Human CD80/IL2 lentivirus-transduced acute myeloid leukaemia (AML) cells promote natural killer (NK) cell activation and cytolytic activity: Implications for a phase i clinical study

British Journal of Haematology

Volumn 145, Issue 6, 2009, Pages 749-760

  Ingram, Wendy ^a   Chan, Lucas ^a   Guven, Hayrettin ^a   Darling, David ^a   Kordasti, Shahram ^a   Hardwick, Nicola ^a   Barber, Linda ^a   Mufti, Ghulam J ^a   Farzaneh, Farzin ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Acute myeloid leukaemia; CD80; IL2; Lentivirus; NK cells

Indexed keywords

ANTIGEN; B7 ANTIGEN; CD244 ANTIGEN; CD69 ANTIGEN; HLA DR ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; LECTIN; LENTIVIRUS VECTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL KILLER CELL RECEPTOR NKG2C; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN P30; PROTEIN P44; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ALLOGENEIC PERIPHERAL BLOOD STEM CELL TRANSPLANTATION; ARTICLE; CELL ACTIVATION; CELL CULTURE; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DOWN REGULATION; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; AGED; ANTIGENS, CD80; CASE-CONTROL STUDIES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FLOW CYTOMETRY; GENETIC VECTORS; HUMANS; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; K562 CELLS; LENTIVIRUS; LEUKEMIA, MYELOID, ACUTE; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NATURAL KILLER T-CELLS; STATISTICS, NONPARAMETRIC; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED; YOUNG ADULT;

EID: 66749142914     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07684.x     Document Type: Article

References (45)

1. Benyunes, M.C., Massumoto, C., York, A., Higuchi, C.M., Buckner, C.D., Thompson, J.A., Petersen, F.B. Fefer, A. (1993) Interleukin-2 with or without lymphokine-activated killer cells as consolidative immunotherapy after autologous bone marrow transplantation for acute myelogenous leukemia. Bone Marrow Transplantation, 12, 159 163. (Pubitemid 23243419)
2. Biassoni, R., Cantoni, C., Pende, D., Sivori, S., Parolini, S., Vitale, M., Bottino, C. Moretta, A. (2001) Human natural killer cell receptors and co-receptors. Immunological Reviews, 181, 203 214. (Pubitemid 32703408)
3. Boughton, B.J. Simpson, A.W. (1999) Acute myeloblastic leukaemia: graft-versus-host and graft-versus-leukaemia responses to autologous IL-2 activated lymphocytes in rapid and slow disease. Cytokines Cellular & Molecular Therapy, 5, 1 6. (Pubitemid 29164354)
4. Bryceson, Y.T., March, M.E., Ljunggren, H.G. Long, E.O. (2006) Activation, coactivation, and costimulation of resting human natural killer cells. Immunological Reviews, 214, 73 91. (Pubitemid 44707903)
5. Cantoni, C., Bottino, C., Vitale, M., Pessino, A., Augugliaro, R., Malaspina, A., Parolini, S., Moretta, L., Moretta, A. Biassoni, R. (1999) NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. Journal of Experimental Medicine, 189, 787 796.
6. Chan, L., Hardwick, N., Darling, D., Galea-Lauri, J., Gaken, J., Devereux, S., Kemeny, M., Mufti, G. Farzaneh, F. (2005) IL-2/B7.1 (CD80) fusagene transduction of AML blasts by a self-inactivating lentiviral vector stimulates T cell responses in vitro: a strategy to generate whole cell vaccines for AML. Molecular Therapy, 11, 120 131. (Pubitemid 40012006)
7. Collins, Jr., R.H., Shpilberg, O., Drobyski, W.R., Porter, D.L., Giralt, S., Champlin, R., Goodman, S.A., Wolff, S.N., Hu, W., Verfaillie, C., List, A., Dalton, W., Ognoskie, N., Chetrit, A., Antin, J.H. Nemunaitis, J. (1997) Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. Journal of Clinical Oncology, 15, 433 444. (Pubitemid 27074209)
8. Costello, R.T., Sivori, S., Marcenaro, E., Lafage-Pochitaloff, M., Mozziconacci, M.J., Reviron, D., Gastaut, J.A., Pende, D., Olive, D. Moretta, A. (2002) Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood, 99, 3661 3667. (Pubitemid 34534536)
9. Dick, J.E. Lapidot, T. (2005) Biology of normal and acute myeloid leukemia stem cells. International Journal of Hematology, 82, 389 396. (Pubitemid 46638686)
10. Emtage, P.C., Wan, Y., Bramson, J.L., Graham, F.L. Gauldie, J. (1998) A double recombinant adenovirus expressing the costimulatory molecule B7-1 (murine) and human IL-2 induces complete tumor regression in a murine breast adenocarcinoma model. Journal of Immunology, 160, 2531 2538. (Pubitemid 28119940)
11. Farag, S.S., George, S.L., Lee, E.J., Baer, M., Dodge, R.K., Becknell, B., Fehniger, T.A., Silverman, L.R., Crawford, J., Bloomfield, C.D., Larson, R.A., Schiffer, C.A. Caligiuri, M.A. (2002a) Postremission therapy with low-dose interleukin 2 with or without intermediate pulse dose interleukin 2 therapy is well tolerated in elderly patients with acute myeloid leukemia: Cancer and Leukemia Group B study 9420. Clinical Cancer Research, 8, 2812 2819.
12. Farag, S.S., Fehniger, T.A., Ruggeri, L., Velardi, A. Caligiuri, M.A. (2002b) Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood, 100, 1935 1947. (Pubitemid 35001221)
13. Farag, S.S., Bacigalupo, A., Eapen, M., Hurley, C., Dupont, B., Caligiuri, M.A., Boudreau, C., Nelson, G., Oudshoorn, M., van Rood, J., Velardi, A., Maiers, M., Setterholm, M., Confer, D., Posch, P.E., Anasetti, C., Kamani, N., Miller, J.S., Weisdorf, D. Davies, S.M. (2006) The effect of KIR ligand incompatibility on the outcome of unrelated donor transplantation: a report from the center for international blood and marrow transplant research, the European blood and marrow transplant registry, and the Dutch registry. Biology of Blood and Marrow Transplantation, 12, 876 884. (Pubitemid 44070674)
14. Fauriat, C., Just-Landi, S., Mallet, F., Arnoulet, C., Sainty, D., Olive, D. Costello, R.T. (2007) Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood, 109, 323 330. (Pubitemid 46053073)
15. Gaken, J.A., Hollingsworth, S.J., Hirst, W.J., Buggins, A.G., Galea-Lauri, J., Peakman, M., Kuiper, M., Patel, P., Towner, P., Patel, P.M., Collins, M.K., Mufti, G.J., Farzaneh, F. Darling, D.C. (1997) Irradiated NC adenocarcinoma cells transduced with both B7.1 and interleukin-2 induce CD4+-mediated rejection of established tumors. Human Gene Therapy, 8, 477 488. (Pubitemid 27140550)
16. Galea-Lauri, J., Darling, D., Gan, S.U., Krivochtchapov, L., Kuiper, M., Gaken, J., Souberbielle, B. Farzaneh, F. (1999) Expression of a variant of CD28 on a subpopulation of human NK cells: implications for B7-mediated stimulation of NK cells. Journal of Immunology, 163, 62 70. (Pubitemid 29295825)
17. Goldstone, A.H., Burnett, A.K., Wheatley, K., Smith, A.G., Hutchinson, R.M. Clark, R.E. (2001) Attempts to improve treatment outcomes in acute myeloid leukemia (AML) in older patients: the results of the United Kingdom Medical Research Council AML11 trial. Blood, 98, 1302 1311.
18. Grimwade, D., Walker, H., Oliver, F., Wheatley, K., Harrison, C., Harrison, G., Rees, J., Hann, I., Stevens, R., Burnett, A. Goldstone, A. (1998) The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood, 92, 2322 2333.
19. Grimwade, D., Walker, H., Harrison, G., Oliver, F., Chatters, S., Harrison, C.J., Wheatley, K., Burnett, A.K. Goldstone, A.H. (2001) The predictive value of hierarchical cytogenetic classification in older adults with acute myeloid leukemia (AML): analysis of 1065 patients entered into the United Kingdom Medical Research Council AML11 trial. Blood, 98, 1312 1320.
20. Hsu, K.C., Gooley, T., Malkki, M., Pinto-Agnello, C., Dupont, B., Bignon, J.D., Bornhauser, M., Christiansen, F., Gratwohl, A., Morishima, Y., Oudshoorn, M., Ringden, O., van Rood, J.J. Petersdorf, E. (2006) KIR ligands and prediction of relapse after unrelated donor hematopoietic cell transplantation for hematologic malignancy. Biology of Blood and Marrow Transplantation, 12, 828 836. (Pubitemid 44070671)
21. Jaffe, E.S., Harris, N.L., Stein, H. Vardiman, J.W 2001) World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. IARC Press, Lyon, France.
22. Kolb, H.J., Schattenberg, A., Goldman, J.M., Hertenstein, B., Jacobsen, N., Arcese, W., Ljungman, P., Ferrant, A., Verdonck, L., Niederwieser, D., van Rhee, F., Mittermueller, J., de Witte, T., Holler, E. Ansari, H. (1995) Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. Blood, 86, 2041 2050.
23. Lim, S.H., Newland, A.C., Kelsey, S., Bell, A., Offerman, E., Rist, C., Gozzard, D., Bareford, D., Smith, M.P. Goldstone, A.H. (1992) Continuous intravenous infusion of high-dose recombinant interleukin-2 for acute myeloid leukaemia - a phase II study. Cancer Immunology Immunotherapy, 34, 337 342.
24. Luo, L. Han, Z.C. (2006) Leukemia stem cells. International Journal of Hematology, 84, 123 127. (Pubitemid 44343974)
25. Maraninchi, D., Vey, N., Viens, P., Stoppa, A.M., Archimbaud, E., Attal, M., Baume, D., Bouabdallah, R., Demeoq, F., Fleury, J., Michallet, M., Olive, D., Reiffers, J., Sainty, D., Tabilio, A., Tiberghien, P., Brandely, M., Hercend, T. Blaise, D. (1998) A phase II study of interleukin-2 in 49 patients with relapsed or refractory acute leukemia. Leukemia & Lymphoma, 31, 343 349. (Pubitemid 29033955)
26. Margolin, K.A., Van Besien, K., Wright, C., Niland, J., Champlin, R., Fung, H.C., Kashyap, A., Molina, A., Nademanee, A.P., O'Donnell, M.R., Parker, P., Smith, E., Spielberger, R., Somlo, G., Snyder, D., Stein, A., Woo, D., Thomas, M., Sniecinski, I. Forman, S.J. (1999) Interleukin-2-activated autologous bone marrow and peripheral blood stem cells in the treatment of acute leukemia and lymphoma. Biology of Blood and Marrow Transplantation, 5, 36 45.
27. Meloni, G., Vignetti, M., Andrizzi, C., Capria, S., Foa, R. Mandelli, F. (1996) Interleukin-2 for the treatment of advanced acute myelogenous leukemia patients with limited disease: updated experience with 20 cases. Leukemia & Lymphoma, 21, 429 435. (Pubitemid 26144767)
28. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M.C., Biassoni, R. Moretta, L. (2001) Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annual Review of Immunology, 19, 197 223. (Pubitemid 32368034)
29. Nowbakht, P., Ionescu, M.C., Rohner, A., Kalberer, C.P., Rossy, E., Mori, L., Cosman, D., De Libero, G. Wodnar-Filipowicz, A. (2005) 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, 105, 3615 3622. (Pubitemid 40628208)
30. Pende, D., Parolini, S., Pessino, A., Sivori, S., Augugliaro, R., Morelli, L., Marcenaro, E., Accame, L., Malaspina, A., Biassoni, R., Bottino, C., Moretta, L. Moretta, A. (1999) Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. Journal of Experimental Medicine, 190, 1505 1516.
31. Pende, D., Spaggiari, G.M., Marcenaro, S., Martini, S., Rivera, P., Capobianco, A., Falco, M., Lanino, E., Pierri, I., Zambello, R., Bacigalupo, A., Mingari, M.C., 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. (Pubitemid 40731793)
32. Pessino, A., Sivori, S., Bottino, C., Malaspina, A., Morelli, L., Moretta, L., Biassoni, R. Moretta, A. (1998) Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. Journal of Experimental Medicine, 188, 953 960. (Pubitemid 28433421)
33. Porter, D.L. (2003) Donor leukocyte infusions in acute myelogenous leukemia. Leukemia, 17, 1035 1037. (Pubitemid 36722232)
34. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W.D., Tosti, A., Posati, S., Rogaia, D., Frassoni, F., Aversa, F., Martelli, M.F. Velardi, A. (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science, 295, 2097 2100. (Pubitemid 34229476)
35. 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, M.F. 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. (Pubitemid 47026866)
36. Salih, H.R., Antropius, H., Gieseke, F., Lutz, S.Z., Kanz, L., Rammensee, H.G. Steinle, A. (2003) Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood, 102, 1389 1396. (Pubitemid 36988048)
37. Schaffer, M., Malmberg, K.J., Ringden, O., Ljunggren, H.G. Remberger, M. (2004) Increased infection-related mortality in KIR-ligand-mismatched unrelated allogeneic hematopoietic stem-cell transplantation. Transplantation, 78, 1081 1085. (Pubitemid 39391875)
38. Sivori, S., Vitale, M., Morelli, L., Sanseverino, L., Augugliaro, R., Bottino, C., Moretta, L. Moretta, A. (1997) p46, a novel natural killer cell-specific surface molecule that mediates cell activation. Journal of Experimental Medicine, 186, 1129 1136. (Pubitemid 27441156)
39. Slovak, M.L., Kopecky, K.J., Cassileth, P.A., Harrington, D.H., Theil, K.S., Mohamed, A., Paietta, E., Willman, C.L., Head, D.R., Rowe, J.M., Forman, S.J. Appelbaum, F.R. (2000) Karyotypic analysis predicts outcome of preremission and postremission therapy in adult acute myeloid leukemia: a Southwest Oncology Group/Eastern Cooperative Oncology Group Study. Blood, 96, 4075 4083.
40. Stripecke, R., Cardoso, A.A., Pepper, K.A., Skelton, D.C., Yu, X.J., Mascarenhas, L., Weinberg, K.I., Nadler, L.M. Kohn, D.B. (2000) Lentiviral vectors for efficient delivery of CD80 and granulocyte-macrophage- colony-stimulating factor in human acute lymphoblastic leukemia and acute myeloid leukemia cells to induce antileukemic immune responses. Blood, 96, 1317 1326. (Pubitemid 30658459)
41. Tajima, F., Kawatani, T., Endo, A. Kawasaki, H. (1996) Natural killer cell activity and cytokine production as prognostic factors in adult acute leukemia. Leukemia, 10, 478 482. (Pubitemid 26128788)
42. Vollmer, M., Li, L., Schmitt, A., Greiner, J., Reinhardt, P., Ringhoffer, M., Wiesneth, M., Dohner, H. Schmitt, M. (2003) Expression of human leucocyte antigens and co-stimulatory molecules on blasts of patients with acute myeloid leukaemia. British Journal of Haematology, 120, 1000 1008. (Pubitemid 36411559)
43. Wheatley, K., Burnett, A.K., Goldstone, A.H., Gray, R.G., Hann, I.M., Harrison, C.J., Rees, J.K., Stevens, R.F. Walker, H. (1999) A simple, robust, validated and highly predictive index for the determination of risk-directed therapy in acute myeloid leukaemia derived from the MRC AML 10 trial. United Kingdom Medical Research Council's Adult and Childhood Leukaemia Working Parties. British Journal of Haematology, 107, 69 79.
44. Whiteway, A., Corbett, T., Anderson, R., Macdonald, I. Prentice, H.G. (2003) Expression of co-stimulatory molecules on acute myeloid leukaemia blasts may effect duration of first remission. British Journal of Haematology, 120, 442 451. (Pubitemid 36241500)
45. Wilson, J.L., Charo, J., Martin-Fontecha, A., Dellabona, P., Casorati, G., Chambers, B.J., Kiessling, R., Bejarano, M.T. Ljunggren, H.G. (1999) NK cell triggering by the human costimulatory molecules CD80 and CD86. Journal of Immunology, 163, 4207 4212. (Pubitemid 29474484)