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04.12.2019 | Progress in Hematology

The ontogeny of murine B-1a cells

verfasst von: Momoko Yoshimoto

Erschienen in: International Journal of Hematology | Ausgabe 5/2020

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Abstract

It has been over 35 years since the discovery of a special subtype of B cells in mice. These IgM+ B cells are named B-1 cells, whereas conventional B cells are referred to as B-2 cells. B-1 cells express Ly-1 (CD5) and CD11b antigen, which are usually expressed in T cells and myeloid cells, respectively, reside mainly in the peritoneal and pleural cavities, and secrete natural IgM antibodies in a T cell-independent manner. B-1 cells are further categorized into CD5+ B-1a cells and CD5 B-1b cells. B-1 cells may develop through positive selection and secrete natural antibodies, including low-affinity-binding autoantibodies. Transplantation assays have revealed that the fetal liver, not the bone marrow (BM), is a major site for the production of B-1a cells, leading to the concept of a fetal origin for B-1a cells. This review introduces how the origin of B-1a cells has been explored, and describes the current state of knowledge gained through various approaches.
Literatur
1.
Zurück zum Zitat Hardy RR, Hayakawa K. A developmental switch in B lymphopoiesis. Proc Natl Acad Sci USA. 1991;88:11550–4.CrossRef Hardy RR, Hayakawa K. A developmental switch in B lymphopoiesis. Proc Natl Acad Sci USA. 1991;88:11550–4.CrossRef
2.
Zurück zum Zitat Hao Z, Rajewsky K. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J Exp Med. 2001;194:1151–64.CrossRef Hao Z, Rajewsky K. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J Exp Med. 2001;194:1151–64.CrossRef
3.
Zurück zum Zitat Ghosn EE, Yamamoto R, Hamanaka S, Yang Y, Herzenberg LA, Nakauchi H, et al. Distinct B-cell lineage commitment distinguishes adult bone marrow hematopoietic stem cells. Proc Natl Acad Sci USA. 2012;109:5394–8.CrossRef Ghosn EE, Yamamoto R, Hamanaka S, Yang Y, Herzenberg LA, Nakauchi H, et al. Distinct B-cell lineage commitment distinguishes adult bone marrow hematopoietic stem cells. Proc Natl Acad Sci USA. 2012;109:5394–8.CrossRef
4.
Zurück zum Zitat Sawai CM, Babovic S, Upadhaya S, Knapp DJ, Lavin Y, Lau CM, et al. Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals. Immunity. 2016;45:597–609.CrossRef Sawai CM, Babovic S, Upadhaya S, Knapp DJ, Lavin Y, Lau CM, et al. Hematopoietic stem cells are the major source of multilineage hematopoiesis in adult animals. Immunity. 2016;45:597–609.CrossRef
5.
Zurück zum Zitat Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature. 2015;518:547–51.CrossRef Gomez Perdiguero E, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature. 2015;518:547–51.CrossRef
6.
Zurück zum Zitat Sawen P, Eldeeb M, Erlandsson E, Kristiansen TA, Laterza C, Kokaia Z, et al. Murine HSCs contribute actively to native hematopoiesis but with reduced differentiation capacity upon aging. Elife. 2018;7:13.CrossRef Sawen P, Eldeeb M, Erlandsson E, Kristiansen TA, Laterza C, Kokaia Z, et al. Murine HSCs contribute actively to native hematopoiesis but with reduced differentiation capacity upon aging. Elife. 2018;7:13.CrossRef
7.
Zurück zum Zitat Gazit R, Mandal PK, Ebina W, Ben-Zvi A, Nombela-Arrieta C, Silberstein LE, et al. Fgd5 identifies hematopoietic stem cells in the murine bone marrow. J Exp Med. 2014;211:1315–31.CrossRef Gazit R, Mandal PK, Ebina W, Ben-Zvi A, Nombela-Arrieta C, Silberstein LE, et al. Fgd5 identifies hematopoietic stem cells in the murine bone marrow. J Exp Med. 2014;211:1315–31.CrossRef
8.
Zurück zum Zitat Holodick NE, Repetny K, Zhong X, Rothstein TL. Adult BM generates CD5+ B1 cells containing abundant N-region additions. Eur J Immunol. 2009;39:2383–94.CrossRef Holodick NE, Repetny K, Zhong X, Rothstein TL. Adult BM generates CD5+ B1 cells containing abundant N-region additions. Eur J Immunol. 2009;39:2383–94.CrossRef
9.
Zurück zum Zitat Duber S, Hafner M, Krey M, Lienenklaus S, Roy B, Hobeika E, et al. Induction of B-cell development in adult mice reveals the ability of bone marrow to produce B-1a cells. Blood. 2009;114:4960–7.CrossRef Duber S, Hafner M, Krey M, Lienenklaus S, Roy B, Hobeika E, et al. Induction of B-cell development in adult mice reveals the ability of bone marrow to produce B-1a cells. Blood. 2009;114:4960–7.CrossRef
10.
Zurück zum Zitat Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992;68:869–77.CrossRef Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992;68:869–77.CrossRef
11.
Zurück zum Zitat Graf R, Seagal J, Otipoby KL, Lam KP, Ayoub S, Zhang B, et al. BCR-dependent lineage plasticity in mature B cells. Science. 2019;363:748–53.CrossRef Graf R, Seagal J, Otipoby KL, Lam KP, Ayoub S, Zhang B, et al. BCR-dependent lineage plasticity in mature B cells. Science. 2019;363:748–53.CrossRef
12.
Zurück zum Zitat Montecino-Rodriguez E, Leathers H, Dorshkind K. Identification of a B-1 B cell-specified progenitor. Nat Immunol. 2006;7:293–301.CrossRef Montecino-Rodriguez E, Leathers H, Dorshkind K. Identification of a B-1 B cell-specified progenitor. Nat Immunol. 2006;7:293–301.CrossRef
13.
Zurück zum Zitat Barber CL, Montecino-Rodriguez E, Dorshkind K. Reduced production of B-1-specified common lymphoid progenitors results in diminished potential of adult marrow to generate B-1 cells. Proc Natl Acad Sci USA. 2011;108:13700–4.CrossRef Barber CL, Montecino-Rodriguez E, Dorshkind K. Reduced production of B-1-specified common lymphoid progenitors results in diminished potential of adult marrow to generate B-1 cells. Proc Natl Acad Sci USA. 2011;108:13700–4.CrossRef
14.
Zurück zum Zitat Ghosn EE, Waters J, Phillips M, Yamamoto R, Long BR, Yang Y, et al. Fetal hematopoietic stem cell transplantation fails to fully regenerate the B-lymphocyte compartment. Stem Cell Rep. 2016;6:137–49.CrossRef Ghosn EE, Waters J, Phillips M, Yamamoto R, Long BR, Yang Y, et al. Fetal hematopoietic stem cell transplantation fails to fully regenerate the B-lymphocyte compartment. Stem Cell Rep. 2016;6:137–49.CrossRef
15.
Zurück zum Zitat Kristiansen TA, Jaensson Gyllenback E, Zriwil A, Bjorklund T, Daniel JA, Sitnicka E, et al. Cellular barcoding links B-1a B cell potential to a fetal hematopoietic stem cell state at the single-cell level. Immunity. 2016;45:346–57.CrossRef Kristiansen TA, Jaensson Gyllenback E, Zriwil A, Bjorklund T, Daniel JA, Sitnicka E, et al. Cellular barcoding links B-1a B cell potential to a fetal hematopoietic stem cell state at the single-cell level. Immunity. 2016;45:346–57.CrossRef
16.
Zurück zum Zitat Beaudin AE, Boyer SW, Perez-Cunningham J, Hernandez GE, Derderian SC, Jujjavarapu C, et al. A transient developmental hematopoietic stem cell gives rise to innate-like B and T cells. Cell Stem Cell. 2016;19:768–83.CrossRef Beaudin AE, Boyer SW, Perez-Cunningham J, Hernandez GE, Derderian SC, Jujjavarapu C, et al. A transient developmental hematopoietic stem cell gives rise to innate-like B and T cells. Cell Stem Cell. 2016;19:768–83.CrossRef
17.
Zurück zum Zitat Herzenberg LA. Toward a layered immune system. Cell. 1989;59:953–4.CrossRef Herzenberg LA. Toward a layered immune system. Cell. 1989;59:953–4.CrossRef
18.
Zurück zum Zitat Montecino-Rodriguez E, Dorshkind K. B-1 B cell development in the fetus and adult. Immunity. 2012;36:13–21.CrossRef Montecino-Rodriguez E, Dorshkind K. B-1 B cell development in the fetus and adult. Immunity. 2012;36:13–21.CrossRef
19.
Zurück zum Zitat Godin I, Dieterlen-Lievre F, Cumano A. Emergence of multipotent hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos, beginning at 8.5 days postcoitus. Proc Natl Acad Sci USA. 1995;92:773–7.CrossRef Godin I, Dieterlen-Lievre F, Cumano A. Emergence of multipotent hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos, beginning at 8.5 days postcoitus. Proc Natl Acad Sci USA. 1995;92:773–7.CrossRef
20.
Zurück zum Zitat Yoshimoto M, Montecino-Rodriguez E, Ferkowicz MJ, Porayette P, Shelley WC, Conway SJ, et al. Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc Natl Acad Sci USA. 2011;108:1468–73.CrossRef Yoshimoto M, Montecino-Rodriguez E, Ferkowicz MJ, Porayette P, Shelley WC, Conway SJ, et al. Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc Natl Acad Sci USA. 2011;108:1468–73.CrossRef
21.
Zurück zum Zitat Kobayashi M, Shelley WC, Seo W, Vemula S, Lin Y, Liu Y, et al. Functional B-1 progenitor cells are present in the hematopoietic stem cell-deficient embryo and depend on Cbfbeta for their development. Proc Natl Acad Sci USA. 2014;111:12151–6.CrossRef Kobayashi M, Shelley WC, Seo W, Vemula S, Lin Y, Liu Y, et al. Functional B-1 progenitor cells are present in the hematopoietic stem cell-deficient embryo and depend on Cbfbeta for their development. Proc Natl Acad Sci USA. 2014;111:12151–6.CrossRef
22.
Zurück zum Zitat Montecino-Rodriguez E, Fice M, Casero D, Berent-Maoz B, Barber CL, Dorshkind K. Distinct genetic networks orchestrate the emergence of specific waves of fetal and adult B-1 and B-2 development. Immunity. 2016;45:527–39.CrossRef Montecino-Rodriguez E, Fice M, Casero D, Berent-Maoz B, Barber CL, Dorshkind K. Distinct genetic networks orchestrate the emergence of specific waves of fetal and adult B-1 and B-2 development. Immunity. 2016;45:527–39.CrossRef
23.
Zurück zum Zitat DeKoter RP, Lee HJ, Singh H. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity. 2002;16:297–309.CrossRef DeKoter RP, Lee HJ, Singh H. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity. 2002;16:297–309.CrossRef
24.
Zurück zum Zitat Rosenbauer F, Owens BM, Yu L, Tumang JR, Steidl U, Kutok JL, et al. Lymphoid cell growth and transformation are suppressed by a key regulatory element of the gene encoding PU.1. Nat Genet. 2006;38:27–37.CrossRef Rosenbauer F, Owens BM, Yu L, Tumang JR, Steidl U, Kutok JL, et al. Lymphoid cell growth and transformation are suppressed by a key regulatory element of the gene encoding PU.1. Nat Genet. 2006;38:27–37.CrossRef
25.
Zurück zum Zitat Kobayashi M, Tarnawsky SP, Wei H, Mishra A, Azevedo Portilho N, Wenzel P, et al. Hemogenic endothelial cells can transition to hematopoietic stem cells through a B-1 lymphocyte-biased state during maturation in the mouse embryo. Stem Cell Rep. 2019;13:21–30.CrossRef Kobayashi M, Tarnawsky SP, Wei H, Mishra A, Azevedo Portilho N, Wenzel P, et al. Hemogenic endothelial cells can transition to hematopoietic stem cells through a B-1 lymphocyte-biased state during maturation in the mouse embryo. Stem Cell Rep. 2019;13:21–30.CrossRef
26.
Zurück zum Zitat Hadland BK, Varnum-Finney B, Poulos MG, Moon RT, Butler JM, Rafii S, et al. Endothelium and NOTCH specify and amplify aorta-gonad-mesonephros-derived hematopoietic stem cells. J Clin Invest. 2015;125:2032–45.CrossRef Hadland BK, Varnum-Finney B, Poulos MG, Moon RT, Butler JM, Rafii S, et al. Endothelium and NOTCH specify and amplify aorta-gonad-mesonephros-derived hematopoietic stem cells. J Clin Invest. 2015;125:2032–45.CrossRef
27.
Zurück zum Zitat Hadland BK, Varnum-Finney B, Mandal PK, Rossi DJ, Poulos MG, Butler JM, et al. A common origin for B-1a and B-2 lymphocytes in clonal pre- hematopoietic stem cells. Stem Cell Rep. 2017;8:1563–72.CrossRef Hadland BK, Varnum-Finney B, Mandal PK, Rossi DJ, Poulos MG, Butler JM, et al. A common origin for B-1a and B-2 lymphocytes in clonal pre- hematopoietic stem cells. Stem Cell Rep. 2017;8:1563–72.CrossRef
28.
Zurück zum Zitat Zhou F, Li X, Wang W, Zhu P, Zhou J, He W, et al. Tracing haematopoietic stem cell formation at single-cell resolution. Nature. 2016;533:487–92.CrossRef Zhou F, Li X, Wang W, Zhu P, Zhou J, He W, et al. Tracing haematopoietic stem cell formation at single-cell resolution. Nature. 2016;533:487–92.CrossRef
29.
Zurück zum Zitat Pei W, Feyerabend TB, Rossler J, Wang X, Postrach D, Busch K, et al. Polylox barcoding reveals haematopoietic stem cell fates realized in vivo. Nature. 2017;548:456–60.CrossRef Pei W, Feyerabend TB, Rossler J, Wang X, Postrach D, Busch K, et al. Polylox barcoding reveals haematopoietic stem cell fates realized in vivo. Nature. 2017;548:456–60.CrossRef
30.
Zurück zum Zitat Yuan J, Nguyen CK, Liu X, Kanellopoulou C, Muljo SA. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science. 2012;335:1195–200.CrossRef Yuan J, Nguyen CK, Liu X, Kanellopoulou C, Muljo SA. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science. 2012;335:1195–200.CrossRef
31.
Zurück zum Zitat Copley MR, Babovic S, Benz C, Knapp DJ, Beer PA, Kent DG, et al. The Lin28b-let-7-Hmga2 axis determines the higher self-renewal potential of fetal haematopoietic stem cells. Nat Cell Biol. 2013;15:916–25.CrossRef Copley MR, Babovic S, Benz C, Knapp DJ, Beer PA, Kent DG, et al. The Lin28b-let-7-Hmga2 axis determines the higher self-renewal potential of fetal haematopoietic stem cells. Nat Cell Biol. 2013;15:916–25.CrossRef
32.
Zurück zum Zitat Zhou Y, Li YS, Bandi SR, Tang L, Shinton SA, Hayakawa K, et al. Lin28b promotes fetal B lymphopoiesis through the transcription factor Arid3a. J Exp Med. 2015;212:569–80.CrossRef Zhou Y, Li YS, Bandi SR, Tang L, Shinton SA, Hayakawa K, et al. Lin28b promotes fetal B lymphopoiesis through the transcription factor Arid3a. J Exp Med. 2015;212:569–80.CrossRef
Metadaten
Titel
The ontogeny of murine B-1a cells
verfasst von
Momoko Yoshimoto
Publikationsdatum
04.12.2019
Verlag
Springer Singapore
Erschienen in
International Journal of Hematology / Ausgabe 5/2020
Print ISSN: 0925-5710
Elektronische ISSN: 1865-3774
DOI
https://doi.org/10.1007/s12185-019-02787-8

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