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B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities

Nature Immunology volume 7, pages 1116–1124 (2006)Cite this article

Abstract

The present paradigm dictates that phagocytosis is accomplished mainly by 'professional' phagocytes (such as macrophages and monocytes), whereas B cells lack phagocytic capabilities. Here we demonstrate that B cells from teleost fish have potent in vitro and in vivo phagocytic activities. Particle uptake by B cells induced activation of 'downstream' degradative pathways, leading to 'phagolysosome' formation and intracellular killing of ingested microbes. Those results indicate a previously unknown function for B cells in the innate immunity of these primitive animals. A considerable proportion of Xenopus laevis B cells were also phagocytic. Our findings support the idea that B cells evolved from an ancestral phagocytic cell type and provide an evolutionary framework for understanding the close relationship between mammalian B lymphocytes and macrophages.

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Figure 1: Phagocytosis by IgM+ and IgM− trout cells.
Figure 2: Gene expression profiles of phagocytic and nonphagocytic IgM+ and IgM− cells.
Figure 3: TEM analysis of phagocytic IgM+ and IgM− cells.
Figure 4: SEM analysis of phagocytic IgM+ and IgM− cells.
Figure 5: Parameters influencing the phagocytic activity of B cells.
Figure 6: Influence of antibody and complement opsonization on the uptake of A. hydrophila by IgM+ and IgM− cells.
Figure 7: Phagolysosome formation and intracellular killing by phagocytic B cells and granulocytes.
Figure 8: Phagocytosis by IgM+ and IgM− X. laevis cells.

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Acknowledgements

We thank X. Zhao (Biomedical Imaging Core, School of Medicine, University of Pennsylvania), R. Meade and N. Shah (Biomedical Imaging Core, School of Medicine, University of Pennsylvania) for technical assistance; and A. Bhandoola, L. Bello, P. Scott and A. Thomas-Tikhonenko for critical reading of the manuscript. Supported by the National Science Foundation (MCB-0417078 to J.O.S.) and the National Research Initiative of the US Department of Agriculture Cooperative State Research, Education and Extension Service (2004-01599 to J.O.S.).

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Author notes

  1. Daniel R Barreda and Yong-An Zhang: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, 19104, Pennsylvania, USA

    Jun Li, Yong-An Zhang, Hani Boshra & J Oriol Sunyer

  2. Hematology and Oncology, School of Medicine, University of Pennsylvania, Philadelphia, 19104, Pennsylvania, USA

    Daniel R Barreda

  3. Department of Cardiothoracic Surgery, Washington University School of Medicine, St. Louis, 63110, Missouri, USA

    Andrew E Gelman

  4. Research Division, Clear Springs Foods, Buhl, 83316, Idaho, USA

    Scott LaPatra

  5. Department of Cell Biology, Unit of Animal Physiology, Physiology and Immunology, Universitat Autonoma de Barcelona, Bellaterra, 08193, Spain

    Lluis Tort

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Correspondence to J Oriol Sunyer.

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Supplementary information

Supplementary Fig. 1

Characterization of trout B cells. (PDF 180 kb)

Supplementary Fig. 2

Phagocytic IgM+ cells are non-adherent. (PDF 105 kb)

Supplementary Fig. 3

Catfish blood B cells are phagocytic. (PDF 2149 kb)

Supplementary Fig. 4

Amino acid sequence alignment. (PDF 148 kb)

Supplementary Fig. 5

Ultrastructural features of bead uptake by trout phagocytic IgM+ cells. (PDF 166 kb)

Supplementary Fig. 6

In vivo analysis of phagocytosis by peritoneal cavity trout IgM+ and IgM− cells. (PDF 90 kb)

Supplementary Table 1

Primers used for RT-PCR. (PDF 45 kb)

Supplementary Methods (PDF 161 kb)

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Li, J., Barreda, D., Zhang, YA. et al. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol 7, 1116–1124 (2006). https://doi.org/10.1038/ni1389

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