Mucosal adenovirus vaccine boosting elicits IgA and durably prevents XBB.1.16 infection in nonhuman primates.


Journal

Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354

Informations de publication

Date de publication:
03 Sep 2024
Historique:
received: 15 01 2024
accepted: 06 08 2024
medline: 4 9 2024
pubmed: 4 9 2024
entrez: 3 9 2024
Statut: aheadofprint

Résumé

A mucosal route of vaccination could prevent severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) replication at the site of infection and limit transmission. We compared protection against heterologous XBB.1.16 challenge in nonhuman primates (NHPs) ~5 months following intramuscular boosting with bivalent mRNA encoding WA1 and BA.5 spike proteins or mucosal boosting with a WA1-BA.5 bivalent chimpanzee adenoviral-vectored vaccine delivered by intranasal or aerosol device. NHPs boosted by either mucosal route had minimal virus replication in the nose and lungs, respectively. By contrast, protection by intramuscular mRNA was limited to the lower airways. The mucosally delivered vaccine elicited durable airway IgG and IgA responses and, unlike the intramuscular mRNA vaccine, induced spike-specific B cells in the lungs. IgG, IgA and T cell responses correlated with protection in the lungs, whereas mucosal IgA alone correlated with upper airway protection. This study highlights differential mucosal and serum correlates of protection and how mucosal vaccines can durably prevent infection against SARS-CoV-2.

Identifiants

pubmed: 39227514
doi: 10.1038/s41590-024-01951-5
pii: 10.1038/s41590-024-01951-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NCI NIH HHS
ID : R01 CA211096
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI157155
Pays : United States
Organisme : NIAID NIH HHS
ID : 75N93021C00017
Pays : United States
Organisme : NIAID NIH HHS
ID : HHSN272201400008C
Pays : United States
Organisme : NIAID NIH HHS
ID : 75N93021C00014
Pays : United States
Organisme : NIAID NIH HHS
ID : 75N93019C00051
Pays : United States
Organisme : ODCDC CDC HHS
ID : P51 OD011132
Pays : United States

Informations de copyright

© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

Références

Andrews, N. et al. Duration of protection against mild and severe disease by COVID-19 vaccines. N. Engl. J. Med. 386, 340–350 (2022).
pubmed: 35021002 doi: 10.1056/NEJMoa2115481
Tseng, H. F. et al. Effectiveness of mRNA-1273 vaccination against SARS-CoV-2 omicron subvariants BA.1, BA.2, BA.2.12.1, BA.4, and BA.5. Nat. Commun. 14, 189 (2023).
pubmed: 36635284 pmcid: 9836332 doi: 10.1038/s41467-023-35815-7
Lin, D. Y. et al. Durability of bivalent boosters against omicron subvariants. N. Engl. J. Med. 388, 1818–1820 (2023).
pubmed: 37043647 doi: 10.1056/NEJMc2302462
Bowe, B., Xie, Y. & Al-Aly, Z. Acute and postacute sequelae associated with SARS-CoV-2 reinfection. Nat. Med. 28, 2398–2405 (2022).
pubmed: 36357676 pmcid: 9671810 doi: 10.1038/s41591-022-02051-3
Malahe, S. R. K. et al. Clinical characteristics and outcomes of immunocompromised patients with coronavirus disease 2019 caused by the Omicron variant: a prospective, observational study. Clin. Infect. Dis. 76, e172–e178 (2023).
pubmed: 35869843 doi: 10.1093/cid/ciac571
Griggs, E. P. et al. Clinical epidemiology and risk factors for critical outcomes among vaccinated and unvaccinated adults hospitalized with COVID-19—VISION Network, 10 States, June 2021–March 2023. Clin. Infect. Dis. 78, 338–348 (2023).
doi: 10.1093/cid/ciad505
Goldberg, Y. et al. Waning immunity after the BNT162b2 vaccine in Israel. N. Engl. J. Med. 385, e85 (2021).
pubmed: 34706170 doi: 10.1056/NEJMoa2114228
Baden, L. R. et al. Phase 3 trial of mRNA-1273 during the Delta-variant surge. N. Engl. J. Med. 385, 2485–2487 (2021).
pubmed: 34731553 doi: 10.1056/NEJMc2115597
Bergwerk, M. et al. COVID-19 breakthrough infections in vaccinated health care workers. N. Engl. J. Med. 385, 1474–1484 (2021).
pubmed: 34320281 doi: 10.1056/NEJMoa2109072
Corbett, K. S. et al. Immune correlates of protection by mRNA-1273 vaccine against SARS-CoV-2 in nonhuman primates. Science 373, eabj0299 (2021).
pubmed: 34529476 pmcid: 8449013 doi: 10.1126/science.abj0299
He, X. et al. Low-dose Ad26.COV2.S protection against SARS-CoV-2 challenge in rhesus macaques. Cell 184, 3467–3473 (2021).
pubmed: 34133941 pmcid: 8166510 doi: 10.1016/j.cell.2021.05.040
Rossler, A. et al. Characterizing SARS-CoV-2 neutralization profiles after bivalent boosting using antigenic cartography. Nat. Commun. 14, 5224 (2023).
pubmed: 37633965 pmcid: 10460376 doi: 10.1038/s41467-023-41049-4
Garcia-Beltran, W. F. et al. Multiple SARS-CoV-2 variants escape neutralization by vaccine-induced humoral immunity. Cell 184, 2372–2383 (2021).
pubmed: 33743213 pmcid: 7953441 doi: 10.1016/j.cell.2021.03.013
Carabelli, A. M. et al. SARS-CoV-2 variant biology: immune escape, transmission and fitness. Nat. Rev. Microbiol. 21, 162–177 (2023).
pubmed: 36653446 pmcid: 9847462
Reynolds, C. J. et al. Immune boosting by B.1.1.529 (Omicron) depends on previous SARS-CoV-2 exposure. Science 377, eabq1841 (2022).
pubmed: 35699621 doi: 10.1126/science.abq1841
Roltgen, K. et al. Immune imprinting, breadth of variant recognition, and germinal center response in human SARS-CoV-2 infection and vaccination. Cell 185, 1025–1040 (2022).
pubmed: 35148837 pmcid: 8786601 doi: 10.1016/j.cell.2022.01.018
Alsoussi, W. B. et al. SARS-CoV-2 Omicron boosting induces de novo B cell response in humans. Nature 617, 592–598 (2023).
pubmed: 37011668 doi: 10.1038/s41586-023-06025-4
Knisely, J. M. et al. Mucosal vaccines for SARS-CoV-2: scientific gaps and opportunities-workshop report. NPJ Vaccines 8, 53 (2023).
pubmed: 37045860 pmcid: 10091310 doi: 10.1038/s41541-023-00654-6
Havervall, S. et al. Anti-spike mucosal IgA protection against SARS-CoV-2 Omicron infection. N. Engl. J. Med. 387, 1333–1336 (2022).
pubmed: 36103621 doi: 10.1056/NEJMc2209651
Zuo, F., Marcotte, H., Hammarstrom, L. & Pan-Hammarstrom, Q. Mucosal IgA against SARS-CoV-2 omicron infection. N. Engl. J. Med. 387, e55 (2022).
pubmed: 36416778
Mao, T. et al. Unadjuvanted intranasal spike vaccine elicits protective mucosal immunity against sarbecoviruses. Science 378, eabo2523 (2022).
pubmed: 36302057 pmcid: 9798903 doi: 10.1126/science.abo2523
Baldeon Vaca, G. et al. Intranasal mRNA-LNP vaccination protects hamsters from SARS-CoV-2 infection. Sci. Adv. 9, eadh1655 (2023).
pubmed: 37738334 pmcid: 10516494 doi: 10.1126/sciadv.adh1655
Le Nouen, C. et al. Intranasal pediatric parainfluenza virus-vectored SARS-CoV-2 vaccine is protective in monkeys. Cell 185, 4811–4825 (2022).
pubmed: 36423629 pmcid: 9684001 doi: 10.1016/j.cell.2022.11.006
Ponce-de-Leon, S. et al. Interim safety and immunogenicity results from an NDV-based COVID-19 vaccine phase I trial in Mexico. NPJ Vaccines 8, 67 (2023).
pubmed: 37164959 pmcid: 10170424 doi: 10.1038/s41541-023-00662-6
Madhavan, M. et al. Tolerability and immunogenicity of an intranasally-administered adenovirus-vectored COVID-19 vaccine: an open-label partially-randomised ascending dose phase I trial. EBioMedicine 85, 104298 (2022).
pubmed: 36229342 pmcid: 9550199 doi: 10.1016/j.ebiom.2022.104298
Wu, S. et al. Safety, tolerability, and immunogenicity of an aerosolised adenovirus type-5 vector-based COVID-19 vaccine (Ad5-nCoV) in adults: preliminary report of an open-label and randomised phase 1 clinical trial. Lancet Infect. Dis. 21, 1654–1664 (2021).
pubmed: 34324836 pmcid: 8313090 doi: 10.1016/S1473-3099(21)00396-0
McMahan, K. et al. Mucosal boosting enhances vaccine protection against SARS-CoV-2 in macaques. Nature 626, 385–391 (2023).
pubmed: 38096903 pmcid: 10849944 doi: 10.1038/s41586-023-06951-3
Singh, C. et al. Phase III pivotal comparative clinical trial of intranasal (iNCOVACC) and intramuscular COVID 19 vaccine (Covaxin). NPJ Vaccines 8, 125 (2023).
pubmed: 37596281 pmcid: 10439197 doi: 10.1038/s41541-023-00717-8
Hassan, A. O. et al. A single-dose intranasal ChAd vaccine protects upper and lower respiratory tracts against SARS-CoV-2. Cell 183, 169–184 (2020).
pubmed: 32931734 pmcid: 7437481 doi: 10.1016/j.cell.2020.08.026
Hassan, A. O. et al. A single intranasal dose of chimpanzee adenovirus-vectored vaccine protects against SARS-CoV-2 infection in rhesus macaques. Cell Rep. Med. 2, 100230 (2021).
pubmed: 33754147 pmcid: 7969912 doi: 10.1016/j.xcrm.2021.100230
Bricker, T. L. et al. A single intranasal or intramuscular immunization with chimpanzee adenovirus-vectored SARS-CoV-2 vaccine protects against pneumonia in hamsters. Cell Rep. 36, 109400 (2021).
pubmed: 34245672 pmcid: 8238649 doi: 10.1016/j.celrep.2021.109400
Ying, B. et al. Mucosal vaccine-induced cross-reactive CD8(.) T cells protect against SARS-CoV-2 XBB.1.5 respiratory tract infection. Nat. Immunol. 25, 537–551 (2024).
pubmed: 38337035 pmcid: 10907304 doi: 10.1038/s41590-024-01743-x
Hassan, A. O. et al. An intranasal vaccine durably protects against SARS-CoV-2 variants in mice. Cell Rep. 36, 109452 (2021).
pubmed: 34289385 pmcid: 8270739 doi: 10.1016/j.celrep.2021.109452
Corbett, K. S. et al. mRNA-1273 protects against SARS-CoV-2 Beta infection in nonhuman primates. Nat. Immunol. 22, 1306–1315 (2021).
pubmed: 34417590 pmcid: 8488000 doi: 10.1038/s41590-021-01021-0
Gagne, M. et al. Protection from SARS-CoV-2 Delta one year after mRNA-1273 vaccination in rhesus macaques coincides with anamnestic antibody response in the lung. Cell 185, 113–130 (2022).
pubmed: 34921774 doi: 10.1016/j.cell.2021.12.002
Gagne, M. et al. mRNA-1273 or mRNA-Omicron boost in vaccinated macaques elicits similar B cell expansion, neutralizing responses, and protection from Omicron. Cell 185, 1556–1571 (2022).
pubmed: 35447072 pmcid: 8947944 doi: 10.1016/j.cell.2022.03.038
Corbett, K. S. et al. Protection against SARS-CoV-2 Beta variant in mRNA-1273 vaccine-boosted nonhuman primates. Science 374, 1343–1353 (2021).
pubmed: 34672695 doi: 10.1126/science.abl8912
Chandrashekar, A. et al. Vaccine protection against the SARS-CoV-2 Omicron variant in macaques. Cell 185, 1549–1555 (2022).
pubmed: 35427477 pmcid: 8926910 doi: 10.1016/j.cell.2022.03.024
Solforosi, L. et al. Booster with Ad26.COV2.S or Omicron-adapted vaccine enhanced immunity and efficacy against SARS-CoV-2 Omicron in macaques. Nat. Commun. 14, 1944 (2023).
pubmed: 37029141 pmcid: 10080532 doi: 10.1038/s41467-023-37715-2
Munster, V. J. et al. Respiratory disease in rhesus macaques inoculated with SARS-CoV-2. Nature 585, 268–272 (2020).
pubmed: 32396922 pmcid: 7486227 doi: 10.1038/s41586-020-2324-7
Routhu, N. K. et al. Efficacy of mRNA-1273 and Novavax ancestral or BA.1 spike booster vaccines against SARS-CoV-2 BA.5 infection in non-human primates. Sci. Immunol. 8, eadg7015 (2023).
pubmed: 37191508 doi: 10.1126/sciimmunol.adg7015
Li, D. et al. Breadth of SARS-CoV-2 neutralization and protection induced by a nanoparticle vaccine. Nat. Commun. 13, 6309 (2022).
pubmed: 36274085 pmcid: 9588772 doi: 10.1038/s41467-022-33985-4
Tseng, H. F. et al. Effectiveness of mRNA-1273 against SARS-CoV-2 Omicron and Delta variants. Nat. Med. 28, 1063–1071 (2022).
pubmed: 35189624 pmcid: 9117141 doi: 10.1038/s41591-022-01753-y
Bar-On, Y. M. et al. Protection by a fourth dose of BNT162b2 against Omicron in Israel. N. Engl. J. Med. 386, 1712–1720 (2022).
pubmed: 35381126 doi: 10.1056/NEJMoa2201570
Mackin, S. R. et al. Fc-γR-dependent antibody effector functions are required for vaccine-mediated protection against antigen-shifted variants of SARS-CoV-2. Nat. Microbiol. 8, 569–580 (2023).
pubmed: 37012355 pmcid: 10797606 doi: 10.1038/s41564-023-01359-1
Suryadevara, N. et al. Neutralizing and protective human monoclonal antibodies recognizing the N-terminal domain of the SARS-CoV-2 spike protein. Cell 184, 2316–2331 (2021).
pubmed: 33773105 pmcid: 7962591 doi: 10.1016/j.cell.2021.03.029
Winkler, E. S. et al. Human neutralizing antibodies against SARS-CoV-2 require intact Fc effector functions for optimal therapeutic protection. Cell 184, 1804–1820 (2021).
pubmed: 33691139 pmcid: 7879018 doi: 10.1016/j.cell.2021.02.026
Schafer, A. et al. Antibody potency, effector function, and combinations in protection and therapy for SARS-CoV-2 infection in vivo. J. Exp. Med. 218, e20201993 (2021).
pubmed: 33211088 doi: 10.1084/jem.20201993
Pegu, A. et al. Durability of mRNA-1273 vaccine-induced antibodies against SARS-CoV-2 variants. Science 373, 1372–1377 (2021).
pubmed: 34385356 pmcid: 8691522 doi: 10.1126/science.abj4176
Barouch, D. H. et al. Durable humoral and cellular immune responses 8 months after Ad26.COV2.S vaccination. N. Engl. J. Med. 385, 951–953 (2021).
pubmed: 34260834 doi: 10.1056/NEJMc2108829
Collier, A. Y. et al. Differential kinetics of immune responses elicited by COVID-19 vaccines. N. Engl. J. Med. 385, 2010–2012 (2021).
pubmed: 34648703 doi: 10.1056/NEJMc2115596
Allie, S. R. et al. The establishment of resident memory B cells in the lung requires local antigen encounter. Nat. Immunol. 20, 97–108 (2019).
pubmed: 30510223 doi: 10.1038/s41590-018-0260-6
Onodera, T. et al. Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. Proc. Natl Acad. Sci. USA 109, 2485–2490 (2012).
pubmed: 22308386 pmcid: 3289300 doi: 10.1073/pnas.1115369109
Scheaffer, S. M. et al. Bivalent SARS-CoV-2 mRNA vaccines increase breadth of neutralization and protect against the BA.5 Omicron variant in mice. Nat. Med. 29, 247–257 (2023).
pubmed: 36265510 doi: 10.1038/s41591-022-02092-8
Schiepers, A. et al. Molecular fate-mapping of serum antibody responses to repeat immunization. Nature 615, 482–489 (2023).
pubmed: 36646114 pmcid: 10023323 doi: 10.1038/s41586-023-05715-3
Bladh, O. et al. Mucosal immune responses following a fourth SARS-CoV-2 vaccine dose. Lancet Microbe 4, e488 (2023).
pubmed: 37086736 doi: 10.1016/S2666-5247(23)00102-7
Liew, F. et al. SARS-CoV-2-specific nasal IgA wanes 9 months after hospitalisation with COVID-19 and is not induced by subsequent vaccination. EBioMedicine 87, 104402 (2023).
pubmed: 36543718 doi: 10.1016/j.ebiom.2022.104402
Francica, J. R. et al. Protective antibodies elicited by SARS-CoV-2 spike protein vaccination are boosted in the lung after challenge in nonhuman primates. Sci. Transl. Med. 13, eabi4547 (2021).
pubmed: 34315825 pmcid: 9266840 doi: 10.1126/scitranslmed.abi4547
Piccoli, L. et al. Mapping neutralizing and immunodominant sites on the SARS-CoV-2 spike receptor-binding domain by structure-guided high-resolution serology. Cell 183, 1024–1042 (2020).
pubmed: 32991844 pmcid: 7494283 doi: 10.1016/j.cell.2020.09.037
Liu, J. et al. CD8 T cells contribute to vaccine protection against SARS-CoV-2 in macaques. Sci. Immunol. 7, eabq7647 (2022).
pubmed: 35943359 doi: 10.1126/sciimmunol.abq7647
Mateus, J. et al. Low-dose mRNA-1273 COVID-19 vaccine generates durable memory enhanced by cross-reactive T cells. Science 374, eabj9853 (2021).
pubmed: 34519540 pmcid: 8542617 doi: 10.1126/science.abj9853
Tarke, A. et al. SARS-CoV-2 vaccination induces immunological T cell memory able to cross-recognize variants from Alpha to Omicron. Cell 185, 847–859 (2022).
pubmed: 35139340 pmcid: 8784649 doi: 10.1016/j.cell.2022.01.015
Egri, N. et al. Cellular and humoral responses after second and third SARS-CoV-2 vaccinations in patients with autoimmune diseases treated with rituximab: specific T cell immunity remains longer and plays a protective role against SARS-CoV-2 reinfections. Front. Immunol. 14, 1146841 (2023).
pubmed: 37180097 pmcid: 10174323 doi: 10.3389/fimmu.2023.1146841
Wherry, E. J. & Barouch, D. H. T cell immunity to COVID-19 vaccines. Science 377, 821–822 (2022).
pubmed: 35981045 doi: 10.1126/science.add2897
Rydyznski Moderbacher, C. et al. Antigen-specific adaptive immunity to SARS-CoV-2 in acute COVID-19 and associations with age and disease severity. Cell 183, 996–1012 (2020).
pubmed: 33010815 pmcid: 7494270 doi: 10.1016/j.cell.2020.09.038
Gilbert, P. B. et al. Immune correlates analysis of the mRNA-1273 COVID-19 vaccine efficacy clinical trial. Science 375, 43–50 (2022).
pubmed: 34812653 doi: 10.1126/science.abm3425
Tang, J. et al. Respiratory mucosal immunity against SARS-CoV-2 after mRNA vaccination. Sci. Immunol. 7, eadd4853 (2022).
pubmed: 35857583 doi: 10.1126/sciimmunol.add4853
Zohar, T. et al. Upper and lower respiratory tract correlates of protection against respiratory syncytial virus following vaccination of nonhuman primates. Cell Host Microbe 30, 41–52 (2022).
pubmed: 34879230 doi: 10.1016/j.chom.2021.11.006
Seibert, C. W. et al. Recombinant IgA is sufficient to prevent influenza virus transmission in guinea pigs. J. Virol. 87, 7793–7804 (2013).
pubmed: 23698296 pmcid: 3700183 doi: 10.1128/JVI.00979-13
Gould, V. M. W. et al. Nasal IgA provides protection against human influenza challenge in volunteers with low serum influenza antibody titre. Front. Microbiol. 8, 900 (2017).
pubmed: 28567036 pmcid: 5434144 doi: 10.3389/fmicb.2017.00900
Shimoda, M. et al. Isotype-specific selection of high affinity memory B cells in nasal-associated lymphoid tissue. J. Exp. Med. 194, 1597–1607 (2001).
pubmed: 11733574 pmcid: 2193529 doi: 10.1084/jem.194.11.1597
Hodge, L. M. et al. Immunoglobulin A (IgA) responses and IgE-associated inflammation along the respiratory tract after mucosal but not systemic immunization. Infect. Immun. 69, 2328–2338 (2001).
pubmed: 11254590 pmcid: 98162 doi: 10.1128/IAI.69.4.2328-2338.2001
Wellford, S. A. et al. Mucosal plasma cells are required to protect the upper airway and brain from infection. Immunity 55, 2118–2134 (2022).
pubmed: 36137543 pmcid: 9649878 doi: 10.1016/j.immuni.2022.08.017
Darrah, P. A. et al. Boosting BCG with proteins or rAd5 does not enhance protection against tuberculosis in rhesus macaques. NPJ Vaccines 4, 21 (2019).
pubmed: 31149352 pmcid: 6538611 doi: 10.1038/s41541-019-0113-9
Darrah, P. A. et al. Aerosol vaccination with AERAS-402 elicits robust cellular immune responses in the lungs of rhesus macaques but fails to protect against high-dose Mycobacterium tuberculosis challenge. J. Immunol. 193, 1799–1811 (2014).
pubmed: 25024382 doi: 10.4049/jimmunol.1400676
Hokey, D. A. et al. A nonhuman primate toxicology and immunogenicity study evaluating aerosol delivery of AERAS-402/Ad35 vaccine: evidence for transient T cell responses in peripheral blood and robust sustained responses in the lungs. Hum. Vaccin. Immunother. 10, 2199–2210 (2014).
pubmed: 25424923 pmcid: 4896762 doi: 10.4161/hv.29108
Riou, C. et al. Escape from recognition of SARS-CoV-2 variant spike epitopes but overall preservation of T cell immunity. Sci. Transl. Med. 14, eabj6824 (2022).
pubmed: 34931886 pmcid: 9434381 doi: 10.1126/scitranslmed.abj6824
Choi, S. J. et al. T cell epitopes in SARS-CoV-2 proteins are substantially conserved in the Omicron variant. Cell. Mol. Immunol. 19, 447–448 (2022).
pubmed: 35043006 pmcid: 8764507 doi: 10.1038/s41423-022-00838-5
Sawicki, G. S., Chou, W., Raimundo, K., Trzaskoma, B. & Konstan, M. W. Randomized trial of efficacy and safety of dornase alfa delivered by eRapid nebulizer in cystic fibrosis patients. J. Cyst. Fibros. 14, 777–783 (2015).
pubmed: 25921451 doi: 10.1016/j.jcf.2015.04.003
Block, S. L., Yi, T., Sheldon, E., Dubovsky, F. & Falloon, J. A randomized, double-blind noninferiority study of quadrivalent live attenuated influenza vaccine in adults. Vaccine 29, 9391–9397 (2011).
pubmed: 21983154 doi: 10.1016/j.vaccine.2011.09.109
Chang, L. A. et al. A prefusion-stabilized RSV F subunit vaccine elicits B cell responses with greater breadth and potency than a postfusion F vaccine. Sci. Transl. Med. 14, eade0424 (2022).
pubmed: 36542692 pmcid: 11345946 doi: 10.1126/scitranslmed.ade0424
McLellan, J. S. et al. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342, 592–598 (2013).
pubmed: 24179220 pmcid: 4461862 doi: 10.1126/science.1243283
Pallesen, J. et al. Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. Proc. Natl Acad. Sci. USA 114, E7348–E7357 (2017).
pubmed: 28807998 pmcid: 5584442 doi: 10.1073/pnas.1707304114
Hawks, S. A. et al. Infectious SARS-CoV-2 is emitted in aerosol particles. mBio 12, e0252721 (2021).
pubmed: 34663099 doi: 10.1128/mBio.02527-21
Hartwell, B. L. et al. Intranasal vaccination with lipid-conjugated immunogens promotes antigen transmucosal uptake to drive mucosal and systemic immunity. Sci. Transl. Med. 14, eabn1413 (2022).
pubmed: 35857825 pmcid: 9835395 doi: 10.1126/scitranslmed.abn1413
Custers, J. et al. Vaccines based on replication incompetent Ad26 viral vectors: standardized template with key considerations for a risk/benefit assessment. Vaccine 39, 3081–3101 (2021).
pubmed: 33676782 pmcid: 7532807 doi: 10.1016/j.vaccine.2020.09.018
Wrapp, D. et al. Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation. Science 367, 1260–1263 (2020).
pubmed: 32075877 pmcid: 7164637 doi: 10.1126/science.abb2507
Hassett, K. J. et al. Optimization of lipid nanoparticles for intramuscular administration of mRNA vaccines. Mol. Ther. Nucleic Acids 15, 1–11 (2019).
pubmed: 30785039 pmcid: 6383180 doi: 10.1016/j.omtn.2019.01.013
Hsieh, C. L. et al. Structure-based design of prefusion-stabilized SARS-CoV-2 spikes. Science 369, 1501–1505 (2020).
pubmed: 32703906 doi: 10.1126/science.abd0826
Maizel, J. V. Jr., White, D. O. & Scharff, M. D. The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology 36, 115–125 (1968).
pubmed: 5669982 doi: 10.1016/0042-6822(68)90121-9
Corbett, K. S. et al. Evaluation of the mRNA-1273 vaccine against SARS-CoV-2 in nonhuman primates. N. Engl. J. Med. 383, 1544–1555 (2020).
pubmed: 32722908 doi: 10.1056/NEJMoa2024671
Song, K. et al. Genetic immunization in the lung induces potent local and systemic immune responses. Proc. Natl Acad. Sci. USA 107, 22213–22218 (2010).
pubmed: 21135247 pmcid: 3009829 doi: 10.1073/pnas.1015536108
Edara, V. V. et al. Infection- and vaccine-induced antibody binding and neutralization of the B.1.351 SARS-CoV-2 variant. Cell Host Microbe 29, 516–521 (2021).
pubmed: 33798491 pmcid: 7980225 doi: 10.1016/j.chom.2021.03.009
Lei, C., Yang, J., Hu, J. & Sun, X. On the calculation of TCID
pubmed: 32458296 doi: 10.1007/s12250-020-00230-5
Edara, V. V., Hudson, W. H., Xie, X., Ahmed, R. & Suthar, M. S. Neutralizing antibodies against SARS-CoV-2 variants after infection and vaccination. JAMA 325, 1896–1898 (2021).
pubmed: 33739374 pmcid: 7980146 doi: 10.1001/jama.2021.4388
Davis-Gardner, M. E. et al. Neutralization against BA.2.75.2, BQ.1.1, and XBB from mRNA bivalent booster. N. Engl. J. Med. 388, 183–185 (2022).
pubmed: 36546661 doi: 10.1056/NEJMc2214293
Edara, V. V. et al. Infection and vaccine-induced neutralizing-antibody responses to the SARS-CoV-2 B.1.617 variants. N. Engl. J. Med. 385, 664–666 (2021).
pubmed: 34233096 doi: 10.1056/NEJMc2107799
Vanderheiden, A. et al. Development of a rapid focus reduction neutralization test assay for measuring SARS-CoV-2 neutralizing antibodies. Curr. Protoc. Immunol. 131, e116 (2020).
pubmed: 33215858 pmcid: 7864545 doi: 10.1002/cpim.116
Katzelnick, L. C. et al. Viridot: an automated virus plaque (immunofocus) counter for the measurement of serological neutralizing responses with application to dengue virus. PLoS Negl. Trop. Dis. 12, e0006862 (2018).
pubmed: 30356267 pmcid: 6226209 doi: 10.1371/journal.pntd.0006862
Teng, I. T. et al. Molecular probes of spike ectodomain and its subdomains for SARS-CoV-2 variants, Alpha through Omicron. PLoS ONE 17, e0268767 (2022).
pubmed: 35609088 pmcid: 9129042 doi: 10.1371/journal.pone.0268767
Roederer, M., Nozzi, J. L. & Nason, M. C. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79, 167–174 (2011).
pubmed: 21265010 pmcid: 3072288 doi: 10.1002/cyto.a.21015
Donaldson, M. M., Kao, S. F. & Foulds, K. E. OMIP-052: an 18-color panel for measuring T
pubmed: 30681265 pmcid: 6414258 doi: 10.1002/cyto.a.23670

Auteurs

Matthew Gagne (M)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Barbara J Flynn (BJ)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Shayne F Andrew (SF)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Josue Marquez (J)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Dillon R Flebbe (DR)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Anna Mychalowych (A)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Evan Lamb (E)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Meredith E Davis-Gardner (ME)

Department of Pediatrics, Center for Childhood Infections and Vaccines of Children's Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA, USA.
Emory Vaccine Center, Emory University, Atlanta, GA, USA.
Emory National Primate Research Center, Atlanta, GA, USA.

Matthew R Burnett (MR)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Leonid A Serebryannyy (LA)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Bob C Lin (BC)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Zohar E Ziff (ZE)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Erin Maule (E)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Robin Carroll (R)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Mursal Naisan (M)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Yogita Jethmalani (Y)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Laurent Pessaint (L)

Bioqual, Inc., Rockville, MD, USA.

John-Paul M Todd (JM)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Nicole A Doria-Rose (NA)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

James Brett Case (JB)

Department of Medicine, Washington University School of Medicine, St. Louis, MO, USA.

Igor P Dmitriev (IP)

Department of Radiation Oncology, Washington University School of Medicine, St. Louis, MO, USA.

Elena A Kashentseva (EA)

Department of Radiation Oncology, Washington University School of Medicine, St. Louis, MO, USA.

Baoling Ying (B)

Department of Medicine, Washington University School of Medicine, St. Louis, MO, USA.

Alan Dodson (A)

Bioqual, Inc., Rockville, MD, USA.

Katelyn Kouneski (K)

Bioqual, Inc., Rockville, MD, USA.

Sijy O'Dell (S)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Bushra Wali (B)

Department of Pediatrics, Center for Childhood Infections and Vaccines of Children's Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA, USA.
Emory Vaccine Center, Emory University, Atlanta, GA, USA.
Emory National Primate Research Center, Atlanta, GA, USA.

Madison Ellis (M)

Department of Pediatrics, Center for Childhood Infections and Vaccines of Children's Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA, USA.
Emory Vaccine Center, Emory University, Atlanta, GA, USA.
Emory National Primate Research Center, Atlanta, GA, USA.

Sucheta Godbole (S)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Farida Laboune (F)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Amy R Henry (AR)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

I-Ting Teng (IT)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Danyi Wang (D)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Lingshu Wang (L)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Qiong Zhou (Q)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Serge Zouantchangadou (S)

Bioqual, Inc., Rockville, MD, USA.

Alex Van Ry (A)

Bioqual, Inc., Rockville, MD, USA.

Mark G Lewis (MG)

Bioqual, Inc., Rockville, MD, USA.

Hanne Andersen (H)

Bioqual, Inc., Rockville, MD, USA.

Peter D Kwong (PD)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

David T Curiel (DT)

Department of Radiation Oncology, Washington University School of Medicine, St. Louis, MO, USA.

Mario Roederer (M)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Martha C Nason (MC)

Biostatistics Research Branch, Division of Clinical Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Kathryn E Foulds (KE)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA.

Mehul S Suthar (MS)

Department of Pediatrics, Center for Childhood Infections and Vaccines of Children's Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA, USA.
Emory Vaccine Center, Emory University, Atlanta, GA, USA.
Emory National Primate Research Center, Atlanta, GA, USA.

Michael S Diamond (MS)

Department of Medicine, Washington University School of Medicine, St. Louis, MO, USA.
Department of Pathology & Immunology, Washington University School of Medicine, St. Louis, MO, USA.
Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO, USA.
The Andrew M. and Jane M. Bursky Center for Human Immunology & Immunotherapy Programs, Washington University School of Medicine, St. Louis, MO, USA.
Center for Vaccines & Immunity to Microbial Pathogens, Washington University School of Medicine, St. Louis, MO, USA.

Daniel C Douek (DC)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA. ddouek@mail.nih.gov.

Robert A Seder (RA)

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA. rseder@mail.nih.gov.

Classifications MeSH