{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,18]],"date-time":"2026-03-18T21:55:24Z","timestamp":1773870924003,"version":"3.50.1"},"reference-count":82,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"31","content-domain":{"domain":["www.science.org"],"crossmark-restriction":true},"short-container-title":["Sci. Adv."],"published-print":{"date-parts":[[2023,8,4]]},"abstract":"<jats:p>Since the initial spread of severe acute respiratory syndrome coronavirus 2 infection, several viral variants have emerged and represent a major challenge for immune control, particularly in the context of vaccination. We evaluated the quantity, quality, and persistence of immunoglobulin G (IgG) and IgA in individuals who received two or three doses of messenger RNA (mRNA) vaccines, compared with previously infected vaccinated individuals. We show that three doses of mRNA vaccine were required to match the humoral responses of preinfected vaccinees. Given the importance of antibody-dependent cell-mediated immunity against viral infections, we also measured the capacity of IgG to recognize spike variants expressed on the cell surface and found that cross-reactivity was also strongly improved by repeated vaccination. Last, we report low levels of CXCL13, a surrogate marker of germinal center activation and formation, in vaccinees both after two and three doses compared with preinfected individuals, providing a potential explanation for the short duration and low quality of Ig induced.<\/jats:p>","DOI":"10.1126\/sciadv.adg2122","type":"journal-article","created":{"date-parts":[[2023,8,4]],"date-time":"2023-08-04T17:58:23Z","timestamp":1691171903000},"update-policy":"https:\/\/doi.org\/10.34133\/aaas_crossmark","source":"Crossref","is-referenced-by-count":6,"title":["Repetitive mRNA vaccination is required to improve the quality of broad-spectrum anti\u2013SARS-CoV-2 antibodies in the absence of CXCL13"],"prefix":"10.1126","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0009-0006-3411-1835","authenticated-orcid":true,"given":"Marne","family":"Azarias Da Silva","sequence":"first","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7981-9163","authenticated-orcid":true,"given":"Pierre","family":"Nioche","sequence":"additional","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."},{"name":"Structural and Molecular Analysis Platform, BioMedTech Facilities INSERM US36-CNRS UMS2009, Universit\u00e9 Paris Cit\u00e9, Paris, France."}]},{"given":"Calaiselvy","family":"Soudaramourty","sequence":"additional","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."}]},{"given":"Anne","family":"Bull-Maurer","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Tours, INSERM, UMR1259 MAVIVH, Tours, France."}]},{"given":"Mounira","family":"Tiouajni","sequence":"additional","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."},{"name":"Structural and Molecular Analysis Platform, BioMedTech Facilities INSERM US36-CNRS UMS2009, Universit\u00e9 Paris Cit\u00e9, Paris, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3779-6666","authenticated-orcid":true,"given":"Dechuan","family":"Kong","sequence":"additional","affiliation":[{"name":"Joint Research Center for Human Retrovirus Infection, Kumamoto University, Kumamoto, Japan."},{"name":"Department of Pathology, National Institute of Infectious Diseases, Tokyo, Japan."}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8502-4068","authenticated-orcid":true,"given":"Ouafa","family":"Zghidi-Abouzid","sequence":"additional","affiliation":[{"name":"CHU de Qu\u00e9bec-Universit\u00e9 Laval Research Center, Qu\u00e9bec City, Qu\u00e9bec, Canada."}]},{"given":"Morgane","family":"Picard","sequence":"additional","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7561-5347","authenticated-orcid":true,"given":"Ana","family":"Mendes-Frias","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5636-575X","authenticated-orcid":true,"given":"Andr\u00e9","family":"Santa-Cruz","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."},{"name":"Department of Internal Medicine, Hospital of Braga, Braga, Portugal."}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5683-3181","authenticated-orcid":true,"given":"Alexandre","family":"Carvalho","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."},{"name":"Department of Internal Medicine, Hospital of Braga, Braga, Portugal."}]},{"given":"Carlos","family":"Capela","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."},{"name":"Department of Internal Medicine, Hospital of Braga, Braga, Portugal."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8204-4888","authenticated-orcid":true,"given":"Jorge","family":"Pedrosa","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4684-4183","authenticated-orcid":true,"given":"Ant\u00f3nio Gil","family":"Castro","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."}]},{"given":"Paul","family":"Loubet","sequence":"additional","affiliation":[{"name":"Service des Maladies Infectieuses et Tropicales, CHU de N\u00eemes, N\u00eemes, France."}]},{"given":"Albert","family":"Sotto","sequence":"additional","affiliation":[{"name":"Service des Maladies Infectieuses et Tropicales, CHU de N\u00eemes, N\u00eemes, France."}]},{"given":"Laurent","family":"Muller","sequence":"additional","affiliation":[{"name":"Service de R\u00e9animation Chirugicale, CHU de N\u00eemes, N\u00eemes, France."}]},{"given":"Jean-Yves","family":"Lefrant","sequence":"additional","affiliation":[{"name":"Service de R\u00e9animation Chirugicale, CHU de N\u00eemes, N\u00eemes, France."}]},{"given":"Claire","family":"Roger","sequence":"additional","affiliation":[{"name":"Service de R\u00e9animation Chirugicale, CHU de N\u00eemes, N\u00eemes, France."}]},{"given":"Pierre-G\u00e9raud","family":"Claret","sequence":"additional","affiliation":[{"name":"Urgences M\u00e9dico-Chirugicales Hospitalisation, CHU de N\u00eemes, N\u00eemes, France."}]},{"given":"Sandra","family":"Duvnjak","sequence":"additional","affiliation":[{"name":"Service de G\u00e9rontologie et Pr\u00e9vention du Vieillissement, CHU de N\u00eemes, N\u00eemes, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6587-1876","authenticated-orcid":true,"given":"Tu-Anh","family":"Tran","sequence":"additional","affiliation":[{"name":"Service de P\u00e9diatrie, CHU de N\u00eemes, N\u00eemes, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2625-5322","authenticated-orcid":true,"given":"Kenzo","family":"Tokunaga","sequence":"additional","affiliation":[{"name":"Department of Pathology, National Institute of Infectious Diseases, Tokyo, Japan."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9270-2717","authenticated-orcid":true,"given":"Ricardo","family":"Silvestre","sequence":"additional","affiliation":[{"name":"Life and Health Sciences Research Institute (ICVS), School of Health Sciences, University of Minho, Braga, Portugal."},{"name":"ICVS\/3B\u2019s-PT Government Associate Laboratory, Braga\/Guimar\u00e3es, Portugal."}]},{"given":"Pierre","family":"Corbeau","sequence":"additional","affiliation":[{"name":"Institut de G\u00e9n\u00e9tique Humaine, UMR9002 CNRS-Universit\u00e9 de Montpellier, Montpellier, France."},{"name":"Laboratoire d\u2019Immunologie, CHU de N\u00eemes, N\u00eemes, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9193-7696","authenticated-orcid":true,"given":"Fabrizio","family":"Mammano","sequence":"additional","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."},{"name":"Universit\u00e9 de Tours, INSERM, UMR1259 MAVIVH, Tours, France."}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9432-8044","authenticated-orcid":true,"given":"J\u00e9r\u00f4me","family":"Estaquier","sequence":"additional","affiliation":[{"name":"INSERM-U1124, Universit\u00e9 Paris Cit\u00e9, Paris, France."},{"name":"CHU de Qu\u00e9bec-Universit\u00e9 Laval Research Center, Qu\u00e9bec City, Qu\u00e9bec, Canada."}]}],"member":"221","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-020-2012-7"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2020.09.037"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2021.02.003"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.immuni.2022.04.003"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.12.046"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.03.028"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1010022"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMc2107799"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMc2119358"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.12.033"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.abn7591"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-04399-5"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.medj.2022.02.006"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-04388-0"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-04386-2"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-04389-z"},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.12.032"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-04385-3"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.02.026"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-21336-8"},{"key":"e_1_3_2_22_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41419-022-05190-0"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41418-022-00936-x"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abn9243"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(21)00183-5"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.immuni.2022.01.001"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2021.19623"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1093\/cid\/ciac262"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa2118946"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abd2223"},{"key":"e_1_3_2_31_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmv.27058"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa2035389"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa2034577"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1001\/jama.2021.15125"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.lanepe.2021.100208"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41564-021-00947-3"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.abm3425"},{"key":"e_1_3_2_38_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-021-01377-8"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1128\/CDLI.6.5.725-728.1999"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1096\/fasebj.8.11.8070632"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1520112113"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2017.01104"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41385-019-0174-0"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-020-0897-1"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1126\/sciimmunol.abe0240"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abd5487"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.0105-2896.2005.00283.x"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abc3103"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-03398-2"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.abn8897"},{"key":"e_1_3_2_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.06.005"},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2021.03.005"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2021.03.029"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.abg5268"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-05053-w"},{"key":"e_1_3_2_56_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMc2207519"},{"key":"e_1_3_2_57_2","first-page":"113","article-title":"Are IgG antibody avidity assays useful in the diagnosis of infectious diseases? A review","volume":"87","author":"Guti\u00e9rrez J.","year":"1996","unstructured":"J.\u00a0Guti\u00e9rrez, C.\u00a0Maroto, Are IgG antibody avidity assays useful in the diagnosis of infectious diseases? A review. Microbios 87, 113\u2013121 (1996).","journal-title":"Microbios"},{"key":"e_1_3_2_58_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-065X.1997.tb00958.x"},{"key":"e_1_3_2_59_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.coi.2011.03.004"},{"key":"e_1_3_2_60_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.290.5489.89"},{"key":"e_1_3_2_61_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20181216"},{"key":"e_1_3_2_62_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa2201570"},{"key":"e_1_3_2_63_2","doi-asserted-by":"publisher","DOI":"10.1111\/imr.13014"},{"key":"e_1_3_2_64_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abi8961"},{"key":"e_1_3_2_65_2","doi-asserted-by":"publisher","DOI":"10.1038\/mt.2008.200"},{"key":"e_1_3_2_66_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.iy.12.040194.005015"},{"key":"e_1_3_2_67_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-03738-2"},{"key":"e_1_3_2_68_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-022-04527-1"},{"key":"e_1_3_2_69_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1004096"},{"key":"e_1_3_2_70_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005393"},{"key":"e_1_3_2_71_2","doi-asserted-by":"crossref","unstructured":"D.\u00a0H.\u00a0Katz B.\u00a0Benacerraf in Advances in Immunology F.\u00a0J.\u00a0Dixon H.\u00a0G.\u00a0Kunkel Eds. (Academic Press 1972) vol. 15 pp.\u00a01\u201394.","DOI":"10.1016\/S0065-2776(08)60683-5"},{"key":"e_1_3_2_72_2","doi-asserted-by":"publisher","DOI":"10.1002\/eji.1830010104"},{"key":"e_1_3_2_73_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0809403105"},{"key":"e_1_3_2_74_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.immuni.2009.04.016"},{"key":"e_1_3_2_75_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2022.03.018"},{"key":"e_1_3_2_76_2","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jiab300"},{"key":"e_1_3_2_77_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2021.108728"},{"key":"e_1_3_2_78_2","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20131244"},{"key":"e_1_3_2_79_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1002634"},{"key":"e_1_3_2_80_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2111400119"},{"key":"e_1_3_2_81_2","doi-asserted-by":"publisher","DOI":"10.1126\/sciimmunol.abn8590"},{"key":"e_1_3_2_82_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abn7842"},{"key":"e_1_3_2_83_2","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abm2311"}],"container-title":["Science Advances"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/sciadv.adg2122","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,9]],"date-time":"2024-01-09T22:19:38Z","timestamp":1704838778000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/sciadv.adg2122"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,4]]},"references-count":82,"journal-issue":{"issue":"31","published-print":{"date-parts":[[2023,8,4]]}},"alternative-id":["10.1126\/sciadv.adg2122"],"URL":"https:\/\/doi.org\/10.1126\/sciadv.adg2122","relation":{},"ISSN":["2375-2548"],"issn-type":[{"value":"2375-2548","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,4]]},"assertion":[{"value":"2022-12-09","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-07-05","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-08-04","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"eadg2122"}}