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Generation of Protective T Cell-Independent Antiviral Antibody Responses in SCID Mice Reconstituted with Follicular or Marginal Zone B Cells¹

Heath M. Guay^2,3,*, Rabinarayan Mishra^2,*, Robert L. Garcea, Raymond M. Welsh^* and Eva Szomolanyi-Tsuda^4,*

^* Department of Pathology, Program in Immunology and Virology, University of Massachusetts Medical School, Worcester, MA 01655; and Department of Molecular, Cellular and Developmental Biology, University of Colorado Boulder, Boulder, CO 80309

B cells generated in the bone marrow of adult mice enter the periphery as transitional B cells and subsequently differentiate into one of two phenotypically and functionally distinct subsets, marginal zone (MZ) or follicular (Fo) B cells. Recent reports indicate, however, that in response to environmental cues, such as lymphopenia, mature Fo B cells can change to display phenotypic markers characteristic of MZ B cells. Previously, we found that splenic B cells transferred to SCID mice responded to polyoma virus (PyV) infection with T cell-independent (TI) IgM and IgG secretion, reducing the viral load and protecting mice from the lethal effect of the infection. The contribution of MZ and Fo B cell subsets to this antiviral TI-2 response, however, has not been addressed. In this study, we show that both sort-purified MZ and Fo B cells generate protective TI Ab responses to PyV infection when transferred into SCID mice. Moreover, the transferred Fo B cells in the spleens of the PyV-infected SCID mice change phenotype, with many of them displaying MZ B cell characteristics. These findings demonstrate the plasticity of the B cell subsets in virus-infected hosts and show for the first time that B cells derived exclusively from Fo B cells can effectively function in antiviral TI-2 responses.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported by National Institute of Health Grants CA66644 and AI073651, Training Grant AI07272, and Institutional Diabetes Endocrinology Research Center Grant DK32520.

² H.M.G. and R.M. equally contributed to this article.

³ Current address: Inflammation, Wyeth Research, Cambridge, MA 02140.

⁴ Address correspondence and reprint requests to Dr. Eva Szomolanyi-Tsuda, University of Massachusetts Medical School, 55 Lake Avenue North, Worcester MA 01655. E-mail address: Eva.Szomolanyi-Tsuda{at}umassmed.edu

⁵ Abbreviations used in this paper: MZ, marginal zone; Fo, follicular; TI, T cell independent; TD, T cell dependent; KO, knockout; PyV, polyoma virus; BAFF, B cell-activating factor of the TNF family; NP, 4-hydroxy-3-nitrophenyl acetyl.