دورية أكاديمية
Mucosal boosting enhances vaccine protection against SARS-CoV-2 in macaques.
العنوان: | Mucosal boosting enhances vaccine protection against SARS-CoV-2 in macaques. |
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المؤلفون: | McMahan K; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Wegmann F; Janssen Vaccines and Prevention, Leiden, Netherlands., Aid M; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Sciacca M; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Liu J; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Hachmann NP; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Miller J; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Jacob-Dolan C; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA.; Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, USA., Powers O; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Hope D; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Wu C; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Pereira J; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Murdza T; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Mazurek CR; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Hoyt A; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA., Boon ACM; Washington University School of Medicine, St Louis, MO, USA., Davis-Gardner M; Emory School of Medicine, Atlanta, GA, USA., Suthar MS; Emory School of Medicine, Atlanta, GA, USA., Martinot AJ; Tufts University Cummings School of Veterinary Medicine, Grafton, MA, USA., Boursiquot M; Bioqual, Rockville, MD, USA., Cook A; Bioqual, Rockville, MD, USA., Pessaint L; Bioqual, Rockville, MD, USA., Lewis MG; Bioqual, Rockville, MD, USA., Andersen H; Bioqual, Rockville, MD, USA., Tolboom J; Janssen Vaccines and Prevention, Leiden, Netherlands., Serroyen J; Janssen Vaccines and Prevention, Leiden, Netherlands., Solforosi L; Janssen Vaccines and Prevention, Leiden, Netherlands., Costes LMM; Janssen Vaccines and Prevention, Leiden, Netherlands., Zahn RC; Janssen Vaccines and Prevention, Leiden, Netherlands., Barouch DH; Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center, Boston, MA, USA. dbarouch@bidmc.harvard.edu.; Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, USA. dbarouch@bidmc.harvard.edu. |
المصدر: | Nature [Nature] 2024 Feb; Vol. 626 (7998), pp. 385-391. Date of Electronic Publication: 2023 Dec 14. |
نوع المنشور: | Comparative Study; Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Nature Publishing Group Country of Publication: England NLM ID: 0410462 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1476-4687 (Electronic) Linking ISSN: 00280836 NLM ISO Abbreviation: Nature Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Basingstoke : Nature Publishing Group Original Publication: London, Macmillan Journals ltd. |
مواضيع طبية MeSH: | COVID-19*/immunology , COVID-19*/prevention & control , COVID-19*/virology , COVID-19 Vaccines*/administration & dosage , COVID-19 Vaccines*/immunology , Immunity, Mucosal*/immunology , Immunization, Secondary*/methods , Macaca mulatta*/immunology , Macaca mulatta*/virology , SARS-CoV-2*/classification , SARS-CoV-2*/immunology, Animals ; Humans ; Administration, Intranasal ; Antibodies, Neutralizing/biosynthesis ; Antibodies, Neutralizing/immunology ; Antibodies, Viral/biosynthesis ; Antibodies, Viral/immunology ; CD4-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/immunology ; Cytokines/immunology ; Immunoglobulin A/immunology ; Immunoglobulin G/immunology ; Injections, Intramuscular ; Killer Cells, Natural/immunology ; Lung/immunology ; mRNA Vaccines/administration & dosage ; mRNA Vaccines/immunology ; Trachea/immunology ; Trachea/virology |
مستخلص: | A limitation of current SARS-CoV-2 vaccines is that they provide minimal protection against infection with current Omicron subvariants 1,2 , although they still provide protection against severe disease. Enhanced mucosal immunity may be required to block infection and onward transmission. Intranasal administration of current vaccines has proven inconsistent 3-7 , suggesting that alternative immunization strategies may be required. Here we show that intratracheal boosting with a bivalent Ad26-based SARS-CoV-2 vaccine results in substantial induction of mucosal humoral and cellular immunity and near-complete protection against SARS-CoV-2 BQ.1.1 challenge. A total of 40 previously immunized rhesus macaques were boosted with a bivalent Ad26 vaccine by the intramuscular, intranasal and intratracheal routes, or with a bivalent mRNA vaccine by the intranasal route. Ad26 boosting by the intratracheal route led to a substantial expansion of mucosal neutralizing antibodies, IgG and IgA binding antibodies, and CD8 + and CD4 + T cell responses, which exceeded those induced by Ad26 boosting by the intramuscular and intranasal routes. Intratracheal Ad26 boosting also led to robust upregulation of cytokine, natural killer, and T and B cell pathways in the lungs. After challenge with a high dose of SARS-CoV-2 BQ.1.1, intratracheal Ad26 boosting provided near-complete protection, whereas the other boosting strategies proved less effective. Protective efficacy correlated best with mucosal humoral and cellular immune responses. These data demonstrate that these immunization strategies induce robust mucosal immunity, suggesting the feasibility of developing vaccines that block respiratory viral infections. (© 2023. The Author(s).) |
References: | Lin, D. Y. et al. Durability of bivalent boosters against Omicron subvariants. N. Engl. J. Med. https://doi.org/10.1056/NEJMc2302462 (2023). Boucau, J. et al. Duration of shedding of culturable virus in SARS-CoV-2 Omicron (BA.1) infection. N. Engl. J. Med. 387, 275–277 (2022). (PMID: 10.1056/NEJMc220209235767428) 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). (PMID: 10.1016/j.ebiom.2022.104298362293429550199) Cokaric Brdovcak, M. et al. ChAdOx1-S adenoviral vector vaccine applied intranasally elicits superior mucosal immunity compared to the intramuscular route of vaccination. Eur. J. Immunol. 52, 936–945 (2022). (PMID: 10.1002/eji.202249823353047419087383) Feng, L. et al. An adenovirus-vectored COVID-19 vaccine confers protection from SARS-COV-2 challenge in rhesus macaques. Nat. Commun. 11, 4207 (2020). (PMID: 10.1038/s41467-020-18077-5328269247442803) van Doremalen, N. et al. Intranasal ChAdOx1 nCoV-19/AZD1222 vaccination reduces viral shedding after SARS-CoV-2 D614G challenge in preclinical models. Sci. Transl. Med. 13, eabh0755 (2021). (PMID: 10.1126/scitranslmed.abh0755343158269267380) 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). (PMID: 10.1016/j.xcrm.2021.100230337541477969912) Tenforde, M. W. et al. Early estimates of bivalent mRNA vaccine effectiveness in preventing COVID-19-associated emergency department or urgent care encounters and hospitalizations among immunocompetent adults—VISION Network, nine states, September–November 2022. MMWR Morb. Mortal. Wkly Rep. 71, 1616–1624 (2022). (PMID: 10.15585/mmwr.mm715152e1365804309812442) Surie, D. et al. Early estimates of bivalent mRNA vaccine effectiveness in preventing COVID-19-associated hospitalization among immunocompetent adults aged ≥65 years—IVY Network, 18 states, September 8–November 30, 2022. MMWR Morb. Mortal. Wkly Rep. 71, 1625–1630 (2022). (PMID: 10.15585/mmwr.mm715152e2365804249812444) Collier, A. Y. et al. Characterization of immune responses in fully vaccinated individuals after breakthrough infection with the SARS-CoV-2 Delta variant. Sci. Transl. Med. 14, eabn6150 (2022). (PMID: 10.1126/scitranslmed.abn615035258323) Tang, J. et al. Respiratory mucosal immunity against SARS-CoV-2 after mRNA vaccination. Sci. Immunol. 7, eadd4853 (2022). (PMID: 10.1126/sciimmunol.add485335857583) Moore, K. A. et al. A research and development (R&D) roadmap for broadly protective coronavirus vaccines: a pandemic preparedness strategy. Vaccine 41, 2101–2112 (2023). (PMID: 10.1016/j.vaccine.2023.02.032368708749941884) Becerra, X. & Jha, A. Project NextGen—defeating SARS-CoV-2 and preparing for the next pandemic. N. Engl. J. Med. 389, 773–775 (2023). (PMID: 10.1056/NEJMp230786737494477) Sadoff, J. et al. Safety and efficacy of single-dose Ad26.COV2.S vaccine against COVID-19. N. Engl. J. Med. 384, 2187–2201 (2021). (PMID: 10.1056/NEJMoa210154433882225) Sadoff, J. et al. Interim results of a phase 1-2a trial of Ad26.COV2.S COVID-19 vaccine. N. Engl. J. Med. 384, 1824–1835 (2021). (PMID: 10.1056/NEJMoa203420133440088) Stephenson, K. E. et al. Immunogenicity of the Ad26.COV2.S Vaccine for COVID-19. JAMA 325, 1535–1544 (2021). (PMID: 10.1001/jama.2021.364533704352) Mercado, N. B. et al. Single-shot Ad26 vaccine protects against SARS-CoV-2 in rhesus macaques. Nature 586, 583–588 (2020). (PMID: 10.1038/s41586-020-2607-z327312577581548) He, X. et al. A homologous or variant booster vaccine after Ad26.COV2.S immunization enhances SARS-CoV-2-specific immune responses in rhesus macaques. Sci. Transl. Med. 14, eabm4996 (2022). (PMID: 10.1126/scitranslmed.abm4996351917699802654) 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). (PMID: 10.1038/s41467-023-37715-23702914110080532) Zou, J. et al. Neutralization of BA.4-BA.5, BA.4.6, BA.2.75.2, BQ.1.1, and XBB.1 with bivalent vaccine. N. Engl. J. Med. 388, 854–857 (2023). (PMID: 10.1056/NEJMc221491636734885) Collier, A. Y. et al. Immunogenicity of BA.5 bivalent mRNA vaccine boosters. N. Engl. J. Med. 388, 565–567 (2023). (PMID: 10.1056/NEJMc221394836630611) Wang, Q. et al. Antibody response to Omicron BA.4-BA.5 bivalent booster. N. Engl. J. Med. 388, 567–569 (2023). (PMID: 10.1056/NEJMc221390736630643) Yu, J. et al. Deletion of the SARS-CoV-2 spike cytoplasmic tail increases infectivity in pseudovirus neutralization assays. J. Virol. https://doi.org/10.1128/JVI.00044-21 (2021). Polinski, J. M. et al. Durability of the single-dose Ad26.COV2.S vaccine in the prevention of COVID-19 infections and hospitalizations in the US before and during the Delta variant surge. JAMA Netw. Open 5, e222959 (2022). (PMID: 10.1001/jamanetworkopen.2022.2959352979698931562) Jacob-Dolan, C. et al. Coronavirus-specific antibody cross reactivity in rhesus macaques following SARS-CoV-2 vaccination and infection. J. Virol. https://doi.org/10.1128/JVI.00117-21 (2021). Liu, J. et al. Vaccines elicit highly conserved cellular immunity to SARS-CoV-2 Omicron. Nature 603, 493–496 (2022). (PMID: 10.1038/s41586-022-04465-y351023128930761) Dagotto, G. et al. Comparison of subgenomic and total RNA in SARS-CoV-2 challenged rhesus macaques. J. Virol. https://doi.org/10.1128/JVI.02370-20 (2021). Yu, J. et al. Protective efficacy of Ad26.COV2.S against SARS-CoV-2 B.1.351 in macaques. Nature 596, 423–427 (2021). (PMID: 10.1038/s41586-021-03732-8341619618373608) Chandrashekar, A. et al. Vaccine protection against the SARS-CoV-2 Omicron variant in macaques. Cell 185, 1549–1555 (2022). (PMID: 10.1016/j.cell.2022.03.024354274778926910) Jeyanathan, V. et al. Differential biodistribution of adenoviral-vectored vaccine following intranasal and endotracheal deliveries leads to different immune outcomes. Front. Immunol. 13, 860399 (2022). (PMID: 10.3389/fimmu.2022.860399357577539231681) Jeyanathan, M. et al. Aerosol delivery, but not intramuscular injection, of adenovirus-vectored tuberculosis vaccine induces respiratory-mucosal immunity in humans. JCI Insight 7, e155655 (2022). (PMID: 10.1172/jci.insight.155655349904088855837) Ivanov, V. et al. Intranasal and intrapulmonary vaccination with an M protein-deficient respiratory syncytial virus (RSV) vaccine improves clinical signs and reduces viral replication in infant baboons after an RSV challenge infection. Vaccine 39, 4063–4071 (2021). (PMID: 10.1016/j.vaccine.2021.06.01334140172) Wu, L. et al. Quantitative comparison of three widely-used pulmonary administration methods in vivo with radiolabeled inhalable nanoparticles. Eur. J. Pharm. Biopharm. 152, 108–115 (2020). (PMID: 10.1016/j.ejpb.2020.05.00432437751) Xu, F. et al. Safety, mucosal and systemic immunopotency of an aerosolized adenovirus-vectored vaccine against SARS-CoV-2 in rhesus macaques. Emerg. Microbes Infect. 11, 438–441 (2022). (PMID: 10.1080/22221751.2022.2030199350946728803102) Li, J. X. et al. Safety, immunogenicity and protection of heterologous boost with an aerosolised Ad5-nCoV after two-dose inactivated COVID-19 vaccines in adults: a multicentre, open-label phase 3 trial. Lancet Infect. Dis. 23, 1143–1152 (2023). (PMID: 10.1016/S1473-3099(23)00350-X37352880) Yu, J. et al. Ad26.COV2.S and SARS-CoV-2 spike protein ferritin nanoparticle vaccine protect against SARS-CoV-2 Omicron BA.5 challenge in macaques. Cell Rep. Med. 4, 101018 (2023). (PMID: 10.1016/j.xcrm.2023.1010183702374610040355) Yu, J. et al. Protection against SARS-CoV-2 Omicron BA.1 variant challenge in macaques by prime-boost vaccination with Ad26.COV2.S and SpFN. Sci. Adv. 8, eade4433 (2022). (PMID: 10.1126/sciadv.ade4433364175259683731) 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). (PMID: 10.1016/j.cell.2022.03.038354470728947944) |
معلومات مُعتمدة: | INV-027406 United States GATES Bill & Melinda Gates Foundation; U01 CA260476 United States CA NCI NIH HHS |
المشرفين على المادة: | 0 (Antibodies, Neutralizing) 0 (Antibodies, Viral) 0 (COVID-19 Vaccines) 0 (Cytokines) 0 (Immunoglobulin A) 0 (Immunoglobulin G) 0 (mRNA Vaccines) |
SCR Organism: | SARS-CoV-2 variants |
تواريخ الأحداث: | Date Created: 20231214 Date Completed: 20240213 Latest Revision: 20240213 |
رمز التحديث: | 20240213 |
مُعرف محوري في PubMed: | PMC10849944 |
DOI: | 10.1038/s41586-023-06951-3 |
PMID: | 38096903 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1476-4687 |
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DOI: | 10.1038/s41586-023-06951-3 |