Immunological memory diversity in the human upper airway
Sette, A. & Crotty, S. Immunological memory to SARS‐CoV‐2 infection and COVID‐19 vaccines. Immunol. Rev. 310, 27–46 (2022).
Allie, S. R. & Randall, T. D. Resident memory B cells. Viral Immunol. 33, 282–293 (2020).
Topol, E. J. & Iwasaki, A. Operation nasal vaccine-lightning speed to counter COVID-19. Sci. Immunol. 7, eadd9947 (2022).
Zheng, M. Z. M. & Wakim, L. M. Tissue resident memory T cells in the respiratory tract. Mucosal Immunol. 15, 379–388 (2022).
Poon, M. M. L. et al. Tissue adaptation and clonal segregation of human memory T cells in barrier sites. Nat. Immunol. 24, 309–319 (2023).
Domínguez Conde, C. et al. Cross-tissue immune cell analysis reveals tissue-specific features in humans. Science 376, eabl5197 (2022).
Clark, R. A. Resident memory T cells in human health and disease. Sci. Transl. Med. 7, 269rv1 (2015).
Lange, J., Rivera-Ballesteros, O. & Buggert, M. Human mucosal tissue-resident memory T cells in health and disease. Mucosal Immunol. 15, 389–397 (2022).
Thome, J. J. C. et al. Spatial map of human T cell compartmentalization and maintenance over decades of life. Cell 159, 814–828 (2014).
Gray, J. I. & Farber, D. L. Tissue-resident immune cells in humans. Annu. Rev. Immunol. 40, 195–220 (2022).
Masopust, D. & Soerens, A. G. Tissue-resident T cells and other resident leukocytes. Annu. Rev. Immunol. 37, 521–546 (2019).
Snyder, M. E. et al. Generation and persistence of human tissue-resident memory T cells in lung transplantation. Sci. Immunol. 4, eaav5581 (2019).
Weisel, N. M. et al. Comprehensive analyses of B-cell compartments across the human body reveal novel subsets and a gut-resident memory phenotype. Blood 136, 2774–2785 (2020).
Havenar-Daughton, C., Lee, J. H. & Crotty, S. Tfh cells and HIV bnAbs, an immunodominance model of the HIV neutralizing antibody generation problem. Immunol. Rev. 275, 49–61 (2017).
Havenar-Daughton, C. et al. Normal human lymph node T follicular helper cells and germinal center B cells accessed via fine needle aspirations. J. Immunol. Methods 479, 112746 (2020).
Alsoussi, W. B. et al. SARS-CoV-2 Omicron boosting induces de novo B cell response in humans. Nature 617, 592–598 (2023).
Leggat, D. J. et al. Vaccination induces HIV broadly neutralizing antibody precursors in humans. Science 378, eadd6502 (2022).
Victora, G. D. & Nussenzweig, M. C. Germinal Centers. Annu. Rev. Immunol. 40, 413–442 (2022).
Xu, Q. et al. Adaptive immune responses to SARS-CoV-2 persist in the pharyngeal lymphoid tissue of children. Nat. Immunol. 24, 186–199 (2023).
Kumar, B. V. et al. Human tissue-resident memory T cells are defined by core transcriptional and functional signatures in lymphoid and mucosal sites. Cell Rep. 20, 2921–2934 (2017).
Kusnadi, A. et al. Severely ill COVID-19 patients display impaired exhaustion features in SARS-CoV-2-reactive CD8+ T cells. Sci. Immunol. 6, eabe4782 (2021).
Meckiff, B. J. et al. Imbalance of regulatory and cytotoxic SARS-CoV-2-reactive CD4+ T cells in COVID-19. Cell 183, 1340–1353.e16 (2020).
Schmiedel, B. J. et al. Single-cell eQTL analysis of activated T cell subsets reveals activation and cell type-dependent effects of disease-risk variants. Sci. Immunol. 7, eabm2508 (2022).
FitzPatrick, M. E. B. et al. Human intestinal tissue-resident memory T cells comprise transcriptionally and functionally distinct subsets. Cell Reports 34, 108661 (2021).
Crotty, S. T follicular helper cell biology: a decade of discovery and diseases. Immunity 50, 1132–1148 (2019).
Mudd, P. A. et al. SARS-CoV-2 mRNA vaccination elicits a robust and persistent T follicular helper cell response in humans. Cell 185, 603–613.e15 (2022).
Nolan, S. et al. A large-scale database of T-cell receptor beta (TCRb) sequences and binding associations from natural and synthetic exposure to SARS-CoV-2. Preprint at Research Square https://doi.org/10.21203/rs.3.rs-51964/v1 (2020).
Goncharov, M. et al. VDJdb in the pandemic era: a compendium of T cell receptors specific for SARS-CoV-2. Nat. Methods 19, 1017–1019 (2022).
Rowntree, L. C. et al. SARS-CoV-2-specific T cell memory with common TCRαβ motifs is established in unvaccinated children who seroconvert after infection. Immunity 55, 1299–1315.e4 (2022).
Pogorelyy, M. V. et al. Resolving SARS-CoV-2 CD4+ T cell specificity via reverse epitope discovery. Cell Rep. Med. 3, 100697 (2022).
Tan, H.-X. et al. Lung-resident memory B cells established after pulmonary influenza infection display distinct transcriptional and phenotypic profiles. Sci. Immunol. 7, eabf5314 (2022).
Barker, K. A. et al. Lung-resident memory B cells protect against bacterial pneumonia. J. Clin. Invest. 131, e141810 (2021).
Gregoire, C. et al. Viral infection engenders bona fide and bystander subsets of lung-resident memory B cells through a permissive mechanism. Immunity 55, 1216–1233.e9 (2022).
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).
Ehrhardt, G. R. A. et al. Expression of the immunoregulatory molecule FcRH4 defines a distinctive tissue-based population of memory B cells. J. Exp. Med. 202, 783–791 (2005).
Ehrhardt, G. R. A. et al. Discriminating gene expression profiles of memory B cell subpopulations. J. Exp. Med. 205, 1807–1817 (2008).
King, H. W. et al. Single-cell analysis of human B cell maturation predicts how antibody class switching shapes selection dynamics. Sci. Immunol. 6, eabe6291 (2021).
Zumaquero, E. et al. IFNγ induces epigenetic programming of human T-bethi B cells and promotes TLR7/8 and IL-21 induced differentiation. eLife 8, e41641 (2019).
Knox, J. J. et al. T-bet+ B cells are induced by human viral infections and dominate the HIV gp140 response. JCI Insight 2, e92943 (2017).
Duan, M. et al. Understanding heterogeneity of human bone marrow plasma cell maturation and survival pathways by single-cell analyses. Cell Rep. 42, 112682 (2023).
Lim, J. M. E. et al. SARS-CoV-2 breakthrough infection in vaccinees induces virus-specific nasal-resident CD8+ and CD4+ T cells of broad specificity. J. Exp. Med. 219, e20220780 (2022).
Dan, J. M. et al. Immunological memory to SARS-CoV-2 assessed for up to 8 months after infection. Science 371, eabf4063 (2021).
Grifoni, A. et al. Targets of T cell responses to SARS-CoV-2 coronavirus in humans with COVID-19 disease and unexposed individuals. Cell 181, 1489–1501.e15 (2020).
Dan, J. M. et al. Recurrent group A Streptococcus tonsillitis is an immunosusceptibility disease involving antibody deficiency and aberrant T FH cells. Sci. Transl. Med. 11, eaau3776 (2019).
Ramirez, S. I. et al. Bamlanivimab therapy for acute COVID-19 does not blunt SARS-CoV-2–specific memory T cell responses. JCI Insight 7, e163471 (2022).
Yu, E. D. et al. Development of a T cell-based immunodiagnostic system to effectively distinguish SARS-CoV-2 infection and COVID-19 vaccination status. Cell Host Microbe 30, 388–399.e3 (2022).
Grifoni, A. et al. SARS-CoV-2 human T cell epitopes: adaptive immune response against COVID-19. Cell Host Microbe 29, 1076–1092 (2021).
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587.e29 (2021).
Korotkevich, G. et al. Fast gene set enrichment analysis. Preprint at bioRXiv https://doi.org/10.1101/060012 (2016).
Lee, J. H. et al. Long-primed germinal centres with enduring affinity maturation and clonal migration. Nature 609, 998–1004 (2022).
Holla, P. et al. Shared transcriptional profiles of atypical B cells suggest common drivers of expansion and function in malaria, HIV, and autoimmunity. Sci. Adv. 7, eabg8384 (2021).
Lopes De Assis, F. et al. Tracking B cell responses to the SARS-CoV-2 mRNA-1273 vaccine. Cell Rep. 42, 112780 (2023).
Yermanos, A. et al. Platypus: an open-access software for integrating lymphocyte single-cell immune repertoires with transcriptomes. NAR Genom. Bioinform. 3, lqab023 (2021).
Gupta, N. T. et al. Change-O: a toolkit for analyzing large-scale B cell immunoglobulin repertoire sequencing data. Bioinformatics 31, 3356–3358 (2015).
Vander Heiden, J. A. et al. pRESTO: a toolkit for processing high-throughput sequencing raw reads of lymphocyte receptor repertoires. Bioinformatics 30, 1930–1932 (2014).
Gupta, N. T. et al. Hierarchical clustering can identify B cell clones with high confidence in Ig repertoire sequencing data. J. Immunol. 198, 2489–2499 (2017).
Nouri, N. & Kleinstein, S. H. Somatic hypermutation analysis for improved identification of B cell clonal families from next-generation sequencing data. PLoS Comput. Biol. 16, e1007977 (2020).
Ye, J., Ma, N., Madden, T. L. & Ostell, J. M. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41, W34–W40 (2013).
Giudicelli, V., Chaume, D. & Lefranc, M.-P. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res. 33, D256–D261 (2005).
Hoehn, K. B. et al. Repertoire-wide phylogenetic models of B cell molecular evolution reveal evolutionary signatures of aging and vaccination. Proc. Natl Acad. Sci. USA 116, 22664–22672 (2019).
Hoehn, K. B. et al. Human B cell lineages associated with germinal centers following influenza vaccination are measurably evolving. eLife 10, e70873 (2021).
Hoehn, K. B., Pybus, O. G. & Kleinstein, S. H. Phylogenetic analysis of migration, differentiation, and class switching in B cells. PLoS Comput. Biol. 18, e1009885 (2022).
Raybould, M. I. J., Kovaltsuk, A., Marks, C. & Deane, C. M. CoV-AbDab: the coronavirus antibody database. Bioinformatics 37, 734–735 (2021).
Kaku, C. I. et al. Evolution of antibody immunity following Omicron BA.1 breakthrough infection. Nat. Commun. 14, 2751 (2023).
Chen, E. C. et al. Convergent antibody responses to the SARS-CoV-2 spike protein in convalescent and vaccinated individuals. Cell Rep. 36, 109604 (2021).
Barnes, C. O. et al. Structures of human antibodies bound to SARS-CoV-2 spike reveal common epitopes and recurrent features of antibodies. Cell 182, 828–842.e16 (2020).
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.e11 (2022).
Hastie, K. M. et al. Potent Omicron-neutralizing antibodies isolated from a patient vaccinated 6 months before Omicron emergence. Cell Rep. 42, 112421 (2023).
Lee, J. H. et al. A broadly neutralizing antibody targets the dynamic HIV envelope trimer apex via a long, rigidified, and anionic β-hairpin structure. Immunity 46, 690–702 (2017).
Zhang, Z. et al. Humoral and cellular immune memory to four COVID-19 vaccines. Cell 185, 2434–2451.e17 (2022).