Identification of Nafamostat as a Potent Inhibitor of Middle East Respiratory Syndrome Coronavirus S Protein-Mediated Membrane Fusion Using the Split-Protein-Based Cell-Cell Fusion Assay

Antimicrob Agents Chemother. 2016 Oct 21;60(11):6532-6539. doi: 10.1128/AAC.01043-16. Print 2016 Nov.

Abstract

Middle East respiratory syndrome (MERS) is an emerging infectious disease associated with a relatively high mortality rate of approximately 40%. MERS is caused by MERS coronavirus (MERS-CoV) infection, and no specific drugs or vaccines are currently available to prevent MERS-CoV infection. MERS-CoV is an enveloped virus, and its envelope protein (S protein) mediates membrane fusion at the plasma membrane or endosomal membrane. Multiple proteolysis by host proteases, such as furin, transmembrane protease serine 2 (TMPRSS2), and cathepsins, causes the S protein to become fusion competent. TMPRSS2, which is localized to the plasma membrane, is a serine protease responsible for the proteolysis of S in the post-receptor-binding stage. Here, we developed a cell-based fusion assay for S in a TMPRSS2-dependent manner using cell lines expressing Renilla luciferase (RL)-based split reporter proteins. S was stably expressed in the effector cells, and the corresponding receptor for S, CD26, was stably coexpressed with TMPRSS2 in the target cells. Membrane fusion between these effector and target cells was quantitatively measured by determining the RL activity. The assay was optimized for a 384-well format, and nafamostat, a serine protease inhibitor, was identified as a potent inhibitor of S-mediated membrane fusion in a screening of about 1,000 drugs approved for use by the U.S. Food and Drug Administration. Nafamostat also blocked MERS-CoV infection in vitro Our assay has the potential to facilitate the discovery of new inhibitors of membrane fusion of MERS-CoV as well as other viruses that rely on the activity of TMPRSS2.

MeSH terms

  • Benzamidines
  • Cathepsins / genetics
  • Cathepsins / metabolism
  • Cell Fusion
  • Cell Membrane / drug effects*
  • Cell Membrane / metabolism
  • Cell Membrane / virology
  • Dipeptidyl Peptidase 4 / genetics
  • Dipeptidyl Peptidase 4 / metabolism
  • Furin / genetics
  • Furin / metabolism
  • Gene Expression Regulation
  • Genes, Reporter
  • Guanidines / pharmacology*
  • HEK293 Cells
  • High-Throughput Screening Assays
  • Host-Pathogen Interactions
  • Humans
  • Intracellular Membranes / drug effects*
  • Intracellular Membranes / metabolism
  • Intracellular Membranes / virology
  • Luciferases / genetics
  • Luciferases / metabolism
  • Membrane Fusion / drug effects*
  • Middle East Respiratory Syndrome Coronavirus / drug effects*
  • Middle East Respiratory Syndrome Coronavirus / genetics
  • Middle East Respiratory Syndrome Coronavirus / growth & development
  • Proteolysis
  • Serine Endopeptidases / genetics
  • Serine Endopeptidases / metabolism
  • Spike Glycoprotein, Coronavirus / antagonists & inhibitors*
  • Spike Glycoprotein, Coronavirus / genetics
  • Spike Glycoprotein, Coronavirus / metabolism
  • Viral Fusion Protein Inhibitors / pharmacology*

Substances

  • Benzamidines
  • Guanidines
  • Spike Glycoprotein, Coronavirus
  • Viral Fusion Protein Inhibitors
  • Luciferases
  • Cathepsins
  • DPP4 protein, human
  • Dipeptidyl Peptidase 4
  • Serine Endopeptidases
  • TMPRSS2 protein, human
  • Furin
  • nafamostat

Grants and funding

This research is partially supported by the Japan Initiative for Global Research Network on Infectious Diseases (J-GRID) from the Ministry of Education, Culture, Sport, Science & Technology in Japan and the Japan Agency for Medical Research and Development (AMED).