Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal

doi:10.1084/jem.177.4.925

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Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal

EA Ranheim and TJ Kipps
Department of Medicine, University of California, San Diego, La Jolla 92093-0663.

Cognate interactions between antigen-presenting B and T cells play crucial roles in immunologic responses. T cells that have been activated via the crosslinking of CD3 are able to induce B cell proliferation and immunoglobulin secretion in a major histocompatibility complex-unrestricted and contact-dependent manner. We find that such activated human CD4+ T cells, but not control Ig- treated T cells, may induce normal or leukemic B cells to express B7/BB1 and significantly higher levels of CD54 intercellular adhesion molecule 1 via a process that also requires direct cell-cell contact. To discern what cell surface molecule(s) may be responsible for signalling B cells to express B7/BB1, we added various monoclonal antibodies (mAbs) specific for T or B cell accessory molecules or control mAbs to cocultures of alpha-CD3-activated T cells and resting B cells. We find that only alpha-CD40 mAbs can significantly inhibit the increased expression of B7/BB1, suggesting that the ligand for CD40 expressed on activated T cells may be an important inducer of B7/BB1 expression. Subsequent experiments in fact demonstrate that alpha-CD40 mAbs, but not control mAbs, induce changes in B cell phenotype similar to those induced by activated T cells when the mAbs are presented on Fc gamma RII (CDw32)-expressing L cells. These phenotypic changes have significant effects on B cell function. Whereas chronic lymphocytic leukemia (CLL) B cells normally are very poor stimulators in allogeneic mixed lymphocyte reactions (MLRs), CLL-B cells preactivated via CD40 crosslinking are significantly better presenters of alloantigen, affecting up to 30-fold-greater stimulation of T cell proliferation than that induced by control treated or nontreated CLL-B cells. Similarly, the MLR of T cells stimulated by allogeneic nonleukemic B cells can be enhanced significantly if the stimulator B cells are preactivated via CD40 crosslinking. The enhanced MLR generated by such preactivated B cells may be inhibited by blocking B7/BB1-CD28 interaction with CTLA4Ig. These studies demonstrate a novel, CD40- dependent pathway for inducing B cell expression of B7/BB1 and enhancing B cell antigen-presenting cell activity that can be initiated via cell-cell contact with alpha-CD3-stimulated CD4+ T cells.
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Kweon, M.-N., Fujihashi, K., Wakatsuki, Y., Koga, T., Yamamoto, M., McGhee, J. R., Kiyono, H. (1999). Mucosally Induced Systemic T Cell Unresponsiveness to Ovalbumin Requires CD40 Ligand-CD40 Interactions. J. Immunol. 162: 1904-1909 [Abstract] [Full Text]
Judge, T. A., Wu, Z., Zheng, X.-G., Sharpe, A. H., Sayegh, M. H., Turka, L. A. (1999). The Role of CD80, CD86, and CTLA4 in Alloimmune Responses and the Induction of Long-Term Allograft Survival. J. Immunol. 162: 1947-1951 [Abstract] [Full Text]
Caligaris-Cappio, F., Hamblin, T. J. (1999). B-Cell Chronic Lymphocytic Leukemia: A Bird of a Different Feather. JCO 17: 399-399 [Abstract] [Full Text]
ROSSINI, A. A., GREINER, D. L., MORDES, J. P. (1999). Induction of Immunologic Tolerance for Transplantation. Physiol. Rev. 79: 99-141 [Abstract] [Full Text]
Lang, S., Whiteside, T. L., Lebeau, A., Zeidler, R., Mack, B., Wollenberg, B. (1999). Impairment of T-Cell Activation in Head and Neck Cancer In Situ and In Vitro: Strategies for an Immune Restoration. Arch Otolaryngol Head Neck Surg 125: 82-88 [Abstract] [Full Text]
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Ding, L., Shevach, E. M. (1998). Differential Effects of CD28 Engagement and IL-12 on T Cell Activation by Altered Peptide Ligands. J. Immunol. 161: 6614-6621 [Abstract] [Full Text]
Behrens, L., Kerschensteiner, M., Misgeld, T., Goebels, N., Wekerle, H., Hohlfeld, R. (1998). Human Muscle Cells Express a Functional Costimulatory Molecule Distinct from B7.1 (CD80) and B7.2 (CD86) In Vitro and in Inflammatory Lesions. J. Immunol. 161: 5943-5951 [Abstract] [Full Text]
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Gurunathan, S., Irvine, K. R., Wu, C.-Y., Cohen, J. I., Thomas, E., Prussin, C., Restifo, N. P., Seder, R. A. (1998). CD40 Ligand/Trimer DNA Enhances Both Humoral and Cellular Immune Responses and Induces Protective Immunity to Infectious and Tumor Challenge. J. Immunol. 161: 4563-4571 [Abstract] [Full Text]
Mutis, T., Schrama, E., Melief, C. J.M., Goulmy, E. (1998). CD80-Transfected Acute Myeloid Leukemia Cells Induce Primary Allogeneic T-Cell Responses Directed at Patient Specific Minor Histocompatibility Antigens and Leukemia-Associated Antigens. Blood 92: 1677-1684 [Abstract] [Full Text]
Seko, Y., Takahashi, N., Azuma, M., Yagita, H., Okumura, K., Yazaki, Y. (1998). Expression of Costimulatory Molecule CD40 in Murine Heart With Acute Myocarditis and Reduction of Inflammation by Treatment With Anti-CD40L/B7-1 Monoclonal Antibodies. Circ. Res. 83: 463-469 [Abstract] [Full Text]
Sayegh, M. H., Turka, L. A. (1998). The Role of T-Cell Costimulatory Activation Pathways in Transplant Rejection. NEJM 338: 1813-1821 [Full Text]
Zhou, P., Seder, R. A. (1998). CD40 Ligand Is Not Essential for Induction of Type 1 Cytokine Responses or Protective Immunity after Primary or Secondary Infection With Histoplasma capsulatum. JEM 187: 1315-1324 [Abstract] [Full Text]
Schattner, E. J., Mascarenhas, J., Reyfman, I., Koshy, M., Woo, C., Friedman, S. M., Crow, M. K. (1998). Chronic Lymphocytic Leukemia B Cells Can Express CD40 Ligand and Demonstrate T-Cell Type Costimulatory Capacity. Blood 91: 2689-2697 [Abstract] [Full Text]
Purkerson, J. M., Parker, D. C. (1998). Differential Coupling of Membrane Ig and CD40 to the Extracellularly Regulated Kinase Signaling Pathway. J. Immunol. 160: 2121-2129 [Abstract] [Full Text]
Seko, Y., Takahashi, N., Ishiyama, S., Nishikawa, T., Kasajima, T., Hiroe, M., Suzuki, S., Ishiwata, S., Kawai, S., Azuma, M., Yagita, H., Okumura, K., Yazaki, Y. (1998). Expression of Costimulatory Molecules B7�1, B7�2, and CD40 in the Heart of Patients With Acute Myocarditis and Dilated Cardiomyopathy. Circulation 97: 637-639 [Abstract] [Full Text]