The Journal of Experimental Medicine
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© The Rockefeller University Press, 0022-1007/1997/12/1997/ $5.00
The Journal of Experimental Medicine, Volume 186, Number 12, December 15, 1997 1997-2004

Article

Distinct Roles of Lymphotoxin {alpha} and the Type I Tumor Necrosis Factor (TNF) Receptor in the Establishment of Follicular Dendritic Cells from Non–Bone Marrow–derived Cells

Mitsuru Matsumoto*,{ddagger}, Yang-Xin Fu*,§, Hector Molina*,{ddagger}, Guangming Huang*,||, Jinho Kim*,§, Dori A. Thomas*,{ddagger}, Moon H. Nahm*,§, and David D. Chaplin*,{ddagger},||

From the * Center for Immunology and the Department of {ddagger} Internal Medicine, the § Department of Laboratory Medicine/Pathology, and the || Howard Hughes Medical Institute, Washington University School of Medicine, St. Louis, Missouri 63110

In mice deficient in either lymphotoxin {alpha} (LT-{alpha}) or type I tumor necrosis factor receptor (TNFR-I), organized clusters of follicular dendritic cells (FDC) and germinal centers (GC) are absent from the spleen. We investigated the role of LT-{alpha} and TNFR-I in the establishment of spleen FDC and GC structure by using reciprocal bone marrow (BM) transfer. When LT-{alpha}–deficient mice were reconstituted with wild-type BM, FDC organization and the ability to form GC were restored, indicating that the LT-{alpha}–expressing cells required to establish organized FDC are derived from BM. The role of LT-{alpha} in establishing organized FDC structure was further investigated by the transfer of complement receptor 1 and 2 (CR1/2)–deficient BM cells into LT-{alpha}–deficient mice. Organized FDC were identified with both the FDC-M1 and anti-CR1 monoclonal antibodies in these BM-chimeric mice, indicating that these cells were derived from the LT-{alpha}–deficient recipient. Thus, expression of LT-{alpha} in the BM-derived cells, but not in the non–BM-derived cells, is required for the maturation of FDC from non-BM precursor cells. In contrast, when TNFR-I–deficient mice were reconstituted with wild-type BM, they showed no detectable FDC clusters or GC formation. This indicates that TNFR-I expression on non–BM-derived cellular components is necessary for the establishment of these lymphoid structures. TNFR-I–deficient BM was able to restore FDC organization and GC formation in LT-{alpha}–deficient mice, indicating that formation of these structures does not require TNFR-I expression on BM-derived cells. The data in this study demonstrate that FDC organization and GC formation are controlled by both LT-{alpha}–expressing BM-derived cells and by TNFR-I-expressing non–BM-derived cells.

Address correspondence to Dr. David D. Chaplin, Howard Hughes Medical Institute and Department of Internal Medicine, Washington University School of Medicine, 660 S. Euclid Ave., Box 8022, St. Louis, MO 63110. Phone: 314-362-9047; FAX: 314-454-0486; E-mail: chaplin{at}im.wustl.edu

D.D. Chaplin is an investigator of the Howard Hughes Medical Institute. Portions of this work were supported by grant AI34580 from the National Institutes of Health (D.D. Chaplin).

1 Abbreviations used in this paper: BM, bone marrow; FDC, follicular dendritic cell(s); GC, germinal center(s); IC, immune complex; LN, lymph node; LT, lymphotoxin; PNA, peanut agglutinin; TNFR, TNF receptor.


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