The Journal of Experimental Medicine
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Published 21 July 2003. doi:10.1084/jem.20030684
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© Rockefeller University Press, 0022-1007/2003/7/333 $5.00
The Journal of Experimental Medicine, Volume 198, Number 2, 333-340

Macrophages Control the Retention and Trafficking of B Lymphocytes in the Splenic Marginal Zone

Mikael C.I. Karlsson1, Rodolphe Guinamard1,3, Silvia Bolland1,4, Marko Sankala5, Ralph M. Steinman2 and Jeffrey V. Ravetch1

1 Laboratory of Molecular Genetics and Immunology, The Rockefeller University, New York, NY 10021
2 Cellular Physiology and Immunology, The Rockefeller University, New York, NY 10021
3 Centre d'Immunologie de Marseille Luminy, CNRS-INSERM-Universite de la Mediterranee, 13288 Marseille, France
4 Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases/National Institutes of Health, Rockville, MD 20852
5 Department of Medical Biochemistry and Biophysics, Division of Matrix Biology, The Karolinska Institute, 17177 Stockholm, Sweden

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: ravetch{at}rockefeller.edu

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.

Key Words: SHIP • Btk • MARCO • migration • Staphylococcus aureus


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