Harnessing natural killer cells engineering for cancer immunotherapy
DOI:
https://doi.org/10.47611/jsrhs.v13i2.6431Keywords:
immunotherapy, cell engineering, NK cells, CAR-NK, non-viral transfection, viral vector transductionAbstract
The use of genetically modified immune cells for cancer therapy is one of the most significant achievements in biotechnology in recent years. Although currently approved cell therapies are dominated by CAR-T cells, natural killer (NK) cells, with their unique cancer killing properties and safety of use, set the stage for the development of more convenient allogeneic therapies. Herein, we reviewed the challenges and strategies in harnessing NK cells for cancer immunotherapy. Various sources for NK cell acquisition are discussed, and genetic engineering methods, including retroviral vectors, lentiviral vectors, adeno-associated virus (AAV) vectors, and non-viral transfection, are explored. NK cells have the potential to address limitations associated with CAR-T therapy, and the paper addresses the need for innovative solutions to overcome technical hurdles associated with NK cell immunotherapy.
Downloads
References or Bibliography
Araki H, Yoshinaga K, Boccuni P, Zhao Y, Hoffman R, Mahmud N. Chromatin-Modifying Agents Permit Human Hematopoietic Stem Cells to Undergo Multiple Cell Divisions While Retaining Their Repopulating Potential. Blood 2007 109:3570–8. DOI: 10.1182/blood-2006-09-044974.
Bachanova V, Burns LJ, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lindgren BR, et al. Allogeneic natural killer cells for refractory lymphoma. Cancer Immunol Immunother. 2010;59:1739–44. DOI: 10.1007/s00262-010-0905-3.
Bari R, Granzin M, Tsang KS, Roy A, Krueger W, Orentas R, Schneider D, Pfeifer R, Moeker N, Verhoeyen E, Dropulic B, Leung W. A Distinct Subset of Highly Proliferative and Lentiviral Vector (LV)-Transducible NK Cells Define a Readily Engineered Subset for Adoptive Cellular Therapy. Front Immunol. 2019 Aug 22;10:2001. DOI: 10.3389/fimmu.2019.02001.
Boissel L, Betancur M, Lu W, Wels WS, Marino T, Van Etten RA, Klingemann H. Comparison of mRNA and lentiviral based transfection of natural killer cells with chimeric antigen receptors recognizing lymphoid antigens. Leuk Lymphoma. 2012 May;53(5):958-65. DOI: 10.3109/10428194.2011.639659.
Büning H, Srivastava A. Capsid Modifications for Targeting and Improving the Efficacy of AAV Vectors. Mol Ther Methods Clin Dev. 2019 12:248-265. DOI: 10.1016/j.omtm.2018.12.006.
Burdett T, Nuseibeh S. Changing trends in the development of AAV-based gene therapies: a meta-analysis of past and present therapies. Gene Ther. 2023 Apr;30(3-4):323-335. DOI: 10.1038/s41434-022-00306-2.
Cepko C, Pear W. Overview of the retrovirus transduction system. Curr Protoc Mol Biol. 2001 May;Chapter 9:Unit9.9. DOI: 10.1002/0471142727.mb0909s00.
Chen Y, You F, Jiang L, Li J, Zhu X, Bao Y, et al. Gene-Modified NK-92MI Cells Expressing a Chimeric CD16-BB-Zeta or CD64-BB-Zeta Receptor Exhibit Enhanced Cancer-Killing Ability in Combination With Therapeutic Antibody. Oncotarget 2017 8:37128–39. DOI: 10.18632/oncotarget.16778.
Childs RW, Carlsten M. Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: the force awakens. Nat Rev Drug Discov. 2015 Jul;14(7):487-98. DOI: 10.1038/nrd4591.
Chin DS, Lim CSY, Nordin F, Arifin N, Jun TG. Antibody-Dependent Cell-Mediated Cytotoxicity Through Natural Killer (NK) Cells: Unlocking NK Cells for Future Immunotherapy. Curr Pharm Biotechnol. 2022;23(4):552-578. DOI: 10.2174/1389201023666220223150227.
Chiossone, L., Dumas, P. Y., Vienne, M. & Vivier, E. Natural killer cells and other innate lymphoid cells in cancer. Nat. Rev. Immunol. 2018 18, 671–688. DOI: 10.1038/s41577-018-0061-z.
Cichocki F, Bjordahl R, Gaidarova S, Mahmood S, Abujarour R, Wang H, et al. iPSC-derived NK cells maintain high cytotoxicity and enhance in vivo tumor control in concert with T cells and anti-PD-1 therapy. Sci Transl Med. 2020 12(568): eaaz5618. DOI: 10.1126/scitranslmed.aaz5618.
Colamartino ABL, Lemieux W, Bifsha P, Nicoletti S, Chakravarti N, Sanz J, Roméro H, Selleri S, Béland K, Guiot M, Tremblay-Laganière C, Dicaire R, Barreiro L, Lee DA, Verhoeyen E, Haddad E. Efficient and Robust NK-Cell Transduction With Baboon Envelope Pseudotyped Lentivector. Front Immunol. 2019 Dec 16;10:2873. DOI: 10.3389/fimmu.2019.02873.
Eyquem J, Mansilla-Soto J, Giavridis T, van der Stegen SJ, Hamieh M, Cunanan KM, Odak A, Gönen M, Sadelain M. Targeting a CAR to the TRAC locus with CRISPR/Cas9 enhances tumour rejection. Nature. 2017 Mar 2;543(7643):113-117. DOI: 10.1038/nature21405.
Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, Eldridge P, Leung WH, Campana D. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 2009 May 1;69(9):4010-7. DOI: 10.1158/0008-5472.CAN-08-3712.
Gargett T, Brown MP. The inducible caspase-9 suicide gene system as a ‘safety switch’ to limit on-target, off-tumor toxicities of chimeric antigen receptor T-cells. Front Pharmacol. 2014;5. DOI: 10.3389/fphar.2014.00126.
Gill S, Olson JA, Negrin RS. Natural killer cells in allogeneic transplantation: effect on engraftment, graft-versus-tumor, and graft-versus-host responses. Biol Blood Marrow Transplant 2009 15:765–76. DOI: 10.1016/j.bbmt.2009.04.006.
Gong JH, Maki G, Klingemann HG. Characterization of a human cell line (NK-92) with phenotypical and functional characteristics of activated natural killer cells. Leukemia. 1994 8(4):652–8. DOI: 10.1038/bjc.1994.411.
Graham C, Jozwik A, Pepper A, Benjamin R. Allogeneic CAR-T cells. More than ease of access? Cells. 2018;7:155. DOI: 10.3390/cells7100155.
Guven H, Konstantinidis KV, Alici E, Aints A, Abedi-Valugerdi M, Christensson B, Ljunggren HG, Dilber MS. Efficient gene transfer into primary human natural killer cells by retroviral transduction. Exp Hematol. 2005 Nov;33(11):1320-8. DOI: 10.1016/j.exphem.2005.07.015.
Han J, Chu J, Keung Chan W, Zhang J, Wang Y, Cohen JB, et al. CAR-engineered NK cells targeting wild-type EGFR and EGFRvIII enhance killing of glioblastoma and patient-derived glioblastoma stem cells. Sci Rep. 2015 5:1–13. DOI: 10.1038/srep11483.
Haraguchi T, Koujin T, Shindo T, Bilir Ş, Osakada H, Nishimura K, Hirano Y, Asakawa H, Mori C, Kobayashi S, Okada Y, Chikashige Y, Fukagawa T, Shibata S, Hiraoka Y. Transfected plasmid DNA is incorporated into the nucleus via nuclear envelope reformation at telophase. Commun Biol. 2022 Jan 20;5(1):78. DOI: 10.1038/s42003-021-02664-3.
Herrera L, Santos S, Vesga MA, Anguita J, Martin-Ruiz I, Carrascosa T, et al. Adult Peripheral Blood and Umbilical Cord Blood NK Cells Are Good Sources for Effective CAR Therapy Against CD19 Positive Leukemic Cells. Sci Rep 2019 9:18729. DOI: 10.1038/s41598-019-55106-2.
Huang Q, Huang M, Meng F, Sun R. Activated Pancreatic Stellate Cells Inhibit NK Cell Function in the Human Pancreatic Cancer Microenvironment. Cell Mol Immunol. 2019 Jan;16(1):87-9. DOI: 10.1038/s41423-018-0027-0.
Hung KL, Meitlis I, Hale M, Chen CY, Singh S, Jackson SW, Miao CH, Khan IF, Rawlings DJ, James RG. Engineering Protein-Secreting Plasma Cells by Homology-Directed Repair in Primary Human B Cells. Mol Ther. 2018 Feb 7;26(2):456-467. DOI: 10.1016/j.ymthe.2017.12.018.
Imai C, Iwamoto S, Campana D. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood. 2005 Jul 1;106(1):376-83. DOI: 10.1182/blood-2004-12-4797.
Ingegnere T, Mariotti FR, Pelosi A, Quintarelli C, De Angelis B, Tumino N, Besi F, Cantoni C, Locatelli F, Vacca P, Moretta L. Human CAR NK Cells: A New Non-viral Method Allowing High Efficient Transfection and Strong Tumor Cell Killing. Front Immunol. 2019 Apr 30;10:957. DOI: 10.3389/fimmu.2019.00957.
June CH, O'Connor RS, Kawalekar OU, Ghassemi S, Milone MC. CAR T cell immunotherapy for human cancer. Science. 2018 Mar 23;359(6382):1361-1365. DOI: 10.1126/science.aar6711.
June CH, Riddell SR, Schumacher TN. Adoptive cellular therapy: a race to the finish line. Sci Transl Med. 2015 7:1–9. DOI: 10.1126/scitranslmed.aaa3643.
Karagiannis P, Kim SI. iPSC-Derived natural killer cells for cancer immunotherapy. Mol Cells. 2021 44(8):541–8. DOI: 10.14348/molcells.2021.0242.
Kaufman DS, Bjordahl R, Zhu H, Blum R, Bahena A, Mahmood S, et al. Off-the-shelf natural killer cells with multi-functional engineering using a novel anti-CD19 chimeric antigen receptor combined with stabilized CD16 and IL15 expression to enhance directed anti-tumor activity. Blood. 2018 132:4541. DOI: 10.1182/blood-2018-05-848512.
Kiessling R, Klein E, Pross H, Wigzell H. "Natural" killer cells in the mouse. II. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Characteristics of the killer cell. Eur J Immunol. 1975 Feb;5(2):117-21. DOI: 10.1002/eji.1830050207.
Klingemann H, Boissel L, Toneguzzo F. Natural Killer Cells for Immunotherapy - Advantages of the NK-92 Cell Line Over Blood NK Cells. Front Immunol. 2016 Mar 31;7:91. DOI: 10.3389/fimmu.2016.00091.
Klingemann HG, Wong E, Maki G. A cytotoxic NK-cell line (NK-92) for ex vivo purging of leukemia from blood. Biol Blood Marrow Transpl. 1996 2:68–75. DOI: 10.1016/S1083-8791(96)80017-7.
Kremer V, Ligtenberg MA, Zendehdel R, Seitz C, Duivenvoorden A, Wennerberg E, Colón E, Scherman-Plogell AH, Lundqvist A. Genetic engineering of human NK cells to express CXCR2 improves migration to renal cell carcinoma. J Immunother Cancer. 2017 Sep 19;5(1):73. DOI: 10.1186/s40425-017-0276-4.
Kundu S, Gurney M, O’Dwyer M. Generating Natural Killer Cells for Adoptive Transfer: Expanding Horizons. Cytotherapy 2021 23:559–66. DOI: 10.1016/j.jcyt.2021.03.007.
Lapteva N, Parihar R, Rollins LA, Gee AP, Rooney CM. Large-Scale Culture and Genetic Modification of Human Natural Killer Cells for Cellular Therapy. Methods Mol Biol. 2016 1441:195-202. DOI: 10.1007/978-1-4939-3684-7_14.
Levine BL, Humeau LM, Boyer J, MacGregor RR, Rebello T, Lu X, Binder GK, Slepushkin V, Lemiale F, Mascola JR, Bushman FD, Dropulic B, June CH. Gene transfer in humans using a conditionally replicating lentiviral vector. Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17372-7. DOI: 10.1073/pnas.0608197103.
Li Y, Hermanson D, Moriarity B, Bjordahl R, Mahmood S, Valamehr B, et al. Engineering human induced pluripotent stem cells with novel chimeric antigen receptors to generate natural killer (NK) cell cancer immunotherapies with targeted anti-tumor activity. Blood. 2017 130:1905–1905. DOI: 10.1182/blood.V130.Suppl_1.1905.1905
Liu E, Marin D, Banerjee P, Macapinlac HA, Thompson P, Basar R, Nassif Kerbauy L, Overman B, Thall P, Kaplan M, Nandivada V, Kaur I, Nunez Cortes A, Cao K, Daher M, Hosing C, Cohen EN, Kebriaei P, Mehta R, Neelapu S, Nieto Y, Wang M, Wierda W, Keating M, Champlin R, Shpall EJ, Rezvani K. Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors. N Engl J Med. 2020 Feb 6;382(6):545-553. DOI: 10.1056/NEJMoa1910607.
Liu E, Tong Y, Dotti G, Shaim H, Savoldo B, Mukherjee M, et al. Cord blood NK cells engineered to express IL-15 and a CD19-targeted CAR show long-term persistence and potent antitumor activity. Leukemia. 2018;32:520–31. DOI: 10.1038/leu.2017.333.
Liu J, Zhou G, Zhang L, Zhao Q. Building Potent Chimeric Antigen Receptor T Cells With CRISPR Genome Editing. Front Immunol. 2019 Mar 19;10:456. DOI: 10.3389/fimmu.2019.00456.
Loo J, Sicher I, Goff A, Kim O, Clary N, Alexeev A, Sulchek T, Zamarayeva A, Han S, Calero-Garcia M. Microfluidic transfection of mRNA into human primary lymphocytes and hematopoietic stem and progenitor cells using ultra-fast physical deformations. Sci Rep. 2021 Nov 1;11(1):21407. DOI: 10.1038/s41598-021-00863-6.
Matosevic S. Viral and Nonviral Engineering of Natural Killer Cells as Emerging Adoptive Cancer Immunotherapies. J Immunol Res. 2018 2018:4054815. DOI: 10.1155/2018/4054815.
McKinlay CJ, Benner NL, Haabeth OA, Waymouth RM, Wender PA. Enhanced mRNA delivery into lymphocytes enabled by lipid-varied libraries of charge-altering releasable transporters. Proc Natl Acad Sci U S A. 2018 Jun 26;115(26): E5859-E5866. DOI: 10.1073/pnas.1805351115.
Micucci F, Zingoni A, Piccoli M, Frati L, Santoni A, Galandrini R. High-efficient lentiviral vector-mediated gene transfer into primary human NK cells. Exp Hematol. 2006 Oct;34(10):1344-52. DOI: 10.1016/j.exphem.2006.05.022.
Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ, Orchard PJ, Blazar BR, Wagner JE, Slungaard A, Weisdorf DJ, Okazaki IJ, McGlave PB. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005 Apr 15;105(8):3051-7. DOI: 10.1182/blood-2004-07-2974.
Mingozzi F. High K.A. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat. Rev. Genet. 2011 12: 341-355. DOI: 10.1038/nrg2988.
Morvan, M. G. & Lanier, L. L. NK cells and cancer: you can teach innate cells new tricks. Nat. Rev. Cancer 2015, 16, 7–19. DOI: 10.1038/nrc.2015.5.
Naeimi Kararoudi M, Likhite S, Elmas E, Yamamoto K, Schwartz M, Sorathia K, de Souza Fernandes Pereira M, Sezgin Y, Devine RD, Lyberger JM, Behbehani GK, Chakravarti N, Moriarity BS, Meyer K, Lee DA. Optimization and validation of CAR transduction into human primary NK cells using CRISPR and AAV. Cell Rep Methods. 2022 Jun 13;2(6):100236. DOI: 10.1016/j.crmeth.2022.100236.
Naeimi Kararoudi M, Tullius BP, Chakravarti N, Pomeroy EJ, Moriarity BS, Beland K, Colamartino ABL, Haddad E, Chu Y, Cairo MS, Lee DA. Genetic and epigenetic modification of human primary NK cells for enhanced antitumor activity. Semin Hematol. 2020 57(4):201-212. DOI: 10.1053/j.seminhematol.2020.11.015.
Nawaz W, Huang B, Xu S, Li Y, Zhu L, Yiqiao H, Wu Z, Wu X. AAV-mediated in vivo CAR gene therapy for targeting human T-cell leukemia. Blood Cancer J. 2021 11(6):119. DOI: 10.1038/s41408-021-00522-2.
Ng YY, Tay JCK, Wang S. CXCR1 Expression to Improve Anti-Cancer Efficacy of Intravenously Injected CAR-NK Cells in Mice with Peritoneal Xenografts. Mol Ther Oncolytics. 2019 Dec 24;16:75-85. DOI: 10.1016/j.omto.2019.12.006.
Nguyen DN, Roth TL, Li PJ, et al. Polymer-stabilized Cas9 nanoparticles and modified repair templates increase genome editing efficiency. Nat Biotechnol. 2020 38(1):44-49. DOI: 10.1038/s41587-019-0344-3.
Nham T, Poznanski SM, Fan IY, Vahedi F, Shenouda MM, Lee AJ, et al. Ex Vivo-expanded Natural Killer Cells Derived From Long-term Cryopreserved Cord Blood are Cytotoxic Against Primary Breast Cancer Cells. J Immunother 2018 41:64–72. DOI: 10.1097/CJI.0000000000000203.
Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol. 2008;8:713–725. DOI: 10.1038/nri2381.
Pfefferle A, Huntington ND. You have got a fast car: chimeric antigen receptor NK cells in cancer therapy. Cancers (Basel). 2020 12:1–23. DOI: 10.3390/cancers12010023.
Pomeroy EJ, Hunzeker JT, Kluesner MG, Lahr WS, Smeester BA, Crosby MR, et al. A genetically engineered primary human natural killer cell platform for cancer immunotherapy. Mol Ther. 2019 Jan 9;28(1):52-63. DOI: 10.1016/j.ymthe.2019.09.003
Rogers GL, Huang C, Clark RDE, Seclén E, Chen HY, Cannon PM. Optimization of AAV6 transduction enhances site-specific genome editing of primary human lymphocytes. Mol Ther Methods Clin Dev. 2021 Sep 10;23:198-209. DOI: 10.1016/j.omtm.2021.07.002.
Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, Leong JW, Abdel-Latif S, Schneider SE, Willey S, Neal CC, Yu L, Oh ST, Lee YS, Mulder A, Claas F, Cooper MA, Fehniger TA. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med. 2016 Sep 21;8(357):357ra123. DOI: 10.1126/scitranslmed.aaf2341.
Sandrin V, Boson B, Salmon P, Gay W, Nègre D, Le Grand R, Trono D, Cosset FL. Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates. Blood. 2002 Aug 1;100(3):823-32. DOI: 10.1182/blood-2002-01-0046.
Shaffer BC, Le Luduec JB, Forlenza C, Jakubowski AA, Perales MA, Young JW, et al. Phase II study of haploidentical natural killer cell infusion for treatment of relapsed or persistent myeloid malignancies following allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2016;22:705–9. DOI: 10.1016/j.bbmt.2015.11.018.
Shah N, Martin-Antonio B, Yang H, Ku S, Lee DA, Cooper LJ, et al. Antigen Presenting Cell-Mediated Expansion of Human Umbilical Cord Blood Yields Log-Scale Expansion of Natural Killer Cells With Anti-Myeloma Activity. PLoS One 2013 8:e76781. DOI: 10.1371/journal.pone.0076781.
Shankar K, Capitini CM, Saha K. Genome Engineering of Induced Pluripotent Stem Cells to Manufacture Natural Killer Cell Therapies. Stem Cell Res Ther. 2020 11:234. DOI: 10.1186/s13287-020-01747-6.
Shimasaki N, Campana D. Engineering of Natural Killer Cells for Clinical Application. In: SG Katz, PM Rabinovich, editors. Cell Reprogramming for Immunotherapy: Methods and Protocols. New York, NY: Springer US 2020 p. 91–105. DOI: 10.1007/978-1-0716-0301-7_6.
Shimasaki N, Fujisaki H, Cho D, et al. A clinically adaptable method to enhance the cytotoxicity of natural killer cells against B-cell malignancies. Cytotherapy. 2012 14(7):830-840. DOI: 10.3109/14653249.2012.689244.
Song L. Li X. Jayandharan G.R. Wang Y. Aslanidi G.V. Ling C. Zhong L. Gao G. Yoder M.C. Ling C. et al. High-efficiency transduction of primary human hematopoietic stem cells and erythroid lineage-restricted expression by optimized AAV6 serotype vectors in vitro and in a murine xenograft model in vivo. PLoS ONE. 2013 8: e58757. DOI: 10.1371/journal.pone.0058757.
Streltsova MA, Barsov E, Erokhina SA, Kovalenko EI. Retroviral gene transfer into primary human NK cells activated by IL-2 and K562 feeder cells expressing membrane-bound IL-21. J Immunol Methods. 2017 Nov;450:90-94. DOI: 10.1016/j.jim.2017.08.003.
Suerth JD, Morgan MA, Kloess S, Heckl D, Neudörfl C, Falk CS, Koehl U, Schambach A. Efficient generation of gene-modified human natural killer cells via alpharetroviral vectors. J Mol Med (Berl). 2016 Jan;94(1):83-93. DOI: 10.1007/s00109-015-1349-0.
Tam YK, Martinson JA, Doligosa K, Klingemann HG. 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. 2003 5(3):259–72. DOI: 10.1080/14653240310003045.
Tang X, Yang L, Li Z, Nalin AP, Dai H, Xu T, et al. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res. 2018 8(6):1083–9. DOI: 10.18282/amor.v8.i6.457.
Trinchieri G. Biology of natural killer cells Adv Immunol. 1989 47, pp. 187-376 DOI: 10.1016/S0065-2776(08)60690-9.
Trompeter HI, Weinhold S, Thiel C, Wernet P, Uhrberg M. Rapid and highly efficient gene transfer into natural killer cells by nucleofection. J Immunol Methods. 2003 Mar 1;274(1-2):245-56. DOI: 10.1016/S0022-1759(02)00434-0.
Verneris MR, Miller JS. The Phenotypic and Functional Characteristics of Umbilical Cord Blood and Peripheral Blood Natural Killer Cells. Br J Haematol. 2009 Jan;147(2):185-91. DOI: 10.1111/j.1365-2141.2009.07878.x.
Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44-9. DOI: 10.1126/science.1198687.
Wang J, DeClercq JJ, Hayward SB, Li PW, Shivak DA, Gregory PD, Lee G, Holmes MC. Highly efficient homology-driven genome editing in human T cells by combining zinc-finger nuclease mRNA and AAV6 donor delivery. Nucleic Acids Res. 2016 Feb 18;44(3):e30. DOI: 10.1093/nar/gkv1503.
Watanabe N, McKenna MK. Generation of CAR T-cells using γ-retroviral vector. Methods Cell Biol. 2022 167:171-183. DOI: 10.1016/bs.mcb.2022.09.003.
Wei J, Han X, Bo J, Han W. Target selection for CAR-T therapy. J Hematol Oncol. 2019 12:62. DOI: 10.1186/s13045-019-0776-4.
Wilk AJ, Weidenbacher NL, Vergara R, Haabeth OAW, Levy R, Waymouth RM, Wender PA, Blish CA. Charge-altering releasable transporters enable phenotypic manipulation of natural killer cells for cancer immunotherapy. Blood Adv. 2020 Sep 8;4(17):4244-4255. DOI: 10.1182/ bloodadvances.2020001910.
Williams SM, Sumstad D, Kadidlo D, Curtsinger J, Luo X, Miller JS, et al. Clinical-Scale Production of cGMP Compliant CD3/CD19 Cell-Depleted NK Cells in the Evolution of NK Cell Immunotherapy at a Single Institution. Transfusion. 2018 Jul;58(7):1458-67. DOI: 10.1111/trf.14602.
Wu SY, Fu T, Jiang YZ, Shao ZM. Natural Killer Cells in Cancer Biology and Therapy. Mol Cancer. 2020;19:120. DOI: 10.1186/s12943-020-01248-1.
Xu X, Huang S, Xiao X, Sun Q, Liang X, Chen S, et al. Challenges and clinical strategies of CAR T-cell therapy for acute lymphoblastic leukemia: overview and developments. Front Immunol. 2020;11:569117. DOI: 10.3389/fimmu.2020.569117.
Yan Y, Steinherz P, Klingemann HG, Dennig D, Childs BH, McGuirk J, et al. Antileukemia activity of a natural killer cell line against human leukemias. Clin Cancer Res. 1998 4:2859–68. DOI: 10.1182/blood-2018-05-848512.
Yang Y, Lim O, Kim TM, Ahn YO, Choi H, Chung H, et al. Phase I study of random healthy donor-derived allogeneic natural killer cell therapy in patients with malignant lymphoma or advanced solid tumors. Cancer Immunol Res. 2016 4:215–24. DOI:10.1158/2326-6066.CIR-15-0110.
Yoon SR, Kim TD, Choi I. Understanding of molecular mechanisms in natural killer cell therapy. Exp Mol Med. 2015 47(2): e141. DOI: 10.1038/emm.2014.111.
Zhang Y, Wallace DL, de Lara CM, Ghattas H, Asquith B, Worth A, Griffin GE, Taylor GP, Tough DF, Beverley PC, Macallan DC. In vivo kinetics of human natural killer cells: the effects of ageing and acute and chronic viral infection. Immunology. 2007;121(2):258-65. DOI: 10.1111/j.1365-2567.2007.02515.x.
Zhao X, Cai L, Hu Y, Wang H. Cord-Blood Natural Killer Cell-Based Immunotherapy for Cancer. Front Immunol. 2020 Oct 22;11:584099. DOI: 10.3389/fimmu.2020.584099.
Zhu H, Blum RH, Bjordahl R, Gaidarova S, Rogers P, Lee TT, et al. Pluripotent stem cell-derived NK cells with high-affinity noncleavable CD16a mediate improved antitumor activity. Blood. 2020 135(6):399–410. DOI: 10.1182/blood.2019003312.
Published
How to Cite
Issue
Section
Copyright (c) 2024 Yunshu Hao; Tara Andersson
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Copyright holder(s) granted JSR a perpetual, non-exclusive license to distriute & display this article.