Acute myeloid leukemia and NK cells: two warriors confront each other

References

• Pandolfi A, Barreyro L, Steidl U. Concise review: preleukemic stem cells: molecular biology and clinical implications of the precursors to leukemia stem cells. Stem Cells Transl Med. 2013;2(2):143–150. doi:10.5966/sctm.2012-0109.
   PubMed Web of Science ®Google Scholar
• Papaemmanuil E, Gerstung M, Bullinger L, Gaidzik VI, Paschka P, Roberts ND, Potter NE, Heuser M, Thol F, Bolli N, et al. Genomic classification and prognosis in acute myeloid leukemia. N Engl J Med. 2016;374(23):2209–2221. doi:10.1056/NEJMoa1516192.
   PubMed Web of Science ®Google Scholar
• Klco JM, Spencer DH, Miller CA, Griffith M, Lamprecht TL, O’Laughlin M, Fronick C, Magrini, Demeter RT, Fulton RS, et al. Functional heterogeneity of genetically defined subclones in acute myeloid leukemia. Cancer Cell. 2014;25(3):379–392. doi:10.1016/j.ccr.2014.01.031.
   PubMed Web of Science ®Google Scholar
• Aziz H, Ping CY, Alias H, AbMutalib NS, Jamal R. Gene mutations as emerging biomarkers and therapeutic targets for relapsed acute myeloid leukemia. Front Pharmacol. 2017;8:897. doi:10.3389/fphar.2017.00897.
   PubMed Web of Science ®Google Scholar
• Rothenberg-Thurley M, Amler S, Goerlich D, Köhnke T, Konstandin NP, Schneider S, Sauerland MC, Herold T, Hubmann M, Ksienzyk B, et al. Persistence of pre-leukemic clones during first remission and risk of relapse in acute myeloid leukemia. Leukemia. 2018;32(7):1598–1608. doi:10.1038/s41375-018-0034-z.
   PubMed Web of Science ®Google Scholar
• Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016;127(20):2391–2405. doi:10.1182/blood-2016-03-643544.
   PubMed Web of Science ®Google Scholar
• Döhner H, Estey E, Grimwade D, Amadori S, Appelbaum FR, Büchner T, Dombret H, Ebert BL, Fenaux P, Larson RA, et al. Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood. 2017;129(4):424–447. doi:10.1182/blood-2016-08-733196.
   PubMed Web of Science ®Google Scholar
• Bertoli S, Tavitian S, Huynh A, Borel C, Guenounou S, Luquet I, Delabesse E, Sarry A, Laurent G, Attal M, et al. Improved outcome for AML patients over the years 2000-2014. Blood Cancer J. 2017;7(12):635. doi:10.1038/s41408-017-0011-1.
   PubMed Web of Science ®Google Scholar
• Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet. 2000;356(9244):1795–1799. doi:10.1016/S0140-6736(00)03231-1.
   PubMed Web of Science ®Google Scholar
• Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097–2100. doi:10.1126/science.1068440.
   PubMed Web of Science ®Google Scholar
• Pegram HJ, Andrews DM, Smyth MJ, Darcy PK, Kershaw MH. Activating and inhibitory receptors of natural killer cells. Immunol Cell Biol. 2011;89(2):216–224. doi:10.1038/icb.2010.78.
   PubMed Web of Science ®Google Scholar
• Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell. 2010;142(6):847–856. doi:10.1016/j.cell.2010.08.031.
   PubMed Web of Science ®Google Scholar
• Sandoval-Borrego D, Moreno-Lafont MC, Vazquez-Sanchez EA, Gutierrez-Hoya A, López-Santiago R, Montiel-Cervantes LA, Ramírez-Saldaña M, Vela-Ojeda J. Overexpression of CD158 and NKG2A inhibitory receptors and underexpression of NKG2D and NKp46 activating receptors on NK cells in acute myeloid leukemia. Arch Med Res. 2016;47(1):55–64. doi:10.1016/j.arcmed.2016.02.001.
   PubMed Web of Science ®Google Scholar
• Sanchez-Correa B, Gayoso I, Bergua JM, Casado JG, Morgado S, Solana R, Tarazona R. Decreased expression of DNAM-1 on NK cells from acute myeloid leukemia patients. Immunol Cell Biol. 2012;90(1):109–115. doi:10.1038/icb.2011.15.
   PubMed Web of Science ®Google Scholar
• Fauriat C, Just-Landi S, Mallet F, Arnoulet C, Sainty D, Olive D, Costello RT. Deficient expression of NCR in NK cells from acute myeloid leukemia: evolution during leukemia treatment and impact of leukemia cells in NCR dull phenotype induction. Blood. 2007;109(1):323–330. doi:10.1182/blood-2005-08-027979.
   PubMed Web of Science ®Google Scholar
• Chretien AS, Fauriat C, Orlanducci F, Rey J, Borg GB, Gautherot E, Granjeaud S, Demerle C, Hamel JF, Cerwenka A, et al. NKp30 expression is a prognostic immune biomarker for stratification of patients with intermediate-risk acute myeloid leukemia. Oncotarget. 2017;8(30):49548–49563. doi:10.18632/oncotarget.17747.
   PubMedGoogle Scholar
• Chretien AS, Devillier R, Fauriat C, Orlanducci F, Harbi S, Le Roy A, Rey J, Bouvier Borg G, Gautherot E, Hamel JF, et al. NKp46 expression on NK cells as a prognostic and predictive biomarker for response to allo-SCT in patients with AML. Oncoimmunology. 2017;6(12):e1307491. doi:10.1080/2162402X.2017.1307491.
   PubMed Web of Science ®Google Scholar
• Nowbakht P, Ionescu MC, Rohner A, Kalberer CP, Rossy E, Mori L, Cosman D, De Libero G, Wodnar-Filipowicz A. Ligands for natural killer cell-activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias. Blood. 2005;105(9):3615–3622. doi:10.1182/blood-2004-07-2585.
   PubMed Web of Science ®Google Scholar
• Pende D, Spaggiari GM, Marcenaro S, Martini S, Rivera P, Capobianco A, Falco M, Lanino E, Pierri I, Zambello R, et al. Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: evidence for the involvement of the Poliovirus receptor (CD155) and Nectin-2 (CD112). Blood. 2005;105(5):2066–2073. doi:10.1182/blood-2004-09-3548.
   PubMed Web of Science ®Google Scholar
• Diermayr S, Himmelreich H, Durovic B, Mathys-Schneeberger A, Siegler U, Langenkamp U, Hofsteenge J, Gratwohl A, Tichelli A, Paluszewska M, et al. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood. 2008;111(3):1428–1436. doi:10.1182/blood-2007-07-101311.
   PubMed Web of Science ®Google Scholar
• Hilpert J, Grosse-Hovest L, Grünebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. JImmunol. 2012;189(3):1360–1371. doi:10.4049/jimmunol.1200796.
   PubMed Web of Science ®Google Scholar
• Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, Rammensee HG, Steinle A. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood. 2003;102(4):1389–1396. doi:10.1182/blood-2003-01-0019.
   PubMed Web of Science ®Google Scholar
• Stringaris K, Sekine T, Khoder A, Alsuliman A, Razzaghi B, Sargeant R, Pavlu J, Brisley G, de Lavallade H, Sarvaria A, et al. Leukemia-induced phenotypic and functional defects in natural killer cells predict failure to achieve remission in acute myeloid leukemia. Haematologica. 2014;99(5):836–847. doi:10.3324/haematol.2013.087536.
   PubMed Web of Science ®Google Scholar
• Geiger TL, Sun JC. Development and maturation of natural killer cells. Curr Opin Immunol. 2016;39:82–89. doi:10.1016/j.coi.2016.01.007.
   PubMed Web of Science ®Google Scholar
• Mundy-Bosse BL, Scoville SD, Chen L, McConnell K, Mao HC, Ahmed EH, Zorko N, Harvey S, Cole J, Zhang X, et al. MicroRNA-29b mediates altered innate immune development in acute leukemia. J Clin Invest. 2016;126(12):4404–4416. doi:10.1172/JCI85413.
   PubMed Web of Science ®Google Scholar
• Björkström NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, Björklund AT, Flodström-Tullberg M, Michaëlsson J, Rottenberg ME, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood. 2010;116(19):3853–3864. doi:10.1182/blood-2010-04-281675.
   PubMed Web of Science ®Google Scholar
• Chretien AS, Fauriat C, Orlanducci F, Galseran C, Rey J, Bouvier Borg G, Gautherot E, Granjeaud S, Hamel-Broza JF, Demerle C, et al. Natural killer defective maturation is associated with adverse clinical outcome in patients with acute myeloid leukemia. Front Immunol. 2017;8:573. doi:10.3389/fimmu.2017.00573.
   PubMed Web of Science ®Google Scholar
• O’Leary JG, Goodarzi M, Drayton DL, von Andrian UH. T cell- and B cell-independent adaptive immunity mediated by natural killer cells. Nat Immunol. 2006;7(5):507–516. doi:10.1038/ni1332.
   PubMed Web of Science ®Google Scholar
• Leong JW, Chase JM, Romee R, Schneider SE, Sullivan RP, Cooper MA, Fehniger TA. 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. 2014;20(4):463–473. doi:10.1016/j.bbmt.2014.01.006.
   PubMed Web of Science ®Google Scholar
• Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, Leong JW, Abdel-Latif S, Schneider SE, Willey S, et al. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. SciTransl Med. 2016;8(357):357ra123. doi:10.1126/scitranslmed.aaf2341.
   Web of Science ®Google Scholar
• Beldi-Ferchiou A, Caillat-Zucman S. Control of NK cell activation by immune checkpoint molecules. Int J Mol Sci. 2017;18(10): pii: E2129. doi:10.3390/ijms18102129.
   PubMed Web of Science ®Google Scholar
• Benson DM Jr, Bakan CE, Mishra A, Hofmeister CC, Efebera Y, Becknell B, Baiocchi RA, Zhang J, Yu J, Smith MK, et al. The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood. 2010;116(13):2286–2294. doi:10.1182/blood-2010-02-271874.
   PubMed Web of Science ®Google Scholar
• Liu Y, Cheng Y, Xu Y, Wang Z, Du X, Li C, Peng J, Gao L, Liang X, Ma C. Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive cancers. Oncogene. 2017;36(44):6143–6153. doi:10.1038/onc.2017.209.
   PubMed Web of Science ®Google Scholar
• Berthon C, Driss V, Liu J, Kuranda K, Leleu X, Jouy N, Hetuin D, Quesnel B. In acute myeloid leukemia, B7-H1 (PD-L1) protection of blasts from cytotoxic T cells is induced by TLR ligands and interferon-gamma and can be reversed using MEK inhibitors. Cancer Immunol Immunother. 2010;59(12):1839–1849. doi:10.1007/s00262-010-0909-y.
   PubMed Web of Science ®Google Scholar
• Goltz D, Gevensleben H, Grünen S, Dietrich J, Kristiansen G, Landsberg J, Dietrich D. PD-L1 (CD274) promoter methylation predicts survival in patients with acute myeloid leukemia. Leukemia. 2017;31(3):738–743. doi:10.1038/leu.2016.328.
   PubMed Web of Science ®Google Scholar
• Folgiero V, Cifaldi L, Li Pira G, Goffredo BM, Vinti L, Locatelli F. TIM-3/Gal-9 interaction induces IFNγ-dependent IDO1 expression in acute myeloid leukemia blast cells. J Hematol Oncol. 2015;8:36. doi:10.1186/s13045-015-0134-4.
   PubMed Web of Science ®Google Scholar
• Kikushige Y, Miyamoto T, Yuda J, Jabbarzadeh-Tabrizi S, Shima T, Takayanagi S, Niiro H, Yurino A, Miyawaki K, Takenaka K, et al. A TIM-3/Gal-9 autocrine stimulatory loop drives self-renewal of human myeloid leukemia stem cells and leukemic progression. Cell Stem Cell. 2015;17(3):341–352. doi:10.1016/j.stem.2015.07.011.
   PubMed Web of Science ®Google Scholar
• Wang M, Bu J, Zhou M, Sido J, Lin Y, Liu G, Lin Q, Xu X, Leavenworth JW, Shen E. CD8+T cells expressing both PD-1 and TIGIT but not CD226 are dysfunctional in acute myeloid leukemia (AML) patients. Clin Immunol. 2018;190:64–73. doi:10.1016/j.clim.2017.08.021.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Bi J, Zheng X, Chen Y, Wang H, Wu W, Wang Z, Wu Q, Peng H, Wei H, et al. Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat Immunol. 2018 Jun 18. [Epub ahead of print]. doi:10.1038/s41590-018-0132-0.
   Web of Science ®Google Scholar
• Rosenberg SA, Lotze MT, Muul LM, Chang AE, Avis FP, Leitman S, Linehan WM, Robertson CN, Lee RE, Rubin JT, et al. A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone. N Engl J Med. 1987;316(15):889–897. doi:10.1056/NEJM198704093161501.
   PubMed Web of Science ®Google Scholar
• Sievers EL, Lange BJ, Sondel PM, Krailo MD, Gan J, Liu-Mares W, Feig SA. Feasibility, toxicity, and biologic response of interleukin-2 after consolidation chemotherapy for acute myelogenous leukemia: a report from the Children’s Cancer Group. J ClinOncol. 1998;16(3):914–919. doi:10.1200/JCO.1998.16.3.914.
   PubMed Web of Science ®Google Scholar
• Ewen EM, Pahl JHW, Miller M, Watzl C, Cerwenka A. KIR downregulation by IL-12/15/18 unleashes human NK cells from KIR/HLA-I inhibition and enhances killing of tumor cells. Eur J Immunol. 2018;48(2):355–365. doi:10.1002/eji.201747128.
   PubMed Web of Science ®Google Scholar
• Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, French AR, Sunwoo JB, Lemieux S, Hansen TH, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436(7051):709–713. doi:10.1038/nature03847.
   PubMed Web of Science ®Google Scholar
• Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105(8):3051–3057. doi:10.1182/blood-2004-07-2974.
   PubMed Web of Science ®Google Scholar
• Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, Pui CH, Leung W. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28(6):955–959. doi:10.1200/JCO.2009.24.4590.
   PubMed Web of Science ®Google Scholar
• Curti A, Ruggeri L, Parisi S, Bontadini A, Dan E, Motta MR, Rizzi S, Trabanelli S, Ocadlikova, Lecciso M, et al. Larger size of donor alloreactive NKcell repertoire correlates with better response to NK cell immunotherapy in elderly acute myeloid leukemia patients. Clin Cancer Res. 2016;22(8):1914–1921. doi:10.1158/1078-0432.CCR-15-1604.
   PubMed Web of Science ®Google Scholar
• Ruggeri L, Mancusi A, Capanni M, Urbani E, Carotti A, Aloisi T, Stern M, Pende D, Perruccio K, Burchielli E, et al. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood. 2007;110(1):433–440. doi:10.1182/blood-2006-07-038687.
   PubMed Web of Science ®Google Scholar
• Cooper MA, Elliott JM, Keyel PA, Yang L, Carrero JA, Yokoyama WM. Cytokine-induced memory-like natural killer cells. Proc Natl Acad Sci U S A. 2009;106(6):1915–1919. doi:10.1073/pnas.0813192106.
   PubMed Web of Science ®Google Scholar
• Romee R, Schneider SE, Leong JW, Chase JM, Keppel CR, Sullivan RP, Cooper MA, Fehniger TA. Cytokine activation induces human memory-like NK cells. Blood. 2012;120(24):4751–4760. doi:10.1182/blood-2012-04-419283.
   PubMed Web of Science ®Google Scholar
• Cichocki F, Cooley S, Davis Z, DeFor TE, Schlums H, Zhang B, Brunstein CG, Blazar BR, Wagner J, Diamond DJ, et al. CD56dim CD57+ NKG2C+ NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia. 2016;30(2):456–463. doi:10.1038/leu.2015.260.
   PubMed Web of Science ®Google Scholar
• Parameswaran R, Ramakrishnan P, Moreton SA, Xia Z, Hou Y, Lee DA, Gupta K, deLima M, Beck RC, Wald DN. Repression of GSK3 restores NK cell cytotoxicity in AML patients. Nat Commun. 2016;7:11154. doi:10.1038/ncomms11154.
   PubMed Web of Science ®Google Scholar
• Lu X, Ohata K, Kondo Y, Espinoza JL, Qi Z, Nakao S. Hydroxyurea upregulates NKG2D ligand expression in myeloid leukemia cells synergistically with valproic acid and potentially enhances susceptibility of leukemic cells to natural killer cell-mediated cytolysis. Cancer Sci. 2010;101(3):609–615. doi:10.1111/j.1349-7006.2009.01439.x.
   PubMed Web of Science ®Google Scholar
• Poggi A, Catellani S, Garuti A, Pierri I, Gobbi M, Zocchi MR. Effective in vivo induction of NKG2D ligands in acute myeloid leukaemias by all-trans-retinoic acid or sodium valproate. Leukemia. 2009;23(4):641–648. doi:10.1038/leu.2008.354.
   PubMed Web of Science ®Google Scholar
• Elias S, Yamin R, Golomb L, Tsukerman P, Stanietsky-Kaynan N, Ben-Yehuda D, Mandelboim O. Immune evasion by oncogenic proteins of acute myeloid leukemia. Blood. 2014;123(10):1535–1543. doi:10.1182/blood-2013-09-526590.
   PubMed Web of Science ®Google Scholar
• BaragañoRaneros A, Martín-Palanco V, Fernandez AF, Rodriguez RM, Fraga MF, Lopez-Larrea C, Suarez-Alvarez B. Methylation of NKG2D ligands contributes to immune system evasion in acute myeloid leukemia. Genes Immun. 2015;16(1):71–82. doi:10.1038/gene.2014.58.
   PubMed Web of Science ®Google Scholar
• Raneros AB, Puras AM, Rodriguez RM, Colado E, Bernal T, Anguita E, Mogorron AV, Gil AC, Vidal-Castiñeira JR, Márquez-Kisinousky L, et al. Increasing TIMP3 expression by hypomethylating agents diminishes soluble MICA, MICB and ULBP2 shedding in acute myeloid leukemia, facilitating NK cell-mediated immune recognition. Oncotarget. 2017;8(19):31959–31976. doi:10.18632/oncotarget.16657.
   PubMedGoogle Scholar
• Poh SL, Linn YC. Immune checkpoint inhibitors enhance cytotoxicity of cytokine-induced killer cells against human myeloid leukaemic blasts. Cancer Immunol Immunother. 2016;65(5):525–536. doi:10.1007/s00262-016-1815-8.
   PubMed Web of Science ®Google Scholar
• Ohs I, Ducimetière L, Marinho J, Kulig P, Becher B, Tugues S. Restoration of natural killer cell antimetastatic activity by IL12 and checkpoint blockade. Cancer Res. 2017;77(24):7059–7071. doi:10.1158/0008-5472.CAN-17-1032.
   PubMed Web of Science ®Google Scholar
• Guo Y, Feng X, Jiang Y, Shi X, Xing X, Liu X, Li N, Fadeel B, Zheng C. PD1 blockade enhances cytotoxicity of in vitro expanded natural killer cells towards myeloma cells. Oncotarget. 2016;7(30):48360–48374. doi:10.18632/oncotarget.10235.
   PubMedGoogle Scholar
• Molgora M, Bonavita E, Ponzetta A, Riva F, Barbagallo M, Jaillon S, Popović B, Bernardini G, Magrini E, Gianni F, et al. IL-1R8 is a checkpoint in NK cells regulating anti-tumour and anti-viral activity. Nature. 2017;551(7678):110–114. doi:10.1038/nature24293.
   PubMed Web of Science ®Google Scholar
• June CH, Sadelain M. Chimeric antigen receptor therapy. N Engl J Med. 2018;379(1):64–73. doi:10.1056/NEJMra1706169.
   PubMed Web of Science ®Google Scholar
• Kenderian SS, Ruella M, Shestova O, Klichinsky M, Aikawa V, Morrissette JJ, Scholler J, Song D, Porter DL, Carroll M, et al. CD33-specific chimeric antigen receptor T cells exhibit potent preclinical activity against human acute myeloid leukemia. Leukemia. 2015;29(8):1637–1647. doi:10.1038/leu.2015.52.
   PubMed Web of Science ®Google Scholar
• Chen L, Mao H, Zhang J, Chu J, Devine S, Caligiuri MA, Yu J. Targeting FLT3 by chimeric antigen receptor T cells for the treatment of acute myeloid leukemia. Leukemia. 2017;31(8):1830–1834. doi:10.1038/leu.2017.147.
   PubMed Web of Science ®Google Scholar
• Mardiros A, Dos Santos C, McDonald T, Brown CE, Wang X, Budde LE, Hoffman L, Aguilar B, Chang WC, Bretzlaff W, et al. T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia. Blood. 2013;122(18):3138–3148. doi:10.1182/blood-2012-12-474056.
   PubMed Web of Science ®Google Scholar
• Perna F, Berman SH, Soni RK, Mansilla-Soto J, Eyquem J, Hamieh M, Hendrickson RC, Brennan CW, Sadelain M. Integrating proteomics and transcriptomics for systematic combinatorial chimeric antigen receptor therapy of AML. Cancer Cell. 2017;32(4):506–19.e5. doi:10.1016/j.ccell.2017.09.004.
   PubMed Web of Science ®Google Scholar
• Petrov JC, Wada M, Pinz KG, Yan LE, Chen KH, Shuai X, Liu H, Chen X, Leung LH, Salman H, et al. Compound CAR T-cells as a double-pronged approach for treating acute myeloid leukemia. Leukemia. 2018;32(6):1317–1326. doi:10.1038/s41375-018-0075-3.
   PubMed Web of Science ®Google Scholar
• Sentman CL, Meehan KR. NKG2D CARs as cell therapy for cancer. Cancer J. 2014;20(2):156–159. doi:10.1097/PPO.0000000000000029.
   PubMed Web of Science ®Google Scholar
• Weiss T, Weller M, Guckenberger M, Sentman CL, Roth P. NKG2D-based CAR T cells and radiotherapy exert synergistic efficacy in glioblastoma. Cancer Res. 2018;78(4):1031–1043. doi:10.1158/0008-5472.CAN-17-1788.
   PubMed Web of Science ®Google Scholar
• Fernández L, Metais JY, Escudero A, Vela M, Valentín J, Vallcorba I, Leivas A, Torres J, Valeri A, Patiño-García A, et al. Memory T cells expressing an NKG2D-CAR efficiently target osteosarcoma cells. Clin Cancer Res. 2017;23(19):5824–5835. doi:10.1158/1078-0432.CCR-17-0075.
   PubMed Web of Science ®Google Scholar
• Sentman ML, Murad JM, Cook WJ, Wu MR, Reder J, Baumeister SH, Dranoff G, Fanger MW, Sentman CL. Mechanisms of acute toxicity in NKG2D chimeric antigen receptor T cell-treated mice. J Immunol. 2016;197(12):4674–4685. doi:10.4049/jimmunol.1600769.
   PubMed Web of Science ®Google Scholar
• Zhang T, Wu MR, Sentman CL. An NKp30-based chimeric antigen receptor promotes T cell effector functions and antitumor efficacy in vivo. Immunol. 2012;189(5):2290–2299. doi:10.4049/jimmunol.1103495.
   Web of Science ®Google Scholar
• Wu MR, Zhang T, DeMars LR, Sentman CL. B7H6-specific chimeric antigen receptors lead to tumor elimination and host antitumor immunity. Gene Ther. 2015;22(8):675–684. doi:10.1038/gt.2015.29.
   PubMed Web of Science ®Google Scholar
• Gacerez AT, Hua CK, Ackerman ME, Sentman CL. Chimeric antigen receptors with human scFvs preferentially induce T cell anti-tumor activity against tumors with high B7H6 expression. Cancer Immunol Immunother. 2018;67(5):749–759. doi:10.1007/s00262-018-2124-1.
   PubMed Web of Science ®Google Scholar
• Liu D, Tian S, Zhang K, Xiong W, Lubaki NM, Chen Z, Han W. Chimeric antigen receptor (CAR)-modified natural killer cell-based immunotherapy and immunological synapse formation in cancer and HIV. Protein Cell. 2017;8(12):861–877. doi:10.1007/s13238-017-0415-5.
   PubMed Web of Science ®Google Scholar
• Tang X, Yang L, Li Z, Nalin AP, Dai H, Xu T, Yin J, You F, Zhu M, Shen W, 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):1083–1089.
   PubMed Web of Science ®Google Scholar