Harnessing the power of alloreactivity without triggering graft-versus-host disease: How non-engrafting alloreactive cellular therapy might change the landscape of acute myeloid leukemia treatment

Blood Reviews

Volumn 28, Issue 6, 2014, Pages 249-261

  Krakow, Elizabeth F ^a   Bergeron, Julie ^a   Lachance, Silvy ^a   Roy, Denis Claude ^a   Delisle, Jean Sébastien ^a  

^a UNIVERSITY OF MONTREAL   (Canada)

Author keywords

Alloreactivity; Cytokines; Graft vs host disease; Immunotherapy; Natural killer cells; Relapsed acute myeloid leukemia (AML); T cells; Transplantation; Tumor associated antigen

Indexed keywords

CD123 ANTIGEN; CD44V6 ANTIGEN; CYCLOPHOSPHAMIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FLUOROURACIL; GEMCITABINE; GRANULOCYTE COLONY STIMULATING FACTOR; MINOR HISTOCOMPATIBILITY ANTIGEN; PIDILIZUMAB; PROGRAMMED DEATH 1 RECEPTOR; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN;

ACUTE GRANULOCYTIC LEUKEMIA; ADOPTIVE IMMUNOTHERAPY; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; BYSTANDER EFFECT; CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER IMMUNOTHERAPY; CANCER RECURRENCE; CANCER SURVIVAL; CELL COMPOSITION; CELL THERAPY; CYTOKINE RELEASE; CYTOKINE STORM; DONOR LYMPHOCYTE INFUSION; DONOR SELECTION; ENGRAFTMENT; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; HUMAN; NATURAL KILLER CELL; NON ENGRAFTING ALLOREACTIVE CELLULAR THERAPY; OVERALL SURVIVAL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REVIEW; RISK MANAGEMENT; RISK REDUCTION; STEM CELL MOBILIZATION; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TARGET CELL; ALLOTRANSPLANTATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; LEUKEMIA, MYELOID, ACUTE; PROCEDURES;

GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LEUKEMIA, MYELOID, ACUTE; TRANSPLANTATION CONDITIONING; TRANSPLANTATION, HOMOLOGOUS;

EID: 84923834564     PISSN: 0268960X     EISSN: 15321681     Source Type: Journal    
DOI: 10.1016/j.blre.2014.08.002     Document Type: Article

References (159)

1. Mato A.R., Morgans A., Luger S.M. Novel strategies for relapsed and refractory acute myeloid leukemia. Curr Opin Hematol 2008, 15(2):108-114.
2. Guo M., Hu K.X., Yu C.L., Sun Q.Y., Qiao J.H., Wang D.H., et al. Infusion of HLA-mismatched peripheral blood stem cells improves the outcome of chemotherapy for acute myeloid leukemia in elderly patients. Blood 2011, 117(3):936-941.
3. Guo M., Hu K.X., Liu G.X., Yu C.L., Qiao J.H., Sun Q.Y., et al. HLA-mismatched stem-cell microtransplantation as postremission therapy for acute myeloid leukemia: long-term follow-up. J Clin Oncol 2012, 30(33):4084-4090.
4. Reagan J.L., Fast L.D., Winer E.S., Safran H., Butera J.N., Quesenberry P.J. Nonengraftment haploidentical cellular therapy for hematologic malignancies. Adv Hematol 2012, 2012:784213.
5. Forés R., Dorado N., Vilches C., Regidor C., García-Marco J.A., De Pablo R., et al. HLA-partially matched cellular therapy (stem-cell microtransplantation) for acute myeloid leukaemia: description of four cases. Br J Haematol 2014, 165(4):580-581.
6. Kolb H.J. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 2008, 112(12):4371-4383.
7. Kolb H.J., Schmid C., Barrett A.J., Schendel D.J. Graft-versus-leukemia reactions in allogeneic chimeras. Blood 2004, 103(3):767-776.
8. Vincent K., Roy D.C., Perreault C. Next-generation leukemia immunotherapy. Blood 2011, 118(11):2951-2959.
9. Bleakley M., Riddell S.R. Molecules and mechanisms of the graft-versus-leukaemia effect. Nat Rev Cancer 2004, 4(5):371-380.
10. Bleakley M., Riddell S.R. Exploiting T cells specific for human minor histocompatibility antigens for therapy of leukemia. Immunol Cell Biol 2011, 89(3):396-407.
11. D'Orsogna L.J., Roelen D.L., Doxiadis I.I., Claas F.H. TCR cross-reactivity and allorecognition: new insights into the immunogenetics of allorecognition. Immunogenetics 2012, 64(2):77-85.
12. Ruggeri L., Capanni M., Urbani E., Perruccio K., Shlomchik W.D., Tosti A., et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002, 295(5562):2097-2100.
13. Rubnitz J.E., Inaba H., Ribeiro R.C., Pounds S., Rooney B., Bell T., et al. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol 2010, 28(6):955-959.
14. Curti A., Ruggeri L., D'Addio A., Bontadini A., Dan E., Motta M.R., et al. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood 2011, 118(12):3273-3279.
15. Fuchs E.J., Huang X.J., Miller J.S. HLA-haploidentical stem cell transplantation for hematologic malignancies. Biol Blood Marrow Transplant 2010, 16(1 Suppl.):S57-S63.
16. Garderet L., Snell V., Przepiorka D., Schenk T., Lu J.G., Marini F., et al. Effective depletion of alloreactive lymphocytes from peripheral blood mononuclear cell preparations. Transplantation 1999, 67(1):124-130.
17. Bastien J.P., Roy J., Roy D.C. Selective T-cell depletion for haplotype-mismatched allogeneic stem cell transplantation. Semin Oncol 2012, 39(6):674-682.
18. Harris D.T., Schumacher M.J., Locascio J., Besencon F.J., Olson G.B., Deluca D., et al. Phenotypic and functional immaturity of human umbilical cord blood T lymphocytes. Proc Natl Acad Sci U S A 1992, 89(21):10006-10010.
19. Ruggeri L., Mancusi A., Capanni M., Urbani E., Carotti A., Aloisi T., et al. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood 2007, 110(1):433-440.
20. Pende D., Marcenaro S., Falco M., Martini S., Bernardo M.E., Montagna D., et al. 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 redefinition of inhibitory KIR specificity. Blood 2009, 113(13):3119-3129.
21. Cheson B.D., Bennett J.M., Kopecky K.J., Büchner T., Willman C.L., Estey E.H., et al. Revised recommendations of the International Working Group for Diagnosis, Standardization of Response Criteria, Treatment Outcomes, and Reporting Standards for Therapeutic Trials in Acute Myeloid Leukemia. J Clin Oncol 2003, 21(24):4642-4649.
22. Willemze R., Rodrigues C.A., Labopin M., Sanz G., Michel G., Socié G., et al. KIR-ligand incompatibility in the graft-versus-host direction improves outcomes after umbilical cord blood transplantation for acute leukemia. Leukemia 2009, 23(3):492-500.
23. Giebel S., Locatelli F., Lamparelli T., Velardi A., Davies S., Frumento G., et al. Survival advantage with KIR ligand incompatibility in hematopoietic stem cell transplantation from unrelated donors. Blood 2003, 102(3):814-819.
24. Beelen D.W., Ottinger H.D., Ferencik S., Elmaagacli A.H., Peceny R., Trenschel R., et al. 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 2005, 105(6):2594-2600.
25. Farag S.S., Bacigalupo A., Eapen M., Hurley C., Dupont B., Caligiuri M.A., et al. 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. Biol Blood Marrow Transplant 2006, 12(8):876-884.
26. Pende D., Spaggiari G.M., Marcenaro S., Martini S., Rivera P., Capobianco A., 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 2005, 105(5):2066-2073.
27. Nowbakht P., Ionescu M.C., Rohner A., Kalberer C.P., Rossy E., Mori L., et al. 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(9):3615-3622.
28. Salih H.R., Antropius H., Gieseke F., Lutz S.Z., Kanz L., Rammensee H.G., et al. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003, 102(4):1389-1396.
29. Baessler T., Krusch M., Schmiedel B.J., Kloss M., Baltz K.M., Wacker A., et al. Glucocorticoid-induced tumor necrosis factor receptor-related protein ligand subverts immunosurveillance of acute myeloid leukemia in humans. Cancer Res 2009, 69(3):1037-1045.
30. Baessler T., Charton J.E., Schmiedel B.J., Grünebach F., Krusch M., Wacker A., et al. CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK-cell reactivity against human acute myeloid leukemia cells. Blood 2010, 115(15):3058-3069.
31. Coles S.J., Wang E.C., Man S., Hills R.K., Burnett A.K., Tonks A., et al. CD200 expression suppresses natural killer cell function and directly inhibits patient anti-tumor response in acute myeloid leukemia. Leukemia 2011, 25(5):792-799.
32. Lim S.H., Worman C.P., Jewell A., Goldstone A.H. Production of tumour-derived suppressor factor in patients with acute myeloid leukaemia. Leuk Res 1991, 15(4):263-268.
33. Bergmann L., Schui D.K., Brieger J., Weidmann E., Mitrou P.S., Hoelzer D. The inhibition of lymphokine-activated killer cells in acute myeloblastic leukemia is mediated by transforming growth factor-beta 1. Exp Hematol 1995, 23(14):1574-1580.
34. Carli C., Giroux M., Delisle J.S. Roles of transforming growth factor-β in graft-versus-host and graft-versus-tumor effects. Biol Blood Marrow Transplant 2012, 18(9):1329-1340.
35. Trotta R., Dal Col J., Yu J., Ciarlariello D., Thomas B., Zhang X., et al. TGF-beta utilizes SMAD3 to inhibit CD16-mediated IFN-gamma production and antibody-dependent cellular cytotoxicity in human NK cells. J Immunol 2008, 181(6):3784-3792.
36. Fauriat C., Moretta A., Olive D., Costello R.T. Defective killing of dendritic cells by autologous natural killer cells from acute myeloid leukemia patients. Blood 2005, 106(6):2186-2188.
37. Lion E., Willemen Y., Berneman Z.N., Van Tendeloo V.F., Smits E.L. Natural killer cell immune escape in acute myeloid leukemia. Leukemia 2012, 26(9):2019-2026.
38. Narni-Mancinelli E., Ugolini S., Vivier E. Tuning the threshold of natural killer cell responses. Curr Opin Immunol 2013, 25(1):53-58.
39. Yu J., Wei M., Becknell B., Trotta R., Liu S., Boyd Z., et al. Pro- and antiinflammatory cytokine signaling: reciprocal antagonism regulates interferon-gamma production by human natural killer cells. Immunity 2006, 24(5):575-590.
40. Park Y.P., Choi S.C., Kiesler P., Gil-Krzewska A., Borrego F., Weck J., et al. Complex regulation of human NKG2D-DAP10 cell surface expression: opposing roles of the γc cytokines and TGF-β1. Blood 2011, 118(11):3019-3027.
41. Reagan J.L., Fast L.D., Safran H., Nevola M., Winer E.S., Castillo J.J., et al. Cellular immunotherapy for refractory hematological malignancies. J Transl Med 2013, 11:150.
42. Freireich E.J., Levin R.H., Whang J., Carbone P.P., Bronson W., Morse E.E. The function and fate of transfused leukocytes from donors with chronic myelocytic leukemia in leukopenic recipients. Ann N Y Acad Sci 1964, 113:1081-1089.
43. Schwarzenberg L., Mathé G., Amiel J.L., Cattan A., Schneider M., Schlumberger J.R. Study of factors determining the usefulness and complications of leukocyte transfusions. Am J Med 1967, 43(2):206-213.
44. Vallejos C., Mccredie K.B., Bodey G.P., Hester J.P., Freireich E.J. White blood cell transfusions for control of infections in neutropenic patients. Transfusion 1975, 15(1):28-33.
45. Schiffer C.A., Aisner J., Dutcher J.P., Wiernik P.H. Sustained post-transfusion granulocyte count increments following transfusion of leukocytes obtained from donors with chronic myelogenous leukemia. Am J Hematol 1983, 15(1):65-74.
46. Bussel A., Benbunan M., Grange M.J., Boiron M., Bernard J. Comparison of clinical results induced by irradiated and non-irradiated chronic myelocytic leukaemia cell transfusions and the relationship to in vitro studies 1975, 395-401. Academic Press, London; New York.
47. Lowenthal R.M., Grossman L., Goldman J.M., Storring R.A., Buskard N.A., Park D.S., et al. Granulocyte transfusion therapy: a comparison of the use of cells obtained from normal donors with those from patients with chronic granulocytic leukaemia 1975, 363-379. Academic Press, London; New York.
48. O'Donnell P.V., Luznik L., Jones R.J., Vogelsang G.B., Leffell M.S., Phelps M., et al. Nonmyeloablative bone marrow transplantation from partially HLA-mismatched related donors using posttransplantation cyclophosphamide. Biol Blood Marrow Transplant 2002, 8(7):377-386.
49. Spitzer T.R., McAfee S., Sackstein R., Colby C., Toh H.C., Multani P., et al. Intentional induction of mixed chimerism and achievement of antitumor responses after nonmyeloablative conditioning therapy and HLA-matched donor bone marrow transplantation for refractory hematologic malignancies. Biol Blood Marrow Transplant 2000, 6(3A):309-320.
50. Dey B.R., McAfee S., Colby C., Sackstein R., Saidman S., Tarbell N., et al. Impact of prophylactic donor leukocyte infusions on mixed chimerism, graft-versus-host disease, and antitumor response in patients with advanced hematologic malignancies treated with nonmyeloablative conditioning and allogeneic bone marrow transplantation. Biol Blood Marrow Transplant 2003, 9(5):320-329.
51. Dey B.R., McAfee S., Colby C., Cieply K., Caron M., Saidman S., et al. Anti-tumour response despite loss of donor chimaerism in patients treated with non-myeloablative conditioning and allogeneic stem cell transplantation. Br J Haematol 2005, 128(3):351-359.
52. Spitzer T.R., Delmonico F., Tolkoff-Rubin N., McAfee S., Sackstein R., Saidman S., et al. Combined histocompatibility leukocyte antigen-matched donor bone marrow and renal transplantation for multiple myeloma with end stage renal disease: the induction of allograft tolerance through mixed lymphohematopoietic chimerism. Transplantation 1999, 68(4):480-484.
53. Bühler L.H., Spitzer T.R., Sykes M., Sachs D.H., Delmonico F.L., Tolkoff-Rubin N., et al. Induction of kidney allograft tolerance after transient lymphohematopoietic chimerism in patients with multiple myeloma and end-stage renal disease. Transplantation 2002, 74(10):1405-1409.
54. Rubio M.T., Kim Y.M., Sachs T., Mapara M., Zhao G., Sykes M. Antitumor effect of donor marrow graft rejection induced by recipient leukocyte infusions in mixed chimeras prepared with nonmyeloablative conditioning: critical role for recipient-derived IFN-gamma. Blood 2003, 102(6):2300-2307.
55. Strair R.K., Schaar D., Medina D., Todd M.B., Aisner J., Dipaola R.S., et al. Antineoplastic effects of partially HLA-matched irradiated blood mononuclear cells in patients with renal cell carcinoma. J Clin Oncol 2003, 21(20):3785-3791.
56. Mccredie K., Hester J., Dicke K., Freireich E. Blood components in the care of the cancer patient. Current problems in cancer 1978, 3:4-37. Chicago Year Book Medical Publishers, Inc. R.C. Hickey (Ed.).
57. Freireich E.J., Lichtiger B., Mattiuzzi G., Martinez F., Reddy V., Kyle Wathen J. A prospective, randomized, double-blind study, comparing unirradiated to irradiated white blood cell transfusions in acute leukemia patients. Leukemia 2013, 27(4):861-865.
58. Medina D.J., Gharibo M., Savage P., Cohler A., Kuriyan M., Balsara B., et al. A pilot study of allogeneic cellular therapy for patients with advanced hematologic malignancies. Leuk Res 2008, 32(12):1842-1848.
59. Müller S., Schulz A., Reiss U., Schwarz K., Schreiner T., Wiesneth M., et al. Definition of a critical T cell threshold for prevention of GVHD after HLA non-identical PBPC transplantation in children. Bone Marrow Transplant 1999, 24(6):575-581.
60. Colvin G.A., Berz D., Ramanathan M., Winer E.S., Fast L., Elfenbein G.J., et al. Nonengraftment haploidentical cellular immunotherapy for refractory malignancies: tumor responses without chimerism. Biol Blood Marrow Transplant 2009, 15(4):421-431.
61. Slavin S., Ackerstein A., Or R., Shapira M.Y., Gesundheit B., Askenasy N., et al. Immunotherapy in high-risk chemotherapy-resistant patients with metastatic solid tumors and hematological malignancies using intentionally mismatched donor lymphocytes activated with rIL-2: a phase I study. Cancer Immunol Immunother 2010, 59(10):1511-1519.
62. Ballester O.F., Fang T., Raptis A., Ballester G., Wilcox P., Hiemenz J., et al. Adoptive immunotherapy with donor lymphocyte infusions and interleukin-2 after high-dose therapy and autologous stem cell rescue for multiple myeloma. Bone Marrow Transplant 2004, 34(5):419-423.
63. Han Y., Yu J., Cao S., Li H., Ren B., An X., et al. Fetal-maternal microchimerism enhances the survival effect of interleukin-2-activated haploidentical peripheral blood stem cell treatment in patients with advanced solid cancer. Cancer Biother Radiopharm 2010, 25(6):741-746.
64. Yuan L., Sun L., Yang L., Jing Y. Acute graft-versus-host disease in a nonhematopoietic stem cell transplantation candidate treated with decitabine followed by granulocyte colony-stimulating factor-primed peripheral blood stem cells infusion: a special entity of the disease?. Transfusion 2014, 54(1):190-193.
65. Ai H., Hu K., Sun Q., Li X., Guo M., Yu C., et al. Microtransplantation with decitabine and cytarabine improves patient outcomes in myelodysplastic syndromes. ASH Annual Meeting Abstracts 2012, 120:1709.
66. Slavin S. Allogeneic cell-mediated immunotherapy at the stage of minimal residual disease following high-dose chemotherapy supported by autologous stem cell transplantation. Acta Haematol 2005, 114(4):214-220.
67. Miller J.S., Soignier Y., Panoskaltsis-Mortari A., Mcnearney S.A., Yun G.H., Fautsch S.K., et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005, 105(8):3051-3057.
68. Klingemann H., Grodman C., Cutler E., Duque M., Kadidlo D., Klein A.K., et al. Autologous stem cell transplant recipients tolerate haploidentical related-donor natural killer cell-enriched infusions. Transfusion 2013, 53(2):412-418. [quiz 1].
69. Hong-Xia Z., Wan-Jun S., Jie L., Hai-Lan H., Hui-Sheng A. Programmed haploidentical hematopoietic stem cell infusion combined with systemic chemotherapy improves the outcomes of patients with refractory or relapsed lymphoma. Leuk Lymphoma 2014, 10.3109/10428194.2014.914196.
70. Bendall L.J., Kortlepel K., Bradstock K.F., Gottlieb D.J. Natural killer cells adhere to bone marrow fibroblasts and inhibit adhesion of acute myeloid leukemia cells. Leukemia 1995, 9(6):999-1005.
71. Anguille S., Van Tendeloo V.F., Berneman Z.N. Leukemia-associated antigens and their relevance to the immunotherapy of acute myeloid leukemia. Leukemia 2012, 26(10):2186-2196.
72. Lowdell M.W., Craston R., Samuel D., Wood M.E., O'Neill E., Saha V., et al. Evidence that continued remission in patients treated for acute leukaemia is dependent upon autologous natural killer cells. Br J Haematol 2002, 117(4):821-827.
73. Montagna D., Maccario R., Locatelli F., Montini E., Pagani S., Bonetti F., et al. Emergence of antitumor cytolytic T cells is associated with maintenance of hematologic remission in children with acute myeloid leukemia. Blood 2006, 108(12):3843-3850.
74. Rezvani K., Grube M., Brenchley J.M., Sconocchia G., Fujiwara H., Price D.A., et al. Functional leukemia-associated antigen-specific memory CD8+ T cells exist in healthy individuals and in patients with chronic myelogenous leukemia before and after stem cell transplantation. Blood 2003, 102(8):2892-2900.
75. Rezvani K., Brenchley J.M., Price D.A., Kilical Y., Gostick E., Sewell A.K., et al. T-cell responses directed against multiple HLA-A*0201-restricted epitopes derived from Wilms' tumor 1 protein in patients with leukemia and healthy donors: identification, quantification, and characterization. Clin Cancer Res 2005, 11(24 Pt 1):8799-8807.
76. Doubrovina E., Carpenter T., Pankov D., Selvakumar A., Hasan A., O'Reilly R.J. Mapping of novel peptides of WT-1 and presenting HLA alleles that induce epitope-specific HLA-restricted T cells with cytotoxic activity against WT-1(+) leukemias. Blood 2012, 120(8):1633-1646.
77. Rezvani K., Yong A.S., Savani B.N., Mielke S., Keyvanfar K., Gostick E., et al. Graft-versus-leukemia effects associated with detectable Wilms tumor-1 specific T lymphocytes after allogeneic stem-cell transplantation for acute lymphoblastic leukemia. Blood 2007, 110(6):1924-1932.
78. Nishida T., Hudecek M., Kostic A., Bleakley M., Warren E.H., Maloney D., et al. Development of tumor-reactive T cells after nonmyeloablative allogeneic hematopoietic stem cell transplant for chronic lymphocytic leukemia. Clin Cancer Res 2009, 15(14):4759-4768.
79. Yong A.S., Stephens N., Weber G., Li Y., Savani B.N., Eniafe R., et al. Improved outcome following allogeneic stem cell transplantation in chronic myeloid leukemia is associated with higher expression of BMI-1 and immune responses to BMI-1 protein. Leukemia 2011, 25(4):629-637.
80. Tyler E.M., Jungbluth A.A., O'Reilly R.J., Koehne G. WT1-specific T-cell responses in high-risk multiple myeloma patients undergoing allogeneic T cell-depleted hematopoietic stem cell transplantation and donor lymphocyte infusions. Blood 2013, 121(2):308-317.
81. Kapp M., Stevanović S., Fick K., Tan S.M., Loeffler J., Opitz A., et al. CD8+ T-cell responses to tumor-associated antigens correlate with superior relapse-free survival after allo-SCT. Bone Marrow Transplant 2009, 43(5):399-410.
82. Horowitz M.M., Gale R.P., Sondel P.M., Goldman J.M., Kersey J., Kolb H.J., et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood 1990, 75(3):555-562.
83. Van Driessche A., Berneman Z.N., Van Tendeloo V.F. Active specific immunotherapy targeting the Wilms' tumor protein 1 (WT1) for patients with hematological malignancies and solid tumors: lessons from early clinical trials. Oncologist 2012, 17(2):250-259.
84. Maeda T., Hosen N., Fukushima K., Tsuboi A., Morimoto S., Matsui T., et al. Maintenance of complete remission after allogeneic stem cell transplantation in leukemia patients treated with Wilms tumor 1 peptide vaccine. Blood Cancer J 2013, 3:e130.
85. Rezvani K. Posttransplantation vaccination: concepts today and on the horizon. Hematology Am Soc Hematol Educ Program 2011, 2011:299-304.
86. Ballen K.K., Becker P.S., Emmons R.V., Fitzgerald T.J., Hsieh C.C., Liu Q., et al. Low-dose total body irradiation followed by allogeneic lymphocyte infusion may induce remission in patients with refractory hematologic malignancy. Blood 2002, 100(2):442-450.
87. Verneris M.R., Brunstein C.G., Barker J., MacMillan M.L., Defor T., McKenna D.H., et al. Relapse risk after umbilical cord blood transplantation: enhanced graft-versus-leukemia effect in recipients of 2 units. Blood 2009, 114(19):4293-4299.
88. Rocha V., Labopin M., Ruggeri A., Podestà M., Caballero D., Bonifazi F., et al. Outcomes after double unit unrelated cord blood transplantation (UCBT) compared with single UCBT in adults with acute leukemia in remission. A Euorcord and ALWP Collaboration study. Blood (ASH Annual Meeting Abstracts) 2010, 116(21):91. [abstract].
89. Scaradavou A., Brunstein C.G., Eapen M., Le-Rademacher J., Barker J.N., Chao N., et al. Double unit grafts successfully extend the application of umbilical cord blood transplantation in adults with acute leukemia. Blood 2013, 121(5):752-758.
90. Gutman J.A., Turtle C.J., Manley T.J., Heimfeld S., Bernstein I.D., Riddell S.R., et al. Single-unit dominance after double-unit umbilical cord blood transplantation coincides with a specific CD8+ T-cell response against the nonengrafted unit. Blood 2010, 115(4):757-765.
91. Rubio M.T., Saito T.I., Kattleman K., Zhao G., Buchli J., Sykes M. Mechanisms of the antitumor responses and host-versus-graft reactions induced by recipient leukocyte infusions in mixed chimeras prepared with nonmyeloablative conditioning: a critical role for recipient CD4+ T cells and recipient leukocyte infusion-derived IFN-gamma-producing CD8+ T cells. J Immunol 2005, 175(2):665-676.
92. Sakata N., Yasui M., Okamura T., Inoue M., Yumura-Yagi K., Kawa K. Kinetics of plasma cytokines after hematopoietic stem cell transplantation from unrelated donors: the ratio of plasma IL-10/sTNFR level as a potential prognostic marker in severe acute graft-versus-host disease. Bone Marrow Transplant 2001, 27(11):1153-1161.
93. Fujii N., Hiraki A., Aoe K., Murakami T., Ikeda K., Masuda K., et al. Serum cytokine concentrations and acute graft-versus-host disease after allogeneic peripheral blood stem cell transplantation: concurrent measurement of ten cytokines and their respective ratios using cytometric bead array. Int J Mol Med 2006, 17(5):881-885.
94. Visentainer J.E., Lieber S.R., Persoli L.B., Vigorito A.C., Aranha F.J., De Brito Eid K.A., et al. Serum cytokine levels and acute graft-versus-host disease after HLA-identical hematopoietic stem cell transplantation. Exp Hematol 2003, 31(11):1044-1050.
95. Imoto S., Oomoto Y., Murata K., Das H., Murayama T., Kajimoto K., et al. Kinetics of serum cytokines after allogeneic bone marrow transplantation: interleukin-5 as a potential marker of acute graft-versus-host disease. Int J Hematol 2000, 72(1):92-97.
96. Liem L.M., Van Houwelingen H.C., Goulmy E. Serum cytokine levels after HLA-identical bone marrow transplantation. Transplantation 1998, 66(7):863-871.
97. Imamura M., Hashino S., Kobayashi H., Kubayashi S., Hirano S., Minagawa T., et al. Serum cytokine levels in bone marrow transplantation: synergistic interaction of interleukin-6, interferon-gamma, and tumor necrosis factor-alpha in graft-versus-host disease. Bone Marrow Transplant 1994, 13(6):745-751.
98. Weston L.E., Geczy A.F., Briscoe H. Production of IL-10 by alloreactive sibling donor cells and its influence on the development of acute GVHD. Bone Marrow Transplant 2006, 37(2):207-212.
99. Miura Y., Thoburn C.J., Bright E.C., Chen W., Nakao S., Hess A.D. Cytokine and chemokine profiles in autologous graft-versus-host disease (GVHD): interleukin 10 and interferon gamma may be critical mediators for the development of autologous GVHD. Blood 2002, 100(7):2650-2658.
100. Kalos M., Levine B.L., Porter D.L., Katz S., Grupp S.A., Bagg A., et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 2011, 3(95):95ra73.
101. Kochenderfer J.N., Dudley M.E., Feldman S.A., Wilson W.H., Spaner D.E., Maric I., et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 2012, 119(12):2709-2720.
102. Buyse M., Squifflet P., Lange B.J., Alonzo T.A., Larson R.A., Kolitz J.E., et al. Individual patient data meta-analysis of randomized trials evaluating IL-2 monotherapy as remission maintenance therapy in acute myeloid leukemia. Blood 2011, 117(26):7007-7013.
103. Ji S.Q., Chen H.R., Wang H.X., Yan H.M., Pan S.P., Xun C.Q. Comparison of outcome of allogeneic bone marrow transplantation with and without granulocyte colony-stimulating factor (lenograstim) donor-marrow priming in patients with chronic myelogenous leukemia. Biol Blood Marrow Transplant 2002, 8(5):261-267.
104. Giralt S., Escudier S., Kantarjian H., Deisseroth A., Freireich E.J., Andersson B.S., et al. Preliminary results of treatment with filgrastim for relapse of leukemia and myelodysplasia after allogeneic bone marrow transplantation. N Engl J Med 1993, 329(11):757-761.
105. Bishop M.R., Tarantolo S.R., Pavletic Z.S., Lynch J.C., Morris M.E., Zacharias D., et al. Filgrastim as an alternative to donor leukocyte infusion for relapse after allogeneic stem-cell transplantation. J Clin Oncol 2000, 18(11):2269-2272.
106. Riley C.L., Mathieu M.G., Clark R.E., Mcardle S.E., Rees R.C. Tumour antigen-targeted immunotherapy for chronic myeloid leukaemia: is it still viable?. Cancer Immunol Immunother 2009, 58(9):1489-1499.
107. Stone R.M., Berg D.T., George S.L., Dodge R.K., Paciucci P.A., Schulman P., et al. Granulocyte-macrophage colony-stimulating factor after initial chemotherapy for elderly patients with primary acute myelogenous leukemia. Cancer and Leukemia Group B. N Engl J Med 1995, 332(25):1671-1677.
108. Löwenberg B., Van Putten W., Theobald M., Gmür J., Verdonck L., Sonneveld P., et al. Effect of priming with granulocyte colony-stimulating factor on the outcome of chemotherapy for acute myeloid leukemia. N Engl J Med 2003, 349(8):743-752.
109. Schiffer C.A. Hematopoietic growth factors and the future of therapeutic research on acute myeloid leukemia. N Engl J Med 2003, 349(8):727-729.
110. Cutler C., Giri S., Jeyapalan S., Paniagua D., Viswanathan A., Antin J.H. Acute and chronic graft-versus-host disease after allogeneic peripheral-blood stem-cell and bone marrow transplantation: a meta-analysis. J Clin Oncol 2001, 19(16):3685-3691.
111. Morton J., Hutchins C., Durrant S. Granulocyte-colony-stimulating factor (G-CSF)-primed allogeneic bone marrow: significantly less graft-versus-host disease and comparable engraftment to G-CSF-mobilized peripheral blood stem cells. Blood 2001, 98(12):3186-3191.
112. Pulsipher M.A., Chitphakdithai P., Miller J.P., Logan B.R., King R.J., Rizzo J.D., et al. Adverse events among 2408 unrelated donors of peripheral blood stem cells: results of a prospective trial from the National Marrow Donor Program. Blood 2009, 113(15):3604-3611.
113. Zitvogel L., Kepp O., Kroemer G. Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 2011, 8(3):151-160.
114. Galluzzi L., Senovilla L., Zitvogel L., Kroemer G. The secret ally: immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012, 11(3):215-233.
115. Ghiringhelli F., Menard C., Puig P.E., Ladoire S., Roux S., Martin F., et al. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007, 56(5):641-648.
116. Vincent J., Mignot G., Chalmin F., Ladoire S., Bruchard M., Chevriaux A., et al. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010, 70(8):3052-3061.
117. Kroemer G., Galluzzi L., Kepp O., Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013, 31:51-72.
118. Almstedt M., Blagitko-Dorfs N., Duque-Afonso J., Karbach J., Pfeifer D., Jäger E., et al. The DNA demethylating agent 5-aza-2'-deoxycytidine induces expression of NY-ESO-1 and other cancer/testis antigens in myeloid leukemia cells. Leuk Res 2010, 34(7):899-905.
119. Goodyear O., Agathanggelou A., Novitzky-Basso I., Siddique S., Mcskeane T., Ryan G., et al. Induction of a CD8+ T-cell response to the MAGE cancer testis antigen by combined treatment with azacitidine and sodium valproate in patients with acute myeloid leukemia and myelodysplasia. Blood 2010, 116(11):1908-1918.
120. Lal G., Zhang N., Van Der Touw W., Ding Y., Ju W., Bottinger E.P., et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 2009, 182(1):259-273.
121. Polansky J.K., Kretschmer K., Freyer J., Floess S., Garbe A., Baron U., et al. DNA methylation controls Foxp3 gene expression. Eur J Immunol 2008, 38(6):1654-1663.
122. Schroeder T., Fröbel J., Cadeddu R.P., Czibere A., Dienst A., Platzbecker U., et al. Salvage therapy with azacitidine increases regulatory T cells in peripheral blood of patients with AML or MDS and early relapse after allogeneic blood stem cell transplantation. Leukemia 2013, 27(9):1910-1913.
123. Goodyear O.C., Dennis M., Jilani N.Y., Loke J., Siddique S., Ryan G., et al. Azacitidine augments expansion of regulatory T cells after allogeneic stem cell transplantation in patients with acute myeloid leukemia (AML). Blood 2012, 119(14):3361-3369.
124. Schroeder T., Czibere A., Platzbecker U., Bug G., Uharek L., Luft T., et al. Azacitidine and donor lymphocyte infusions as first salvage therapy for relapse of AML or MDS after allogeneic stem cell transplantation. Leukemia 2013, 27(6):1229-1235.
125. Czibere A., Bruns I., Kröger N., Platzbecker U., Lind J., Zohren F., et al. 5-Azacytidine for the treatment of patients with acute myeloid leukemia or myelodysplastic syndrome who relapse after allo-SCT: a retrospective analysis. Bone Marrow Transplant 2010, 45(5):872-876.
126. Lübbert M., Bertz H., Wäsch R., Marks R., Rüter B., Claus R., et al. Efficacy of a 3-day, low-dose treatment with 5-azacytidine followed by donor lymphocyte infusions in older patients with acute myeloid leukemia or chronic myelomonocytic leukemia relapsed after allografting. Bone Marrow Transplant 2010, 45(4):627-632.
127. Fredly H., Ersvær E., Gjertsen B.T., Bruserud O. Immunogenic apoptosis in human acute myeloid leukemia (AML): primary human AML cells expose calreticulin and release heat shock protein (HSP) 70 and HSP90 during apoptosis. Oncol Rep 2011, 25(6):1549-1556.
128. Fredly H., Gjertsen B.T., Bruserud O. Histone deacetylase inhibition in the treatment of acute myeloid leukemia: the effects of valproic acid on leukemic cells, and the clinical and experimental evidence for combining valproic acid with other antileukemic agents. Clin Epigenetics 2013, 5(1):12.
129. Spear P., Wu M.R., Sentman M.L., Sentman C.L. NKG2D ligands as therapeutic targets. Cancer Immun 2013, 13:8.
130. Eljaafari A., Van Snick J., Voisin A., Cormont F., Farre A., Bienvenu J., et al. Alloreaction increases or restores CD40, CD54, and/or HLA molecule expression in acute myelogenous leukemia blasts, through secretion of inflammatory cytokines: Dominant role for TNFbeta, in concert with IFNgamma. Leukemia 2006, 20(11):1992-2001.
131. Rezvani K., Barrett A.J. Characterizing and optimizing immune responses to leukaemia antigens after allogeneic stem cell transplantation. Best Pract Res Clin Haematol 2008, 21(3):437-453.
132. Rezvani K., Yong A.S., Mielke S., Savani B.N., Jafarpour B., Eniafe R., et al. Lymphodepletion is permissive to the development of spontaneous T-cell responses to the self-antigen PR1 early after allogeneic stem cell transplantation and in patients with acute myeloid leukemia undergoing WT1 peptide vaccination following chemotherapy. Cancer Immunol Immunother 2012, 61(7):1125-1136.
133. Pardoll D., Drake C. Immunotherapy earns its spot in the ranks of cancer therapy. J Exp Med 2012, 209(2):201-209.
134. Norde W.J., Hobo W., Van Der Voort R., Dolstra H. Coinhibitory molecules in hematologic malignancies: targets for therapeutic intervention. Blood 2012, 120(4):728-736.
135. Thumar J.R., Kluger H.M. Ipilimumab: a promising immunotherapy for melanoma. Oncology (Williston Park) 2010, 24(14):1280-1288.
136. Calabrò L., Danielli R., Sigalotti L., Maio M. Clinical studies with anti-CTLA-4 antibodies in non-melanoma indications. Semin Oncol 2010, 37(5):460-467.
137. Pérez-García A., Brunet S., Berlanga J.J., Tormo M., Nomdedeu J., Guardia R., et al. CTLA-4 genotype and relapse incidence in patients with acute myeloid leukemia in first complete remission after induction chemotherapy. Leukemia 2009, 23(3):486-491.
138. Labelle J.L., Hanke C.A., Blazar B.R., Truitt R.L. Negative effect of CTLA-4 on induction of T-cell immunity in vivo to B7-1+, but not B7-2+, murine myelogenous leukemia. Blood 2002, 99(6):2146-2153.
139. Pistillo M.P., Tazzari P.L., Palmisano G.L., Pierri I., Bolognesi A., Ferlito F., et al. CTLA-4 is not restricted to the lymphoid cell lineage and can function as a target molecule for apoptosis induction of leukemic cells. Blood 2003, 101(1):202-209.
140. Bashey A., Medina B., Corringham S., Pasek M., Carrier E., Vrooman L., et al. CTLA4 blockade with ipilimumab to treat relapse of malignancy after allogeneic hematopoietic cell transplantation. Blood 2009, 113(7):1581-1588.
141. Chen X., Liu S., Wang L., Zhang W., Ji Y., Ma X. Clinical significance of B7-H1 (PD-L1) expression in human acute leukemia. Cancer Biol Ther 2008, 7(5):622-627.
142. Saudemont A., Quesnel B. In a model of tumor dormancy, long-term persistent leukemic cells have increased B7-H1 and B7.1 expression and resist CTL-mediated lysis. Blood 2004, 104(7):2124-2133.
143. Norde W.J., Maas F., Hobo W., Korman A., Quigley M., Kester M.G., et al. PD-1/PD-L1 interactions contribute to functional T-cell impairment in patients who relapse with cancer after allogeneic stem cell transplantation. Cancer Res 2011, 71(15):5111-5122.
144. Zhang L., Gajewski T.F., Kline J. PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 2009, 114(8):1545-1552.
145. Zhou Q., Munger M.E., Highfill S.L., Tolar J., Weigel B.J., Riddle M., et al. Program death-1 signaling and regulatory T cells collaborate to resist the function of adoptively transferred cytotoxic T lymphocytes in advanced acute myeloid leukemia. Blood 2010, 116(14):2484-2493.
146. Berger R., Rotem-Yehudar R., Slama G., Landes S., Kneller A., Leiba M., et al. Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res 2008, 14(10):3044-3051.
147. Tettamanti S., Marin V., Pizzitola I., Magnani C.F., Giordano Attianese G.M., Cribioli E., et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br J Haematol 2013, 161(3):389-401.
148. Gill S., Tasian S.K., Ruella M., Shestova O., Li Y., Porter D.L., et al. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 2014, 123(15):2343-2354.
149. Mardiros A., Dos Santos C., McDonald T., Brown C.E., Wang X., Budde L.E., et al. T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia. Blood 2013, 122(18):3138-3148.
150. Marin V., Pizzitola I., Agostoni V., Attianese G.M., Finney H., Lawson A., et al. Cytokine-induced killer cells for cell therapy of acute myeloid leukemia: improvement of their immune activity by expression of CD33-specific chimeric receptors. Haematologica 2010, 95(12):2144-2152.
151. Casucci M., Nicolis Di Robilant B., Falcone L., Camisa B., Norelli M., Genovese P., et al. CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood 2013, 122(20):3461-3472.
152. Peinert S., Prince H.M., Guru P.M., Kershaw M.H., Smyth M.J., Trapani J.A., et al. Gene-modified T cells as immunotherapy for multiple myeloma and acute myeloid leukemia expressing the Lewis Y antigen. Gene Ther 2010, 17(5):678-686.
153. Ritchie D.S., Neeson P.J., Khot A., Peinert S., Tai T., Tainton K., et al. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol Ther 2013, 21(11):2122-2129.
154. Chaise C., Buchan S.L., Rice J., Marquet J., Rouard H., Kuentz M., et al. DNA vaccination induces WT1-specific T-cell responses with potential clinical relevance. Blood 2008, 112(7):2956-2964.
155. Chapuis A.G., Ragnarsson G.B., Nguyen H.N., Chaney C.N., Pufnock J.S., Schmitt T.M., et al. Transferred WT1-recactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci Trans Med 2013, 5(174):174ra27. http://dx.doi.org/10.1126/scitranslmed.3004916.
156. Weber G., Gerdemann U., Caruana I., Savoldo B., Hensel N.F., Rabin K.R., et al. Generation of multi-leukemia antigen-specific T cells to enhance the graft-versus-leukemia effect after allogeneic stem cell transplant. Leukemia 2013, 27(7):1538-1547.
157. Patriarca F., Luznik L., Medeot M., Zecca M., Bacigalupo A., Di Bartolomeo P., et al. Experts' considerations on HLA-haploidentical stem cell transplantation. Eur J Haematol 2014, 93(3):187-197.
158. Van Rood J.J., Scaradavou A., Stevens C.E. Indirect evidence that maternal microchimerism in cord blood mediates a graft-versus-leukemia effect in cord blood transplantation. Proc Natl Acad Sci U S A 2012, 109(7):2509-2514.
159. Baron C., Somogyi R., Greller L.D., Rineau V., Wilkinson P., Cho C.R., et al. Prediction of graft-versus-host disease in humans by donor gene-expression profiling. PLoS Med 2007, 4(1):e23.