Selection and expansion of natural killer cells for NK cell-based immunotherapy

Cancer Immunology, Immunotherapy

Volumn 65, Issue 4, 2016, Pages 477-484

  Becker, Petra S A ^a   Suck, Garnet ^b   Nowakowska, Paulina ^a   Ullrich, Evelyn ^c   Seifried, Erhard ^a   Bader, Peter ^c   Tonn, Torsten ^d   Seidl, Christian ^a  

^a Institute of Transfusion Medicine and Immunohematology   (Germany)

^b Institute for Transfusion Medicine   (Germany)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^d CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Hematopoietic stem cell transplantation; Immunotherapy; Killer cell immunoglobulin like receptor; Natural killer cells

Indexed keywords

CD137 LIGAND; CD69 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 2; INTERLEUKIN 21; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 2; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; OKT 3; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CANCER IMMUNOTHERAPY; CELL ACTIVATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL MEDIATED CYTOTOXICITY; CELL PROLIFERATION; CELL SELECTION; CELL SURVIVAL; EMBRYONIC STEM CELL; FEEDER CELL; GENE TRANSFER; GOOD MANUFACTURING PRACTICE; HUMAN; HUMAN EMBRYONIC STEM CELL; IN VITRO STUDY; LEUKAPHERESIS; LYMPHOKINE ACTIVATED KILLER CELL; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL (TOPIC); PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; UMBILICAL CORD BLOOD; ADOPTIVE IMMUNOTHERAPY; BIOLOGICAL MODEL; CELL CULTURE; CELL CULTURE TECHNIQUE; CYTOTOXICITY; DRUG EFFECTS; IMMUNOLOGY; PROCEDURES; TRANSPLANTATION;

CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; KILLER CELLS, NATURAL; MODELS, IMMUNOLOGICAL; RECEPTORS, KIR;

EID: 84955312560     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-016-1792-y     Document Type: Article

References (75)

1. Luetke-Eversloh M, Killig M, Romagnani C (2013) Signatures of human NK cell development and terminal differentiation. Front Immunol 4:499
2. Navarro F, Llano M, Bellon T, Colonna M, Geraghty DE, Lopez-Botet M (1999) The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur J Immunol 29:277–283
3. Moretta L, Pietra G, Montaldo E, Vacca P, Pende D, Falco M, Del Zotto G, Locatelli F, Moretta A, Mingari MC (2014) Human NK cells: from surface receptors to the therapy of leukemias and solid tumors. Front Immunol 5:87
4. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F, Martelli MF, Velardi A (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295:2097–2100
5. Locatelli F, Pende D, Mingari MC, Bertaina A, Falco M, Moretta A, Moretta L (2013) Cellular and molecular basis of haploidentical hematopoietic stem cell transplantation in the successful treatment of high-risk leukemias: role of alloreactive NK cells. Front Immunol 4:15
6. Aversa F, Martelli MF, Velardi A (2012) Haploidentical hematopoietic stem cell transplantation with a megadose T-cell-depleted graft: harnessing natural and adaptive immunity. Semin Oncol 39:643–652
7. Martelli MF, Di Ianni M, Ruggeri L, Pierini A, Falzetti F, Carotti A, Terenzi A, Reisner Y, Aversa F, Falini B, Velardi A (2014) “Designed” grafts for HLA-haploidentical stem cell transplantation. Blood 123:967–973
8. Hsu KC, Keever-Taylor CA, Wilton A, Pinto C, Heller G, Arkun K, O’Reilly RJ, Horowitz MM, Dupont B (2005) Improved outcome in HLA-identical sibling hematopoietic stem-cell transplantation for acute myelogenous leukemia predicted by KIR and HLA genotypes. Blood 105(12):4878–4884
9. Park S, Kim K, Jang JH, Kim SJ, Kim WS, Kang ES, Jung CW (2015) KIR alloreactivity based on the receptor-ligand model is associated with improved clinical outcomes of allogeneic hematopoietic stem cell transplantation: result of single center prospective study. Hum Immunol 76(9):636–643
10. Leung W, Iyengar R, Triplett B, Turner V, Behm FG, Holladay MS, Houston J, Handgretinger R (2005) Comparison of killer Ig-like receptor genotyping and phenotyping for selection of allogeneic blood stem cell donors. J Immunol 174(10):6540–6545
11. Cooley S, Weisdorf DJ, Guethlein LA, Klein JP, Wang T et al (2010) Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood 116:2411–2419
12. Venstrom JM, Dupont B, Hsu KC, Pittari G, Gooley TA, Chewning JH, Spellman S, Haagenson M, Gallagher MM, Malkki M, Petersdorf E (2014) Donor activating KIR2DS1 in leukemia. N Engl J Med 371(21):2042
13. Pittari G, Liu XR, Selvakumar A, Zhao Z, Merino E, Huse M, Chewning JH, Hsu KC, Dupont B (2013) NK cell tolerance of self-specific activating receptor KIR2DS1 in individuals with cognate HLA-C2 ligand. J Immunol 190(9):4650–4660
14. Cooley S, Trachtenberg E, Bergemann TL, Saeteurn K, Klein J, Le CT et al (2009) Donors with group B KIR haplotypes improve relapse-free survival after unrelated hematopoietic cell transplantation for acute myelogenous leukemia. Blood 113:726–732
15. Oevermann L, Michaelis SU, Mezger M, Lang P, Toporski J, Bertaina A, Zecca M, Moretta L, Locatelli F, Handgretinger R (2014) KIR B haplotype donors confer a reduced risk for relapse after haploidentical transplantation in children with ALL. Blood 124(17):2744–2747
16. Venstrom JM, Gooley TA, Spellman S, Pring J, Malkki M, Dupont B et al (2010) Donor activating KIR3DS1 is associated with decreased acute GvHD in unrelated allogeneic hematopoietic cell transplantation. Blood 115:3162–3165
17. Venstrom JM, Pittari G, Gooley TA, Chewning JH, Spellman S, Haagenson M, Gallagher MM, Malkki M, Petersdorf E, Dupont B, Hsu KC (2012) HLA-C-dependent prevention of leukemia relapse by donor activating KIR2DL1. N Engl J Med 367:805–816
18. Yawata M, Yawata N, Draghi M, Little AM, Partheniou F, Parham P (2006) Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med 203:633–645
19. Bari R, Rujkijyanont P, Sullivan E, Kang G, Turner V, Gan K, Leung W (2013) Effect of donor KIR2DL1 allelic polymorphism on the outcome of pediatric allogeneic hematopoietic stem-cell transplantation. J Clin Oncol 31(30):3782–3790
20. Foley B, Cooley S, Verneris MR, Pitt M, Curtsinger J, Luo X, Lopez-Verges S, Lanier LL, Weisdorf D, Miller JS (2012) Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 119:2665–2674
21. Green ML, Leisenring WM, Xie H, Walter RB, Mielcarek M, Sandmaier BM, Riddell SR, Boeckh M (2013) CMV reactivation after allogeneic HCT and relapse risk: evidence for early protection in acute myeloid leukemia. Blood 122:1316–1324
22. Zambello R, Teramo A, Barila G, Gattazzo C, Semenzato G (2014) Activating KIRs in chronic lymphoproliferative disorder of NK cells: protection from viruses and disease induction? Front Immunol 5:72
23. Burns LJ, Weisdorf DJ, DeFor TE, Vesole DH, Repka TL, Blazar BR et al (2003) IL-2-based immunotherapy after autologous transplantation for lymphoma and breast cancer induces immune activation and cytokine release: a phase I/II trial. Bone Marrow Transplant 32:177–186
24. Sakamoto N, Ishikawa T, Kokura S, Okayama T, Oka K, Ideno M, Sakai F, Kato A, Tanabe M, Enoki T, Mineno J, Naito Y, Itoh Y, Yoshikawa T (2015) Phase I clinical trial of autologous NK cell therapy using novel expansion method in patients with advanced digestive cancer. J Transl Med 13(1):277
25. Miller JS, Soignier Y, Panoskaltsis-Mortari A et al (2005) Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105(8):3051–3057
26. Ruggeri L, Mancusi A, Capanni M, Martelli MF, Velardi A (2011) Exploitation of alloreactive NK cells in adoptive immunotherapy of cancer. Curr Opin Immunol 17(2):211–217
27. Suck G, Oei VY, Linn YC, Ho SH, Chu S, Choong A, Niam M, Koh MB (2011) Interleukin-15 supports generation of highly potent clinical-grade natural killer cells in long-term cultures for targeting hematological malignancies. Exp Hematol 39:904–914
28. Brehm C, Huenecke S, Quaiser A, Esser R, Bremm M, Kloess S, Soerensen J, Kreyenberg H, Seidl C, Becker PS, Mühl H, Klingebiel T, Bader P, Passweg JR, Schwabe D, Koehl U (2011) 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 6(11):e27351
29. 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
30. Binyamin L, Alpaugh RK, Hughes TL, Lutz CT, Campbell KS, Weiner LM (2008) Blocking NK cell inhibitory self-recognition promotes antibody-dependent cellular cytotoxicity in a model of anti-lymphoma therapy. J Immunol 180:6392–6401
31. Nijhof IS, Lammerts van Bueren JJ, van Kessel B, Andre P, Morel Y, Lokhorst HM, van de Donk NW, Parren PW, Mutis T (2015) Daratumumab-mediated lysis of primary multiple myeloma cells is enhanced in combination with the human anti-KIR antibody IPH2102 and lenalidomide. Haematologica 100(2):263–268
32. Alderson KL, Sondel PM (2011) Clinical cancer therapy by NK cells via antibody-dependent cell-mediated cytotoxicity. J Biomed Biotechnol 2011:379123
33. Du J, Lopez-Verges S, Pitcher BN, Johnson J, Jung SH, Zhou L, Hsu K, Czuczman MS, Cheson B, Kaplan L, Lanier LL, Venstrom JM (2014) CALGB 150905 (Alliance): rituximab broadens the antilymphoma response by activating unlicensed NK cells. Cancer Immunol Res 2(9):878–889
34. Nijhof IS, Groen RW, Lokhorst HM, van Kessel B, Bloem AC, van Velzen J, de Jong-Korlaar R, Yuan H, Noort WA, Klein SK, Martens AC, Doshi P, Sasser K, Mutis T, van de Donk NW (2015) Upregulation of CD38 expression on multiple myeloma cells by all-trans retinoic acid improves the efficacy of daratumumab. Leukemia 29(10):2039–2049
35. 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(1):4–13
36. Monteverde M, Milano G, Strola G, Maffi M, Lattanzio L, Vivenza D, Tonissi F, Merlano M, Lo Nigro C (2015) The relevance of ADCC for EGFR targeting: a review of the literature and a clinically-applicable method of assessment in patients. Crit Rev Oncol Hematol 95(2):179–190
37. 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(5):355–361
38. 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(4):652–658
39. 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(4):535–544
40. 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
41. Arai S, Meagher R, Swearingen M et al (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
42. 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(10):e26527
43. Hermanson DL, Kaufman DS (2015) Utilizing chimeric antigen receptors to direct natural killer cell activity. Front Immunol 6:195
44. Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, Ettinghausen SE, Matory YL, Skibber JM, Shiloni E, Vetto JT et al (1985) Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med 313:1485–1492
45. Rosenberg SA (1988) The development of new immunotherapies for the treatment of cancer using interleukin-2. A review. Ann Surg 208:121–135
46. Rosenberg SA, Lotze MT, Yang JC, Aebersold PM, Linehan WM, Seipp CA, White DE (1989) Experience with the use of high-dose interleukin-2 in the treatment of 652 cancer patients. Ann Surg 210:474–484
47. Knorr DA, Bachanova V, Verneris MR, Miller JS (2014) Clinical utility of natural killer cells in cancer therapy and transplantation. Semin Immunol 26(2):161–172
48. Skrombolas D, Frelinger JG (2014) Challenges and developing solutions for increasing the benefits of IL-2 treatment in tumor therapy. Expert Rev Clin Immunol 10(2):207–217
49. Leong JW, Chase JM, Romee R, Schneider SE, Sullivan RP, Cooper MA, Fehniger TA (2014) Preactivation with IL-12, IL-15, and IL-18 induces CD25 and a functional high-affinity IL-2 receptor on human cytokine-induced memory-like natural killer cells. Biol Blood Marrow Transplant 20:463–473
50. Klingemann H (2015) Challenges of cancer therapy with natural killer cells. Cytotherapy 17(3):245–249
51. Childs RW, Berg M (2013) Bringing natural killer cells to the clinic: ex vivo manipulation. Hematology/the Education Program of the American Society of Hematology American Society of Hematology Education Program, pp 234–246
52. Koehl U, Brehm C, Huenecke S, Zimmermann SY, Kloess S, Bremm M, Ullrich E, Soerensen J, Quaiser A, Erben S, Wunram C, Gardlowski T, Auth E, Tonn T, Seidl C, Meyer-Monard S, Stern M, Passweg J, Klingebiel T, Bader P, Schwabe D, Esser R (2013) Clinical grade purification and expansion of NK cell products for an optimized manufacturing protocol. Front Oncol 3:118
53. Linn YC, Yong HX, Niam M, Lim TJ, Chu S, Choong A, Chuah C, Goh YT, Hwang W, Loh Y, Ng HJ, Suck G, Chan M, Koh M (2012) A phase I/II clinical trial of autologous cytokine-induced killer cells as adjuvant immunotherapy for acute and chronic myeloid leukemia in clinical remission. Cytotherapy 14(7):851–859
54. Ahn Yong-Oon, Kim Saerom, Kim Tae Min, Song Eun Young, Park Myoung Hee, Heo Dae Seog (2013) Irradiated and activated autologous PBMCs induce expansion of highly cytotoxic human NK cells in vitro. J Immunother 36:373–381
55. Lim O, Lee Y, Chung H, Her JH, Kang SM, Jung MY, Min B, Shin H, Kim TM, Heo DS, Hwang YK, Shin EC (2013) GMP-compliant, large-scale expanded allogeneic natural killer cells have potent cytolytic activity against cancer cells in vitro and in vivo. PLoS One 8(1):e53611
56. Lim SA, Kim TJ, Lee JE, Sonn CH, Kim K, Kim J, Choi JG, Choi IK, Yun CO, Kim JH, Yee C, Kumar V, Lee KM (2013) Ex vivo expansion of highly cytotoxic human NK cells by cocultivation with irradiated tumor cells for adoptive immunotherapy. Cancer Res 73(8):2598–25607
57. 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
58. Denman CJ, Senyukov VV, Somanchi SS, Phatarpekar PV, Kopp LM et al (2012) Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS One 7(1):e30264
59. Wang X, Lee DA, Wang Y, Wang L, Yao Y, Lin Z, Cheng J, Zhu S (2013) Membrane-bound interleukin-21 and CD137 ligand induce functional human natural killer cells from peripheral blood mononuclear cells through STAT-3 activation. Clin Exp Immunol 172(1):104–112
60. Baek HJ, Kim JS, Yoon M, Lee JJ, Shin MG, Ryang DW, Kook H, Kim SK, Cho D (2013) Ex vivo expansion of natural killer cells using cryopreserved irradiated feeder cells. Anticancer Res 33(5):2011–2019
61. Uhrberg M, Valiante NM, Shum BP, Shilling HG, Lienert-Weidenbach K, Corliss B, Tyan D, Lanier LL, Parham P (1997) Human diversity in killer cell inhibitory receptor genes. Immunity 7:753–763
62. Langenkamp U, Siegler U, Jörger S, Diermayr S, Gratwohl A, Kalberer CP, Wodnar-Filipowicz A (2009) Human acute myeloid leukemia CD34+CD38- stem cells are susceptible to allorecognition and lysis by single KIR-expressing natural killer cells. Haematologica 94(11):1590–1594
63. Siegler U, Meyer-Monard S, Jörger S, Stern M, Tichelli A, Gratwohl A, Wodnar-Filipowicz A, Kalberer CP (2010) 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 12(6):750–763
64. Schönberg K, Fischer JC, Kögler G, Uhrberg M (2011) Neonatal NK-cell repertoires are functionally, but not structurally, biased toward recognition of self HLA class I. Blood 117(19):5152–5156
65. Fluevano M, Domogala A, Blundell M, Jackson N, Pedroza-Pacheco I, Derniame S et al (2014) Frozen cord blood hematopoietic stem cells differentiate into higher numbers of functional natural killer cells in vitro that mobilized hematopoietic stem cells or freshly isolated cord blood hematopoietic stem cells. PLoS One 9:e87086
66. Pinho MJ, Punze M, Sousa M, Barros A (2011) Ex vivo differentiation of natural killer cells from human umbilical cord blood CD34+ progenitor cells. Cell Commun Adhes 18:45–55
67. Frias AM, Porada CD, Crapnell KB, Cabral JM, Zanjani ED, Almeida-Porada G (2008) Generation of functional natural killer and dendritic cells in a human stromal- based serum-free culture system designed for cord blood expansion. Exp Hematol 36:61–68
68. Spanholtz J, Preijers F, Tordoir M, Trilsbeek C, Paardekooper J, deWitte T et al (2011) Clinical-grade generation of active NK cells from cord blood hematopoietic progenitor cells for immunotherapy using a closed-system culture process. PLoS One 6:e20740
69. Spanholtz J, Tordoir M, Eissens D, Preijers F, van der Meer A, Joosten I et al (2010) High log-scale expansion of functional human natural killer cells from umbilical cord blood CD34-positive cells for adoptive cancer immunotherapy. PLoS One 5:e9221
70. Chouaib S, Pittari G, Nanbakhsh A, El Ayoubi H, Amsellem S, Bourhis JH, Spanholtz J (2014) Improving the outcome of leukemia by natural killer cell-based immunotherapeutic strategies. Front Immunol 5:95
71. Eguizabal C, Zenarruzabeitia O, Monge J, Santos S, Angel Vesga Maruri N, Arrieta A, Rinon M, Tamayo-Orbegozo E, Amo L, Larrucea S, Borrego F (2014) Natural killer cells for cancer immunotherapy: pluripotent stem cells-derived NK cells as an immunotherapeutic perspective. Front, Immunol Article 439
72. Woll PS, Grzywacz B, Tian X, Marcus RK, Knorr DA, Verneris MR et al (2009) Human embryonic stem cells differentiate into a homogeneous population of natural killer cells with potent in vivo antitumor activity. Blood 113:6094–6101
73. Woll PS, Martin CH, Miller JS, Kaufman DS (2005) Human embryonic stem cell-derived NK cells acquire functional receptors and cytolytic activity. J Immunol 175:5095–5103
74. Knorr DA, Bock A, Brentjens RJ, Kaufman DS (2013) Engineered human embryonic stem cell-derived lymphocytes to study in vivo trafficking and immunotherapy. Stem Cells Dev 22:1861–1869
75. Knorr DA, Ni Z, Hermanson D, Hexum MK, Bendzick L, Cooper LJ et al (2013) Clinical-scale derivation of natural killer cells from human pluripotent stem cells for cancer therapy. Stem Cells Transl Med 2:274–283