Thymic NK-Cells and Their Potential in Cancer Immunotherapy

References

• Huntington ND, Vosshenrich CAJ, Di Santo JP. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat Rev Immunol. 2007;7(9):703–714. doi:10.1038/nri2154
   PubMed Web of Science ®Google Scholar
• Amand M, Iserentant G, Poli A, et al. Human CD56dimCD16dimCells as an individualized natural killer cell subset. Front Immunol. 2017;8:699. doi:10.3389/fimmu.2017.00699
   PubMed Web of Science ®Google Scholar
• Abel AM, Yang C, Thakar MS, et al. Natural killer cells: development, maturation, and clinical utilization. Front Immunol. 2018;9:1869. doi:10.3389/fimmu.2018.01869
   PubMed Web of Science ®Google Scholar
• Michaud A, Dardari R, Charrier E, et al. IL-7 enhances survival of human CD56bright NK cells. J Immunother. 2010;33(4):382–390. doi:10.1097/CJI.0b013e3181cd872d
   PubMed Web of Science ®Google Scholar
• Wu SY, Fu T, Jiang YZ, et al. Natural killer cells in cancer biology and therapy. Mol Cancer. 2020;19(1):120. doi:10.1186/s12943-020-01238-x
   PubMed Web of Science ®Google Scholar
• Molgora M, Cortez VS, Colonna M. Killing the invaders: NK cell impact in tumors and anti-tumor therapy. Cancers. 2021;13(4):595. doi:10.3390/cancers13040595
   PubMed Web of Science ®Google Scholar
• Raulet DH. Missing self recognition and self tolerance of natural killer (NK) cells. Semin Immunol. 2006;18(3):145–150. doi:10.1016/j.smim.2006.03.003
   PubMed Web of Science ®Google Scholar
• Cornel AM, Mimpen IL, Nierkens S. MHC class I downregulation in cancer: underlying mechanisms and potential targets for cancer immunotherapy. Cancers. 2020;12(7):1760. doi:10.3390/cancers12071760
   PubMed Web of Science ®Google Scholar
• Vosshenrich CAJ, García-Ojeda ME, Samson-Villéger SI, et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol. 2006;7(11):1217–1224. doi:10.1038/ni1395
   PubMed Web of Science ®Google Scholar
• Lanier LL, Spits H, Phillips JH. The developmental relationship between NK cells and T cells. Immunol Today. 1992;13(10):392–395. doi:10.1016/0167-5699(92)90087-N
   PubMedGoogle Scholar
• Spits H, Blom B, Jaleco AC, et al. Early stages in the development of human T, natural killer and thymic dendritic cells. Immunol Rev. 1998;165:75–86. doi:10.1111/j.1600-065X.1998.tb01231.x
   PubMed Web of Science ®Google Scholar
• Hashemi E, Malarkannan S. Tissue-Resident NK cells: development, maturation, and clinical relevance. Cancers. 2020;12(6):1553. doi:10.3390/cancers12061553
   PubMed Web of Science ®Google Scholar
• Vargas CL, Poursine-Laurent J, Yang L, et al. Development of thymic NK cells from double negative 1 thymocyte precursors. Blood. 2011;118(13):3570–3578. doi:10.1182/blood-2011-06-359679
   PubMed Web of Science ®Google Scholar
• De Smedt M, Taghon T, Van De Walle I, et al. Notch signaling induces cytoplasmic CD3ε expression in human differentiating NK cells. Blood. 2007;110(7):2696–2703. doi:10.1182/blood-2007-03-082206
   PubMed Web of Science ®Google Scholar
• Alves PCM, De Angelo Andrade LAL, Petta CA, et al. Ex vivo Expansion of CD56 + NK and NKT-like lymphocytes from peripheral blood mononuclear cells of patients with ovarian neoplasia. Scand J Immunol. 2011;74(3):244–252. doi:10.1111/j.1365-3083.2011.02576.x
   PubMed Web of Science ®Google Scholar
• Bi J, Wang X. Molecular regulation of NK cell maturation. Front Immunol. 2020;11:1945. doi:10.3389/fimmu.2020.01945
   PubMed Web of Science ®Google Scholar
• Yu H, Fehniger TA, Fuchshuber P, et al. Flt3 ligand promotes the generation of a distinct CD34+ human natural killer cell progenitor that responds to interleukin-15. Blood. 1998;92(10):3647–3657. doi:10.1182/blood.V92.10.3647
   PubMed Web of Science ®Google Scholar
• Grzywacz B, Kataria N, Sikora M, et al. Coordinated acquisition of inhibitory and activating receptors and functional properties by developing human natural killer cells. Blood. 2006;108(12):3824–3833. doi:10.1182/blood-2006-04-020198
   PubMed Web of Science ®Google Scholar
• Di Santo JP, Vosshenrich CAJ. Bone marrow versus thymic pathways of natural killer cell development. Immunol Rev. 2006;214:35–46. doi:10.1111/j.1600-065X.2006.00461.x
   PubMed Web of Science ®Google Scholar
• Freud AG, Yu J, Caligiuri MA. Human natural killer cell development in secondary lymphoid tissues. Semin Immunol. 2014;26(2):132–137. doi:10.1016/j.smim.2014.02.008
   PubMed Web of Science ®Google Scholar
• Di Santo JP. Natural killer cell developmental pathways: a question of balance. Annu Rev Immunol. 2006;24:257–286. doi:10.1146/annurev.immunol.24.021605.090700
   PubMed Web of Science ®Google Scholar
• Valero-Pacheco N, Beaulieu AM. Transcriptional regulation of mouse tissue-resident natural killer cell development. Front Immunol. 2020;11:309. doi:10.3389/fimmu.2020.00309
   PubMed Web of Science ®Google Scholar
• Gabrielli S, Sun M, Bell A, et al. Murine thymic NK cells are distinct from ILC1s and have unique transcription factor requirements. Eur J Immunol. 2017;47(5):800–805. doi:10.1002/eji.201646871
   PubMed Web of Science ®Google Scholar
• Ribeiro VSG, Hasan M, Wilson A, et al. Cutting edge: thymic NK cells develop independently from T cell precursors. J Immunol. 2010;185(9):4993–4997. doi:10.4049/jimmunol.1002273
   PubMed Web of Science ®Google Scholar
• Veinotte LL, Halim TYF, Takei F. Unique subset of natural killer cells develops from progenitors in lymph node. Blood. 2008;111(8):4201–4208. doi:10.1182/blood-2007-04-087577
   PubMed Web of Science ®Google Scholar
• Veinotte LL, Greenwood CP, Mohammadi N, et al. Expression of rearranged TCRγ genes in natural killer cells suggests a minor thymus-dependent pathway of lineage commitment. Blood. 2006;107(7):2673–2679. doi:10.1182/blood-2005-07-2797
   PubMed Web of Science ®Google Scholar
• Nozad Charoudeh H, Tang Y, Cheng M, et al. Identification of an NK/T cell-restricted progenitor in adult bone marrow contributing to bone marrow- and thymic-dependent NK cells. Blood. 2010;116(2):183–192. doi:10.1182/blood-2009-10-247130
   PubMed Web of Science ®Google Scholar
• Van De Walle I, Dolens AC, Durinck K, et al. GATA3 induces human T-cell commitment by restraining Notch activity and repressing NK-cell fate. Nat Commun. 2016;7:11171. doi:10.1038/ncomms11171
   PubMed Web of Science ®Google Scholar
• Stewart CA, Walzer T, Robbins SH, et al. Germ-line and rearranged Tcrd transcription distinguish bona fide NK cells and NK-like γδ T cells. Eur J Immunol. 2007;37(6):1442–1452. doi:10.1002/eji.200737354
   PubMed Web of Science ®Google Scholar
• Gerstner S, Köhler W, Heidkamp G, et al. Specific phenotype and function of CD56-expressing innate immune cell subsets in human thymus. J Leukoc Biol. 2016;100(6):1297–1310. doi:10.1189/jlb.1A0116-038R
   PubMed Web of Science ®Google Scholar
• Krabbendam L, Bernink JH, Spits H. Innate lymphoid cells: from helper to killer. Curr Opin Immunol. 2021;68:28–33. doi:10.1016/j.coi.2020.08.007
   PubMed Web of Science ®Google Scholar
• Seillet C, Brossay L, Vivier E. Natural killers or ILC1s? That is the question. Curr Opin Immunol. 2021;68:48–53. doi:10.1016/j.coi.2020.08.009
   PubMed Web of Science ®Google Scholar
• Shin SB, McNagny KM. ILC-you in the thymus: a fresh look at innate lymphoid cell development. Front Immunol. 2021;12:681110. doi:10.3389/fimmu.2021.681110
   PubMed Web of Science ®Google Scholar
• Spits H, Cupedo T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu Rev Immunol. 2012;30:647–675. doi:10.1146/annurev-immunol-020711-075053
   PubMed Web of Science ®Google Scholar
• Vivier E, Artis D, Colonna M, et al. Innate Lymphoid Cells: 10 Years On. Cell. 2018;174(5):1054–1066. doi:10.1016/j.cell.2018.07.017
   PubMed Web of Science ®Google Scholar
• Krijgsman D, Hokland M, Kuppen PJK. The role of natural killer T cells in cancer-A phenotypical and functional approach. Front Immunol. 2018;9:367. doi:10.3389/fimmu.2018.00367
   PubMed Web of Science ®Google Scholar
• Dhodapkar MV, Kumar V. Type II Natural Killer T (NKT) cells and their emerging role in health and disease. J Immunol. 2017;198(3):1015–1021. doi:10.4049/jimmunol.1601399
   PubMedGoogle Scholar
• Albano F, Vecchio E, Renna M, et al. Insights into thymus development and viral thymic infections. Viruses. 2019;11(9):836. doi:10.3390/v11090836
   PubMed Web of Science ®Google Scholar
• Kaszubowska L, Foerster J, Kwiatkowski P, et al. NKT-like cells reveal higher than T lymphocytes expression of cellular protective proteins HSP70 and SOD2 and comparably increased expression of SIRT1 in the oldest seniors. Folia Histochem Cytobiol. 2018;56(4):231–240. doi:10.5603/FHC.a2018.0025
   PubMed Web of Science ®Google Scholar
• Almeida JS, Couceiro P, López-Sejas N, et al. NKT-like (CD3+CD56+) cells in chronic myeloid leukemia patients treated with tyrosine kinase inhibitors. Front Immunol. 2019;10:2493. doi:10.3389/fimmu.2019.02493
   PubMed Web of Science ®Google Scholar
• Yu J, Mitsui T, Wei M, et al. NKp46 identifies an NKT cell subset susceptible to leukemic transformation in mouse and human. J Clin Invest. 2011;121(4):1456–1470. doi:10.1172/JCI43242
   PubMed Web of Science ®Google Scholar
• Seillet C, Huntington ND, Gangatirkar P, et al. Differential requirement for Nfil3 during NK cell development. J Immunol. 2014;192(6):2667–2676. doi:10.4049/jimmunol.1302605
   PubMed Web of Science ®Google Scholar
• Pistoia V, Tumino N, Vacca P, et al. Human γδ T-cells: from surface receptors to the therapy of high-risk leukemias. Front Immunol. 2018;9:984. doi:10.3389/fimmu.2018.00984
   PubMed Web of Science ®Google Scholar
• Parker ME, Ciofani M. Regulation of γδ T cell effector diversification in the thymus. Front Immunol. 2020;11:42. doi:10.3389/fimmu.2020.00042
   PubMed Web of Science ®Google Scholar
• Sánchez MJ, Spits H, Lanier LL, et al. Human natural killer cell committed thymocytes and their relation to the T cell lineage. J Exp Med. 1993;178(6):1857–1866. doi:10.1084/jem.178.6.1857
   PubMed Web of Science ®Google Scholar
• Li YR, Zhou K, Wilson M, et al. Mucosal-associated invariant T cells for cancer immunotherapy. Mol Ther. 2023;31(3):631–646. doi:10.1016/j.ymthe.2022.11.019
   PubMed Web of Science ®Google Scholar
• Godfrey DI, Koay HF, McCluskey J, et al. The biology and functional importance of MAIT cells. Nat Immunol. 2019;20(9):1110–1128. doi:10.1038/s41590-019-0444-8
   PubMed Web of Science ®Google Scholar
• De Smedt M, Hoebeke I, Reynvoet K, et al. Different thresholds of Notch signaling bias human precursor cells toward B-, NK-, monocytic/dendritic-, or T-cell lineage in thymus microenvironment. Blood. 2005;106(10):3498–3506. doi:10.1182/blood-2005-02-0496
   PubMed Web of Science ®Google Scholar
• Woo SY, Jung YJ, Ryu KH, et al. In vitro differentiation of natural killer T cells from human cord blood CD34 + cells. Br J Haematol. 2003;121(1):148–156. doi:10.1046/j.1365-2141.2003.04230.x
   PubMed Web of Science ®Google Scholar
• Ritz J, Campen TJ, Schmidt RE, et al. Analysis of T-cell receptor gene rearrangement and expression in human natural killer clones. Science. 1985;228(4707):1540–1543. doi:10.1126/science.2409597
   PubMed Web of Science ®Google Scholar
• Rodewald HR, Moingeon P, Lucich JL, et al. A population of early fetal thymocytes expressing FcγRII III contains precursors of T lymphocytes and natural killer cells. Cell. 1992;69(1):139–150. doi:10.1016/0092-8674(92)90125-V
   PubMed Web of Science ®Google Scholar
• Klein Wolterink RGJ, García-Ojeda ME, Vosshenrich CAJ, et al. The intrathymic crossroads of T and NK cell differentiation. Immunol Rev. 2010;238(1):126–137. doi:10.1111/j.1600-065X.2010.00960.x
   PubMedGoogle Scholar
• Vaz F, Srour EF, Almeida-Porada G, et al. Human thymic stroma supports human natural killer (NK) cell development from immature progenitors. Cell Immunol. 1998;186(2):133–139. doi:10.1006/cimm.1998.1303
   PubMed Web of Science ®Google Scholar
• Michie AM, Carlyle JR, Schmitt TM, et al. Clonal characterization of a bipotent T Cell and NK cell progenitor in the mouse fetal thymus. J Immunol. 2000;164(4):1730–1733. doi:10.4049/jimmunol.164.4.1730
   PubMed Web of Science ®Google Scholar
• Hidalgo L, Martínez VG, Valencia J, et al. Expression of BMPRIA on human thymic NK cell precursors: role of BMP signaling in intrathymic NK cell development. Blood. 2012;119(8):1861–1871. doi:10.1182/blood-2011-07-370650
   PubMed Web of Science ®Google Scholar
• Cheng M, Nozad Charoudeh H, Brodin P, et al. Distinct and overlapping patterns of cytokine regulation of thymic and bone marrow-derived NK cell development. J Immunol. 2009;182(3):1460–1468. doi:10.4049/jimmunol.182.3.1460
   PubMed Web of Science ®Google Scholar
• Wagner JA, Rosario M, Romee R, et al. CD56bright NK cells exhibit potent antitumor responses following IL-15 priming. J Clin Invest. 2017;127(11):4042–4058. doi:10.1172/JCI90387
   PubMed Web of Science ®Google Scholar
• Björkström NK, Ljunggren HG, Michaëlsson J. Emerging insights into natural killer cells in human peripheral tissues. Nat Rev Immunol. 2016;16(5):310–320. doi:10.1038/nri.2016.34
   PubMed Web of Science ®Google Scholar
• Hansson M, Kärre K, Kiessling R, et al. Natural NK-cell targets in the mouse thymus: characteristics of the sensitive cell population. J Immunol. 1979;123(2):765–771. doi:10.4049/jimmunol.123.2.765
   PubMed Web of Science ®Google Scholar
• Garni-Wagner BA, Witte PL, Tutt MM, et al. Natural killer cells in the thymus. Studies in mice with severe combined immune deficiency. J Immunol. 1990;144(3):796–803. doi:10.4049/jimmunol.144.3.796
   PubMed Web of Science ®Google Scholar
• Schott E, Bonasio R, Ploegh HL. Elimination in vivo of developing T cells by natural killer cells. J Exp Med. 2003;198(8):1213–1224. doi:10.1084/jem.20030918
   PubMed Web of Science ®Google Scholar
• McNerney KO, Karageorgos SA, Hogarty MD, et al. Enhancing neuroblastoma immunotherapies by engaging iNKT and NK cells. Front Immunol. 2020;11:873. doi:10.3389/fimmu.2020.00873
   PubMed Web of Science ®Google Scholar
• Chu J, Gao F, Yan M, et al. Natural killer cells: a promising immunotherapy for cancer. J Transl Med. 2022;20(1):240. doi:10.1186/s12967-022-03437-0
   PubMed Web of Science ®Google Scholar
• Spel L, Schiepers A, Boes M. NFκB and MHC-1 Interplay in Neuroblastoma and Immunotherapy. Trends Cancer. 2018;4(11):715–717. doi:10.1016/j.trecan.2018.09.006
   PubMed Web of Science ®Google Scholar
• Pasqualini C, Kozaki T, Bruschi M, et al. Modeling the interaction between the microenvironment and tumor cells in brain tumors. Neuron. 2020;108(6):1025–1044. doi:10.1016/j.neuron.2020.09.018
   PubMed Web of Science ®Google Scholar
• Spel L, Boelens JJ, Van Der Steen DM, et al. Natural killer cells facilitate PRAME-specific T-cell reactivity against neuroblastoma. Oncotarget. 2015;6(34):35770–35781. doi:10.18632/oncotarget.5657
   PubMedGoogle Scholar
• Custers L, Khabirova E, Coorens THH, et al. Somatic mutations and single-cell transcriptomes reveal the root of malignant rhabdoid tumours. Nat Commun. 2021;12(1):1407. doi:10.1038/s41467-021-21675-6
   PubMed Web of Science ®Google Scholar
• Yarmarkovich M, Maris JM. When cold is hot: immune checkpoint inhibition therapy for rhabdoid tumors. Cancer Cell. 2019;36(6):575–576. doi:10.1016/j.ccell.2019.11.006
   PubMed Web of Science ®Google Scholar
• Karahan ZS, Aras M, Sütlü T. TCR-NK cells: a novel source for adoptive immunotherapy of cancer. Turk J Hematol. 2023;40(1):1–10. doi:10.4274/tjh.galenos.2023.2022.0534
   PubMed Web of Science ®Google Scholar
• Lowe E, Truscott LC, De Oliveira SN. In vitro generation of human NK cells expressing chimeric antigen receptor through differentiation of gene- modified hematopoietic stem cells. Methods Mol Biol. 2016;1441:241–251.
   PubMedGoogle Scholar
• Dolstra H, Roeven MWH, 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. 2017;23(15):4107–4118. doi:10.1158/1078-0432.CCR-16-2981
   PubMed Web of Science ®Google Scholar
• Lehmann D, Spanholtz J, Osl M, et al. Ex vivo generated natural killer cells acquire typical natural killer receptors and display a cytotoxic gene expression profile similar to peripheral blood natural killer cells. Stem Cells Dev. 2012;21(16):2926–2938. doi:10.1089/scd.2011.0659
   PubMed Web of Science ®Google Scholar
• Spanholtz J, Preijers F, Tordoir M, et al. Clinical-grade generation of active NK cells from cord blood hematopoietic progenitor cells for immunotherapy using a closed-system culture process. PLoS One. 2011;6(6):e20740. doi:10.1371/journal.pone.0020740
   PubMed Web of Science ®Google Scholar
• Li YR, Dunn ZS, Yu Y, et al. Advancing cell-based cancer immunotherapy through stem cell engineering. Cell Stem Cell. 2023;30(5):592–610. doi:10.1016/j.stem.2023.02.009
   PubMed Web of Science ®Google Scholar