Disialoganglioside-specific human natural killer cells are effective against drug-resistant neuroblastoma

Cancer Immunology, Immunotherapy

Volumn 64, Issue 5, 2015, Pages 621-634

  Seidel, Diana ^a,d   Shibina, Anastasia ^b,d   Siebert, Nikolai ^a   Wels, Winfried S ^c   Reynolds, C Patrick ^d   Huebener, Nicole ^a,d,e   Lode, Holger N ^a  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^b Klinikum Frankfurt/Oder   (Germany)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

^d TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Chimeric antigen receptor; Natural killer cell; Neuroblastoma GD2; Single chain antibody

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; DISIALOGANGLIOSIDE; GANGLIOSIDE; INTERLEUKIN 2; UNCLASSIFIED DRUG; ANTIIDIOTYPIC ANTIBODY; GANGLIOSIDE, GD2; LYMPHOCYTE ANTIGEN RECEPTOR; SIALOGANGLIOSIDES; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; CANCER IMMUNOTHERAPY; CELL KILLING; CONTROLLED STUDY; CYTOTOXICITY; CYTOTOXICITY ASSAY; DOWN REGULATION; DRUG RESISTANT NEUROBLASTOMA; EFFECTOR CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; LYSIS; MOUSE; NATURAL KILLER CELL; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TARGET CELL; THERAPY EFFECT; TUMOR GROWTH; TUMOR XENOGRAFT; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BIOSYNTHESIS; CANCER TRANSPLANTATION; CELL LINE; DRUG RESISTANCE; GENETIC ENGINEERING; GENETICS; IMMUNOLOGY; NONOBESE DIABETIC MOUSE; PROCEDURES;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; DRUG RESISTANCE, NEOPLASM; FEMALE; GANGLIOSIDES; GENETIC ENGINEERING; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MICE; MICE, INBRED NOD; NEOPLASM TRANSPLANTATION; NEUROBLASTOMA; RECEPTORS, ANTIGEN; SINGLE-CHAIN ANTIBODIES;

EID: 84938423903     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1669-5     Document Type: Article

References (45)

1. Westermann F, Schwab M (2002) Genetic parameters of neuroblastomas. Cancer Lett 184:127–147
2. Maris JM, Hogarty MD, Bagatell R, Cohn SL (2007) Neuroblastoma. Lancet 369:2106–2120
3. van Noesel MM, Versteeg R (2004) Pediatric neuroblastomas: genetic and epigenetic ‘danse macabre’. Gene 325:1–15
4. Keshelava N, Seeger RC, Groshen S, Reynolds CP (1998) Drug resistance patterns of human neuroblastoma cell lines derived from patients at different phases of therapy. Cancer Res 58:5396–5405
5. Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, Shimada H, Grupp SA, Seeger R, Reynolds CP, Buxton A, Reisfeld RA, Gillies SD, Cohn SL, Maris JM, Sondel PM (2010) Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 363:1324–1334
6. Mujoo K, Cheresh DA, Yang HM, Reisfeld RA (1987) Disialoganglioside GD2 on human neuroblastoma cells: Target antigen for monoclonal antibody-mediated cytolysis and suppression of tumor growth. Cancer Res 47:1098–1104
7. Yang RK, Sondel PM (2010) Anti-GD2 strategy in the treatment of neuroblastoma. Drugs Future 35:665
8. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 17:189–220
9. Trinchieri G (1989) Biology of natural killer cells. Adv Immunol 47:187–376
10. Cullen SP, Martin SJ (2008) Mechanisms of granule-dependent killing. Cell Death Differ 15:251–262
11. Schmitz I, Kirchhoff S, Krammer PH (2000) Regulation of death receptor-mediated apoptosis pathways. Int J Biochem Cell Biol 32:1123–1136
12. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM (2000) In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci USA 97:2731–2736
13. Gong JH, Maki G, Klingemann HG (1994) Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia 8:652–658
14. Klingemann HG, Wong E, Maki G (1996) A cytotoxic NK-cell line (NK-92) for ex vivo purging of leukemia from blood. Biol Blood Marrow Transplant 2:68–75
15. Tam YK, Martinson JA, Doligosa K, Klingemann HG (2003) Ex vivo expansion of the highly cytotoxic human natural killer-92 cell-line under current good manufacturing practice conditions for clinical adoptive cellular immunotherapy. Cytotherapy 5:259–272
16. Yan Y, Steinherz P, Klingemann HG, Dennig D, Childs BH, McGuirk J, O’Reilly RJ (1998) Antileukemia activity of a natural killer cell line against human leukemias. Clin Cancer Res 4(11):2859–2868
17. Arai S, Meagher R, Swearingen M, Myint H, Rich E, Martinson J, Klingemann H (2008) Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: A phase I trial. Cytotherapy 10(6):625–632
18. Tonn T, Schwabe D, Klingemann HG, Becker S, Esser R, Koehl U, Suttorp M, Seifried E, Ottmann OG, Bug G (2013) Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy 15(12):1563–1570
19. Groh V, Wu J, Yee C, Spies T (2002) Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419:734–738
20. Lee JC, Lee KM, Kim DW, Heo DS (2004) Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol 172:7335–7340
21. Uherek C, Groner B, Wels W (2001) Chimeric antigen receptors for the retargeting of cytotoxic effector cells. J Hematother Stem Cell Res 10:523–534
22. Esser R, Muller T, Stefes D, Kloess S, Seidel D, Gillies SD, Aperlo-Iffland C, Huston JS, Uherek C, Schonfeld K, Tonn T, Huebener N, Lode HN, Koehl U, Wels WS (2012) NK cells engineered to express a GD2 -specific antigen receptor display built-in ADCC-like activity against tumour cells of neuroectodermal origin. J Cell Mol Med 16(3):569–581
23. Keshelava N, Zuo JJ, Chen P, Waidyaratne SN, Luna MC, Gomer CJ, Triche TJ, Reynolds CP (2001) Loss of p53 function confers high-level multidrug resistance in neuroblastoma cell lines. Cancer Res 61(16):6185–6193
24. Keshelava N, Davicioni E, Wan Z, Ji L, Sposto R, Triche TJ, Reynolds CP (2007) Histone deacetylase 1 gene expression and sensitization of multidrug-resistant neuroblastoma cell lines to cytotoxic agents by depsipeptide. J Natl Cancer Inst 99(14):1107–1119
25. Uherek C, Tonn T, Uherek B, Becker S, Schnierle B, Klingemann HG, Wels W (2002) Retargeting of natural killer-cell cytolytic activity to ErbB2-expressing cancer cells results in efficient and selective tumor cell destruction. Blood 100(4):1265–1273
26. Lode HN, Schmidt M, Seidel D, Huebener N, Brackrock D, Bleeke M, Reker D, Brandt S, Mueller HP, Helm C, Siebert N (2013) Vaccination with anti-idiotype antibody ganglidiomab mediates a GD(2)-specific anti-neuroblastoma immune response. Cancer Immunol Immunother 62(6):999–1010
27. Raffaghello L, Prigione I, Airoldi I, Camoriano M, Morandi F, Bocca P, Gambini C, Ferrone S, Pistoia V (2005) Mechanisms of immune evasion of human neuroblastoma. Cancer Lett 228(1–2):155–161
28. Farag SS, Fehniger TA, Ruggeri L, Velardi A, Caligiuri MA (2002) Natural killer cell receptors: new biology and insights into the graft-versus-leukemia effect. Blood 100:1935–1947
29. Papamichail M, Perez SA, Gritzapis AD, Baxevanis CN (2004) Natural killer lymphocytes: biology, development, and function. Cancer Immunol Immunother 53:176–186
30. Suck G (2006) Novel approaches using natural killer cells in cancer therapy. Semin Cancer Biol 16:412–418
31. Sutlu T, Alici E (2009) Natural killer cell-based immunotherapy in cancer: current insights and future prospects. J Intern Med 266:154–181
32. Ruggeri L, Mancusi A, Capanni M, Martelli MF, Velardi A (2005) Exploitation of alloreactive NK cells in adoptive immunotherapy of cancer. Curr Opin Immunol 17:211–217
33. Velardi A, Ruggeri L, Mancusi A, Aversa F, Christiansen FT (2009) Natural killer cell allorecognition of missing self in allogeneic hematopoietic transplantation: A tool for immunotherapy of leukemia. Curr Opin Immunol 21:525–530
34. Voskens CJ, Watanabe R, Rollins S, Campana D, Hasumi K, Mann DL (2010) Ex-vivo expanded human NK cells express activating receptors that mediate cytotoxicity of allogeneic and autologous cancer cell lines by direct recognition and antibody directed cellular cytotoxicity. J Exp Clin Cancer Res 29:134
35. Kloess S, Huenecke S, Piechulek D, Esser R, Koch J, Brehm C, Soerensen J, Gardlowski T, Brinkmann A, Bader P, Passweg J, Klingebiel T, Schwabe D, Koehl U (2010) IL-2-activated haploidentical NK cells restore NKG2D-mediated NK-cell cytotoxicity in neuroblastoma patients by scavenging of plasma MICA. Eur J Immunol 40(11):3255–3267
36. Altvater B, Landmeier S, Pscherer S, Temme J, Schweer K, Kailayangiri S, Campana D, Juergens H, Pule M, Rossig C (2009) 2B4 (CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin Cancer Res 15(15):4857–4866
37. Imai C, Iwamoto S, Campana D (2005) Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood 106:376–383
38. Liu Y, Wu HW, Sheard MA, Sposto R, Somanchi SS, Cooper LJ, Lee DA, Seeger RC (2013) Growth and activation of natural killer cells ex vivo from children with neuroblastoma for adoptive cell therapy. Clin Cancer Res 19(8):2132–2143
39. Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, Eldridge P, Leung WH, Campana D (2009) Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res 69(9):4010–4017
40. Benjamin JE, Gill S, Negrin RS (2010) Biology and clinical effects of natural killer cells in allogeneic transplantation. Curr Opin Oncol 22(2):130–137
41. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia Frassoni F, Aversa F, Martelli MF, Velardi A (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295(5562):2097–2100
42. Campbell KS, Hasegawa J (2013) Natural killer cell biology: An update and future directions. J Allergy Clin Immunol 132(3):536–544
43. Porter DL, Levine BL, Kalos M, Bagg A, June CH (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365(8):725–733
44. Tonn T, Becker S, Esser R, Schwabe D, Seifried E (2001) Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92. J Hematother Stem Cell Res 10:535–544
45. Muller T, Uherek C, Maki G, Chow KU, Schimpf A, Klingemann HG, Tonn T, Wels WS (2008) Expression of a CD20-specific chimeric antigen receptor enhances cytotoxic activity of NK cells and overcomes NK-resistance of lymphoma and leukemia cells. Cancer Immunol Immunother 57(3):411–423