Good manufacturing practice-compliant cell sorting and large-scale expansion of single KIR-positive alloreactive human natural killer cells for multiple infusions to leukemia patients

References

• Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;354:1813–26.
   PubMed Web of Science ®Google Scholar
• Moretta L, Ferlazzo G, Bottino C, Vitale M, Pende D, Mingari MC, . Effector and regulatory events during natural killer-dendritic cell interactions. Immunol Rev. 2006;214:219–28.
   PubMed Web of Science ®Google Scholar
• Andoniou CE, Coudert JD, Degli-Esposti MA. Killers and beyond: NK-cell-mediated control of immune responses. Eur J Immunol. 2008;38:2938–42.
   Google Scholar
• Caligiuri MA. Human natural killer cells. Blood. 2008;112: 461–9.
   PubMed Web of Science ®Google Scholar
• Farag SS, Fehniger TA, Ruggeri L, Velardi A, Caligiuri MA. Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood. 2002;100:1935–47.
   PubMed Web of Science ®Google Scholar
• Ruggeri L, Aversa F, Martelli MF, Velardi A. Allogeneic hematopoietic transplantation and natural killer cell recognition of missing self. Immunol Rev. 2006;214:202–18.
   PubMed Web of Science ®Google Scholar
• Verheyden S, Demanet C. NK cell receptors and their ligands in leukemia. Leukemia. 2008;22:249–57.
   PubMed Web of Science ®Google Scholar
• Passweg JR, Stern M, Koehl U, Uharek L, Tichelli A. Use of natural killer cells in hematopoetic stem cell transplantation. Bone Marrow Transplant. 2005;35:637–43.
   PubMed Web of Science ®Google Scholar
• Ljunggren HG, Malmberg KJ. Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol. 2007;7:329–39.
   PubMed Web of Science ®Google Scholar
• Terme M, Ullrich E, Delahaye NF, Chaput N, Zitvogel L. Natural killer cell-directed therapies: moving from unexpected results to successful strategies. Nat Immunol. 2008;9:486–94.
   PubMed Web of Science ®Google Scholar
• Grzywacz B, Miller JS, Verneris MR. Use of natural killer cells as immunotherapy for leukaemia. Best Pract Res Clin Haematol. 2008;21:467–83.
   PubMed Web of Science ®Google Scholar
• Parham P. Taking license with natural killer cell maturation and repertoire development. Immunol Rev. 2006;214:155–60.
   PubMed Web of Science ®Google Scholar
• Raulet DH, Vance RE, McMahon CW. Regulation of the natural killer cell receptor repertoire. Annu Rev Immunol. 2001;19:291–330.
   PubMed Web of Science ®Google Scholar
• Lanier LL. NK cell recognition. Annu Rev Immunol. 2005;23:225–74.
   PubMed Web of Science ®Google Scholar
• Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, . Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol. 2001;19:197–223.
   PubMed Web of Science ®Google Scholar
• Vitale M, Bottino C, Sivori S, Sanseverino L, Castriconi R, Marcenaro E, . NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J Exp Med. 1998;187:2065–72.
   PubMed Web of Science ®Google Scholar
• Sutherland CL, Chalupny NJ, Schooley K, VandenBos T, Kubin M, Cosman D. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. J Immunol. 2002;168:671–9.
   PubMed Web of Science ®Google Scholar
• Baeriswyl V, Wodnar-Filipowicz A, Kalberer CP. The effect of silencing NKG2D through RNA interference on receptor functions in interleukin-2-activated human natural killer cells. Haematologica. 2006;91:1538–41.
   PubMed Web of Science ®Google Scholar
• Becknell B, Caligiuri MA. Interleukin-2, interleukin-15, and their roles in human natural killer cells. Adv Immunol. 2005;86:209–39.
   PubMed Web of Science ®Google Scholar
• Sutlu T, Alici E. Natural killer cell-based immunotherapy in cancer: current insights and future prospects. J Intern Med. 2009;266:154–81.
   PubMed Web of Science ®Google Scholar
• Meyer-Monard S, Passweg J, Siegler U, Kalberer C, Koehl U, Rovo A, . Clinical-grade purification of natural killer cells in haploidentical hematopoietic stem cell transplantation. Transfusion. 2009;49:362–71.
   PubMed Web of Science ®Google Scholar
• Siegler U, Kalberer CP, Nowbakht P, Sendelov S, Meyer-Monard S, Wodnar-Filipowicz A. Activated natural killer cells from patients with acute myeloid leukemia are cytotoxic against autologous leukemic blasts in NOD/SCID mice. Leukemia. 2005;19:2215–22.
   PubMed Web of Science ®Google Scholar
• Diermayr S, Himmelreich H, Durovic B, Mathys-Schneeberger A, Siegler U, Langenkamp U, . 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. 2008;111:1428–36.
   PubMed Web of Science ®Google Scholar
• Ishikawa F, Yoshida S, Saito Y, Hijikata A, Kitamura H, Tanaka S, . Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol. 2007;25:1315–21.
   PubMed Web of Science ®Google Scholar
• Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, . Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med. 2005;201:1307–18.
   PubMed Web of Science ®Google Scholar
• Lewalle P, Triffet A, Delforge A, Crombez P, Selleslag D, De Muynck H, . Donor lymphocyte infusions in adult haploidentical transplant: a dose finding study. Bone Marrow Transplant. 2003;31:39–44.
   PubMed Web of Science ®Google Scholar
• Kolb HJ. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood. 2008;112:4371–83.
   PubMed Web of Science ®Google Scholar
• Chklovskaia E, Nowbakht P, Nissen C, Gratwohl A, Bargetzi M, Wodnar-Filipowicz A. Reconstitution of dendritic and natural killer-cell subsets after allogeneic stem cell transplantation: effects of endogenous flt3 ligand. Blood. 2004;103:3860–8.
   PubMed Web of Science ®Google Scholar
• Nguyen S, Dhedin N, Vernant JP, Kuentz M, Al Jijakli A, Rouas-Freiss N, . NK-cell reconstitution after haploidentical hematopoietic stem-cell transplantations: immaturity of NK cells and inhibitory effect of NKG2A override GvL effect. Blood. 2005;105:4135–42.
   PubMed Web of Science ®Google Scholar
• Vago L, Forno B, Sormani MP, Crocchiolo R, Zino E, Di Terlizzi S, . Temporal, quantitative, and functional characteristics of single-KIR-positive alloreactive natural killer cell recovery account for impaired graft-versus-leukemia activity after haploidentical hematopoietic stem cell transplantation. Blood. 2008;112:3488–99.
   PubMed Web of Science ®Google Scholar
• Koehl U, Sorensen J, Esser R, Zimmermann S, Gruttner HP, Tonn T, . IL-2 activated NK cell immunotherapy of three children after haploidentical stem cell transplantation. Blood Cells Mol Dis. 2004;33:261–6.
   PubMed Web of Science ®Google Scholar
• Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, . Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105:3051–7.
   PubMed Web of Science ®Google Scholar
• Passweg JR, Tichelli A, Meyer-Monard S, Heim D, Stern M, Kuhne T, . Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia. 2004;18:1835–8.
   PubMed Web of Science ®Google Scholar
• Berg M, Lundqvist A, , McCoy P JrSamsel L, Fan Y, Tawab A, . Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy. 2009;11:341–55.
   PubMed Web of Science ®Google Scholar
• Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, . Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 2009;69:4010–7.
   PubMed Web of Science ®Google Scholar
• Luhm J, Brand JM, Koritke P, Hoppner M, Kirchner H, Frohn C. Large-scale generation of natural killer lymphocytes for clinical application. J Hematother Stem Cell Res. 2002;11:651–7.
   PubMedGoogle Scholar
• Koehl U, Esser R, Zimmermann S, Tonn T, Kotchetkov R, Bartling T, . Ex vivo expansion of highly purified NK cells for immunotherapy after haploidentical stem cell transplantation in children. Klin Padiatr. 2005;217:345–50.
   PubMed Web of Science ®Google Scholar
• Fauriat C, Andersson S, Bjorklund AT, Carlsten M, Schaffer M, Bjorkstrom NK, . Estimation of the size of the alloreactive NK cell repertoire: studies in individuals homozygous for the group A KIR haplotype. J Immunol. 2008;181:6010–9.
   PubMed Web of Science ®Google Scholar
• Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, Stewart CA, . Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25:331–42.
   PubMed Web of Science ®Google Scholar
• Cooley S, Xiao F, Pitt M, Gleason M, McCullar V, Bergemann TL, . A subpopulation of human peripheral blood NK cells that lacks inhibitory receptors for self-MHC is developmentally immature. Blood. 2007;110:578–86.
   PubMed Web of Science ®Google Scholar
• Carlens S, Gilljam M, Chambers BJ, Aschan J, Guven H, Ljunggren HG, . A new method for in vitro expansion of cytotoxic human CD3−CD56+ natural killer cells. Hum Immunol. 2001;62:1092–8.
   PubMed Web of Science ®Google Scholar
• Brentjens RJ, Latouche JB, Santos E, Marti F, Gong MC, Lyddane C, . Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med. 2003;9:279–86.
   PubMed Web of Science ®Google Scholar
• Huntington ND, Puthalakath H, Gunn P, Naik E, Michalak EM, Smyth MJ, . Interleukin 15-mediated survival of natural killer cells is determined by interactions among Bim, Noxa and Mcl-1. Nat Immunol. 2007;8:856–63.
   PubMed Web of Science ®Google Scholar
• Vago L, Perna SK, Zanusi M, Mazzi B, Barlassina C, Stanghellini MT, . Loss of mismatched HLA in leukemia after stem-cell transplantation. N Engl J Med. 2009;361: 478–88.
   PubMed Web of Science ®Google Scholar
• Romagne F, Andre P, Spee P, Zahn S, Anfossi N, Gauthier L, . Pre-clinical characterization of 1-7F9, a novel human anti-KIR therapeutic antibody that augments NK-mediated killing of tumor cells. Blood. 2009;114:2267–77.
   Web of Science ®Google Scholar
• Pende D, Spaggiari GM, Marcenaro S, Martini S, Rivera P, Capobianco A, . 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. 2005;105:2066–73.
   PubMed Web of Science ®Google Scholar
• Nowbakht P, Ionescu MC, Rohner A, Kalberer CP, Rossy E, Mori L, . 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. 2005;105:3615–22.
   PubMed Web of Science ®Google Scholar
• Rohner A, Langenkamp U, Siegler U, Kalberer CP, Wodnar-Filipowicz A. Differentiation-promoting drugs up-regulate NKG2D ligand expression and enhance the susceptibility of acute myeloid leukemia cells to natural killer cell-mediated lysis. Leuk Res. 2007;31:1393–402.
   PubMed Web of Science ®Google Scholar
• Langenkamp U, Siegler U, Jorger S, Diermayr S, Gratwohl A, Kalberer CP, . Human acute myeloid leukemia CD34+CD38− stem cells are susceptible to allorecognition and lysis by single KIR-expressing natural killer cells. Haematologica. 2009;94:1590–4.
   PubMed Web of Science ®Google Scholar
• Hope KJ, Jin L, Dick JE. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat Immunol. 2004;5:738–43.
   PubMed Web of Science ®Google Scholar
• Nervi B, Ramirez P, Rettig MP, Uy GL, Holt MS, Ritchey JK, . Chemosensitization of acute myeloid leukemia (AML) following mobilization by the CXCR4 antagonist AMD3100. Blood. 2009;113:6206–14.
   PubMed Web of Science ®Google Scholar
• Cooley S, Trachtenberg E, Bergemann TL, Saeteurn K, Klein J, Le CT, . Donors with group B KIR haplotypes improve relapse-free survival after unrelated hematopoietic cell transplantation for acute myelogenous leukemia. Blood 2009; 113:726–732.
   PubMed Web of Science ®Google Scholar