Cellular Dynamics of Memory B Cell Populations: IgM+ and IgG+ Memory B Cells Persist Indefinitely As Quiescent Cells

Overview

Journal J Immunol

Specialty Allergy & Immunology

Date 2015 Oct 7

PMID 26438523

Citations 37

Authors

Derek D Jones

Joel R Wilmore

David Allman

Affiliations

Soon will be listed here.

Abstract

Despite their critical role in long-term immunity, the life span of individual memory B cells remains poorly defined. Using a tetracycline-regulated pulse-chase system, we measured population turnover rates and individual t1/2 of pre-established Ag-induced Ig class-switched and IgM-positive memory B cells over 402 d. Our results indicate that, once established, both IgG-positive and less frequent IgM-positive memory populations are exceptionally stable, with little evidence of attrition or cellular turnover. Indeed, the vast majority of cells in both pools exhibited t1/2 that appear to exceed the life span of the mouse, contrasting dramatically with mature naive B cells. These results indicate that recall Ab responses are mediated by stable pools of extremely long-lived cells, and suggest that Ag-experienced B cells employ remarkably efficient survival mechanisms.

Citing Articles

Reduced response to SARS-CoV-2 vaccination is associated with impaired immunoglobulin class switch recombination in SLE patients.

Montamat G, Meehan C, Bradford H, Yildirim R, Guimaraes F, Johnson M Clin Exp Immunol. 2024; 219(1).

PMID: 39658056 PMC: 11773804. DOI: 10.1093/cei/uxae119.

B Cell Receptor Transgenic Mice as Tools to Study Memory B Cells.

Quast I Methods Mol Biol. 2024; 2826:131-139.

PMID: 39017890 DOI: 10.1007/978-1-0716-3950-4_10.

Poly(I:C) and R848 ligands show better adjuvanticity to induce B and T cell responses against the antigen(s).

Tandel N, Patel D, Thakkar M, Shah J, Tyagi R, Dalai S Heliyon. 2024; 10(5):e26887.

PMID: 38455541 PMC: 10918150. DOI: 10.1016/j.heliyon.2024.e26887.

Envelope protein-specific B cell receptors direct lentiviral vector tropism in vivo.

Takano K, Wong A, Brown R, Situ K, Chua B, Abu A Mol Ther. 2024; 32(5):1311-1327.

PMID: 38449314 PMC: 11081870. DOI: 10.1016/j.ymthe.2024.03.002.

Evaluation of quantitative biomarkers of aging in human PBMCs.

Owen B, Phie J, Huynh J, Needham S, Fraser C Front Aging. 2023; 4:1260502.

PMID: 37780865 PMC: 10540680. DOI: 10.3389/fragi.2023.1260502.

References

Anderson S, Tomayko M, Ahuja A, Haberman A, Shlomchik M . New markers for murine memory B cells that define mutated and unmutated subsets. J Exp Med. 2007; 204(9):2103-14. PMC: 2118690. DOI: 10.1084/jem.20062571. View

Tomayko M, Steinel N, Anderson S, Shlomchik M . Cutting edge: Hierarchy of maturity of murine memory B cell subsets. J Immunol. 2010; 185(12):7146-50. PMC: 3133669. DOI: 10.4049/jimmunol.1002163. View

Pape K, Taylor J, Maul R, Gearhart P, Jenkins M . Different B cell populations mediate early and late memory during an endogenous immune response. Science. 2011; 331(6021):1203-7. PMC: 3993090. DOI: 10.1126/science.1201730. View

Taylor J, Pape K, Jenkins M . A germinal center-independent pathway generates unswitched memory B cells early in the primary response. J Exp Med. 2012; 209(3):597-606. PMC: 3302224. DOI: 10.1084/jem.20111696. View

Good-Jacobson K, Song E, Anderson S, Sharpe A, Shlomchik M . CD80 expression on B cells regulates murine T follicular helper development, germinal center B cell survival, and plasma cell generation. J Immunol. 2012; 188(9):4217-25. PMC: 3331930. DOI: 10.4049/jimmunol.1102885. View

Kaji T, Ishige A, Hikida M, Taka J, Hijikata A, Kubo M . Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J Exp Med. 2012; 209(11):2079-97. PMC: 3478929. DOI: 10.1084/jem.20120127. View

Yates J, Racine R, McBride K, Winslow G . T cell-dependent IgM memory B cells generated during bacterial infection are required for IgG responses to antigen challenge. J Immunol. 2013; 191(3):1240-9. PMC: 3720767. DOI: 10.4049/jimmunol.1300062. View

Zuccarino-Catania G, Sadanand S, Weisel F, Tomayko M, Meng H, Kleinstein S . CD80 and PD-L2 define functionally distinct memory B cell subsets that are independent of antibody isotype. Nat Immunol. 2014; 15(7):631-7. PMC: 4105703. DOI: 10.1038/ni.2914. View

Chernova I, Jones D, Wilmore J, Bortnick A, Yucel M, Hershberg U . Lasting antibody responses are mediated by a combination of newly formed and established bone marrow plasma cells drawn from clonally distinct precursors. J Immunol. 2014; 193(10):4971-9. PMC: 4234148. DOI: 10.4049/jimmunol.1401264. View

10.

McHeyzer-Williams L, Milpied P, Okitsu S, McHeyzer-Williams M . Class-switched memory B cells remodel BCRs within secondary germinal centers. Nat Immunol. 2015; 16(3):296-305. PMC: 4333102. DOI: 10.1038/ni.3095. View

11.

Lindner C, Thomsen I, Wahl B, Ugur M, Sethi M, Friedrichsen M . Diversification of memory B cells drives the continuous adaptation of secretory antibodies to gut microbiota. Nat Immunol. 2015; 16(8):880-8. DOI: 10.1038/ni.3213. View

12.

Maruyama M, Lam K, Rajewsky K . Memory B-cell persistence is independent of persisting immunizing antigen. Nature. 2000; 407(6804):636-42. DOI: 10.1038/35036600. View

13.

Fearon D, Manders P, Wagner S . Arrested differentiation, the self-renewing memory lymphocyte, and vaccination. Science. 2001; 293(5528):248-50. DOI: 10.1126/science.1062589. View

14.

Barrington R, Pozdnyakova O, Zafari M, Benjamin C, Carroll M . B lymphocyte memory: role of stromal cell complement and FcgammaRIIB receptors. J Exp Med. 2002; 196(9):1189-99. PMC: 2194107. DOI: 10.1084/jem.20021110. View

15.

Bernasconi N, Traggiai E, Lanzavecchia A . Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 2002; 298(5601):2199-202. DOI: 10.1126/science.1076071. View

16.

Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, Ahmed R . Cutting edge: long-term B cell memory in humans after smallpox vaccination. J Immunol. 2003; 171(10):4969-73. DOI: 10.4049/jimmunol.171.10.4969. View

17.

Gowans J, UHR J . The carriage of immunological memory by small lymphocytes in the rat. J Exp Med. 1966; 124(5):1017-30. PMC: 2138263. DOI: 10.1084/jem.124.5.1017. View

18.

Sprent J, Basten A . Circulating T and B lymphocytes of the mouse. II. Lifespan. Cell Immunol. 1973; 7(1):40-59. DOI: 10.1016/0008-8749(73)90181-0. View

19.

Jack R, Rajewsky K . Idiotypic analysis of the response of C57BL/6 mice to the (4-hydroxy-3-nitrophenyl)acetyl group. Eur J Immunol. 1977; 7(8):559-65. DOI: 10.1002/eji.1830070813. View

20.

Reth M, Hammerling G, Rajewsky K . Analysis of the repertoire of anti-NP antibodies in C57BL/6 mice by cell fusion. I. Characterization of antibody families in the primary and hyperimmune response. Eur J Immunol. 1978; 8(6):393-400. DOI: 10.1002/eji.1830080605. View