The marginal zone of the spleen is a precisely ordered region that contains specialized subsets of B lymphocytes and macrophages. Disruption of the negative signaling inositol phosphatase, SH2-containing inositol-5-phosphatase 1 (SHIP), results in the loss of marginal zone B cells (MZBs) with reorganization of marginal zone macrophages (MZMOs) to the red pulp of the spleen. This primary macrophage defect, as revealed by selectively depleting SHIP in myeloid cells shows that MZMOs are specifically required for the retention of MZBs. The MZMO phenotype was reverted in SHIP/Bruton's tyrosine kinase (Btk) double knockout mice, thus identifying the Btk activating pathway as an essential component being regulated by SHIP. Furthermore, we identified a direct interaction between the MARCO scavenger receptor on MZMOs and MZBs. Activation or disruption of this interaction results in MZB migration to the follicle. The migration of the MZMOs was further studied after the response to Staphylococcus aureus, which induced MZMOs to move into the red pulp while MZBs migrated into the follicular zone. The marginal zone is therefore a dynamic structure in which retention and trafficking of B cells requires specific macrophage–B cell interactions.
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21 July 2003
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July 21 2003
Macrophages Control the Retention and Trafficking of B Lymphocytes in the Splenic Marginal Zone
Mikael C.I. Karlsson,
Mikael C.I. Karlsson
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
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Rodolphe Guinamard,
Rodolphe Guinamard
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
3Centre d'Immunologie de Marseille Luminy, CNRS-INSERM-Universite de la Mediterranee, 13288 Marseille, France
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Silvia Bolland,
Silvia Bolland
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
4Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases/National Institutes of Health, Rockville, MD 20852
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Marko Sankala,
Marko Sankala
5Department of Medical Biochemistry and Biophysics, Division of Matrix Biology, The Karolinska Institute, 17177 Stockholm, Sweden
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Ralph M. Steinman,
Ralph M. Steinman
2Cellular Physiology and Immunology, The Rockefeller University, New York, NY 10021
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Jeffrey V. Ravetch
Jeffrey V. Ravetch
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
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Mikael C.I. Karlsson
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
Rodolphe Guinamard
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
3Centre d'Immunologie de Marseille Luminy, CNRS-INSERM-Universite de la Mediterranee, 13288 Marseille, France
Silvia Bolland
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
4Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases/National Institutes of Health, Rockville, MD 20852
Marko Sankala
5Department of Medical Biochemistry and Biophysics, Division of Matrix Biology, The Karolinska Institute, 17177 Stockholm, Sweden
Ralph M. Steinman
2Cellular Physiology and Immunology, The Rockefeller University, New York, NY 10021
Jeffrey V. Ravetch
1Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
Address correspondence to Jeffrey V. Ravetch, Laboratory of Molecular Genetics and Immunology, The Rockefeller University, Box 98, 1230 York Avenue, New York, NY 10021. Phone: 212-327-7321; Fax: 212-327-7318; E-mail: [email protected]
*
Abbreviations used in this paper: Btk, Bruton's tyrosine kinase; ES, embryonic stem; MZB, marginal zone B cell; MZMO, marginal zone macrophage; SHIP, SH2-containing inositol-5-phosphatase 1.
Received:
April 25 2003
Revision Received:
April 25 2003
Accepted:
May 20 2003
Online ISSN: 1540-9538
Print ISSN: 0022-1007
The Rockefeller University Press
2003
J Exp Med (2003) 198 (2): 333–340.
Article history
Received:
April 25 2003
Revision Received:
April 25 2003
Accepted:
May 20 2003
Citation
Mikael C.I. Karlsson, Rodolphe Guinamard, Silvia Bolland, Marko Sankala, Ralph M. Steinman, Jeffrey V. Ravetch; Macrophages Control the Retention and Trafficking of B Lymphocytes in the Splenic Marginal Zone . J Exp Med 21 July 2003; 198 (2): 333–340. doi: https://doi.org/10.1084/jem.20030684
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