Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response

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Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response

M Pasparakis, L Alexopoulou, V Episkopou and G Kollias
Department of Molecular Genetics, Hellenic Pasteur Institute, Athens, Greece.

To investigate the role of TNF alpha in the development of in vivo immune response we have generated TNF alpha-deficient mice by gene targeting. Homozygous mutant mice are viable and fertile, develop lymph nodes and Peyer's patches and show no apparent phenotypic abnormalities, indicating that TNF alpha is not required for normal mouse development. In the absence of TNF alpha mice readily succumb to L. monocytogenes infections and show reduced contact hypersensitivity responses. Furthermore, TNF alpha knockout mice are resistant to the systemic toxicity of LPS upon D-galactosamine sensitization, yet they remain sensitive to high doses of LPS alone. Most interestingly, TNF alpha knockout mice completely lack splenic primary B cell follicles and cannot form organized follicular dendritic cell (FDC) networks and germinal centers. However, despite the absence of B cell follicles, Ig class-switching can still occur, yet deregulated humoral immune responses against either thymus-dependent (TD) or thymus-independent (TI) antigens are observed. Complementation of TNF alpha functioning by the expression of either human or murine TNF alpha transgenes is sufficient to reconstitute these defects, establishing a physiological role for TNF alpha in regulating the development and organization of splenic follicular architecture and in the maturation of the humoral immune response.
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Berg, R. E., Crossley, E., Murray, S., Forman, J. (2003). Memory CD8+ T Cells Provide Innate Immune Protection against Listeria monocytogenes in the Absence of Cognate Antigen. J. Exp. Med. 198: 1583-1593 [Abstract] [Full Text]
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Christensen, J. P., Kauffmann, S. O., Thomsen, A. R. (2003). Deficient CD4+ T Cell Priming and Regression of CD8+ T Cell Functionality in Virus-Infected Mice Lacking a Normal B Cell Compartment. J. Immunol. 171: 4733-4741 [Abstract] [Full Text]
Park, S.-M., Park, H.-Y., Lee, T. H. (2003). Functional Effects of TNF-{alpha} on a Human Follicular Dendritic Cell Line: Persistent NF-{kappa}B Activation and Sensitization for Fas-Mediated Apoptosis. J. Immunol. 171: 3955-3962 [Abstract] [Full Text]
Endres, R., Hacker, G., Brosch, I., Pfeffer, K. (2003). Apparently Normal Tumor Necrosis Factor Receptor 1 Signaling in the Absence of the Silencer of Death Domains. Mol. Cell. Biol. 23: 6609-6617 [Abstract] [Full Text]
Choi, I.-W., Kim, Y.-S., Kim, D.-K., Choi, J.-H., Seo, K.-H., Im, S.-Y., Kwon, K.-S., Lee, M.-S., Ha, T.-Y., Lee, H.-K. (2003). Platelet-activating Factor-mediated NF-{kappa}B Dependency of a Late Anaphylactic Reaction. J. Exp. Med. 198: 145-151 [Abstract] [Full Text]
Wuthrich, M., Filutowicz, H. I., Warner, T., Deepe, G. S. Jr., Klein, B. S. (2003). Vaccine Immunity to Pathogenic Fungi Overcomes the Requirement for CD4 Help in Exogenous Antigen Presentation to CD8+ T Cells: Implications for Vaccine Development in Immune-deficient Hosts. J. Exp. Med. 197: 1405-1416 [Abstract] [Full Text]
Ehlers, S., Holscher, C., Scheu, S., Tertilt, C., Hehlgans, T., Suwinski, J., Endres, R., Pfeffer, K. (2003). The Lymphotoxin {beta} Receptor Is Critically Involved in Controlling Infections with the Intracellular Pathogens Mycobacterium tuberculosis and Listeria monocytogenes. J. Immunol. 170: 5210-5218 [Abstract] [Full Text]
Scott, K. A., Moore, R. J., Arnott, C. H., East, N., Thompson, R. G., Scallon, B. J., Shealy, D. J., Balkwill, F. R. (2003). An Anti-Tumor Necrosis Factor-{alpha} Antibody Inhibits the Development of Experimental Skin Tumors. Molecular Cancer Therapeutics 2: 445-451 [Abstract] [Full Text]
Miura, T. A., Morris, K., Ryan, S., Cook, J. L., Routes, J. M. (2003). Adenovirus E1A, Not Human Papillomavirus E7, Sensitizes Tumor Cells to Lysis by Macrophages Through Nitric Oxide- and TNF-{alpha}-Dependent Mechanisms Despite Up-Regulation of 70-kDa Heat Shock Protein. J. Immunol. 170: 4119-4126 [Abstract] [Full Text]
Pihlgren, M., Tougne, C., Bozzotti, P., Fulurija, A., Duchosal, M. A., Lambert, P.-H., Siegrist, C.-A. (2003). Unresponsiveness to Lymphoid-Mediated Signals at the Neonatal Follicular Dendritic Cell Precursor Level Contributes to Delayed Germinal Center Induction and Limitations of Neonatal Antibody Responses to T-Dependent Antigens. J. Immunol. 170: 2824-2832 [Abstract] [Full Text]
Abe, K., Yarovinsky, F. O., Murakami, T., Shakhov, A. N., Tumanov, A. V., Ito, D., Drutskaya, L. N., Pfeffer, K., Kuprash, D. V., Komschlies, K. L., Nedospasov, S. A. (2003). Distinct contributions of TNF and LT cytokines to the development of dendritic cells in vitro and their recruitment in vivo. Blood 101: 1477-1483 [Abstract] [Full Text]
Nakae, S., Komiyama, Y., Narumi, S., Sudo, K., Horai, R., Tagawa, Y.-i., Sekikawa, K., Matsushima, K., Asano, M., Iwakura, Y. (2003). IL-1-induced tumor necrosis factor-{alpha} elicits inflammatory cell infiltration in the skin by inducing IFN-{gamma}-inducible protein 10 in the elicitation phase of the contact hypersensitivity response. Int Immunol 15: 251-260 [Abstract] [Full Text]
Akassoglou, K., Douni, E., Bauer, J., Lassmann, H., Kollias, G., Probert, L. (2003). Exclusive tumor necrosis factor (TNF) signaling by the p75TNF receptor triggers inflammatory ischemia in the CNS of transgenic mice. Proc. Natl. Acad. Sci. USA 100: 709-714 [Abstract] [Full Text]
von Stebut, E., Metz, M., Milon, G., Knop, J., Maurer, M. (2003). Early macrophage influx to sites of cutaneous granuloma formation is dependent on MIP-1alpha /beta released from neutrophils recruited by mast cell-derived TNFalpha. Blood 101: 210-215 [Abstract] [Full Text]
Kuprash, D. V., Alimzhanov, M. B., Tumanov, A. V., Grivennikov, S. I., Shakhov, A. N., Drutskaya, L. N., Marino, M. W., Turetskaya, R. L., Anderson, A. O., Rajewsky, K., Pfeffer, K., Nedospasov, S. A. (2002). Redundancy in Tumor Necrosis Factor (TNF) and Lymphotoxin (LT) Signaling In Vivo: Mice with Inactivation of the Entire TNF/LT Locus versus Single-Knockout Mice. Mol. Cell. Biol. 22: 8626-8634 [Abstract] [Full Text]