cell membrane-anchored anti-HIV single-chain antibodies and bifunctional inhibitors targeting the gp41 fusion protein: new strategies for HIV gene therapy

Emerg Microbes Infect. 2022 Dec;11(1):30-49. doi: 10.1080/22221751.2021.2011616.

Abstract

Emerging studies indicate that infusion of HIV-resistant cells could be an effective strategy to achieve a sterilizing or functional cure. We recently reported that glycosylphosphatidylinositol (GPI)-anchored nanobody or a fusion inhibitory peptide can render modified cells resistant to HIV-1 infection. In this study, we comprehensively characterized a panel of newly isolated HIV-1-neutralizing antibodies as GPI-anchored inhibitors. Fusion genes encoding the single-chain variable fragment (scFv) of 3BNC117, N6, PGT126, PGT128, 10E8, or 35O22 were constructed with a self-inactivating lentiviral vector, and they were efficiently expressed in the lipid raft sites of target cell membrane without affecting the expression of HIV-1 receptors (CD4, CCR5 and CXCR4). Significantly, transduced cells exhibited various degrees of resistance to cell-free HIV-1 infection and cell-associated HIV-1 transmission, as well as viral Env-mediated cell-cell fusion, with the cells modified by GPI-10E8 showing the most potent and broad anti-HIV activity. In mechanism, GPI-10E8 also interfered with the processing of viral Env in transduced cells and attenuated the infectivity of progeny viruses. By genetically linking 10E8 with a fusion inhibitor peptide, we subsequently designed a group of eight bifunctional constructs as cell membrane-based inhibitors, designated CMI01∼CMI08, which rendered cells completely resistant to HIV-1, HIV-2, and simian immunodeficiency virus (SIV). In human CD4+ T cells, GPI-10E8 and its bifunctional derivatives blocked both CCR5- and CXCR4-tropic HIV-1 isolates efficiently, and the modified cells displayed robust survival selection under HIV-1 infection. Therefore, our studies provide new strategies for generating HIV-resistant cells, which can be used alone or with other gene therapy approaches.

Keywords: HIV; broadly neutralizing antibodies (bNAbs); fusion inhibitory peptide; gene therapy; glycosylphosphatidylinositol (GPI).

MeSH terms

  • Anti-HIV Agents / pharmacology
  • Broadly Neutralizing Antibodies / genetics
  • Broadly Neutralizing Antibodies / immunology
  • CD4-Positive T-Lymphocytes / virology
  • Cell Fusion
  • Cell Line
  • Genetic Therapy
  • Glycosylphosphatidylinositols
  • HIV Antibodies / genetics
  • HIV Antibodies / immunology*
  • HIV Envelope Protein gp41 / antagonists & inhibitors*
  • HIV Envelope Protein gp41 / immunology
  • HIV Fusion Inhibitors / pharmacology
  • HIV Infections / therapy*
  • HIV Infections / virology
  • HIV-1 / immunology
  • HIV-1 / physiology*
  • HIV-2 / immunology
  • HIV-2 / physiology
  • Humans
  • Membrane Microdomains
  • Peptide Fragments / genetics
  • Peptide Fragments / pharmacology*
  • Receptors, HIV / metabolism
  • Simian Immunodeficiency Virus / immunology
  • Simian Immunodeficiency Virus / physiology
  • Single-Chain Antibodies / genetics
  • Single-Chain Antibodies / immunology*
  • Transgenes
  • Viral Tropism

Substances

  • Anti-HIV Agents
  • Broadly Neutralizing Antibodies
  • Glycosylphosphatidylinositols
  • HIV Antibodies
  • HIV Envelope Protein gp41
  • HIV Fusion Inhibitors
  • Peptide Fragments
  • Receptors, HIV
  • Single-Chain Antibodies

Grants and funding

This work was supported by National Natural Science Foundation of China: [Grant Number 81630061]; National Science and Technology Major Project of China: [Grant Number 2017ZX10202102-001-003,2018ZX10301103]; CAMS Innovation Fund for Medical Sciences: [Grant Number 2017-I2M-1-014,2021-I2M-1-037].