Host-Primed Ebola Virus GP Exposes a Hydrophobic NPC1 Receptor-Binding Pocket, Revealing a Target for Broadly Neutralizing Antibodies.

Zachary A Bornholdt1 Esther Ndungo2 Marnie L Fusco1 Shridhar Bale1 Andrew I Flyak3 James E Crowe4 Kartik Chandran5 Erica Ollmann Saphire6
Affiliations 6 institutions
  1. Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, California, USA.
  2. Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, USA.
  3. Department of Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA.
  4. Department of Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA Department of Pediatrics, Vanderbilt University, Nashville, Tennessee, USA Vanderbilt Vaccine Center, Vanderbilt University, Nashville, Tennessee, USA.
  5. Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, USA [email protected] [email protected].
  6. Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, California, USA The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, California, USA [email protected] [email protected].

Abstract

The filovirus surface glycoprotein (GP) mediates viral entry into host cells. Following viral internalization into endosomes, GP is cleaved by host cysteine proteases to expose a receptor-binding site (RBS) that is otherwise hidden from immune surveillance. Here, we present the crystal structure of proteolytically cleaved Ebola virus GP to a resolution of 3.3 Å. We use this structure in conjunction with functional analysis of a large panel of pseudotyped viruses bearing mutant GP proteins to map the Ebola virus GP endosomal RBS at molecular resolution. Our studies indicate that binding of GP to its endosomal receptor Niemann-Pick C1 occurs in two distinct stages: the initial electrostatic interactions are followed by specific interactions with a hydrophobic trough that is exposed on the endosomally cleaved GP1 subunit. Finally, we demonstrate that monoclonal antibodies targeting the filovirus RBS neutralize all known filovirus GPs, making this conserved pocket a promising target for the development of panfilovirus therapeutics. Ebola virus uses its glycoprotein (GP) to enter new host cells. During entry, GP must be cleaved by human enzymes in order for receptor binding to occur. Here, we provide the crystal structure of the cleaved form of Ebola virus GP. We demonstrate that cleavage exposes a site at the top of GP and that this site binds the critical domain C of the receptor, termed Niemann-Pick C1 (NPC1). We perform mutagenesis to find parts of the site essential for binding NPC1 and map distinct roles for an upper, charged crest and lower, hydrophobic trough in cleaved GP. We find that this 3-dimensional site is conserved across the filovirus family and that antibody directed against this site is able to bind cleaved GP from every filovirus tested and neutralize viruses bearing those GPs.

Supporting text Virus Host Location
Antibodies, Neutralizing 80 Antibodies, Viral 212 Carrier Proteins 4 Cell Line 158 Crystallography, X-Ray 32 Ebolavirus 31 Hemorrhagic Fever, Ebola 27 Humans 1440 Hydrophobic and Hydrophilic Interactions 2 Intracellular Signaling Peptides and Proteins 6 Membrane Glycoproteins 26 Mutagenesis 7 Mutation 209 Niemann-Pick C1 Protein 4 Protein Binding 193 Receptors, Virus 204 Viral Envelope Proteins 60 Virus Internalization 100 envelope glycoprotein, Ebola virus 4 NPC1 protein, human 1

Evidence records

1 total
Functional Mechanism
1 records · 1 evidence types
Evidence type
1 records
OVE2287
Key finding

Ebola virus glycoprotein (GP) binds the human Niemann-Pick C1 (NPC1) receptor through specific interactions exposed after endosomal cleavage of GP1.

Virus
Host
Location
Not specified
Supporting text

Ebola virus uses its glycoprotein (GP) to enter new host cells. During entry, GP must be cleaved by human enzymes in order for receptor binding to occur. We demonstrate that cleavage exposes a site at the top of GP and that this site binds the critical domain C of the receptor, termed Niemann-Pick C1 (NPC1).

Method
crystal structure determination | pseudovirus assay | mutagenesis analysis | receptor binding assay
Receptors
Niemann-Pick C1 (NPC1)
Host factors
host cysteine proteases