537
Views
0
CrossRef citations to date
0
Altmetric
Review

CAR-NK cells: a promising cellular immunotherapy in lymphoma

&
Pages 37-47 | Received 14 Jul 2022, Accepted 30 Nov 2022, Published online: 05 Dec 2022

References

  • Khanmohammadi S, Shabani M, Tabary M, et al. Lymphoma in the setting of autoimmune diseases: a review of association and mechanisms. Crit Rev Oncol Hematol. 2020;150:102945.
  • Ng AK, LaCasce A, Travis LB. Long-term complications of lymphoma and its treatment.J Clin Oncol. 2011 [2011 May 10];29(14):1885–1892.
  • Barrett AJ, Battiwalla M. Relapse after allogeneic stem cell transplantation. Expert Rev Hematol. 2010;3(4):429–441.
  • Heyman B, Yang Y. New developments in immunotherapy for lymphoma. Cancer Biol Med. 2018;15(3):189–209.
  • Zhang T, Cao L, Xie J, et al. Efficiency of CD19 chimeric antigen receptor-modified T cells for treatment of B cell malignancies in phase I clinical trials: a meta-analysis. Oncotarget. 2015 Oct 20 6(32):33961–33971.
  • Lu H, Zhao X, Li Z, et al. From CAR-T Cells to CAR-NK cells: a developing immunotherapy method for hematological malignancies. Front Oncol. 2021;11:720501.
  • Marofi F, Abdul-Rasheed OF, Rahman HS, et al. CAR-NK cell in cancer immunotherapy; A promising frontier. Cancer Sci. 2021 Sep;112(9):3427–3436.
  • Yonekura K, Kusumoto S, Choi I, et al. Mogamulizumab for adult T-cell leukemia-lymphoma: a multicenter prospective observational study. Blood Adv. 2020 Oct 27 4(20):5133–5145.
  • Chu Y, Yahr A, Huang B, et al. Romidepsin alone or in combination with anti-CD20 chimeric antigen receptor expanded natural killer cells targeting Burkitt lymphoma in vitro and in immunodeficient mice. Oncoimmunology. 2017;6(9):e1341031.
  • Marofi F, Saleh MM, Rahman HS, et al. CAR-engineered NK cells; a promising therapeutic option for treatment of hematological malignancies. Stem Cell Res Ther. 2021 [2021 July 02];12(1):374.
  • Xie G, Dong H, Liang Y, et al. CAR-NK cells: a promising cellular immunotherapy for cancer. eBioMedicine. 2020; 59.
  • Yoon SR, Kim T-D, Choi I. Understanding of molecular mechanisms in natural killer cell therapy.Exp Mol Med. 2015 [2015 Feb 1];47(2):e141–e141.
  • Cornel AM, Mimpen IL, Nierkens S. MHC class I downregulation in cancer: underlying mechanisms and potential targets for cancer immunotherapy. Cancers (Basel). 2020;12(7):1760.
  • Myers JA, Schirm D, Bendzick L, et al. Balanced engagement of activating and inhibitory receptors mitigates human NK cell exhaustion. JCI Insight. 2022 Aug 8;7(15).
  • Smyth MJ, Thia KYT, Street SEA, et al. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous Lymphoma. J Exp Med. 2000;192(5):755–760.
  • Prager I, Watzl C. Mechanisms of natural killer cell-mediated cellular cytotoxicity [https://doi.org/10.1002/JLB.MR0718-269R]. J Leukoc Biol. 2019;2019( 06/01;105(6):1319-1329).
  • Zhu Y, Huang B, Shi J. Fas ligand and lytic granule differentially control cytotoxic dynamics of natural killer cell against cancer target. Oncotarget. 2016;7(30).
  • Screpanti V, Wallin RPA, Ljunggren H-G, et al. A central role for death receptor-mediated apoptosis in the rejection of tumors by NK Cells. J Immunol. 2001;167(4):2068.
  • Lo Nigro C, Macagno M, Sangiolo D, et al. NK-mediated antibody-dependent cell-mediated cytotoxicity in solid tumors: biological evidence and clinical perspectives. Ann Transl Med. 2019;7(5):105.
  • Wang W, Erbe AK, Hank JA, et al. NK cell-mediated antibody-dependent cellular cytotoxicity in cancer immunotherapy [Review]. Front Immunol. 2015 [2015-July-27];6:6.
  • Vitale M, Cantoni C, Pietra G, et al. Effect of tumor cells and tumor microenvironment on NK-cell function [https://doi.org/10.1002/eji.201344272]. Eur J Immunol. 2014;2014( 06/01;44(6):1582-1592).
  • Kobayashi T, Lam PY, Jiang H, et al. Increased lipid metabolism impairs NK cell function and mediates adaptation to the lymphoma environment. Blood. 2020;136(26):3004–3017.
  • Balsamo M, Scordamaglia F, Pietra G, et al. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc Natl Acad Sci U S A. 2009 Dec 8 106(49):20847–20852.
  • Hoechst B, Voigtlaender T, Ormandy L, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 2009 Sep;50(3):799–807.
  • Ghiringhelli F, Ménard C, Martin F, et al. The role of regulatory T cells in the control of natural killer cells: relevance during tumor progression. Immunol Rev. 2006 Dec;214(1):229–238.
  • Castriconi R, Cantoni C, Della Chiesa M, et al. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci U S A. 2003 Apr 1 100(7):4120–4125.
  • Sitrin J, Ring A, Garcia KC, et al. Regulatory T cells control NK cells in an insulitic lesion by depriving them of IL-2. J Exp Med. 2013 Jun 3 210(6):1153–1165.
  • Smyth MJ, Teng MWL, Swann J, et al. CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J Immunol. 2006;176(3):1582.
  • El-Gazzar A, Groh V, Spies T. Immunobiology and conflicting roles of the human NKG2D lymphocyte receptor and its ligands in cancer. J Immunol. 2013 Aug 15; 191(4):1509–1515.
  • Ashiru O, Boutet P, Fernández-Messina L, et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res. 2010;70(2):481–489.
  • Reiners KS, Kessler J, Sauer M, et al. Rescue of impaired nk cell activity in hodgkin lymphoma with bispecific antibodies in vitro and in patients. Mol Ther. 2013 [2013 April 01];21(4):895–903.
  • Balsamo M, Vermi W, Parodi M, et al. Melanoma cells become resistant to NK-cell-mediated killing when exposed to NK-cell numbers compatible with NK-cell infiltration in the tumor. Eur J Immunol. 2012 Jul;42(7):1833–1842.
  • Huang B, Zhao J, Li H, et al. Toll-like receptors on tumor cells facilitate evasion of immune surveillance. Cancer Res. 2005;65(12):5009–5014.
  • Ishida T, Ishii T, Inagaki A, et al. Specific recruitment of cc chemokine receptor 4–positive regulatory T cells in Hodgkin lymphoma fosters immune Privilege. Cancer Res. 2006;66(11):5716–5722.
  • Khawar MB, Sun H. Car-Nk cells: from natural basis to design for kill [Review]. Front Immunol. 2021 [2021-December-14];12.
  • Gong Y, Klein Wolterink RGJ, Wang J, et al. Chimeric antigen receptor natural killer (CAR-NK) cell design and engineering for cancer therapy. J Hematol Oncol. 2021 [2021 May 01];14(1):73.
  • Li Y, Hermanson DL, Moriarity BS, et al. Human iPSC-derived natural killer cells engineered with chimeric antigen receptors enhance anti-tumor activity. Cell Stem Cell. 2018 Aug 2 23(2):181–192.e5.
  • Buller CW, Mathew PA, Mathew SO. Roles of NK cell receptors 2B4 (CD244), CS1 (CD319), and LLT1 (CLEC2D) in Cancer. Cancers (Basel). 2020;12(7):1755.
  • Sun L, Gang X, Li Z, et al. Advances in understanding the roles of CD244 (SLAMF4) in immune regulation and associated diseases [Review]. Front Immunol. 2021 [2021-March-24];12.
  • Sentman CL, Meehan KR. NKG2D CARs as cell therapy for cancer. Cancer J. 2014 Mar-Apr;20(2):156–159.
  • Goodridge JP, Mahmood S, Zhu H, et al. FT596: translation of first-of-kind multi-antigen targeted off-the-shelf car-NK cell with engineered persistence for the Treatment of B cell Malignancies. Blood. 2019;134(Supplement_1):301.
  • Töpfer K, Cartellieri M, Michen S, et al. DAP12-based activating chimeric antigen receptor for NK cell tumor immunotherapy. J Immunol. 2015 Apr 1 194(7):3201–3212.
  • Billadeau DD, Upshaw JL, Schoon RA, et al. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat Immunol. 2003 Jun;4(6):557–564.
  • Klingemann H, Boissel L, Toneguzzo F. Natural Killer Cells for Immunotherapy – advantages of the NK-92 cell line over blood nk cells [Review]. Front Immunol. 2016;7:2016-March-14.
  • 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 Apr;8(4):652–658.
  • Maki G, Klingemann HG, Martinson JA, et al. Factors regulating the cytotoxic activity of the human natural killer cell line, NK-92. J Hematother Stem Cell Res. 2001 Jun;10(3):369–383.
  • Rezvani K, Rouce RH. The application of natural killer cell immunotherapy for the treatment of cancer. Front Immunol. 2015;6:578.
  • Tonn T, Becker S, Esser R, et al. Cellular immunotherapy of malignancies using the clonal natural killer cell line NK-92. J Hematother Stem Cell Res. 2001 Aug;10(4):535–544.
  • Shoae-Hassani A, Behfar M, Mortazavi-Tabatabaei SA, et al. Natural killer cells from the subcutaneous adipose tissue underexpress the NKp30 and NKp44 in obese persons and are less active against major histocompatibility complex Class I Non-Expressing Neoplastic Cells [Original Research]. Front Immunol. 2017 [2017-November-07];8:8.
  • Martín-Antonio B, Suñe G, Perez-Amill L, et al. Natural Killer cells: angels and devils for immunotherapy. Int J Mol Sci. 2017 Aug 29 18(9):1868.
  • Bae DS, Lee JK. Development of NK cell expansion methods using feeder cells from human myelogenous leukemia cell line. Blood Res. 2014;49(3):154–161.
  • Sarvaria A, Jawdat D, Madrigal JA, et al. Umbilical cord blood natural killer cells, their characteristics, and potential clinical applications. Front Immunol. 2017;8:329.
  • Miller JS, Soignier Y, Panoskaltsis-Mortari A, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005 Apr 15 105(8):3051–3057.
  • Cichocki F, Grzywacz B, Miller JS. Human NK Cell Development: one Road or Many? [Review]. Front Immunol. 2019;10:10. 2019-August-29.
  • Kao IT, Yao CL, Kong ZL, et al. Generation of natural killer cells from serum-free, expanded human umbilical cord blood CD34+ cells. Stem Cells Dev. 2007 Dec;16(6):1043–1051.
  • Bozzano F, Perrone C, Moretta L, et al. NK cell precursors in human bone marrow in health and inflammation. Front Immunol. 2019;10:2045.
  • Sconocchia G, Provenzano M, Rezvani K, et al. CD34+ cells cultured in stem cell factor and interleukin-2 generate CD56+ cells with antiproliferative effects on tumor cell lines. J Transl Med. 2005 [2005 April 14];3(1):15.
  • Miller JS, McCullar V, Punzel M, et al. Single adult human CD34(+)/Lin-/CD38(-) progenitors give rise to natural killer cells, B-lineage cells, dendritic cells, and myeloid cells. Blood. 1999 Jan 1 93(1):96–106.
  • Petit I, Szyper-Kravitz M, Nagler A, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol. 2002 Jul;3(7):687–694.
  • Kaufman DS, Hanson ET, Lewis RL, et al. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2001 Sep 11 98(19):10716–10721.
  • Saetersmoen ML, Hammer Q, Valamehr B, et al. Off-the-shelf cell therapy with induced pluripotent stem cell-derived natural killer cells. Semin Immunopathol. 2019 Jan;41(1):59–68.
  • Goldenson BH, Zhu H, Wang YM, et al. Umbilical cord blood and iPSC-derived natural killer cells demonstrate key differences in cytotoxic activity and kir profiles [original research]. Front Immunol. 2020 [2020-October-15];11:11.
  • Schmidt P, Raftery MJ, Pecher G. Engineering NK Cells for CAR therapy—recent advances in gene transfer methodology [Mini Review]. Front Immunol. 2021 [2021-January-07];11.
  • Warnock J, Daigre C, Al-Rubeai M. Introduction to viral vectors. Methods Mol Biol. 2011 April 02;737:1–25.
  • Ingegnere T, Mariotti FR, Pelosi A, et al. Human CAR NK Cells: a new non-viral method allowing high efficient transfection and strong tumor cell killing. Front Immunol. 2019;10:957.
  • Hacein-Bey-Abina S, Garrigue A, Wang GP, et al. Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest. 2008 Sep;118(9):3132–3142.
  • Pomeroy EJ, Lahr WS, Chang JW, et al. Non-Viral Engineering of CAR-NK and CAR-T cells using the <em>Tc Buster</em&#x003E. Transposon System™. bioRxiv 2021; 2021.08.02.454772
  • Elmas E, Saljoughian N, de Souza Fernandes Pereira M, et al. CRISPR Gene Editing of Human Primary NK and T Cells for Cancer Immunotherapy [Review]. Front Oncol. 2022 [2022-April-05];12.
  • Kararoudi MN, Likhite S, Elmas E, et al. CD33 targeting primary CAR-NK cells generated by CRISPR mediated gene insertion show enhanced anti-AML activity. Blood. 2020;136(Supplement 1):3.
  • Wang K, Wei G, Liu D. CD19: a biomarker for B cell development, lymphoma diagnosis and therapy.Exp Hematol Oncol. 2012 [2012 Nov 29];1(1):36.
  • Prevodnik VK, Lavrenčak J, Horvat M, et al. The predictive significance of CD20 expression in B-cell lymphomas. Diagn Pathol. 2011;6(1):33.
  • Yin Z, Zhang Y, Wang X. Advances in chimeric antigen receptor T-cell therapy for B-cell non-Hodgkin lymphoma.Biomark Res. 2021 [2021 July 13];9(1):58.
  • Gang M, Marin ND, Wong P, et al. CAR-modified memory-like NK cells exhibit potent responses to NK-resistant lymphomas. Blood. 2020 Nov 12 136(20):2308–2318.
  • Liu Q, Xu Y, Mou J, et al. Irradiated chimeric antigen receptor engineered NK-92MI cells show effective cytotoxicity against CD19(+) malignancy in a mouse model. Cytotherapy. 2020 Oct;22(10):552–562.
  • Liu E, Marin D, Banerjee P, et al. Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors. N Engl J Med. 2020 Feb 6;382(6):545–553.
  • Bachanova V, Cayci Z, Lewis D, et al. Initial clinical activity of ft596, a first-in-class, multi-antigen targeted, off-the-shelf, ipsc-derived CD19 CAR NK cell therapy in relapsed/refractory B-Cell Lymphoma. Blood. 2020 2020 Nov 05 136. 8.
  • Müller T, Uherek C, Maki G, et al. 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. 2008 Mar;57(3):411–423.
  • Chu Y, Hochberg J, Yahr A, et al. Targeting CD20+ Aggressive B-cell Non-Hodgkin Lymphoma by Anti-CD20 CAR mRNA-modified expanded natural killer cells in vitro and in NSG Mice. Cancer Immunol Res. 2015 Apr;3(4):333–344.
  • Phan A, Veldman R, Lechowicz MJ. T-cell Lymphoma Epidemiology: the Known and Unknown. Curr Hematol Malig Rep. 2016 Dec;11(6):492–503.
  • Safarzadeh Kozani P, Safarzadeh Kozani P, Rahbarizadeh F. CAR-T cell therapy in T-cell malignancies: is success a low-hanging fruit? Stem Cell Res Ther. 2021 [2021 Oct 07];12(1):527.
  • Chen KH, Wada M, Firor AE, et al. Novel anti-CD3 chimeric antigen receptor targeting of aggressive T cell malignancies. Oncotarget. 2016 Aug 30;7(35):56219–56232.
  • Chen KH, Wada M, Pinz KG, et al. Preclinical targeting of aggressive T-cell malignancies using anti-CD5 chimeric antigen receptor. Leukemia. 2017 Oct;31(10):2151–2160.
  • Pinz KG, Yakaboski E, Jares A, et al. Targeting T-cell malignancies using anti-CD4 CAR NK-92 cells. Oncotarget. 2017;8(68):112783–112796.
  • Xu Y, Liu Q, Zhong M, et al. 2B4 costimulatory domain enhancing cytotoxic ability of anti-CD5 chimeric antigen receptor engineered natural killer cells against T cell malignancies. J Hematol Oncol. 2019 [2019 May 16];12(1):49.
  • Lee DW, Kochenderfer JN, Stetler-Stevenson M, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet. 2015;385(9967):517–528.
  • Baghery Saghchy Khorasani A, Yousefi AM, Bashash D. CAR NK cell therapy in hematologic malignancies and solid tumors; obstacles and strategies to overcome the challenges. Int Immunopharmacol. 2022 Sep;110:109041.
  • Mehta RS, Rezvani K. Chimeric antigen receptor expressing natural killer cells for the immunotherapy of cancer. Front Immunol. 2018;9:283.
  • Carlsten M, Childs RW, Bancu I. Genetic Manipulation of NK Cells for Cancer Immunotherapy: techniques and Clinical Implications [Review]. Front Immunol. 2015 [2015-June-10];6:6.
  • Naldini L, Blömer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996 Apr 12 272(5259):263–267.
  • Imamura M, Shook D, Kamiya T, et al. Autonomous growth and increased cytotoxicity of natural killer cells expressing membrane-bound interleukin-15. Blood. 2014 Aug 14 124(7):1081–1088.
  • Micucci F, Zingoni A, Piccoli M, et al. High-efficient lentiviral vector-mediated gene transfer into primary human NK cells. Exp Hematol. 2006 Oct;34(10):1344–1352.
  • Piras F, Riba M, Petrillo C, et al. Lentiviral vectors escape innate sensing but trigger p53 in human hematopoietic stem and progenitor cells. EMBO Mol Med. 2017;9(9):1198–1211.
  • Howe SJ, Mansour MR, Schwarzwaelder K, et al. Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest. 2008;118(9):3143–3150.
  • Glienke W, Esser R, Priesner C, et al. Advantages and applications of CAR-expressing natural killer cells [Mini Review]. Front Pharmacol. 2015 [2015 February 12];6:6.
  • Lee DA. Cellular therapy: adoptive immunotherapy with expanded natural killer cells. Immunol Rev. 2019;290(1):85–99.
  • Li R, Johnson R, Yu G, et al. Preservation of cell-based immunotherapies for clinical trials. Cytotherapy. 2019;21(9):943–957.
  • Min B, Choi H, Her JH, et al. Optimization of large-scale expansion and cryopreservation of human natural killer cells for anti-tumor therapy. Immune Netw. 2018;18(4).
  • Pasley S, Zylberberg C, Matosevic S. Natural killer-92 cells maintain cytotoxic activity after long-term cryopreservation in novel DMSO-free media. Immunol Lett. 2017 Dec;192:35–41.
  • Afolabi LO, Adeshakin AO, Sani MM, et al. Genetic reprogramming for NK cell cancer immunotherapy with CRISPR/Cas9. Immunology. 2019 Oct;158(2):63–69.
  • Murray S, Lundqvist A. Targeting the tumor microenvironment to improve natural killer cell-based immunotherapies: on being in the right place at the right time, with resilience. Hum Vaccin Immunother. 2016 Mar 3; 12(3):607–611.
  • Bi J, Tian Z. NK Cell Dysfunction and Checkpoint Immunotherapy [Review]. Front Immunol. 2019 [2019-August-21];10:10.
  • Naeimi Kararoudi M, Dolatshad H, Trikha P, et al. Generation of knock-out primary and expanded human nk cells using Cas9 Ribonucleoproteins. J Vis Exp. 2018 Jun;14(136).
  • Guo C, Fan Y, Aronov A, et al. Abstract 5512: CBLB, CISH and CD70 multiplexed gene knockout with CRISPR/Cas9 enhances cytotoxicity of CD70-CAR NK cells and provides greater resistance to TGF-β for cancer immunotherapy. Cancer Res. 2022;82(12_Supplement):5512.
  • Fujisaki H, Kakuda H, Shimasaki N, et al. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 2009 May 1 69(9):4010–4017.
  • Pedroza-Pacheco I, Madrigal A, Saudemont A. Interaction between natural killer cells and regulatory T cells: perspectives for immunotherapy. Cell Mol Immunol. 2013 May;10(3):222–229.
  • Konstantinidis KV, Alici E, Aints A, et al. Targeting IL-2 to the endoplasmic reticulum confines autocrine growth stimulation to NK-92 cells. Exp Hematol. 2005 Feb;33(2):159–164.
  • Uddin F, Rudin CM, Sen T. CRISPR Gene Therapy: applications, Limitations, and Implications for the Future. Front Oncol. 2020;10:1387.
  • Zhang L, Meng Y, Feng X, et al. CAR-NK cells for cancer immunotherapy: from bench to bedside. Biomark Res. 2022 [2022 Mar 18];10(1):12.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.