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The development of mucosal vaccines has been limited by the poor efficiency of antigen display and the risk of adjuvants. Here, we report an engineered yeast vaccine integrating a well-displayed antigen with an intrinsic adjuvant for the development of innate and adaptive immunity to the intestinal mucosa. Compared with antigen-secretory yeast, antigen-anchored yeast significantly activated gut dendritic cells (DCs) and promoted follicular helper T (Tfh) cell differentiation, thereby amplifying the immune response by the interaction with Tfh-B cells. Consequently, oral vaccination of SARS-CoV-2 receptor-binding domain (RBD)-anchored yeast triggered stronger RBD-specific IgA-neutralizing effects, providing potential adaptive protections. Given its corresponding impact on the functionality of both innate and adaptive mucosal responses, the proposed RBD-anchored yeast outperformed RBD-anchored bacteria and biomimetic nanovaccine in the production of RBD-specific IgA and IgG. Together, these results revealed how antigen-displaying patterns could be modulated to elicit intestinal mucosal immunity and demonstrated the translational potential of antigen-displayed yeast for effective mucosal protection.<\/jats:p>","DOI":"10.1021\/acsnano.4c14690","type":"journal-article","created":{"date-parts":[[2025,3,13]],"date-time":"2025-03-13T21:57:51Z","timestamp":1741903071000},"page":"10841-10853","source":"Crossref","is-referenced-by-count":13,"title":["Orally\nAntigen-Engineered Yeast Vaccine Elicits Robust\nIntestinal Mucosal Immunity"],"prefix":"10.1021","volume":"19","author":[{"given":"Xuenian","family":"Chen","sequence":"first","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tongfei","family":"Shi","sequence":"additional","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]},{"name":"South China University of Technology, Guangzhou International Campus , , , ,","place":["Guangzhou, Guangdong, P.R. China, 511442"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1054-8806","authenticated-orcid":true,"given":"Fangman","family":"Chen","sequence":"additional","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaochun","family":"Xie","sequence":"additional","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Fang","sequence":"additional","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziping","family":"Wu","sequence":"additional","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Liu","sequence":"additional","affiliation":[{"name":"University of Chinese Academy of Sciences , , ,","place":["Beijing, P.R. China, 101408"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yubiao","family":"Huang","sequence":"additional","affiliation":[{"name":"University of Chinese Academy of Sciences , , ,","place":["Beijing, P.R. China, 101408"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qin","family":"Wang","sequence":"additional","affiliation":[{"name":"Binzhou Medical University , , , ,","place":["Yantai, Shandong, P.R. China, 264003"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5040-9793","authenticated-orcid":true,"given":"Guangjun","family":"Nie","sequence":"additional","affiliation":[{"name":"University of Chinese Academy of Sciences , , ,","place":["Beijing, P.R. China, 101408"]},{"name":"National Center for Nanoscience and Technology , , ,","place":["Beijing, P.R. China, 100190"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4625-4132","authenticated-orcid":true,"given":"Jiaqi","family":"Xu","sequence":"additional","affiliation":[{"name":"University of Chinese Academy of Sciences , , ,","place":["Beijing, P.R. China, 101408"]},{"name":"National Center for Nanoscience and Technology , , ,","place":["Beijing, P.R. China, 100190"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5243-042X","authenticated-orcid":true,"given":"Dan","family":"Shao","sequence":"additional","affiliation":[{"name":"South China University of Technology , , , ,","place":["Guangzhou, Guangdong, P.R. China, 510006"]},{"name":"South China University of Technology, Guangzhou International Campus , , , ,","place":["Guangzhou, Guangdong, P.R. China, 511442"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2025,3,13]]},"reference":[{"key":"2026081813162794200_cit1","doi-asserted-by":"publisher","DOI":"10.34133\/research.0099","article-title":"Real-World COVID-19 Vaccine Protection\nRates against Infection in the Delta and Omicron Eras","volume":"6","author":"Zhu","year":"2023","journal-title":"Research"},{"issue":"7610","key":"2026081813162794200_cit2","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1038\/nature18848","article-title":"The microbiota in\nadaptive immune homeostasis and disease","volume":"535","author":"Honda","year":"2016","journal-title":"Nature"},{"issue":"3","key":"2026081813162794200_cit3","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1038\/nri2710","article-title":"Immune\nadaptations that maintain homeostasis with the\nintestinal microbiota","volume":"10","author":"Hooper","year":"2010","journal-title":"Nat. Rev. Immunol."},{"issue":"3","key":"2026081813162794200_cit4","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1038\/nri.2015.17","article-title":"Mucosal immunity\nto pathogenic intestinal bacteria","volume":"16","author":"Perez-Lopez","year":"2016","journal-title":"Nat. Rev.\nImmunol."},{"issue":"3","key":"2026081813162794200_cit5","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1093\/infdis\/151.3.420","article-title":"Oral poliovirus\nvaccine: history of its development and use and current challenge\nto eliminate poliomyelitis from the world","volume":"151","author":"Sabin","year":"1985","journal-title":"J.\nInfect. Dis."},{"key":"2026081813162794200_cit6","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.addr.2015.03.007","article-title":"Delivery strategies to enhance oral\nvaccination against\nenteric infections","volume":"91","author":"Davitt","year":"2015","journal-title":"Adv. Drug Delivery Rev."},{"issue":"7","key":"2026081813162794200_cit7","doi-asserted-by":"publisher","first-page":"480","DOI":"10.1007\/s13238-015-0164-2","article-title":"Intranasal and oral vaccination with\nprotein-based antigens: advantages, challenges and formulation strategies","volume":"6","author":"Wang","year":"2015","journal-title":"Protein Cell"},{"issue":"4","key":"2026081813162794200_cit8","doi-asserted-by":"publisher","first-page":"236","DOI":"10.1038\/s41577-021-00583-2","article-title":"Mucosal vaccines - fortifying the\nfrontiers","volume":"22","author":"Lavelle","year":"2022","journal-title":"Nat. Rev. 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Lett."},{"issue":"2","key":"2026081813162794200_cit18","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1016\/j.immuni.2021.12.002","article-title":"Inhibition of transcription\nfactor NFAT activity in activated platelets enhances their aggregation\nand exacerbates gram-negative bacterial septicemia","volume":"55","author":"Poli","year":"2022","journal-title":"Immunity"},{"issue":"6","key":"2026081813162794200_cit19","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1038\/s41579-021-00661-1","article-title":"Biology and\nevolution of bacterial toxin-antitoxin systems","volume":"20","author":"Jure\u0307nas","year":"2022","journal-title":"Nat. Rev. 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Biol. Macromol."},{"issue":"6851","key":"2026081813162794200_cit23","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1038\/35092620","article-title":"Immune recognition.\nA new receptor for beta-glucans","volume":"413","author":"Brown","year":"2001","journal-title":"Nature"},{"issue":"1","key":"2026081813162794200_cit24","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-27750-2","article-title":"Yeast-derived nanoparticles\nremodel the immunosuppressive microenvironment\nin tumor and tumor-draining lymph nodes to suppress tumor growth","volume":"13","author":"Xu","year":"2022","journal-title":"Nat. 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Natl. Acad. Sci. U.S.A."},{"issue":"2","key":"2026081813162794200_cit31","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1038\/nrmicro1087","article-title":"The humanization of N-glycosylation pathways in yeast","volume":"3","author":"Wildt","year":"2005","journal-title":"Nat. Rev. Microbiol."},{"issue":"5637","key":"2026081813162794200_cit32","doi-asserted-by":"publisher","first-page":"1244","DOI":"10.1126\/science.1088166","article-title":"Production\nof complex human glycoproteins in yeast","volume":"301","author":"Hamilton","year":"2003","journal-title":"Science"},{"issue":"51","key":"2026081813162794200_cit33","doi-asserted-by":"publisher","DOI":"10.1002\/adma.202104139","article-title":"Engineering Nano- and Microparticles as Oral Delivery\nVehicles to Promote Intestinal Lymphatic Drug Transport","volume":"33","author":"Miao","year":"2021","journal-title":"Adv. Mater."},{"issue":"7807","key":"2026081813162794200_cit34","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1038\/s41586-020-2179-y","article-title":"Structural basis of\nreceptor recognition by SARS-CoV-2","volume":"581","author":"Shang","year":"2020","journal-title":"Nature"},{"key":"2026081813162794200_cit35","doi-asserted-by":"publisher","DOI":"10.34133\/research.0124","article-title":"SARS-CoV-2 RBD and Its Variants Can Induce Platelet Activation and\nClearance: Implications for Antibody Therapy and Vaccinations against\nCOVID-19","volume":"6","author":"Ma","year":"2023","journal-title":"Research"},{"key":"2026081813162794200_cit36","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1016\/j.jconrel.2022.04.032","article-title":"Yeast as carrier for drug delivery and vaccine construction","volume":"346","author":"Tan","year":"2022","journal-title":"J. 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Commun."},{"key":"2026081813162794200_cit39","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2023.1150412","article-title":"Yeast oral\nvaccines against infectious diseases","volume":"14","author":"Austriaco","year":"2023","journal-title":"Front\nMicrobiol."},{"issue":"3","key":"2026081813162794200_cit40","doi-asserted-by":"publisher","DOI":"10.3390\/biom13030441","article-title":"Industrial\nProduction of Proteins with Pichia pastoris-Komagataella phaffii","volume":"13","author":"Barone","year":"2023","journal-title":"Biomolecules"},{"issue":"2","key":"2026081813162794200_cit41","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1021\/acssynbio.5b00199","article-title":"A Toolbox of Diverse\nPromoters Related to Methanol Utilization: Functionally Verified Parts\nfor Heterologous Pathway Expression in Pichia pastoris","volume":"5","author":"Vogl","year":"2016","journal-title":"ACS Synth. Biol."},{"issue":"1","key":"2026081813162794200_cit42","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1006\/prep.2000.1229","article-title":"High-level production of recombinant fungal endo-beta-1,4-xylanase\nin the methylotrophic yeast Pichia pastoris","volume":"19","author":"Berrin","year":"2000","journal-title":"Protein Expression Purif."},{"issue":"7830","key":"2026081813162794200_cit43","doi-asserted-by":"publisher","first-page":"572","DOI":"10.1038\/s41586-020-2599-8","article-title":"A vaccine targeting the RBD of the S protein of SARS-CoV-2 induces\nprotective immunity","volume":"586","author":"Yang","year":"2020","journal-title":"Nature"},{"issue":"42","key":"2026081813162794200_cit44","doi-asserted-by":"publisher","DOI":"10.1126\/sciimmunol.aax1027","article-title":"Early-life\nprogramming of mesenteric lymph node stromal cell identity by the\nlymphotoxin pathway regulates adult mucosal immunity","volume":"4","author":"Li","year":"2019","journal-title":"Sci. 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Immunol."},{"issue":"1","key":"2026081813162794200_cit46","doi-asserted-by":"publisher","DOI":"10.1038\/s41541-021-00370-z","article-title":"Codominant\nIgG and IgA expression with minimal vaccine mRNA in milk of BNT162b2\nvaccinees","volume":"6","author":"Low","year":"2021","journal-title":"npj Vaccines"},{"issue":"6553","key":"2026081813162794200_cit47","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1126\/science.abg9857","article-title":"Scent of a vaccine","volume":"373","author":"Lund","year":"2021","journal-title":"Science"},{"issue":"4","key":"2026081813162794200_cit48","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1038\/s43018-022-00356-3","article-title":"Cell type and gene\nexpression deconvolution with BayesPrism enables Bayesian integrative\nanalysis across bulk and single-cell RNA sequencing in oncology","volume":"3","author":"Chu","year":"2022","journal-title":"Nat. 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