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Blood, Vol. 94 No. 1 (July 1), 1999:
pp. 333-339
By
From the Division of Hematology and Clinical Immunology, the
Department of Clinical and Experimental Medicine, University of
Perugia, Perugia, Italy; and the Division of Bone Marrow
Transplantation, the Department of Medicine, Stanford University,
Stanford, CA 94305.
Because of the expression of inhibitory receptors (KIR) for major
histocompatibility complex (MHC) class I allotypes, a person's natural
killer (NK) cells will not recognize and will, therefore, kill cells
from individuals lacking his/her KIR epitopes. This study investigated
the role of NK cell alloreactivity in human HLA haplotype-mismatched
hematopoietic stem cell transplantation and, specifically, the role of
the three major NK specificities, ie, those for HLA-C group 1, HLA-C
group 2, and HLA-Bw4 alleles. In 20 of 60 donor-recipient pairs, KIR
epitope incompatibility and functional analyses of donor NK cell clones
predicted donor NK cells could cause graft-versus-host
(GVH)/graft-versus-leukemia (GVL) reactions. NK cell clones of donor
origin were obtained from transplanted recipients and tested for lysis
of recipient's cryopreserved pretransplant lymphocytes. Despite the
absence of GVH disease, we detected high frequencies of NK clones which
killed recipient's target cells. Lysis followed the rules of NK cell alloreactivity, being blocked only by the MHC class I KIR epitope which
was missing in the recipient. The alloreactive NK clones also killed
the allogeneic leukemia. Transplants from these KIR epitope
incompatible donors had higher engraftment rates. Therefore, a GVL
effector and engraftment facilitating mechanism, which is independent
of T-cell-mediated GVH reactions, may be operational in HLA mismatched
hematopoietic cell transplants.
INHIBITION OF natural killer (NK) cell
lysis is signaled through specific receptors which bind to polymorphic
determinants of major histocompatibility complex (MHC) class I
molecules.1,2 In humans, one receptor is the lectin-like
heterodimer CD94-NKG2A, which recognizes human leukocyte antigen
(HLA)-E, a nonclassical MHC class Ib molecule whose expression is, in
turn, upregulated by the binding of signal sequence peptides of other
MHC class I molecules.3,4 Other receptors are a family of
Ig-like molecules known as killer cell inhibitory receptors
(KIR).5-7 The KIRs with two Ig domains (KIR2D) identify
HLA-C allotypes: KIR2DL2 (formerly designated p58.1) recognizes an
epitope shared by group 1 HLA-C allotypes (Cw2, 4, 5, and 6), whereas
KIR2DL1 (p58.2) recognizes an epitope shared by the reciprocal group 2 HLA-C allotypes (Cw1, 3, 7, and 8). One KIR with three Ig domains
KIR3DL1 (p70) recognizes an epitope shared by HLA-Bw4 alleles. Finally,
a homodimer of molecules with three Ig domains KIR3DL2 (p140)
recognizes HLA-A3 and -A11.8
KIR genes, each expressed by some of the individual's NK cells, vary
considerably among individuals.9 It is believed that during
development each NK cell precursor makes a random choice of which KIR
genes it will express, and the different combinations of HLA class I
molecules select NK cells that express receptors for self HLA class I. Consequently, the NK cells from any given individual will be
alloreactive toward cells from others which lack their KIR ligands and,
conversely, will be tolerant of cells from another individual who has
the same or additional KIR ligands.
Although KIR epitope mismatches are well-known causes of NK cell
alloreactivity,10-17 their role in human transplantation
have not been evaluated. Full haplotype-mismatched hematopoietic stem cell transplants have recently been used for treatment of bad-risk leukemia patients lacking a matched donor.18,19 In this
context, host and/or donor NK cells may be responsible for three
situations: (1) a potential for graft-versus-host (GVH) reactions, ie,
when the recipient fails to express the donor's KIR epitopes; (2) a potential for NK cell-mediated graft rejection, ie, when the donor fails to express the recipient's KIR epitopes; (3) no NK cell alloreactions, ie, when the donor and recipient mismatched alleles express the same KIR epitopes. One aim of the present study was, therefore, to evaluate whether mismatches for the three major KIR
epitopes, ie, those of the HLA-C group 1, HLA-C group 2, and HLA-Bw4
alleles, have any impact on transplantation outcome.
Moreover, the very fast donor-type NK cell recovery20 (and
this report) strongly suggests that postgrafting NK cells derive, not
from expansion of mature NK cells contaminating the stem cell graft,
but from large-scale maturation of the engrafted stem cells. This
maturation occurs under the influence of KIR epitopes expressed in the
donor's hematopoietic cells and the host's marrow stromal cells.21 Because little is known about the cell types which drive selection of the NK cells, KIR epitope mismatched transplants appear to be a convenient model for analyzing the selection of human NK
cell repertoires.
Patients
HLA Typing
Transplantation
Assessment of Chimerism Starting on day +12 after transplantation, chimerism of peripheral blood and bone marrow cells was determined by bimonthly assessment of polymerase chain reaction (PCR) amplification of a panel of variable number tandem repeat regions with different DNA polymorphism patterns in donor and recipient cells. All postengraftment blood samples used for the NK cell studies shown here exhibited 100% donor chimerism.Immunofluorescence and Flow Cytometry Indirect immunofluorescence with primary monoclonal antibodies (MoAbs) plus secondary fluorochrome-conjugated goat anti-mouse Ig antibodies (Southern Biotechnology Associates, Birmingham, AL) and flow cytometry (FACSCalibur; Becton Dickinson, San Jose, CA) determined NK cell phenotypes. NK cell clones were identified using an anti-CD16 MoAb (Immunotech, Marseille, France). Expression of KIRs recognizing group 1 HLA-C alleles (KIR2DL2), group 2 HLA-C alleles (KIR2DL1), and HLA-Bw4 alleles (KIR3DL1) was determined with MoAbs EB6, GL183 and Z27 respectively22 (kindly provided by L. Moretta, University of Genova, Genova, Italy). LFA-1 expression by allogeneic NK targets was measured by indirect immunofluorescence and flow cytometry with an anti-CD11a MoAb from Immunotech.Preparation of NK Cell Clones Peripheral blood mononuclear cells depleted of T cells by negative immuno-magnetic selection with anti-CD3 MoAb (OKT3 obtained from American Tissue Culture Collection [ATCC], Manassas, VA) were plated at the concentration of 10 cells per well in 96-well microtiter plates, activated with phytohemagglutinin (PHA), and cultured with interleukin-2 (IL-2) and irradiated feeder cells as described elsewhere.20 Cloned NK cells were used as effectors in standard 51Cr release cytotoxicity assays using as targets allogeneic PHA lymphoblasts or Epstein-Barr virus-transformed B-lymphoblastoid cell lines (BLCL), leukemia cells, and cell lines expressing single class I alleles. Effector to target (E:T) ratio was 10:1.Analysis of NK Cell Allospecificity Standard 51Cr release cytotoxicity assays against cell lines transfected with class I genes (kindly provided by L. Moretta) determined the three main NK allospecificities. Specificities for group 1 (Cw4-related) and group 2 (Cw3-related) HLA-C allotypes were analyzed using the HLA class I-negative cell line 721.221 and the same cell line transfected with Cw*0401 or Cw*0302 genes, respectively.23 Specificity for HLA-Bw4 allotypes (such as HLA-B27) was analyzed using untransfected C1R cells and C1R cells transfected with the B*2705 gene.22 Specificity for the nonclassical MHC class Ib molecule HLA-E was analyzed using C1R cells expressing HLA-B7 (Bw6)21 (cell-surface expression of HLA-E is regulated by the binding of peptides derived from the signal sequence of some other MHC class I molecules, such as HLA-B7).3,4 E:T ratio was 10:1. Results are presented as percentage inhibition compared with lysis of the untransfected 721.221 or C1R cells. NK clones lysed the untransfected cells at levels exceeding 60%, and were considered specific for a given allotype when this was reduced by at least 50%.
Transplantation Into Recipients Failing to Express the Donor's KIR Epitopes, ie, With a Potential for NK Cell-Mediated GVH Reactions Eight of the 20 patients in this group had AML, 5 CML, and 7 ALL. All patients engrafted successfully and reached 1,000 neutrophils/µL in 8 to 19 days (median, 11 days) and 50,000 platelets in 13 to 124 days (median, 29 days). No GVHD was observed. One hundred percent donor-type chimerism was detected in peripheral blood and bone marrow on all assessments (except at relapse). At a median follow-up of 6 months (range, 1 to 39 months), 0 of 8 AML, 0 of 5 CML, and 5 of 7 ALL patients relapsed.Postgrafting emergence of donor-versus-recipient alloreactive NK
cells.
Table 2 illustrates the HLA typing of these
20 donor-recipient pairs. Specific donor KIR ligands were missing in
the recipient. Some of the donor's NK cells could, therefore, lyse the
recipient's cells and cause GVHD. GVHD potential was assessed directly
in 14 pairs by pretransplant analysis of donor NK cell clones. Table 3 (left column) shows some donor NK cell
clones killed recipient target cells (PHA lymphoblasts or BLCLs),
indicating that donors possessed antirecipient NK cells in their
repertoires before transplant. Lysis by these clones could only be
blocked by transfected cell lines expressing the donor's MHC class I
allotypic group which was missing in the recipient (data not shown).
MHC specificity of donor-versus-recipient alloreactive NK cells.
Posttransplant killing of recipient cells might be triggered by
nonrecognition of recipient MHC. To test this hypothesis, clones were
analyzed for MHC specificity using target cells expressing the HLA-Bw4
allele B27, the group 2 HLA-C allele Cw3, and the group 1 HLA-C allele
Cw4. Expression of the corresponding KIR was determined by
immunofluorescence. Control targets, not recognized by KIRs, were cells
expressing the HLA-Bw6 allele B7 (see refs 3 and 4). As illustrated in
Fig 2 for the alloreactive NK clones from
transplants 7 and 9 (shown as examples), lysis could only be blocked by
target cells expressing the donor allele group that was missing in the
recipient. If the missing allele belonged to HLA-C group 1 (as in
transplant 7), the postgrafting donor-versus-recipient alloreactive NK
clones were only equipped with KIR2DL2, the receptor for HLA-C group 1. Their lysis could be blocked only by cells expressing an HLA-C group 1 allele (such as Cw4), and not by cells expressing allele groups
recognized by other KIRs, such as HLA-C group 2, or HLA-Bw4 (and
obviously not by cells bearing alleles, such as B7, which are not
recognized by KIRs). This phenomenon was observed in all cases
analyzed, ie, in transplants no. 7 and 9 (shown in the figure), as well
as in transplants 12, 13, and 14 (not shown).
Antileukemic effect of alloreactive NK cells.
To test the hypothesis that NK allorecognition may serve as a
graft-versus-leukemia (GVL) effector, we evaluated the susceptibility to allogeneic NK lysis of a set of leukemic cells and compared it with
reference targets (PHA lymphoblasts and BLCLs from the same leukemia
patients). NK clones that lysed allogeneic PHA lymphoblasts or BLCLs
from leukemia patients were tested for their ability to lyse leukemic
cells from the same individuals. Leukemia cells from 4 CML, 4 AML, and
5 ALL (calla+) patients were used as targets. The
alloreactive NK clones efficiently killed all the acute and chronic
myeloid leukemias (top panel in Fig 3). Only two of five ALLs were
killed (bottom left panel Fig 3). Killing
of susceptible leukemias followed the rules of NK cell allorecognition,
as leukemias were killed by 100% of the alloreactive NK clones (24 of
24, E:T ratio = 10:1), and were not killed by 50 of 50 nonalloreactive NK clones (even at E:T ratio of 50:1).
Immunofluorescence analysis of several adhesion molecules showed all
NK-resistant ALLs exhibited lower surface expression of lymphocyte
function antigen-1 (LFA-1) compared with the NK-susceptible ALLs and
with all the CMLs and AMLs (bottom right panel in Fig 3).
Transplantation From Donors Failing to Express the Recipient's KIR
Epitopes, ie, With a Potential for NK Cell-Mediated Graft Rejection
KIR Epitope-Matched Transplants, ie, With No Potential for NK Cell Alloreactions Twenty-three donor-recipient pairs were matched for all known KIR ligands, that is, HLA-A3/A11 in addition to HLA-C group 1, HLA-C group 2, HLA-Bw4. Six rejections (2 reversed by a second transplant) occurred. However, (1) none of 208 NK cell clones obtained before conditioning from three recipients who afterward rejected the graft lysed the donor's target cells; (2) at the end of conditioning, no host NK cells were detected by immunofluorescence, nor could they be cultured even by processing large (100 mL) samples of the recipient's blood; (3) at the time of rejection, no NK cells could be identified by immunofluorescence nor could they be cultured from the bone marrow or peripheral blood (not shown). Consequently, these tests failed to detect any role for NK cells in rejection in KIR epitope-matched transplants.
This study investigated the role of NK cell alloreactivity in clinical hematopoietic cell transplantation and, specifically, the role of the three major NK allospecificities, ie, those for the KIR epitopes of the HLA-C group 1, HLA-C group 2, and HLA-Bw4 alleles. Rejection and GVHD mediated by these NK specificities could have occurred in 37 of 60 high-risk leukemia patients who underwent mismatched hematopoietic stem cell transplants.
We thank Lorenzo Moretta (University of Genova, Genova, Italy) for antibodies and cell lines, Antonella Santucci for statistical analyses, and Geraldine Ann Boyd for assistance in the writing of the manuscript.
Submitted October 19, 1998; accepted February 18, 1999.
Supported by a grant from Associazione Italiana per la Ricerca sul Cancro (AIRC). L.R. and I.V. are supported by fellowships from Fondazione Italiana per la Ricerca sul Cancro (FIRC).
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. section 1734 solely to indicate this fact.
Address reprint requests to Andrea Velardi, MD, Sezione di Ematologia e Immunologia Clinica, Università di Perugia, Policlinico Monteluce, 06122-Perugia, Italy; e-mail: velardi{at}unipg.it.
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G. M. Spaggiari, A. Capobianco, H. Abdelrazik, F. Becchetti, M. C. Mingari, and L. Moretta Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2 Blood, February 1, 2008; 111(3): 1327 - 1333. [Abstract] [Full Text] [PDF]
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S. Diermayr, H. Himmelreich, B. Durovic, A. Mathys-Schneeberger, U. Siegler, U. Langenkamp, J. Hofsteenge, A. Gratwohl, A. Tichelli, M. Paluszewska, et al. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities Blood, February 1, 2008; 111(3): 1428 - 1436. [Abstract] [Full Text] [PDF]
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J. Yu, G. Heller, J. Chewning, S. Kim, W. M. Yokoyama, and K. C. Hsu Hierarchy of the Human Natural Killer Cell Response Is Determined by Class and Quantity of Inhibitory Receptors for Self-HLA-B and HLA-C Ligands J. Immunol., November 1, 2007; 179(9): 5977 - 5989. [Abstract] [Full Text] [PDF]
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H. Wang, B. Grzywacz, D. Sukovich, V. McCullar, Q. Cao, A. B. Lee, B. R. Blazar, D. N. Cornfield, J. S. Miller, and M. R. Verneris The unexpected effect of cyclosporin A on CD56+CD16 and CD56+CD16+ natural killer cell subpopulations Blood, September 1, 2007; 110(5): 1530 - 1539. [Abstract] [Full Text] [PDF]
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 R. A. Cahill, D. Wenkert, S. A. Perlman, A. Steele, S. P. Coburn, W. H. McAlister, S. Mumm, and M. P. Whyte Infantile Hypophosphatasia: Transplantation Therapy Trial Using Bone Fragments and Cultured Osteoblasts J. Clin. Endocrinol. Metab., August 1, 2007; 92(8): 2923 - 2930. [Abstract] [Full Text] [PDF]
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J. H. Chewning, C. N. Gudme, K. C. Hsu, A. Selvakumar, and B. Dupont KIR2DS1-Positive NK Cells Mediate Alloresponse against the C2 HLA-KIR Ligand Group In Vitro J. Immunol., July 15, 2007; 179(2): 854 - 868. [Abstract] [Full Text] [PDF]
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L. Ruggeri, A. Mancusi, M. Capanni, E. Urbani, A. Carotti, T. Aloisi, M. Stern, D. Pende, K. Perruccio, E. Burchielli, et al. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood, July 1, 2007; 110(1): 433 - 440. [Abstract] [Full Text] [PDF]
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R. Flierman, G. Westerhuis, M. Hameetman, L. M. van Duivenvoorde, T. van Hall, J. M. van Laar, W. E. Fibbe, and R. E. M. Toes Targeting host B-cell immune responses by persistent donor NK-cell alloreactivity following nonmyeloablative allogeneic stem cell transplantation Blood, June 15, 2007; 109(12): 5524 - 5525. [Full Text] [PDF]
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J. S. Miller, S. Cooley, P. Parham, S. S. Farag, M. R. Verneris, K. L. McQueen, L. A. Guethlein, E. A. Trachtenberg, M. Haagenson, M. M. Horowitz, et al. Missing KIR ligands are associated with less relapse and increased graft-versus-host disease (GVHD) following unrelated donor allogeneic HCT Blood, June 1, 2007; 109(11): 5058 - 5061. [Abstract] [Full Text] [PDF]
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L. Zamai, C. Ponti, P. Mirandola, G. Gobbi, S. Papa, L. Galeotti, L. Cocco, and M. Vitale NK Cells and Cancer J. Immunol., April 1, 2007; 178(7): 4011 - 4016. [Abstract] [Full Text] [PDF]
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H. Fujii, J. D. Trudeau, D. T. Teachey, J. D. Fish, S. A. Grupp, K. R. Schultz, and G. S. D. Reid In vivo control of acute lymphoblastic leukemia by immunostimulatory CpG oligonucleotides Blood, March 1, 2007; 109(5): 2008 - 2013. [Abstract] [Full Text] [PDF]
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A. Mullally and J. Ritz Beyond HLA: the significance of genomic variation for allogeneic hematopoietic stem cell transplantation Blood, February 15, 2007; 109(4): 1355 - 1362. [Abstract] [Full Text] [PDF]
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A. Lundqvist, S. I. Abrams, D. S. Schrump, G. Alvarez, D. Suffredini, M. Berg, and R. Childs Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: a novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res., July 15, 2006; 66(14): 7317 - 7325. [Abstract] [Full Text] [PDF]
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 B. N. Savani, A. Montero, S. Mielke, K. Rezvani, A. Shenoy, R. Childs, and A. J. Barrett Transplant Outcome in Acute Myeloid but Not Acute Lymphocytic Leukemia Following T Cell Depleted Allogeneic Stem Cell Transplantation May Be Favorably Influenced by Early Recovery of NK Cells. Blood (ASH Annual Meeting Abstracts), November 16, 2005; 106(11): 1405 - 1405. [Abstract]
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G. Sconocchia, M. Lau, M. Provenzano, K. Rezvani, W. Wongsena, H. Fujiwara, N. Hensel, J. Melenhorst, J. Li, S. Ferrone, et al. The antileukemia effect of HLA-matched NK and NK-T cells in chronic myelogenous leukemia involves NKG2D-target-cell interactions Blood, November 15, 2005; 106(10): 3666 - 3672. [Abstract] [Full Text] [PDF]
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 A. P. Williams, A. R. Bateman, and S. I. Khakoo HANGING IN THE BALANCE: KIR and Their Role in Disease Mol. Interv., August 1, 2005; 5(4): 226 - 240. [Abstract] [Full Text] [PDF]
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M. Terme, C. Borg, F. Guilhot, C. Masurier, C. Flament, E. F. Wagner, S. Caillat-Zucman, A. Bernheim, A. G. Turhan, A. Caignard, et al. BCR/ABL Promotes Dendritic Cell-Mediated Natural Killer Cell Activation Cancer Res., July 15, 2005; 65(14): 6409 - 6417. [Abstract] [Full Text] [PDF]
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C. Imai, S. Iwamoto, and D. Campana Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells Blood, July 1, 2005; 106(1): 376 - 383. [Abstract] [Full Text] [PDF]
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K. C. Hsu, C. A. Keever-Taylor, A. Wilton, C. Pinto, G. Heller, K. Arkun, R. J. O'Reilly, M. M. Horowitz, and B. Dupont Improved outcome in HLA-identical sibling hematopoietic stem-cell transplantation for acute myelogenous leukemia predicted by KIR and HLA genotypes Blood, June 15, 2005; 105(12): 4878 - 4884. [Abstract] [Full Text] [PDF]
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S. Nguyen, N. Dhedin, J.-P. Vernant, M. Kuentz, A. A. Jijakli, N. Rouas-Freiss, E. D. Carosella, A. Boudifa, P. Debre, and V. Vieillard NK-cell reconstitution after haploidentical hematopoietic stem-cell transplantations: immaturity of NK cells and inhibitory effect of NKG2A override GvL effect Blood, May 15, 2005; 105(10): 4135 - 4142. [Abstract] [Full Text] [PDF]
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P. Nowbakht, M.-C. S. Ionescu, A. Rohner, C. P. Kalberer, E. Rossy, L. Mori, D. Cosman, G. De Libero, and A. Wodnar-Filipowicz Ligands for natural killer cell-activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias Blood, May 1, 2005; 105(9): 3615 - 3622. [Abstract] [Full Text] [PDF]
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C. Cebo, I. A. Voutsadakis, S. Da Rocha, J.-H. Bourhis, A. Jalil, B. Azzarone, A. G. Turhan, M. Chelbi-Alix, S. Chouaib, and A. Caignard Altered IFN{gamma} Signaling and Preserved Susceptibility to Activated Natural Killer Cell-Mediated Lysis of BCR/ABL Targets Cancer Res., April 1, 2005; 65(7): 2914 - 2920. [Abstract] [Full Text] [PDF]
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D. W. Beelen, H. D. Ottinger, S. Ferencik, A. H. Elmaagacli, R. Peceny, R. Trenschel, and H. Grosse-Wilde Genotypic inhibitory killer immunoglobulin-like receptor ligand incompatibility enhances the long-term antileukemic effect of unmodified allogeneic hematopoietic stem cell transplantation in patients with myeloid leukemias Blood, March 15, 2005; 105(6): 2594 - 2600. [Abstract] [Full Text] [PDF]
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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. [Abstract] [Full Text] [PDF]
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S. Reich-Zeliger, E. Bachar-Lustig, J. Gan, and Y. Reisner Tolerance Induction by Veto CTLs in the TCR Transgenic 2C Mouse Model. I. Relative Reactivity of Different Veto Cells J. Immunol., December 1, 2004; 173(11): 6654 - 6659. [Abstract] [Full Text] [PDF]
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J. Tanaka, T. Toubai, Y. Tsutsumi, Y. Miura, N. Kato, S. Umehara, K. Kahata, A. Mori, N. Toyoshima, S. Ota, et al. Cytolytic activity and regulatory functions of inhibitory NK cell receptor-expressing T cells expanded from granulocyte colony-stimulating factor-mobilized peripheral blood mononuclear cells Blood, August 1, 2004; 104(3): 768 - 774. [Abstract] [Full Text] [PDF]
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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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E. Chklovskaia, P. Nowbakht, C. Nissen, A. Gratwohl, M. Bargetzi, and A. Wodnar-Filipowicz Reconstitution of dendritic and natural killer-cell subsets after allogeneic stem cell transplantation: effects of endogenous flt3 ligand Blood, May 15, 2004; 103(10): 3860 - 3868. [Abstract] [Full Text] [PDF]
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P. Lang, K. Barbin, T. Feuchtinger, J. Greil, M. Peipp, S. J. Zunino, M. Pfeiffer, R. Handgretinger, D. Niethammer, and G. H. Fey Chimeric CD19 antibody mediates cytotoxic activity against leukemic blasts with effector cells from pediatric patients who received T-cell-depleted allografts Blood, May 15, 2004; 103(10): 3982 - 3985. [Abstract] [Full Text] [PDF]
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M. Bornhauser, R. Schwerdtfeger, H. Martin, K.-H. Frank, C. Theuser, G. Ehninger, F. Locatelli, A. Velardi, and S. Giebel Role of KIR ligand incompatibility in hematopoietic stem cell transplantation using unrelated donors Blood, April 1, 2004; 103(7): 2860 - 2861. [Full Text] [PDF]
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M. A. Cook, D. W. Milligan, C. D. Fegan, P. J. Darbyshire, P. Mahendra, C. F. Craddock, P. A. H. Moss, and D. C. Briggs The impact of donor KIR and patient HLA-C genotypes on outcome following HLA-identical sibling hematopoietic stem cell transplantation for myeloid leukemia Blood, February 15, 2004; 103(4): 1521 - 1526. [Abstract] [Full Text] [PDF]
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H.-J. Kolb, C. Schmid, A. J. Barrett, and D. J. Schendel Graft-versus-leukemia reactions in allogeneic chimeras Blood, February 1, 2004; 103(3): 767 - 776. [Abstract] [Full Text] [PDF]
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W. Leung, R. Iyengar, V. Turner, P. Lang, P. Bader, P. Conn, D. Niethammer, and R. Handgretinger Determinants of Antileukemia Effects of Allogeneic NK Cells J. Immunol., January 1, 2004; 172(1): 644 - 650. [Abstract] [Full Text] [PDF]
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M. A. Caligiuri, A. Velardi, D. A. Scheinberg, and I. M. Borrello Immunotherapeutic Approaches for Hematologic Malignancies Hematology, January 1, 2004; 2004(1): 337 - 353. [Abstract] [Full Text] [PDF]
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M. Zoller Tumor Vaccination after Allogeneic Bone Marrow Cell Reconstitution of the Nonmyeloablatively Conditioned Tumor-Bearing Murine Host J. Immunol., December 15, 2003; 171(12): 6941 - 6953. [Abstract] [Full Text] [PDF]
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J.-X. Gao, X. Liu, J. Wen, M. A. Caligiuri, I. Stroynowski, P. Zheng, and Y. Liu Two-signal requirement for activation and effector function of natural killer cell response to allogeneic tumor cells Blood, December 15, 2003; 102(13): 4456 - 4463. [Abstract] [Full Text] [PDF]
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A. R. Rao, M. P. Quinones, E. Garavito, Y. Kalkonde, F. Jimenez, C. Gibbons, J. Perez, P. Melby, W. Kuziel, R. L. Reddick, et al. CC Chemokine Receptor 2 Expression in Donor Cells Serves an Essential Role in Graft-versus-Host-Disease J. Immunol., November 1, 2003; 171(9): 4875 - 4885. [Abstract] [Full Text] [PDF]
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S. Giebel, F. Locatelli, T. Lamparelli, A. Velardi, S. Davies, G. Frumento, R. Maccario, F. Bonetti, J. Wojnar, M. Martinetti, et al. Survival advantage with KIR ligand incompatibility in hematopoietic stem cell transplantation from unrelated donors Blood, August 1, 2003; 102(3): 814 - 819. [Abstract] [Full Text] [PDF]
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C. P. Kalberer, U. Siegler, and A. Wodnar-Filipowicz Human NK cell development in NOD/SCID mice receiving grafts of cord blood CD34+ cells Blood, July 1, 2003; 102(1): 127 - 135. [Abstract] [Full Text] [PDF]
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H. G. Shilling, K. L. McQueen, N. W. Cheng, J. A. Shizuru, R. S. Negrin, and P. Parham Reconstitution of NK cell receptor repertoire following HLA-matched hematopoietic cell transplantation Blood, May 1, 2003; 101(9): 3730 - 3740. [Abstract] [Full Text] [PDF]
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P. Lang, R. Handgretinger, D. Niethammer, P. G. Schlegel, M. Schumm, J. Greil, P. Bader, C. Engel, H. Scheel-Walter, M. Eyrich, et al. Transplantation of highly purified CD34+ progenitor cells from unrelated donors in pediatric leukemia Blood, February 15, 2003; 101(4): 1630 - 1636. [Abstract] [Full Text] [PDF]
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P. J. Amrolia, S. D. Reid, L. Gao, B. Schultheis, G. Dotti, M. K. Brenner, J. V. Melo, J. M. Goldman, and H. J. Stauss Allorestricted cytotoxic T cells specific for human CD45 show potent antileukemic activity Blood, February 1, 2003; 101(3): 1007 - 1014. [Abstract] [Full Text] [PDF]
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A. J. Barrett, K. Rezvani, S. Solomon, A. M. Dickinson, X. N. Wang, G. Stark, H. Cullup, M. Jarvis, P. G. Middleton, and N. Chao New Developments in Allotransplant Immunology Hematology, January 1, 2003; 2003(1): 350 - 371. [Abstract] [Full Text] [PDF]
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S. S. Farag, T. A. Fehniger, L. Ruggeri, A. Velardi, and M. A. Caligiuri Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect Blood, August 28, 2002; 100(6): 1935 - 1947. [Abstract] [Full Text] [PDF]
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A. D. Billiau, S. Fevery, O. Rutgeerts, W. Landuyt, and M. Waer Crucial role of timing of donor lymphocyte infusion in generating dissociated graft-versus-host and graft-versus-leukemia responses in mice receiving allogeneic bone marrow transplants Blood, August 13, 2002; 100(5): 1894 - 1902. [Abstract] [Full Text] [PDF]
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H. G. Shilling, N. Young, L. A. Guethlein, N. W. Cheng, C. M. Gardiner, D. Tyan, and P. Parham Genetic Control of Human NK Cell Repertoire J. Immunol., July 1, 2002; 169(1): 239 - 247. [Abstract] [Full Text] [PDF]
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M. Guimond, A. Balassy, M. Barrette, S. Brochu, C. Perreault, and D. C. Roy P-glycoprotein targeting: a unique strategy to selectively eliminate immunoreactive T cells Blood, June 28, 2002; 100(2): 375 - 382. [Abstract] [Full Text] [PDF]
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Y. Morishima, T. Sasazuki, H. Inoko, T. Juji, T. Akaza, K. Yamamoto, Y. Ishikawa, S. Kato, H. Sao, H. Sakamaki, et al. The clinical significance of human leukocyte antigen (HLA) allele compatibility in patients receiving a marrow transplant from serologically HLA-A, HLA-B, and HLA-DR matched unrelated donors Blood, May 13, 2002; 99(11): 4200 - 4206. [Abstract] [Full Text] [PDF]
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F. Baron, A. G. Turhan, J. Giron-Michel, B. Azzarone, M. Bentires-Alj, V. Bours, J. H. Bourhis, S. Chouaib, and A. Caignard Leukemic target susceptibility to natural killer cytotoxicity: relationship with BCR-ABL expression Blood, March 15, 2002; 99(6): 2107 - 2113. [Abstract] [Full Text] [PDF]
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F. J. Giles, A. Keating, A. H. Goldstone, I. Avivi, C. L. Willman, and H. M. Kantarjian Acute Myeloid Leukemia Hematology, January 1, 2002; 2002(1): 73 - 110. [Abstract] [Full Text]
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V. T. Ho and R. J. Soiffer The history and future of T-cell depletion as graft-versus-host disease prophylaxis for allogeneic hematopoietic stem cell transplantation Blood, December 1, 2001; 98(12): 3192 - 3204. [Full Text] [PDF]
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I. Volpi, K. Perruccio, A. Tosti, M. Capanni, L. Ruggeri, S. Posati, F. Aversa, A. Tabilio, L. Romani, M. F. Martelli, et al. Postgrafting administration of granulocyte colony-stimulating factor impairs functional immune recovery in recipients of human leukocyte antigen haplotype-mismatched hematopoietic transplants Blood, April 15, 2001; 97(8): 2514 - 2521. [Abstract] [Full Text] [PDF]
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A. Mencacci, K. Perruccio, A. Bacci, E. Cenci, R. Benedetti, M. F. Martelli, F. Bistoni, R. Coffman, A. Velardi, and L. Romani Defective antifungal T-helper 1 (TH1) immunity in a murine model of allogeneic T-cell-depleted bone marrow transplantation and its restoration by treatment with TH2 cytokine antagonists Blood, March 1, 2001; 97(5): 1483 - 1490. [Abstract] [Full Text] [PDF]
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E. Chklovskaia, C. Nissen, L. Landmann, C. Rahner, O. Pfister, and A. Wodnar-Filipowicz Cell-surface trafficking and release of flt3 ligand from T lymphocytes is induced by common cytokine receptor {gamma}-chain signaling and inhibited by cyclosporin A Blood, February 15, 2001; 97(4): 1027 - 1034. [Abstract] [Full Text] [PDF]
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R. F. Storb, R. Champlin, S. R. Riddell, M. Murata, S. Bryant, and E. H. Warren Non-Myeloablative Transplants for Malignant Disease Hematology, January 1, 2001; 2001(1): 375 - 391. [Abstract] [Full Text] [PDF]
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R. W. Storms, M. A. Goodell, A. Fisher, R. C. Mulligan, and C. Smith Hoechst dye efflux reveals a novel CD7+CD34- lymphoid progenitor in human umbilical cord blood Blood, September 15, 2000; 96(6): 2125 - 2133. [Abstract] [Full Text] [PDF]
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TOP
ABSTRACT
INTRODUCTION
), and of the autologous donor's cells (
). E:T ratio = 10:1.
Shown are cytotoxicity assays with NK cell clones from four
representative recipients (see Table 
) were tested for their ability to
lyse pretransplant crypreserved leukemic cells from the same
individuals (
lymphocytes in mixed lymphocyte culture.
J Exp Med
168:2403, 1988