Role of natural killer cell subsets and natural cytotoxicity receptors for the outcome of immunotherapy in acute myeloid leukemia

OncoImmunology

Volumn 5, Issue 1, 2016, Pages

  Martner, Anna ^a   Rydström, Anna ^a   Riise, Rebecca E ^a   Aurelius, Johan ^a,b   Anderson, Harald ^c   Brune, Mats ^b   Foà, Robin ^d   Hellstrand, Kristoffer ^a   Thorén, Fredrik B ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Acute myeloid leukemia; Immunotherapy; Natural cytotoxicity receptors; Natural killer cells

Indexed keywords

ALDESLEUKIN; AMSACRINE; CD16 ANTIGEN; CD56 ANTIGEN; CYTARABINE; DAUNORUBICIN; ETOPOSIDE; FLUDARABINE; FLUORESCEIN ISOTHIOCYANATE; HISTAMINE; IDARUBICIN DERIVATIVE; INTERLEUKIN 2; METHOTREXATE; MITOXANTRONE; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; OZOGAMICIN;

ACUTE MYELOBLASTIC LEUKEMIA; ADULT; AGED; ALLOTRANSPLANTATION; ARTICLE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; CANCER IMMUNOTHERAPY; CANCER RECURRENCE; CANCER SURVIVAL; CELL VIABILITY; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; HUMAN; LYMPHOCYTE COUNT; MAJOR CLINICAL STUDY; MULTICENTER STUDY; MULTIPLE CYCLE TREATMENT; NATURAL KILLER CELL; OUTCOME ASSESSMENT; PHARMACODYNAMICS; PHASE 4 CLINICAL TRIAL; PHENOTYPE; POST HOC ANALYSIS; TREATMENT OUTCOME;

EID: 84954431921     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1041701     Document Type: Article

References (51)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015; 65:5-29; PMID:25559415; http://dx. doi. org/10. 3322/caac. 21254
2. Breems DA, Van Putten WL, Huijgens PC, Ossenkoppele GJ, Verhoef GE, Verdonck LF, Vellenga E, De Greef GE, Jacky E, Van der Lelie J et al. Prognostic index for adult patients with acute myeloid leukemia in first relapse. J Clin Oncol 2005; 23:1969-78; PMID:15632409; http://dx. doi. org/ 10. 1200/JCO. 2005. 06. 027
3. Burnett AK, Goldstone A, Hills RK, Milligan D, Prentice A, Yin J, Wheatley K, Hunter A, Russell N. Curability of patients with acute myeloid leukemia who did not undergo transplantation in first remission. J Clin Oncol 2013; 31:1293-301; PMID:23439754; http://dx. doi. org/10. 1200/ JCO. 2011. 40. 5977
4. Tallman MS, Gilliland DG, Rowe JM. Drug therapy for acute myeloid leukemia. Blood 2005; 106:1154-63; PMID:15870183; http://dx. doi. org/10. 1182/blood-2005-01-0178
5. Juliusson G, Lazarevic V, Horstedt AS, Hagberg O, Hoglund M, Swedish Acute Leukemia Registry G. Acute myeloid leukemia in the real world: why population-based registries are needed. Blood 2012; 119:3890-9; PMID:22383796; http://dx. doi. org/ 10. 1182/blood-2011-12-379008
6. Costello RT, Sivori S, Marcenaro E, Lafage-Pochitaloff M, Mozziconacci MJ, Reviron D, Gastaut JA, Pende D, Olive D, Moretta A. Defective expression and function of natural killer cell-triggering receptors in patients with acute myeloid leukemia. Blood 2002; 99:3661-7; PMID:11986221; http://dx. doi. org/10. 1182/blood. V99. 10. 3661
7. Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, Olive D, Costello RT. 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 2007; 109:323-30; PMID:16940427; http://dx. doi. org/ 10. 1182/blood-2005-08-027979
8. Lauria F, Raspadori D, Rondelli D, Ventura MA, Foa R. In vitro susceptibility of acute leukemia cells to the cytotoxic activity of allogeneic and autologous lymphokine activated killer (LAK) effectors: correlation with the rate and duration of complete remission and with survival. Leukemia 1994; 8:724-8; PMID:8182932
9. Orleans-Lindsay JK, Barber LD, Prentice HG, Lowdell MW. Acute myeloid leukaemia cells secrete a soluble factor that inhibits T and NK cell proliferation but not cytolytic function-implications for the adoptive immunotherapy of leukaemia. Clin Exp Immunol 2001; 126:403-11; PMID:11737054; http://dx. doi. org/ 10. 1046/j. 1365-2249. 2001. 01692. x
10. Panoskaltsis N, Reid CD, Knight SC. Quantification and cytokine production of circulating lymphoid and myeloid cells in acute myelogenous leukaemia. Leukemia 2003; 17:716-30; PMID:12682629; http://dx. doi. org/10. 1038/sj. leu. 2402835
11. Tajima F, Kawatani T, Endo A, Kawasaki H. Natural killer cell activity and cytokine production as prognostic factors in adult acute leukemia. Leukemia 1996; 10:478-82; PMID:8642865
12. Lion E, Willemen Y, Berneman ZN, Van Tendeloo VF, Smits EL. Natural killer cell immune escape in acute myeloid leukemia. Leukemia 2012; 26:2019-26; PMID:22446501; http://dx. doi. org/10. 1038/ leu. 2012. 87
13. Martner A, Thoren FB, Aurelius J, Hellstrand K. Immunotherapeutic strategies for relapse control in acute myeloid leukemia. Blood Rev 2013; 27:209-16; PMID:23871358; http://dx. doi. org/10. 1016/j. blre. 2013. 06. 006
14. Sanchez-Correa B, Morgado S, Gayoso I, Bergua JM, Casado JG, Arcos MJ, Bengochea ML, Duran E, Solana R, Tarazona R. Human NK cells in acute myeloid leukaemia patients: analysis of NK cell-activating receptors and their ligands. Cancer Immunol Immunother 2011; 60:1195-205; PMID:21644031; http://dx. doi. org/10. 1007/s00262-011-1050-2
15. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002; 295:2097-100; PMID:11896281; http://dx. doi. org/10. 1126/science. 1068440
16. Hsu KC, Keever-Taylor CA, Wilton A, Pinto C, Heller G, Arkun K, O'Reilly RJ, Horowitz MM, Dupont B. Improved outcome in HLA-identical sibling hematopoietic stem-cell transplantation for acute myelogenous leukemia predicted by KIR and HLA genotypes. Blood 2005; 105:4878-84; PMID:15731175; http://dx. doi. org/10. 1182/blood-2004-12-4825
17. Moretta L, Locatelli F, Pende D, Marcenaro E, Mingari MC, Moretta A. Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 2011; 117:764-71; PMID:20889923; http://dx. doi. org/ 10. 1182/blood-2010-08-264085
18. Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol 1989; 143:3183-91; PMID:2530273
19. Caligiuri MA. Human natural killer cells. Blood 2008; 112:461-9; PMID:18650461; http://dx. doi. org/ 10. 1182/blood-2007-09-077438
20. Chan A, Hong DL, Atzberger A, Kollnberger S, Filer AD, Buckley CD, McMichael A, Enver T, Bowness P. CD56bright human NK cells differentiate into CD56dim cells: role of contact with peripheral fibroblasts. J Immunol 2007; 179:89-94; PMID:17579025; http://dx. doi. org/10. 4049/jimmunol. 179. 1. 89
21. Poli A, Michel T, Theresine M, Andres E, Hentges F, Zimmer J. CD56bright natural killer (NK) cells: an important NK cell subset. Immunology 2009; 126:458-65; PMID:19278419; http://dx. doi. org/ 10. 1111/j. 1365-2567. 2008. 03027. x
22. Romagnani C, Juelke K, Falco M, Morandi B, D'Agostino A, Costa R, Ratto G, Forte G, Carrega P, Lui G et al. CD56brightCD16-killer Ig-like receptor-NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J Immunol 2007; 178:4947-55; PMID:17404276; http://dx. doi. org/10. 4049/jimmunol. 178. 8. 4947
23. Babor F, Fischer JC, Uhrberg M. The role of KIR genes and ligands in leukemia surveillance. Frontiers in immunology 2013; 4:27; PMID:23404428; http://dx. doi. org/10. 3389/fimmu. 2013. 00027
24. Lanier LL. NK cell recognition. Annu Rev Immunol 2005; 23:225-74; PMID:15771571; http://dx. doi. org/ 10. 1146/annurev. immunol. 23. 021704. 115526
25. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol 2013; 31:227-58; PMID:23516982; http://dx. doi. org/ 10. 1146/annurev-immunol-020711-075005
26. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 2001; 19:197-223; PMID:11244035; http://dx. doi. org/ 10. 1146/annurev. immunol. 19. 1. 197
27. Geller MA, Miller JS. Use of allogeneic NK cells for cancer immunotherapy. Immunotherapy 2011; 3:1445-59; PMID:22091681; http://dx. doi. org/ 10. 2217/imt. 11. 131
28. Brune M, Castaigne S, Catalano J, Gehlsen K, Ho AD, Hofmann WK, Hogge DE, Nilsson B, Or R, Romero AI et al. 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 2006; 108:88-96; PMID:16556892; http://dx. doi. org/ 10. 1182/blood-2005-10-4073
29. Aurelius J, Martner A, Brune M, Palmqvist L, Hansson M, Hellstrand K, Thoren FB. Remission maintenance in acute myeloid leukemia: impact of functional histamine H2 receptors expressed by leukemic cells. Haematologica 2012; 97:1904-8; PMID:22689678; http://dx. doi. org/10. 3324/haematol. 2012. 066399
30. Aurelius J, Thoren FB, Akhiani AA, Brune M, Palmqvist L, Hansson M, Hellstrand K, Martner A. Monocytic AML cells inactivate antileukemic lymphocytes: role of NADPH oxidase/gp91(phox) expression and the PARP-1/PAR pathway of apoptosis. Blood 2012; 119:5832-7; PMID:22550344; http://dx. doi. org/ 10. 1182/blood-2011-11-391722
31. Hellstrand K, Asea A, Dahlgren C, Hermodsson S. Histaminergic regulation of NK cells. Role of monocyte-derived reactive oxygen metabolites. J Immunol 1994; 153:4940-7; PMID:7963557
32. Hellstrand K, Hermodsson S. Histamine H2-receptormediated regulation of human natural killer cell activity. J Immunol 1986; 137:656-60; PMID:3722819
33. Hellstrand K, Asea A, Hermodsson S. Role of histamine in natural killer cell-mediated resistance against tumor cells. J Immunol 1990; 145:4365-70; PMID:2147942
34. Thoren FB, Aurelius J, Martner A. Antitumor properties of histamine in vivo. Nature medicine 2011; 17:537; PMID:21546964; http://dx. doi. org/10. 1038/ nm0511-537a
35. Buyse M, Squifflet P, Lucchesi KJ, Brune ML, Castaigne S, Rowe JM. Assessment of the consistency and robustness of results from a multicenter trial of remission maintenance therapy for acute myeloid leukemia. Trials 2011; 12:86; PMID:21429214; http:// dx. doi. org/10. 1186/1745-6215-12-86
36. Berry SM, Broglio KR, Berry DA. Addressing the incremental benefit of histamine dihydrochloride when added to interleukin-2 in treating acute myeloid leukemia: a Bayesian meta-analysis. Cancer Invest 2011; 29:293-9; PMID:21469978; http://dx. doi. org/ 10. 3109/07357907. 2011. 568563
37. Dauguet N, Recher C, Demur C, Fournie JJ, Poupot M, Poupot R. Pre-eminence and persistence of immature natural killer cells in acute myeloid leukemia patients in first complete remission. Am J Hematol 2011; 86:209-13; PMID:21264910; http://dx. doi. org/ 10. 1002/ajh. 21906
38. Lichtenegger FS, Lorenz R, Gellhaus K, Hiddemann W, Beck B, Subklewe M. Impaired NK cells and increased T regulatory cell numbers during cytotoxic maintenance therapy in AML. Leuk Res 2014; 38:964-9; PMID:24957413; http://dx. doi. org/10. 1016/j. leukres. 2014. 05. 014
39. Hallner A, Aurelius J, Thoren FB, Sander FE, Brune M, Hellstrand K, Martner A. Immunotherapy with histamine dihydrochloride and low-dose interleukin-2 favors sustained lymphocyte recovery in acute myeloid leukemia. Eur J Haematol 2015; 94:279-80; PMID:25256820; http://dx. doi. org/10. 1111/ejh. 12454
40. Baer MR, George SL, Caligiuri MA, Sanford BL, Bothun SM, Mrozek K, Kolitz JE, Powell BL, Moore JO, Stone RM et al. Low-dose interleukin-2 immunotherapy does not improve outcome of patients age 60 years and older with acute myeloid leukemia in first complete remission: Cancer and Leukemia Group B Study 9720. J Clin Oncol 2008; 26:4934-9; PMID:18591543; http://dx. doi. org/10. 1200/ JCO. 2008. 17. 0472
41. Blaise D, Attal M, Reiffers J, Michallet M, Bellanger C, Pico JL, Stoppa AM, Payen C, Marit G, Bouabdallah R et al. Randomized study of recombinant interleukin-2 after autologous bone marrow transplantation for acute leukemia in first complete remission. Eur Cytokine Netw 2000; 11:91-8; PMID:10705305
42. Kolitz JE, George SL, Benson DM, Jr., Maharry K, Marcucci G, Vij R, et al. Recombinant interleukin-2 in patients aged younger than 60 years with acute myeloid leukemia in first complete remission: results from Cancer and Leukemia Group B 19808. Cancer 2014; 120:1010-7. PMID:24382782; http:// dx. doi. org/ 10. 1002/cncr. 28516
43. Lange BJ, Smith FO, Feusner J, Barnard DR, Dinndorf P, Feig S, Heerema NA, Arndt C, Arceci RJ, Seibel N et al. Outcomes in CCG-2961, a children's oncology group phase 3 trial for untreated pediatric acute myeloid leukemia: a report from the children's oncology group. Blood 2008; 111:1044-53; PMID:18000167; http://dx. doi. org/10. 1182/blood-2007-04-084293
44. Lotzova E, Savary CA, Herberman RB. Induction of NK cell activity against fresh human leukemia in culture with interleukin 2. J Immunol 1987; 138:2718-27; PMID:3494084
45. Pautas C, Merabet F, Thomas X, Raffoux E, Gardin C, Corm S, Bourhis JH, Reman O, Turlure P, Contentin N et al. Randomized study of intensified anthracycline doses for induction and recombinant interleukin-2 for maintenance in patients with acute myeloid leukemia age 50 to 70 years: results of the ALFA-9801 study. J Clin Oncol 2010; 28:808-14; PMID:20048183; http://dx. doi. org/10. 1200/JCO. 2009. 23. 2652
46. Buchner T, Urbanitz D, Hiddemann W, Ruhl H, Ludwig WD, Fischer J, Aul HC, Vaupel HA, Kuse R, Zeile G. Intensified induction and consolidation with or without maintenance chemotherapy for acute myeloid leukemia (AML): two multicenter studies of the German AML Cooperative Group. J Clin Oncol 1985; 3:1583-9; PMID:3906048
47. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9:162-74; PMID:19197294; http:// dx. doi. org/10. 1038/nri2506
48. Hellstrand K, Hermodsson S. Synergistic activation of human natural killer cell cytotoxicity by histamine and interleukin-2. Int Arch Allergy Appl Immunol 1990; 92:379-89; PMID:2150668; http://dx. doi. org/ 10. 1159/000235169
49. Donskov F, Middleton M, Fode K, Meldgaard P, Mansoor W, Lawrance J, Thatcher N, Nellemann H, von der Maase H. Two randomised phase II trials of subcutaneous interleukin-2 and histamine dihydrochloride in patients with metastatic renal cell carcinoma. Br J Cancer 2005; 93:757-62; PMID:16136045; http://dx. doi. org/10. 1038/sj. bjc. 6602768
50. Agarwala SS, Glaspy J, O'Day SJ, Mitchell M, Gutheil J, Whitman E, Gonzalez R, Hersh E, Feun L, Belt R et al. Results from a randomized phase III study comparing combined treatment with histamine dihydrochloride plus interleukin-2 versus interleukin-2 alone in patients with metastatic melanoma. J Clin Oncol 2002; 20:125-33; PMID:11773161; http://dx. doi. org/ 10. 1200/JCO. 20. 1. 125
51. Dohner H, Estey EH, Amadori S, Appelbaum FR, Buchner T, Burnett AK, Dombret H, Fenaux P, Grimwade D, Larson RA et al. Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European LeukemiaNet. Blood 2010; 115:453-74; PMID:19880497; http://dx. doi. org/10. 1182/blood-2009-07-235358