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Science 295 (5562): 2097-2100

Copyright © 2002 by the American Association for the Advancement of Science

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}

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Langerhans cells are not required for graft-versus-host disease.
H. Li, D. H. Kaplan, C. Matte-Martone, H. S. Tan, S. Venkatesan, K. Johnson, A. J. Demetris, J. McNiff, M. J. Shlomchik, and W. D. Shlomchik (2011)
Blood 117, 697-707
   Abstract »    Full Text »    PDF »
Innate or Adaptive Immunity? The Example of Natural Killer Cells.
E. Vivier, D. H. Raulet, A. Moretta, M. A. Caligiuri, L. Zitvogel, L. L. Lanier, W. M. Yokoyama, and S. Ugolini (2011)
Science 331, 44-49
   Abstract »    Full Text »    PDF »
Analyses of HLA-C-specific KIR repertoires in donors with group A and B haplotypes suggest a ligand-instructed model of NK cell receptor acquisition.
K. Schonberg, M. Sribar, J. Enczmann, J. C. Fischer, and M. Uhrberg (2011)
Blood 117, 98-107
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Human Pluripotent Stem Cells Produce Natural Killer Cells That Mediate Anti-HIV-1 Activity by Utilizing Diverse Cellular Mechanisms.
Z. Ni, D. A. Knorr, C. L. Clouser, M. K. Hexum, P. Southern, L. M. Mansky, I.-H. Park, and D. S. Kaufman (2011)
J. Virol. 85, 43-50
   Abstract »    Full Text »    PDF »
Graft-versus-Host Disease Is Independent of Innate Signaling Pathways Triggered by Pathogens in Host Hematopoietic Cells.
H. Li, C. Matte-Martone, H. S. Tan, S. Venkatesan, J. McNiff, A. J. Demetris, D. Jain, F. Lakkis, D. Rothstein, and W. D. Shlomchik (2011)
J. Immunol. 186, 230-241
   Abstract »    Full Text »    PDF »
The requirement for NKG2D in NK cell-mediated rejection of parental bone marrow grafts is determined by MHC class I expressed by the graft recipient.
J. N. Beilke, J. Benjamin, and L. L. Lanier (2010)
Blood 116, 5208-5216
   Abstract »    Full Text »    PDF »
Pediatric Acute Lymphoblastic Leukemia: Is There Still a Role for Transplant?.
S. M. Davies and P. A. Mehta (2010)
Hematology 2010, 363-367
   Abstract »    Full Text »    PDF »
The Rapid Induction of HLA-E Is Essential for the Survival of Antigen-Activated Naive CD4 T Cells from Attack by NK Cells.
S. Takao, T. Ishikawa, K. Yamashita, and T. Uchiyama (2010)
J. Immunol. 185, 6031-6040
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Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia.
S. Cooley, D. J. Weisdorf, L. A. Guethlein, J. P. Klein, T. Wang, C. T. Le, S. G. E. Marsh, D. Geraghty, S. Spellman, M. D. Haagenson, et al. (2010)
Blood 116, 2411-2419
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Interaction between KIR3DS1 and HLA-Bw4 predicts for progression-free survival after autologous stem cell transplantation in patients with multiple myeloma.
I. H. Gabriel, R. Sergeant, R. Szydlo, J. F. Apperley, H. deLavallade, A. Alsuliman, A. Khoder, D. Marin, E. Kanfer, N. Cooper, et al. (2010)
Blood 116, 2033-2039
   Abstract »    Full Text »    PDF »
Biological individuality and the new frontiers of immunological tolerance in hematopoietic stem cell transplantation.
G. R. Burgio, M. Zecca, P. Comoli, and R. Maccario (2010)
Haematologica 95, 1447-1451
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Long-Term Human CD34+ Stem Cell-Engrafted Nonobese Diabetic/SCID/IL-2R{gamma}null Mice Show Impaired CD8+ T Cell Maintenance and a Functional Arrest of Immature NK Cells.
M. C. Andre, A. Erbacher, C. Gille, V. Schmauke, B. Goecke, A. Hohberger, P. Mang, A. Wilhelm, I. Mueller, W. Herr, et al. (2010)
J. Immunol. 185, 2710-2720
   Abstract »    Full Text »    PDF »
Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor.
B. Jena, G. Dotti, and L. J. N. Cooper (2010)
Blood 116, 1035-1044
   Abstract »    Full Text »    PDF »
Reconstitution of natural killer cell receptors influences natural killer activity and relapse rate after haploidentical transplantation of T- and B-cell depleted grafts in children.
M. M. Pfeiffer, T. Feuchtinger, H.-M. Teltschik, M. Schumm, I. Muller, R. Handgretinger, and P. Lang (2010)
Haematologica 95, 1381-1388
   Abstract »    Full Text »    PDF »
Cytotoxicity of Activated Natural Killer Cells against Pediatric Solid Tumors.
D. Cho, D. R. Shook, N. Shimasaki, Y.-H. Chang, H. Fujisaki, and D. Campana (2010)
Clin. Cancer Res. 16, 3901-3909
   Abstract »    Full Text »    PDF »
Combined Genotypic and Phenotypic Killer Cell Ig-Like Receptor Analyses Reveal KIR2DL3 Alleles Displaying Unexpected Monoclonal Antibody Reactivity: Identification of the Amino Acid Residues Critical for Staining.
M. Falco, E. Romeo, S. Marcenaro, S. Martini, M. Vitale, C. Bottino, M. C. Mingari, L. Moretta, A. Moretta, and D. Pende (2010)
J. Immunol. 185, 433-441
   Abstract »    Full Text »    PDF »
NK Cells Delay Allograft Rejection in Lymphopenic Hosts by Downregulating the Homeostatic Proliferation of CD8+ T Cells.
D. Zecher, Q. Li, M. H. Oberbarnscheidt, A. J. Demetris, W. D. Shlomchik, D. M. Rothstein, and F. G. Lakkis (2010)
J. Immunol. 184, 6649-6657
   Abstract »    Full Text »    PDF »
NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects.
J. A. Olson, D. B. Leveson-Gower, S. Gill, J. Baker, A. Beilhack, and R. S. Negrin (2010)
Blood 115, 4293-4301
   Abstract »    Full Text »    PDF »

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