Central nervous system acute lymphoblastic leukemia: Role of natural killer cells

Blood

Volumn 125, Issue 22, 2015, Pages 3420-3431

  Frishman Levy, Liron ^a,b   Shemesh, Avishai ^c   Bar Sinai, Allan ^d   Ma, Chao ^e   Ni, Zhenya ^e   Frenkel, Shahar ^f   Muench, Vera ^g   Bruckmueller, Hilke ^h   Vokuhl, Christian ^h   Debatin, Klaus Michael ^g   Eckert, Cornelia ⁱ   Stanulla, Martin ^j   Schrappe, Martin ^h   Campbell, Kerry S ^k   Loewenthal, Ron ^a   Schewe, Denis M ^h   Hochman, Jacob ^d   Meyer, Lueder H ^g   Kaufman, Dan ^e   Cario, Gunnar ^h   Porgador, Angel ^c   Izraeli, Shai ^a,b   more..

^a SHEBA MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^f HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^g UNIVERSITY HOSPITAL ULM   (Germany)

^h UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

ⁱ CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^j HANNOVER MEDICAL SCHOOL   (Germany)

^k FOX CHASE CANCER CENTER   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL KILLER CELL RECEPTOR NKG2D;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B CELL LEUKEMIA; BONE MARROW; CANCER RISK; CELL ACTIVATION; CELL KILLING; CENTRAL NERVOUS SYSTEM LEUKEMIA; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HEMATOLOGIC MALIGNANCY; HUMAN; HUMAN CELL; LEUKEMIA RELAPSE; LYMPHOBLAST; MALE; MOUSE; NATURAL KILLER CELL; NOD SCID MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CENTRAL NERVOUS SYSTEM TUMOR; IMMUNOLOGY; JURKAT CELL LINE; METABOLISM; MORTALITY; NEWBORN; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM NEOPLASMS; HUMANS; INTERLEUKIN-15; JURKAT CELLS; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA;

EID: 84930941932     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-08-595108     Document Type: Article

References (73)

1. Laningham FH, Kun LE, Reddick WE, Ogg RJ, Morris EB, Pui CH. Childhood central nervous system leukemia: historical perspectives, current therapy, and acute neurological sequelae. Neuroradiology. 2007;49(11):873-888.
2. Aur RJ, Simone J, Hustu HO, et al. Central nervous system therapy and combination chemotherapy of childhood lymphocytic leukemia. Blood. 1971;37(3):272-281.
3. Silverman LB, Declerck L, Gelber RD, et al. Results of Dana-Farber Cancer Institute Consortium protocols for children with newly diagnosed acute lymphoblastic leukemia (1981-1995). Leukemia. 2000;14(12):2247-2256.
4. Schrappe M, Camitta B, Pui CH, et al. Long-term results of large prospective trials in childhood acute lymphoblastic leukemia. Leukemia. 2000; 14(12):2193-2194.
5. Clarke M, Gaynon P, Hann I, et al; Childhood ALL Collaborative Group. CNS-directed therapy for childhood acute lymphoblastic leukemia: Childhood ALL Collaborative Group overview of 43 randomized trials. J Clin Oncol. 2003;21(9): 1798-1809.
6. Vagace JM, de la Maya MD, Caceres-Marzal C, Gonzalez de Murillo S, Gervasini G. Central nervous system chemotoxicity during treatment of pediatric acute lymphoblastic leukemia/lymphoma. Crit Rev Oncol Hematol. 2012;84(2): 274-286.
7. Butler RW, Haser JK. Neurocognitive effects of treatment for childhood cancer. Ment Retard Dev Disabil Res Rev. 2006;12(3):184-191.
8. Pui CH, Cheng C, Leung W, et al. Extended follow-up of long-term survivors of childhood acute lymphoblastic leukemia. N Engl J Med. 2003; 349(7):640-649.
9. Genschaft M, Huebner T, Plessow F, et al. Impact of chemotherapy for childhood leukemia on brain morphology and function. PLoS ONE. 2013;8(11): e78599.
10. Lange BJ, Bostrom BC, Cherlow JM, et al; Children's Cancer Group. Double-delayed intensification improves event-free survival for children with intermediate-risk acute lymphoblastic leukemia: a report from the Children's Cancer Group. Blood. 2002;99(3): 825-833.
11. Bostrom BC, Sensel MR, Sather HN, et al; Children's Cancer Group. Dexamethasone versus prednisone and daily oral versus weekly intravenous mercaptopurine for patients with standard-risk acute lymphoblastic leukemia: a report from the Children's Cancer Group. Blood. 2003;101(10):3809-3817.
12. Hutchinson RJ, Gaynon PS, Sather H, et al; Children's Cancer Group/Children's Oncology Group. Intensification of therapy for children with lower-risk acute lymphoblastic leukemia: longterm follow-up of patients treated on Children's Cancer Group Trial 1881. J Clin Oncol. 2003; 21(9):1790-1797.
13. Hagedorn N, Acquaviva C, Fronkova E, et al; Resistant Disease Committee of the International BFM study group. Submicroscopic bone marrow involvement in isolated extramedullary relapses in childhood acute lymphoblastic leukemia: a more precise definition of "isolated" and its possible clinical implications, a collaborative study of the Resistant Disease Committee of the International BFM study group. Blood. 2007;110(12): 4022-4029.
14. Parker C, Waters R, Leighton C, et al. Effect of mitoxantrone on outcome of children with first relapse of acute lymphoblastic leukaemia (ALL R3): an open-label randomised trial. Lancet. 2010; 376(9757):2009-2017.
15. Krishnan S, Wade R, Moorman AV, et al. Temporal changes in the incidence and pattern of central nervous system relapses in children with acute lymphoblastic leukaemia treated on four consecutive Medical Research Council trials, 1985-2001. Leukemia. 2010;24(2):450-459.
16. Holland M, Castro FV, Alexander S, et al. RAC2, AEP, and ICAM1 expression are associated with CNS disease in a mouse model of pre-B childhood acute lymphoblastic leukemia. Blood. 2011;118(3):638-649.
17. Cario G, Izraeli S, Teichert A, et al. High interleukin-15 expression characterizes childhood acute lymphoblastic leukemia with involvement of the CNS. J Clin Oncol. 2007;25(30):4813-4820.
18. Döbbeling U, Dummer R, Laine E, Potoczna N, Qin JZ, Burg G. Interleukin-15 is an autocrine/paracrine viability factor for cutaneous T-cell lymphoma cells. Blood. 1998;92(1):252-258.
19. Qin JZ, Zhang CL, Kamarashev J, Dummer R, Burg G, Döbbeling U. Interleukin-7 and interleukin-15 regulate the expression of the bcl-2 and c-myb genes in cutaneous T-cell lymphoma cells. Blood. 2001;98(9):2778-2783.
20. Wu S, Fischer L, Gökbuget N, et al. Expression of interleukin 15 in primary adult acute lymphoblastic leukemia. Cancer. 2010;116(2):387-392.
21. Yang JJ, Cheng C, Yang W, et al. Genome-wide interrogation of germline genetic variation associated with treatment response in childhood acute lymphoblastic leukemia. JAMA. 2009; 301(4):393-403.
22. Williams MT, Yousafzai Y, Cox C, et al. Interleukin-15 enhances cellular proliferation and upregulates CNS homing molecules in pre-B acute lymphoblastic leukemia. Blood. 2014; 123(20):3116-3127.
23. Lanier LL. NK cell receptors. Annu Rev Immunol. 1998;16:359-393.
24. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu Rev Immunol. 2013;31:227-258.
25. Carson WE, Fehniger TA, Haldar S, et al. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J Clin Invest. 1997;99(5):937-943.
26. Cooper MA, Bush JE, Fehniger TA, et al. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood. 2002; 100(10):3633-3638.
27. Fehniger TA, Caligiuri MA. Interleukin 15: biology and relevance to human disease. Blood. 2001; 97(1):14-32.
28. Carson WE, Giri JG, Lindemann MJ, et al. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J Exp Med. 1994;180(4):1395-1403.
29. Kobayashi H, Dubois S, Sato N, et al. Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance. Blood. 2005;105(2):721-727.
30. Mrózek E, Anderson P, Caligiuri MA. Role of interleukin-15 in the development of human CD561 natural killer cells from CD341 hematopoietic progenitor cells. Blood. 1996;87(7): 2632-2640.
31. Szczepanski MJ, Szajnik M, Welsh A, Foon KA, Whiteside TL, Boyiadzis M. Interleukin-15 enhances natural killer cell cytotoxicity in patients with acute myeloid leukemia by upregulating the activating NK cell receptors. Cancer Immunol Immunother. 2010;59(1):73-79.
32. Zhang C, Zhang J, Niu J, Zhang J, Tian Z. Interleukin-15 improves cytotoxicity of natural killer cells via up-regulating NKG2D and cytotoxic effector molecule expression as well as STAT1 and ERK1/2 phosphorylation. Cytokine. 2008; 42(1):128-136.
33. Sutherland CL, Rabinovich B, Chalupny NJ, Brawand P, Miller R, Cosman D. ULBPs, human ligands of the NKG2D receptor, stimulate tumor immunity with enhancement by IL-15. Blood. 2006;108(4):1313-1319.
34. Hochman J, Katz A, Levy E, Eshel S. Substrate-adhering lymphoid cells show impaired tumorigenicity and increased immunogenicity. Nature. 1981;290(5803):248-249.
35. Hochman J, Levy E, Mador N, Gottesman MM, Shearer GM, Okon E. Cell adhesiveness is related to tumorigenicity in malignant lymphoid cells. J Cell Biol. 1984;99(4 Pt 1):1282-1288.
36. Bock AM, Knorr D, Kaufman DS. Development, expansion, and in vivo monitoring of human NK cells from human embryonic stem cells (hESCs) and and induced pluripotent stem cells (iPSCs). J Vis Exp. 2013;(74):e50337.
37. Bloushtain N, Qimron U, Bar-Ilan A, et al. Membrane-associated heparan sulfate proteoglycans are involved in the recognition of cellular targets by NKp30 and NKp46. J Immunol. 2004;173(4):2392-2401.
38. Hecht ML, Rosental B, Horlacher T, et al. Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J Proteome Res. 2009;8(2):712-720.
39. Cerwenka A, Bakker AB, McClanahan T, et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity. 2000;12(6):721-727.
40. Rosental B, Brusilovsky M, Hadad U, et al. Proliferating cell nuclear antigen is a novel inhibitory ligand for the natural cytotoxicity receptor NKp44. J Immunol. 2011;187(11): 5693-5702.
41. Assaf N, Hasson T, Hoch-Marchaim H, et al. An experimental model for infiltration of malignant lymphoma to the eye and brain. Virchows Arch. 1997;431(6):459-467.
42. Hochman J, Assaf N, Deckert-Schlüter M, Wiestler OD, Pe'er J. Entry routes of malignant lymphoma into the brain and eyes in a mouse model. Cancer Res. 2001;61(13):5242-5247.
43. Kaikov Y. Optic nerve head infiltration in acute leukemia in children: an indication for emergency optic nerve radiation therapy. Med Pediatr Oncol. 1996;26(2):101-104.
44. Russo V, Scott IU, Querques G, Stella A, Barone A, Delle Noci N. Orbital and ocular manifestations of acute childhood leukemia: clinical and statistical analysis of 180 patients. Eur J Ophthalmol. 2008;18(4):619-623.
45. Eckhoff SM, Queudeville M, Debatin KM, Meyer LH. A novel B cell precursor ALL cell line (018Z) with prominent neurotropism and isolated CNS leukemia in a NOD/SCID/huALL xenotransplantation model. Blood. 2009;114(22): 652-652.
46. Siegler U, Kalberer CP, Nowbakht P, Sendelov S, Meyer-Monard S, Wodnar-Filipowicz A. Activated natural killer cells from patients with acute myeloid leukemia are cytotoxic against autologous leukemic blasts in NOD/SCID mice. Leukemia. 2005;19(12):2215-2222.
47. Shultz LD, Lyons BL, Burzenski LM, et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol. 2005;174(10):6477-6489.
48. Meyer LH, Eckhoff SM, Queudeville M, et al. Early relapse in ALL is identified by time to leukemia in NOD/SCID mice and is characterized by a gene signature involving survival pathways. Cancer Cell. 2011;19(2):206-217.
49. Krause S, Pfeiffer C, Strube S, et al. Mer tyrosine kinase promotes the survival of t(1;19) positive acute lymphoblastic leukemia (ALL) in the central nervous system (CNS). Blood. 2015;125(5): 820-830.
50. Jeha S, Pei D, Raimondi SC, et al. Increased risk for CNS relapse in pre-B cell leukemia with the t(1;19)/TCF3-PBX1. Leukemia. 2009;23(8): 1406-1409.
51. de Smith AJ, Walsh KM, Ladner MB, et al. The role of KIR genes and their cognate HLA class I ligands in childhood acute lymphoblastic leukemia. Blood. 2014;123(16):2497-2503.
52. Moretta A, Bottino C, Vitale M, et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol. 2001;19:197-223.
53. Coudert JD, Held W. The role of the NKG2D receptor for tumor immunity. Semin Cancer Biol. 2006;16(5):333-343.
54. Eagle RA, Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol. 2007; 7(9):737-744.
55. Shibuya A, Campbell D, Hannum C, et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity. 1996;4(6):573-581.
56. Torelli GF, Peragine N, Raponi S, et al. Recognition of adult and pediatric acute lymphoblastic leukemia blasts by natural killer cells. Haematologica. 2014;99(7):1248-1254.
57. Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L. Thermal-and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS ONE. 2011;6(2):e16899.
58. Song H, Kim J, Cosman D, Choi I. Soluble ULBP suppresses natural killer cell activity via down-regulating NKG2D expression. Cell Immunol. 2006;239(1):22-30.
59. Kübler A, Woiterski J, Witte KE, et al. Both mature KIR1 and immature KIR-NK cells control pediatric acute B-cell precursor leukemia in NOD. Cg-Prkdcscid IL2rgtmWjl/Sz mice. Blood. 2014; 124(26):3914-3923.
60. Leung W, Iyengar R, Turner V, et al. Determinants of antileukemia effects of allogeneic NK cells. J Immunol. 2004;172(1):644-650.
61. 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.
62. Ruggeri L, Mancusi A, Burchielli E, et al. NK cell alloreactivity and allogeneic hematopoietic stem cell transplantation. Blood Cells Mol Dis. 2008; 40(1):84-90.
63. Pfeiffer MM, Feuchtinger T, Teltschik HM, et al. Reconstitution of natural killer cell receptors influences natural killer activity and relapse rate after haploidentical transplantation of T-and B-cell depleted grafts in children. Haematologica. 2010;95(8):1381-1388.
64. Zhou H, Bao X, Wu X, et al. Donor selection for killer immunoglobulin-like receptors B haplotype of the centromeric motifs can improve the outcome after HLA-identical sibling hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2014;20(1):98-105.
65. Oevermann L, Michaelis SU, Mezger M, et al. KIR B haplotype donors confer a reduced risk for relapse after haploidentical transplantation in children with ALL. Blood. 2014;124(17): 2744-2747.
66. Fei F, Lim M, George AA, et al. Cytotoxicity of CD56-positive lymphocytes against autologous B-cell precursor acute lymphoblastic leukemia cells. Leukemia. 2015;29(4):788-797.
67. Jardine L, Hambleton S, Bigley V, Pagan S, Wang XN, Collin M. Sensitizing primary acute lymphoblastic leukemia to natural killer cell recognition by induction of NKG2D ligands. Leuk Lymphoma. 2013;54(1):167-173.
68. Peragine N, Torelli GF, Mariglia P, et al. Immunophenotypic and functional characterization of ex vivo expanded natural killer cells for clinical use in acute lymphoblastic leukemia patients. Cancer Immunol Immunother. 2015;64(2):201-211.
69. Satwani P, Bavishi S, Saha A, et al. Upregulation of NKG2D ligands in acute lymphoblastic leukemia and non-Hodgkin lymphoma cells by romidepsin and enhanced in vitro and in vivo natural killer cell cytotoxicity [published online May 20, 2014 ahead of print]. Cytotherapy. doi:10.1016/j.jcyt.2014.03.008.
70. Torelli GF, Guarini A, Maggio R, Alfieri C, Vitale A, Foà R. Expansion of natural killer cells with lytic activity against autologous blasts from adult and pediatric acute lymphoid leukemia patients in complete hematologic remission. Haematologica. 2005;90(6):785-792.
71. Almalte Z, Samarani S, Iannello A, et al. Novel associations between activating killer-cell immunoglobulin-like receptor genes and childhood leukemia. Blood. 2011;118(5): 1323-1328.
72. Lühl NC, Zirngibl F, Dorneburg C, et al. Attenuated measles virus controls pediatric acute B-lineage lymphoblastic leukemia in NOD/SCID mice. Haematologica. 2014;99(6):1050-1061.
73. Queudeville M, Seyfried F, Eckhoff SM, et al. Rapid engraftment of human ALL in NOD/SCID mice involves deficient apoptosis signaling. Cell Death Dis. 2012;3:e364.