Distinct graft-versus-leukemic stem cell effects of early or delayed donor leukocyte infusions in a mouse chronic myeloid leukemia model

Blood

Volumn 119, Issue 1, 2012, Pages 273-284

  Lu, Yi Fen ^a,b   Gavrilescu, L Cristina ^a   Betancur, Monica ^a   Lazarides, Katherine ^a   Klingemann, Hans ^a   Van Etten, Richard A ^a  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTILEUKEMIC AGENT; BCR ABL PROTEIN; BCR ABL1 PROTEIN; CD11B ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; CELL THERAPY AGENT; IMATINIB; UNCLASSIFIED DRUG;

ALLOGENEIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CANCER STEM CELL; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHIMERA; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; DELAYED DONOR LYMPHOCYTE INFUSION; DISEASE SEVERITY; DONOR LYMPHOCYTE INFUSION; DRUG DOSE REDUCTION; EARLY DONOR LYMPHOCYTE INFUSION; ENGRAFTMENT; FEMALE; GRAFT VERSUS LEUKEMIA EFFECT; LEUKEMIA RELAPSE; LEUKEMIA STEM CELL; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION DOSE; SPLEEN CELL;

EID: 84862907710     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-01-331009     Document Type: Article

References (49)

1. Quintás-Cardama A, Cortes J. Molecular biology of bcr-abl1-positive chronic myeloid leukemia. Blood. 2009;113(8):1619-1630.
2. Barrett J. Allogeneic stem cell transplantation for chronic myeloid leukemia. Semin Hematol. 2003;40(1):59-71. (Pubitemid 36160110)
3. Horowitz MM, Gale RP, Sondel PM, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75(3):555-562. (Pubitemid 20069191)
4. Kolb HJ, Mittermuller J, Clemm C, et al. Donor leukocyte transfusions for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients. Blood. 1990;76(12):2462-2465.
5. Porter DL, Roth MS, McGarigle C, Ferrara JL, Antin JH. Induction of graft-versus-host disease as immunotherapy for relapsed chronic myeloid leukemia. N Engl J Med. 1994;330(2):100-106.
6. Kolb HJ, Schattenberg A, Goldman JM, et al. Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. Blood. 1995;86(5):2041-2050.
7. Collins RHJ, Shpilberg O, Drobyski WR, et al. Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. J Clin Oncol. 1997;15(2):433-444. (Pubitemid 27074209)
8. Kolb HJ, Schmidt C, Barrett AJ, Schendel DJ. Graft-versus-leukemia reactions in allogeneic chimeras. Blood. 2004;103(3):767-776. (Pubitemid 38129531)
9. Mackinnon S, Papadopoulos EB, Carabasi MH, et al. Adoptive immunotherapy evaluating escalating doses of donor leukocytes for relapse of chronic myeloid leukemia after bone marrow transplantation: separation of graft-versus-leukemia responses from graft-versus-host disease. Blood. 1995;86(4):1261-1268.
10. Giralt S, Hester J, Huh Y, et al. CD8-depleted donor leukocyte infusions as treatment for relapsed chronic myelogenous leukemia after allogeneic bone marrow transplantation: graft vs. leukemia without graft vs. host disease. Blood. 1995;86(11):4337-4343.
11. Alyea EP, Soiffer RJ, Canning C, et al. Toxicity and efficacy of defined doses of CD4(+) donor lymphocytes for treatment of relapse after allogeneic bone marrow transplant. Blood. 1998;91(10):3671-3680. (Pubitemid 28225734)
12. O'Brien SG, Guilhot F, Larson RA, et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase myeloid leukemia. N Engl J Med. 2003;348(11):994-1004. (Pubitemid 36302244)
13. Hughes TP, Kaeda J, Branford S, et al. Frequency of major molecular responses to imatinib or interferon alfa plus cytarabine in newly diagnosed chronic myeloid leukemia. N Engl J Med. 2003;349:1423-1432. (Pubitemid 37211057)
14. Druker BJ, Guilhot F, O'Brien SG, et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med. 2006;355(23):2408-2417. (Pubitemid 44903745)
15. Rousselot P, Huguet F, Rea D, et al. Imatinib mesylate discontinuation in patients with chronic myelogenous leukemia in complete molecular remission for more than 2 years. Blood. 2007;109(1):58-60. (Pubitemid 46053043)
16. Mahon FX, Rea D, Guilhot J, et al. Discontinuation of imatinib in patients with chronic myeloid leukaemia who have maintained complete molecular remission for at least 2 years: the prospective, multicentre Stop Imatinib (STIM) trial. Lancet Oncol. 2010;11(11):1029-1035.
17. Graham SM, Jorgensen HG, Allan E, et al. Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood. 2002;99(1):319-325.
18. Bhatia R, Holtz M, Niu N, et al. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood. 2003;101(12):4701-4707. (Pubitemid 36857723)
19. Gratwohl A, Heim D. Current role of stem cell transplantation in chronic myeloid leukaemia. Best Pract Res Clin Haematol. 2009;22(3):431-443.
20. Champlin R, de Lima M, Kebriaei P, et al. Nonmyeloablative allogeneic stem cell transplantation for chronic myelogenous leukemia in the imatinib era. Clin Lymphoma Myeloma. 2009;9 Suppl 3:S261-265.
21. Krause DS, Van Etten RA. Adoptive immunotherapy of BCR-ABL-induced chronic myeloid leukemia-like myeloproliferative disease in a murine model. Blood. 2004;104(13):4236-4244. (Pubitemid 39620178)
22. Matte CC, Cormier J, Anderson BE, et al. Graft-versus-leukemia in a retrovirally induced murine CML model: mechanisms of T cell killing. Blood. 2004;103(11):4353-4361. (Pubitemid 38685384)
23. Li S, Ilaria RL, Million RP, Daley GQ, Van Etten RA. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med. 1999;189(9):1399-1412. (Pubitemid 29227526)
24. McClive PJ, Sinclair AH. Rapid DNA extraction and PCR-sexing of mouse embryos. Mol Reprod Dev. 2001;60(2):225-226. (Pubitemid 32847133)
25. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000;404(6744):193- 197. (Pubitemid 30154488)
26. Ildstad ST, Sachs DH. Reconstitution with syngeneic plus allogeneic or xenogeneic bone marrow leads to specific acceptance of allografts or xenografts. Nature. 1984;307(5947):168-170. (Pubitemid 14132903)
27. Lapidot T, Lubin I, Terenzi A, Faktorowich Y, Erlich P, Reisner Y. Enhancement of bone marrow allografts from nude mice into mismatched recipients by T cells void of graft-versus-host activity. Proc Natl Acad Sci U S A. 1990;87(12):4595-4599.
28. Matte-Martone C, Liu J, Jain D, McNiff J, Shlomchik WD. 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(7):3884-3892.
29. Pear WS, Miller JP, Xu L, et al. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood. 1998;92(10):3780-3792. (Pubitemid 28525205)
30. Jiang X, Stuible M, Chalandon Y, et al. Evidence for a positive role of SHIP in BCR-ABL-mediated transformation of primitive murine hematopoietic cells and in human chronic myeloid leukemia. Blood. 2003;102(8):2976-2984. (Pubitemid 37248873)
31. Hu Y, Swerdlow S, Duffy TM, Weinmann R, Lee FY, Li S. Targeting multiple kinase pathways in leukemic progenitors and stem cells is essential for improved treatment of Ph+ leukemia in mice. Proc Natl Acad Sci U S A. 2006;103(45):16870-16875. (Pubitemid 44737345)
32. Hu Y, Liu Y, Pelletier S, et al. Requirement of Src kinases Lyn, Hck and Fgr for BCR-ABL1-induced B-lymphoblastic leukemia but not chronic myeloid leukemia. Nat Genet. 2004;36(5):453-461. (Pubitemid 38620028)
33. Olavarria E, Siddique S, Griffiths MJ, et al. Post-transplantation imatinib as a strategy to postpone the requirement for immunotherapy in patients undergoing reduced-intensity allografts for chronic myeloid leukemia. Blood. 2007;110(13):4614-4617. (Pubitemid 351377831)
34. Savani BN, Montero A, Kurlander R, Childs R, Hensel N, Barrett AJ. Imatinib synergizes with donor lymphocyte infusions to achieve rapid molecular remission of CML relapsing after allogeneic stem cell transplantation. Bone Marrow Transplant. 2005;36(11):1009-1015. (Pubitemid 41741565)
35. Wolff NC, Veach DR, Tong WP, et al. PD166326, a novel tyrosine kinase inhibitor, has greater antileukemic activity than imatinib mesylate in a murine model of chronic myeloid leukemia. Blood. 2005;105(10):3995-4003. (Pubitemid 40656148)
36. Cook MA, Milligan DW, Fegan CD, et al. The impact of donor KIR and patient HLA-C genotypes on outcome following HLA-identical sibling hematopoietic stem cell transplantation for myeloid leukemia. Blood. 2004;103(4):1521-1526. (Pubitemid 38168673)
37. Elmaagacli AH, Ottinger H, Koldehoff M, et al. Reduced risk for molecular disease in patients with chronic myeloid leukemia after transplantation from a KIR-mismatched donor. Transplantation. 2005;79(12):1741-1747. (Pubitemid 40885275)
38. van der Meer A, Schaap NP, Schattenberg AV, van Cranenbroek B, Tijssen HJ, Joosten I. KIR2DS5 is associated with leukemia free survival after HLA identical stem cell transplantation in chronic myeloid leukemia patients. Mol Immunol. 2008;45(13):3631-3638.
39. Khouri IF, Keating M, Korbling, et al. Transplantlite: Induction of graft-versus-malignancy using fludarabine-based nonablative chemotherapy and allogeneic blood progenitor-cell transplantation as treatment for lymphoid malignancies. J Clin Oncol. 1998;16(8):2817-2824. (Pubitemid 28363047)
40. Sykes M, Preffer F, McAfee S, et al. Mixed lymphohematopoietic chimerism and graft-versuslymphoma effects after nonmyeloablative therapy and HLA-mismatched bone marrow transplantation. Lancet. 1999;353(9166):1755-1759. (Pubitemid 29240375)
41. Iizuka K, Scalzo AA, Xian H, Yokoyama WM. Regulation of the NK cell alloreactivity to bone marrow cells by the combination of the host NK gene complex and MHC haplotypes. J Immunol. 2008;180(5):3260-3267.
42. Porter DL, Hexner EO, Cooley S, Miller JS. Cellular adoptive immunotherapy after autologous and allogeneic hematopoietic stem cell transplantation. Cancer Treat Res. 2009;144:497-537.
43. Matte CC, Liu J, Cormier J, et al. Donor APCs are required for maximal GVHD but not for GVL. Nat Med. 2004;10(9):987-992. (Pubitemid 39273741)
44. Anderson BE, McNiff J, Yan J, et al. Memory CD4+ T cells do not induce graft-versus-host disease. J Clin Invest. 2003;112(1):101-108. (Pubitemid 38056381)
45. Teshima T, Ordemann R, Reddy P, et al. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat Med. 2002;8(6):575-581. (Pubitemid 34633434)
46. Hauch M, Gazzola MV, Small T, et al. Antileukemia potential of interleukin-2 activated natural killer cells after bone marrow transplantation for chronic myelogenous leukemia. Blood. 1990;75(11):2250-2262. (Pubitemid 20181179)
47. 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(10):3666-3672. (Pubitemid 41609209)
48. Savani BN, 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(10):2145-2152. (Pubitemid 47423804)
49. Ruggeri L, Capanni M, Urbani E, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097-2100. (Pubitemid 34229476)