B-1 and B-2 Cell-derived Immunoglobulin M Antibodies Are Nonredundant Components of the Protective Response to Influenza Virus Infection

doi:10.1084/jem.192.2.271

Published online 17 July 2000.

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© The Rockefeller University Press, 0022-1007/2000/7/271/ $5.00
The Journal of Experimental Medicine, Volume 192, Number 2, July 17, 2000 271-280

Original Article

B-1 and B-2 Cell–derived Immunoglobulin M Antibodies Are Nonredundant Components of the Protective Response to Influenza Virus Infection

Nicole Baumgarth^a, Ometa C. Herman^a, Gina C. Jager^a, Lorena E. Brown^b, Leonore A. Herzenberg^a, and Jianzhu Chen^c
^a Department of Genetics, Stanford University School of Medicine, Stanford, California 94305
^b Department of Microbiology, University of Melbourne, Victoria 3056, Australia
^c Center for Cancer Research and Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Correspondence to: Nicole Baumgarth, Center for Comparative Medicine, University of California, Davis, CA 95616. Tel:530-754-5813 Fax:530-752-7914 E-mail:nbaumgarth{at}ucdavis.edu.

We have studied the role of secreted immunoglobulin (Ig)M inprotection from infection with influenza virus and delineatedthe relative contributions of B-1 versus B-2 cell–derivedIgM in this process. Mice deficient in secreted IgM but capableof expressing surface IgM and secreting other Ig classes showsignificantly reduced virus clearance and survival rates comparedwith wild-type controls. Irradiation chimeras in which onlyeither B-1 or B-2 cells lack the ability to secrete IgM showmortality rates similar to those of mice in which neither B-1nor B-2 cells secrete IgM. Dependence on both sources of IgMfor survival is partially explained by findings in allotypechimeras that broadly cross-reactive B-1 cell–derivednatural IgM is present before infection, whereas virus strain–specific,B-2 cell–derived IgM appears only after infection. Furthermore,lack of IgM secreted from one or both sources significantlyimpairs the antiviral IgG response. Reconstitution of chimeraslacking B-1 cell–derived IgM only with IgM-containingserum from noninfected mice improved both survival rates andserum levels of virus-specific IgG. Thus, virus-induced IgMmust be secreted in the presence of natural IgM for efficientinduction of specific IgG and for immune protection, identifyingB-1 and B-2 cell–derived IgM antibodies as nonredundantcomponents of the antiviral response.

Key Words: B cells, immunoglobulin M, immune protection, CD5⁺ B cell, respiratorytract

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