Nanobodies targeting norovirus capsid reveal functional epitopes and potential mechanisms of neutralization

PLoS Pathog. 2017 Nov 2;13(11):e1006636. doi: 10.1371/journal.ppat.1006636. eCollection 2017 Nov.

Abstract

Norovirus is the leading cause of gastroenteritis worldwide. Despite recent developments in norovirus propagation in cell culture, these viruses are still challenging to grow routinely. Moreover, little is known on how norovirus infects the host cells, except that histo-blood group antigens (HBGAs) are important binding factors for infection and cell entry. Antibodies that bind at the HBGA pocket and block attachment to HBGAs are believed to neutralize the virus. However, additional neutralization epitopes elsewhere on the capsid likely exist and impeding the intrinsic structural dynamics of the capsid could be equally important. In the current study, we investigated a panel of Nanobodies in order to probe functional epitopes that could trigger capsid rearrangement and/ or interfere with HBGA binding interactions. The precise binding sites of six Nanobodies (Nano-4, Nano-14, Nano-26, Nano-27, Nano-32, and Nano-42) were identified using X-ray crystallography. We showed that these Nanobodies bound on the top, side, and bottom of the norovirus protruding domain. The impact of Nanobody binding on norovirus capsid morphology was analyzed using electron microscopy and dynamic light scattering. We discovered that distinct Nanobody epitopes were associated with varied changes in particle structural integrity and assembly. Interestingly, certain Nanobody-induced capsid morphological changes lead to the capsid protein degradation and viral RNA exposure. Moreover, Nanobodies employed multiple inhibition mechanisms to prevent norovirus attachment to HBGAs, which included steric obstruction (Nano-14), allosteric interference (Nano-32), and violation of normal capsid morphology (Nano-26 and Nano-85). Finally, we showed that two Nanobodies (Nano-26 and Nano-85) not only compromised capsid integrity and inhibited VLPs attachment to HBGAs, but also recognized a broad panel of norovirus genotypes with high affinities. Consequently, Nano-26 and Nano-85 have a great potential to function as novel therapeutic agents against human noroviruses.

Publication types

  • Comparative Study

MeSH terms

  • Antibodies, Neutralizing / chemistry
  • Antibodies, Neutralizing / metabolism
  • Antibodies, Neutralizing / pharmacology*
  • Antibody Affinity
  • Antiviral Agents / chemistry
  • Antiviral Agents / metabolism
  • Antiviral Agents / pharmacology*
  • Binding Sites, Antibody
  • Binding, Competitive
  • Blood Group Antigens / chemistry
  • Blood Group Antigens / metabolism
  • Capsid / chemistry
  • Capsid / drug effects*
  • Capsid / metabolism
  • Capsid / ultrastructure
  • Capsid Proteins / antagonists & inhibitors*
  • Capsid Proteins / chemistry
  • Capsid Proteins / metabolism
  • Cross Reactions
  • Crystallography, X-Ray
  • Dynamic Light Scattering
  • Epitopes
  • Kinetics
  • Microscopy, Electron, Transmission
  • Models, Molecular*
  • Norovirus / chemistry
  • Norovirus / drug effects*
  • Norovirus / metabolism
  • Norovirus / ultrastructure
  • Protein Conformation
  • Protein Interaction Domains and Motifs
  • Single-Domain Antibodies / chemistry
  • Single-Domain Antibodies / metabolism
  • Single-Domain Antibodies / pharmacology*
  • Thermodynamics

Substances

  • Antibodies, Neutralizing
  • Antiviral Agents
  • Blood Group Antigens
  • Capsid Proteins
  • Epitopes
  • Single-Domain Antibodies

Grants and funding

This work was supported by funding from Bundesministerium für Bildung und Forschung BMBF VIP+ (NATION, 03VP00912): https://www.bmbf.de/de/vip-technologische-und-gesellschaftliche-innovationspotenziale-erschliessen-563.html; CHS foundation: http://www.chs-stiftung.de; Helmholtz-Chinese Academy of Sciences (HCJRG-202): https://www.helmholtz.de. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.