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Science 15 March 2002:
Vol. 295. no. 5562, pp. 2097 - 2100
DOI: 10.1126/science.1068440
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Reports

Effectiveness of Donor Natural Killer Cell Alloreactivity in Mismatched Hematopoietic Transplants

Loredana Ruggeri,1 Marusca Capanni,1 Elena Urbani,1 Katia Perruccio,1 Warren D. Shlomchik,2 Antonella Tosti,1 Sabrina Posati,1 Daniela Rogaia,1 Francesco Frassoni,3 Franco Aversa,1 Massimo F. Martelli,1 Andrea Velardi1*

T cells that accompany allogeneic hematopoietic grafts for treating leukemia enhance engraftment and mediate the graft-versus-leukemia effect. Unfortunately, alloreactive T cells also cause graft-versus-host disease (GVHD). T cell depletion prevents GVHD but increases the risk of graft rejection and leukemic relapse. In human transplants, we show that donor-versus-recipient natural killer (NK)-cell alloreactivity could eliminate leukemia relapse and graft rejection and protect patients against GVHD. In mice, the pretransplant infusion of alloreactive NK cells obviated the need for high-intensity conditioning and reduced GVHD. NK cell alloreactivity may thus provide a powerful tool for enhancing the efficacy and safety of allogeneic hematopoietic transplantation.

1 Department of Clinical and Experimental Medicine, Section of Hematology and Clinical Immunology, Perugia University School of Medicine, Perugia, Italy.
2 Department of Medicine, Sections of Hematology and Oncology, Yale University School of Medicine, New Haven, CT 06520, USA.
3 Department of Hematology, Ospedale San Martino, Genoa, Italy.
*   To whom correspondence should be addressed. E-mail: velardi{at}unipg.it

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Blood 109, 323-330
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Superiority of Allogeneic Hematopoietic Stem-Cell Transplantation Compared With Chemotherapy Alone in High-Risk Childhood T-Cell Acute Lymphoblastic Leukemia: Results From ALL-BFM 90 and 95.
A. Schrauder, A. Reiter, H. Gadner, D. Niethammer, T. Klingebiel, B. Kremens, C. Peters, W. Ebell, M. Zimmermann, F. Niggli, et al. (2006)
J. Clin. Oncol. 24, 5742-5749
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The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function.
M. D. Chiesa, S. Carlomagno, G. Frumento, M. Balsamo, C. Cantoni, R. Conte, L. Moretta, A. Moretta, and M. Vitale (2006)
Blood 108, 4118-4125
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Inhibition of Human Tumor-Infiltrating Lymphocyte Effector Functions by the Homophilic Carcinoembryonic Cell Adhesion Molecule 1 Interactions.
G. Markel, R. Seidman, N. Stern, T. Cohen-Sinai, O. Izhaki, G. Katz, M. Besser, A. J. Treves, R. S. Blumberg, R. Loewenthal, et al. (2006)
J. Immunol. 177, 6062-6071
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Thymosin {alpha}1 activates dendritic cell tryptophan catabolism and establishes a regulatory environment for balance of inflammation and tolerance.
L. Romani, F. Bistoni, K. Perruccio, C. Montagnoli, R. Gaziano, S. Bozza, P. Bonifazi, G. Bistoni, G. Rasi, A. Velardi, et al. (2006)
Blood 108, 2265-2274
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Trans-presentation of donor-derived interleukin 15 is necessary for the rapid onset of acute graft-versus-host disease but not for graft-versus-tumor activity.
B. W. Blaser, N. R. Schwind, S. Karol, D. Chang, S. Shin, S. Roychowdhury, B. Becknell, A. K. Ferketich, D. F. Kusewitt, B. R. Blazar, et al. (2006)
Blood 108, 2463-2469
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Enhanced Antitumor Activity of Murine-Human Hybrid T-Cell Receptor (TCR) in Human Lymphocytes Is Associated with Improved Pairing and TCR/CD3 Stability..
C. J. Cohen, Y. Zhao, Z. Zheng, S. A. Rosenberg, and R. A. Morgan (2006)
Cancer Res. 66, 8878-8886
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Single-Cell Cloning of Human, Donor-Derived Antileukemia T-Cell Lines for In vitro Separation of Graft-versus-Leukemia Effect from Graft-versus-Host Reaction..
D. Montagna, L. Daudt, F. Locatelli, E. Montini, I. Turin, D. Lisini, G. Giorgiani, M. E. Bernardo, and R. Maccario (2006)
Cancer Res. 66, 7310-7316
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Control of Metastasized Pancreatic Carcinomas in SCID/Beige Mice with Human IL-2/TKD-Activated NK Cells.
S. Stangl, A. Wortmann, U. Guertler, and G. Multhoff (2006)
J. Immunol. 176, 6270-6276
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Cmv4, a New Locus Linked to the NK Cell Gene Complex, Controls Innate Resistance to Cytomegalovirus in Wild-Derived Mice.
S. G. Adam, A. Caraux, N. Fodil-Cornu, J. C. Loredo-Osti, S. Lesjean-Pottier, J. Jaubert, I. Bubic, S. Jonjic, J.-L. Guenet, S. M. Vidal, et al. (2006)
J. Immunol. 176, 5478-5485
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Recipient {gamma}{delta} T cells in graft-versus-host disease..
B. E. Anderson, W. D. Shlomchik, M. J. Shlomchik, J. L. M. Ferrara, and P. Reddy (2006)
Blood 107, 3808-3809
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Hematopoietic stem-cell transplantation..
E. A. Copelan (2006)
N. Engl. J. Med. 354, 1813-1826
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IFN-{gamma} Acts on T Cells to Induce NK Cell Mobilization and Accumulation in Target Organs..
O. Wald, I. D. Weiss, H. Wald, H. Shoham, Y. Bar-Shavit, K. Beider, E. Galun, L. Weiss, L. Flaishon, I. Shachar, et al. (2006)
J. Immunol. 176, 4716-4729
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Remodeling specific immunity by use of MHC tetramers: demonstration in a graft-versus-host disease model.
B. J. Kappel, J. Pinilla-Ibarz, A. A. Kochman, J. M. Eng, V. M. Hubbard, I. Leiner, E. G. Pamer, G. Heller, M. R. M. van den Brink, and D. A. Scheinberg (2006)
Blood 107, 2045-2051
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Suicide gene therapy of graft-versus-host disease induced by central memory human T lymphocytes.
A. Bondanza, V. Valtolina, Z. Magnani, M. Ponzoni, K. Fleischhauer, M. Bonyhadi, C. Traversari, F. Sanvito, S. Toma, M. Radrizzani, et al. (2006)
Blood 107, 1828-1836
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Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction.
D. Pende, R. Castriconi, P. Romagnani, G. M. Spaggiari, S. Marcenaro, A. Dondero, E. Lazzeri, L. Lasagni, S. Martini, P. Rivera, et al. (2006)
Blood 107, 2030-2036
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Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation.
G. M. Spaggiari, A. Capobianco, S. Becchetti, M. C. Mingari, and L. Moretta (2006)
Blood 107, 1484-1490
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Immunotherapy of high-risk acute leukemia with a recipient (autologous) vaccine expressing transgenic human CD40L and IL-2 after chemotherapy and allogeneic stem cell transplantation.
R. F. Rousseau, E. Biagi, A. Dutour, E. S. Yvon, M. P. Brown, T. Lin, Z. Mei, B. Grilley, E. Popek, H. E. Heslop, et al. (2006)
Blood 107, 1332-1341
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CD4+CD25+ T Regulatory Cells Suppress NK Cell-Mediated Immunotherapy of Cancer.
M. J. Smyth, M. W. L. Teng, J. Swann, K. Kyparissoudis, D. I. Godfrey, and Y. Hayakawa (2006)
J. Immunol. 176, 1582-1587
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