Apoptosis and antigen affinity limit effector cell differentiation of a single naïve B cell

Taylor, Justin J.; Pape, Kathryn A.; Steach, Holly R.; Jenkins, Marc K.

doi:10.1126/science.aaa1342

Cited by 164T-cell and B-cell ImmunologyImmunotherapy and Immune ResponsesImmune responses and vaccinations

Apoptosis and antigen affinity limit effector cell differentiation of a single naïve B cell

Open access

Taylor, Justin J., Pape, Kathryn A., Steach, Holly R., Jenkins, Marc K.·2015·Science

DOI 10.1126/science.aaa1342PMC PMC4412594

Open this paper in CoChat — free account

Abstract

For a single B cell, many roads to take: To successfully fight a pathogen, immunological B cells must wage a multipronged attack: They can differentiate into antibody-secreting plasma cells or become T cell–helping germinal center cells, or even long-lived memory cells. But can a single B cell acquire all of these different fates? To find out, Taylor et al. tracked the responses of single B cells in mice. Although some B cells acquired only one fate, others differentiated into all three. The authors linked the ability of B cells to differentiate into multiple subsets to their ability to proliferate and resist cell death, and the affinity of their antigen receptor. Science , this issue p. 784

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1126/science.aaa1342

Cites

24 of 24 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Persistent clones expand without accumulating large numbers of additional mutations, indicating that clonal expansion of human memory B cells does not require re-entry into germinal centres and occurs in the activated B cell compartment.
“The persistent clones expand without accumulating large numbers of additional mutations, indicating that clonal expansion of human memory B cells does not require re-entry into germinal centres and occurs in the activated B cell compartment17,27–31.”
From Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection (2021) · cites this paper as [31]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Class Switch Recombination and Hypermutation Require Activation-Induced Cytidine Deaminase (AID), a Potential RNA Editing Enzyme
Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., & Honjo, T. (2000) · Cell · doi:10.1016/s0092-8674(00)00078-7 · Cited by 3,475 · see citing works
Determination of lymphocyte division by flow cytometry
Lyons, A. B., & Parish, C. R. (1994) · Journal of Immunological Methods · doi:10.1016/0022-1759(94)90236-4 · Cited by 1,664 · see citing works
Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice
Goodnow, C. C., Crosbie, J. C., Adelstein, S., Lavoie, T., Smith‐Gill, S. J., Brink, R. A., Pritchard-Briscoe, H., Wotherspoon, J. S., Loblay, R. H., Raphael, K., et al. (1988) · Nature · doi:10.1038/334676a0 · Cited by 1,568 · see citing works
Proapoptotic Bcl-2 Relative Bim Required for Certain Apoptotic Responses, Leukocyte Homeostasis, and to Preclude Autoimmunity
Bouillet, P., Metcalf, D., Huang, D. C. S., Tarlinton, D. M., Kay, T. W. H., Köntgen, F., Adams, J. M., & Strasser, A. (1999) · Science · doi:10.1126/science.286.5445.1735 · Cited by 1,504 · see citing works
Limiting dilution assays for the determination of immunocompetent cell frequencies. I. Data analysis.
Taswell, C. (1981) · The Journal of Immunology · doi:10.4049/jimmunol.126.4.1614 · Cited by 1,249 · see citing works
Visualization of Specific B and T Lymphocyte Interactions in the Lymph Node
Garside, P., Ingulli, E. G., Merica, R. R., Johnson, J. G., Noelle, R. J., & Jenkins, M. K. (1998) · Science · doi:10.1126/science.281.5373.96 · Cited by 774 · see citing works
Self-citation
Different B Cell Populations Mediate Early and Late Memory During an Endogenous Immune Response
Pape, K. A., Taylor, J. J., Maul, R. W., Gearhart, P. J., & Jenkins, M. K. (2011) · Science · doi:10.1126/science.1201730 · Cited by 572 · see citing works
Self-citation
Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation
Paus, D., Phan, T. G., Chan, T. D., Gardam, S., Basten, A., & Brink, R. A. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060087 · Cited by 568 · see citing works
Resolution of Three Nonproliferative Immature Splenic B Cell Subsets Reveals Multiple Selection Points During Peripheral B Cell Maturation
Allman, D., Lindsley, R. C., DeMuth, W., Rudd, K., Shinton, S. A., & Hardy, R. R. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.12.6834 · Cited by 551 · see citing works
Transcriptional Regulation of Germinal Center B and Plasma Cell Fates by Dynamical Control of IRF4
Ochiai, K., Maienschein‐Cline, M., Simonetti, G., Chen, J., Rosenthal, R. L., Brink, R. A., Chong, A. S., Klein, U., Dinner, A. R., Singh, H., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.04.009 · Cited by 469 · see citing works
Single Naive CD4+ T Cells from a Diverse Repertoire Produce Different Effector Cell Types during Infection
Tubo, N. J., Pagán, A. J., Taylor, J. J., Nelson, R. W., Linehan, J. L., Ertelt, J. M., Huseby, E. S., Way, S. S., & Jenkins, M. K. (2013) · Cell · doi:10.1016/j.cell.2013.04.007 · Cited by 444 · see citing works
Self-citation
A dynamic T cell–limited checkpoint regulates affinity-dependent B cell entry into the germinal center
Schwickert, T. A., Victora, G. D., Fooksman, D., Kamphorst, A. O., Mugnier, M. R., Gitlin, A. D., Dustin, M. L., & Nussenzweig, M. C. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20102477 · Cited by 427 · see citing works
Disparate Individual Fates Compose Robust CD8 + T Cell Immunity
Buchholz, V. R., Floßdorf, M., Hensel, I., Kretschmer, L., Weißbrich, B., Gräf, P., Verschoor, A., Schiemann, M., Höfer, T., & Busch, D. H. (2013) · Science · doi:10.1126/science.1235454 · Cited by 406 · see citing works
Limiting dilution assays for the determination of immunocompetent cell frequencies.
Taswell, C. (1981) · Medical Entomology and Zoology · Cited by 395 · see citing works
A germinal center–independent pathway generates unswitched memory B cells early in the primary response
Taylor, J. J., Pape, K. A., & Jenkins, M. K. (2012) · The Journal of Experimental Medicine · doi:10.1084/jem.20111696 · Cited by 387 · see citing works
Self-citation
Heterogeneous Differentiation Patterns of Individual CD8 + T Cells
Gerlach, C., Rohr, J., Perié, L., van Rooij, N., van Heijst, J. W. J., Velds, A., Urbanus, J. H. M., Naik, S. H., Jacobs, H., Beltman, J. B., et al. (2013) · Science · doi:10.1126/science.1235487 · Cited by 361 · see citing works
The fate of self-reactive B cells depends primarily on the degree of antigen receptor engagement and availability of T cell help.
Fulcher, D. A., Lyons, A. B., Korn, S., Cook, M., Koleda, C., Parish, C. R., Groth, B. F. D. S., & Basten, A. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.183.5.2313 · Cited by 246 · see citing works
Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice.
Goodnow, C. C., Crosbie, J., Adelstein, S., Lavoie, T., Smith‐Gill, S. J., Brink, R. A., Pritchard-Briscoe, H., Wotherspoon, J. S., Loblay, R. H., Raphael, K., et al. (2009) · PubMed · Cited by 221 · see citing works
Activation-Induced B Cell Fates Are Selected by Intracellular Stochastic Competition
Duffy, K. R., Wellard, C. J., Markham, J. F., Zhou, J. H. S., Holmberg, R., Hawkins, E. D., Hasbold, J., Dowling, M. R., & Hodgkin, P. D. (2012) · Science · doi:10.1126/science.1213230 · Cited by 207 · see citing works
Environmental cues dictate the fate of individual CD8+ T cells responding to infection
Plumlee, C. R., Sheridan, B., Cicek, B. B., & Lefrançois, L. (2013) · Immunity · doi:10.1016/j.immuni.2013.07.014 · Cited by 160 · see citing works
Experimental analysis by site-directed mutagenesis of somatic mutation effects on affinity and fine specificity in antibodies specific for lysozyme
Lavoie, T., Drohan, W. N., & Smith‐Gill, S. J. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.2.503 · Cited by 142 · see citing works
Imprinting the Fate of Antigen-Reactive B Cells through the Affinity of the B Cell Receptor
O’Connor, B. P., Vogel, L. A., Zhang, W., Loo, W. M., Shnider, D., Lind, E. F., Ratliff, M., Noelle, R. J., & Erickson, L. D. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.11.7723 · Cited by 104 · see citing works
Determining germinal centre B cell fate
Zotos, D., & Tarlinton, D. M. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.04.003 · Cited by 86 · see citing works
Heterogeneity in the differentiation and function of memory B cells
Taylor, J. J., Jenkins, M. K., & Pape, K. A. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.07.005 · Cited by 72 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

Germinal Center B Cell Dynamics
Mesin, L., Ersching, J., & Victora, G. D. (2016) · Immunity · doi:10.1016/j.immuni.2016.09.001 · Cited by 977 · see citing works
Naturally enhanced neutralizing breadth against SARS-CoV-2 one year after infection
Wang, Z., Muecksch, F., Schaefer-Babajew, D., Finkin, S., Viant, C., Gaebler, C., Hoffmann, H. H., Barnes, C. O., Cipolla, M., Ramos, V., et al. (2021) · Nature · doi:10.1038/s41586-021-03696-9 · Cited by 721 · see citing works
Transcriptional regulation of memory B cell differentiation
Laidlaw, B. J., & Cyster, J. G. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-00446-2 · Cited by 286 · see citing works
Multifaceted Effects of Antigen Valency on B Cell Response Composition and Differentiation In Vivo
Kato, Y., Abbott, R. K., Freeman, B. L., Haupt, S., Gröschel, B., Silva, M., Menis, S., Irvine, D. J., Schief, W. R., & Crotty, S. (2020) · Immunity · doi:10.1016/j.immuni.2020.08.001 · Cited by 267 · see citing works
Anti-SARS-CoV-2 receptor-binding domain antibody evolution after mRNA vaccination
Cho, A., Muecksch, F., Schaefer-Babajew, D. J., Wang, Z., Finkin, S., Gaebler, C., Ramos, V., Cipolla, M., Mendoza, P., Agudelo, M., et al. (2021) · Nature · doi:10.1038/s41586-021-04060-7 · Cited by 254 · see citing works
Antibody Affinity Shapes the Choice between Memory and Germinal Center B Cell Fates
Viant, C., Weymar, G. H. J., Escolano, A., Chen, S., Hartweger, H., Cipolla, M., Gazumyan, A., & Nussenzweig, M. C. (2020) · Cell · doi:10.1016/j.cell.2020.09.063 · Cited by 233 · see citing works
Memory B cells
Inoue, T., & Kurosaki, T. (2023) · Nature reviews. Immunology · doi:10.1038/s41577-023-00897-3 · Cited by 227 · see citing works
Generation of memory B cells and their reactivation
Inoue, T., Moran, I., Shinnakasu, R., Phan, T. G., & Kurosaki, T. (2018) · Immunological Reviews · doi:10.1111/imr.12640 · Cited by 181 · see citing works
Tfh cells and HIV bnAbs, an immunodominance model of the HIV neutralizing antibody generation problem
Havenar‐Daughton, C., Lee, J. H., & Crotty, S. (2017) · Immunological Reviews · doi:10.1111/imr.12512 · Cited by 170 · see citing works
Plasma cell differentiation is coupled to division-dependent DNA hypomethylation and gene regulation
Barwick, B. G., Scharer, C. D., Bally, A. P. R., & Boss, J. M. (2016) · Nature Immunology · doi:10.1038/ni.3519 · Cited by 152 · see citing works
Independent Roles of Switching and Hypermutation in the Development and Persistence of B Lymphocyte Memory
Gitlin, A. D., von Boehmer, L., Gazumyan, A., Shulman, Z., Oliveira, T. Y., & Nussenzweig, M. C. (2016) · Immunity · doi:10.1016/j.immuni.2016.01.011 · Cited by 138 · see citing works
Affinity-Restricted Memory B Cells Dominate Recall Responses to Heterologous Flaviviruses
Wong, R., Belk, J. A., Govero, J., Uhrlaub, J. L., Reinartz, D. M., Zhao, H., Errico, J. M., D’Souza, L. J., Ripperger, T. J., Nikolich‐Žugich, J., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.09.001 · Cited by 128 · see citing works
B cell activation and plasma cell differentiation are inhibited by de novo DNA methylation
Barwick, B. G., Scharer, C. D., Martinez, R. J., Price, M. J., Wein, A. N., Haines, R. R., Bally, A. P. R., Kohlmeier, J. E., & Boss, J. M. (2018) · Nature Communications · doi:10.1038/s41467-018-04234-4 · Cited by 121 · see citing works
Anti–HIV-1 B cell responses are dependent on B cell precursor frequency and antigen-binding affinity
Dosenovic, P., Kara, E. E., Pettersson, A.-K., McGuire, A. T., Gray, M. D., Hartweger, H., Thientosapol, E. S., Stamatatos, L., & Nussenzweig, M. C. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803457115 · Cited by 119 · see citing works
IL-2 imprints human naive B cell fate towards plasma cell through ERK/ELK1-mediated BACH2 repression
Hipp, N., Symington, H. L., Pastoret, C., Caron, G., Monvoisin, C., Tarte, K., Fest, T., & Delaloy, C. (2017) · Nature Communications · doi:10.1038/s41467-017-01475-7 · Cited by 114 · see citing works
The aryl hydrocarbon receptor controls cell-fate decisions in B cells
Vaidyanathan, B., Chaudhry, A., Yewdell, W. T., Angeletti, D., Yen, W.-F., Wheatley, A. K., Bradfield, C. A., McDermott, A. B., Yewdell, J. W., Rudensky, A. Y., et al. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20160789 · Cited by 111 · see citing works
Factors in B cell competition and immunodominance
Abbott, R. K., & Crotty, S. (2020) · Immunological Reviews · doi:10.1111/imr.12861 · Cited by 107 · see citing works
Emerging understanding of apoptosis in mediating mesenchymal stem cell therapy
Fu, Y., Sui, B., Xiang, L., Yan, X., Wu, D., Shi, S., & Hu, X. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03883-6 · Cited by 105 · see citing works
High-affinity memory B cells induced by SARS-CoV-2 infection produce more plasmablasts and atypical memory B cells than those primed by mRNA vaccines
Pape, K. A., Dileepan, T., Kabage, A. J., Kozysa, D., Batres, R., Evert, C., Matson, M., Lopez, S., Krueger, P. D., Graiziger, C. T., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109823 · Cited by 101 · see citing works
Self-citation
CD4+ T cell effector commitment coupled to self-renewal by asymmetric cell divisions
Nish, S. A., Zens, K. D., Kratchmarov, R., Lin, W.-H. W., Adams, W. C. T., Chen, Y.-H., Yen, B., Rothman, N. J., Bhandoola, A., Xue, H., et al. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20161046 · Cited by 100 · see citing works
Regulation of memory B and plasma cell differentiation
Shinnakasu, R., & Kurosaki, T. (2017) · Current Opinion in Immunology · doi:10.1016/j.coi.2017.03.003 · Cited by 99 · see citing works
Germinal center–dependent and –independent memory B cells produced throughout the immune response
Viant, C., Wirthmiller, T., ElTanbouly, M. A., Chen, S. T., Kara, E. E., Cipolla, M., Ramos, V., Oliveira, T. Y., Stamatatos, L., & Nussenzweig, M. C. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20202489 · Cited by 99 · see citing works
ICAMs support B cell interactions with T follicular helper cells and promote clonal selection
Zaretsky, I., Atrakchi, O., Mazor, R. D., Stoler‐Barak, L., Biram, A., Feigelson, S. W., Gitlin, A. D., Engelhardt, B., & Shulman, Z. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20171129 · Cited by 96 · see citing works
NF-kB’s contribution to B cell fate decisions
Guldenpfennig, C., Teixeiro, E., & Daniëls, M. A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1214095 · Cited by 94 · see citing works
Regulation of germinal center responses, memory B cells and plasma cell formation — an update
Corcoran, L. M., & Tarlinton, D. M. (2016) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.12.008 · Cited by 93 · see citing works
Continuous germinal center invasion contributes to the diversity of the immune response
Hägglöf, T., Cipolla, M., Loewe, M., Chen, S. T., Kara, E. E., Mesin, L., Hartweger, H., ElTanbouly, M. A., Cho, A., Gazumyan, A., et al. (2022) · Cell · doi:10.1016/j.cell.2022.11.032 · Cited by 93 · see citing works
Longitudinal dynamics of the human B cell response to the yellow fever 17D vaccine
Wec, A. Z., Haslwanter, D., Abdiche, Y., Shehata, L., Pedreño-Lopez, N., Moyer, C., Bornholdt, Z., Lilov, A., Nett, J., Jangra, R., et al. (2020) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1921388117 · Cited by 96 · see citing works
Limited access to antigen drives generation of early B cell memory while restraining the plasmablast response
Glaros, V., Rauschmeier, R., Artemov, A. V., Reinhardt, A., Ols, S., Emmanouilidi, A., Gustafsson, C., You, Y., Mirabello, C., Björklund, Å. K., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.08.017 · Cited by 91 · see citing works
Plasma cell differentiation during the germinal center reaction
Ise, W., & Kurosaki, T. (2019) · Immunological Reviews · doi:10.1111/imr.12751 · Cited by 87 · see citing works
Antibody-secreting cell destiny emerges during the initial stages of B-cell activation
Scharer, C. D., Patterson, D. G., Tian, M., Price, M. J., Hicks, S. L., & Boss, J. M. (2020) · Nature Communications · doi:10.1038/s41467-020-17798-x · Cited by 76 · see citing works
Distinct Surface Expression of Activating Receptor Ly49H Drives Differential Expansion of NK Cell Clones upon Murine Cytomegalovirus Infection
Grassmann, S. A., Pachmayr, L. O., Leube, J., Mihatsch, L., Andrä, I., Flommersfeld, S., Oduro, J. D., Čičin‐Šain, L., Schiemann, M., Floßdorf, M., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.04.015 · Cited by 74 · see citing works
When designing vaccines, consider the starting material: the human B cell repertoire
Havenar‐Daughton, C., Abbott, R. K., Schief, W. R., & Crotty, S. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.08.002 · Cited by 71 · see citing works
Transcriptional and Metabolic Control of Memory B Cells and Plasma Cells
Ripperger, T. J., & Bhattacharya, D. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-125603 · Cited by 70 · see citing works
Recall of B cell memory depends on relative locations of prime and boost immunization
Kuraoka, M., Yeh, C., Bajic, G., Kotaki, R., Song, S., Windsor, I. W., Harrison, S. C., & Kelsoe, G. H. (2022) · Science Immunology · doi:10.1126/sciimmunol.abn5311 · Cited by 66 · see citing works
Molecular regulation of peripheral B cells and their progeny in immunityPreprint
Boothby, M. R., Hodges, E. C., & Thomas, J. W. (2019) · Genes & Development · doi:10.1101/gad.320192.118 · Cited by 65 · see citing works
Instructing durable humoral immunity for COVID-19 and other vaccinable diseases
Bhattacharya, D. (2022) · Immunity · doi:10.1016/j.immuni.2022.05.004 · Cited by 63 · see citing works
Pulmonary immunity to viruses
Allie, S. R., & Randall, T. D. (2017) · Clinical Science · doi:10.1042/cs20160259 · Cited by 61 · see citing works
Spoiling for a Fight: B Lymphocytes As Initiator and Effector Populations within Tertiary Lymphoid Organs in Autoimmunity and Transplantation
Alsughayyir, J., Pettigrew, G. J., & Motallebzadeh, R. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01639 · Cited by 60 · see citing works
Supplying the trip to antibody production—nutrients, signaling, and the programming of cellular metabolism in the mature B lineage
Boothby, M. R., Brookens, S. K., Raybuck, A. L., & Cho, S. H. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00782-w · Cited by 59 · see citing works
How intrinsic and extrinsic regulators of plasma cell survival might intersect for durable humoral immunity
Robinson, M. J., Webster, R. H., & Tarlinton, D. M. (2020) · Immunological Reviews · doi:10.1111/imr.12895 · Cited by 58 · see citing works
Time-resolved transcriptomes reveal diverse B cell fate trajectories in the early response to Epstein-Barr virus infection
SoRelle, E. D., Dai, J., Reinoso-Vizcaíno, N. M., Barry, A. P., Chan, C. C. W., & Luftig, M. A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111286 · Cited by 55 · see citing works
Transcription factors regulating B cell fate in the germinal centre
Recaldin, T., & Fear, D. J. (2015) · Clinical & Experimental Immunology · doi:10.1111/cei.12702 · Cited by 54 · see citing works
Biologics to treat substance use disorders: Current status and new directions
Pravetoni, M. (2016) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2016.1212785 · Cited by 51 · see citing works
Single-Cell Analysis Suggests that Ongoing Affinity Maturation Drives the Emergence of Pemphigus Vulgaris Autoimmune Disease
Cho, A., Caldara, A. L., Ran, N. A., Menne, Z., Kauffman, R. C., Affer, M., Llovet, A., Norwood, C., Scanlan, A., Mantus, G. E., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.066 · Cited by 51 · see citing works
Avid binding by B cells to the Plasmodium circumsporozoite protein repeat suppresses responses to protective subdominant epitopes
Chatterjee, D., Lewis, F. J., Sutton, H. J., Kaczmarski, J. A., Gao, X., Cai, Y., McNamara, H. A., Jackson, C. J., & Cockburn, I. A. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108996 · Cited by 51 · see citing works
B Cell Responses against Influenza Viruses: Short-Lived Humoral Immunity against a Life-Long Threat
Guthmiller, J. J., Utset, H. A., & Wilson, P. C. (2021) · Viruses · doi:10.3390/v13060965 · Cited by 52 · see citing works
CD301b+ dendritic cells suppress T follicular helper cells and antibody responses to protein antigens
Kumamoto, Y., Hirai, T., Wong, P., Kaplan, D. H., & Iwasaki, A. (2016) · eLife · doi:10.7554/elife.17979 · Cited by 50 · see citing works
The Amount of BCL6 in B Cells Shortly after Antigen Engagement Determines Their Representation in Subsequent Germinal Centers
Robinson, M. J., Ding, Z., Pitt, C., Brodie, E. J., Quast, I., Tarlinton, D. M., & Zotos, D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.009 · Cited by 50 · see citing works
Temporal dynamics of persistent germinal centers and memory B cell differentiation following respiratory virus infection
Yewdell, W. T., Smolkin, R. M., Belcheva, K. T., Mendoza, A., Michaels, A. J., Cols, M., Angeletti, D., Yewdell, J. W., & Chaudhuri, J. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109961 · Cited by 49 · see citing works
Epigenetic recording of stimulation history reveals BLIMP1–BACH2 balance in determining memory B cell fate upon recall challenge
Shao, W., Wang, Y., Fang, Q., Shi, W., & Qi, H. (2024) · Nature Immunology · doi:10.1038/s41590-024-01900-2 · Cited by 48 · see citing works
Polymicrobial Sepsis Chronic Immunoparalysis Is Defined by Diminished Ag-Specific T Cell-Dependent B Cell Responses
Sjaastad, F. V., Condotta, S. A., Kotov, J. A., Pape, K. A., Dail, C., Danahy, D. B., Kucaba, T. A., Tygrett, L. T., Murphy, K. A., Cabrera-Pérez, J., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02532 · Cited by 47 · see citing works
Self-citation
The geography of memory B cell reactivation in vaccine‐induced immunity and in autoimmune disease relapses
Dhenni, R., & Phan, T. G. (2020) · Immunological Reviews · doi:10.1111/imr.12862 · Cited by 46 · see citing works
FB5P-seq: FACS-Based 5-Prime End Single-Cell RNA-seq for Integrative Analysis of Transcriptome and Antigen Receptor Repertoire in B and T Cells
Attaf, N., Cervera-Marzal, I., Dong, C., Gil, L., Renand, A., Spinelli, L., & Milpied, P. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00216 · Cited by 45 · see citing works
The evolutionary and functional significance of germline immunoglobulin gene variation
Pennell, M., Rodriguez, O. L., Watson, C. T., & Greiff, V. (2022) · Trends in Immunology · doi:10.1016/j.it.2022.11.001 · Cited by 44 · see citing works
Regulation of metabolic supply and demand during B cell activation and subsequent differentiation
Egawa, T., & Bhattacharya, D. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.10.003 · Cited by 43 · see citing works
Germinal center-dependent and -independent immune responses of tumor-infiltrating B cells in human cancers
Playoust, E., Remark, R., Vivier, É., & Milpied, P. J. (2023) · Cellular and Molecular Immunology · doi:10.1038/s41423-023-01060-7 · Cited by 42 · see citing works
Programming Isotype-Specific Plasma Cell Function
Higgins, B. W., McHeyzer‐Williams, L. J., & McHeyzer‐Williams, M. G. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.01.012 · Cited by 42 · see citing works
Anti- SARS-CoV-2 Receptor Binding Domain Antibody Evolution after mRNA Vaccination
Cho, A., Muecksch, F., Schaefer-Babajew, D., Wang, Z., Finkin, S., Gaebler, C., Ramos, V., Cipolla, M., Mendoza, P., Agudelo, M., et al. (2021) · doi:10.1101/2021.07.29.454333 · Cited by 275 · see citing works
Basics of memory B‐cell responses: lessons from and for the real world
Wong, R., & Bhattacharya, D. (2018) · Immunology · doi:10.1111/imm.13019 · Cited by 35 · see citing works
Regulation of B cell responses by distinct populations of CD4 T cells
Aloulou, M., & Fazilleau, N. (2019) · Biomedical Journal · doi:10.1016/j.bj.2019.06.002 · Cited by 35 · see citing works
Two-dose priming immunization amplifies humoral immunity by synchronizing vaccine delivery with the germinal center response
Bhagchandani, S. H., Yang, L., Lam, J. H., Maiorino, L., Ben‐Akiva, E., Rodrigues, K. A., Romanov, A. M., Suh, H., Aung, A., Wu, S., et al. (2024) · Science Immunology · doi:10.1126/sciimmunol.adl3755 · Cited by 34 · see citing works
Alternative B Cell Differentiation During Infection and Inflammation
Courey‐Ghaouzi, A., Kleberg, L., & Sundling, C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.908034 · Cited by 33 · see citing works
An IRF4–MYC–mTORC1 Integrated Pathway Controls Cell Growth and the Proliferative Capacity of Activated B Cells during B Cell Differentiation In Vivo
Patterson, D. G., Kania, A. K., Price, M. J., Rose, J. R., Scharer, C. D., & Boss, J. M. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100440 · Cited by 33 · see citing works
Antibodies to repeat-containing antigens in Plasmodium falciparum are exposure-dependent and short-lived in children in natural malaria infections
Raghavan, M., Kalantar, K., Duarte, E. M., Teyssier, N., Takahashi, S., Kung, A. F., Rajan, J. V., Rek, J. C., Tetteh, K. K. A., DRAKELEY, C. J., et al. (2023) · eLife · doi:10.7554/elife.81401 · Cited by 30 · see citing works
Production and use of antigen tetramers to study antigen-specific B cells
Phelps, A., Pazos‐Castro, D., Urselli, F., Grydziuszko, E., Mann-Delany, O., Fang, A., Walker, T. D., Guruge, R. T., Tomé‐Amat, J., Díaz‐Perales, A., et al. (2024) · Nature Protocols · doi:10.1038/s41596-023-00930-8 · Cited by 30 · see citing works
Self-citation
N-WASP is required for B-cell–mediated autoimmunity in Wiskott-Aldrich syndrome
Volpi, S., Santori, E., Abernethy, K., Mizui, M., Dahlberg, C. I. M., Recher, M., Capuder, K., Csizmadia, E., Ryan, D., Mathew, D., et al. (2015) · Blood · doi:10.1182/blood-2015-05-643817 · Cited by 27 · see citing works
Atypical chemokine receptor 4 shapes activated B cell fate
Kara, E. E., Bastow, C. R., McKenzie, D. R., Whyte, C. E., Fenix, K. A., Babb, R., Norton, T. S., Zotos, D., Rodda, L. B., Hermes, J. R., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20171067 · Cited by 27 · see citing works
Detection and activation of HIV broadly neutralizing antibody precursor B cells using anti-idiotypes
Bancroft, T., DeBuysscher, B. L., Weidle, C., Schwartz, A., Wall, A., Gray, M. D., Feng, J., Steach, H. R., Fitzpatrick, K. S., Gewe, M. M., et al. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190164 · Cited by 26 · see citing works
Self-citation
System-Level Scenarios for the Elucidation of T Cell-Mediated Germinal Center B Cell Differentiation
Verstegen, N. J. M., Ubels, V., Westerhoff, H. V., van Ham, S. M., & Barberis, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.734282 · Cited by 25 · see citing works
Enhancer-instructed epigenetic landscape and chromatin compartmentalization dictate a primary antibody repertoire protective against specific bacterial pathogens
Barajas-Mora, E. M., Lee, L., Lu, H., Valderrama, J. A., Bjånes, E., Nizet, V., Feeney, A. J., Hu, M., & Murre, C. (2023) · Nature Immunology · doi:10.1038/s41590-022-01402-z · Cited by 25 · see citing works
Lineage tracing reveals B cell antibody class switching is stochastic, cell-autonomous, and tuneable
Horton, M. B., Cheon, H., Duffy, K. R., Brown, D. V., Naik, S. H., Alvarado, C., Groom, J. R., Heinzel, S., & Hodgkin, P. D. (2022) · Immunity · doi:10.1016/j.immuni.2022.08.004 · Cited by 24 · see citing works
BCR signaling in germinal center B cell selection
Inoue, T., Baba, Y., & Kurosaki, T. (2024) · Trends in Immunology · doi:10.1016/j.it.2024.07.005 · Cited by 23 · see citing works
BCR Affinity Influences T-B Interactions and B Cell Development in Secondary Lymphoid Organs
Wishnie, A. J., Chwat-Edelstein, T., Attaway, M., & Vuong, B. Q. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.703918 · Cited by 23 · see citing works
Signals 1, 2 and B cell fate or: Where, when and for how long?
Turner, J. S., Benet, Z. L., & Grigorova, I. (2020) · Immunological Reviews · doi:10.1111/imr.12865 · Cited by 22 · see citing works
The strength of BCR signaling shapes terminal development of follicular helper T cells in mice
Sacquin, A., Gador, M., & Fazilleau, N. (2017) · European Journal of Immunology · doi:10.1002/eji.201746952 · Cited by 22 · see citing works
Signaling Activation and Modulation in Extrafollicular B Cell Responses
Staniek, J., & Rizzi, M. (2025) · Immunological Reviews · doi:10.1111/imr.70004 · Cited by 21 · see citing works
Phenotypic determinism and stochasticity in antibody repertoires of clonally expanded plasma cells
Neumeier, D., Yermanos, A., Agrafiotis, A., Csepregi, L., Chowdhury, T., Ehling, R. A., Kuhn, R., Cotet, T.-S., Roberto, R. B.-D., Tacchio, M. D., et al. (2021) · bioRxiv · doi:10.1073/pnas.2113766119 · Cited by 23 · see citing works
The follicular dendritic cell: At the germinal center of autoimmunity?
Krimpenfort, L., Degn, S. E., & Heesters, B. A. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113869 · Cited by 21 · see citing works
Rabies virus lipopeptide conjugated to a TLR7 agonist improves the magnitude and quality of the Th1-biased humoral immune response in mice
Liu, R., Wang, J., Yang, Y., Khan, I., & Zhu, N. (2016) · Virology · doi:10.1016/j.virol.2016.06.019 · Cited by 20 · see citing works
Single‐cell resolution of plasma cell fate programming in health and disease
Delaloy, C., Schuh, W., Jäck, H., Bonaud, A., & Espéli, M. (2021) · European Journal of Immunology · doi:10.1002/eji.202149216 · Cited by 19 · see citing works
Bach2 regulates B cell survival to maintain germinal centers and promote B cell memory
Hu, Q., Xu, T., Zhang, W., & Huang, C. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.06.009 · Cited by 19 · see citing works
Cross-Reactivity with Self-Antigen Tunes the Functional Potential of Naive B Cells Specific for Foreign Antigens
Steach, H. R., DeBuysscher, B. L., Schwartz, A., Boonyaratanakornkit, J. B., Baker, M. L., Tooley, M. R., Pease, N. A., & Taylor, J. J. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900799 · Cited by 19 · see citing works
Self-citation
Self-assembling synthetic nanoadjuvant scaffolds cross-link B cell receptors and represent new platform technology for therapeutic antibody production
Senapati, S., Darling, R. J., Ross, K. A., Wannemuehler, M. J., Narasimhan, B., & Mallapragada, S. K. (2021) · Science Advances · doi:10.1126/sciadv.abj1691 · Cited by 19 · see citing works
Defining and Studying B Cell Receptor and TCR Interactions
Rappazzo, C. G., Fernández‐Quintero, M. L., Mayer, A., Wu, N. C., Greiff, V., & Guthmiller, J. J. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2300136 · Cited by 18 · see citing works
Epigenetic gene regulation in plasma cells
Patterson, D. G., Kania, A. K., Zuo, Z., Scharer, C. D., & Boss, J. M. (2021) · Immunological Reviews · doi:10.1111/imr.12975 · Cited by 18 · see citing works
Immune-related microRNA signature for predicting prognosis and the immune microenvironment in hepatocellular carcinoma
Li, Y., He, X., Zhang, X., Xu, Y., Wu, Y.-G., & Xu, X. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118799 · Cited by 17 · see citing works
Diverging regulation of Bach2 protein and RNA expression determine cell fate in early B cell response
Hu, Q., Xu, T., Zhang, M., Zhang, H., Liu, Y., Li, H., Chen, C., Zheng, J., Zhang, Z., Li, F., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111035 · Cited by 16 · see citing works
The frequency of early-activated hapten-specific B cell subsets predicts the efficacy of vaccines for nicotine dependence
Laudenbach, M., Tucker, A. M., Runyon, S. P., Carroll, F. I., & Pravetoni, M. (2015) · Vaccine · doi:10.1016/j.vaccine.2015.09.015 · Cited by 16 · see citing works
Stem-cell dynamics and lineage topology from in vivo fate mapping in the hematopoietic system
Höfer, T., Barile, M., & Floßdorf, M. (2016) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2016.04.001 · Cited by 15 · see citing works
Structure of iglb12 Fab in complex with anti-idiotype ib3 Fab
Weidle, C., & Pancera, M. (2019) · Worldwide Protein Data Bank · doi:10.2210/pdb6ol5/pdb · Cited by 15 · see citing works
BOB.1 controls memory B-cell fate in the germinal center reaction
Levels, M. J., Fehres, C. M., van Baarsen, L. G. M., van Uden, N. O. P., Germar, K., O’Toole, T. G., Blijdorp, I. C. J., Semmelink, J. F., Doorenspleet, M. E., Bakker, A. Q., et al. (2019) · Journal of Autoimmunity · doi:10.1016/j.jaut.2019.04.011 · Cited by 14 · see citing works
Immunology of SARS-CoV-2 infections and vaccines
Schenten, D., & Bhattacharya, D. (2021) · Advances in immunology · doi:10.1016/bs.ai.2021.08.002 · Cited by 14 · see citing works
Order by chance: origins and benefits of stochasticity in immune cell fate control
Abadie, K., Pease, N. A., Wither, M. J., & Kueh, H. Y. (2019) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2019.10.013 · Cited by 14 · see citing works
Splenic Dendritic Cells and Macrophages Drive B Cells to Adopt a Plasmablast Cell Fate
McNamara, H. A., Lahoud, M. H., Cai, Y., Durrant-Whyte, J., O’Connor, J. H., Caminschi, I., & Cockburn, I. A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.825207 · Cited by 13 · see citing works
B Cell Tetramer Development for Veterinary Vaccinology
Rahe, M. C., Gustafson, K. L., & Murtaugh, M. P. (2017) · Viral Immunology · doi:10.1089/vim.2017.0073 · Cited by 13 · see citing works
Extrafollicular B Cell Responses—Is One Tent Big Enough?
Baumgarth, N. (2025) · Immunological Reviews · doi:10.1111/imr.70066 · Cited by 11 · see citing works
Validation of Ligand Tetramers for the Detection of Antigen-Specific Lymphocytes
Fitzpatrick, K. S., Degefu, H. N., Poljakov, K., Bibby, M. G., Remington, A. J., Searles, T. G., Gray, M. D., Boonyaratanakornkit, J. B., Rosato, P. C., & Taylor, J. J. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200934 · Cited by 11 · see citing works
Self-citation
Regulation of the germinal center response by nuclear receptors and implications for autoimmune diseases
Olson, W. J., Jakic, B., & Hermann‐Kleiter, N. (2020) · FEBS Journal · doi:10.1111/febs.15312 · Cited by 11 · see citing works
B cell intrinsic expression of IFNλ receptor suppresses the acute humoral immune response to experimental blood-stage malaria
Hahn, W. O., Pepper, M., & Liles, W. C. (2020) · Virulence · doi:10.1080/21505594.2020.1768329 · Cited by 11 · see citing works
TACI is required for the survival of short- and long-lived plasma cells
Funakoshi, K., Koike, T., Ise, W., Tai, Y., Narazaki, M., Kumanogoh, A., Inoue, T., & Kurosaki, T. (2025) · International Immunology · doi:10.1093/intimm/dxaf067 · Cited by 10 · see citing works

Each naïve B cell within a polyclonal repertoire produces a different frequency and pattern of effector cells (LYM6P.769)
Taylor, J. J., Pape, K. A., & Jenkins, M. K. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.192.supp.131.6
Self-citation
Analysis of the differentiation of single antigen-specific B cells early in the primary response (P1477)
Taylor, J. J., Pape, K. A., & Jenkins, M. K. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.190.supp.174.24
Self-citation
Affinity of antigen encounter and other early B-cell signals determine B-cell fate
Benson, M. J., Erickson, L. D., Gleeson, M. W., & Noelle, R. J. (2007) · Current Opinion in Immunology · doi:10.1016/j.coi.2007.04.009 · Cited by 83 · see citing works
For a single B cell, many roads to take
Mueller, K. L. (2015) · Science · doi:10.1126/science.347.6223.732-f
Memory B Cells Are Biased Towards Terminal Differentiation: A Strategy That May Prevent Repertoire Freezing
Arpin, C., Banchereau, J., & Liu, Y.-J. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.6.931 · Cited by 163 · see citing works

Authors: Taylor, J. J., Pape, K. A., Steach, H. R., & Jenkins, M. K.
Affiliations: University of Minnesota (US)
Fred Hutch Cancer Center (US)
Corresponding author: Taylor, Justin J.
ORCID: Taylor, Justin J.
Steach, Holly R.
Jenkins, Marc K.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2015-02-13
Volume: 347
Issue: 6223
Pages: 784-787
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.aaa1342
PMC: PMC4412594
OpenAlex: W2115345021
Cited by: 161
References: 24
Citations by year: 2026: 17 · 2025: 18 · 2024: 9 · 2023: 12 · 2022: 17 · 2021: 22 · 2020: 18 · 2019: 11 · 2018: 10 · 2017: 12 · 2016: 10 · 2015: 5
FWCI: 6.08
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.sciencemag.org/about/science-licenses-journal-article-reuse (vor, 365 d)
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (P01AI035296, R01AI036914, R37AI027998)
Cancer Research Institute
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
Keywords: naive B cells, apoptosis, plasma cells, germinal center cells, memory B cells, clonal heterogeneity, class switch recombination, primary immune response, B cell fate
MeSH terms: Animals, Antibody-Producing Cells, Antigens, B-Lymphocytes, Cell Differentiation, Mice, Inbred C57BL, B-Lymphocyte Subsets, Apoptosis, Immunoglobulin Class Switching, Mice, Immunity, Humoral

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Apoptosis and antigen affinity limit effector cell differentiation of a single naïve B cell

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks