Cancer immunotherapy via stem cell-derived NK cells

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

• 1. Wolf NK, Kissiov DU, Raulet DH. Roles of natural killer cells in immunity to cancer, and applications to immunotherapy. Nat. Rev. Immunol. 23(2), 90–105 (2023).
  Medline CASGoogle Scholar
• 2. Sainiteesh M, John LS, John BS. Emerging NK cell therapies for cancer and the promise of next generation engineering of iPSC-derived NK cells. J. Immunother. Cancer 10(5), e004693 (2022).
  MedlineGoogle Scholar
• 3. Shimasaki N, Jain A, Campana D. NK cells for cancer immunotherapy. Nat. Rev. Drug Discov. 19(3), 200–218 (2020).
  Medline CASGoogle Scholar
• 4. Wu SY, Fu T, Jiang YZ, Shao ZM. Natural killer cells in cancer biology and therapy. Mol. Cancer 19(1), 120 (2020).
  Medline CASGoogle Scholar
• 5. Chiossone L, Dumas P-Y, Vienne M, Vivier E. Natural killer cells and other innate lymphoid cells in cancer. Nat. Rev. Immunol. 18(11), 671–688 (2018).
  Medline CASGoogle Scholar
• 6. Rezvani K. Adoptive cell therapy using engineered natural killer cells. Bone Marrow Transplant. 54(2), 785–788 (2019). • A timely review in the field.
  Medline CASGoogle Scholar
• 7. Rubnitz JE, Inaba H, Ribeiro RC et al. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J. Clin. Oncol. 28(6), 955 (2010). • A pioneer study in the field.
  Medline CASGoogle Scholar
• 8. Alkhaled M, Elazzazy A, Almaghrabia O. In vivo developing immunotherapy of ex vivo expansion of human natural killer cells from thalassemia patients for leukaemia. Indian J. Pharm. Sci. 84(2), 42–47 (2022).
  CASGoogle Scholar
• 9. Guillerey C, Huntington ND, Smyth MJ. Targeting natural killer cells in cancer immunotherapy. Nat. Immunol. 17(9), 1025–1036 (2016).
  Medline CASGoogle Scholar
• 10. Salagianni M, Baxevanis CN, Papamichail M, Perez SA. New insights into the role of NK cells in cancer immunotherapy. Oncoimmunology 1(2), 205–207 (2012).
  Medline CASGoogle Scholar
• 11. Lian G, Mak TS-K, Yu X, Lan H-Y. Challenges and recent advances in NK cell-targeted immunotherapies in solid tumors. Int. J. Mol. Sci. 23(1), 164 (2021).
  MedlineGoogle Scholar
• 12. Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-derived natural killer cells engineered with chimeric antigen receptors enhance anti-tumor activity. Cell Stem Cell 23(2), 181–192.e5 (2018).
  Medline CASGoogle Scholar
• 13. Zhu H, Kaufman DS. Engineered human pluripotent stem cell-derived natural killer cells: the next frontier for cancer immunotherapy. Blood Sci. 1(1), 4–11 (2019).
  MedlineGoogle Scholar
• 14. Morvan MG, Lanier LL. NK cells and cancer: you can teach innate cells new tricks. Nat. Rev. Cancer 16(1), 7–19 (2016).
  Medline CASGoogle Scholar
• 15. Crinier A, Narni-Mancinelli E, Ugolini S, Vivier E. SnapShot: natural killer cells. Cell 180(6), 1280–1280.e1 (2020).
  Medline CASGoogle Scholar
• 16. Jacobs R, Hintzen G, Kemper A et al. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur. J. Immunol. 31(10), 3121–3126 (2001).
  Medline CASGoogle Scholar
• 17. Raulet DH, Vance RE, McMahon CW. Regulation of the natural killer cell receptor repertoire. Annu. Rev. Immunol. 19, 291 (2001).
  Medline CASGoogle Scholar
• 18. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. Controlling NK cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol. 31, 227–258 (2013).
  Medline CASGoogle Scholar
• 19. Ljunggren H-G, Kärre K. In search of the ‘missing self’: MHC molecules and NK cell recognition. Immunol. Today 11, 237–244 (1990).
  Medline CASGoogle Scholar
• 20. Martínez-Lostao L, Anel A, Pardo J. How do cytotoxic lymphocytes kill cancer cells? Clin. Cancer Res. 21(22), 5047–5056 (2015).
  Medline CASGoogle Scholar
• 21. Vujanovic NL. Role of TNF family ligands in antitumor activity of natural killer cells. Int. Rev. Immunol. 20(3–4), 415–437 (2001).
  Medline CASGoogle Scholar
• 22. Müller L, Aigner P, Stoiber D. Type I interferons and natural killer cell regulation in cancer. Front. Immunol. 8, 304 (2017).
  MedlineGoogle Scholar
• 23. Yeap WH, Wong KL, Shimasaki N et al. CD16 is indispensable for antibody-dependent cellular cytotoxicity by human monocytes. Sci. Rep. 6(1), 1–22 (2016).
  MedlineGoogle Scholar
• 24. Shin MH, Kim J, Lim SA, Kim J, Kim S-J, Lee K-M. NK cell-based immunotherapies in cancer. Immune Netw. 20(2), e14 (2020).
  MedlineGoogle Scholar
• 25. Hegde UP, Mukherji B. Current status of chimeric antigen receptor engineered T cell-based and immune checkpoint blockade-based cancer immunotherapies. Cancer Immunol. Immunother. 66(9), 1113–1121 (2017).
  Medline CASGoogle Scholar
• 26. Hartmann J, Schüßler-Lenz M, Bondanza A, Buchholz CJ. Clinical development of CAR T cells – challenges and opportunities in translating innovative treatment concepts. EMBO Mol. Med. 9(9), 1183–1197 (2017).
  Medline CASGoogle Scholar
• 27. June C, Lim WA. The principles of engineering immune cells to treat cancer. Cell 168(4), 724–740 (2017).
  MedlineGoogle Scholar
• 28. June CH, O'Connor RS, Kawalekar OU, Ghassemi S, Milone MC. CAR T cell immunotherapy for human cancer. Science 359(6382), 1361–1365 (2018).
  Medline CASGoogle Scholar
• 29. Yang Y, Jacoby E, Fry TJ. Challenges and opportunities of allogeneic donor-derived CAR T cells. Curr. Opin. Hematol. 22(6), 509 (2015).
  Medline CASGoogle Scholar
• 30. Acharya UH, Dhawale T, Yun S et al. Management of cytokine release syndrome and neurotoxicity in chimeric antigen receptor (CAR) T cell therapy. Expert Rev. Hematol. 12(3), 195–205 (2019).
  Medline CASGoogle Scholar
• 31. 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 105(8), 3051–3057 (2005). • A pioneer study in the field.
  Medline CASGoogle Scholar
• 32. Du W, Cui L, Zhang J et al. Generation of universal natural killer cells from a cryopreserved cord blood mononuclear cell-derived induced pluripotent stem cell library. FEBS Open Bio 12(10), 1771–1781 (2022).
  Medline CASGoogle Scholar
• 33. Della Chiesa M, Falco M, Podesta M et al. Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus? Blood 119(2), 399–410 (2012). • A study that guides the field.
  MedlineGoogle Scholar
• 34. Kimbrel EA, Lu S-J. Potential clinical applications for human pluripotent stem cell-derived blood components. Stem Cells Int. 2011, doi: 10.4061/2011/273076 (2011) (Online).
  Google Scholar
• 35. Sarvaria A, Jawdat D, Madrigal JA, Saudemont A. Umbilical cord blood natural killer cells, their characteristics, and potential clinical applications. Front. Immunol. 8, 329 (2017).
  MedlineGoogle Scholar
• 36. Karagiannis P, Kim S-I. iPSC-derived natural killer cells for cancer immunotherapy. Mol. Cells 44(8), 541 (2021).
  Medline CASGoogle Scholar
• 37. Zhu H, Kaufman DS. Engineered human pluripotent stem cell-derived natural killer cells: the next frontier for cancer immunotherapy. Blood Sci. 1(01), 4–11 (2019).
  MedlineGoogle Scholar
• 38. Knorr DA, Ni Z, Hermanson D et al. Clinical-scale derivation of natural killer cells from human pluripotent stem cells for cancer therapy. Stem Cells Transl. Med. 2(4), 274–283 (2013).
  Medline CASGoogle Scholar
• 39. Zhang L, Liu M, Yang S, Wang J, Feng X, Han Z. Natural killer cells: of-the-shelf cytotherapy for cancer immunosurveillance. Am. J. Cancer Res. 11(4), 1770–1791 (2021).
  Medline CASGoogle Scholar
• 40. Uppendahl LD, Felices M, Bendzick L et al. Cytokine-induced memory-like natural killer cells have enhanced function, proliferation, and in vivo expansion against ovarian cancer cells. Gynecol. Oncol. 153(1), 149–157 (2019).
  Medline CASGoogle Scholar
• 41. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet 373(9674), 1550–1561 (2009).
  Medline CASGoogle Scholar
• 42. Siegler U, Meyer-Monard S, Jörger S et al. 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 (2010).
  Medline CASGoogle Scholar
• 43. Hermanson DL, Ni Z, Kaufman DS. Human pluripotent stem cells as a renewable source of natural killer cells. In: Hematopoietic Differentiation of Human Pluripotent Stem Cells. Springer, NY, USA, 69–79 (2015).
  Google Scholar
• 44. Hsu L-J, Liu C-L, Kuo M-L, Shen C-N, Shen C-R. An alternative cell therapy for cancers: induced pluripotent stem cell (iPSC)-derived natural killer cells. Biomedicines 9(10), 1323 (2021).
  Medline CASGoogle Scholar
• 45. Woll PS, Grzywacz B, Tian X et al. Human embryonic stem cells differentiate into a homogeneous population of natural killer cells with potent in vivo antitumor activity. Blood 113(24), 6094–6101 (2009).
  Medline CASGoogle Scholar
• 46. Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-derived natural killer cells engineered with chimeric antigen receptors enhance anti-tumor activity. Cell Stem Cell 23(2), 181–192.e5 (2018). •• A pioneer study on the use of chimeric antigen receptor-expressing induced pluripotent stem cells-derived NK cells.
  Medline CASGoogle Scholar
• 47. Alireza P. Evaluation of anti-cancer function in natural killer cells generated from rat hematopoietic stem cells. Thesis for PhD fulfilment, KULA LUMPUR, Malaya. Universiti Malaya. (2020).
  Google Scholar
• 48. Armstrong R. Spin Embryoid Bodies as an Improved Method of Blood Cell Differentiation in Human Embryonic Stem Cells and Induced Pluripotent Stem Cells. University of Minnesota, MN, USA (2010).
  Google Scholar
• 49. Denman CJ, Senyukov VV, Somanchi SS et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PlOS ONE 7(1), e30264 (2012).
  Medline CASGoogle Scholar
• 50. Oberoi P, Kamenjarin K, Villena Ossa JF, Uherek B, Bönig H, Wels WS. Directed differentiation of mobilized hematopoietic stem and progenitor cells into functional NK cells with enhanced antitumor activity. Cells 9(4), 811 (2020).
  Medline CASGoogle Scholar
• 51. Hermanson DL, Bendzick L, Pribyl L, McCullar V, Vogel RI, Miller JS et al. Induced pluripotent stem cell-derived natural killer cells for treatment of ovarian cancer. Stem Cells 34(1), 93–101 (2016). •• Potential of induced pluripotent stem cells-derived NK cells in cancer treatment.
  Medline CASGoogle Scholar
• 52. Shankar K, Capitini CM, Saha K. Genome engineering of induced pluripotent stem cells to manufacture natural killer cell therapies. Stem Cell Res. Ther. 11(1), 1–14 (2020).
  MedlineGoogle Scholar
• 53. Ni Z, Knorr DA, Bendzick L, Allred J, Kaufman DS. Expression of chimeric receptor CD4 ζ by natural killer cells derived from human pluripotent stem cells improves in vitro activity but does not enhance suppression of HIV infection in vivo. Stem Cells 32(4), 1021–1031 (2014).
  Medline CASGoogle Scholar
• 54. Abreu TR, Fonseca NA, Gonçalves N, Moreira JN. Current challenges and emerging opportunities of CAR-T cell therapies. J. Control. Rel. 319, 246–261 (2020).
  Medline CASGoogle Scholar
• 55. Wang L, Dou M, Ma Q, Yao R, Liu J. Chimeric antigen receptor (CAR)-modified NK cells against cancer: opportunities and challenges. Int. Immunopharmacol. 74, doi: 10.1016/j.intimp.2019.105695 (2019) (Online).
  Google Scholar
• 56. Ruggeri L, Capanni M, Casucci M et al. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 94(1), 333–339 (1999).
  Medline CASGoogle Scholar
• 57. Ruggeri L, Capanni M, Urbani E et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295(5562), 2097–2100 (2002).
  Medline CASGoogle Scholar
• 58. Rezvani K, Rouce R, Liu E, Shpall E. Engineering natural killer cells for cancer immunotherapy. Mol. Ther. 25(8), 1769–1781 (2017).
  Medline CASGoogle Scholar
• 59. Imai C, Iwamoto S, Campana D. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood 106(1), 376–383 (2005).
  Medline CASGoogle Scholar
• 60. Galat Y, Elcheva I, Dambaeva S et al. Application of small molecule CHIR99021 leads to the loss of hemangioblast progenitor and increased hematopoiesis of human pluripotent stem cells. Exp. Hematol. 65, 38–48.e1 (2018).
  Medline CASGoogle Scholar
• 61. Mangal JL, Handlos JL, Esrafili A et al. Engineering metabolism of chimeric antigen receptor (CAR) cells for developing efficient immunotherapies. Cancers 13(5), 1123 (2021).
  Medline CASGoogle Scholar
• 62. Wang J, Lupo KB, Chambers AM, Matosevic S. Purinergic targeting enhances immunotherapy of CD73+ solid tumors with piggyBac-engineered chimeric antigen receptor natural killer cells. J. Immunother. Cancer 6(1), 1–14 (2018).
  MedlineGoogle Scholar
• 63. Chang Y-H, Connolly J, Shimasaki N, Mimura K, Kono K, Campana D. A chimeric receptor with NKG2D specificity enhances natural killer cell activation and killing of tumor cells. Cancer Res. 73(6), 1777–1786 (2013).
  Medline CASGoogle Scholar
• 64. 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 14(7), 830–840 (2012).
  Medline CASGoogle Scholar
• 65. Liu E, Tong Y, Dotti G 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 32(2), 520–531 (2018).
  Medline CASGoogle Scholar
• 66. Han J, Chu J, Keung Chan W et al. CAR-engineered NK cells targeting wild-type EGFR and EGFRvIII enhance killing of glioblastoma and patient-derived glioblastoma stem cells. Sci. Rep. 5(1), 1–13 (2015).
  CASGoogle Scholar
• 67. 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. 12(1), 1–13 (2019).
  MedlineGoogle Scholar
• 68. Schnalzger TE, de Groot MH, Zhang C et al. 3D model for CAR-mediated cytotoxicity using patient-derived colorectal cancer organoids. EMBO J. 38(12), e100928 (2019).
  MedlineGoogle Scholar
• 69. Schönfeld K, Sahm C, Zhang C et al. Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol. Ther. 23(2), 330–338 (2015).
  MedlineGoogle Scholar
• 70. Biederstädt A, Rezvani K. Engineering the next generation of CAR-NK immunotherapies. Int. J. Hematol. 114(5), 554–571 (2021).
  MedlineGoogle Scholar
• 71. Yong CS, John LB, Devaud C et al. A role for multiple chimeric antigen receptor-expressing leukocytes in antigen-specific responses to cancer. Oncotarget 7(23), 34582–34598 (2016).
  MedlineGoogle Scholar
• 72. Zhang C, Hu Y, Xiao W, Tian Z. Chimeric antigen receptor-and natural killer cell receptor-engineered innate killer cells in cancer immunotherapy. Cell. Mol. Immunol. 18(9), 2083–2100 (2021).
  Medline CASGoogle Scholar
• 73. Berraondo P, Sanmamed MF, Ochoa MC et al. Cytokines in clinical cancer immunotherapy. Br. J. Cancer 120(1), 6–15 (2019).
  Medline CASGoogle Scholar
• 74. Lotze MT, Grimm EA, Mazumder A, Strausser JL, Rosenberg SA. Lysis of fresh and cultured autologous tumor by human lymphocytes cultured in T-cell growth factor. Cancer Res. 41(11 Part 1), 4420–4425 (1981).
  Medline CASGoogle Scholar
• 75. McMichael EL, Jaime-Ramirez AC, Guenterberg KD et al. IL-21 enhances natural killer cell response to cetuximab-coated pancreatic tumor cells. Clin. Cancer Res. 23(2), 489–502 (2017).
  Medline CASGoogle Scholar
• 76. Li Q, Ye L-J, Ren H-L et al. Multiple effects of IL-21 on human NK cells in ex vivo expansion. Immunobiology 220(7), 876–888 (2015).
  Medline CASGoogle Scholar
• 77. Carson WE, Giri JG, Lindemann MJ et al. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 180(4), 1395–1403 (1994).
  Medline CASGoogle Scholar
• 78. Heinze A, Grebe B, Bremm M et al. The synergistic use of IL-15 and IL-21 for the generation of NK cells from CD3/CD19-depleted grafts improves their ex vivo expansion and cytotoxic potential against neuroblastoma: perspective for optimized immunotherapy post haploidentical stem cell transplantation. Front. Immunol. 10, 2816 (2019).
  Medline CASGoogle Scholar
• 79. Reina Ortiz C, Bernal AA. Expansion of NK Cells for the Treatment of Multiple Myeloma. University of Zaragoza, CIEN, Zaragoza, Spain, MSc. Thesis (2018).
  Google Scholar
• 80. Choi YH, Lim EJ, Kim SW, Moon YW, Park KS, An H-J. IL-27 enhances IL-15/IL-18-mediated activation of human natural killer cells. J. Immunother. Cancer 7(1), 1–12 (2019).
  MedlineGoogle Scholar
• 81. Dolstra H, Roeven MW, Spanholtz J et al. Successful transfer of umbilical cord blood CD34+ hematopoietic stem and progenitor-derived NK cells in older acute myeloid leukemia patients. Clin. Cancer Res. 23(15), 4107–4118 (2017).
  Medline CASGoogle Scholar
• 82. Handgretinger R, Lang P, André MC. Exploitation of natural killer cells for the treatment of acute leukemia. Blood 127(26), 3341–3349 (2016).
  Medline CASGoogle Scholar
• 83. Zhu H, Lai Y-S, Li Y, Blum RH, Kaufman DS. Concise review: human pluripotent stem cells to produce cell-based cancer immunotherapy. Stem Cells 36(2), 134–145 (2018).
  MedlineGoogle Scholar
• 84. Williams BA, Law AD, Routy B et al. A phase I trial of NK-92 cells for refractory hematological malignancies relapsing after autologous hematopoietic cell transplantation shows safety and evidence of efficacy. Oncotarget 8(51), 89256–89268 (2017).
  MedlineGoogle Scholar
• 85. Geller MA, Cooley S, Judson PL et al. A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy 13(1), 98–107 (2011).
  Medline CASGoogle Scholar
• 86. Chambers AM, Lupo KB, Matosevic S. Tumor microenvironment-induced immunometabolic reprogramming of natural killer cells. Front. Immunol. 9, 2517 (2018).
  MedlineGoogle Scholar
• 87. Hosseini R, Sarvnaz H, Arabpour M et al. Cancer exosomes and natural killer cells dysfunction: biological roles, clinical significance and implications for immunotherapy. Mol. Cancer 21(1), 15 (2022). •• Explaining the tumor-associated factors, exosomes, contributing to NK cells-based immunotherapy subversion.
  Medline CASGoogle Scholar
• 88. Klingemann H-G, Wong E, Maki G. A cytotoxic NK-cell line (NK-92) for ex vivo purging of leukemia from blood. Bio. Blood Marrow Transplant. 2(2), 68–75 (1996).
  Medline CASGoogle Scholar
• 89. Klingemann H, Boissel L, Toneguzzo F. Natural killer cells for immunotherapy – advantages of the NK-92 cell line over blood NK cells. Front. Immunol. 7, 91 (2016). •• Potential utility of NK-92 cells for cancer immunotherapy.
  MedlineGoogle Scholar
• 90. Lapteva N, Parihar R, Rollins LA, Gee AP, Rooney CM. Large-scale culture and genetic modification of human natural killer cells for cellular therapy. In: Natural Killer Cells. Springer, Clifton, NJ, USA, 195–202 (2016).
  Google Scholar
• 91. Ruella M, Xu J, Barrett DM et al. Induction of resistance to chimeric antigen receptor T cell therapy by transduction of a single leukemic B cell. Nat. Med. 24(10), 1499–1503 (2018).
  Medline CASGoogle Scholar
• 92. Zhang C, Oberoi P, Oelsner S et al. Chimeric antigen receptor-engineered NK-92 cells: an off-the-shelf cellular therapeutic for targeted elimination of cancer cells and induction of protective antitumor immunity. Front. Immunol. 8, 533 (2017).
  MedlineGoogle Scholar
• 93. Clémenceau B, Vivien R, Pellat C, Foss M, Thibault G, Vié H. The human natural killer cytotoxic cell line NK-92, once armed with a murine CD16 receptor, represents a convenient cellular tool for the screening of mouse mAbs according to their ADCC potential. In: MAbs. Taylor andFrancis, NY, USA, 587–594 (2013)
  Google Scholar
• 94. Li F, Liu S. Focusing on NK cells and ADCC: a promising immunotherapy approach in targeted therapy for HER2-positive breast cancer. Front. Immunol. 13, doi: 10.3389/fimmu.2022.1083462 (2022) (Online).
  Google Scholar
• 95. Zhang J, Zheng H, Diao Y. Natural killer cells and current applications of chimeric antigen receptor-modified NK-92 cells in tumor immunotherapy. Int. J. Mol. Sci. 20(2), 317 (2019).
  MedlineGoogle Scholar
• 96. Sivori S, Meazza R, Quintarelli C et al. NK cell-based immunotherapy for hematological malignancies. J. Clin. Med. 8(10), 1702 (2019).
  Medline CASGoogle Scholar
• 97. Zhou Y, Li M, Zhou K et al. Engineering induced pluripotent stem cells for cancer immunotherapy. Cancers (Basel) 14(9), 2266 (2022).
  Medline CASGoogle Scholar
• 98. Crow D. Could iPSCs enable ‘off-the-shelf’ cell therapy? Cell 177(7), 1667–1669 (2019).
  Medline CASGoogle Scholar
• 99. Jung IH, Kim DH, Yoo DK et al. In vivo study of natural killer (NK) cell cytotoxicity against cholangiocarcinoma in a nude mouse model. In Vivo 32(4), 771 (2018).
  Medline CASGoogle Scholar
• 100. Dahlberg CI, Sarhan D, Chrobok M, Duru AD, Alici E. Natural killer cell-based therapies targeting cancer: possible strategies to gain and sustain anti-tumor activity. Front. Immunol. 6, 605 (2015).
  MedlineGoogle Scholar
• 101. Burga RA, Nguyen T, Zulovich J et al. Improving efficacy of cancer immunotherapy by genetic modification of natural killer cells. Cytotherapy 18(11), 1410–1421 (2016).
  Medline CASGoogle Scholar
• 102. 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. 12(3), 607–611 (2016).
  MedlineGoogle Scholar
• 103. Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur. J. Immunol. 44(6), 1582–1592 (2014).
  Medline CASGoogle Scholar
• 104. Ghiringhelli F, Ménard C, Terme M et al. CD4+ CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor–β–dependent manner. J. Exp. Med. 202(8), 1075–1085 (2005).
  Medline CASGoogle Scholar
• 105. Beavis PA, Divisekera U, Paget C et al. Blockade of A2A receptors potently suppresses the metastasis of CD73+ tumors. Proc. Natl Acad. Sci. USA 110(36), 14711–14716 (2013).
  Medline CASGoogle Scholar
• 106. Kai S, Goto S, Tahara K, Sasaki A, Kawano K, Kitano S. Inhibition of indoleamine 2, 3-dioxygenase suppresses NK cell activity and accelerates tumor growth. J. Exp. Ther. Oncol. 3(6), 336–345 (2003).
  Medline CASGoogle Scholar
• 107. Fauriat C, Just-Landi S, Mallet F et al. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCRdull phenotype induction. Blood 109(1), 323–330 (2007).
  Medline CASGoogle Scholar
• 108. Sanchez-Correa B, Gayoso I, Bergua JM et al. Decreased expression of DNAM-1 on NK cells from acute myeloid leukemia patients. Immunol. Cell Biol. 90(1), 109–115 (2012).
  Medline CASGoogle Scholar