Prophylactic use of low-dose interleukin-2 and the clinical outcomes of hematopoietic stem cell transplantation: A randomized study

OncoImmunology

Volumn 5, Issue 12, 2016, Pages

  Zhao, Xiang Yu ^a   Zhao, Xiao Su ^a   Wang, Yu Tong ^a   Chen, Yu Hong ^a   Xu, Lan Ping ^a   Zhang, Xiao Hui ^a   Han, Wei ^a   Chen, Huan ^a   Wang, Yu ^a   Yan, Chen Hua ^a   Wang, Feng Rong ^a   Wang, Jing Zhi ^a   Liu, Kai Yan ^a   Chang, Ying Jun ^a   Huang, Xiao Jun ^a,b  

^a PEKING UNIVERSITY   (China)

^b Tsinghua University   (China)

Author keywords

cGVHD; IL 2; MRD; NK; Treg

Indexed keywords

BUSULFAN; CYCLOPHOSPHAMIDE; CYTARABINE; HYDROXYUREA; INTERLEUKIN 2;

ADOLESCENT; ADULT; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CLINICAL OUTCOME; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOTOXICITY; DONOR LYMPHOCYTE INFUSION; EPSTEIN BARR VIRUS; FEMALE; FOLLOW UP; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEPATITIS; HUMAN; LEUKEMIA RELAPSE; LOW DRUG DOSE; MAJOR CLINICAL STUDY; MALE; MINIMAL RESIDUAL DISEASE; MULTIPLE CYCLE TREATMENT; NATURAL KILLER CELL; PROPHYLAXIS; RANDOMIZED CONTROLLED TRIAL; REGULATORY T LYMPHOCYTE;

EID: 85007459979     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1250992     Document Type: Article

References (39)

1. Vago L, Forno B, Sormani MP, Crocchiolo R, Zino E, Di Terlizzi S, Stanghellini MTL, Mazzi B, Perna SK, Bondanza A, et al. Temporal, quantitative, and functional characteristics of single-KIR-positive alloreactive natural killer cell recovery account for impaired graft-versus-leukemia activity after haploidentical hematopoietic stem cell transplantation. Blood 2008; 112(8):3488-99; PMID:18645039; http://dx.doi.org/10.1182/blood-2007-07-103325
2. Zhao XY, Chang YJ, Zhao XS, Xu LP, Zhang XH, Liu KY, Li D, Huang XJ. Recipient expression of ligands for donor inhibitory KIRs enhances NK-cell function to control leukemic relapse after haploidentical transplantation. Eur J Immunol 2015; 45(8):2396-408; PMID:25952732; http://dx.doi.org/10.1002/eji.201445057
3. 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(5562):2097-100; PMID:11896281; http://dx.doi.org/10.1126/science.1068440
4. Liston A, Gray DHD. Homeostatic control of regulatory T cell diversity. Nat Rev Immunol 2014; 14(3):154-65; PMID:24481337; http://dx.doi.org/10.1038/nri3605
5. Matsuoka K, Kim HT, McDonough S, Bascug G, Warshauer B, Koreth J, Cutler C, Ho VT, Alyea EP, Antin JH, et al. Altered regulatory T cell homeostasis in patients with CD4+ lymphopenia following allogeneic hematopoietic stem cell transplantation. J Clin Invest 2010; 120(5):1479-93; PMID:20389017; http://dx.doi.org/10.1172/JCI41072
6. Rosenberg SA. IL-2:the first effective immunotherapy for human cancer. J Immun 2014; 192(12):5451-8; PMID:24907378; http://dx.doi.org/10.4049/jimmunol.1490019
7. Liao W, Lin JX, Leonard Warren J. Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. Immunity 2013; 38(1):13-25; PMID:23352221; http://dx.doi.org/10.1016/j.immuni.2013.01.004
8. Boyman O, Sprent J. The role of interleukin-2 during homeostasis and activation of the immune system. Nat Rev Immunol 2012; 12(3):180-90; PMID:22343569; http://dx.doi.org/10.1038/nri3156
9. Mohty M, Kuentz M, Michallet M, Bourhis JH, Milpied N, Sutton L, Jouet JP, Attal M, Bordigoni P, Cahn JY, et al. Chronic graft-versus-host disease after allogeneic blood stem cell transplantation:long-term results of a randomized study. Blood 2002; 100(9):3128-34; PMID:12384409; http://dx.doi.org/10.1182/blood.V100.9.3128
10. Ringden O, Pavletic SZ, Anasetti C, Barrett AJ, Wang T, Wang D, Antin JH, Di Bartolomeo P, Bolwell BJ, Bredeson C, et al. The graft-versus-leukemia effect using matched unrelated donors is not superior to HLA-identical siblings for hematopoietic stem cell transplantation. Blood 2009; 113(13):3110-8; PMID:19059878; http://dx.doi.org/10.1182/blood-2008-07-163212
11. Hallett WH, Ames E, Alvarez M, Barao I, Taylor PA, Blazar BR, Murphy WJ. Combination therapy using IL-2 and anti-CD25 results in augmented natural killer cell-mediated antitumor responses. Biol Blood Marrow Transplantation 2008; 14(10):1088-99; PMID:18804038; http://dx.doi.org/10.1016/j.bbmt.2008.08.001
12. Bachanova V, Cooley S, Defor TE, Verneris MR, Zhang B, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lewis D, Hippen K, et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood 2014; 123(25):3855-63; PMID:24719405; http://dx.doi.org/10.1182/blood-2013-10-532531
13. Verneris MR. Natural killer cells and regulatory T cells:how to manipulate a graft for optimal GVL. ASH Educ Program Book 2013; 2013(1):335-41
14. Koreth J, Matsuoka K, Kim HT, McDonough SM, Bindra B, Alyea EP, 3rd, Armand P, Cutler C, Ho VT, Treister NS, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Eng J Med 2011; 365(22):2055-66; PMID:22129252; http://dx.doi.org/10.1056/NEJMoa1108188
15. Kennedy-Nasser AA, Ku S, Castillo-Caro P, Hazrat Y, Wu MF, Liu H, Melenhorst J, Barrett AJ, Ito S, Foster A, et al. Ultra low-dose IL-2 for GVHD prophylaxis after allogeneic hematopoietic stem cell transplantation mediates expansion of regulatory T cells without diminishing antiviral and antileukemic activity. Clin Cancer Res 2014; 20(8):2215-25; PMID:24573552; http://dx.doi.org/10.1158/1078-0432.CCR-13-3205
16. Koreth J, Kim HT, Jones KT, Lange PB, Reynolds CG, Chammas MJ, Dusenbury K, Whangbo J, Nikiforow S, Alyea EP, 3rd et al. Efficacy, durability, and response predictors of low-dose interleukin-2 therapy for chronic graft vs. host disease. Blood 2016; 128(1):130-7; PMID:27073224; http://dx.doi.org/10.1182/blood-2016-02-702852
17. Imanguli MM, Cowen EW, Rose J, Dhamala S, Swaim W, Lafond S, Yagi B, Gress RE, Pavletic SZ, Hakim FT. Comparative analysis of FoxP3+ regulatory T Cells in the target tissues and blood in chronic graft versus host disease. Leukemia 2014; 28(10):2016-2027; PMID:24577531; http://dx.doi.org/10.1038/leu.2014.92
18. Zorn E, Kim HT, Lee SJ, Floyd BH, Litsa D, Arumugarajah S, Bellucci R, Alyea EP, Antin JH, Soiffer RJ, et al. Reduced frequency of FOXP3+ CD4+CD25+ regulatory T cells in patients with chronic graft-versus-host disease. Blood 2005; 106(8):2903-11; PMID:15972448; http://dx.doi.org/10.1182/blood-2005-03-1257
19. 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(4):458-65; PMID:19278419; http://dx.doi.org/10.1111/j.1365-2567.2008.03027.x
20. Huang XJ, Chang YJ, Zhao XY. Maintaining hyporesponsiveness and polarization potential of T cells after in vitro mixture of G-CSF mobilized peripheral blood grafts and G-CSF primed bone marrow grafts in different proportions. Transpl Immunol 2007; 17(3):193-7; PMID:17331846; http://dx.doi.org/10.1016/j.trim.2006.10.002
21. Chang YJ, Zhao XY, Huang XJ. Effects of the NK cell recovery on outcomes of unmanipulated haploidentical blood and marrow transplantation for patients with hematologic malignancies. Biol Blood Marrow Transplantation 2008; 14(3):323-34; PMID:18275899; http://dx.doi.org/10.1016/j.bbmt.2007.12.497
22. Bielekova B, Catalfamo M, Reichert-Scrivner S, Packer A, Cerna M, Waldmann TA, McFarland H, Henkart PA, Martin R. Regulatory CD56(bright) natural killer cells mediate immunomodulatory effects of IL-2Ralpha-targeted therapy (daclizumab) in multiple sclerosis. Proc Natl Acad Sci USA 2006; 103(15):5941-6; PMID:16585503; http://dx.doi.org/10.1073/pnas.0601335103
23. Kheav VD, Busson M, Scieux C, Peffault de Latour R, Maki G, Haas P, Mazeron M-C, Carmagnat M, Masson E, Xhaard A, et al. Favorable impact of natural killer cell reconstitution on chronic graft-versus-host disease and cytomegalovirus reactivation after allogeneic hematopoietic stem cell transplantation. Haematologica 2014; 99(12):1860-1867; PMID:25085354; http://dx.doi.org/10.3324/haematol.2014.108407
24. Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M, Caligiuri MA. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2:a potential new link between adaptive and innate immunity. Blood 2003; 101(8):3052-7; PMID:12480696; http://dx.doi.org/10.1182/blood-2002-09-2876
25. Goldszmid RS, Caspar P, Rivollier A, White S, Dzutsev A, Hieny S, Kelsall B, Trinchieri G, Sher A. NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 2012; 36(6):1047-59; PMID:22749354; http://dx.doi.org/10.1016/j.immuni.2012.03.026
26. Zhao XS, Jin S, Zhu HH, Xu LP, Liu DH, Chen H, Liu KY, Huang XJ. Wilms' tumor gene 1 expression:an independent acute leukemia prognostic indicator following allogeneic hematopoietic SCT. Bone Marrow Transplant 2012; 47(4):499-507; PMID:21643023; http://dx.doi.org/10.1038/bmt.2011.121
27. Wang Y, Liu QF, Xu LP, Liu KY, Zhang XH, Ma X, Fan ZP, Wu DP, Huang XJ, et al. Haploidentical vs identical-sibling transplant for AML in remission:a multicenter, prospective study. Blood 2015; 125(25):3956-62; PMID:25940714; http://dx.doi.org/10.1182/blood-2015-02-627786
28. Chang YJ, Xu LP, Wang Y, Zhang XH, Chen H, Chen YH, Wang FR, Han W, Sun YQ, Yan CH, et al. Controlled, randomized, open-label trial of risk-stratified corticosteroid prevention of acute graft-versus-host disease after haploidentical transplantation. J Clin Oncol 2016; 34(16):1855-63; PMID:27091717; http://dx.doi.org/10.1200/JCO.2015.63.8817
29. Lai YR, Chen YH, Hu DM, Jiang M, Liu QF, Liu L, Hou J, Schwarzenberger P, Li QC, Zhang ZM, et al. Multicenter phase II study of a combination of cyclosporine a, methotrexate and mycophenolate mofetil for GVHD prophylaxis:results of the Chinese Bone Marrow Transplant Cooperative Group (CBMTCG). J Hematol Oncol 2014; 7:59; PMID:25139202; http://dx.doi.org/10.1186/s13045-014-0059-3
30. Gao L, Zhang C, Gao L, Liu Y, Su Y, Wang S, Li B, Yang T, Yuan Z, Zhang X. Favorable outcome of haploidentical hematopoietic stem cell transplantation in Philadelphia chromosome-positive acute lymphoblastic leukemia:a multicenter study in Southwest China. J Hematol Oncol 2015; 8:90; PMID:26208715; http://dx.doi.org/10.1186/s13045-015-0186-5
31. Wang Y, Fu HX, Liu DH, Xu LP, Zhang XH, Chang YJ, Chen YH, Wang FR, Sun YQ, Tang FF, et al. Influence of two different doses of antithymocyte globulin in patients with standard-risk disease following haploidentical transplantation:a randomized trial. Bone Marrow Transplant 2014; 49(3):426-33; PMID:24292519; http://dx.doi.org/10.1038/bmt.2013.191
32. Zhao XS, Yan CH, Liu DH, Xu LP, Liu YR, Liu KY, Qin YZ, Wang Y, Huang XJ. Combined use of WT1 and flow cytometry monitoring can promote sensitivity of predicting relapse after allogeneic HSCT without affecting specificity. Annals Hematol 2013; 92(8):1111-9; PMID:23680867; http://dx.doi.org/10.1007/s00277-013-1733-1
33. Yan CH, Liu DH, Liu KY, Xu LP, Liu YR, Chen H, Han W, Wang Y, Qin YZ, Huang XJ. Risk stratification-directed donor lymphocyte infusion could reduce relapse of standard-risk acute leukemia patients after allogeneic hematopoietic stem cell transplantation. Blood 2012; 119(14):3256-62; PMID:22337715; http://dx.doi.org/10.1182/blood-2011-09-380386
34. Yan CH, Wang JZ, Liu DH, Xu LP, Chen H, Liu KY, Huang XJ. Chemotherapy followed by modified donor lymphocyte infusion as a treatment for relapsed acute leukemia after haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion:superior outcomes compared with chemotherapy alone and an analysis of prognostic factors. Eur J Haematol 2013; 91(4):304-14; PMID:23837640; http://dx.doi.org/10.1111/ejh.12168
35. Kong Y, Chang YJ, Wang YZ, Chen YH, Han W, Wang Y, Sun YQ, Yan CH, Wang FR, Liu YR, et al. Association of an impaired bone marrow microenvironment with secondary poor graft function after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplantation 2013; 19(10):1465-73; PMID:23879970; http://dx.doi.org/10.1016/j.bbmt.2013.07.014
36. Chang YJ, Zhao XY, Xu LP, Zhang XH, Wang Y, Han W, Chen H, Wang FR, Mo XD, Zhang YY, et al. Donor-specific anti-human leukocyte antigen antibodies were associated with primary graft failure after unmanipulated haploidentical blood and marrow transplantation:a prospective study with randomly assigned training and validation sets. J Hematol Oncol 2015; 8:84; PMID:26156584; http://dx.doi.org/10.1186/s13045-015-0182-9
37. Holtan SG, DeFor TE, Lazaryan A, Bejanyan N, Arora M, Brunstein CG, Blazar BR, MacMillan ML, Weisdorf DJ. Composite end point of graft-versus-host disease-free, relapse-free survival after allogeneic hematopoietic cell transplantation. Blood 2015; 125(8):1333-8; PMID:25593335; http://dx.doi.org/10.1182/blood-2014-10-609032
38. Glucksberg H, Storb R, Fefer A, Buckner CD, Neiman PE, Clift RA, Lerner KG, Thomas ED. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation 1974; 18(4):295-304; PMID:4153799; http://dx.doi.org/10.1097/00007890-197410000-00001
39. Filipovich AH, Weisdorf D, Pavletic S, Socie G, Wingard JR, Lee SJ, Martin P, Chien J, Przepiorka D, Couriel D, et al. National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease:I. Diagnosis and staging working group report. Biol Blood Marrow Transplantation 2005; 11(12):945-56; PMID:16338616; http://dx.doi.org/10.1016/j.bbmt.2005.09.004