Protective RBD-dimer vaccines against SARS-CoV-2 and its variants produced in glycoengineered Pichia pastoris

PLoS Pathog. 2024 Aug 30;20(8):e1012487. doi: 10.1371/journal.ppat.1012487. eCollection 2024 Aug.

Abstract

Protective vaccines are crucial for preventing and controlling coronavirus disease 2019 (COVID-19). Updated vaccines are needed to confront the continuously evolving and circulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants. These vaccines should be safe, effective, amenable to easily scalable production, and affordable. Previously, we developed receptor binding domain (RBD) dimer-based protein subunit vaccines (ZF2001 and updated vaccines) in mammalian cells. In this study, we explored a strategy for producing RBD-dimer immunogens in Pichia pastoris. We found that wild-type P. pastoris produced hyperglycosylated RBD-dimer protein containing four N-glycosylation sites in P. pastoris. Therefore, we engineered the wild type P. pastoris (GS strain) into GSΔOCH1pAO by deleting the OCH1 gene (encoding α-1,6-mannosyltransferase enzyme) to decrease glycosylation, as well as by overexpressing the HIS4 gene (encoding histidine dehydrogenase) to increase histidine synthesis for better growth. In addition, RBD-dimer protein was truncated to remove the R328/F329 cleavage sites in P. pastoris. Several homogeneous RBD-dimer proteins were produced in the GSΔOCH1pAO strain, demonstrating the feasibility of using the P. pastoris expression system. We further resolved the cryo-EM structure of prototype-Beta RBD-dimer complexed with the neutralizing antibody CB6 to reveal the completely exposed immune epitopes of the RBDs. In a murine model, we demonstrated that the yeast-produced RBD-dimer induces robust and protective antibody responses, which is suitable for boosting immunization. This study developed the yeast system for producing SARS-CoV-2 RBD-dimer immunogens, providing a promising platform and pipeline for the future continuous updating and production of SARS-CoV-2 vaccines.

MeSH terms

  • Animals
  • Antibodies, Neutralizing / immunology
  • Antibodies, Viral / immunology
  • COVID-19 Vaccines* / immunology
  • COVID-19* / immunology
  • COVID-19* / prevention & control
  • Female
  • Glycosylation
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • Pichia / genetics
  • Pichia / metabolism
  • SARS-CoV-2* / genetics
  • SARS-CoV-2* / immunology
  • Saccharomycetales / genetics
  • Saccharomycetales / immunology
  • Saccharomycetales / metabolism
  • Spike Glycoprotein, Coronavirus / genetics
  • Spike Glycoprotein, Coronavirus / immunology

Substances

  • COVID-19 Vaccines
  • Spike Glycoprotein, Coronavirus
  • Antibodies, Neutralizing
  • Antibodies, Viral
  • spike protein, SARS-CoV-2

Supplementary concepts

  • Komagataella pastoris
  • SARS-CoV-2 variants

Grants and funding

This work was supported by the National Key Research and Development Program of China [2021YFC2301300 (H.S.), 2020YFA0907100 (G.F.G.), https://service.most.gov.cn/index/] and the Excellent Young Scientist Program from National Natural Science Foundation of China (NSFC) [82122031 (L.D.), https://www.nsfc.gov.cn/english/site_1/index.html]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.