Immunophenotypic and functional characterization of ex vivo expanded natural killer cells for clinical use in acute lymphoblastic leukemia patients

Cancer Immunology, Immunotherapy

Volumn 64, Issue 2, 2015, Pages 201-211

  Peragine, Nadia ^a   Torelli, Giovanni F ^a   Mariglia, Paola ^a   Pauselli, Simona ^a   Vitale, Antonella ^a   Guarini, Anna ^a   Foà, Robin ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

ALL; Expansion; Immunotherapy; NK

Indexed keywords

DNAM1 PROTEIN; INTERLEUKIN 15; INTERLEUKIN 2; LYMPHOCYTE RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; UNCLASSIFIED DRUG; MEMBRANE ANTIGEN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADULT; ARTICLE; CANCER IMMUNOTHERAPY; CD3+ T LYMPHOCYTE; CELL EXPANSION; CELL ISOLATION; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; ENRICHMENT CULTURE; EX VIVO STUDY; FEEDER CELL; GOOD MANUFACTURING PRACTICE; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IRRADIATION; K562 CELL LINE; LEUKEMIA REMISSION; LYMPHOCYTE ACTIVATION; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; T CELL DEPLETION; UPREGULATION; ADOPTIVE IMMUNOTHERAPY; CULTURE TECHNIQUE; CYTOLOGY; CYTOTOXICITY; IMMUNOLOGY; METABOLISM; PHENOTYPE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA;

ANTIGENS, SURFACE; CELL CULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; K562 CELLS; KILLER CELLS, NATURAL; PHENOTYPE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA;

EID: 84925487710     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1614-z     Document Type: Article

References (43)

1. Robertson MJ, Ritz J (1990) Biology and clinical relevance of human natural killer cells. Blood 76:2421–2438
2. Miller JS (2001) The biology of natural killer cells in cancer, infection, and pregnancy. Exp Hematol 29:1157–1168
3. Thielens A, Vivier E, Romagné F (2012) NK cell MHC class I specific receptors [KIR]: from biology to clinical intervention. Curr Opin Immunol 24:239–245
4. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L (2001) Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 19:197–223
5. Coudert JD, Held W (2006) The role of the NKG2D receptor for tumor immunity. Semin Cancer Biol 16:333–343
6. Eagle RA, Trowsdale J (2007) Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 7:737–744
7. Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T, Hannum C, Kitamura T, Nicholl J, Sutherland GR, Lanier LL, Phillips JH (1996) DNAM1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 4:573–581
8. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225–274
9. Stewart CA, Laugier-Anfossi F, Vély F, Saulquin X, Riedmuller J, Tisserant A, Gauthier L, Romagné F, Ferracci G, Arosa FA, Moretta A, Sun PD, Ugolini S, Vivier E (2005) Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc Natl Acad Sci USA 102:13224–13229
10. Cheng M, Chen Y, Xiao W, Sun R, Tian Z (2013) NK cell-based immunotherapy for malignant diseases. Cell Mol Immunol 10:230–252
11. Siegler U, Kalberer CP, Nowbakht P, Sendelov S, Meyer-Monard S, Wodnar-Filipowicz A (2005) Activated natural killer cells from patients with acute myeloid leukemia are cytotoxic against autologous leukemic blasts in NOD/SCID mice. Leukemia 19:2215–2222
12. Adler A, Chervenick PA, Whiteside TL, Lotzová E, Herberman RB (1988) Interleukin 2 induction of lymphokine-activated killer (LAK) activity in the peripheral blood and bone marrow of acute leukemia patients. I. Feasibility of LAK generation in adult patients with active disease and in remission. Blood 71:709–716
13. Fierro MT, Liao XS, Lusso P, Bonferroni M, Matera L, Cesano A, Lista P, Arione R, Forni G, Foa R (1988) In vitro and in vivo susceptibility of human leukemic cells to lymphokine activated killer activity. Leukemia 2:50–54
14. Brune M, Castaigne S, Catalano J, Gehlsen K, Ho AD, Hofmann WK, Hogge DE, Nilsson B, Or R, Romero AI, Rowe JM, Simonsson B, Spearing R, Stadtmauer EA, Szer J, Wallhult E, Hellstrand K (2006) Improved leukemia-free survival after postconsolidation immunotherapy with histamine dihydrochloride and interleukin-2 in acute myeloid leukemia: results of a randomized phase 3 trial. Blood 108:88–96
15. Ruggeri L, Capanni M, Casucci M, Volpi I, Tosti A, Perruccio K, Urbani E, Negrin RS, Martelli MF, Velardi A (1999) Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 94:333–339
16. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F, Martelli MF, Velardi A (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295:2097–2100
17. Ruggeri L, Mancusi A, Capanni M, Urbani E, Carotti A, Aloisi T, Stern M, Pende D, Perruccio K, Burchielli E, Topini F, Bianchi E, Aversa F, Martelli MF, Velardi A (2007) Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood 110:433–440
18. Pende D, Spaggiari GM, Marcenaro S, Martini S, Rivera P, Capobianco A, Falco M, Lanino E, Pierri I, Zambello R, Bacigalupo A, Mingari MC, Moretta A, Moretta L (2005) 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 105:2066–2073
19. Pende D, Marcenaro S, Falco M, Martini S, Bernardo ME, Montagna D, Romeo E, Cognet C, Martinetti M, Maccario R, Mingari MC, Vivier E, Moretta L, Locatelli F, Moretta A (2009) Anti-leukemia activity of alloreactive NK cells in KIR ligand-mismatched haploidentical HSCT for pediatric patients: evaluation of the functional role of activating KIR and re-definition of inhibitory KIR specificity. Blood 113:3119–3129
20. Jardine L, Hambleton S, Bigley V, Pagan S, Wang XN, Collin M (2013) Sensitizing primary acute lymphoblastic leukemia to natural killer cell recognition by induction of NKG2D ligands. Leuk Lymphoma 54:167–173
21. Torelli GF, Guarini A, Maggio R, Alfieri C, Vitale A, Foà R (2005) Expansion of natural killer cells with lytic activity against autologous blasts from adult and pediatric acute lymphoid leukemia patients in complete hematologic remission. Haematologica 90:785–792
22. Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, Ettinghausen SE, Matory YL, Skibber JM, Shiloni E, Vetto JT, Seipp CA, Simpson C, Reichert CM (1985) Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med 313:1485–1492
23. Stern M, Passweg JR, Meyer-Monard S, Esser R, Tonn T, Soerensen J, Paulussen M, Gratwohl A, Klingebiel T, Bader P, Tichelli A, Schwabe D, Koehl U (2013) Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: a prospective phase II study in two centers. Bone Marrow Transplant 48:433–438
24. Carlens S, Gilljam M, Chambers BJ, Aschan J, Guven H, Ljunggren HG, Christensson B, Dilber MS (2001) A new method for in vitro expansion of cytotoxic human CD3−CD56+ natural killer cells. Hum Immunol 62:1092–1098
25. McKenna DH Jr, Sumstad D, Bostrom N, Kadidlo DM, Fautsch S, McNearney S, Dewaard R, McGlave PB, Weisdorf DJ, Wagner JE, McCullough J, Miller JS (2007) Good manufacturing practices production of natural killer cells for immunotherapy: a six-year single-institution experience. Transfusion 47:520–528
26. Luhm J, Brand JM, Koritke P, Hoppner M, Kirchner H, Frohn C (2002) Large-scale generation of natural killer lymphocytes for clinical application. J Hematother Stem Cell Res 11:651–657
27. Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, Eldridge P, Leung WH, Campana D (2009) Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res 69:4010–4017
28. Perussia B, Ramoni C, Anegon I, Cuturi MC, Faust J, Trinchieri G (1987) Preferential proliferation of natural killer cells among peripheral blood mononuclear cells cocultured with B lymphoblastoid cell lines. Nat Immun Cell Growth Regul 6:171–188
29. Miller JS, Oelkers S, Verfaillie C, McGlave P (1992) Role of monocytes in the expansion of human activated natural killer cells. Blood 80:2221–2229
30. Boissel L, Tuncer HH, Betancur M, Wolfberg A, Klingemann H (2008) Umbilical cord mesenchymal stem cells increase expansion of cord blood natural killer cells. Biol Blood Marrow Transplant 14:1031–1038
31. Alici E, Sutlu T, Björkstrand B, Gilljam M, Stellan B, Nahi H, Quezada HC, Gahrton G, Ljunggren H, Dilber MS (2008) Autologous antitumor activity by NK cells expanded from myeloma patients using GMP-compliant components. Blood 111:3155–3162
32. Lim SA, Kim TJ, Lee JE, Sonn CH, Kim K, Kim J, Choi JG, Choi IK, Yun CO, Kim JH, Yee C, Kumar V, Lee KM (2013) Ex vivo expansion of highly cytotoxic human NK cells by cocultivation with irradiated tumor cells for adoptive immunotherapy. Cancer Res 73:2598–2607
33. Suck G, Koh MB (2010) Emerging natural killer cell immunotherapies: large-scale ex vivo production of highly potent anticancer effectors. Hematol Oncol Stem Cell Ther 3:135–142
34. Miller JS (2009) Should natural killer cells be expanded in vivo or ex vivo to maximize their therapeutic potential? Cytotherapy 11:259–260
35. Koehl U, Esser R, Zimmermann S, Tonn T, Kotchetkov R, Bartling T, Sörensen J, Grüttner HP, Bader P, Seifried E, Martin H, Lang P, Passweg JR, Klingebiel T, Schwabe D (2005) Ex vivo expansion of highly purified NK cells for immunotherapy after haploidentical stem cell transplantation in children. Klin Padiatr 217:345–350
36. Harada H, Saijo K, Watanabe S, Tsuboi K, Nose T, Ishiwata I, Ohno T (2002) Selective expansion of human natural killer cells from peripheral blood mononuclear cells by the cell line, HFWT. Jpn J Cancer Res 93:313–319
37. Shook DR, Campana D (2011) Natural killer cell engineering for cellular therapy of cancer. Tissue Antigens 78:409–415
38. Lapteva N, Durett AG, Sun J, Rollins LA, Huye LL, Fang J, Dandekar V, Mei Z, Jackson K, Vera J, Ando J, Ngo MC, Coustan-Smith E, Campana D, Szmania S, Garg T, Moreno-Bost A, Vanrhee F, Gee AP, Rooney CM (2012) Large-scale ex vivo expansion and characterization of natural killer cells for clinical applications. Cytotherapy 14:1131–1143
39. Lin CY, Chuang TF, Liao KW, Huang YJ, Pai CC, Chu RM (2008) Combined immunogene therapy of IL-6 and IL-15 enhances anti-tumor activity through augmented NK cytotoxicity. Cancer Lett 272:285–295
40. Spanholtz J, Tordoir M, Eissens D, Preijers F, van der Meer A, Joosten I, Schaap N, de Witte TM, Dolstra H (2010) High log-scale expansion of functional human natural killer cells from umbilical cord blood CD34-positive cells for adoptive cancer immunotherapy. PLoS ONE 5:e9221
41. Huenecke S, Zimmermann SY, Kloess S, Esser R, Brinkmann A, Tramsen L, Koenig M, Erben S, Seidl C, Tonn T, Eggert A, Schramm A, Bader P, Klingebiel T, Lehrnbecher T, Passweg JR, Soerensen J, Schwabe D, Koehl U (2010) IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16− subpopulations and in vivo influence after haploidentical NK cell infusion. J Immunother 33:200–210
42. Béziat V, Descours B, Parizot C, Debré P, Vieillard V (2010) NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS One 5:e11966
43. Torelli GF, Peragine N, Raponi S, Pagliara D, De Propris MS, Vitale A, Bertaina A, Barberi W, Moretta L, Basso G, Santoni A, Guarini A, Locatelli F, Foa’ R (2014) Recognition of adult and pediatric acute lymphoblastic leukemia blasts by natural killer cells. Haematologica 99:1248–1254