T cell depletion and no post transplant immune suppression allow separation of graft versus leukemia from graft versus host disease.
Journal
Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459
Informations de publication
Date de publication:
08 2019
08 2019
Historique:
entrez:
22
8
2019
pubmed:
23
8
2019
medline:
9
9
2020
Statut:
ppublish
Résumé
Allogeneic hematopoietic cell transplantation from a human leukocyte antigen (HLA) haplotype mismatched donor (haploidentical transplantation) was not feasible for the treatment of hematologic malignancies until the early 1990s, due to the high risk of rejection and graft-versus-host disease (GVHD). The first successful protocol of haploidentical transplantation was based on a highly myeloablative and immunosuppressive conditioning regimen and the infusion of a "mega-dose" of T-cell-depleted hematopoietic stem cells. More than 90% of patients engrafted and <10% developed GVHD. The protocol did not include post-transplant immunosuppression, which favored the graft-versus-tumor effect mediated by alloreactive NK cells and residual alloreactive T cells. However, donor post-transplant immune reconstitution was slow with a high risk of infection-related mortality. More recently, T-cell-depleted haploidentical transplantation has become the platform for innovative cell therapies that aim to enhance T-cell immunity while preventing adverse reactions against host tissues. One strategy is adoptive immunotherapy with conventional T cells and regulatory T cells. Preclinical studies and clinical trials have proven that regulatory T cells control GVHD caused by co-infused conventional T cells while the graft-versus-tumor effect is retained. The use of regulatory T cells in the absence of any other form of immune suppression allowed for a conventional T cell-mediated full eradication of disease in the vast majority of high-risk acute leukemia patients.
Identifiants
pubmed: 31431701
doi: 10.1038/s41409-019-0597-y
pii: 10.1038/s41409-019-0597-y
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
775-779Références
Appelbaum FR, Forman SJ, Negrin RS, Blume KG. Thomas’ hematopoietic cell transplantation Oxford, United Kingdom: Wiley-Blackwell; 2009.
doi: 10.1002/9781444303537
Anasetti C, Aversa F, Velardi A. Hematopoietic cell transplantation from human leukocyte antigen partially matched related donors. In: Appelbaum FR, Forman SJ, Negrin RS, Blume KG, eds. Thomas’ hematopoietic cell transplantation. Oxford, United Kingdom: Wiley-Blackwell; 2009. p. 657–74.
doi: 10.1002/9781444303537.ch46
Reisner Y, Hagin D, Martelli MF. Haploidentical hematopoietic transplantation: current status and future perspectives. Blood. 2011;118:6006–17.
pubmed: 21921045
doi: 10.1182/blood-2011-07-338822
Velardi A. Haplo-BMT: which approach? [commentary]. Blood. 2013;121:719–20.
pubmed: 23372150
doi: 10.1182/blood-2012-12-469981
Mancusi A, Ruggeri L, Velardi A. Haploidentical hematopoietic transplantation for the cure of leukemia: from its biology to clinical translation. Blood. 2016;128:2616–23.
pubmed: 27697774
doi: 10.1182/blood-2016-07-730564
Bachar–Lustig E, Rachamin N, Li HW, et al. Megadose of T-cell depleted bone marrow overcomes MHC barriers in sublethally irradiated mice. Nat Med. 1995;1:1268–73.
pubmed: 7489407
doi: 10.1038/nm1295-1268
Aversa F, Tabilio A, Terenzi A, et al. Successful engraftment of T-cell-depleted haploidentical” three-loci” incompatible transplants in leukemia patients by addition of recombinant human granulocyte colony-stimulating factor-mobilized peripheral blood progenitor cells to bone marrow inoculum. Blood. 1994;84:3948–55.
pubmed: 7524753
doi: 10.1182/blood.V84.11.3948.bloodjournal84113948
Aversa F, Tabilio A, Velardi A, et al. Treatment of high-risk acute leukemia with T-cell-depleted stem cells from related donors with one fully mismatched HLA haplotype. N Engl J Med. 1998;339:1186–93.
pubmed: 9780338
doi: 10.1056/NEJM199810223391702
Aversa F, Terenzi A, Tabilio A, et al. Full haplotype-mismatched hematopoietic stem-cell transplantation: a phase II study in patients with acute leukemia at high risk of relapse. J Clin Oncol. 2005;23:3447–54.
pubmed: 15753458
doi: 10.1200/JCO.2005.09.117
Martelli MF, Di Ianni M, Ruggeri L, et al. “Designed” grafts for HLA-haploidentical stem cell transplantation. Blood. 2014;123:967–73.
pubmed: 24363403
doi: 10.1182/blood-2013-10-531764
Ciceri F, Labopin M, Aversa F, et al. A survey of fully haploidentical hematopoietic stem cell transplantation in adults with high-risk acute leukemia: a risk factor analysis of outcomes for patients in remission at transplantation. Blood. 2008;112:3574–81.
pubmed: 18606875
doi: 10.1182/blood-2008-02-140095
Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331:44–49.
pubmed: 21212348
pmcid: 3089969
doi: 10.1126/science.1198687
Ruggeri L, Capanni M, Casucci M, et al. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood. 1999;94:333–9.
pubmed: 10381530
pmcid: 10381530
doi: 10.1182/blood.V94.1.333.413a31_333_339
Ruggeri L, Capanni M, Urbani E, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295:2097–2100.
pubmed: 11896281
doi: 10.1126/science.1068440
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;110:433–40.
pubmed: 17371948
pmcid: 1896125
doi: 10.1182/blood-2006-07-038687
Shlomchik WD, Couzens MS, Tang CB, et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 1999;285:412–5.
pubmed: 10411505
doi: 10.1126/science.285.5426.412
Leung W, Iyengar R, Turner V, et al. Determinants of antileukemia effects of allogeneic NK cells. J Immunol. 2004;172:644–50.
pubmed: 14688377
doi: 10.4049/jimmunol.172.1.644
pmcid: 14688377
Pende D, Marcenaro S, Falco M, 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;113:3119–29.
pubmed: 18945967
doi: 10.1182/blood-2008-06-164103
pmcid: 18945967
Miller JS, 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;105:3051–7.
pubmed: 15632206
doi: 10.1182/blood-2004-07-2974
pmcid: 15632206
Rubnitz JE, Inaba H, Ribeiro RC, 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;28:955–9.
pubmed: 20085940
pmcid: 2834435
doi: 10.1200/JCO.2009.24.4590
Curti A, Ruggeri L, D’Addio A, 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;118:3273–9.
pubmed: 21791425
doi: 10.1182/blood-2011-01-329508
Curti A, Ruggeri L, Parisi S, et al. Larger size of donor alloreactive NK cell repertoire correlates with better response to NK cell immunotherapy in elderly acute myeloid leukemia patients. Clin Cancer Res. 2016;22:1914–21.
pubmed: 26787753
doi: 10.1158/1078-0432.CCR-15-1604
Stern M, Ruggeri L, Mancusi A, et al. Survival after T cell-depleted haploidentical stem cell transplantation is improved using the mother as donor. Blood. 2008;112:2990–5.
pubmed: 18492955
pmcid: 2962448
doi: 10.1182/blood-2008-01-135285
Velardi A, Ziagkos D, van Biezen A, et al. Mother donors improve outcomes after HLA haploidentical T cell-depleted hematopoietic transplantation: a Retrospective Study by the Cell Therapy and Immunobiology Working Party of the EBMT. Bone Marrow Transplant. 2016;51(S1):S150. Abstract P076
Maloney S, Smith A, Furst DE, et al. Microchimerism of maternal origin persists into adult life. J Clin Invest. 1999;104:41–47.
pubmed: 10393697
pmcid: 408407
doi: 10.1172/JCI6611
van Kampen CA. Versteeg-van der Voort Maarschalk MF, Langerak-Langerak J, van Beelen E, Roelen DL, Claas FH. Pregnancy can induce long-persisting primed CTLs specific for inherited paternal HLA antigens. Hum Immunol. 2001;62:201–7.
pubmed: 11250037
doi: 10.1016/S0198-8859(01)00209-9
pmcid: 11250037
Verdijk RM, Kloosterman A, Pool J, et al. Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells: implications for stem cell transplantation and immunotherapy. Blood. 2004;103:1961–4.
pubmed: 14592836
doi: 10.1182/blood-2003-05-1625
pmcid: 14592836
Edinger M, Hoffmann P, Ermann J, et al. CD4 + CD25 + regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9:1144–50.
pubmed: 12925844
doi: 10.1038/nm915
Nguyen VH, Zeiser R, Dasilva DL, et al. In vivo dynamics of regulatory T-cell trafficking and survival predict effective strategies to control graft-versus-host disease following allogeneic transplantation. Blood. 2007;109:2649–56.
pubmed: 17095616
doi: 10.1182/blood-2006-08-044529
Nguyen VH, Shashidhar S, Chang DS, et al. The impact of regulatory T cells on T-cell immunity following hematopoietic cell transplantation. Blood. 2008;111:945–53.
pubmed: 17916743
pmcid: 2200838
doi: 10.1182/blood-2007-07-103895
Pierini A, Colonna L, Alvarez M, et al. Donor requirements for regulatory T cell suppression of murine graft-versus-host disease. J Immunol. 2015;195:347–55.
pubmed: 25994967
pmcid: 4475671
doi: 10.4049/jimmunol.1402861
Fujisaki J, Wu J, Carlson AL, et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature. 2011;474:216–9.
pubmed: 21654805
pmcid: 3725645
doi: 10.1038/nature10160
Pierini A, Nishikii H, Baker J, et al. Foxp3
pubmed: 28485401
pmcid: 5436085
doi: 10.1038/ncomms15068
Di Ianni M, Falzetti F, Carotti A, et al. Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood. 2011;117:3921–8.
pubmed: 21292771
doi: 10.1182/blood-2010-10-311894
Martelli MF, Di Ianni M, Ruggeri L, et al. HLA-haploidentical transplantation with regulatory and conventional T cell adoptive immunotherapy prevents acute leukemia relapse. Blood. 2014;124:638–44.
pubmed: 24923299
doi: 10.1182/blood-2014-03-564401
Mancusi A, Ruggeri L, Velardi A. Haploidentical hematopoietic transplantation for the cure of leukemia: from its biology to clinical translation. Blood. 2016;128:2616–23.
pubmed: 27697774
doi: 10.1182/blood-2016-07-730564
Del Papa B, Ruggeri L, Urbani E, et al. linical-grade-expanded regulatory T cells prevent graft-versus-host disease while allowing a powerful T cell-dependent graft-versus-leukemia effect in murine models. Biol Blood Marrow Transplant. 2017;23:1847–51.
pubmed: 28729148
doi: 10.1016/j.bbmt.2017.07.009
Hippen KL1, Merkel SC, Schirm DK, et al. Massive ex vivo expansion of human natural regulatory T cells (T(regs)) with minimal loss of in vivo functional activity. Sci Transl Med. 2011;3:83ra41.
pubmed: 21593401
pmcid: 3551476
doi: 10.1126/scitranslmed.3001809
Brunstein CG, Miller JS, Cao Q, et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood. 2011;117:1061–70.
pubmed: 20952687
pmcid: 3035067
doi: 10.1182/blood-2010-07-293795
Brunstein CG, Miller JS, McKenna DH, et al. Umbilical cord blood-derived T regulatory cells to prevent GVHD: kinetics, toxicity profile, and clinical effect. Blood. 2016;127:1044–51.
pubmed: 26563133
pmcid: 4768428
doi: 10.1182/blood-2015-06-653667
Koreth J, Matsuoka K, Kim HT, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med. 2011;365:2055–66.
pubmed: 22129252
pmcid: 3727432
doi: 10.1056/NEJMoa1108188
Trotta E, Bessette PH, Silveria SL, et al. A human anti-IL-2 antibody that potentiates regulatory T cells by a structure-based mechanism. Nat Med. 2018;24:1005–14.
pubmed: 29942088
pmcid: 6398608
doi: 10.1038/s41591-018-0070-2
Pierini A, Strober W, Moffett C, et al. TNF-α priming enhances CD4 + FoxP3 + regulatory T-cell suppressive function in murine GVHD prevention and treatment. Blood. 2016;128:866–71.
pubmed: 27365424
pmcid: 4982455
doi: 10.1182/blood-2016-04-711275
Mancusi A, Piccinelli S, Velardi A, Pierini A. The effect of TNF-α on regulatory T cell function in graft-versus-host disease. Front Immunol. 2018;9:356.
pubmed: 29541073
pmcid: 5835761
doi: 10.3389/fimmu.2018.00356
MacDonald KG, Hoeppli RE, Huang Q, et al. Alloantigen-specific regulatory T cells generated with a chimeric antigen receptor. J Clin Invest. 2016;126:1413–24.
pubmed: 26999600
pmcid: 4811124
doi: 10.1172/JCI82771
Pierini A, Iliopoulou BP, Peiris H, et al. T cells expressing chimeric antigen receptor promote immune tolerance. JCI Insight. 2017;2:92865.
pubmed: 29046484
doi: 10.1172/jci.insight.92865
pmcid: 29046484