Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Two distinct subpopulations of marginal zone B cells exhibit differential antibody-producing capacities and radioresistance

Cellular & Molecular Immunology volume 21, pages 393–408 (2024)Cite this article

Subjects

Abstract

Marginal zone (MZ) B cells, which are splenic innate-like B cells that rapidly secrete antibodies (Abs) against blood-borne pathogens, are composed of heterogeneous subpopulations. Here, we showed that MZ B cells can be divided into two distinct subpopulations according to their CD80 expression levels. CD80high MZ B cells exhibited greater Ab-producing, proliferative, and IL-10-secreting capacities than did CD80low MZ B cells. Notably, CD80high MZ B cells survived 2-Gy whole-body irradiation, whereas CD80low MZ B cells were depleted by irradiation and then repleted with one month after irradiation. Depletion of CD80low MZ B cells led to accelerated development of type II collagen (CII)-induced arthritis upon immunization with bovine CII. CD80high MZ B cells exhibited higher expression of genes involved in proliferation, plasma cell differentiation, and the antioxidant response. CD80high MZ B cells expressed more autoreactive B cell receptors (BCRs) that recognized double-stranded DNA or CII, expressed more immunoglobulin heavy chain sequences with shorter complementarity-determining region 3 sequences, and included more clonotypes with no N-nucleotides or with B-1a BCR sequences than CD80low MZ B cells. Adoptive transfer experiments showed that CD21+CD23+ transitional 2 MZ precursors preferentially generated CD80low MZ B cells and that a proportion of CD80low MZ B cells were converted into CD80high MZ B cells; in contrast, CD80high MZ B cells stably remained CD80high MZ B cells. In summary, MZ B cells can be divided into two subpopulations according to their CD80 expression levels, Ab-producing capacity, radioresistance, and autoreactivity, and these findings may suggest a hierarchical composition of MZ B cells with differential stability and BCR specificity.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data availability

The raw BCR sequencing and gene expression data were deposited in the NCBI database under accession number PRJNA938995.

References

  1. Allman D, Pillai S. Peripheral B cell subsets. Curr Opin Immunol. 2008;20:149–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Somers V, Dunn-Walters DK, van der Burg M, Fraussen J. Editorial: new insights into B cell subsets in health and disease. Front Immunol. 2022;13:854889.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Garraud O, Borhis G, Badr G, Degrelle S, Pozzetto B, Cognasse F, et al. Revisiting the B-cell compartment in mouse and humans: more than one B-cell subset exists in the marginal zone and beyond. BMC Immunol. 2012;13:63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Revilla IDR, Bilic I, Vilagos B, Tagoh H, Ebert A, Tamir IM, et al. The B-cell identity factor Pax5 regulates distinct transcriptional programmes in early and late B lymphopoiesis. EMBO J. 2012;31:3130–46.

    Article  Google Scholar 

  5. King JK, Ung NM, Paing MH, Contreras JR, Alberti MO, Fernando TR, et al. Regulation of marginal zone B-cell differentiation by MicroRNA-146a. Front Immunol. 2016;7:670.

    PubMed  Google Scholar 

  6. Haas KM. B-1 lymphocytes in mice and nonhuman primates. Ann N Y Acad Sci. 2015;1362:98–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Zouali M, Richard Y. Marginal zone B-cells, a gatekeeper of innate immunity. Front Immunol. 2011;2:63.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Martin F, Kearney JF. Marginal-zone B cells. Nat Rev Immunol. 2002;2:323–35.

    Article  CAS  PubMed  Google Scholar 

  9. Cerutti A, Cols M, Puga I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol. 2013;13:118–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Palm AE, Kleinau S. Marginal zone B cells: from housekeeping function to autoimmunity? J Autoimmun. 2021;119:102627.

    Article  CAS  PubMed  Google Scholar 

  11. Cinamon G, Zachariah MA, Lam OM, Foss FW Jr., Cyster JG. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol. 2008;9:54–62.

    Article  CAS  PubMed  Google Scholar 

  12. Arnon TI, Horton RM, Grigorova IL, Cyster JG. Visualization of splenic marginal zone B-cell shuttling and follicular B-cell egress. Nature. 2013;493:684–8.

    Article  CAS  PubMed  Google Scholar 

  13. Attanavanich K, Kearney JF. Marginal zone, but not follicular B cells, are potent activators of naive CD4 T cells. J Immunol. 2004;172:803–11.

    Article  CAS  PubMed  Google Scholar 

  14. Wang JH, Wu Q, Yang P, Li H, Li J, Mountz JD. et al. Type I interferon-dependent CD86(high) marginal zone precursor B cells are potent T cell costimulators in mice. Arthritis Rheum. 2011;63:1054–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ferguson AR, Youd ME, Corley RB. Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int Immunol. 2004;16:1411–22.

    Article  CAS  PubMed  Google Scholar 

  16. Cariappa A, Tang M, Parng C, Nebelitskiy E, Carroll M, Georgopoulos K, et al. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity. 2001;14:603–15.

    Article  CAS  PubMed  Google Scholar 

  17. Pillai S, Cariappa A. The follicular versus marginal zone B lymphocyte cell fate decision. Nat Rev Immunol. 2009;9:767–77.

    Article  CAS  PubMed  Google Scholar 

  18. Martin F, Chen X, Kearney JF. Development of VH81X transgene-bearing B cells in fetus and adult: sites for expansion and deletion in conventional and CD5/B1 cells. Int Immunol. 1997;9:493–505.

    Article  CAS  PubMed  Google Scholar 

  19. Park C, Kho IS, In Yang J, Kim MJ, Park S, Cha HS, et al. Positive selection of type II collagen-reactive CD80(high) marginal zone B cells in DBA/1 mice. Clin Immunol. 2017;178:64–73.

    Article  CAS  PubMed  Google Scholar 

  20. Li Y, Li H, Weigert M. Autoreactive B cells in the marginal zone that express dual receptors. J Exp Med. 2002;195:181–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kishi Y, Higuchi T, Phoon S, Sakamaki Y, Kamiya K, Riemekasten G, et al. Apoptotic marginal zone deletion of anti-Sm/ribonucleoprotein B cells. Proc Natl Acad Sci USA. 2012;109:7811–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Carey JB, Moffatt-Blue CS, Watson LC, Gavin AL, Feeney AJ. Repertoire-based selection into the marginal zone compartment during B cell development. J Exp Med. 2008;205:2043–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Palm AK, Friedrich HC, Mezger A, Salomonsson M, Myers LK, Kleinau S. Function and regulation of self-reactive marginal zone B cells in autoimmune arthritis. Cell Mol Immunol. 2015;12:493–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Marino E, Batten M, Groom J, Walters S, Liuwantara D, Mackay F, et al. Marginal-zone B-cells of nonobese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes, and present autoantigen to diabetogenic T-cells. Diabetes. 2008;57:395–404.

    Article  CAS  PubMed  Google Scholar 

  25. Lechner M, Engleitner T, Babushku T, Schmidt-Supprian M, Rad R, Strobl LJ, et al. Notch2-mediated plasticity between marginal zone and follicular B cells. Nat Commun. 2021;12:1111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lenschow DJ, Sperling AI, Cooke MP, Freeman G, Rhee L, Decker DC, et al. Differential up-regulation of the B7-1 and B7-2 costimulatory molecules after Ig receptor engagement by antigen. J Immunol. 1994;153:1990–7.

    Article  CAS  PubMed  Google Scholar 

  27. Yuseff MI, Reversat A, Lankar D, Diaz J, Fanget I, Pierobon P, et al. Polarized secretion of lysosomes at the B cell synapse couples antigen extraction to processing and presentation. Immunity. 2011;35:361–74.

    Article  CAS  PubMed  Google Scholar 

  28. Goodnow CC, Crosbie J, Adelstein S, Lavoie TB, Smith-Gill SJ, Brink RA, et al. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature. 1988;334:676–82.

    Article  CAS  PubMed  Google Scholar 

  29. Duong BH, Tian H, Ota T, Completo G, Han S, Vela JL, et al. Decoration of T-independent antigen with ligands for CD22 and Siglec-G can suppress immunity and induce B cell tolerance in vivo. J Exp Med. 2010;207:173–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kinnunen T, Chamberlain N, Morbach H, Choi J, Kim S, Craft J, et al. Accumulation of peripheral autoreactive B cells in the absence of functional human regulatory T cells. Blood. 2013;121:1595–603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Freeman GJ, Borriello F, Hodes RJ, Reiser H, Hathcock KS, Laszlo G, et al. Uncovering of functional alternative CTLA-4 counter-receptor in B7-deficient mice. Science. 1993;262:907–9.

    Article  CAS  PubMed  Google Scholar 

  32. Carnrot C, Prokopec KE, Rasbo K, Karlsson MC, Kleinau S. Marginal zone B cells are naturally reactive to collagen type II and are involved in the initiation of the immune response in collagen-induced arthritis. Cell Mol Immunol. 2011;8:296–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Won WJ, Kearney JF. CD9 is a unique marker for marginal zone B cells, B1 cells, and plasma cells in mice. J Immunol. 2002;168:5605–11.

    Article  CAS  PubMed  Google Scholar 

  34. Rubtsov AV, Swanson CL, Troy S, Strauch P, Pelanda R, Torres RM. TLR agonists promote marginal zone B cell activation and facilitate T-dependent IgM responses. J Immunol. 2008;180:3882–8.

    Article  CAS  PubMed  Google Scholar 

  35. Martin F, Oliver AM, Kearney JF. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity. 2001;14:617–29.

    Article  CAS  PubMed  Google Scholar 

  36. Meyer-Bahlburg A, Bandaranayake AD, Andrews SF, Rawlings DJ. Reduced c-myc expression levels limit follicular mature B cell cycling in response to TLR signals. J Immunol. 2009;182:4065–75.

    Article  CAS  PubMed  Google Scholar 

  37. Dominguez-Villar M, Hafler DA. Regulatory T cells in autoimmune disease. Nat Immunol. 2018;19:665–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ray A, Dittel BN. Mechanisms of regulatory B cell function in autoimmune and inflammatory diseases beyond IL-10. J Clin Med. 2017;6:12.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kieback E, Hilgenberg E, Stervbo U, Lampropoulou V, Shen P, Bunse M, et al. Thymus-derived regulatory T cells are positively selected on natural self-antigen through cognate interactions of high functional avidity. Immunity. 2016;44:1114–26.

    Article  CAS  PubMed  Google Scholar 

  40. Maseda D, Smith SH, DiLillo DJ, Bryant JM, Candando KM, Weaver CT, et al. Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J Immunol. 2012;188:1036–48.

    Article  CAS  PubMed  Google Scholar 

  41. Sun J, Wang J, Pefanis E, Chao J, Rothschild G, Tachibana I, et al. Transcriptomics identify CD9 as a marker of murine IL-10-competent regulatory B cells. Cell Rep. 2015;13:1110–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Riggs JE, Lussier A, Lee S, Appel M, Woodland R. Differential radiosensitivity among B cell subpopulations. J Immunol. 1988;141:1799–807.

    Article  CAS  PubMed  Google Scholar 

  43. Taneja N, Davis M, Choy JS, Beckett MA, Singh R, Kron SJ, et al. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J Biol Chem. 2004;279:2273–80.

    Article  CAS  PubMed  Google Scholar 

  44. Dubois F, Limou S, Chesneau M, Degauque N, Brouard S, Danger R. Transcriptional meta-analysis of regulatory B cells. Eur J Immunol. 2020;50:1757–69.

    Article  CAS  PubMed  Google Scholar 

  45. Kassambara A, Reme T, Jourdan M, Fest T, Hose D, Tarte K, et al. GenomicScape: an easy-to-use web tool for gene expression data analysis. Application to investigate the molecular events in the differentiation of B cells into plasma cells. PLoS Comput Biol. 2015;11:e1004077.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Venturi V, Kedzierska K, Tanaka MM, Turner SJ, Doherty PC, Davenport MP. Method for assessing the similarity between subsets of the T cell receptor repertoire. J Immunol Methods. 2008;329:67–80.

    Article  CAS  PubMed  Google Scholar 

  47. Kin NW, Crawford DM, Liu J, Behrens TW, Kearney JF. DNA microarray gene expression profile of marginal zone versus follicular B cells and idiotype positive marginal zone B cells before and after immunization with Streptococcus pneumoniae. J Immunol. 2008;180:6663–74.

    Article  CAS  PubMed  Google Scholar 

  48. Cariappa A, Boboila C, Moran ST, Liu H, Shi HN, Pillai S. The recirculating B cell pool contains two functionally distinct, long-lived, posttransitional, follicular B cell populations. J Immunol. 2007;179:2270–81.

    Article  CAS  PubMed  Google Scholar 

  49. Song H, Cerny J. Functional heterogeneity of marginal zone B cells revealed by their ability to generate both early antibody-forming cells and germinal centers with hypermutation and memory in response to a T-dependent antigen. J Exp Med. 2003;198:1923–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Radice E, Ameti R, Melgrati S, Foglierini M, Antonello P, Stahl RAK, et al. Marginal zone formation requires ACKR3 expression on B cells. Cell Rep. 2020;32:107951.

    Article  CAS  PubMed  Google Scholar 

  51. Grimaldi CM, Michael DJ, Diamond B. Cutting edge: expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. J Immunol. 2001;167:1886–90.

    Article  CAS  PubMed  Google Scholar 

  52. Mandik-Nayak L, Racz J, Sleckman BP, Allen PM. Autoreactive marginal zone B cells are spontaneously activated but lymph node B cells require T cell help. J Exp Med. 2006;203:1985–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Gies V, Bouis D, Martin M, Pasquali JL, Martin T, Korganow AS, et al. Phenotyping of autoreactive B cells with labeled nucleosomes in 56R transgenic mice. Sci Rep. 2017;7:13232.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kanayama N, Cascalho M, Ohmori H. Analysis of marginal zone B cell development in the mouse with limited B cell diversity: role of the antigen receptor signals in the recruitment of B cells to the marginal zone. J Immunol. 2005;174:1438–45.

    Article  CAS  PubMed  Google Scholar 

  55. Julien S, Soulas P, Garaud JC, Martin T, Pasquali JL. B cell positive selection by soluble self-antigen. J Immunol. 2002;169:4198–204.

    Article  CAS  PubMed  Google Scholar 

  56. Makowska A, Faizunnessa NN, Anderson P, Midtvedt T, Cardell S. CD1high B cells: a population of mixed origin. Eur J Immunol. 1999;29:3285–94.

    Article  CAS  PubMed  Google Scholar 

  57. Ichikawa D, Asano M, Shinton SA, Brill-Dashoff J, Formica AM, Velcich A, et al. Natural anti-intestinal goblet cell autoantibody production from marginal zone B cells. J Immunol. 2015;194:606–14.

    Article  CAS  PubMed  Google Scholar 

  58. Scharer CD, Barwick BG, Guo M, Bally APR, Boss JM. Plasma cell differentiation is controlled by multiple cell division-coupled epigenetic programs. Nat Commun. 2018;9:1698.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Gaudette BT, Roman CJ, Ochoa TA, Gomez Atria D, Jones DD, Siebel CW, et al. Resting innate-like B cells leverage sustained Notch2/mTORC1 signaling to achieve rapid and mitosis-independent plasma cell differentiation. J Clin Invest. 2021;131:e151975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Chen TT, Tsai MH, Kung JT, Lin KI, Decker T, Lee CK. STAT1 regulates marginal zone B cell differentiation in response to inflammation and infection with blood-borne bacteria. J Exp Med. 2016;213:3025–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Collins AV, Brodie DW, Gilbert RJ, Iaboni A, Manso-Sancho R, Walse B, et al. The interaction properties of costimulatory molecules revisited. Immunity. 2002;17:201–10.

    Article  CAS  PubMed  Google Scholar 

  62. Pentcheva-Hoang T, Egen JG, Wojnoonski K, Allison JP. B7-1 and B7-2 selectively recruit CTLA-4 and CD28 to the immunological synapse. Immunity. 2004;21:401–13.

    Article  CAS  PubMed  Google Scholar 

  63. Hathcock KS, Laszlo G, Pucillo C, Linsley P, Hodes RJ. Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J Exp Med. 1994;180:631–40.

    Article  CAS  PubMed  Google Scholar 

  64. Sansom DM, Manzotti CN, Zheng Y. What’s the difference between CD80 and CD86? Trends Immunol. 2003;24:314–9.

    Article  CAS  PubMed  Google Scholar 

  65. Anderson SM, Tomayko MM, Ahuja A, Haberman AM, Shlomchik MJ. New markers for murine memory B cells that define mutated and unmutated subsets. J Exp Med. 2007;204:2103–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Bar-Or A, Oliveira EM, Anderson DE, Krieger JI, Duddy M, O’Connor KC, et al. Immunological memory: contribution of memory B cells expressing costimulatory molecules in the resting state. J Immunol. 2001;167:5669–77.

    Article  CAS  PubMed  Google Scholar 

  67. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28:639–50.

    Article  CAS  PubMed  Google Scholar 

  68. Nibbs RJ, Wylie SM, Pragnell IB, Graham GJ. Cloning and characterization of a novel murine beta chemokine receptor, D6. Comparison to three other related macrophage inflammatory protein-1alpha receptors, CCR-1, CCR-3, and CCR-5. J Biol Chem. 1997;272:12495–504.

    Article  CAS  PubMed  Google Scholar 

  69. Nibbs RJ, Graham GJ. Immune regulation by atypical chemokine receptors. Nat Rev Immunol. 2013;13:815–29.

    Article  PubMed  Google Scholar 

  70. Lee S, Ko Y, Kim TJ. Homeostasis and regulation of autoreactive B cells. Cell Mol Immunol. 2020;17:561–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Reyes-Ruiz A, Dimitrov JD. How can polyreactive antibodies conquer rapidly evolving viruses? Trends Immunol. 2021;42:654–7.

    Article  CAS  PubMed  Google Scholar 

  72. Ehrenstein MR, Notley CA. The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol. 2010;10:778–86.

    Article  CAS  PubMed  Google Scholar 

  73. Zhou ZH, Zhang Y, Hu YF, Wahl LM, Cisar JO, Notkins AL. The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies. Cell Host Microbe. 2007;1:51–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Bendelac A, Bonneville M, Kearney JF. Autoreactivity by design: innate B and T lymphocytes. Nat Rev Immunol. 2001;1:177–86.

    Article  CAS  PubMed  Google Scholar 

  75. Blighe, K, Rana, S, Lewis, M. EnhancedVolcano: publication-ready volcano plots with enhanced colouring and labeling. R package version 1.16.0. 2022. https://github.com/kevinblighe/EnhancedVolcano.

  76. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102:15545–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Chaudhary N, Wesemann DR. Analyzing immunoglobulin repertoires. Front Immunol. 2018;9:462.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by National Research Foundation of Korea grant funded by the Korea government (MSIT) (2023R1A2C2004510); Korea Basic Science Institute (National Research Facilities and Equipment Center) grant (2020R1A6C101A191) of the Ministry of Education (Korea); and the BK21 FOUR Program (Graduate School Innovation) of Sungkyunkwan University.

Author information

Author notes

  1. Yeunjung Ko

    Present address: Immunology and Microbiology Graduate Program, Baylor College of Medicine, Houston, TX, 77030, USA

Authors and Affiliations

  1. Department of Immunology, Graduate School of Basic Medical Science, Sungkyunkwan University School of Medicine, Suwon, 16419, Republic of Korea

    Sujin Lee, Yeunjung Ko, Hyun Woo Lee, Won Joon Oh, Hun Gi Hong, Se Jin Im & Tae Jin Kim

  2. Department of Immunology and Molecular Medicine, Faculty of Medical Sciences, University of Sri Jayewardenepura, Nugegoda, Sri Lanka

    Dinuka Ariyaratne

Authors
  1. Sujin Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yeunjung Ko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hyun Woo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Won Joon Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hun Gi Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dinuka Ariyaratne
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Se Jin Im
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tae Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: SL, SJI, TJK. Methodology, validation, and analysis: SL, HWL, DA, WJO, HGH; Data curation: SL, DA, YK, HWL; BCR sequencing and RNA-seq data analysis: SL, DA, HWL, WJO, HGH; Writing – original draft: SL, TJK; Writing – review, editing: SL, SJI, TJK.

Corresponding authors

Correspondence to Se Jin Im or Tae Jin Kim.

Ethics declarations

Competing interests

The authors declare no competing interests.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, S., Ko, Y., Lee, H.W. et al. Two distinct subpopulations of marginal zone B cells exhibit differential antibody-producing capacities and radioresistance. Cell Mol Immunol 21, 393–408 (2024). https://doi.org/10.1038/s41423-024-01126-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41423-024-01126-0

Keywords

Search

Advanced search

Quick links