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[Cancer Research 62, 6178-6186, November 1, 2002]
© 2002 American Association for Cancer Research

Immunology

Major Histocompatibility Complex Class I-related Chain A and UL16-Binding Protein Expression on Tumor Cell Lines of Different Histotypes

Analysis of Tumor Susceptibility to NKG2D-dependent Natural Killer Cell Cytotoxicity1

Daniela Pende2, Paola Rivera, Stefania Marcenaro, Chien-Chung Chang, Roberto Biassoni, Romana Conte, Marek Kubin, David Cosman, Soldano Ferrone, Lorenzo Moretta and Alessandro Moretta

Istituto Nazionale per la Ricerca sul Cancro, 16132 Genova, Italy [D. P., R. B., R. C.]; Dipartimento di Medicina Sperimentale [P. R., L. M., A. M.] and Centro di Eccellenza per le Ricerche Biomediche [L. M., A. M.], Università degli Studi di Genova, 16132 Genova, Italy; Istituto Giannina Gaslini, 16148 Genova, Italy [S. M., L. M.]; Department of Immunology, Roswell Park Cancer Institute, Buffalo, New York 14263 [C-C. C., S. F.]; and Departments of Immunobiology [M. K.] and Molecular Biology [D. C.], Immunex, Seattle, Washington 98101

NKG2D, together with NKp46 and NKp30, represents a major triggering receptor involved in the induction of cytotoxicity by both resting and activated human natural killer cells. In this study, we analyzed the expression and the functional relevance of MHC class I-related chain A (MICA) and UL16 binding protein (ULBP), the major cellular ligands for human NKG2D, in human tumor cell lines of different histological origin. We show that MICA and ULBP are frequently coexpressed by carcinoma cell lines, whereas MICA is expressed more frequently than ULBP by melanoma cell lines. Interestingly, the MICA- ULBP+ phenotype was detected in most T cell leukemia cell lines, whereas the MICA- ULBP- phenotype characterized all acute myeloid leukemia and most B-cell lymphoma cell lines analyzed. These results, together with functional experiments, based on monoclonal antibody-mediated blocking of either NKG2D or its ligands, showed that killing of certain MICA- cell tumors is at least in part NKG2D dependent. Indeed, leukemic T cells as well as certain B-cell lymphomas were killed in a NKG2D-dependent fashion upon recognition of ULBP molecules. Moreover, ULBP could induce NKG2D-mediated NK cell triggering also in tumors coexpressing MICA. Our data suggest that the involvement of NKG2D in natural killer cell-mediated cytotoxicity strictly correlates with the expression and the surface density of MICA and ULBP on target cell tumors of different histotypes.




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D. Pende, G. M. Spaggiari, S. Marcenaro, S. Martini, P. Rivera, A. Capobianco, M. Falco, E. Lanino, I. Pierri, R. Zambello, et al.
Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: evidence for the involvement of the Poliovirus receptor (CD155) and Nectin-2 (CD112)
Blood, March 1, 2005; 105(5): 2066 - 2073.
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C.-C. Chang, M. Campoli, N. P. Restifo, X. Wang, and S. Ferrone
Immune Selection of Hot-Spot {beta}2-Microglobulin Gene Mutations, HLA-A2 Allospecificity Loss, and Antigen-Processing Machinery Component Down-Regulation in Melanoma Cells Derived from Recurrent Metastases following Immunotherapy
J. Immunol., February 1, 2005; 174(3): 1462 - 1471.
[Abstract] [Full Text] [PDF]

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E. Carbone, P. Neri, M. Mesuraca, M. T. Fulciniti, T. Otsuki, D. Pende, V. Groh, T. Spies, G. Pollio, D. Cosman, et al.
HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells
Blood, January 1, 2005; 105(1): 251 - 258.
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C. Munz, T. Dao, G. Ferlazzo, M. A. de Cos, K. Goodman, and J. W. Young
Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells
Blood, January 1, 2005; 105(1): 266 - 273.
[Abstract] [Full Text] [PDF]

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A. Poggi, C. Venturino, S. Catellani, M. Clavio, M. Miglino, M. Gobbi, A. Steinle, P. Ghia, S. Stella, F. Caligaris-Cappio, et al.
V{delta}1 T Lymphocytes from B-CLL Patients Recognize ULBP3 Expressed on Leukemic B Cells and Up-Regulated by Trans-Retinoic Acid
Cancer Res., December 15, 2004; 64(24): 9172 - 9179.
[Abstract] [Full Text] [PDF]

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R. Castriconi, A. Dondero, M. V. Corrias, E. Lanino, D. Pende, L. Moretta, C. Bottino, and A. Moretta
Natural Killer Cell-Mediated Killing of Freshly Isolated Neuroblastoma Cells: Critical Role of DNAX Accessory Molecule-1-Poliovirus Receptor Interaction
Cancer Res., December 15, 2004; 64(24): 9180 - 9184.
[Abstract] [Full Text] [PDF]

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M. J. Smyth, J. Swann, J. M. Kelly, E. Cretney, W. M. Yokoyama, A. Diefenbach, T. J. Sayers, and Y. Hayakawa
NKG2D Recognition and Perforin Effector Function Mediate Effective Cytokine Immunotherapy of Cancer
J. Exp. Med., November 15, 2004; 200(10): 1325 - 1335.
[Abstract] [Full Text] [PDF]

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L. L. Molinero, M. B. Fuertes, M. V. Girart, L. Fainboim, G. A. Rabinovich, M. A. Costas, and N. W. Zwirner
NF-{kappa}B Regulates Expression of the MHC Class I-Related Chain A Gene in Activated T Lymphocytes
J. Immunol., November 1, 2004; 173(9): 5583 - 5590.
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L. Bacon, R. A. Eagle, M. Meyer, N. Easom, N. T. Young, and J. Trowsdale
Two Human ULBP/RAET1 Molecules with Transmembrane Regions Are Ligands for NKG2D
J. Immunol., July 15, 2004; 173(2): 1078 - 1084.
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T. Igarashi, J. Wynberg, R. Srinivasan, B. Becknell, J. P. McCoy Jr, Y. Takahashi, D. A. Suffredini, W. M. Linehan, M. A. Caligiuri, and R. W. Childs
Enhanced cytotoxicity of allogeneic NK cells with killer immunoglobulin-like receptor ligand incompatibility against melanoma and renal cell carcinoma cells
Blood, July 1, 2004; 104(1): 170 - 177.
[Abstract] [Full Text] [PDF]

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J.-C. Lee, K.-M. Lee, D.-W. Kim, and D. S. Heo
Elevated TGF-{beta}1 Secretion and Down-Modulation of NKG2D Underlies Impaired NK Cytotoxicity in Cancer Patients
J. Immunol., June 15, 2004; 172(12): 7335 - 7340.
[Abstract] [Full Text] [PDF]

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I. B. Bayer-Garner, D. Ivan, M. R. Schwartz, and J. A. Tschen
The Immunopathology of Regression in Benign Lichenoid Keratosis, Keratoacanthoma and Halo Nevus
Clin. Med. Res., May 1, 2004; 2(2): 89 - 97.
[Abstract] [Full Text] [PDF]

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M. R. Verneris, M. Karami, J. Baker, A. Jayaswal, and R. S. Negrin
Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells
Blood, April 15, 2004; 103(8): 3065 - 3072.
[Abstract] [Full Text] [PDF]

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G. Ferlazzo and C. Munz
NK Cell Compartments and Their Activation by Dendritic Cells
J. Immunol., February 1, 2004; 172(3): 1333 - 1339.
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G. Ferlazzo, D. Thomas, S.-L. Lin, K. Goodman, B. Morandi, W. A. Muller, A. Moretta, and C. Munz
The Abundant NK Cells in Human Secondary Lymphoid Tissues Require Activation to Express Killer Cell Ig-Like Receptors and Become Cytolytic
J. Immunol., February 1, 2004; 172(3): 1455 - 1462.
[Abstract] [Full Text] [PDF]

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F. Lozupone, D. Pende, V. L. Burgio, C. Castelli, M. Spada, M. Venditti, F. Luciani, L. Lugini, C. Federici, C. Ramoni, et al.
Effect Of Human Natural Killer and {gamma}{delta} T Cells on the Growth of Human Autologous Melanoma Xenografts in SCID Mice
Cancer Res., January 1, 2004; 64(1): 378 - 385.
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C. Bottino, R. Castriconi, D. Pende, P. Rivera, M. Nanni, B. Carnemolla, C. Cantoni, J. Grassi, S. Marcenaro, N. Reymond, et al.
Identification of PVR (CD155) and Nectin-2 (CD112) as Cell Surface Ligands for the Human DNAM-1 (CD226) Activating Molecule
J. Exp. Med., August 18, 2003; 198(4): 557 - 567.
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H. R. Salih, H. Antropius, F. Gieseke, S. Z. Lutz, L. Kanz, H.-G. Rammensee, and A. Steinle
Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia
Blood, August 15, 2003; 102(4): 1389 - 1396.
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C. Dunn, N. J. Chalupny, C. L. Sutherland, S. Dosch, P.V. Sivakumar, D. C. Johnson, and D. Cosman
Human Cytomegalovirus Glycoprotein UL16 Causes Intracellular Sequestration of NKG2D Ligands, Protecting Against Natural Killer Cell Cytotoxicity
J. Exp. Med., June 2, 2003; 197(11): 1427 - 1439.
[Abstract] [Full Text] [PDF]


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