Broad immunity to SARS-CoV-2 variants of concern mediated by a SARS-CoV-2 receptor-binding domain protein vaccine.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jun 2023
Historique:
received: 15 09 2022
revised: 02 03 2023
accepted: 01 04 2023
medline: 19 6 2023
pubmed: 6 5 2023
entrez: 6 5 2023
Statut: ppublish

Résumé

The SARS-CoV-2 global pandemic has fuelled the generation of vaccines at an unprecedented pace and scale. However, many challenges remain, including: the emergence of vaccine-resistant mutant viruses, vaccine stability during storage and transport, waning vaccine-induced immunity, and concerns about infrequent adverse events associated with existing vaccines. We report on a protein subunit vaccine comprising the receptor-binding domain (RBD) of the ancestral SARS-CoV-2 spike protein, dimerised with an immunoglobulin IgG1 Fc domain. These were tested in conjunction with three different adjuvants: a TLR2 agonist R4-Pam2Cys, an NKT cell agonist glycolipid α-Galactosylceramide, or MF59® squalene oil-in-water adjuvant, using mice, rats and hamsters. We also developed an RBD-human IgG1 Fc vaccine with an RBD sequence of the immuno-evasive beta variant (N501Y, E484K, K417N). These vaccines were also tested as a heterologous third dose booster in mice, following priming with whole spike vaccine. Each formulation of the RBD-Fc vaccines drove strong neutralising antibody (nAb) responses and provided durable and highly protective immunity against lower and upper airway infection in mouse models of COVID-19. The 'beta variant' RBD vaccine, combined with MF59® adjuvant, induced strong protection in mice against the beta strain as well as the ancestral strain. Furthermore, when used as a heterologous third dose booster, the RBD-Fc vaccines combined with MF59® increased titres of nAb against other variants including alpha, delta, delta+, gamma, lambda, mu, and omicron BA.1, BA.2 and BA.5. These results demonstrated that an RBD-Fc protein subunit/MF59® adjuvanted vaccine can induce high levels of broadly reactive nAbs, including when used as a booster following prior immunisation of mice with whole ancestral-strain spike vaccines. This vaccine platform offers a potential approach to augment some of the currently approved vaccines in the face of emerging variants of concern, and it has now entered a phase I clinical trial. This work was supported by grants from the Medical Research Future Fund (MRFF) (2005846), The Jack Ma Foundation, National Health and Medical Research Council of Australia (NHMRC; 1113293) and Singapore National Medical Research Council (MOH-COVID19RF-003). Individual researchers were supported by an NHMRC Senior Principal Research Fellowship (1117766), NHMRC Investigator Awards (2008913 and 1173871), Australian Research Council Discovery Early Career Research Award (ARC DECRA; DE210100705) and philanthropic awards from IFM investors and the A2 Milk Company.

Sections du résumé

BACKGROUND BACKGROUND
The SARS-CoV-2 global pandemic has fuelled the generation of vaccines at an unprecedented pace and scale. However, many challenges remain, including: the emergence of vaccine-resistant mutant viruses, vaccine stability during storage and transport, waning vaccine-induced immunity, and concerns about infrequent adverse events associated with existing vaccines.
METHODS METHODS
We report on a protein subunit vaccine comprising the receptor-binding domain (RBD) of the ancestral SARS-CoV-2 spike protein, dimerised with an immunoglobulin IgG1 Fc domain. These were tested in conjunction with three different adjuvants: a TLR2 agonist R4-Pam2Cys, an NKT cell agonist glycolipid α-Galactosylceramide, or MF59® squalene oil-in-water adjuvant, using mice, rats and hamsters. We also developed an RBD-human IgG1 Fc vaccine with an RBD sequence of the immuno-evasive beta variant (N501Y, E484K, K417N). These vaccines were also tested as a heterologous third dose booster in mice, following priming with whole spike vaccine.
FINDINGS RESULTS
Each formulation of the RBD-Fc vaccines drove strong neutralising antibody (nAb) responses and provided durable and highly protective immunity against lower and upper airway infection in mouse models of COVID-19. The 'beta variant' RBD vaccine, combined with MF59® adjuvant, induced strong protection in mice against the beta strain as well as the ancestral strain. Furthermore, when used as a heterologous third dose booster, the RBD-Fc vaccines combined with MF59® increased titres of nAb against other variants including alpha, delta, delta+, gamma, lambda, mu, and omicron BA.1, BA.2 and BA.5.
INTERPRETATION CONCLUSIONS
These results demonstrated that an RBD-Fc protein subunit/MF59® adjuvanted vaccine can induce high levels of broadly reactive nAbs, including when used as a booster following prior immunisation of mice with whole ancestral-strain spike vaccines. This vaccine platform offers a potential approach to augment some of the currently approved vaccines in the face of emerging variants of concern, and it has now entered a phase I clinical trial.
FUNDING BACKGROUND
This work was supported by grants from the Medical Research Future Fund (MRFF) (2005846), The Jack Ma Foundation, National Health and Medical Research Council of Australia (NHMRC; 1113293) and Singapore National Medical Research Council (MOH-COVID19RF-003). Individual researchers were supported by an NHMRC Senior Principal Research Fellowship (1117766), NHMRC Investigator Awards (2008913 and 1173871), Australian Research Council Discovery Early Career Research Award (ARC DECRA; DE210100705) and philanthropic awards from IFM investors and the A2 Milk Company.

Identifiants

pubmed: 37148585
pii: S2352-3964(23)00139-1
doi: 10.1016/j.ebiom.2023.104574
pmc: PMC10159263
pii:
doi:

Substances chimiques

Carrier Proteins 0
COVID-19 Vaccines 0
MF59 oil emulsion 0
spike protein, SARS-CoV-2 0
Protein Subunits 0
Adjuvants, Immunologic 0
Antibodies, Neutralizing 0
Antibodies, Viral 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104574

Informations de copyright

Copyright © 2023. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of interests Two provisional patents (PCT/AU2021/051553 and PCT/AU2023/050093) covering the RBD-Fc vaccines described in this study, and underlying technology, have been submitted through The University of Melbourne, with D.I.G., G.D., N.A.G., D.C.J. and D.F.J.P. as co-inventors. C.W.T. and L.-f.W. are co-inventors of a patent on the surrogate virus neutralization test (sVNT) platform. S.R.L. receives consulting fees from ViiV, Vaxxinity, Esfam, Abbvie, and Gilead. S.R.L. has received honoraria from Merck, Sharpe and Dohme, and from Gilead. K.S. is on a DSMB for a vaccine study in Thailand, and is Chair of the WHO Technical Advisory Group on COVID-19 vaccines (TAG-CO-VAC). T.N. receives research contracts to conduct clinical trials, with funding to institution from Moderna, SanofiPasteur, GSK, Iliad Biotechnologies, Dynavax, Seqirus, Janssen, MSD. T.N. receives consulting fees from GSK, Seqirus, MSD, SanofiPasteur, AstraZeneca, Moderna, BioNet, Pfizer. T.N. serves on DSMBs for Seqirus, Clover, Moderna, Emergent, Serum Institute of India, SK Bioscience Korea, Emergent Biosolutions, Novavax. S.R. is an employee of CSL Seqirus that is a maker of influenza vaccines. D.C.J. is a founder and shareholder of Ena Respiratory. C.Y.W. and W.Z. are shareholders of Ena Respiratory. D.I.G. has received research funding from CSL for an unrelated project. All other authors declare no conflict of interests.

Auteurs

Georgia Deliyannis (G)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Nicholas A Gherardin (NA)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Chinn Yi Wong (CY)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Samantha L Grimley (SL)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

James P Cooney (JP)

Walter and Eliza Hall Institute, Infectious Diseases & Immune Defence Division, Parkville, Victoria 3052, Australia.

Samuel J Redmond (SJ)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Paula Ellenberg (P)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Kathryn C Davidson (KC)

Walter and Eliza Hall Institute, Infectious Diseases & Immune Defence Division, Parkville, Victoria 3052, Australia.

Francesca L Mordant (FL)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Tim Smith (T)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Marianne Gillard (M)

Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland, Australia.

Ester Lopez (E)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Julie McAuley (J)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Chee Wah Tan (CW)

Duke NUS Medical School, Programme for Emerging Infectious Diseases, Singapore.

Jing J Wang (JJ)

Department of Immunology, Flinders University and SA Pathology, Flinders Medical Centre, Bedford Park, Adelaide, South Australia 5042, Australia.

Weiguang Zeng (W)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Mason Littlejohn (M)

Doherty Directorate, The Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Runhong Zhou (R)

Department of Microbiology, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China.

Jasper Fuk-Woo Chan (J)

Department of Microbiology, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China; Centre for Virology, Vaccinology and Therapeutics, Hong Kong Science and Technology Park, Hong Kong Special Administrative Region, China.

Zhi-Wei Chen (ZW)

Department of Microbiology, School of Clinical Medicine, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong Special Administrative Region, China; Centre for Virology, Vaccinology and Therapeutics, Hong Kong Science and Technology Park, Hong Kong Special Administrative Region, China.

Airn E Hartwig (AE)

Biomedical Sciences, Colorado State University, Fort Collins, CO 80523, USA.

Richard Bowen (R)

Biomedical Sciences, Colorado State University, Fort Collins, CO 80523, USA.

Jason M Mackenzie (JM)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Elizabeth Vincan (E)

Victorian Infectious Diseases Reference Laboratory (VIDRL) at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia; Department of Infectious Diseases, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Joseph Torresi (J)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Katherine Kedzierska (K)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Colin W Pouton (CW)

Monash Institute of Pharmaceutical Sciences, Parkville, Victoria 3052, Australia.

Tom P Gordon (TP)

Department of Immunology, Flinders University and SA Pathology, Flinders Medical Centre, Bedford Park, Adelaide, South Australia 5042, Australia.

Lin-Fa Wang (LF)

Duke NUS Medical School, Programme for Emerging Infectious Diseases, Singapore.

Stephen J Kent (SJ)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Adam K Wheatley (AK)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Sharon R Lewin (SR)

Department of Infectious Diseases, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia; Victorian Infectious Diseases Service, Royal Melbourne Hospital at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia; Department of Infectious Diseases, The Alfred Hospital and Monash University, Melbourne, 3010 Australia.

Kanta Subbarao (K)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia; WHO Collaborating Centre for Reference and Research on Influenza at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Amy W Chung (AW)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Marc Pellegrini (M)

Walter and Eliza Hall Institute, Infectious Diseases & Immune Defence Division, Parkville, Victoria 3052, Australia.

Trent Munro (T)

Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland, Australia.

Terry Nolan (T)

Department of Infectious Diseases, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia; Vaccine and Immunisation Research Group (VIRGo), Department of Infectious Disease, Peter Doherty Institute for Infection and Immunity, University of Melbourne, and Murdoch Children's Research Institute, Victoria 3010, Australia.

Steven Rockman (S)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia; Seqirus, Vaccine Innovation Unit, Parkville, Victoria, 3052, Australia.

David C Jackson (DC)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Damian F J Purcell (DFJ)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia.

Dale I Godfrey (DI)

Department of Microbiology & Immunology, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria 3000, Australia. Electronic address: godfrey@unimelb.edu.au.

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