NK-92: an ‘off-the-shelf therapeutic’ for adoptive natural killer cell-based cancer immunotherapy

Cancer Immunology, Immunotherapy

Volumn 65, Issue 4, 2016, Pages 485-492

  Suck, Garnet ^a   Odendahl, Marcus ^b   Nowakowska, Paulina ^c   Seidl, Christian ^c   Wels, Winfried S ^d   Klingemann, Hans G ^e   Tonn, Torsten ^b,c,f  

^a Institute for Transfusion Medicine   (Germany)

^b Red Cross Donor Service Sachsen   (Germany)

^c Institute for Transfusion Medicine and Immunohematology   (Germany)

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

^e NantKwest   (United States)

^f DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

CAR; Cellular immunotherapy; Clinical trial; NK cell line; NK 92; Tumor targeting

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; IMMUNOMODULATING AGENT; NK 92; UNCLASSIFIED DRUG;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN RECOGNITION; ARTICLE; AUTOLOGOUS HEMATOPOIETIC STEM CELL TRANSPLANTATION; CANCER CELL; CANCER IMMUNOTHERAPY; CRYOPRESERVATION; GOOD MANUFACTURING PRACTICE; HUMAN; NATURAL KILLER CELL; PRIORITY JOURNAL; T LYMPHOCYTE; ADOPTIVE IMMUNOTHERAPY; CELL CULTURE; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); CYTOTOXICITY; IMMUNOLOGY; NEOPLASMS; PROCEDURES; TRANSPLANTATION; TREATMENT OUTCOME; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; CLINICAL TRIALS AS TOPIC; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; NEOPLASMS; TREATMENT OUTCOME;

EID: 84946780179     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1761-x     Document Type: Article

References (54)

1. Klingemann HG, Martinson J (2004) Ex vivo expansion of natural killer cells for clinical applications. Cytotherapy 6:15–22
2. Suck G, Koh MB (2010) Emerging natural killer cell immunotherapies: large-scale ex vivo production of highly potent anticancer effectors. Hematol Oncol Stem Cell Ther 3:135–142
3. Childs RW, Berg M (2013) Bringing natural killer cells to the clinic: ex vivo manipulation. Hematol Am Soc Hematol Educ Progr 2013:234–246
4. 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
5. 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
6. 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
7. Maki G, Klingemann HG, Martinson JA, Tam YK (2001) Factors regulating the cytotoxic activity of the human natural killer cell line, nk-92. J Hematother Stem Cell Res 10:369–383
8. Luetke-Eversloh M, Killig M, Romagnani C (2013) Signatures of human nk cell development and terminal differentiation. Front Immunol 4:499
9. Matsuo Y, Drexler HG (2003) Immunoprofiling of cell lines derived from natural killer-cell and natural killer-like t-cell leukemia-lymphoma. Leuk Res 27:935–945
10. Cooley S, Xiao F, Pitt M, Gleason M, McCullar V, Bergemann TL, McQueen KL, Guethlein LA, Parham P, Miller JS (2007) A subpopulation of human peripheral blood nk cells that lacks inhibitory receptors for self-mhc is developmentally immature. Blood 110:578–586
11. Faure M, Long EO (2002) Kir2dl4 (cd158d), an nk cell-activating receptor with inhibitory potential. J Immunol 168:6208–6214
12. Pazmany L, Mandelboim O, Vales-Gomez M, Davis DM, Reyburn HT, Strominger JL (1996) Protection from natural killer cell-mediated lysis by hla-g expression on target cells. Science 274:792–795
13. Romanski A, Bug G, Becker S, Kampfmann M, Seifried E, Hoelzer D, Ottmann OG, Tonn T (2005) Mechanisms of resistance to natural killer cell-mediated cytotoxicity in acute lymphoblastic leukemia. Exp Hematol 33:344–352
14. Burshtyn DN, Scharenberg AM, Wagtmann N, Rajagopalan S, Berrada K, Yi T, Kinet JP, Long EO (1996) Recruitment of tyrosine phosphatase hcp by the killer cell inhibitor receptor. Immunity 4:77–85
15. Heidenreich S, ZuEulenburg C, Hildebrandt Y, Stubig T, Sierich H, Badbaran A, Eiermann TH, Binder TM, Kroger N (2012) Impact of the nk cell receptor lir-1 (ilt-2/cd85j/lilrb1) on cytotoxicity against multiple myeloma. Clin Dev immunol. 2012:652130
16. Suck G, Branch DR, Smyth MJ, Miller RG, Vergidis J, Fahim S, Keating A (2005) Khyg-1, a model for the study of enhanced natural killer cell cytotoxicity. Exp Hematol 33:1160–1171
17. 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
18. 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 Biol Blood Marrow Transplant 2:68–75
19. 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 4:2859–2868
20. Lowdell MW, Theocharous P (1997) “Less is more”: the role of purging in hematopoietic stem cell transplantation. Oncologist 2:268–274
21. Yahng SA, Yoon JH, Shin SH, Lee SE, Cho BS, Eom KS, Kim YJ, Lee S, Kim HJ, Min CK, Kim DW, Lee JW, Min WS, Park CW, Kim Y, Cho SG (2014) Influence of ex vivo purging with clinimacs cd34(+) selection on outcome after autologous stem cell transplantation in non-Hodgkin lymphoma. Br J Haematol 164:555–564
22. Bais S, Bartee E, Rahman MM, McFadden G, Cogle CR (2012) Oncolytic virotherapy for hematological malignancies. Adv Virol 2012:186512
23. Maki G, Tam YK, Berkahn L, Klingemann HG (2003) Ex vivo purging with nk-92 prior to autografting for chronic myelogenous leukemia. Bone Marrow Transplant 31:1119–1125
24. Maki G (2001) Ex vivo purging of stem cell autografts using cytotoxic cells. J Hematother Stem Cell Res 10:545–551
25. Klingemann HG (2013) Cellular therapy of cancer with natural killer cells-where do we stand? Cytotherapy 15:1185–1194
26. Tonn T, Seifried E (2006) Natural killer cells for the treatment of malignancies. Transfus Med Hemother 33:144–149
27. 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 15:1563–1570
28. 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 10:625–632
29. Tam YK, Miyagawa B, Ho VC, Klingemann HG (1999) Immunotherapy of malignant melanoma in a scid mouse model using the highly cytotoxic natural killer cell line nk-92. J Hematother 8:281–290
30. Whiteside TL, Griffin DL, Stanson J, Gooding W, McKenna D, Sumstad D, Kadidlo D, Gee A, Durett A, Lindblad R, Wood D, Styers D (2011) Shipping of therapeutic somatic cell products. Cytotherapy 13:201–213
31. Koepsell SA, Kadidlo DM, Fautsch S, McCullough J, Klingemann H, Wagner JE, Miller JS, McKenna DH Jr (2013) Successful “in-flight” activation of natural killer cells during long-distance shipping. Transfusion 53:398–403
32. Suck G, Branch DR, Aravena P, Mathieson M, Helke S, Keating A (2006) Constitutively polarized granules prime khyg-1 nk cells. Int Immunol 18:1347–1354
33. Suck G, Branch DR, Keating A (2006) Irradiated khyg-1 retains cytotoxicity: Potential for adoptive immunotherapy with a natural killer cell line. Int J Radiat Biol 82:355–361
34. Suck G, Tan SM, Chu S, Niam M, Vararattanavech A, Lim TJ, Koh MB (2011) Khyg-1 and nk-92 represent different subtypes of lfa-1-mediated nk cell adhesiveness. Front Biosci 3:166–178
35. Mallett CL, McFadden C, Chen Y, Foster PJ (2012) Migration of iron-labeled khyg-1 natural killer cells to subcutaneous tumors in nude mice, as detected by magnetic resonance imaging. Cytotherapy 14:743–751
36. Swift BE, Williams BA, Kosaka Y, Wang XH, Medin JA, Viswanathan S, Martinez-Lopez J, Keating A (2012) Natural killer cell lines preferentially kill clonogenic multiple myeloma cells and decrease myeloma engraftment in a bioluminescent xenograft mouse model. Haematologica 97:1020–1028
37. Yagita M, Huang CL, Umehara H, Matsuo Y, Tabata R, Miyake M, Konaka Y, Takatsuki K (2000) A novel natural killer cell line (khyg-1) from a patient with aggressive natural killer cell leukemia carrying a p53 point mutation. Leukemia 14:922–930
38. 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 365:725–733
39. Wieczorek A, Uharek L (2013) Genetically modified t cells for the treatment of malignant disease. Transfus Med Hemother 40:388–402
40. Bhat R, Watzl C (2007) Serial killing of tumor cells by human natural killer cells–enhancement by therapeutic antibodies. PLoS ONE 2:e326
41. Choi PJ, Mitchison TJ (2013) Imaging burst kinetics and spatial coordination during serial killing by single natural killer cells. Proc Natl Acad Sci USA 110:6488–6493
42. Boissel L, Betancur M, Lu W, Wels WS, Marino T, Van Etten RA, Klingemann H (2012) Comparison of mRNA and lentiviral based transfection of natural killer cells with chimeric antigen receptors recognizing lymphoid antigens. Leuk Lymphoma 53:958–965
43. Suck G (2006) Novel approaches using natural killer cells in cancer therapy. Semin Cancer Biol 16:412–418
44. Boissel L, Betancur M, Wels WS, Tuncer H, Klingemann H (2009) Transfection with mrna for cd19 specific chimeric antigen receptor restores nk cell mediated killing of cll cells. Leuk Res 33:1255–1259
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 57:411–423
46. Boissel L, Betancur-Boissel M, Lu W, Krause DS, Van Etten RA, Wels WS, Klingemann H (2013) Retargeting nk-92 cells by means of cd19- and cd20-specific chimeric antigen receptors compares favorably with antibody-dependent cellular cytotoxicity. Oncoimmunology 2:e26527
47. Miller JS (2013) Therapeutic applications: Natural killer cells in the clinic. Hematol Am Soc Hematol Educ Progr 2013:247–253
48. 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 100:1265–1273
49. Daldrup-Link HE, Meier R, Rudelius M, Piontek G, Piert M, Metz S, Settles M, Uherek C, Wels W, Schlegel J, Rummeny EJ (2005) In vivo tracking of genetically engineered, anti-her2/neu directed natural killer cells to her2/neu positive mammary tumors with magnetic resonance imaging. Eur Radiol 15:4–13
50. Meier R, Piert M, Piontek G, Rudelius M, Oostendorp RA, Senekowitsch-Schmidtke R, Henning TD, Wels WS, Uherek C, Rummeny EJ, Daldrup-Link HE (2008) Tracking of [18f]fdg-labeled natural killer cells to her2/neu-positive tumors. Nucl Med Biol 35:579–588
51. Schönfeld K, Sahm C, Zhang C, Naundorf S, Brendel C, Odendahl M, Nowakowska P, Bönig H, Köhl U, Kloess S, Köhler S, Holtgreve-Grez H, Jauch A, Schmidt M, Schubert R, Kühlcke K, Seifried E, Klingemann HG, Rieger MA, Tonn T, Grez M, Wels WS (2015) Selective inhibition of tumor growth by NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol Ther 23:330–338
52. Tam YK, Maki G, Miyagawa B, Hennemann B, Tonn T, Klingemann HG (1999) Characterization of genetically altered, interleukin 2-independent natural killer cell lines suitable for adoptive cellular immunotherapy. Hum Gene Ther 10:1359–1373
53. Reid GS, Bharya S, Klingemann HG, Schultz KR (2002) Differential killing of pre-b acute lymphoblastic leukaemia cells by activated nk cells and the nk-92 ci cell line. Clin Exp Immunol 129:265–271
54. Sahm C, Schonfeld K, Wels WS (2012) Expression of il-15 in nk cells results in rapid enrichment and selective cytotoxicity of gene-modified effectors that carry a tumor-specific antigen receptor. Cancer Immunol Immunother 61:1451–1461