The Latest Breakthroughs in Immunotherapy for Acute Myeloid Leukemia, with a Special Focus on NKG2D Ligands
Abstract
:1. Introduction
2. Immunotherapeutic Strategies for AML
2.1. Immune Checkpoint Inhibitors (ICI)
2.2. T and Natural Killer-Based Cellular Therapies
2.3. Antibody-Based Approaches
3. Targeting NKG2D Ligands
3.1. NKG2D Receptor-Based Cellular Therapies
3.2. Drug-Mediated Increase of NKG2DL Gene Expression
3.3. ADCC and Antibody-Mediated Inhibition of MICA and MICB Shedding
Preclinical Data | Clinical Data | |
---|---|---|
NKG2D-based cellular therapies | ||
NKG2D CAR-T cells | NCT03466320 NCT02203825 NCT04658004 NCT03018405 | |
NKG2D CAR-NK cells | NCT05247957 NCT04623944 | |
NKG2DL induction | ||
PARP1 inhibition | siRNA, AG-14361 [48] | NCT05319249 |
HDAC inhibition | Romidepsin [50] | |
Valproic acid [51,64] | ||
HMA | 5azaC and DAC [49] | |
other | all-trans-retinoic acid [64] | |
Ab targeting of NKG2DL | ||
ADCC induction | NKG2D-Fc-ADCC [52] | |
bispecific | NKG2D-CD3/CD16 [53] | |
shedding inhibition | [50] |
4. Conclusions
5. Patents
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Terwilliger, T.; Abdul-Hay, M. Acute lymphoblastic leukemia: A comprehensive review and 2017 update. Blood Cancer J. 2017, 7, e577. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vakiti, A.; Mewawalla, P. Acute Myeloid Leukemia. In StatPearls; StatPearls Publishing LLC.: Treasure Island, FL, USA, 2022. [Google Scholar]
- Saultz, J.N.; Garzon, R. Acute Myeloid Leukemia: A Concise Review. J. Clin. Med. 2016, 5, 33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xing, S.; Ferrari de Andrade, L. NKG2D and MICA/B shedding: A ‘tag game’ between NK cells and malignant cells. Clin. Transl. Immunol. 2020, 9, e1230. [Google Scholar] [CrossRef]
- Cen, D.; Hu, G.; Zhou, Y.; Yang, L.; Chen, S.; Schmidt, C.A.; Li, Y. Enhancement of specific cellular immune response induced by DNA vaccines encoding PML-RARalpha and hIL-2 genes. Hematology 2010, 15, 88–95. [Google Scholar] [CrossRef] [PubMed]
- Gambacortipasserini, C.; Grignani, F.; Arienti, F.; Pandolfi, P.P.; Pelicci, P.G.; Parmiani, G. Human Cd4 Lymphocytes Specifically Recognize a Peptide Representing the Fusion Region of the Hybrid Protein Pml Rar-Alpha Present in Acute Promyelocytic Leukemia-Cells. Blood 1993, 81, 1369–1375. [Google Scholar] [CrossRef] [Green Version]
- Jetani, H.; Garcia-Cadenas, I.; Nerreter, T.; Thomas, S.; Rydzek, J.; Meijide, J.B.; Bonig, H.; Herr, W.; Sierra, J.; Einsele, H.; et al. CAR T-cells targeting FLT3 have potent activity against FLT3(-)ITD(+) AML and act synergistically with the FLT3-inhibitor crenolanib. Leukemia 2018, 32, 1168–1179. [Google Scholar] [CrossRef]
- Greiner, J.; Goetz, M.; Schuler, P.J.; Bulach, C.; Hofmann, S.; Schrezenmeier, H.; Dohner, H.; Schneider, V.; Guinn, B.A. Enhanced stimulation of antigen-specific immune responses against nucleophosmin 1 mutated acute myeloid leukaemia by an anti-programmed death 1 antibody. Br. J. Haematol. 2022, 198, 866–874. [Google Scholar] [CrossRef]
- Rosenblatt, J.; Stone, R.M.; Uhl, L.; Neuberg, D.; Joyce, R.; Levine, J.D.; Arnason, J.; McMasters, M.; Luptakova, K.; Jain, S.; et al. Individualized vaccination of AML patients in remission is associated with induction of antileukemia immunity and prolonged remissions. Sci. Transl. Med. 2016, 8, 368ra171. [Google Scholar] [CrossRef] [Green Version]
- Goodyear, O.; Agathanggelou, A.; Novitzky-Basso, I.; Siddique, S.; McSkeane, T.; Ryan, G.; Vyas, P.; Cavenagh, J.; Stankovic, T.; Moss, P.; et al. Induction of a CD8+ T-cell response to the MAGE cancer testis antigen by combined treatment with azacitidine and sodium valproate in patients with acute myeloid leukemia and myelodysplasia. Blood 2010, 116, 1908–1918. [Google Scholar] [CrossRef] [Green Version]
- Gutierrez-Cosio, S.; de la Rica, L.; Ballestar, E.; Santamaria, C.; Sanchez-Abarca, L.I.; Caballero-Velazquez, T.; Blanco, B.; Calderon, C.; Herrero-Sanchez, C.; Carrancio, S.; et al. Epigenetic regulation of PRAME in acute myeloid leukemia is different compared to CD34+ cells from healthy donors: Effect of 5-AZA treatment. Leukemia Res. 2012, 36, 895–899. [Google Scholar] [CrossRef]
- Polakova, K.; Bandzuchova, E.; Sabty, F.A.; Mistrik, M.; Demitrovicova, L.; Russ, G. Activation of HLA-G expression by 5-aza-2′-deoxycytidine in malignant hematopoetic cells isolated from leukemia patients. Neoplasma 2009, 56, 514–520. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Davids, M.S.; Kim, H.T.; Bachireddy, P.; Costello, C.; Liguori, R.; Savell, A.; Lukez, A.P.; Avigan, D.; Chen, Y.B.; McSweeney, P.; et al. Ipilimumab for Patients with Relapse after Allogeneic Transplantation. N. Engl. J. Med. 2016, 375, 143–153. [Google Scholar] [CrossRef] [PubMed]
- Garcia, J.S.; Werner, L.; Tomlinson, B.K.; Keng, M.; Nahas, M.; Brunner, A.; Khaled, S.K.; Savell, A.; Luskin, M.; Steensma, D.P.; et al. Clinical and Immunologic Activity of Ipilimumab Following Decitabine Priming in Post-Allogeneic Transplant and Transplant-Naive Patients with Relapsed or Refractory Myelodysplastic Syndromes and Acute Myeloid Leukemia: A Multi-Center Phase 1, Two-Arm, Dose-Escalation Study. Blood 2019, 134, 2015. [Google Scholar] [CrossRef]
- Gojo, I.; Stuart, R.K.; Webster, J.; Blackford, A.; Varela, J.C.; Morrow, J.; DeZern, A.E.; Foster, M.C.; Levis, M.J.; Coombs, C.C.; et al. Multi-Center Phase 2 Study of Pembroluzimab (Pembro) and Azacitidine (AZA) in Patients with Relapsed/Refractory Acute Myeloid Leukemia (AML) and in Newly Diagnosed (>=65 Years) AML Patients. Blood 2019, 134, 832. [Google Scholar] [CrossRef]
- Lindblad, K.E.; Thompson, J.; Gui, G.G.; Valdez, J.; Worthy, T.; Tekleab, H.; Hughes, T.; Goswami, M.; Oetjen, K.; Kim, D.Y.; et al. Pembrolizumab and Decitabine for Refractory or Relapsed Acute Myeloid Leukemia. Blood 2018, 132, 1437. [Google Scholar] [CrossRef]
- Zeidan, A.M.; Cavenagh, J.; Voso, M.T.; Taussig, D.; Tormo, M.; Boss, I.; Copeland, W.B.; Gray, V.E.; Previtali, A.; O’Connor, T.; et al. Efficacy and Safety of Azacitidine (AZA) in Combination with the Anti-PD-L1 Durvalumab (durva) for the Front-Line Treatment of Older Patients (pts) with Acute Myeloid Leukemia (AML) Who Are Unfit for Intensive Chemotherapy (IC) and Pts with Higher-Risk Myelodysplastic Syndromes (HR-MDS): Results from a Large, International, Randomized Phase 2 Study. Blood 2019, 134, 829. [Google Scholar] [CrossRef]
- Daver, N.; Garcia-Manero, G.; Basu, S.; Boddu, P.C.; Alfayez, M.; Cortes, J.E.; Konopleva, M.; Ravandi-Kashani, F.; Jabbour, E.; Kadia, T.; et al. Efficacy, Safety, and Biomarkers of Response to Azacitidine and Nivolumab in Relapsed/Refractory Acute Myeloid Leukemia: A Nonrandomized, Open-Label, Phase II Study. Cancer Discov. 2019, 9, 370–383. [Google Scholar] [CrossRef] [Green Version]
- Daver, N.G.; Garcia-Manero, G.; Konopleva, M.Y.; Alfayez, M.; Pemmaraju, N.; Kadia, T.M.; DiNardo, C.D.; Cortes, J.E.; Ravandi, F.; Abbas, H. Azacitidine (AZA) with nivolumab (Nivo), and AZA with Nivo+ ipilimumab (Ipi) in relapsed/refractory acute myeloid leukemia: A non-randomized, prospective, phase 2 study. Blood 2019, 134, 830. [Google Scholar] [CrossRef]
- André, P.; Denis, C.; Soulas, C.; Bourbon-Caillet, C.; Lopez, J.; Arnoux, T.; Bléry, M.; Bonnafous, C.; Gauthier, L.; Morel, A. Anti-NKG2A mAb is a checkpoint inhibitor that promotes anti-tumor immunity by unleashing both T and NK cells. Cell 2018, 175, 1731-1743.e13. [Google Scholar] [CrossRef] [Green Version]
- Ruggeri, L.; Urbani, E.; André, P.; Mancusi, A.; Tosti, A.; Topini, F.; Bléry, M.; Animobono, L.; Romagné, F.; Wagtmann, N. Effects of anti-NKG2A antibody administration on leukemia and normal hematopoietic cells. Haematologica 2016, 101, 626–633. [Google Scholar] [CrossRef]
- Devillier, R.; Furst, S.; Chammard, A.B.; Pagliardini, T.; Harbi, S.; Maisano, V.; Granata, A.; Legrand, F.; Pakradouni, J.; Boher, J.M.; et al. Safety of Anti-NKG2A Blocking Antibody Monalizumab As Maintenance Therapy after Allogeneic Hematopoietic Stem Cell Transplantation: A Phase I Study. Blood 2021, 138, 1817. [Google Scholar] [CrossRef]
- Perna, F.; Espinoza-Gutarra, M.R.; Bombaci, G.; Farag, S.S.; Schwartz, J.E. Immune-Based Therapeutic Interventions for Acute Myeloid Leukemia. Cancer Treat. Res. 2022, 183, 225–254. [Google Scholar] [CrossRef] [PubMed]
- Brunner, A.M.; Esteve, J.; Porkka, K.; Knapper, S.; Vey, N.; Scholl, S.; Garcia-Manero, G.; Wermke, M.; Janssen, J.; Traer, E.; et al. Efficacy and Safety of Sabatolimab (MBG453) in Combination with Hypomethylating Agents (HMAs) in Patients with Acute Myeloid Leukemia (AML) and High-Risk Myelodysplastic Syndrome (HR-MDS): Updated Results from a Phase 1b Study. Blood 2020, 136, 1–2. [Google Scholar] [CrossRef]
- Riether, C.; Pabst, T.; Hopner, S.; Bacher, U.; Hinterbrandner, M.; Banz, Y.; Muller, R.; Manz, M.G.; Gharib, W.H.; Francisco, D.; et al. Targeting CD70 with cusatuzumab eliminates acute myeloid leukemia stem cells in patients treated with hypomethylating agents. Nat. Med. 2020, 26, 1459–1467. [Google Scholar] [CrossRef]
- Bewersdorf, J.P.; Shallis, R.M.; Zeidan, A.M. Immune checkpoint inhibition in myeloid malignancies: Moving beyond the PD-1/PD-L1 and CTLA-4 pathways. Blood Rev. 2021, 45, 100709. [Google Scholar] [CrossRef]
- Passweg, J.R.; Baldomero, H.; Chabannon, C.; Basak, G.W.; Corbacioglu, S.; Duarte, R.; Dolstra, H.; Lankester, A.C.; Mohty, M.; Montoto, S.; et al. The EBMT activity survey on hematopoietic-cell transplantation and cellular therapy 2018: CAR-T’s come into focus. Bone Marrow. Transplant. 2020, 55, 1604–1613. [Google Scholar] [CrossRef] [Green Version]
- Walter, R.B.; Gooley, T.A.; Wood, B.L.; Milano, F.; Fang, M.; Sorror, M.L.; Estey, E.H.; Salter, A.I.; Lansverk, E.; Chien, J.W.; et al. Impact of pretransplantation minimal residual disease, as detected by multiparametric flow cytometry, on outcome of myeloablative hematopoietic cell transplantation for acute myeloid leukemia. J. Clin. Oncol. 2011, 29, 1190–1197. [Google Scholar] [CrossRef] [Green Version]
- Vago, L.; Gojo, I. Immune escape and immunotherapy of acute myeloid leukemia. J. Clin. Investig. 2020, 130, 1552–1564. [Google Scholar] [CrossRef]
- Ruggeri, L.; Parisi, S.; Urbani, E.; Curti, A. Alloreactive Natural Killer Cells for the Treatment of Acute Myeloid Leukemia: From Stem Cell Transplantation to Adoptive Immunotherapy. Front. Immunol. 2015, 6, 479. [Google Scholar] [CrossRef] [Green Version]
- Berrien-Elliott, M.M.; Foltz, J.A.; Russler-Germain, D.A.; Neal, C.C.; Tran, J.; Gang, M.; Wong, P.; Fisk, B.; Cubitt, C.C.; Marin, N.D.; et al. Hematopoietic cell transplantation donor-derived memory-like NK cells functionally persist after transfer into patients with leukemia. Sci. Transl. Med. 2022, 14, eabm1375. [Google Scholar] [CrossRef]
- Han, K.P.; Zhu, X.; Liu, B.; Jeng, E.; Kong, L.; Yovandich, J.L.; Vyas, V.V.; Marcus, W.D.; Chavaillaz, P.A.; Romero, C.A.; et al. IL-15:IL-15 receptor alpha superagonist complex: High-level co-expression in recombinant mammalian cells, purification and characterization. Cytokine 2011, 56, 804–810. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Q.S.; Wang, Y.; Lv, H.Y.; Han, Q.W.; Fan, H.; Guo, B.; Wang, L.L.; Han, W.D. Treatment of CD33-directed chimeric antigen receptor-modified T cells in one patient with relapsed and refractory acute myeloid leukemia. Mol. Ther. 2015, 23, 184–191. [Google Scholar] [CrossRef] [Green Version]
- Liu, E.L.; Marin, D.; Banerjee, P.; Macapinlac, H.A.; Thompson, P.; Basar, R.; Kerbauy, L.N.; Overman, B.; Thall, P.; Kaplan, M.; et al. Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors. N. Eng. J. Med. 2020, 382, 545–553. [Google Scholar] [CrossRef]
- Godwin, C.D.; McDonald, G.B.; Walter, R.B. Sinusoidal obstruction syndrome following CD33-targeted therapy in acute myeloid leukemia. Blood 2017, 129, 2330–2332. [Google Scholar] [CrossRef] [Green Version]
- Xie, G.; Ivica, N.A.; Jia, B.; Li, Y.; Dong, H.; Liang, Y.; Brown, D.; Romee, R.; Chen, J. CAR-T cells targeting a nucleophosmin neoepitope exhibit potent specific activity in mouse models of acute myeloid leukaemia. Nat. Biomed. Eng. 2021, 5, 399–413. [Google Scholar] [CrossRef] [PubMed]
- Dong, H.; Ham, J.D.; Hu, G.; Xie, G.; Vergara, J.; Liang, Y.; Ali, A.; Tarannum, M.; Donner, H.; Baginska, J.; et al. Memory-like NK cells armed with a neoepitope-specific CAR exhibit potent activity against NPM1 mutated acute myeloid leukemia. Proc. Natl. Acad. Sci. USA 2022, 119, e2122379119. [Google Scholar] [CrossRef] [PubMed]
- Sekeres, M.A.; Lancet, J.E.; Wood, B.L.; Grove, L.E.; Sandalic, L.; Sievers, E.L.; Jurcic, J.G. Randomized phase IIb study of low-dose cytarabine and lintuzumab versus low-dose cytarabine and placebo in older adults with untreated acute myeloid leukemia. Haematologica 2013, 98, 119–128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Daver, N.; Vyas, P.; Kambhampati, S.; Malki, M.A.; Larson, R.; Asch, A.; Mannis, G.; Chai-Ho, W.; Tanaka, T.; Bradley, T.; et al. AML-464 Tolerability and Efficacy of the First-In-Class Anti-CD47 Antibody Magrolimab Combined With Azacitidine in Frontline Patients With TP53-Mutated Acute Myeloid Leukemia (AML): Phase 1b Results. Clin. Lymphoma Myeloma Leuk. 2022, 22 (Suppl. 2), S253–S254. [Google Scholar] [CrossRef]
- Bauer, S.; Groh, V.; Wu, J.; Steinle, A.; Phillips, J.H.; Lanier, L.L.; Spies, T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285, 727–729. [Google Scholar] [CrossRef]
- Groh, V.; Rhinehart, R.; Randolph-Habecker, J.; Topp, M.S.; Riddell, S.R.; Spies, T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2001, 2, 255–260. [Google Scholar] [CrossRef]
- Raulet, D.H.; Gasser, S.; Gowen, B.G.; Deng, W.; Jung, H. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 2013, 31, 413–441. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hilpert, J.; Grosse-Hovest, L.; Grunebach, F.; Buechele, C.; Nuebling, T.; Raum, T.; Steinle, A.; Salih, H.R. Comprehensive analysis of NKG2D ligand expression and release in leukemia: Implications for NKG2D-mediated NK cell responses. J. Immunol. 2012, 189, 1360–1371. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sallman, D.A.; Brayer, J.B.; Poire, X.; Havelange, V.; Awada, A.; Lewalle, P.; Odunsi, K.; Wang, E.S.; Lonez, C.; Lequertier, T.; et al. Results from the Completed Dose-Escalation of the Hematological Arm of the Phase I Think Study Evaluating Multiple Infusions of NKG2D-Based CAR T-Cells As Standalone Therapy in Relapse/Refractory Acute Myeloid Leukemia and Myelodysplastic Syndrome Patients. Blood 2019, 134, 3826. [Google Scholar] [CrossRef]
- Al-Homsi, A.S.; Purev, E.; Lewalle, P.; Abdul-Hay, M.; Pollyea, D.A.; Salaroli, A.; Lequertier, T.; Alcantar-Orozco, E.; Borghese, F.; Lonez, C.; et al. Interim Results from the Phase I Deplethink Trial Evaluating the Infusion of a NKG2D CAR T-Cell Therapy Post a Non-Myeloablative Conditioning in Relapse or Refractory Acute Myeloid Leukemia and Myelodysplastic Syndrome Patients. Blood 2019, 134, 3844. [Google Scholar] [CrossRef]
- Baumeister, S.H.; Murad, J.; Werner, L.; Daley, H.; Trebeden-Negre, H.; Gicobi, J.K.; Schmucker, A.; Reder, J.; Sentman, C.L.; Gilham, D.E.; et al. Phase I Trial of Autologous CAR T Cells Targeting NKG2D Ligands in Patients with AML/MDS and Multiple Myeloma. Cancer Immunol. Res. 2019, 7, 100–112. [Google Scholar] [CrossRef]
- Mason, D.M.; Friedensohn, S.; Weber, C.R.; Jordi, C.; Wagner, B.; Meng, S.M.; Ehling, R.A.; Bonati, L.; Dahinden, J.; Gainza, P.; et al. Optimization of therapeutic antibodies by predicting antigen specificity from antibody sequence via deep learning. Nat. Biomed. Eng. 2021, 5, 600–612. [Google Scholar] [CrossRef] [PubMed]
- Paczulla, A.M.; Rothfelder, K.; Raffel, S.; Konantz, M.; Steinbacher, J.; Wang, H.; Tandler, C.; Mbarga, M.; Schaefer, T.; Falcone, M.; et al. Absence of NKG2D ligands defines leukaemia stem cells and mediates their immune evasion. Nature 2019, 572, 254–259. [Google Scholar] [CrossRef]
- Baragano Raneros, A.; Martin-Palanco, V.; Fernandez, A.F.; Rodriguez, R.M.; Fraga, M.F.; Lopez-Larrea, C.; Suarez-Alvarez, B. Methylation of NKG2D ligands contributes to immune system evasion in acute myeloid leukemia. Genes Immun. 2015, 16, 71–82. [Google Scholar] [CrossRef]
- Alves da Silva, P.H.; Xing, S.; Kotini, A.G.; Papapetrou, E.P.; Song, X.; Wucherpfennig, K.W.; Mascarenhas, J.; Ferrari de Andrade, L. MICA/B antibody induces macrophage-mediated immunity against acute myeloid leukemia. Blood 2022, 139, 205–216. [Google Scholar] [CrossRef]
- 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, 1428–1436. [Google Scholar] [CrossRef]
- Steinbacher, J.; Baltz-Ghahremanpour, K.; Schmiedel, B.J.; Steinle, A.; Jung, G.; Kubler, A.; Andre, M.C.; Grosse-Hovest, L.; Salih, H.R. An Fc-optimized NKG2D-immunoglobulin G fusion protein for induction of natural killer cell reactivity against leukemia. Int. J. Cancer 2015, 136, 1073–1084. [Google Scholar] [CrossRef]
- Marklin, M.; Hagelstein, I.; Koerner, S.P.; Rothfelder, K.; Pfluegler, M.S.; Schumacher, A.; Grosse-Hovest, L.; Jung, G.; Salih, H.R. Bispecific NKG2D-CD3 and NKG2D-CD16 fusion proteins for induction of NK and T cell reactivity against acute myeloid leukemia. J. Immunother. Cancer 2019, 7, 143. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kaiser, B.K.; Yim, D.; Chow, I.T.; Gonzalez, S.; Dai, Z.; Mann, H.H.; Strong, R.K.; Groh, V.; Spies, T. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 2007, 447, 482–486. [Google Scholar] [CrossRef] [PubMed]
- Boutet, P.; Agüera-González, S.; Atkinson, S.; Pennington, C.J.; Edwards, D.R.; Murphy, G.; Reyburn, H.T.; Valés-Gómez, M. Cutting edge: The metalloproteinase ADAM17/TNF-alpha-converting enzyme regulates proteolytic shedding of the MHC class I-related chain B protein. J. Immunol. 2009, 182, 49–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Waldhauer, I.; Goehlsdorf, D.; Gieseke, F.; Weinschenk, T.; Wittenbrink, M.; Ludwig, A.; Stevanovic, S.; Rammensee, H.G.; Steinle, A. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008, 68, 6368–6376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Badrinath, S.; Dellacherie, M.O.; Li, A.; Zheng, S.W.; Zhang, X.X.; Sobral, M.; Pyrdol, J.W.; Smith, K.L.; Lu, Y.H.; Haag, S.; et al. A vaccine targeting resistant tumours by dual T cell plus NK cell attack. Nature 2022, 606, 992–998. [Google Scholar] [CrossRef]
- Ferrari de Andrade, L.; Tay, R.E.; Pan, D.; Luoma, A.M.; Ito, Y.; Badrinath, S.; Tsoucas, D.; Franz, B.; May, K.F., Jr.; Harvey, C.J.; et al. Antibody-mediated inhibition of MICA and MICB shedding promotes NK cell-driven tumor immunity. Science 2018, 359, 1537–1542. [Google Scholar] [CrossRef] [Green Version]
- de Andrade, L.F.; Kumar, S.; Luoma, A.M.; Ito, Y.; da Silva, P.H.A.; Pan, D.; Pyrdol, J.W.; Yoon, C.H.; Wucherpfennig, K.W. Inhibition of MICA and MICB Shedding Elicits NK-Cell–Mediated Immunity against Tumors Resistant to Cytotoxic T Cells. Cancer Immunol. Res. 2020, 8, 769–780. [Google Scholar] [CrossRef] [Green Version]
- Armeanu, S.; Bitzer, M.; Lauer, U.M.; Venturelli, S.; Pathil, A.; Krusch, M.; Kaiser, S.; Jobst, J.; Smirnow, I.; Wagner, A.; et al. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res. 2005, 65, 6321–6329. [Google Scholar] [CrossRef] [Green Version]
- Skov, S.; Pedersen, M.T.; Andresen, L.; Straten, P.T.; Woetmann, A.; Odum, N. Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-related chain A and B. Cancer Res. 2005, 65, 11136–11145. [Google Scholar] [CrossRef]
- Zhang, C.; Wang, Y.; Zhou, Z.; Zhang, J.; Tian, Z. Sodium butyrate upregulates expression of NKG2D ligand MICA/B in HeLa and HepG2 cell lines and increases their susceptibility to NK lysis. Cancer Immunol. Immun. 2009, 58, 1275–1285. [Google Scholar] [CrossRef] [PubMed]
- Chu, Y.; Yahr, A.; Huang, B.; Ayello, J.; Barth, M.; Cairo, S.M. 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, e1341031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Poggi, A.; Catellani, S.; Garuti, A.; Pierri, I.; Gobbi, M.; Zocchi, M.R. Effective in vivo induction of NKG2D ligands in acute myeloid leukaemias by all-trans-retinoic acid or sodium valproate. Leukemia 2009, 23, 641–648. [Google Scholar] [CrossRef]
- Jaiswal, S.; Jamieson, C.H.; Pang, W.W.; Park, C.Y.; Chao, M.P.; Majeti, R.; Traver, D.; van Rooijen, N.; Weissman, I.L. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009, 138, 271–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pietsch, E.C.; Dong, J.; Cardoso, R.; Zhang, X.; Chin, D.; Hawkins, R.; Dinh, T.; Zhou, M.; Strake, B.; Feng, P.H.; et al. Anti-leukemic activity and tolerability of anti-human CD47 monoclonal antibodies. Blood Cancer J. 2017, 7, e536. [Google Scholar] [CrossRef] [PubMed]
- Willingham, S.B.; Volkmer, J.P.; Gentles, A.J.; Sahoo, D.; Dalerba, P.; Mitra, S.S.; Wang, J.; Contreras-Trujillo, H.; Martin, R.; Cohen, J.D.; et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc. Natl. Acad. Sci. USA 2012, 109, 6662–6667. [Google Scholar] [CrossRef] [PubMed]
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Maurer, S.; Zhong, X.; Prada, B.D.; Mascarenhas, J.; de Andrade, L.F. The Latest Breakthroughs in Immunotherapy for Acute Myeloid Leukemia, with a Special Focus on NKG2D Ligands. Int. J. Mol. Sci. 2022, 23, 15907. https://doi.org/10.3390/ijms232415907
Maurer S, Zhong X, Prada BD, Mascarenhas J, de Andrade LF. The Latest Breakthroughs in Immunotherapy for Acute Myeloid Leukemia, with a Special Focus on NKG2D Ligands. International Journal of Molecular Sciences. 2022; 23(24):15907. https://doi.org/10.3390/ijms232415907
Chicago/Turabian StyleMaurer, Stefanie, Xiaoxuan Zhong, Betsy Deza Prada, John Mascarenhas, and Lucas Ferrari de Andrade. 2022. "The Latest Breakthroughs in Immunotherapy for Acute Myeloid Leukemia, with a Special Focus on NKG2D Ligands" International Journal of Molecular Sciences 23, no. 24: 15907. https://doi.org/10.3390/ijms232415907
APA StyleMaurer, S., Zhong, X., Prada, B. D., Mascarenhas, J., & de Andrade, L. F. (2022). The Latest Breakthroughs in Immunotherapy for Acute Myeloid Leukemia, with a Special Focus on NKG2D Ligands. International Journal of Molecular Sciences, 23(24), 15907. https://doi.org/10.3390/ijms232415907