Pre-emptive immunotherapy with purified natural killer cells after haploidentical SCT: A prospective phase II study in two centers

Bone Marrow Transplantation

Volumn 48, Issue 3, 2013, Pages 433-438

  Stern, M ^a   Passweg, J R ^a   Meyer Monard, S ^a   Esser, R ^b   Tonn, T ^c   Soerensen, J ^b   Paulussen, M ^a   Gratwohl, A ^a   Klingebiel, T ^b   Bader, P ^b   Tichelli, A ^a   Schwabe, D ^b   Koehl, U ^b,d  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b GOETHE UNIVERSITY   (Germany)

^c Red Cross Blood Donor Center   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

DLI; haploidentical; leukemia; NK cells

Indexed keywords

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ADOPTIVE TRANSFER; ADULT; ARTICLE; CANCER IMMUNOTHERAPY; CANCER RECURRENCE; CAUSE OF DEATH; CELL ENGINEERING; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FOLLOW UP; GRAFT FAILURE; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HODGKIN DISEASE; HUMAN; HUMAN CELL; MULTICENTER STUDY; NATURAL KILLER T CELL; NEUROTOXICITY; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROSPECTIVE STUDY; SALVAGE THERAPY; SARCOMA; SCHOOL CHILD; SURVIVAL RATE; SURVIVAL TIME; THERAPY EFFECT;

ADOLESCENT; ADULT; CHILD; HAPLOIDY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; LEUKEMIA; NEOPLASMS; PROSPECTIVE STUDIES; TRANSPLANTATION CONDITIONING; YOUNG ADULT;

EID: 84875230309     PISSN: 02683369     EISSN: 14765365     Source Type: Journal    
DOI: 10.1038/bmt.2012.162     Document Type: Article

References (37)

1. Kanda J, Chao NJ, Rizzieri DA. Haploidentical transplantation for leukemia. Curr Oncol Rep 2010; 12: 292-301.
2. Klingebiel T, Cornish J, Labopin M, Locatelli F, Darbyshire P, Handgretinger R et al. Results and factors influencing outcome after fully haploidentical hematopoietic stem cell transplantation in children with very high-risk acute lymphoblastic leukemia: impact of center size: an analysis on behalf of the Acute Leukemia and Pediatric Disease Working Parties of the European Blood and Marrow Transplant Group. Blood 2010; 115: 3437-3446.
3. Aversa F, Tabilio A, Velardi A, Cunningham I, Terenzi A, Falzetti F 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: 1186-1193.
4. 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.
5. Kolb HJ, Mittermuller 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.
6. Lewalle P, Triffet A, Delforge A, Crombez P, Selleslag D, De Muynck H et al. Donor lymphocyte infusions in adult haploidentical transplant: a dose finding study. Bone Marrow Transplant 2003; 31: 39-44.
7. Moretta L, Locatelli F, Pende D, Marcenaro E, Mingari MC, Moretta A. Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 2011; 117: 764-771.
8. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002; 295: 2097-2100.
9. Nguyen S, Dhedin N, Vernant JP, Kuentz M, Al Jijakli A, Rouas-Freiss N et al. NK-cell reconstitution after haploidentical hematopoietic stem-cell transplantations: immaturity of NK cells and inhibitory effect of NKG2A override GvL effect. Blood 2005; 105: 4135-4142.
10. Stern M, de Angelis C, Urbani E, Mancusi A, Aversa F, Velardi A et al. Natural killer-cell KIR repertoire reconstitution after haploidentical SCT. Bone Marrow Transplant 2010; 45: 1607-1610.
11. Passweg JR, Koehl U, Uharek L, Meyer-Monard S, Tichelli A. Natural-killer-cell-based treatment in haematopoietic stem-cell transplantation. Best Pract Res Clin Haematol 2006; 19: 811-824.
12. Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005; 105: 3051-3057.
13. Curti A, Ruggeri L, D'Addio A, Bontadini A, Dan E, Motta MR 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: 3273-3279.
14. Rubnitz JE, Inaba H, Dahl G, Ribeiro RC, Bowman WP, Taub J et al. Minimal residual disease-directed therapy for childhood acute myeloid leukaemia: results of the AML02 multicentre trial. Lancet Oncol 2010; 11: 543-552.
15. Koehl U, Sorensen J, Esser R, Zimmermann S, Gruttner HP, Tonn T et al. IL-2 activated NK cell immunotherapy of three children after haploidentical stem cell transplantation. Blood Cells Mol Dis 2004; 33: 261-266.
16. Passweg JR, Tichelli A, Meyer-Monard S, Heim D, Stern M, Kuhne T et al. Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia 2004; 18: 1835-1838.
17. Koehl U, Beck O, Esser R, Seifried E, Klingebiel T, Schwabe D et al. Quantitative analysis of chimerism after allogeneic stem cell transplantation by PCR amplification of microsatellite markers and capillary electrophoresis with fluorescence detection: the Frankfurt experience. Leukemia 2003; 17: 232-236.
18. Koehl U, Esser R, Zimmermann S, Tonn T, Kotchetkov R, Bartling T et al. Ex vivo expansion of highly purified NK cells for immunotherapy after haploidentical stem cell transplantation in children. Klin Padiatr 2005; 217: 345-350.
19. Meyer-Monard S, Passweg J, Siegler U, Kalberer C, Koehl U, Rovo A et al. Clinical-grade purification of natural killer cells in haploidentical hematopoietic stem cell transplantation. Transfusion 2009; 49: 362-371.
20. Brando B, Barnett D, Janossy G, Mandy F, Autran B, Rothe G et al. Cytofluorometric methods for assessing absolute numbers of cell subsets in blood. European Working Group on Clinical Cell Analysis. Cytometry 2000; 42: 327-346.
21. Koehl U, Bochennek K, Esser R, Brinkmann A, Quaritsch R, Becker M et al. ISHAGE-based single-platform flowcytometric analysis for measurement of absolute viable T cells in fresh or cryopreserved products: CD34/CD133 selected or CD3/CD19 depleted stem cells, DLI and purified CD56 + CD3-NK cells. Int J Hematol 2008; 87: 98-105.
22. Huenecke S, Zimmermann SY, Kloess S, Esser R, Brinkmann A, Tramsen L et al. IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16-subpopulations and in vivo influence after haploidentical NK cell infusion. J Immunother 33: 200-210.
23. Zimmermann SY, Esser R, Rohrbach E, Klingebiel T, Koehl U. A novel four-colour flow cytometric assay to determine natural killer cell or T-cell-mediated cellular cytotoxicity against leukaemic cells in peripheral or bone marrow specimens containing greater than 20% of normal cells. J Immunol Methods 2005; 296: 63-76.
24. Aversa F, Tabilio A, Terenzi A, Velardi A, Falzetti F, Giannoni C 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: 3948-3955.
25. Fischer A, Landais P, Friedrich W, Morgan G, Gerritsen B, Fasth A et al. European experience of bone-marrow transplantation for severe combined immunodeficiency. Lancet 1990; 336: 850-854.
26. Fischer JC, Ottinger H, Ferencik S, Sribar M, Punzel M, Beelen DW et al. Relevance of C1 and C2 epitopes for hemopoietic stem cell transplantation: role for sequential acquisition of HLA-C-specific inhibitory killer Ig-like receptor. J Immunol 2007; 178: 3918-3923.
27. Siegler U, Meyer-Monard S, Jorger S, Stern M, Tichelli A, Gratwohl A et al. Good manufacturing practice-compliant cell sorting and large-scale expansion of single KIR-positive alloreactive human natural killer cells for multiple infusions to leukemia patients. Cytotherapy 2010; 12: 750-763.
28. Huenecke S, Zimmermann SY, Kloess S, Esser R, Brinkmann A, Tramsen L et al. IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16-subpopulations and in vivo influence after haploidentical NK cell infusion. J Immunother 2010; 33: 200-210.
29. Iyengar R, Handgretinger R, Babarin-Dorner A, Leimig T, Otto M, Geiger TL et al. Purification of human natural killer cells using a clinical-scale immunomagnetic method. Cytotherapy 2003; 5: 479-484.
30. Ljunggren HG, Malmberg KJ. Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol 2007; 7: 329-339.
31. Malmberg KJ, Bryceson YT, Carlsten M, Andersson S, Bjorklund A, Bjorkstrom NK et al. NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy. Cancer Immunol Immunother 2008; 57: 1541-1552.
32. Choi SS, Chhabra VS, Nguyen QH, Ank BJ, Stiehm ER, Roberts RL. Interleukin-15 enhances cytotoxicity, receptor expression, and expansion of neonatal natural killer cells in long-term culture. Clin Diagn Lab Immunol 2004; 11: 879-888.
33. de Rham C, Ferrari-Lacraz S, Jendly S, Schneiter G, Dayer JM, Villard J. The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Res Ther 2007; 9: R125.
34. Dunne J, Lynch S, O'Farrelly C, Todryk S, Hegarty JE, Feighery C et al. Selective expansion and partial activation of human NK cells and NK receptor-positive T cells by IL-2 and IL-15. J Immunol 2001; 167: 3129-3138.
35. Brehm C, Huenecke S, Quaiser A, Esser R, Bremm M, Kloess S et al. IL-2 Stimulated but not unstimulated NK Cells induce selective disappearance of peripheral blood cells: concomitant results to a phase I/II study. PLoS One 2011; 6: e27351.
36. Kloess S, Huenecke S, Piechulek D, Esser R, Koch J, Brehm C et al. IL-2-Activated haploidentical NK cells restore NKG2D-mediated NK-cell cytotoxicity in neuro-blastoma patients by scavenging of plasma MICA. Eur J Immunol 2010; 40: 3255-3267.
37. Diermayr S, Himmelreich H, Durovic B, Mathys-Schneeberger A, Siegler U, Langenkamp U et al. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood 2008; 111: 1428-1436.