NCI First International Workshop on The Biology, Prevention, and Treatment of Relapse After Allogeneic Hematopoietic Stem Cell Transplantation: Report from the Committee on the Biology Underlying Recurrence of Malignant Disease following Allogeneic HSCT: Graft-versus-Tumor/Leukemia Reaction

Biology of Blood and Marrow Transplantation

Volumn 16, Issue 5, 2010, Pages 565-586

  Miller, Jeffrey S ^a   Warren, Edus H ^b   van den Brink, Marcel R M ^c   Ritz, Jerome ^d   Shlomchik, Warren D ^e   Murphy, William J ^f   Barrett, A John ^g   Kolb, Hans Jochem ^h   Giralt, Sergio ⁱ   Bishop, Michael R ^j   Blazar, Bruce R ^a   Falkenburg, J H Frederik ^k  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d DANA FARBER CANCER INSTITUTE   (United States)

^e YALE CANCER CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^h UNIVERSITY OF MUNICH   (Germany)

ⁱ UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^j NATIONAL CANCER INSTITUTE   (United States)

^k LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

more..

Author keywords

Graft versus host disease; Graft versus leukemia reaction; HCT; Immune modulation; Relapse

Indexed keywords

HLA DP ANTIGEN; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 7; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LYMPHOCYTE ANTIBODY; MINOR HISTOCOMPATIBILITY ANTIGEN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; B LYMPHOCYTE; CANCER IMMUNOTHERAPY; CANCER RECURRENCE; CANCER RELAPSE; CYTOLYSIS; DISEASE FREE SURVIVAL; DRUG MEGADOSE; GENETIC VARIABILITY; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; IMMUNE DEFICIENCY; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; LOW DRUG DOSE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; MEMORY T LYMPHOCYTE; MICROENVIRONMENT; MOLECULAR BIOLOGY; NATURAL KILLER CELL; NONHUMAN; REVIEW; T LYMPHOCYTE ACTIVATION; WORKSHOP;

ANTIGEN PRESENTATION; B-LYMPHOCYTES; EDUCATION; GRAFT VS LEUKEMIA EFFECT; HEMATOLOGIC NEOPLASMS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; KILLER CELLS, NATURAL; NATIONAL CANCER INSTITUTE (U.S.); RECURRENCE; T-LYMPHOCYTES; TRANSPLANTATION, HOMOLOGOUS; UNITED STATES;

EID: 77951149575     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2010.02.005     Document Type: Review

References (183)

1. Sallusto F., Geginat J., Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004, 22:745-763.
2. Hand T.W., Kaech S.M. Intrinsic and extrinsic control of effector T cell survival and memory T cell development. Immunol Res 2009, 45:46-61.
3. Chen B.J., Cui X., Sempowski G.D., Liu C., Chao N.J. Transfer of allogeneic CD62L- memory T cells without graft-versus-host disease. Blood 2004, 103:1534-1541.
4. + T cells mediate graft-versus-leukemia without inducing graft-versus-host disease. Blood 2008, 111:2476-2484.
5. Zheng H., Matte-Martone C., Jain D., McNiff J., Shlomchik W.D. Central memory CD8+ T cells induce graft-versus-host disease and mediate graft-versus-leukemia. J Immunol 2009, 182:5938-5948.
6. Klebanoff C.A., Gattinoni L., Torabi-Parizi P., et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 2005, 102:9571-9576.
7. Berger C., Jensen M.C., Lansdorp P.M., Gough M., Elliott C., Riddell S.R. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 2008, 118:294-305.
8. Hinrichs C.S., Borman Z.A., Cassard L., et al. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci USA 2009, 106:17469-17474.
9. Shlomchik W.D., Matte-Martone C., Gilliland D.G., Chen L.P. Mechanisms of GVL against a murine blast crisis CML. Blood 2006, 108:60A-61A.
10. Matte C.C., Cormier J., Anderson B.E., et al. Graft-versus-leukemia in a retrovirally induced murine CML model: mechanisms of T-cell killing. Blood 2004, 103:4353-4361.
11. Matte-Martone C., Liu J., Jain D., McNiff J., Shlomchik W.D. CD8+ but not CD4+ T cells require cognate interactions with target tissues to mediate GVHD across only minor H antigens, whereas both CD4+ and CD8+ T cells require direct leukemic contact to mediate GVL. Blood 2008, 111:3884-3892.
12. Reddy P., Maeda Y., Liu C., Krijanovski O.I., Korngold R., Ferrara J.L. A crucial role for antigen-presenting cells and alloantigen expression in graft-versus-leukemia responses. Nat Med 2005, 11:1244-1249.
13. Kaech S.M., Wherry E.J. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 2007, 27:393-405.
14. Choi E.Y., Christianson G.J., Yoshimura Y., et al. Real-time T-cell profiling identifies H60 as a major minor histocompatibility antigen in murine graft-versus-host disease. Blood 2002, 100:4259-4265.
15. Shlomchik W.D. Graft-versus-host disease. Nat Rev Immunol 2007, 7:340-352.
16. Jones S.C., Murphy G.F., Friedman T.M., Korngold R. Importance of minor histocompatibility antigen expression by nonhematopoietic tissues in a CD4+ T cell-mediated graft-versus-host disease model. J Clin Invest 2003, 112:1880-1886.
17. Anderson B.E., McNiff J.M., Jain D., Blazar B.R., Shlomchik W.D., Shlomchik M.J. Distinct roles for donor- and host-derived antigen-presenting cells and costimulatory molecules in murine chronic graft-versus-host disease: requirements depend on target organ. Blood 2005, 105:2227-2234.
18. Meunier M.C., Roy-Proulx G., Labrecque N., Perreault C. Tissue distribution of target antigen has a decisive influence on the outcome of adoptive cancer immunotherapy. Blood 2003, 101:766-770.
19. Blackburn S.D., Shin H., Haining W.N., et al. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009, 10:29-37.
20. Barber D.L., Wherry E.J., Masopust D., et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006, 439:682-687.
21. Le Bon A., Etchart N., Rossmann C., et al. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 2003, 4:1009-1015.
22. Kurts C., Carbone F.R., Barnden M., et al. CD4+ T cell help impairs CD8+ T cell deletion induced by cross-presentation of self-antigens and favors autoimmunity. J Exp Med 1997, 186:2057-2062.
23. Kuchtey J., Chefalo P.J., Gray R.C., Ramachandra L., Harding C.V. Enhancement of dendritic cell antigen cross-presentation by CpG DNA involves type I IFN and stabilization of class I MHC mRNA. J Immunol 2005, 175:2244-2251.
24. Ackerman A.L., Cresswell P. Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol 2004, 5:678-684.
25. Heath W.R., Belz G.T., Behrens G.M., et al. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev 2004, 199:9-26.
26. Schulz O., Diebold S.S., Chen M., et al. Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005, 433:887-892.
27. Yu X.Z., Bidwell S.J., Martin P.J., Anasetti C. CD28-specific antibody prevents graft-versus-host disease in mice. J Immunol 2000, 164:4564-4568.
28. Nurieva R.I., Mai X.M., Forbush K., Bevan M.J., Dong C. B7h is required for T cell activation, differentiation, and effector function. Proc Natl Acad Sci USA 2003, 100:14163-14168.
29. Dong C., Juedes A.E., Temann U.A., et al. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 2001, 409:97-101.
30. Hubbard V.M., Eng J.M., Ramirez-Montagut T., et al. Absence of inducible costimulator on alloreactive T cells reduces graft versus host disease and induces Th2 deviation. Blood 2005, 106:3285-3292.
31. Taylor P.A., Panoskaltsis-Mortari A., Freeman G.J., et al. Targeting of inducible costimulator (ICOS) expressed on alloreactive T cells down-regulates graft-versus-host disease (GVHD) and facilitates engraftment of allogeneic bone marrow (BM). Blood 2005, 105:3372-3380.
32. Raimondi G., Shufesky W.J., Tokita D., Morelli A.E., Thomson A.W. Regulated compartmentalization of programmed cell death-1 discriminates CD4+CD25+ resting regulatory T cells from activated T cells. J Immunol 2006, 176:2808-2816.
33. Yu X.Z., Liang Y., Nurieva R.I., Guo F., Anasetti C., Dong C. Opposing effects of ICOS on graft-versus-host disease mediated by CD4 and CD8 T cells. J Immunol 2006, 176:7394-7401.
34. Blazar B.R., Carreno B.M., Panoskaltsis-Mortari A., et al. Blockade of programmed death-1 engagement accelerates graft-versus-host disease lethality by an IFN-gamma-dependent mechanism. J Immunol 2003, 171:1272-1277.
35. Blazar B.R., Sharpe A.H., Chen A.I., et al. Ligation of OX40 (CD134) regulates graft-versus-host disease (GVHD) and graft rejection in allogeneic bone marrow transplant recipients. Blood 2003, 101:3741-3748.
36. Blazar B.R., Taylor P.A., Panoskaltsis-Mortari A., et al. Blockade of CD40 ligand-CD40 interaction impairs CD4+ T cell-mediated alloreactivity by inhibiting mature donor T cell expansion and function after bone marrow transplantation. J Immunol 1997, 158:29-39.
37. Buhlmann J.E., Gonzalez M., Ginther B., et al. Cutting edge: sustained expansion of CD8+ T cells requires CD154 expression by Th cells in acute graft versus host disease. J Immunol 1999, 162:4373-4376.
38. Saito K., Sakurai J., Ohata J., et al. Involvement of CD40 ligand-CD40 and CTLA4-B7 pathways in murine acute graft-versus-host disease induced by allogeneic T cells lacking CD28. J Immunol 1998, 160:4225-4231.
39. Taylor P.A., Lees C., Noelle R., et al. Superior GVHD prevention by combined costimulatory blockade: comparison of single and combined pathway blockade of CD28/CTLA4:B7, CD40L: CD40 and OX40:OX40L pathways. Blood 2002, 100:A818-A819.
40. Kwon B.S., Weissman S.M. cDNA sequences of two inducible T-cell genes. Proc Natl Acad Sci USA 1989, 86:1963-1967.
41. Melero I., Johnston J.V., Shufford W.W., Mittler R.S., Chen L. NK1.1 cells express 4-1BB (CDw137) costimulatory molecule and are required for tumor immunity elicited by anti-4-1BB monoclonal antibodies. Cell Immunol 1998, 190:167-172.
42. Nozawa K., Ohata J., Sakurai J., et al. Preferential blockade of CD8(+) T cell responses by administration of anti-CD137 ligand monoclonal antibody results in differential effect on development of murine acute and chronic graft-versus-host diseases. J Immunol 2001, 167:4981-4986.
43. Blazar B.R., Kwon B.S., Panoskaltsis-Mortari A., Kwak K.B., Peschon J.J., Taylor P.A. Ligation of 4-1BB (CDw137) regulates graft-versus-host disease, graft-versus-leukemia, and graft rejection in allogeneic bone marrow transplant recipients. J Immunol 2001, 166:3174-3183.
44. Shimizu J., Yamazaki S., Takahashi T., Ishida Y., Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002, 3:135-142.
45. Muriglan S.J., Ramirez-Montagut T., Alpdogan O., et al. GITR activation induces an opposite effect on alloreactive CD4(+) and CD8(+) T cells in graft-versus-host disease. J Exp Med 2004, 200:149-157.
46. Curtsinger J.M., Lins D.C., Mescher M.F. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med 2003, 197:1141-1151.
47. Valenzuela J.O., Hammerbeck C.D., Mescher M.F. Cutting edge: Bcl-3 up-regulation by signal 3 cytokine (IL-12) prolongs survival of antigen-activated CD8 T cells. J Immunol 2005, 174:600-604.
48. Curtsinger J.M., Lins D.C., Johnson C.M., Mescher M.F. Signal 3 tolerant CD8 T cells degranulate in response to antigen but lack granzyme B to mediate cytolysis. J Immunol 2005, 175:4392-4399.
49. Curtsinger J.M., Gerner M.Y., Lins D.C., Mescher M.F. Signal 3 availability limits the CD8 T cell response to a solid tumor. J Immunol 2007, 178:6752-6760.
50. Wysocki C.A., Panoskaltsis-Mortari A., Blazar B.R., Serody J.S. Leukocyte migration and graft-versus-host disease. Blood 2005, 105:4191-4199.
51. Sims T.N., Dustin M.L. The immunological synapse: integrins take the stage. Immunol Rev 2002, 186:100-117.
52. Gunn M.D., Tangemann K., Tam C., Cyster J.G., Rosen S.D., Williams L.T. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc Natl Acad Sci USA 1998, 95:258-263.
53. Potsch C., Vohringer D., Pircher H. Distinct migration patterns of naive and effector CD8 T cells in the spleen: correlation with CCR7 receptor expression and chemokine reactivity. Eur J Immunol 1999, 29:3562-3570.
54. Terwey T.H., Kim T.D., Kochman A.A., et al. CCR2 is required for CD8-induced graft-versus-host disease. Blood 2005, 106:3322-3330.
55. Petrovic A., Alpdogan O., Willis L.M., et al. LPAM (alpha 4 beta 7 integrin) is an important homing integrin on alloreactive T cells in the development of intestinal graft-versus-host disease. Blood 2004, 103:1542-1547.
56. Waldman E., Lu S.X., Hubbard V.M., et al. Absence of beta7 integrin results in less graft-versus-host disease because of decreased homing of alloreactive T cells to intestine. Blood 2006, 107:1703-1711.
57. Feagan B.G., Greenberg G.R., Wild G., et al. Treatment of ulcerative colitis with a humanized antibody to the alpha4beta7 integrin. N Engl J Med 2005, 352:2499-2507.
58. Rudick R.A., Stuart W.H., Calabresi P.A., et al. Natalizumab plus interferon beta-1a for relapsing multiple sclerosis. N Engl J Med 2006, 354:911-923.
59. Polman C.H., O'Connor P.W., Havrdova E., et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. N Engl J Med 2006, 354:899-910.
60. Hyams J.S., Wilson D.C., Thomas A., et al. Natalizumab therapy for moderate to severe Crohn disease in adolescents. J Pediatr Gastroenterol Nutr 2007, 44:185-191.
61. Sands B.E., Kozarek R., Spainhour J., et al. Safety and tolerability of concurrent natalizumab treatment for patients with Crohn's disease not in remission while receiving infliximab. Inflamm Bowel Dis 2007, 13:2-11.
62. Hamann A., Andrew D.P., Jablonski-Westrich D., Holzmann B., Butcher E.C. Role of alpha 4-integrins in lymphocyte homing to mucosal tissues in vivo. J Immunol 1994, 152:3282-3293.
63. van den Brink M.R., Burakoff S.J. Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol 2002, 2:273-281.
64. Otten H.G., van Ginkel W.G., Hagenbeek A., Petersen E.J. Prevalence and clinical significance of resistance to perforin- and FAS-mediated cell death in leukemia. Leukemia 2004, 18:1401-1405.
65. Hsieh M.H., Korngold R. Differential use of FasL- and perforin-mediated cytolytic mechanisms by T-cell subsets involved in graft-versus-myeloid leukemia responses. Blood 2000, 96:1047-1055.
66. Baker M.B., Altman N.H., Podack E.R., Levy R.B. The role of cell-mediated cytotoxicity in acute GVHD after MHC-matched allogeneic bone marrow transplantation in mice. J Exp Med 1996, 183:2645-2656.
67. Hill G.R., Teshima T., Gerbitz A., et al. Differential roles of IL-1 and TNF-alpha on graft-versus-host disease and graft versus leukemia. J Clin Invest 1999, 104:459-467.
68. Slager E.H., Honders M.W., van der Meijden E.D., et al. Identification of the angiogenic endothelial-cell growth factor-1/thymidine phosphorylase as a potential target for immunotherapy of cancer. Blood 2006, 107:4954-4960.
69. van Bergen C.A., Kester M.G., Jedema I., et al. Multiple myeloma-reactive T cells recognize an activation-induced minor histocompatibility antigen encoded by the ATP-dependent interferon-responsive (ADIR) gene. Blood 2007, 109:4089-4096.
70. Kawase T., Akatsuka Y., Torikai H., et al. Alternative splicing due to an intronic SNP in HMSD generates a novel minor histocompatibility antigen. Blood 2007, 110:1055-1063.
71. de Rijke B., van Horssen-Zoetbrood A., Beekman J.M., et al. A frameshift polymorphism in P2X5 elicits an allogeneic cytotoxic T lymphocyte response associated with remission of chronic myeloid leukemia. J Clin Invest 2005, 115:3506-3516.
72. Murata M., Warren E.H., Riddell S.R. A human minor histocompatibility antigen resulting from differential expression due to a gene deletion. J Exp Med 2003, 197:1279-1289.
73. Terakura S., Murata M., Warren E.H., et al. A single minor histocompatibility antigen encoded by UGT2B17 and presented by human leukocyte antigen-A*2902 and -B*4403. Transplantation 2007, 83:1242-1248.
74. Kamei M., Nannya Y., Torikai H., et al. HapMap scanning of novel human minor histocompatibility antigens. Blood 2009, 113:5041-5048.
75. Vogt M.H., van den Muijsenberg J.W., Goulmy E., et al. The DBY gene codes for an HLA-DQ5-restricted human male-specific minor histocompatibility antigen involved in graft-versus-host disease. Blood 2002, 99:3027-3032.
76. Griffioen M., van der Meijden E.D., Slager E.H., et al. Identification of phosphatidylinositol 4-kinase type II beta as HLA class II-restricted target in graft versus leukemia reactivity. Proc Natl Acad Sci USA 2008, 105:3837-3842.
77. Stumpf A.N., van der Meijden E.D., van Bergen C.A., Willemze R., Falkenburg J.H., Griffioen M. Identification of 4 new HLA-DR-restricted minor histocompatibility antigens as hematopoietic targets in antitumor immunity. Blood 2009, 114:3684-3692.
78. Falkenburg J.H., Goselink H.M., van der Harst D., et al. Growth inhibition of clonogenic leukemic precursor cells by minor histocompatibility antigen-specific cytotoxic T lymphocytes. J Exp Med 1991, 174:27-33.
79. Faber L.M., van der Hoeven J., Goulmy E., et al. Recognition of clonogenic leukemic cells, remission bone marrow and HLA-identical donor bone marrow by CD8+ or CD4+ minor histocompatibility antigen-specific cytotoxic T lymphocytes. J Clin Invest 1995, 96:877-883.
80. Lapidot T., Sirard C., Vormoor J., et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
81. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997, 3:730-737.
82. Bonnet D., Warren E.H., Greenberg P.D., Dick J.E., Riddell S.R. CD8(+) minor histocompatibility antigen-specific cytotoxic T lymphocyte clones eliminate human acute myeloid leukemia stem cells. Proc Natl Acad Sci USA 1999, 96:8639-8644.
83. Rosinski K.V., Fujii N., Mito J.K., et al. DDX3Y encodes a class I MHC-restricted H-Y antigen that is expressed in leukemic stem cells. Blood 2008, 111:4817-4826.
84. Hambach L., Nijmeijer B.A., Aghai Z., et al. Human cytotoxic T lymphocytes specific for a single minor histocompatibility antigen HA-1 are effective against human lymphoblastic leukaemia in NOD/scid mice. Leukemia 2006, 20:371-374.
85. Marijt W.A., Heemskerk M.H., Kloosterboer F.M., et al. Hematopoiesis-restricted minor histocompatibility antigens HA-1- or HA-2-specific T cells can induce complete remissions of relapsed leukemia. Proc Natl Acad Sci USA 2003, 100:2742-2747.
86. Takami A., Sugimori C., Feng X., et al. Expansion and activation of minor histocompatibility antigen HY-specific T cells associated with graft-versus-leukemia response. Bone Marrow Transplant 2004, 34:703-709.
87. Claret E.J., Alyea E.P., Orsini E., et al. Characterization of T cell repertoire in patients with graft-versus-leukemia after donor lymphocyte infusion. J Clin Invest 1997, 100:855-866.
88. Zorn E., Wang K.S., Hochberg E.P., et al. Infusion of CD4+ donor lymphocytes induces the expansion of CD8+ donor T cells with cytolytic activity directed against recipient hematopoietic cells. Clin Cancer Res 2002, 8:2052-2060.
89. Kloosterboer F.M., van Luxemburg-Heijs S.A., van Soest R.A., et al. Minor histocompatibility antigen-specific T cells with multiple distinct specificities can be isolated by direct cloning of IFNgamma-secreting T cells from patients with relapsed leukemia responding to donor lymphocyte infusion. Leukemia 2005, 19:83-90.
90. Nishida T., Hudecek M., Kostic A., et al. Development of tumor-reactive T cells after nonmyeloablative allogeneic hematopoietic stem cell transplant for chronic lymphocytic leukemia. Clin Cancer Res 2009, 15:4759-4768.
91. Randolph S.S., Gooley T.A., Warren E.H., Appelbaum F.R., Riddell S.R. Female donors contribute to a selective graft-versus-leukemia effect in male recipients of HLA-matched, related hematopoietic stem cell transplants. Blood 2004, 103:347-352.
92. Stern M., Brand R., de Witte T., et al. Female-versus-male alloreactivity as a model for minor histocompatibility antigens in hematopoietic stem cell transplantation. Am J Transplant 2008, 8:2149-2157.
93. Molldrem J.J., Lee P.P., Wang C., et al. Evidence that specific T lymphocytes may participate in the elimination of chronic myelogenous leukemia. Nat Med 2000, 6:1018-1023.
94. Rezvani K., Grube M., Brenchley J.M., 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, 102:2892-2900.
95. Molldrem J., Dermime S., Parker K., et al. Targeted T-cell therapy for human leukemia: cytotoxic T lymphocytes specific for a peptide derived from proteinase 3 preferentially lyse human myeloid leukemia cells. Blood 1996, 88:2450-2457.
96. Molldrem J.J., Clave E., Jiang Y.Z., et al. Cytotoxic T lymphocytes specific for a nonpolymorphic proteinase 3 peptide preferentially inhibit chronic myeloid leukemia colony-forming units. Blood 1997, 90:2529-2534.
97. Rezvani K., Yong A.S., Savani B.N., 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, 110:1924-1932.
98. Orsini E., Bellucci R., Alyea E.P., et al. Expansion of tumor-specific CD8+ T cell clones in patients with relapsed myeloma after donor lymphocyte infusion. Cancer Res 2003, 63:2561-2568.
99. Atanackovic D., Arfsten J., Cao Y., et al. Cancer-testis antigens are commonly expressed in multiple myeloma and induce systemic immunity following allogeneic stem cell transplantation. Blood 2007, 109:1103-1112.
100. Hoogendoorn M., Jedema I., Barge R.M., et al. Characterization of graft-versus-leukemia responses in patients treated for advanced chronic lymphocytic leukemia with donor lymphocyte infusions after in vitro T-cell depleted allogeneic stem cell transplantation following reduced-intensity conditioning. Leukemia 2007, 21:2569-2574.
101. Rutten C.E., van Luxemburg-Heijs S.A., Griffioen M., et al. HLA-DP as specific target for cellular immunotherapy in HLA class II-expressing B-cell leukemia. Leukemia 2008, 22:1387-1394.
102. Rutten C.E., van Luxemburg-Heijs S.A., van der Meijden E.D., Griffioen M., Oudshoorn M., Willemze R., Falkenburg J.H. Both permissive and nonpermissive HLA-DPB1 mismatches can induce polyclonal HLA-DPB1 specific immune responses in vivo and in vitro. Blood 2010, 115:151-153.
103. Shaw B.E., Gooley T.A., Malkki M., et al. The importance of HLA-DPB1 in unrelated donor hematopoietic cell transplantation. Blood 2007, 110:4560-4566.
104. Kawase T., Matsuo K., Kashiwase K., et al. HLA mismatch combinations associated with decreased risk of relapse: implications for the molecular mechanism. Blood 2009, 113:2851-2858.
105. Kolb H.J. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 2008, 112:4371-4383.
106. Mackall C.L., Fleisher T.A., Brown M.R., et al. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N Engl J Med 1995, 332:143-149.
107. Asavaroengchai W., Kotera Y., Mule J.J. Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery. Proc Natl Acad Sci USA 2002, 99:931-936.
108. Sun J.C., Bevan M.J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 2003, 300:339-342.
109. Dotti G. Blocking PD-1 in cancer immunotherapy. Blood 2009, 114:1457-1458.
110. Bollard C.M., Rossig C., Calonge M.J., et al. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 2002, 99:3179-3187.
111. Curti A., Pandolfi S., Valzasina B., et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood 2007, 109:2871-2877.
112. Mellor A.L., Munn D.H. Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat Rev Immunol 2008, 8:74-80.
113. Baban B., Chandler P.R., Sharma M.D., et al. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 2009, 183:2475-2483.
114. Chen W., Liang X., Peterson A.J., Munn D.H., Blazar B.R. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 2008, 181:5396-5404.
115. Mizoguchi H., O'Shea J.J., Longo D.L., Loeffler C.M., McVicar D.W., Ochoa A.C. Alterations in signal transduction molecules in T lymphocytes from tumor-bearing mice. Science 1992, 258:1795-1798.
116. Rodriguez P.C., Ochoa A.C. Arginine regulation by myeloid derived suppressor cells and tolerance in cancer: mechanisms and therapeutic perspectives. Immunol Rev 2008, 222:180-191.
117. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009, 9:162-174.
118. Sinha P., Clements V.K., Fulton A.M., Ostrand-Rosenberg S. Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res 2007, 67:4507-4513.
119. Bronte V. Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur J Immunol 2009, 39:2670-2672.
120. Rodriguez P.C., Ernstoff M.S., Hernandez C., et al. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res 2009, 69:1553-1560.
121. Gabrilovich D., Ishida T., Oyama T., et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood 1998, 92:4150-4166.
122. Berner V., Liu H., Zhou Q., et al. IFN-gamma mediates CD4+ T-cell loss and impairs secondary antitumor responses after successful initial immunotherapy. Nat Med 2007, 13:354-360.
123. Guimond M., Veenstra R.G., Grindler D.J., et al. Interleukin 7 signaling in dendritic cells regulates the homeostatic proliferation and niche size of CD4+ T cells. Nat Immunol 2009, 10:149-157.
124. Boyman O., Kovar M., Rubinstein M.P., Surh C.D., Sprent J. Selective stimulation of T cell subsets with antibody-cytokine immune complexes. Science 2006, 311:1924-1927.
125. Prlic M., Kamimura D., Bevan M.J. Rapid generation of a functional NK-cell compartment. Blood 2007, 110:2024-2026.
126. Sportes C., Hakim F.T., Memon S.A., et al. Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J Exp Med 2008, 205:1701-1714.
127. Huntington N.D., Legrand N., Alves N.L., et al. IL-15 trans-presentation promotes human NK cell development and differentiation in vivo. J Exp Med 2009, 206:25-34.
128. Spolski R., Leonard W.J. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu Rev Immunol 2008, 26:57-79.
129. Hinrichs C.S., Spolski R., Paulos C.M., et al. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 2008, 111:5326-5333.
130. Ribas A., Camacho L.H., Lopez-Berestein G., et al. Antitumor activity in melanoma and anti-self responses in a phase I trial with the anti-cytotoxic T lymphocyte-associated antigen 4 monoclonal antibody CP-675,206. J Clin Oncol 2005, 23:8968-8977.
131. Sharma S., Yang S.C., Zhu L., et al. Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FOXP3 expression and CD4+ CD25+ T regulatory cell activities in lung cancer. Cancer Res 2005, 65:5211-5220.
132. Ozao-Choy J., Ma G., Kao J., et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res 2009, 69:2514-2522.
133. Li H., Han Y., Guo Q., Zhang M., Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 2009, 182:240-249.
134. Marigo I., Dolcetti L., Serafini P., Zanovello P., Bronte V. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 2008, 222:162-179.
135. Morgan R.A., Dudley M.E., Wunderlich J.R., et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006, 314:126-129.
136. Zhou Q., Bucher C., Munger M.E., et al. Depletion of endogenous tumor-associated regulatory T cells improves the efficacy of adoptive cytotoxic T-cell immunotherapy in murine acute myeloid leukemia. Blood 2009, 114:3793-3802.
137. Wrzesinski C., Paulos C.M., Gattinoni L., et al. Hematopoietic stem cells promote the expansion and function of adoptively transferred antitumor CD8 T cells. J Clin Invest 2007, 117:492-501.
138. Wu C.J., Yang X.F., McLaughlin S., et al. Detection of a potent humoral response associated with immune-induced remission of chronic myelogenous leukemia. J Clin Invest 2000, 106:705-714.
139. Yang X.F., Wu C.J., Chen L., et al. CML28 is a broadly immunogenic antigen, which is overexpressed in tumor cells. Cancer Res 2002, 62:5517-5522.
140. Bellucci R., Alyea E.P., Weller E., et al. Immunologic effects of prophylactic donor lymphocyte infusion after allogeneic marrow transplantation for multiple myeloma. Blood 2002, 99:4610-4617.
141. Bellucci R., Wu C.J., Chiaretti S., et al. Complete response to donor lymphocyte infusion in multiple myeloma is associated with antibody responses to highly expressed antigens. Blood 2004, 103:656-663.
142. Pfistershammer K., Lawitschka A., Klauser C., et al. Allogeneic disparities in immunoglobulin-like transcript 5 induce potent antibody responses in hematopoietic stem cell transplant recipients. Blood 2009, 114:2323-2332.
143. Bellucci R., Alyea E.P., Chiaretti S., et al. Graft-versus-tumor response in patients with multiple myeloma is associated with antibody response to BCMA, a plasma-cell membrane receptor. Blood 2005, 105:3945-3950.
144. Miklos D.B., Kim H.T., Miller K.H., et al. Antibody responses to H-Y minor histocompatibility antigens correlate with chronic graft-versus-host disease and disease remission. Blood 2005, 105:2973-2978.
145. Zorn E., Miklos D.B., Floyd B.H., et al. Minor histocompatibility antigen DBY elicits a coordinated B and T cell response after allogeneic stem cell transplantation. J Exp Med 2004, 199:1133-1142.
146. Jinushi M., Vanneman M., Munshi N.C., et al. MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proc Natl Acad Sci USA 2008, 105:1285-1290.
147. Ho V.T., Vanneman M., Kim H., et al. Biologic activity of irradiated, autologous, GM-CSF-secreting leukemia cell vaccines early after allogeneic stem cell transplantation. Proc Natl Acad Sci USA 2009, 106:15825-15830.
148. Boukouaci W., Busson M., Peffault de Latour R., et al. MICA-129 genotype, soluble MICA and anti-MICA antibodies as biomarkers of chronic graft versus host disease. Blood 2009, 114:5216-5224.
149. Reuschenbach M., von Knebel Doeberitz M., Wentzensen N. A systematic review of humoral immune responses against tumor antigens. Cancer Immunol Immunother 2009, 58:1535-1544.
150. Gnjatic S., Nishikawa H., Jungbluth A.A., et al. NY-ESO-1: review of an immunogenic tumor antigen. Adv Cancer Res 2006, 95:1-30.
151. Qin Z., Richter G., Schuler T., et al. B cells inhibit induction of T cell-dependent tumor immunity. Nat Med 1998, 4:627-630.
152. Sarantopoulos S., Stevenson K.E., Kim H.T., et al. High levels of B-cell activating factor in patients with active chronic graft-versus-host disease. Clin Cancer Res 2007, 13:6107-6114.
153. Sarantopoulos S., Stevenson K.E., Kim H.T., et al. Altered B-cell homeostasis and excess BAFF in human chronic graft-versus-host disease. Blood 2009, 113:3865-3874.
154. Shimabukuro-Vornhagen A., Hallek M.J., Storb R.F., von Bergwelt-Baildon M.S. The role of B cells in the pathogenesis of graft-versus-host disease. Blood 2009, 114:4919-4927.
155. Cutler C., Miklos D., Kim H.T., et al. Rituximab for steroid-refractory chronic graft-versus-host disease. Blood 2006, 108:756-762.
156. Zaja F., Bacigalupo A., Patriarca F., et al. Treatment of refractory chronic GVHD with rituximab: a GITMO study. Bone Marrow Transplant 2007, 40:273-277.
157. Kharfan-Dabaja M.A., Mhaskar A.R., Djulbegovic B., Cutler C., Mohty M., Kumar A. Efficacy of rituximab in the setting of steroid-refractory chronic graft-versus-host disease: a systematic review and meta-analysis. Biol Blood Marrow Transplant 2009, 15:1005-1013.
158. Sun J.C., Beilke J.N., Lanier L.L. Adaptive immune features of natural killer cells. Nature 2009, 457:557-561.
159. Kim S., Poursine-Laurent J., Truscott S.M., et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005, 436:709-713.
160. Gasser S., Raulet D.H. Activation and self-tolerance of natural killer cells. Immunol Rev 2006, 214:130-142.
161. Anfossi N., Andre P., Guia S., et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006, 25:331-342.
162. Joncker N.T., Fernandez N.C., Treiner E., Vivier E., Raulet D.H. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J Immunol 2009, 182:4572-4580.
163. Brodin P., Karre K., Hoglund P. NK cell education: not an on-off switch but a tunable rheostat. Trends Immunol 2009, 30:143-149.
164. Ruggeri L., Capanni M., Casucci M., et al. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 1999, 94:333-339.
165. Savani B.N., Mielke S., Adams S., et al. Rapid natural killer cell recovery determines outcome after T-cell-depleted HLA-identical stem cell transplantation in patients with myeloid leukemias but not with acute lymphoblastic leukemia. Leukemia 2007, 21:2145-2152.
166. Welte S., Kuttruff S., Waldhauer I., Steinle A. Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nat Immunol 2006, 7:1334-1342.
167. Sconocchia G., Lau M., Provenzano M., et al. The antileukemia effect of HLA-matched NK and NK-T cells in chronic myelogenous leukemia involves NKG2D-target-cell interactions. Blood 2005, 106:3666-3672.
168. Yong A.S., Keyvanfar K., Hensel N., et al. Primitive quiescent CD34+ cells in chronic myeloid leukemia are targeted by in vitro expanded natural killer cells, which are functionally enhanced by bortezomib. Blood 2009, 113:875-882.
169. Giebel S., Locatelli F., Lamparelli T., et al. Survival advantage with KIR ligand incompatibility in hematopoietic stem cell transplantation from unrelated donors. Blood 2003, 102:814-819.
170. Beelen D.W., Ottinger H.D., Ferencik S., 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, 105:2594-2600.
171. Ruggeri L., Mancusi A., Capanni M., et al. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood 2007, 110:433-440.
172. Davies S.M., Ruggieri L., DeFor T., et al. Evaluation of KIR ligand incompatibility in mismatched unrelated donor hematopoietic transplants. Killer immunoglobulin-like receptor. Blood 2002, 100:3825-3827.
173. Bishara A., De Santis D., Witt C.C., et al. The beneficial role of inhibitory KIR genes of HLA class I NK epitopes in haploidentically mismatched stem cell allografts may be masked by residual donor-alloreactive T cells causing GVHD. Tissue Antigens 2004, 63:204-211.
174. Bornhauser M., Schwerdtfeger R., Martin H., Frank K.H., Theuser C., Ehninger G. Role of KIR ligand incompatibility in hematopoietic stem cell transplantation using unrelated donors. Blood 2004, 103:2860-2861. author reply 2862.
175. Farag S.S., Bacigalupo A., Eapen M., 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 Rransplant Registry, and the Dutch Registry. Biol Blood Marrow Transplant 2006, 12:876-884.
176. Kroger N., Binder T., Zabelina T., et al. Low number of donor activating killer immunoglobulin-like receptors (KIR) genes but not KIR-ligand mismatch prevents relapse and improves disease-free survival in leukemia patients after in vivo T-cell depleted unrelated stem cell transplantation. Transplantation 2006, 82:1024-1030.
177. Cooley S., Trachtenberg E., Bergemann T.L., et al. Donors with group B KIR haplotypes improve relapse-free survival after unrelated hematopoietic cell transplantation for acute myelogenous leukemia. Blood 2009, 113:726-732.
178. Dummer W., Niethammer A.G., Baccala R., et al. T cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 2002, 110:185-192.
179. Dudley M.E., Wunderlich J.R., Robbins P.F., et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002, 298:850-854.
180. Miller J.S., Soignier Y., Panoskaltsis-Mortari A., et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005, 105:3051-3057.
181. Berger C., Berger M., Hackman R.C., et al. Safety and immunologic effects of IL-15 administration in nonhuman primates. Blood 2009, 114:2417-2426.
182. Fujisaki H., Kakuda H., Shimasaki N., et al. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res 2009, 69:4010-4017.
183. Berg M., Lundqvist A., McCoy P., et al. 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, 11:341-355.