The Journal of Experimental Medicine
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Published online 8 December 2003 doi:10.1084/jem.20031498
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© Rockefeller University Press, 0022-1007/2003/12/1923 $5.00
The Journal of Experimental Medicine, Volume 198, Number 12, 1923-1935

Functional Heterogeneity of Marginal Zone B Cells Revealed by Their Ability to Generate Both Early Antibody-forming Cells and Germinal Centers with Hypermutation and Memory in Response to a T-dependent Antigen

Haifeng Song and Jan Cerny

Department of Microbiology and Immunology, University of Maryland, School of Medicine, Baltimore, MD 21201

Address correspondence to Jan Cerny, Dept. of Microbiology and Immunology, University of Maryland, School of Medicine, 655 West Baltimore St., Rm. 13-015 BRB, Baltimore, MD 21201-1559. Phone: (410) 706-7114; Fax: (410) 706-2129; email: ojone002{at}umaryland.edu

Marginal zone (MZ) B cells play a major role in the first-line responses against blood-born T-independent bacterial antigens (TI), but the full scope of their immune functions is not known. Here we compare the responses of MZ and follicular (FO) B cells to a T-dependent antigen (TD), hapten–(4-hydroxy-3-nitrophenyl)acetyl (NP) coupled to chicken {gamma}-globulin, in a cell transfer system. Consistent with the conventional paradigm, MZ B cells but not FO B cells rapidly generated the early burst of NP-specific antibody-forming cells (AFC), high levels of IgM Ab, and early IgG with relatively high affinity to NP. However, MZ B cells were also capable of forming germinal centers (GCs) albeit with a delay, compared with FO B cells. The early AFCs and the GCs originated from different MZ precursors, but the MZ- and FO-derived GCs were similar in VH gene repertoire, somatic mutation, and production of late AFC and IgG Ab. Surprisingly, the MZ but not the FO memory response included IgM Ab. We conclude that MZ B cells are heterogeneous, comprising cells for both early AFC response and GC/memory pathway against TD antigens.

Key Words: B cells • marginal zone • T-dependent Ag • antibody-forming cells • germinal center

Abbreviations used in this paper: AFC, antibody-forming cell; BCR, B cell receptor; CGG, chicken gammaglobulin; CSR, class-switch recombination; DN, double negative; FO, follicular; GC, germinal center; HRP, horseradish peroxidase; MZ, marginal zone; NIP, 4-hydroxy-5-iodo-3-nitrophenyl acetyl; NP, (4-hydroxy-3-nitrophenyl)acetyl; PALS, periarteriolar lymphoid sheath; PNA, peanut agglutinin; R/S, replacement to silent; SA-ALPH, Streptavidin conjugated to alkaline phosphatase; SHM, somatic hypermutation; TD, T-dependent Ag; TI, T-independent Ag; TI-I, TI type I Ag; TI-II, TI type II Ag.


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