{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T10:38:29Z","timestamp":1787567909770,"version":"build-2736575974"},"reference-count":88,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2024,12,18]],"date-time":"2024-12-18T00:00:00Z","timestamp":1734480000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2024,12,18]],"date-time":"2024-12-18T00:00:00Z","timestamp":1734480000000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2024,12,18]],"date-time":"2024-12-18T00:00:00Z","timestamp":1734480000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["679403"],"award-info":[{"award-number":["679403"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"publisher","award":["310030_197941"],"award-info":[{"award-number":["310030_197941"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elifesciences.org"],"crossmark-restriction":false},"short-container-title":[],"accepted":{"date-parts":[[2024,10,30]]},"abstract":"<jats:p>Diverse antibody repertoires spanning multiple lymphoid organs (i.e., bone marrow, spleen, lymph nodes) form the foundation of protective humoral immunity. Changes in their composition across lymphoid organs are a consequence of B-cell selection and migration events leading to a highly dynamic and unique physiological landscape of antibody repertoires upon antigenic challenge (e.g., vaccination). However, to what extent B cells encoding identical or similar antibody sequences (clones) are distributed across multiple lymphoid organs and how this is shaped by the strength of a humoral response remains largely unexplored. Here, we performed an in-depth systems analysis of antibody repertoires across multiple distinct lymphoid organs of immunized mice and discovered that organ-specific antibody repertoire features (i.e., germline V-gene usage and clonal expansion profiles) equilibrated upon a strong humoral response (multiple immunizations and high serum titers). This resulted in a surprisingly high degree of repertoire consolidation, characterized by highly connected and overlapping B-cell clones across multiple lymphoid organs. Finally, we revealed distinct physiological axes indicating clonal migrations and showed that antibody repertoire consolidation directly correlated with antigen specificity. Our study uncovered how a strong humoral response resulted in a more uniform but redundant physiological landscape of antibody repertoires, indicating that increases in antibody serum titers were a result of synergistic contributions from antigen-specific B-cell clones distributed across multiple lymphoid organs. Our findings provide valuable insights for the assessment and design of vaccine strategies.<\/jats:p>","DOI":"10.7554\/elife.92718","type":"journal-article","created":{"date-parts":[[2024,11,7]],"date-time":"2024-11-07T05:15:10Z","timestamp":1730956510000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.92718","source":"Crossref","is-referenced-by-count":1,"title":["The physiological landscape and specificity of antibody repertoires are consolidated by multiple immunizations"],"prefix":"10.7554","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0709-4244","authenticated-orcid":true,"given":"Lucia","family":"Csepregi","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0411-4307","authenticated-orcid":true,"given":"Kenneth","family":"Hoehn","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03v76x132","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Pathology, Yale University School of Medicine","place":["New Haven, United States"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"given":"Daniel","family":"Neumeier","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"methodology","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1345-6122","authenticated-orcid":true,"given":"Joseph M","family":"Taft","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"methodology","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"}]},{"given":"Simon","family":"Friedensohn","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]},{"name":"Alloy Therapeutics AG","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"methodology","vocabulary":"credit"}]},{"given":"C\u00e9dric R","family":"Weber","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]},{"name":"Alloy Therapeutics AG","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Arkadij","family":"Kummer","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"formal-analysis","vocabulary":"credit"}]},{"given":"Fabian","family":"Sesterhenn","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/02s376052","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Bioengineering, \u00c9cole Polytechnique F\u00e9d\u00e9rale de Lausanne","place":["Lausanne, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"resources","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7377-8636","authenticated-orcid":true,"given":"Bruno E","family":"Correia","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/02s376052","id-type":"ROR","asserted-by":"publisher"}],"name":"Institute of Bioengineering, \u00c9cole Polytechnique F\u00e9d\u00e9rale de Lausanne","place":["Lausanne, Switzerland"]},{"id":[{"id":"https:\/\/ror.org\/002n09z45","id-type":"ROR","asserted-by":"publisher"}],"name":"SIB Swiss Institute of Bioinformatics","place":["Lausanne, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"resources","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9177-0857","authenticated-orcid":true,"given":"Sai T","family":"Reddy","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/05a28rw58","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biosystems Science and Engineering, ETH Z\u00fcrich","place":["Basel, Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"},{"role":"corresponding-author","vocabulary":"crossref"},{"role":"conceptualization","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]}],"member":"4374","published-online":{"date-parts":[[2024,12,18]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"4228","DOI":"10.1111\/febs.16385","type":"journal-article","article-title":"Dynamic organization of the bone marrow plasma cell niche","volume":"289","author":"Aaron","year":"2022","journal-title":"The FEBS Journal"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"1270","DOI":"10.1080\/19420862.2017.1371386","type":"journal-article","article-title":"Rare, high-affinity mouse anti-PD-1 antibodies that function in checkpoint blockade, discovered using microfluidics and molecular genomics","volume":"9","author":"Adler","year":"2017","journal-title":"mAbs"},{"key":"bib3","doi-asserted-by":"publisher","DOI":"10.1016\/j.ebiom.2021.103429","type":"journal-article","article-title":"TCR repertoire diversity in Multiple Sclerosis: High-dimensional bioinformatics analysis of sequences from brain, cerebrospinal fluid and peripheral blood","volume":"68","author":"Amoriello","year":"2021","journal-title":"EBioMedicine"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1080\/19420862.2019.1583995","type":"journal-article","article-title":"Antibody repertoire analysis of mouse immunization protocols using microfluidics and molecular genomics","volume":"11","author":"Asensio","year":"2019","journal-title":"mAbs"},{"key":"bib5","doi-asserted-by":"publisher","first-page":"1874","DOI":"10.1101\/gr.154815.113","type":"journal-article","article-title":"Network properties derived from deep sequencing of human B-cell receptor repertoires delineate B-cell populations","volume":"23","author":"Bashford-Rogers","year":"2013","journal-title":"Genome Research"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1038\/s41586-019-1595-3","type":"journal-article","article-title":"Analysis of the B cell receptor repertoire in six immune-mediated diseases","volume":"574","author":"Bashford-Rogers","year":"2019","journal-title":"Nature"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1038\/nri2454","type":"journal-article","article-title":"The who, how and where of antigen presentation to B cells","volume":"9","author":"Batista","year":"2009","journal-title":"Nature Reviews. Immunology"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1093\/protein\/gzq002","type":"journal-article","article-title":"An improved yeast transformation method for the generation of very large human antibody libraries","volume":"23","author":"Benatuil","year":"2010","journal-title":"Protein Engineering, Design & Selection"},{"key":"bib9","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2021.108733","type":"journal-article","article-title":"Plasma cell dynamics in the bone marrow niche","volume":"34","author":"Benet","year":"2021","journal-title":"Cell Reports"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1084\/jem.20042060","type":"journal-article","article-title":"Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization","volume":"201","author":"Blink","year":"2005","journal-title":"The Journal of Experimental Medicine"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1038\/nbt0697-553","type":"journal-article","article-title":"Yeast surface display for screening combinatorial polypeptide libraries","volume":"15","author":"Boder","year":"1997","journal-title":"Nature Biotechnology"},{"key":"bib12","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0100839","type":"journal-article","article-title":"Tissue-specific expressed antibody variable gene repertoires","volume":"9","author":"Briney","year":"2014","journal-title":"PLOS ONE"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1038\/s41586-019-0879-y","type":"journal-article","article-title":"Commonality despite exceptional diversity in the baseline human antibody repertoire","volume":"566","author":"Briney","year":"2019","journal-title":"Nature"},{"key":"bib14","type":"software","article-title":"The igraph software package for complex network research, interjournal, 975 complex systems 1695","volume-title":"Igraph","author":"Csardi","year":"2006","unstructured":"Csardi G, Nepusz T. 2006. The igraph software package for complex network research, interjournal, 975 complex systems 1695. Igraph. 1.0. https:\/\/igraph.org."},{"key":"bib15","doi-asserted-by":"publisher","DOI":"10.1016\/j.isci.2020.101519","type":"journal-article","article-title":"Immune literacy: reading, writing, and editing adaptive immunity","volume":"23","author":"Csepregi","year":"2020","journal-title":"iScience"},{"key":"bib16","type":"software","article-title":"The physiological landscape and specificity of antibody repertoires is consolidated by multiple immunizations","volume-title":"Software Heritage","author":"Csepregi","year":"2023","unstructured":"Csepregi L. 2023. The physiological landscape and specificity of antibody repertoires is consolidated by multiple immunizations. Software Heritage. swh:1:rev:8c84da23d542c9f93d017847a6eebe7e4117da62. https:\/\/archive.softwareheritage.org\/swh:1:dir:02729ed427f5a23066489eac3f249e06fdaf2478;origin=https:\/\/github.com\/luciacsep\/Physiologicallandscape;visit=swh:1:snp:e6cf1d784e2f339ecc8496e2766d09d66c7b7910;anchor=swh:1:rev:8c84da23d542c9f93d017847a6eebe7e4117da62."},{"key":"bib17","doi-asserted-by":"publisher","DOI":"10.1126\/science.abl5197","type":"journal-article","article-title":"Cross-tissue immune cell analysis reveals tissue-specific features in humans","volume":"376","author":"Dom\u00ednguez Conde","year":"2022","journal-title":"Science"},{"key":"bib18","type":"software","article-title":"Venn: draw venn diagrams","volume-title":"R Package","author":"Dusa","year":"2020","unstructured":"Dusa A. 2020. Venn: draw venn diagrams. R Package. 1.9. https:\/\/CRAN.R-project.org\/package=venn."},{"key":"bib19","doi-asserted-by":"publisher","first-page":"3805","DOI":"10.1182\/blood-2003-09-3109","type":"journal-article","article-title":"Antigen-selected, immunoglobulin-secreting cells persist in human spleen and bone marrow","volume":"103","author":"Ellyard","year":"2004","journal-title":"Blood"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1038\/nbt785","type":"journal-article","article-title":"Flow-cytometric isolation of human antibodies from a nonimmune Saccharomyces cerevisiae surface display library","volume":"21","author":"Feldhaus","year":"2003","journal-title":"Nature Biotechnology"},{"key":"bib21","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.01401","type":"journal-article","article-title":"Synthetic standards combined with error and bias correction improve the accuracy and quantitative resolution of antibody repertoire sequencing in human na\u00efve and memory B cells","volume":"9","author":"Friedensohn","year":"2018","journal-title":"Frontiers in Immunology"},{"key":"bib22","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2015.00531","type":"journal-article","article-title":"In-depth assessment of within-individual and inter-individual variation in the B cell receptor repertoire","volume":"6","author":"Galson","year":"2015","journal-title":"Frontiers in Immunology"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"D256","DOI":"10.1093\/nar\/gki010","type":"journal-article","article-title":"IMGT\/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes","volume":"33","author":"Giudicelli","year":"2005","journal-title":"Nucleic Acids Research"},{"key":"bib24","doi-asserted-by":"publisher","DOI":"10.1186\/s13073-015-0169-8","type":"journal-article","article-title":"A bioinformatic framework for immune repertoire diversity profiling enables detection of immunological status","volume":"7","author":"Greiff","year":"2015","journal-title":"Genome Medicine"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"1467","DOI":"10.1016\/j.celrep.2017.04.054","type":"journal-article","article-title":"Systems analysis reveals high genetic and antigen-driven predetermination of antibody repertoires throughout B cell development","volume":"19","author":"Greiff","year":"2017","journal-title":"Cell Reports"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"2985","DOI":"10.4049\/jimmunol.1700594","type":"journal-article","article-title":"Learning the high-dimensional immunogenomic features that predict public and private antibody repertoires","volume":"199","author":"Greiff","year":"2017","journal-title":"Journal of Immunology"},{"key":"bib27","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01168","type":"journal-article","article-title":"Lymphatic migration of immune cells","volume":"10","author":"Hampton","year":"2019","journal-title":"Frontiers in Immunology"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1016\/j.jim.2007.11.012","type":"journal-article","article-title":"Lymph node mapping in the mouse","volume":"332","author":"Harrell","year":"2008","journal-title":"Journal of Immunological Methods"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"427","DOI":"10.2307\/1934352","type":"journal-article","article-title":"Diversity and evenness: a unifying notation and its consequences","volume":"54","author":"Hill","year":"1973","journal-title":"Ecology"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"22664","DOI":"10.1073\/pnas.1906020116","type":"journal-article","article-title":"Repertoire-wide phylogenetic models of B cell molecular evolution reveal evolutionary signatures of aging and vaccination","volume":"116","author":"Hoehn","year":"2019","journal-title":"PNAS"},{"key":"bib31","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1009885","type":"journal-article","article-title":"Phylogenetic analysis of migration, differentiation, and class switching in B cells","volume":"18","author":"Hoehn","year":"2022","journal-title":"PLOS Computational Biology"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"978","DOI":"10.1038\/nmat3775","type":"journal-article","article-title":"Engineering synthetic vaccines using cues from natural immunity","volume":"12","author":"Irvine","year":"2013","journal-title":"Nature Materials"},{"key":"bib33","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.888555","type":"journal-article","article-title":"A BALB\/C IGHV reference set, defined by haplotype analysis of long-read VDJ-C sequences from F1 (BALB\/C x C57BL\/6) Mice","volume":"13","author":"Jackson","year":"2022","journal-title":"Frontiers in Immunology"},{"key":"bib34","doi-asserted-by":"publisher","DOI":"10.1126\/science.abl4896","type":"journal-article","article-title":"The tabula sapiens: a multiple-organ, single-cell transcriptomic atlas of humans","volume":"376","author":"Jones","year":"2022","journal-title":"Science"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1111\/j.2006.0030-1299.14714.x","type":"journal-article","article-title":"Entropy and diversity","volume":"113","author":"Jost","year":"2006","journal-title":"Oikos"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"967","DOI":"10.1084\/jem.20040973","type":"journal-article","article-title":"Plasma cell ontogeny defined by quantitative changes in blimp-1 expression","volume":"200","author":"Kallies","year":"2004","journal-title":"The Journal of Experimental Medicine"},{"key":"bib37","type":"software","article-title":"Ggpubr: \u201cggplot2\u201d based publication ready plots","volume-title":"R Package","author":"Kassambara","year":"2020","unstructured":"Kassambara A. 2020. Ggpubr: \u201cggplot2\u201d based publication ready plots. R Package. 0.4.0. https:\/\/rpkgs.datanovia.com\/ggpubr\/."},{"key":"bib38","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.1501371","type":"journal-article","article-title":"Accurate and predictive antibody repertoire profiling by molecular amplification fingerprinting","volume":"2","author":"Khan","year":"2016","journal-title":"Science Advances"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"1303","DOI":"10.1093\/protein\/10.11.1303","type":"journal-article","article-title":"Isolation of anti-T cell receptor scFv mutants by yeast surface display","volume":"10","author":"Kieke","year":"1997","journal-title":"Protein Engineering Design and Selection"},{"key":"bib40","type":"software","article-title":"Pheatmap: pretty heatmaps","volume-title":"R Package Version","author":"Kolde","year":"2019","unstructured":"Kolde R. 2019. Pheatmap: pretty heatmaps. R Package Version. 1.0.12. https:\/\/CRAN.Rproject.org\/package=pheatmap."},{"key":"bib41","doi-asserted-by":"publisher","first-page":"2259","DOI":"10.1073\/pnas.1317793111","type":"journal-article","article-title":"Identification and characterization of the constituent human serum antibodies elicited by vaccination","volume":"111","author":"Lavinder","year":"2014","journal-title":"PNAS"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"1281","DOI":"10.1016\/j.immuni.2020.11.009","type":"journal-article","article-title":"SARS-CoV-2 mRNA vaccines foster potent antigen-specific germinal center responses associated with neutralizing antibody generation","volume":"53","author":"Lederer","year":"2020","journal-title":"Immunity"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"D964","DOI":"10.1093\/nar\/gkz822","type":"journal-article","article-title":"OGRDB: a reference database of inferred immune receptor genes","volume":"48","author":"Lees","year":"2020","journal-title":"Nucleic Acids Research"},{"key":"bib44","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-16857-7","type":"journal-article","article-title":"Profiling immunoglobulin repertoires across multiple human tissues using RNA sequencing","volume":"11","author":"Mandric","year":"2020","journal-title":"Nature Communications"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1038\/40540","type":"journal-article","article-title":"Lifetime of plasma cells in the bone marrow","volume":"388","author":"Manz","year":"1997","journal-title":"Nature"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1146\/annurev.immunol.23.021704.115723","type":"journal-article","article-title":"Maintenance of serum antibody levels","volume":"23","author":"Manz","year":"2005","journal-title":"Annual Review of Immunology"},{"key":"bib47","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2021.109286","type":"journal-article","article-title":"Single-cell BCR and transcriptome analysis after influenza infection reveals spatiotemporal dynamics of antigen-specific B cells","volume":"35","author":"Mathew","year":"2021","journal-title":"Cell Reports"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"879","DOI":"10.1038\/nbt.3942","type":"journal-article","article-title":"An atlas of B-cell clonal distribution in the human body","volume":"35","author":"Meng","year":"2017","journal-title":"Nature Biotechnology"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1016\/j.cell.2019.11.032","type":"journal-article","article-title":"Restricted clonality and limited germinal center reentry characterize memory B cell reactivation by boosting","volume":"180","author":"Mesin","year":"2020","journal-title":"Cell"},{"key":"bib50","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-09278-8","type":"journal-article","article-title":"Large-scale network analysis reveals the sequence space architecture of antibody repertoires","volume":"10","author":"Miho","year":"2019","journal-title":"Nature Communications"},{"key":"bib51","doi-asserted-by":"publisher","DOI":"10.1186\/s12859-015-0613-1","type":"journal-article","article-title":"tcR: an R package for T cell receptor repertoire advanced data analysis","volume":"16","author":"Nazarov","year":"2015","journal-title":"BMC Bioinformatics"},{"key":"bib52","type":"software","article-title":"Immunarch \u2014 fast and seamless exploration of single-cell and bulk T-cell\/antibody immune repertoires in R","volume-title":"Immunarch","author":"Nazarov","year":"2021","unstructured":"Nazarov VI, Rumynskiy VO, Lorenc E, Moore A, Greiff DJ, ImmunoMind V. 2021. Immunarch \u2014 fast and seamless exploration of single-cell and bulk T-cell\/antibody immune repertoires in R. Immunarch. 0.1. https:\/\/immunarch.com\/."},{"key":"bib53","type":"software","article-title":"RColorBrewer: colorbrewer palettes","volume-title":"R Package","author":"Neuwirth","year":"2014","unstructured":"Neuwirth E. 2014. RColorBrewer: colorbrewer palettes. R Package. 1.1-2. https:\/\/CRAN.R-project.org\/package=RColorBrewer."},{"key":"bib54","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0034714","type":"journal-article","article-title":"Imaging of bubonic plague dynamics by in vivo tracking of bioluminescent Yersinia pestis","volume":"7","author":"Nham","year":"2012","journal-title":"PLOS ONE"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"i341","DOI":"10.1093\/bioinformatics\/bty235","type":"journal-article","article-title":"A spectral clustering-based method for identifying clones from high-throughput B cell repertoire sequencing data","volume":"34","author":"Nouri","year":"2018","journal-title":"Bioinformatics"},{"key":"bib56","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01787","type":"journal-article","article-title":"Remembrance of things past: long-term B cell memory after infection and vaccination","volume":"10","author":"Palm","year":"2019","journal-title":"Frontiers in Immunology"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"1367","DOI":"10.1080\/19420862.2019.1662691","type":"journal-article","article-title":"Antibody discovery and engineering by enhanced CRISPR-Cas9 integration of variable gene cassette libraries in mammalian cells","volume":"11","author":"Parola","year":"2019","journal-title":"mAbs"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"1389","DOI":"10.1002\/eji.201747019","type":"journal-article","article-title":"A new staining protocol for detection of murine antibody\u2010secreting plasma cell subsets by flow cytometry","volume":"47","author":"Pracht","year":"2017","journal-title":"European Journal of Immunology"},{"key":"bib59","type":"software","article-title":"R: A language and environment for statistical computing","author":"R Development Core Team","year":"2020","unstructured":"R Development Core Team. 2020. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https:\/\/www.R-project.org."},{"key":"bib60","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/j.jconrel.2006.01.006","type":"journal-article","article-title":"In vivo targeting of dendritic cells in lymph nodes with poly(propylene sulfide) nanoparticles","volume":"112","author":"Reddy","year":"2006","journal-title":"Journal of Controlled Release"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1038\/nbt.1673","type":"journal-article","article-title":"Monoclonal antibodies isolated without screening by analyzing the variable-gene repertoire of plasma cells","volume":"28","author":"Reddy","year":"2010","journal-title":"Nature Biotechnology"},{"key":"bib62","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-16464-6","type":"journal-article","article-title":"Discrete populations of isotype-switched memory B lymphocytes are maintained in murine spleen and bone marrow","volume":"11","author":"Riedel","year":"2020","journal-title":"Nature Communications"},{"key":"bib63","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.01472","type":"journal-article","article-title":"Computational evaluation of B-cell clone sizes in bulk populations","volume":"9","author":"Rosenfeld","year":"2018","journal-title":"Frontiers in Immunology"},{"key":"bib64","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.3000164","type":"journal-article","article-title":"Boosting subdominant neutralizing antibody responses with a computationally designed epitope-focused immunogen","volume":"17","author":"Sesterhenn","year":"2019","journal-title":"PLOS Biology"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1038\/ni.3154","type":"journal-article","article-title":"Transcriptional profiling of mouse B cell terminal differentiation defines a signature for antibody-secreting plasma cells","volume":"16","author":"Shi","year":"2015","journal-title":"Nature Immunology"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"1895","DOI":"10.1128\/JVI.69.3.1895-1902.1995","type":"journal-article","article-title":"Bone marrow is a major site of long-term antibody production after acute viral infection","volume":"69","author":"Slifka","year":"1995","journal-title":"Journal of Virology"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1016\/s1074-7613(00)80541-5","type":"journal-article","article-title":"Humoral immunity due to long-lived plasma cells","volume":"8","author":"Slifka","year":"1998","journal-title":"Immunity"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"3128","DOI":"10.4049\/jimmunol.1301163","type":"journal-article","article-title":"Plasma cell homeostasis: the effects of chronic antigen stimulation and inflammation","volume":"191","author":"Slocombe","year":"2013","journal-title":"Journal of Immunology"},{"key":"bib69","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1038\/s41586-019-0934-8","type":"journal-article","article-title":"High frequency of shared clonotypes in human B cell receptor repertoires","volume":"566","author":"Soto","year":"2019","journal-title":"Nature"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1084\/jem.187.6.885","type":"journal-article","article-title":"In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection","volume":"187","author":"Takahashi","year":"1998","journal-title":"The Journal of Experimental Medicine"},{"key":"bib71","doi-asserted-by":"publisher","first-page":"1048","DOI":"10.1126\/science.aad3439","type":"journal-article","article-title":"Visualizing antibody affinity maturation in germinal centers","volume":"351","author":"Tas","year":"2016","journal-title":"Science"},{"key":"bib72","doi-asserted-by":"publisher","first-page":"1930","DOI":"10.1093\/bioinformatics\/btu138","type":"journal-article","article-title":"pRESTO: a toolkit for processing high-throughput sequencing raw reads of lymphocyte receptor repertoires","volume":"30","author":"Vander Heiden","year":"2014","journal-title":"Bioinformatics"},{"key":"bib73","type":"software","article-title":"Stringdist: approximate string matching, fuzzy text search, and string distance functions","volume-title":"Package \u2018Stringdist.\u2019","author":"van der Loo","year":"2021","unstructured":"van der Loo M, van der LJ, Logan N, Muir C, Gruber J, R Core Team. 2021. Stringdist: approximate string matching, fuzzy text search, and string distance functions. Package \u2018Stringdist.\u2019. GPL-3. https:\/\/cran.r-project.org\/web\/packages\/stringdist\/stringdist.pdf."},{"key":"bib74","doi-asserted-by":"publisher","first-page":"690","DOI":"10.4161\/mabs.25592","type":"journal-article","article-title":"Comparing CDRH3 diversity captured from secondary lymphoid organs for the generation of recombinant human antibodies","volume":"5","author":"Venet","year":"2013","journal-title":"mAbs"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1016\/j.jim.2007.01.019","type":"journal-article","article-title":"Methods for comparing the diversity of samples of the T cell receptor repertoire","volume":"321","author":"Venturi","year":"2007","journal-title":"Journal of Immunological Methods"},{"key":"bib76","doi-asserted-by":"publisher","first-page":"1108","DOI":"10.1126\/science.abg5268","type":"journal-article","article-title":"Prevalent, protective, and convergent IgG recognition of SARS-CoV-2 non-RBD spike epitopes","volume":"372","author":"Voss","year":"2021","journal-title":"Science"},{"key":"bib77","doi-asserted-by":"publisher","DOI":"10.1038\/srep13926","type":"journal-article","article-title":"Facile discovery of a diverse panel of anti-ebola virus antibodies by immune repertoire mining","volume":"5","author":"Wang","year":"2015","journal-title":"Scientific Reports"},{"key":"bib78","doi-asserted-by":"publisher","first-page":"1035","DOI":"10.1080\/19420862.2016.1190059","type":"journal-article","article-title":"Discovery of high affinity anti-ricin antibodies by B cell receptor sequencing and by yeast display of combinatorial VH:VL libraries from immunized animals","volume":"8","author":"Wang","year":"2016","journal-title":"mAbs"},{"key":"bib79","doi-asserted-by":"publisher","first-page":"1019","DOI":"10.1016\/0264-410x(96)00062-x","type":"journal-article","article-title":"Vaccine induced immunologic memory for hepatitis B surface antigen: implications for policy on booster vaccination","volume":"14","author":"West","year":"1996","journal-title":"Vaccine"},{"key":"bib80","type":"software","article-title":"Ggplot2: create elegant data visualisations using the grammar of graphics","volume-title":"Ggplot2","author":"Wickham","year":"2021","unstructured":"Wickham H. 2021. Ggplot2: create elegant data visualisations using the grammar of graphics. Ggplot2. 3.5.1. https:\/\/ggplot2.tidyverse.org\/reference\/ggplot2-package.html."},{"key":"bib81","type":"software","article-title":"Cowplot: streamlined plot theme and plot annotations for \u201cggplot2","volume-title":"R Project","author":"Wilke","year":"2020","unstructured":"Wilke CO. 2020. Cowplot: streamlined plot theme and plot annotations for \u201cggplot2. R Project. 1.1.3. https:\/\/cran.r-project.org\/web\/packages\/cowplot\/index.html."},{"key":"bib82","doi-asserted-by":"publisher","first-page":"839","DOI":"10.4049\/jimmunol.1700461","type":"journal-article","article-title":"Here, there, and anywhere? arguments for and against the physical plasma cell survival niche","volume":"199","author":"Wilmore","year":"2017","journal-title":"Journal of Immunology"},{"key":"bib83","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1038\/nri.2016.116","type":"journal-article","article-title":"Dendritic cell migration in health and disease","volume":"17","author":"Worbs","year":"2017","journal-title":"Nature Reviews. Immunology"},{"key":"bib84","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2013.00358","type":"journal-article","article-title":"Models of somatic hypermutation targeting and substitution based on synonymous mutations from high-throughput immunoglobulin sequencing data","volume":"4","author":"Yaari","year":"2013","journal-title":"Frontiers in Immunology"},{"key":"bib85","doi-asserted-by":"publisher","first-page":"738","DOI":"10.1126\/science.abf6648","type":"journal-article","article-title":"Shared B cell memory to coronaviruses and other pathogens varies in human age groups and tissues","volume":"372","author":"Yang","year":"2021","journal-title":"Science"},{"key":"bib86","doi-asserted-by":"publisher","first-page":"W34","DOI":"10.1093\/nar\/gkt382","type":"journal-article","article-title":"IgBLAST: an immunoglobulin variable domain sequence analysis tool","volume":"41","author":"Ye","year":"2013","journal-title":"Nucleic Acids Research"},{"key":"bib87","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1111\/2041-210X.12628","type":"journal-article","article-title":"ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data","volume":"8","author":"Yu","year":"2017","journal-title":"Methods in Ecology and Evolution"},{"key":"dataset1","type":"dataset","article-title":"IgG VH deep sequencing of Mus musculus: lymph nodes, spleen and bone marrow","volume-title":"NCBI Sequence Read Archive","author":"Csepregi","year":"2021","unstructured":"Csepregi L, Hoehn KB, Neumeier D, Taft JM, Friedensohn S, Weber CR, Kummer A, Sesterhenn F, Correia BE, Reddy ST. 2021. IgG VH deep sequencing of Mus musculus: lymph nodes, spleen and bone marrow. NCBI Sequence Read Archive. https:\/\/www.ncbi.nlm.nih.gov\/sra\/PRJNA763201. PRJNA763201."}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/92718\/elife-92718-v1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/92718\/elife-92718-v1.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/92718","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T09:57:08Z","timestamp":1787565428000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/92718"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,18]]},"references-count":88,"alternative-id":["10.7554\/eLife.92718"],"URL":"https:\/\/doi.org\/10.7554\/elife.92718","archive":["CLOCKSS"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.09.15.460420","asserted-by":"subject"}],"is-supplemented-by":[{"id-type":"accession","id":"PRJNA763201","asserted-by":"subject"},{"id-type":"uri","id":"https:\/\/archive.softwareheritage.org\/swh:1:dir:02729ed427f5a23066489eac3f249e06fdaf2478;origin=https:\/\/github.com\/luciacsep\/Physiologicallandscape;visit=swh:1:snp:e6cf1d784e2f339ecc8496e2766d09d66c7b7910;anchor=swh:1:rev:8c84da23d542c9f93d017847a6eebe7e4117da62","asserted-by":"subject"}],"has-review":[{"id-type":"doi","id":"10.7554\/eLife.92718.sa2","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.92718.sa1","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.92718.sa0","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,18]]},"assertion":[{"value":"single anonymised","name":"peer_review_transparency","label":"Peer review transparency","group":{"name":"peer_review_taxonomy"}},{"value":"other reviewer(s), editor","name":"peer_review_interaction","label":"Peer review interaction","group":{"name":"peer_review_taxonomy"}},{"value":"review summaries, review reports, author\/editor communication, reviewer identities reviewer opt in, editor identities","name":"peer_review_published","label":"Peer review published","group":{"name":"peer_review_taxonomy"}},{"value":"open (sign in with ORCID iD required)","name":"post_publication_commenting","label":"Post publication commenting","group":{"name":"post_publication_commenting"}}],"article-number":"e92718"}}