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Bmi1 Maintains the Self-Renewal Property of Innate-like B Lymphocytes

Michihiro Kobayashi, Yang Lin, Akansha Mishra, Chris Shelly, Rui Gao, Colton W. Reeh, Paul Zhiping Wang, Rongwen Xi, Yunlong Liu, Pamela Wenzel, Eliver Ghosn, Yan Liu and Momoko Yoshimoto
J Immunol April 29, 2020, ji2000030; DOI: https://doi.org/10.4049/jimmunol.2000030
Michihiro Kobayashi
*Center for Stem Cell Research and Regenerative Medicine, Institute for Molecular Medicine, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030;
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Yang Lin
†Wells Center for Pediatric Research, Department of Pediatrics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Akansha Mishra
†Wells Center for Pediatric Research, Department of Pediatrics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Chris Shelly
†Wells Center for Pediatric Research, Department of Pediatrics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Rui Gao
†Wells Center for Pediatric Research, Department of Pediatrics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Colton W. Reeh
*Center for Stem Cell Research and Regenerative Medicine, Institute for Molecular Medicine, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030;
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Paul Zhiping Wang
‡Center for Computational Biology and Bioinformatics, Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Rongwen Xi
§National Institute of Biological Science, Beijing 102206, China;
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Yunlong Liu
‡Center for Computational Biology and Bioinformatics, Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Pamela Wenzel
*Center for Stem Cell Research and Regenerative Medicine, Institute for Molecular Medicine, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030;
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Eliver Ghosn
¶Department of Medicine, Lowance Center for Human Immunology, Emory Vaccine Center, Emory University, Atlanta, GA 30322; and
‖Department of Pediatrics, Lowance Center for Human Immunology, Emory Vaccine Center, Emory University, Atlanta, GA 30322
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Yan Liu
†Wells Center for Pediatric Research, Department of Pediatrics, Indiana University School of Medicine, Indianapolis, IN 46202;
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Momoko Yoshimoto
*Center for Stem Cell Research and Regenerative Medicine, Institute for Molecular Medicine, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030;
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Key Points

  • Bmi1 regulates self-renewal ability of B-1a cells via Ink4-Arf and possibly Kdm5b.

  • Bmi1 may be involved in the developmental process of B-1 progenitors to B-1a cells.

  • FALCs, the niche for B-1a cells, are not altered in Bmi1−/− mice.

Abstract

The self-renewal ability is a unique property of fetal-derived innate-like B-1a lymphocytes, which survive and function without being replenished by bone marrow (BM) progenitors. However, the mechanism by which IgM-secreting mature B-1a lymphocytes self-renew is poorly understood. In this study, we showed that Bmi1 was critically involved in this process. Although Bmi1 is considered essential for lymphopoiesis, the number of mature conventional B cells was not altered when Bmi1 was deleted in the B cell lineage. In contrast, the number of peritoneal B-1a cells was significantly reduced. Peritoneal cell transfer assays revealed diminished self-renewal ability of Bmi1-deleted B-1a cells, which was restored by additional deletion of Ink4-Arf, the well-known target of Bmi1. Fetal liver cells with B cell–specific Bmi1 deletion failed to repopulate peritoneal B-1a cells, but not other B-2 lymphocytes after transplantation assays, suggesting that Bmi1 may be involved in the developmental process of B-1 progenitors to mature B-1a cells. Although Bmi1 deletion has also been shown to alter the microenvironment for hematopoietic stem cells, fat-associated lymphoid clusters, the reported niche for B-1a cells, were not impaired in Bmi1−/− mice. RNA expression profiling suggested lysine demethylase 5B (Kdm5b) as another possible target of Bmi1, which was elevated in Bmi1−/− B-1a cells in a stress setting and might repress B-1a cell proliferation. Our work has indicated that Bmi1 plays pivotal roles in self-renewal and maintenance of fetal-derived B-1a cells.

Footnotes

  • This work was supported by National Institute of Allergy and Infectious Diseases R56AI110831 and R01AI121197 (to M.Y.).

  • The microarray data presented in this article have been submitted to the Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE97202.

  • The online version of this article contains supplemental material.

  • Received January 9, 2020.
  • Accepted April 6, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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Bmi1 Maintains the Self-Renewal Property of Innate-like B Lymphocytes
Michihiro Kobayashi, Yang Lin, Akansha Mishra, Chris Shelly, Rui Gao, Colton W. Reeh, Paul Zhiping Wang, Rongwen Xi, Yunlong Liu, Pamela Wenzel, Eliver Ghosn, Yan Liu, Momoko Yoshimoto
The Journal of Immunology April 29, 2020, ji2000030; DOI: 10.4049/jimmunol.2000030

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Bmi1 Maintains the Self-Renewal Property of Innate-like B Lymphocytes
Michihiro Kobayashi, Yang Lin, Akansha Mishra, Chris Shelly, Rui Gao, Colton W. Reeh, Paul Zhiping Wang, Rongwen Xi, Yunlong Liu, Pamela Wenzel, Eliver Ghosn, Yan Liu, Momoko Yoshimoto
The Journal of Immunology April 29, 2020, ji2000030; DOI: 10.4049/jimmunol.2000030
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Print ISSN 0022-1767        Online ISSN 1550-6606