Escalated lymphodepletion followed by donor lymphocyte infusion can induce a graft-versus-host response without overwhelming toxicity

Bone Marrow Transplantation

Volumn 47, Issue 8, 2012, Pages 1112-1117

  Guillaume, T ^a,b,c   Gaugler, B ^d,e,f,g   Chevallier, P ^a,b,c   Delaunay, J ^a,c   Ayari, S ^a,c   Clavert, A ^a,c   Rialland, F ^a,b   Le Gouill, S ^a,c,h   Blin, N ^a,c   Gastinne, T ^a,c   Mahe B ^a,c   Dubruille, V ^a,c   Moreau, P ^a,b,c,h   Mohty, M ^a,b,c,h  

^a NANTES UNIVERSITY HOSPITAL   (France)

^b Team 12   (France)

^c Centre D'Investigation Clinique en Cancérologie CI2C   (France)

^d INSERM   (France)

^e ETABLISSEMENT FRANÇAIS DU SANG   (France)

^f UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^g Plateforme de Biomonitoring   (France)

^h UNIVERSITÉ DE NANTES   (France)

Author keywords

donor lymphocyte infusion; GVHD; lymphodepletion

Indexed keywords

CYCLOPHOSPHAMIDE; FLUDARABINE; INTERLEUKIN 15; INTERLEUKIN 7;

ADULT; AGED; ALLOGENEIC STEM CELL TRANSPLANTATION; ARTICLE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER RELAPSE; CANCER SURVIVAL; CHRONIC GRAFT VERSUS HOST DISEASE; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DONOR LYMPHOCYTE INFUSION; DOSE RESPONSE; DRUG DOSE ESCALATION; DRUG EFFICACY; ENTEROPATHY; FEMALE; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNOLOGICAL MONITORING; IMMUNOSUPPRESSIVE TREATMENT; LIVER DISEASE; LYMPHODEPLETION; MALE; PATIENT MONITORING; PILOT STUDY; PRIORITY JOURNAL; PROSPECTIVE STUDY; REDUCED INTENSITY CONDITIONING; SALVAGE THERAPY; SKIN DISEASE; T LYMPHOCYTE SUBPOPULATION;

ADOLESCENT; ADULT; AGED; FEMALE; GRAFT VS HOST DISEASE; HEMATOLOGIC NEOPLASMS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INCIDENCE; INTERLEUKIN-5; INTERLEUKIN-7; LIVING DONORS; LYMPHOCYTE DEPLETION; LYMPHOCYTE TRANSFUSION; MALE; MIDDLE AGED; PILOT PROJECTS; PROSPECTIVE STUDIES; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84864866385     PISSN: 02683369     EISSN: 14765365     Source Type: Journal    
DOI: 10.1038/bmt.2011.231     Document Type: Article

References (35)

1. Shaw BE, Russell NH. Treatment options for the management of acute leukaemia relapsing following an allogeneic transplant. Bone Marrow Transplant 2008; 41: 495-503. (Pubitemid 351386714)
2. Porter DL, Alyea EP, Antin JH, DeLima M, Estey E, Falkenburg JH et al. NCI First international workshop on the biology, prevention, and treatment of relapse after allogeneic hematopoietic stem cell transplantation: report from the committee on treatment of relapse after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2010; 16: 1467-1503.
3. Kolb HJ, Mittermü ller J, Clemm C, Holler E, Ledderose G, Brehm G et al. Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. Blood 1990; 76: 2462-2465.
4. Kolb HJ. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 2008; 112: 4371-4383.
5. Dazzi F, Szydlo RM, Cross NC, Craddock C, Kaeda J, Kanfer E et al. Durability of responses following donor lymphocyte infusions for patients who relapse after allogeneic stem cell transplantation for chronic myeloid leukemia. Blood 2000; 96: 2712-2716.
6. Dazzi F, Szydlo RM, Craddock C, Cross NC, Kaeda J, Chase A et al. Comparison of single-dose and escalating-dose regimens of donor lymphocyte infusion for relapse after allografting for chronic myeloid leukemia. Blood 2000; 95: 67-71. (Pubitemid 30017226)
7. Porter DL, Collins Jr RH, Hardy C, Kernan NA, Drobyski WR, Giralt S et al. Treatment of relapsed leukemia after unrelated donor marrow transplantation with unrelated donor leukocyte infusions. Blood 2000; 95: 1214-1221. (Pubitemid 30099829)
8. Schmid C, Labopin M, Nagler A, Bornhäuser M, Finke J, Fassas A et al. Donor lymphocyte infusion in the treatment of first hematological relapse after allogeneic stem-cell transplantation in adults with acute myeloid leukemia: A retrospective risk factors analysis and comparison with other strategies by the EBMT Acute Leukemia Working Party. J Clin Oncol 2007; 25: 4938-4945. (Pubitemid 350225492)
9. Muranski P, Boni A, Wrzesinski C, Citrin DE, Rosenberg SA, Childs R et al. Increased intensity lymphodepletion and adoptive immunotherapy, how far can we go? Nat Clin Pract Oncol 2006; 3: 668-681. (Pubitemid 44843125)
10. Klebanoff CA, Khong HT, Antony PA, Palmer DC, Restifo NP. Sinks, suppressors and antigen presenters: how lymphodepletion enhances T cell-mediated tumor immunotherapy. Trends Immunol 2005; 26: 111-117.
11. Greenberg PD. Therapy of murine leukemia with cyclophosphamide and immune Lyt-2+ cells: cytolytic T cells can mediate eradication of disseminated leukemia. J Immunol 1986; 136: 1917-1922. (Pubitemid 16119610)
12. Awwad M, North RJ. CYclophosphamide (CY)-facilitated adoptive immunotherapy of a CY-resistant tumour. Evidence that CY permits the expression of adoptive T-cell mediated immunity by removing suppressor T cells rather than by reducing tumour burden. Immunology 1988; 65: 87-92.
13. Miller JS, Weisdorf DJ, Burns LJ, Slungaard A, Wagner JE, Verneris MR et al. Lymphodepletion followed by donor lymphocyte infusion (DLI) causes signifi-cantly more acute graft-versus-host disease than DLI alone. Blood 2007; 110: 2761-2763. (Pubitemid 47523203)
14. O'Reilly RJ, Dao T, Koehne G, Scheinberg D, Doubrovina E. Adoptive transfer of unselected or leukemia reactive T cells in the treatment of relapse following allogeneic hematopoietic transplantation. Semin Immunology 2010; 22: 162-172.
15. Slavin S, Naparstek E, Nagler A, Ackerstein A, Samuel S, Kapelushnik J et al. Allogeneic cell therapy with donor peripheral blood cells and recombinant human interleukin-2 to treat leukemia relapse post-allogeneic bone marrow transplantation. Blood 1996; 87: 2195-2204. (Pubitemid 26086858)
16. Porter DL, Levine BL, Bunin N, Stadtmauer EA, Luger SM, Goldstein S et al. A phase 1 trial of donor lymphocyte infusions expanded and activated ex vivo via CD3/ CD28 costimulation. Blood 2006; 107: 1325-1331. (Pubitemid 43242365)
17. Warren EH, Fujii N, Akatsuka Y, Chaney CN, Mito JK, Loeb KR et al. Therapy of relapsed leukemia after allogeneic hematopoietic cell transplantation with T cells specific for minor histocompatibility antigens. Blood 2010; 115: 3869-3878.
18. Dummer W, Niethammer AG, Baccala R, Lawson BR, Wagner N, Reisfeld RA et al. T-cell homeostatic proliferation elicits effective antitumor autoimmunity. J Clin Invest 2002; 110: 185-192. (Pubitemid 34787355)
19. Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med 2005; 202: 907-912. (Pubitemid 41396891)
20. Wrzesinski C, Paulos CM, Kaiser A, Muranski P, Palmer DC, Gattinoni L et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. J Immunother 2010; 33: 1-7.
21. Brode S, Cooke A. Immune-potentiating effects of the chemotherapeutic drug cyclophosphamide. Crit Rev Immunol 2008; 28: 109-126. (Pubitemid 351507425)
22. Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C et al. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004; 34: 336-344. (Pubitemid 39255944)
23. Mitsuoka A, Baba M, Morikawa S. Enhancement of delayed hypersensitivity by depletion of suppressor T cells with cyclophosphamide in mice. Nature 1976; 262: 77-78.
24. Rollinghoff M, Starzinski-Powitz A, Pfizenmaier K, Wagner H. CYclophosphamidesensitive T lymphocytes suppress the in vivo generation of antigen-specific T lymphocytes. J Exp Med 1977; 145: 455-459. (Pubitemid 8032100)
25. North RJ. CYclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells. J Exp Med 1982; 155: 1063-1074. (Pubitemid 12142723)
26. Ikezawa Y, Nakazawa M, Tamura C, Takahashi K, Minami M, Ikezawa Z. CYclophosphamide decreases the number, percentage and the function of CD25+CD4+ regulatory T cells, which suppress induction of contact hypersensitivity. J Dermat Sc 2005; 39: 105-112. (Pubitemid 41073976)
27. Lutsiak MEC, Semnani RT, De Pascalis R, Kashmiri SVS, Schlom J, Sabzevari H. Inhibition of CD4+25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005; 105: 2862-2868. (Pubitemid 40446280)
28. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002; 298: 850-854. (Pubitemid 35231542)
29. Dudley ME, Yang JC, Sherry R, Hughes MS, Royal R, Kammula U et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 2008; 26: 5233-5239.
30. Maury S, Lemoine FM, Hicheri Y, Rosenzwajg M, Badoual C, Chera?̈ M et al. CD4+CD25+ regulatory T cell depletion improves the graft-versus-tumor effect of donor lymphocytes after allogeneic hematopoietic stem cell transplantation. Sci Transl Med 2010; 2: 41-52.
31. Colombo MP, Piconese S. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat Rev Cancer 2007; 7: 880-887. (Pubitemid 350006256)
32. Phipps RP, Mandel TE, Schnizlein CT, Tew JG. Anamnestic reponses induced by antigen persisting on follicular dendritic cells from cyclophosphamide- treated mice. Immunology 1984; 51: 387-397. (Pubitemid 14220446)
33. Limpens J, Van Meijer M, Van santen HM, Germeraad WT, Hoeben-Schornagel K, Breel M et al. Alterations in dendritic cell phenotype and function associated with immunoenhancing effects of a subcutaneously administered cyclophosphamide derivative. Immunology 1991; 73: 255-263.
34. Salem ML, Al-Kami AA, El-Naggar SA, D?́az-Montero CM, Chen Y, Cole DJ. Cyclophosphamide induces dynamic alterations in the host microenvironments resulting in a Flt3 ligand-dependent expansion of dendritic cells. J Immunol 2010; 184: 1737-1747.
35. van Rhee F, Lin F, Cullis JO, Spencer A, Cross NC, Chase A et al. Relapse of chronic myeloid leukemia after allogeneic bone marrow transplant: the case for giving donor leukocyte transfusions before the onset of hematologic relapse. Blood 1994; 83: 3377-3383. (Pubitemid 24158488)