Natural Killer cells at the frontline in the fight against cancer.
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
23 Aug 2024
23 Aug 2024
Historique:
received:
23
02
2024
accepted:
05
08
2024
revised:
31
07
2024
medline:
24
8
2024
pubmed:
24
8
2024
entrez:
23
8
2024
Statut:
epublish
Résumé
Natural Killer (NK) cells are innate immune cells that play a pivotal role as first line defenders in the anti-tumor response. To prevent tumor development, NK cells are searching for abnormal cells within the body and appear to be key players in immunosurveillance. Upon recognition of abnormal cells, NK cells will become activated to destroy them. In order to fulfill their anti-tumoral function, they rely on the secretion of lytic granules, expression of death receptors and production of cytokines. Additionally, NK cells interact with other cells in the tumor microenvironment. In this review, we will first focus on NK cells' activation and cytotoxicity mechanisms as well as NK cells behavior during serial killing. Lastly, we will review NK cells' crosstalk with the other immune cells present in the tumor microenvironment.
Identifiants
pubmed: 39179536
doi: 10.1038/s41419-024-06976-0
pii: 10.1038/s41419-024-06976-0
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
614Subventions
Organisme : Fondation pour la Recherche Médicale (Foundation for Medical Research in France)
ID : FDT202304016765
Organisme : Fondation pour la Recherche Médicale (Foundation for Medical Research in France)
ID : FDT202304016666
Organisme : Institut National Du Cancer (French National Cancer Institute)
ID : PRT-K program 2021 (2021-014)
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-10-LABX-53
Organisme : Fondation ARC pour la Recherche sur le Cancer (ARC Foundation for Cancer Research)
ID : ARCPJA2021060003768
Informations de copyright
© 2024. The Author(s).
Références
Kiessling R, Klein E, Wigzell H. ‘’Natural’’ killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur J Immunol. 1975;5:112–7.
pubmed: 1234049
doi: 10.1002/eji.1830050208
Kiessling R, Petranyi G, Klein G, Wigzel H. Genetic variation of in vitro cytolytic activity and in vivo rejection potential of non-immunized semi-syngeneic mice against a mouse lymphoma line. Int J Cancer. 1975;15:933–40.
pubmed: 1150347
doi: 10.1002/ijc.2910150608
Savoy SKA, Boudreau JE. The evolutionary arms race between virus and NK cells: diversity enables population-level virus control. Viruses. 2019;11:959.
pubmed: 31627371
pmcid: 6832630
doi: 10.3390/v11100959
Wu SY, Fu T, Jiang YZ, Shao ZM. Natural killer cells in cancer biology and therapy. Mol Cancer. 2020;19:120.
pubmed: 32762681
pmcid: 7409673
doi: 10.1186/s12943-020-01238-x
Liu M, Liang S, Zhang C. NK cells in autoimmune diseases: protective or pathogenic? Front Immunol. 2021;12:624687.
pubmed: 33777006
pmcid: 7994264
doi: 10.3389/fimmu.2021.624687
Kucuksezer UC, Aktas Cetin E, Esen F, Tahrali I, Akdeniz N, Gelmez MY, et al. The role of natural killer cells in autoimmune diseases. Front Immunol. 2021;12:622306.
pubmed: 33717125
pmcid: 7947192
doi: 10.3389/fimmu.2021.622306
Li Y, Wang F, Imani S, Tao L, Deng Y, Cai Y. Natural killer cells: friend or foe in metabolic diseases? Front Immunol. 2021;12:614429.
pubmed: 33717101
pmcid: 7943437
doi: 10.3389/fimmu.2021.614429
Romagnani C, Juelke K, Falco M, Morandi B, D’Agostino A, Costa R, et al. CD56brightCD16− killer Ig-like receptor− NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J Immunol. 2007;178:4947–55.
pubmed: 17404276
doi: 10.4049/jimmunol.178.8.4947
Chan A, Hong DL, Atzberger A, Kollnberger S, Filer AD, Buckley CD, et al. CD56bright human NK cells differentiate into cd56dim cells: role of contact with peripheral fibroblasts. J Immunol. 2007;179:89–94.
pubmed: 17579025
doi: 10.4049/jimmunol.179.1.89
Cooper MA, Fehniger TA, Turner SC, Chen KS, Ghaheri BA, Ghayur T, et al. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood. 2001;97:3146–51.
pubmed: 11342442
doi: 10.1182/blood.V97.10.3146
Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol Balt Md 1950. 1989;143:3183–91.
Björkström NK, Ljunggren HG, Michaëlsson J. Emerging insights into natural killer cells in human peripheral tissues. Nat Rev Immunol. 2016;16:310–20.
pubmed: 27121652
doi: 10.1038/nri.2016.34
Wagner JA, Rosario M, Romee R, Berrien-Elliott MM, Schneider SE, Leong JW, et al. CD56bright NK cells exhibit potent antitumor responses following IL-15 priming. J Clin Invest. 2017;127:4042–58.
pubmed: 28972539
pmcid: 5663359
doi: 10.1172/JCI90387
Yu J, Freud AG, Caligiuri MA. Location and cellular stages of natural killer cell development. Trends Immunol. 2013;34:573–82.
pubmed: 24055329
doi: 10.1016/j.it.2013.07.005
Crinier A, Milpied P, Escalière B, Piperoglou C, Galluso J, Balsamo A, et al. High-dimensional single-cell analysis identifies organ-specific signatures and conserved NK cell subsets in humans and mice. Immunity. 2018;49:971–986.e5.
pubmed: 30413361
pmcid: 6269138
doi: 10.1016/j.immuni.2018.09.009
Gordon SM, Chaix J, Rupp LJ, Wu J, Madera S, Sun JC, et al. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity. 2012;36:55–67.
pubmed: 22261438
pmcid: 3381976
doi: 10.1016/j.immuni.2011.11.016
Wong P, Foltz JA, Chang L, Neal CC, Yao T, Cubitt CC, et al. T-BET and EOMES sustain mature human NK cell identity and antitumor function. J Clin Invest. 2023;133:e162530.
pubmed: 37279078
pmcid: 10313375
doi: 10.1172/JCI162530
Persyn E, Wahlen S, Kiekens L, Van Loocke W, Siwe H, Van Ammel E, et al. IRF2 is required for development and functional maturation of human NK cells. Front Immunol. 2022;13:1038821.
pubmed: 36544762
pmcid: 9762550
doi: 10.3389/fimmu.2022.1038821
Crinier A, Narni-Mancinelli E, Ugolini S, Vivier E. SnapShot: natural killer cells. Cell. 2020;180:1280–1280.e1.
pubmed: 32200803
doi: 10.1016/j.cell.2020.02.029
Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM. In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci. 2000;97:2731–6.
pubmed: 10694580
pmcid: 15998
doi: 10.1073/pnas.050588297
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 Lond Engl. 2000;356:1795–9.
doi: 10.1016/S0140-6736(00)03231-1
Seymour F, Cavenagh JD, Mathews J, Gribben JG. NK cells CD56bright and CD56dim subset cytokine loss and exhaustion is associated with impaired survival in myeloma. Blood Adv. 2022;6:5152–9.
pubmed: 35834731
pmcid: 9631618
doi: 10.1182/bloodadvances.2022007905
Shafer D, Smith MR, Borghaei H, Millenson MM, Li T, Litwin S, et al. Low NK cell counts in peripheral blood are associated with inferior overall survival in patients with follicular lymphoma. Leuk Res. 2013;37:1213–5.
pubmed: 23968916
pmcid: 3976217
doi: 10.1016/j.leukres.2013.07.038
Nersesian S, Schwartz SL, Grantham SR, MacLean LK, Lee SN, Pugh-Toole M, et al. NK cell infiltration is associated with improved overall survival in solid cancers: A systematic review and meta-analysis. Transl Oncol. 2021;14:100930.
pubmed: 33186888
doi: 10.1016/j.tranon.2020.100930
Ichise H, Tsukamoto S, Hirashima T, Konishi Y, Oki C, Tsukiji S, et al. Functional visualization of NK cell-mediated killing of metastatic single tumor cells. Rothlin CV, editor. eLife. 2022;11:e76269.
pubmed: 35113018
pmcid: 8849286
doi: 10.7554/eLife.76269
Bakir B, Chiarella AM, Pitarresi JR, Rustgi AK. EMT, MET, plasticity, and tumor metastasis. Trends Cell Biol. 2020;30:764–76.
pubmed: 32800658
pmcid: 7647095
doi: 10.1016/j.tcb.2020.07.003
Chockley PJ, Chen J, Chen G, Beer DG, Standiford TJ, Keshamouni VG. Epithelial-mesenchymal transition leads to NK cell–mediated metastasis-specific immunosurveillance in lung cancer. J Clin Invest. 2018;128:1384–96.
pubmed: 29324443
pmcid: 5873856
doi: 10.1172/JCI97611
Vyas M, Requesens M, Nguyen TH, Peigney D, Azin M, Demehri S. Natural killer cells suppress cancer metastasis by eliminating circulating cancer cells. Front Immunol. 2023;13:1098445.
pubmed: 36733396
pmcid: 9887278
doi: 10.3389/fimmu.2022.1098445
Zhang W, Zhao Z, Li F. Natural killer cell dysfunction in cancer and new strategies to utilize NK cell potential for cancer immunotherapy. Mol Immunol. 2022;144:58–70.
pubmed: 35203022
doi: 10.1016/j.molimm.2022.02.015
Dean I, Lee CYC, Tuong ZK, Li Z, Tibbitt CA, Willis C, et al. Rapid functional impairment of natural killer cells following tumor entry limits anti-tumor immunity. Nat Commun. 2024;15:683.
pubmed: 38267402
pmcid: 10808449
doi: 10.1038/s41467-024-44789-z
Mace EM, Dongre P, Hsu HT, Sinha P, James AM, Mann SS, et al. Cell biological steps and checkpoints in accessing NK cell cytotoxicity. Immunol Cell Biol. 2014;92:245–55.
pubmed: 24445602
pmcid: 3960583
doi: 10.1038/icb.2013.96
Mace EM, Zhang J, Siminovitch KA, Takei F. Elucidation of the integrin LFA-1–mediated signaling pathway of actin polarization in natural killer cells. Blood. 2010;116:1272–9.
pubmed: 20472831
doi: 10.1182/blood-2009-12-261487
Barber DF, Faure M, Long EO. LFA-1 contributes an early signal for NK cell cytotoxicity. J Immunol Balt Md 1950. 2004;173:3653–9.
Brown ACN, Dobbie IM, Alakoskela JM, Davis I, Davis DM. Super-resolution imaging of remodeled synaptic actin reveals different synergies between NK cell receptors and integrins. Blood. 2012;120:3729–40.
pubmed: 22966166
pmcid: 4238744
doi: 10.1182/blood-2012-05-429977
Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005;202:1001–12.
pubmed: 16203869
pmcid: 2213171
doi: 10.1084/jem.20051143
Nitta T, Yagita H, Sato K, Okumura K. Involvement of CD56 (NKH-1/Leu-19 antigen) as an adhesion molecule in natural killer-target cell interaction. J Exp Med. 1989;170:1757–61.
pubmed: 2478655
doi: 10.1084/jem.170.5.1757
Gunesch JT, Dixon AL, Ebrahim TA, Berrien-Elliott MM, Tatineni S, Kumar T, et al. CD56 regulates human NK cell cytotoxicity through Pyk2. eLife. 2020;9:e57346.
pubmed: 32510326
pmcid: 7358009
doi: 10.7554/eLife.57346
Wang MS, Hu Y, Sanchez EE, Xie X, Roy NH, de Jesus M, et al. Mechanically active integrins target lytic secretion at the immune synapse to facilitate cellular cytotoxicity. Nat Commun. 2022;13:3222.
pubmed: 35680882
pmcid: 9184626
doi: 10.1038/s41467-022-30809-3
Orange JS. Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol. 2008;8:713–25.
pubmed: 19172692
pmcid: 2772177
doi: 10.1038/nri2381
Ham H, Medlyn M, Billadeau DD. Locked and loaded: mechanisms regulating natural killer cell lytic granule biogenesis and release. Front Immunol. 2022;13:871106.
pubmed: 35558071
pmcid: 9088006
doi: 10.3389/fimmu.2022.871106
Netter P, Anft M, Watzl C. Termination of the activating NK cell immunological synapse is an active and regulated process. J Immunol Balt Md 1950. 2017;199:2528–35.
Chan CJ, Smyth MJ, Martinet L. Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ. 2014;21:5–14.
pubmed: 23579243
doi: 10.1038/cdd.2013.26
Medjouel Khlifi H, Guia S, Vivier E, Narni-Mancinelli E. Role of the ITAM-bearing receptors expressed by natural killer cells in cancer. Front Immunol. 2022;13:898745.
pubmed: 35757695
pmcid: 9231431
doi: 10.3389/fimmu.2022.898745
Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9:495–502.
pubmed: 18425106
pmcid: 2669298
doi: 10.1038/ni1581
Pogge von Strandmann E, Simhadri VR, von Tresckow B, Sasse S, Reiners KS, Hansen HP, et al. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity. 2007;27:965–74.
pubmed: 18055229
doi: 10.1016/j.immuni.2007.10.010
Cao G, Wang J, Zheng X, Wei H, Tian Z, Sun R. Tumor therapeutics work as stress inducers to enhance tumor sensitivity to natural killer (NK) cell cytolysis by up-regulating NKp30 ligand B7-H6. J Biol Chem. 2015;290:29964–73.
pubmed: 26472927
pmcid: 4705966
doi: 10.1074/jbc.M115.674010
Rusakiewicz S, Perier A, Semeraro M, Pitt JM, Pogge von Strandmann E, Reiners KS, et al. NKp30 isoforms and NKp30 ligands are predictive biomarkers of response to imatinib mesylate in metastatic GIST patients. OncoImmunology. 2017;6:e1137418.
pubmed: 28197361
doi: 10.1080/2162402X.2015.1137418
Chretien AS, Fauriat C, Orlanducci F, Rey J, Borg GB, Gautherot E, et al. NKp30 expression is a prognostic immune biomarker for stratification of patients with intermediate-risk acute myeloid leukemia. Oncotarget. 2017;8:49548–63.
pubmed: 28548938
pmcid: 5564787
doi: 10.18632/oncotarget.17747
Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest. 2011;121:3609–22.
pubmed: 21841316
pmcid: 3171102
doi: 10.1172/JCI45816
Costello RT, Knoblauch B, Sanchez C, Mercier D, Le Treut T, Sébahoun G. Expression of natural killer cell activating receptors in patients with chronic lymphocytic leukaemia. Immunology. 2012;135:151–7.
pubmed: 22044312
pmcid: 3277717
doi: 10.1111/j.1365-2567.2011.03521.x
Gutierrez‐Silerio GY, Bueno‐Topete MR, Vega‐Magaña AN, Bastidas‐Ramirez BE, Gutierrez‐Franco J, Escarra‐Senmarti M, et al. Non‐fitness status of peripheral NK cells defined by decreased NKP30 and perforin, and increased soluble B7H6, in cervical cancer patients. Immunology. 2023;168:538–53.
pubmed: 36271832
doi: 10.1111/imm.13593
Parodi M, Favoreel H, Candiano G, Gaggero S, Sivori S, Mingari MC, et al. NKp44-NKp44 ligand interactions in the regulation of natural killer cells and other innate lymphoid cells in humans. Front Immunol. 2019;10:719.
pubmed: 31024551
pmcid: 6465645
doi: 10.3389/fimmu.2019.00719
Shemesh A, Brusilovsky M, Hadad U, Teltsh O, Edri A, Rubin E, et al. Survival in acute myeloid leukemia is associated with NKp44 splice variants. Oncotarget. 2016;7:32933–45.
pubmed: 27102296
pmcid: 5078064
doi: 10.18632/oncotarget.8782
Marrufo AM, Mathew SO, Chaudhary P, Malaer JD, Ahmed N, Vishwanatha JK, et al. Blocking PCNA interaction with NKp44 enhances primary natural killer cell-mediated lysis of triple-negative breast cancer cells. Am J Cancer Res. 2023;13:1082–90.
pubmed: 37034219
pmcid: 10077055
Barrow AD, Edeling MA, Trifonov V, Luo J, Goyal P, Bohl B, et al. Natural killer cells control tumor growth by sensing a growth factor. Cell. 2018;172:534–548.e19.
pubmed: 29275861
doi: 10.1016/j.cell.2017.11.037
Gaggero S, Bruschi M, Petretto A, Parodi M, Del Zotto G, et al. Nidogen-1 is a novel extracellular ligand for the NKp44 activating receptor. Oncoimmunology. 2018;7:e1470730.
pubmed: 30228939
pmcid: 6140582
doi: 10.1080/2162402X.2018.1470730
Zhang B, Xu C, Liu J, Yang J, Gao Q, Ye F. Nidogen-1 expression is associated with overall survival and temozolomide sensitivity in low-grade glioma patients. Aging. 2021;13:9085–107.
pubmed: 33735110
pmcid: 8034893
doi: 10.18632/aging.202789
Baychelier F, Sennepin A, Ermonval M, Dorgham K, Debré P, Vieillard V. Identification of a cellular ligand for the natural cytotoxicity receptor NKp44. Blood. 2013;122:2935–42.
pubmed: 23958951
doi: 10.1182/blood-2013-03-489054
Blackhall FH, Merry CLR, Davies EJ, Jayson GC. Heparan sulfate proteoglycans and cancer. Br J Cancer. 2001;85:1094–8.
pubmed: 11710818
pmcid: 2375159
doi: 10.1054/bjoc.2001.2054
Hershkovitz O, Jivov S, Bloushtain N, Zilka A, Landau G, Bar-Ilan A, et al. Characterization of the recognition of tumor cells by the natural cytotoxicity receptor, NKp44. Biochemistry. 2007;46:7426–36.
pubmed: 17536787
doi: 10.1021/bi7000455
Rossi GR, Gonçalves JP, McCulloch T, Delconte RB, Hennessy RJ, Huntington ND, et al. The antitumor effect of heparin is not mediated by direct NK cell activation. J Clin Med. 2020;9:2666.
pubmed: 32824699
pmcid: 7463539
doi: 10.3390/jcm9082666
Sivori S, Pende D, Bottino C, Marcenaro E, Pessino A, Biassoni R, et al. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur J Immunol. 1999;29:1656–66.
pubmed: 10359120
doi: 10.1002/(SICI)1521-4141(199905)29:05<1656::AID-IMMU1656>3.0.CO;2-1
Chretien AS, Devillier R, Fauriat C, Orlanducci F, Harbi S, Le Roy A, 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:e1307491.
pubmed: 29209559
pmcid: 5706596
doi: 10.1080/2162402X.2017.1307491
Garcia-Iglesias T, Del Toro-Arreola A, Albarran-Somoza B, Del Toro-Arreola S, Sanchez-Hernandez PE, Ramirez-Dueñas MG, et al. Low NKp30, NKp46 and NKG2D expression and reduced cytotoxic activity on NK cells in cervical cancer and precursor lesions. BMC Cancer. 2009;9:186.
pubmed: 19531227
pmcid: 2704222
doi: 10.1186/1471-2407-9-186
Krijgsman D, de Vries NL, Skovbo A, Andersen MN, Swets M, Bastiaannet E, et al. Characterization of circulating T-, NK-, and NKT cell subsets in patients with colorectal cancer: the peripheral blood immune cell profile. Cancer Immunol Immunother. 2019;68:1011–24.
pubmed: 31053876
pmcid: 6529387
doi: 10.1007/s00262-019-02343-7
Sen Santara S, Lee DJ, Crespo Â, Hu JJ, Walker C, Ma X, et al. The NK cell receptor NKp46 recognizes ecto-calreticulin on ER-stressed cells. Nature. 2023;616:348–56.
pubmed: 37020026
pmcid: 10165876
doi: 10.1038/s41586-023-05912-0
Liu P, Zhao L, Kepp O, Kroemer G. Quantitation of calreticulin exposure associated with immunogenic cell death. Methods Enzymol. 2020;632:1–13.
pubmed: 32000891
doi: 10.1016/bs.mie.2019.05.011
Textor S, Fiegler N, Arnold A, Porgador A, Hofmann TG, Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res. 2011;71:5998–6009.
pubmed: 21764762
doi: 10.1158/0008-5472.CAN-10-3211
Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, et al. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity. 2008;28:571–80.
pubmed: 18394936
pmcid: 3528789
doi: 10.1016/j.immuni.2008.02.016
Dhar P, Wu JD. NKG2D and its ligands in cancer. Curr Opin Immunol. 2018;51:55–61.
pubmed: 29525346
pmcid: 6145810
doi: 10.1016/j.coi.2018.02.004
Hu B, Xin Y, Hu G, Li K, Tan Y. Fluid shear stress enhances natural killer cell’s cytotoxicity toward circulating tumor cells through NKG2D-mediated mechanosensing. APL Bioeng. 2023;7:036108.
pubmed: 37575881
pmcid: 10423075
doi: 10.1063/5.0156628
McGilvray RW, Eagle RA, Watson NFS, Al-Attar A, Ball G, Jafferji I, et al. NKG2D ligand expression in human colorectal cancer reveals associations with prognosis and evidence for immunoediting. Clin Cancer Res J Am Assoc Cancer Res. 2009;15:6993–7002.
doi: 10.1158/1078-0432.CCR-09-0991
Lerner EC, Woroniecka KI, D’Anniballe VM, Wilkinson DS, Mohan AA, Lorrey SJ, et al. CD8+ T cells maintain killing of MHC-I-negative tumor cells through the NKG2D–NKG2DL axis. Nat Cancer. 2023;4:1258–72.
pubmed: 37537301
pmcid: 10518253
doi: 10.1038/s43018-023-00600-4
Lanier LL, Corliss B, Wu J, Phillips JH. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity. 1998;8:693–701.
pubmed: 9655483
doi: 10.1016/S1074-7613(00)80574-9
Coupel S, Moreau A, Hamidou M, Horejsi V, Soulillou JP, Charreau B. Expression and release of soluble HLA-E is an immunoregulatory feature of endothelial cell activation. Blood. 2007;109:2806–14.
pubmed: 17179229
doi: 10.1182/blood-2006-06-030213
Cichocki F, Cooley S, Davis Z, DeFor TE, Schlums H, Zhang B, et al. CD56dimCD57+NKG2C+ NK cell expansion is associated with reduced leukemia relapse after reduced intensity HCT. Leukemia. 2016;30:456–63.
pubmed: 26416461
doi: 10.1038/leu.2015.260
Olson JA, Leveson-Gower DB, Gill S, Baker J, Beilhack A, Negrin RS. NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects. Blood. 2010;115:4293–301.
pubmed: 20233969
pmcid: 2879101
doi: 10.1182/blood-2009-05-222190
Kordelas L, Steckel NK, Horn P, Beelen D, Rebmann V. The activating NKG2C receptor is significantly reduced in NK cells after allogeneic stem cell transplantation in patients with severe graft-versus-host disease. Int J Mol Sci. 2016;17:1797.
pubmed: 27801784
pmcid: 5133798
doi: 10.3390/ijms17111797
Multhoff G, Botzler C, Wiesnet M, Müller E, Meier T, Wilmanns W, et al. A stress‐inducible 72‐kDa heat‐shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int J Cancer. 1995;61:272–9.
pubmed: 7705958
doi: 10.1002/ijc.2910610222
Botzler C, Issels R, Multhoff G. Heat-shock protein 72 cell-surface expression on human lung carcinoma cells is associated with an increased sensitivity to lysis mediated by adherent natural killer cells. Cancer Immunol Immunother. 1996;43:226–30.
pubmed: 9003468
doi: 10.1007/s002620050326
Gross C, Hansch D, Gastpar R, Multhoff G. Interaction of heat shock protein 70 peptide with NK cells involves the NK receptor CD94. Biol Chem. 2003;384:267–79.
pubmed: 12675520
doi: 10.1515/BC.2003.030
Paolini R, Molfetta R. Dysregulation of DNAM-1-mediated NK cell anti-cancer responses in the tumor microenvironment. Cancers. 2023;15:4616.
pubmed: 37760586
pmcid: 10527063
doi: 10.3390/cancers15184616
Tahara-Hanaoka S. Functional characterization of DNAM-1 (CD226) interaction with its ligands PVR (CD155) and nectin-2 (PRR-2/CD112). Int Immunol. 2004;16:533–8.
pubmed: 15039383
doi: 10.1093/intimm/dxh059
Bottino C, Castriconi R, Pende D, Rivera P, Nanni M, Carnemolla B, et al. Identification of PVR (CD155) and Nectin-2 (CD112) as Cell Surface Ligands for the Human DNAM-1 (CD226) Activating Molecule. J Exp Med. 2003;198:557–67.
pubmed: 12913096
pmcid: 2194180
doi: 10.1084/jem.20030788
Guillamón CF, Martínez-Sánchez MV, Gimeno L, Mrowiec A, Martínez-García J, Server-Pastor G, et al. NK cell education in tumor immune surveillance: DNAM-1/KIR receptor ratios as predictive biomarkers for solid tumor outcome. Cancer Immunol Res. 2018;6:1537–47.
pubmed: 30242020
doi: 10.1158/2326-6066.CIR-18-0022
Guillamón CF, Martínez-Sánchez MV, Gimeno L, Campillo JA, Server-Pastor G, Martínez-García J, et al. Activating KIRs on Educated NK Cells Support Downregulation of CD226 and Inefficient Tumor Immunosurveillance. Cancer Immunol Res. 2019;7:1307–17.
pubmed: 31239317
doi: 10.1158/2326-6066.CIR-18-0847
Iguchi-Manaka A, Kai H, Yamashita Y, Shibata K, Tahara-Hanaoka S, Honda Sichiro, et al. Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med. 2008;205:2959–64.
pubmed: 19029379
pmcid: 2605241
doi: 10.1084/jem.20081611
Gilfillan S, Chan CJ, Cella M, Haynes NM, Rapaport AS, Boles KS, et al. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J Exp Med. 2008;205:2965–73.
pubmed: 19029380
pmcid: 2605240
doi: 10.1084/jem.20081752
Nimmerjahn F, Ravetch JV. Fcgamma receptors as regulators of immune responses. Nat Rev Immunol. 2008;8:34–47.
pubmed: 18064051
doi: 10.1038/nri2206
Woof JM, Burton DR. Human antibody-Fc receptor interactions illuminated by crystal structures. Nat Rev Immunol. 2004;4:89–99.
pubmed: 15040582
doi: 10.1038/nri1266
Blázquez-Moreno A, Park S, Im W, Call MJ, Call ME, Reyburn HT. Transmembrane features governing Fc receptor CD16A assembly with CD16A signaling adaptor molecules. Proc Natl Acad Sci USA. 2017;114:E5645–54.
pubmed: 28652325
pmcid: 5514760
doi: 10.1073/pnas.1706483114
Wu J, Edberg JC, Redecha PB, Bansal V, Guyre PM, Coleman K, et al. A novel polymorphism of FcgammaRIIIa (CD16) alters receptor function and predisposes to autoimmune disease. J Clin Invest. 1997;100:1059–70.
pubmed: 9276722
pmcid: 508280
doi: 10.1172/JCI119616
Nowacki TM, Kuerten S, Zhang W, Shive CL, Kreher CR, Boehm BO, et al. Granzyme B production distinguishes recently activated CD8(+) memory cells from resting memory cells. Cell Immunol. 2007;247:36–48.
pubmed: 17825804
pmcid: 2134935
doi: 10.1016/j.cellimm.2007.07.004
Law RHP, Lukoyanova N, Voskoboinik I, Caradoc-Davies TT, Baran K, Dunstone MA, et al. The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature. 2010;468:447–51.
pubmed: 21037563
doi: 10.1038/nature09518
Lopez JA, Susanto O, Jenkins MR, Lukoyanova N, Sutton VR, Law RHP, et al. Perforin forms transient pores on the target cell plasma membrane to facilitate rapid access of granzymes during killer cell attack. Blood. 2013;121:2659–68.
pubmed: 23377437
doi: 10.1182/blood-2012-07-446146
Andrade F, Roy S, Nicholson D, Thornberry N, Rosen A, Casciola-Rosen L. Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis. Immunity. 1998;8:451–60.
pubmed: 9586635
doi: 10.1016/S1074-7613(00)80550-6
Sutton VR, Davis JE, Cancilla M, Johnstone RW, Ruefli AA, Sedelies K, et al. Initiation of apoptosis by granzyme B requires direct cleavage of bid, but not direct granzyme B-mediated caspase activation. J Exp Med. 2000;192:1403–14.
pubmed: 11085743
pmcid: 2193191
doi: 10.1084/jem.192.10.1403
Barry M, Heibein JA, Pinkoski MJ, Lee SF, Moyer RW, Green DR, et al. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol Cell Biol. 2000;20:3781–94.
pubmed: 10805722
pmcid: 85698
doi: 10.1128/MCB.20.11.3781-3794.2000
Zychlinsky A, Zheng LM, Liu CC, Young JD. Cytolytic lymphocytes induce both apoptosis and necrosis in target cells. J Immunol Balt Md 1950. 1991;146:393–400.
Anderson DH, Sawaya MR, Cascio D, Ernst W, Modlin R, Krensky A, et al. Granulysin crystal structure and a structure-derived lytic mechanism. J Mol Biol. 2003;325:355–65.
pubmed: 12488100
doi: 10.1016/S0022-2836(02)01234-2
Kaspar AA, Okada S, Kumar J, Poulain FR, Drouvalakis KA, Kelekar A, et al. A distinct pathway of cell-mediated apoptosis initiated by granulysin. J Immunol. 2001;167:350–6.
pubmed: 11418670
doi: 10.4049/jimmunol.167.1.350
Ambrose AR, Hazime KS, Worboys JD, Niembro-Vivanco O, Davis DM. Synaptic secretion from human natural killer cells is diverse and includes supramolecular attack particles. Proc Natl Acad Sci. 2020;117:23717–20.
pubmed: 32900953
pmcid: 7519227
doi: 10.1073/pnas.2010274117
Cohnen A, Chiang SC, Stojanovic A, Schmidt H, Claus M, Saftig P, et al. Surface CD107a/LAMP-1 protects natural killer cells from degranulation-associated damage. Blood. 2013;122:1411–8.
pubmed: 23847195
doi: 10.1182/blood-2012-07-441832
Thiery J, Keefe D, Boulant S, Boucrot E, Walch M, Martinvalet D, et al. Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol. 2011;12:770–7.
pubmed: 21685908
pmcid: 3140544
doi: 10.1038/ni.2050
Zamai L, Ahmad M, Bennett IM, Azzoni L, Alnemri ES, Perussia B. Natural killer (NK) cell-mediated cytotoxicity: differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J Exp Med. 1998;188:2375–80.
pubmed: 9858524
pmcid: 2212426
doi: 10.1084/jem.188.12.2375
Montel AH, Bochan MR, Hobbs JA, Lynch DH, Brahmi Z. Fas involvement in cytotoxicity mediated by human NK cells. Cell Immunol. 1995;166:236–46.
pubmed: 7497525
doi: 10.1006/cimm.1995.9974
Risso V, Lafont E, Le Gallo M. Therapeutic approaches targeting CD95L/CD95 signaling in cancer and autoimmune diseases. Cell Death Dis. 2022;13:1–32.
doi: 10.1038/s41419-022-04688-x
Lee J, Dieckmann NMG, Edgar JR, Griffiths GM, Siegel RM. Fas Ligand localizes to intraluminal vesicles within NK cell cytolytic granules and is enriched at the immune synapse. Immun Inflamm Dis. 2018;6:312–21.
pubmed: 29642281
pmcid: 5946154
doi: 10.1002/iid3.219
Bossi G, Griffiths GM. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat Med. 1999;5:90–6.
pubmed: 9883845
doi: 10.1038/4779
Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM, Kayagaki N, et al. Tumor necrosis factor–related apoptosis-inducing ligand (trail) contributes to interferon γ–dependent natural killer cell protection from tumor metastasis. J Exp Med. 2001;193:661–70.
pubmed: 11257133
pmcid: 2193421
doi: 10.1084/jem.193.6.661
Takeda K, Hayakawa Y, Smyth MJ, Kayagaki N, Yamaguchi N, Kakuta S, et al. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat Med. 2001;7:94–100.
pubmed: 11135622
doi: 10.1038/83416
Sheppard S, Schuster IS, Andoniou CE, Cocita C, Adejumo T, Kung SKP, et al. The murine natural cytotoxic receptor NKp46/NCR1 controls TRAIL protein expression in NK cells and ILC1s. Cell Rep. 2018;22:3385–92.
pubmed: 29590608
pmcid: 5896200
doi: 10.1016/j.celrep.2018.03.023
Prager I, Liesche C, van Ooijen H, Urlaub D, Verron Q, Sandström N, et al. NK cells switch from granzyme B to death receptor-mediated cytotoxicity during serial killing. J Exp Med. 2019;216:2113–27.
pubmed: 31270246
pmcid: 6719417
doi: 10.1084/jem.20181454
Monleón I, Martínez-Lorenzo MJ, Monteagudo L, Lasierra P, Taulés M, Iturralde M, et al. Differential secretion of fas ligand- or APO2 Ligand/TNF-related apoptosis-inducing ligand-carrying microvesicles during activation-induced death of human T cells. J Immunol. 2001;167:6736–44.
pubmed: 11739488
doi: 10.4049/jimmunol.167.12.6736
Reefman E, Kay JG, Wood SM, Offenhäuser C, Brown DL, Roy S, et al. Cytokine secretion is distinct from secretion of cytotoxic granules in NK cells. J Immunol Balt Md 1950. 2010;184:4852–62.
Sanderson NSR, Puntel M, Kroeger KM, Bondale NS, Swerdlow M, Iranmanesh N, et al. Cytotoxic immunological synapses do not restrict the action of interferon-γ to antigenic target cells. Proc Natl Acad Sci. 2012;109:7835–40.
pubmed: 22547816
pmcid: 3356634
doi: 10.1073/pnas.1116058109
Wang X, Lin Y. Tumor necrosis factor and cancer, buddies or foes? Acta Pharm Sin. 2008;29:1275–88.
doi: 10.1111/j.1745-7254.2008.00889.x
Castro F, Cardoso AP, Gonçalves RM, Serre K, Oliveira MJ. Interferon-gamma at the crossroads of tumor immune surveillance or evasion. Front Immunol. 2018;9:847.
pubmed: 29780381
pmcid: 5945880
doi: 10.3389/fimmu.2018.00847
Almishri W, Santodomingo-Garzon T, Le T, Stack D, Mody CH, Swain MG. TNFα Augments Cytokine-Induced NK Cell IFNγ Production through TNFR2. J Innate Immun. 2016;8:617–29.
pubmed: 27560480
pmcid: 6738838
doi: 10.1159/000448077
Bhat P, Leggatt G, Waterhouse N, Frazer IH. Interferon-γ derived from cytotoxic lymphocytes directly enhances their motility and cytotoxicity. Cell Death Dis. 2017;8:e2836.
pubmed: 28569770
pmcid: 5520949
doi: 10.1038/cddis.2017.67
Verron Q, Forslund E, Brandt L, Leino M, Frisk TW, Olofsson PE, et al. NK cells integrate signals over large areas when building immune synapses but require local stimuli for degranulation. Sci Signal. 2021;14:eabe2740.
pubmed: 34035142
doi: 10.1126/scisignal.abe2740
Tang JJJ, Sung AP, Guglielmo MJ, Navarrete-Galvan L, Redelman D, Smith-Gagen J, et al. Natural Killer (NK) Cell Expression of CD2 as a Predictor of Serial Antibody-Dependent. Cell-Mediated Cytotox (ADCC) Antibodies Basel Switz. 2020;9:54.
Deaglio S, Capobianco A, Calì A, Bellora F, Alberti F, Righi L, et al. Structural, functional, and tissue distribution analysis of human transferrin receptor-2 by murine monoclonal antibodies and a polyclonal antiserum. Blood. 2002;100:3782–9.
pubmed: 12393650
doi: 10.1182/blood-2002-01-0076
Cartron G, Dacheux L, Salles G, Solal-Celigny P, Bardos P, Colombat P, et al. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood. 2002;99:754–8.
pubmed: 11806974
doi: 10.1182/blood.V99.3.754
Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol J Am Soc Clin Oncol. 2008;26:1789–96.
doi: 10.1200/JCO.2007.14.8957
Fan X, Yuan Z, Zhao Y, Xiong W, Hsiao HC, Pare R, et al. Impairment of IgG Fc functions promotes tumor progression and suppresses NK cell antitumor actions. Commun Biol. 2022;5:1–14.
doi: 10.1038/s42003-022-03931-7
Muntasell A, Rojo F, Servitja S, Rubio-Perez C, Cabo M, Tamborero D, et al. NK cell infiltrates and HLA class I expression in primary HER2+ breast cancer predict and uncouple pathological response and disease-free survival. Clin Cancer Res. 2019;25:1535–45.
pubmed: 30523021
doi: 10.1158/1078-0432.CCR-18-2365
Klanova M, Oestergaard MZ, Trněný M, Hiddemann W, Marcus R, Sehn LH, et al. Prognostic impact of natural killer cell count in follicular lymphoma and diffuse large B-cell lymphoma patients treated with immunochemotherapy. Clin Cancer Res J Am Assoc Cancer Res. 2019;25:4634–43.
doi: 10.1158/1078-0432.CCR-18-3270
Choi PJ, Mitchison TJ. Imaging burst kinetics and spatial coordination during serial killing by single natural killer cells. Proc Natl Acad Sci. 2013;110:6488–93.
pubmed: 23576740
pmcid: 3631668
doi: 10.1073/pnas.1221312110
Gwalani LA, Orange JS. Single degranulations in NK cells can mediate target cell killing. J Immunol Balt Md 1950. 2018;200:3231–43.
Srpan K, Ambrose A, Karampatzakis A, Saeed M, Cartwright ANR, Guldevall K, et al. Shedding of CD16 disassembles the NK cell immune synapse and boosts serial engagement of target cells. J Cell Biol. 2018;217:3267–83.
pubmed: 29967280
pmcid: 6122987
doi: 10.1083/jcb.201712085
Zhu Y, Huang B, Shi J. Fas ligand and lytic granule differentially control cytotoxic dynamics of natural killer cell against cancer target. Oncotarget. 2016;7:47163–72.
pubmed: 27323411
pmcid: 5216932
doi: 10.18632/oncotarget.9980
Anft M, Netter P, Urlaub D, Prager I, Schaffner S, Watzl C. NK cell detachment from target cells is regulated by successful cytotoxicity and influences cytokine production. Cell Mol Immunol. 2020;17:347–55.
pubmed: 31471588
doi: 10.1038/s41423-019-0277-2
Lajoie L, Congy-Jolivet N, Bolzec A, Gouilleux-Gruart V, Sicard E, Sung HC, et al. ADAM17-mediated shedding of FcγRIIIA on human NK cells: identification of the cleavage site and relationship with activation. J Immunol Balt Md 1950. 2014;192:741–51.
Romee R, Foley B, Lenvik T, Wang Y, Zhang B, Ankarlo D, et al. NK cell CD16 surface expression and function is regulated by a disintegrin and metalloprotease-17 (ADAM17). Blood. 2013;121:3599–608.
pubmed: 23487023
pmcid: 3643761
doi: 10.1182/blood-2012-04-425397
Mishra HK, Pore N, Michelotti EF, Walcheck B. Anti-ADAM17 monoclonal antibody MEDI3622 increases IFNγ production by human NK cells in the presence of antibody-bound tumor cells. Cancer Immunol Immunother CII. 2018;67:1407–16.
pubmed: 29978334
doi: 10.1007/s00262-018-2193-1
Krzywinska E, Allende-Vega N, Cornillon A, Vo DN, Cayrefourcq L, Panabieres C, et al. Identification of Anti-tumor Cells Carrying Natural Killer (NK) Cell Antigens in Patients With Hematological Cancers. EBioMedicine. 2015;2:1364–76.
pubmed: 26629531
pmcid: 4634619
doi: 10.1016/j.ebiom.2015.08.021
Krzywinska E, Cornillon A, Allende-Vega N, Vo DN, Rene C, Lu ZY, et al. CD45 Isoform Profile Identifies Natural Killer (NK) Subsets with Differential Activity. PloS One. 2016;11:e0150434.
pubmed: 27100180
pmcid: 4839597
doi: 10.1371/journal.pone.0150434
Vo DN, Alexia C, Allende-Vega N, Morschhauser F, Houot R, Menard C, et al. NK cell activation and recovery of NK cell subsets in lymphoma patients after obinutuzumab and lenalidomide treatment. Oncoimmunology. 2018;7:e1409322.
pubmed: 29632722
doi: 10.1080/2162402X.2017.1409322
Vo DN, Constantinides M, Allende-Vega N, Alexia C, Cartron G, Villalba M. Dissecting the NK cell population in hematological cancers confirms the presence of tumor cells and their impact on NK population function. Vaccines. 2020;8:727.
pubmed: 33276644
pmcid: 7761578
doi: 10.3390/vaccines8040727
Soma L, Wu D, Chen X, Edlefsen K, Fromm JR, Wood B. Apparent CD19 expression by natural killer cells: a potential confounder for minimal residual disease detection by flow cytometry in B lymphoblastic leukemia. Cytom B Clin Cytom. 2015;88:145–7.
doi: 10.1002/cytob.21179
Hasim MS, Marotel M, Hodgins JJ, Vulpis E, Makinson OJ, Asif S, et al. When killers become thieves: Trogocytosed PD-1 inhibits NK cells in cancer. Sci Adv. 2022;8:eabj3286.
pubmed: 35417234
pmcid: 9007500
doi: 10.1126/sciadv.abj3286
Caumartin J, Favier B, Daouya M, Guillard C, Moreau P, Carosella ED, et al. Trogocytosis-based generation of suppressive NK cells. EMBO J. 2007;26:1423–33.
pubmed: 17318190
pmcid: 1817622
doi: 10.1038/sj.emboj.7601570
Vo DN, Leventoux N, Campos-Mora M, Gimenez S, Corbeau P, Villalba M. NK cells acquire CCR5 and CXCR4 by trogocytosis in people living with HIV-1. Vaccines. 2022;10:688.
pubmed: 35632444
pmcid: 9145773
doi: 10.3390/vaccines10050688
Nakayama M, Takeda K, Kawano M, Takai T, Ishii N, Ogasawara K. Natural killer (NK)-dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4+ T cells. Proc Natl Acad Sci USA. 2011;108:18360–5.
pubmed: 22042851
pmcid: 3215013
doi: 10.1073/pnas.1110584108
Suzuki E, Kataoka TR, Hirata M, Kawaguchi K, Nishie M, Haga H, et al. Trogocytosis-mediated expression of HER2 on immune cells may be associated with a pathological complete response to trastuzumab-based primary systemic therapy in HER2-overexpressing breast cancer patients. BMC Cancer. 2015;15:39.
pubmed: 25655677
pmcid: 4329225
doi: 10.1186/s12885-015-1041-3
Pan Y, Yu Y, Wang X, Zhang T. Tumor-associated macrophages in tumor immunity. Front Immunol. 2020;11:583084.
pubmed: 33365025
pmcid: 7751482
doi: 10.3389/fimmu.2020.583084
Gao J, Liang Y, Wang L. Shaping polarization of tumor-associated macrophages in cancer immunotherapy. Front Immunol. 2022;13:888713.
pubmed: 35844605
pmcid: 9280632
doi: 10.3389/fimmu.2022.888713
Mattiola I, Pesant M, Tentorio PF, Molgora M, Marcenaro E, Lugli E, et al. Priming of human resting NK cells by autologous M1 macrophages via the engagement of IL-1β, IFN-β, and IL-15 pathways. J Immunol. 2015;195:2818–28.
pubmed: 26276870
doi: 10.4049/jimmunol.1500325
Zhou Z, Zhang C, Zhang J, Tian Z. Macrophages help NK cells to attack tumor cells by stimulatory NKG2D ligand but protect themselves from NK killing by inhibitory ligand Qa-1. Zimmer J, editor. PLoS ONE. 2012 May 18;7:e36928.
De Groen RA, Boltjes A, Hou J, Liu B, McPhee F, Friborg J, et al. IFN‐λ‐mediated IL‐12 production in macrophages induces IFN‐γ production in human NK cells. Eur J Immunol. 2015;45:250–9.
pubmed: 25316442
doi: 10.1002/eji.201444903
Chiba S, Ikushima H, Ueki H, Yanai H, Kimura Y, Hangai S, et al. Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses. eLife. 2014;3:e04177.
pubmed: 25149452
pmcid: 4161974
doi: 10.7554/eLife.04177
Nuñez SY, Ziblat A, Secchiari F, Torres NI, Sierra JM, Raffo Iraolagoitia XL, et al. Human M2 macrophages limit NK cell effector functions through secretion of TGF-β and engagement of CD85j. J Immunol. 2018;200:1008–15.
pubmed: 29282306
doi: 10.4049/jimmunol.1700737
Peng LS, Zhang JY, Teng YS, Zhao YL, Wang TT, Mao FY, et al. Tumor-associated monocytes/macrophages impair NK-cell function via TGFβ1 in human gastric cancer. Cancer Immunol Res. 2017;5:248–56.
pubmed: 28148545
doi: 10.1158/2326-6066.CIR-16-0152
Krneta T, Gillgrass A, Poznanski S, Chew M, Lee AJ, Kolb M, et al. M2-polarized and tumor-associated macrophages alter NK cell phenotype and function in a contact-dependent manner. J Leukoc Biol. 2017;101:285–95.
pubmed: 27493241
doi: 10.1189/jlb.3A1215-552R
Klose R, Krzywinska E, Castells M, Gotthardt D, Putz EM, Kantari-Mimoun C, et al. Targeting VEGF-A in myeloid cells enhances natural killer cell responses to chemotherapy and ameliorates cachexia. Nat Commun. 2016;7:12528.
pubmed: 27538380
pmcid: 4992172
doi: 10.1038/ncomms12528
Gallazzi M, Baci D, Mortara L, Bosi A, Buono G, Naselli A, et al. Prostate cancer peripheral blood nk cells show enhanced CD9, CD49a, CXCR4, CXCL8, MMP-9 production and secrete monocyte-recruiting and polarizing factors. Front Immunol. 2021;11:586126.
pubmed: 33569050
pmcid: 7868409
doi: 10.3389/fimmu.2020.586126
Sun C, Mezzadra R, Schumacher TN. Regulation and function of the PD-L1 checkpoint. Immunity. 2018;48:434–52.
pubmed: 29562194
pmcid: 7116507
doi: 10.1016/j.immuni.2018.03.014
Hsu J, Hodgins JJ, Marathe M, Nicolai CJ, Bourgeois-Daigneault MC, Trevino TN, et al. Contribution of NK cells to immunotherapy mediated by PD-1/PD-L1 blockade. J Clin Invest. 2018;128:4654–68.
pubmed: 30198904
pmcid: 6159991
doi: 10.1172/JCI99317
Li K, Shi H, Zhang B, Ou X, Ma Q, Chen Y, et al. Myeloid-derived suppressor cells as immunosuppressive regulators and therapeutic targets in cancer. Signal Transduct Target Ther. 2021;6:1–25.
Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 2009;50:799–807.
pubmed: 19551844
doi: 10.1002/hep.23054
Li H, Han Y, Guo Q, Zhang M, Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-β1. J Immunol. 2009;182:240–9.
pubmed: 19109155
doi: 10.4049/jimmunol.182.1.240
Stiff A, Trikha P, Mundy-Bosse B, McMichael E, Mace TA, Benner B, et al. Nitric oxide production by myeloid-derived suppressor cells plays a role in impairing Fc receptor-mediated natural killer cell function. Clin Cancer Res J Am Assoc Cancer Res. 2018;24:1891–904.
doi: 10.1158/1078-0432.CCR-17-0691
Nausch N, Galani IE, Schlecker E, Cerwenka A. Mononuclear myeloid-derived “suppressor” cells express RAE-1 and activate natural killer cells. Blood. 2008;112:4080–9.
pubmed: 18753637
pmcid: 2582006
doi: 10.1182/blood-2008-03-143776
Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, et al. Dendritic cells directly trigger NK cell functions: Cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med. 1999;5:405–11.
pubmed: 10202929
doi: 10.1038/7403
Böttcher JP, Bonavita E, Chakravarty P, Blees H, Cabeza-Cabrerizo M, Sammicheli S, et al. NK cells stimulate recruitment of cDC1 into the tumor microenvironment promoting cancer immune control. Cell. 2018;172:1022–1037.e14.
pubmed: 29429633
pmcid: 5847168
doi: 10.1016/j.cell.2018.01.004
Allen F, Bobanga ID, Rauhe P, Barkauskas D, Teich N, Tong C, et al. CCL3 augments tumor rejection and enhances CD8+ T cell infiltration through NK and CD103+ dendritic cell recruitment via IFNγ. Oncoimmunology. 2018;7:e1393598.
pubmed: 29399390
doi: 10.1080/2162402X.2017.1393598
Barry KC, Hsu J, Broz ML, Cueto FJ, Binnewies M, Combes AJ, et al. A natural killer–dendritic cell axis defines checkpoint therapy–responsive tumor microenvironments. Nat Med. 2018;24:1178–91.
pubmed: 29942093
pmcid: 6475503
doi: 10.1038/s41591-018-0085-8
Holmes TD, Wilson EB, Black EVI, Benest AV, Vaz C, Tan B, et al. Licensed human natural killer cells aid dendritic cell maturation via TNFSF14/LIGHT. Proc Natl Acad Sci USA. 2014;111:E5688–5696.
pubmed: 25512551
pmcid: 4284554
doi: 10.1073/pnas.1411072112
Vitale M, Chiesa MD, Carlomagno S, Pende D, Aricò M, Moretta L, et al. NK-dependent DC maturation is mediated by TNFα and IFNγ released upon engagement of the NKp30 triggering receptor. Blood. 2005;106:566–71.
pubmed: 15784725
doi: 10.1182/blood-2004-10-4035
Russick J, Joubert PE, Gillard-Bocquet M, Torset C, Meylan M, Petitprez F, et al. Natural killer cells in the human lung tumor microenvironment display immune inhibitory functions. J Immunother Cancer. 2020;8:e001054.
pubmed: 33067317
pmcid: 7570244
doi: 10.1136/jitc-2020-001054
Lee SC, Srivastava RM, López-Albaitero A, Ferrone S, Ferris RL. Natural killer (NK):dendritic cell (DC) cross talk induced by therapeutic monoclonal antibody triggers tumor antigen-specific T cell immunity. Immunol Res. 2011;50:248–54.
pubmed: 21717064
pmcid: 3415245
doi: 10.1007/s12026-011-8231-0
Kijima M, Yamaguchi T, Ishifune C, Maekawa Y, Koyanagi A, Yagita H, et al. Dendritic cell-mediated NK cell activation is controlled by Jagged2–Notch interaction. Proc Natl Acad Sci. 2008;105:7010–5.
pubmed: 18458347
pmcid: 2383942
doi: 10.1073/pnas.0709919105
Perez-Martinez A, Iyengar R, Gan K, Chotsampancharoen T, Rooney B, Holladay M, et al. Blood dendritic cells suppress NK cell function and increase the risk of leukemia relapse after hematopoietic cell transplantation. Biol Blood Marrow Transpl J Am Soc Blood Marrow Transpl. 2011;17:598–607.
doi: 10.1016/j.bbmt.2010.10.019
Masucci MT, Minopoli M, Carriero MV. Tumor associated neutrophils. their role in tumorigenesis, metastasis, prognosis and therapy. Front Oncol. 2019;9:1146.
pubmed: 31799175
pmcid: 6874146
doi: 10.3389/fonc.2019.01146
Ogura K, Sato-Matsushita M, Yamamoto S, Hori T, Sasahara M, Iwakura Y, et al. NK cells control tumor-promoting function of neutrophils in mice. Cancer Immunol Res. 2018;6:348–57.
pubmed: 29362222
doi: 10.1158/2326-6066.CIR-17-0204
Schäkel K, Von Kietzell M, Hänsel A, Ebling A, Schulze L, Haase M, et al. Human 6-Sulfo LacNAc-expressing dendritic cells are principal producers of early interleukin-12 and are controlled by erythrocytes. Immunity. 2006;24:767–77.
pubmed: 16782032
doi: 10.1016/j.immuni.2006.03.020
Costantini C, Calzetti F, Perbellini O, Micheletti A, Scarponi C, Lonardi S, et al. Human neutrophils interact with both 6-sulfo LacNAc+ DC and NK cells to amplify NK-derived IFN{gamma}: role of CD18, ICAM-1, and ICAM-3. Blood. 2011;117:1677–86.
pubmed: 21098395
doi: 10.1182/blood-2010-06-287243
Sun R, Xiong Y, Liu H, Gao C, Su L, Weng J, et al. Tumor-associated neutrophils suppress antitumor immunity of NK cells through the PD-L1/PD-1 axis. Transl Oncol. 2020;13:100825.
pubmed: 32698059
pmcid: 7372151
doi: 10.1016/j.tranon.2020.100825
Valayer A, Brea D, Lajoie L, Avezard L, Combes-Soia L, Labas V, et al. Neutrophils can disarm NK cell response through cleavage of NKp46. J Leukoc Biol. 2017;101:253–9.
pubmed: 27587403
doi: 10.1189/jlb.3AB0316-140RR
Godfrey DI, Koay HF, McCluskey J, Gherardin NA. The biology and functional importance of MAIT cells. Nat Immunol. 2019;20:1110–28.
pubmed: 31406380
doi: 10.1038/s41590-019-0444-8
Petley EV, Koay HF, Henderson MA, Sek K, Todd KL, Keam SP, et al. MAIT cells regulate NK cell-mediated tumor immunity. Nat Commun. 2021;12:4746.
pubmed: 34362900
pmcid: 8346465
doi: 10.1038/s41467-021-25009-4
Speiser DE, Chijioke O, Schaeuble K, Münz C. CD4+ T cells in cancer. Nat Cancer. 2023;4:317–29.
pubmed: 36894637
doi: 10.1038/s43018-023-00521-2
Nakayama M, Takeda K, Kawano M, Takai T, Ishii N, Ogasawara K. Natural killer (NK)–dendritic cell interactions generate MHC class II-dressed NK cells that regulate CD4
pubmed: 22042851
pmcid: 3215013
doi: 10.1073/pnas.1110584108
Adam C, King S, Allgeier T, Braumüller H, Lüking C, Mysliwietz J, et al. DC-NK cell cross talk as a novel CD4+ T-cell–independent pathway for antitumor CTL induction. Blood. 2005;106:338–44.
pubmed: 15769894
doi: 10.1182/blood-2004-09-3775
Brillard E, Pallandre JR, Chalmers D, Ryffel B, Radlovic A, Seilles E, et al. Natural killer cells prevent CD28-mediated Foxp3 transcription in CD4+CD25– T lymphocytes. Exp Hematol. 2007;35:416–25.
pubmed: 17309822
doi: 10.1016/j.exphem.2006.12.004
Martín-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-γ for TH1 priming. Nat Immunol. 2004;5:1260–5.
pubmed: 15531883
doi: 10.1038/ni1138
Prins RM, Vo DD, Khan-Farooqi H, Yang MY, Soto H, Economou JS, et al. NK and CD4 cells collaborate to protect against melanoma tumor formation in the brain. J Immunol Balt Md 1950. 2006;177:8448–55.
Wang Z, Chimenti MS, Strouse C, Weiner GJ. T cells, particularly activated CD4+ cells, maintain anti-CD20-mediated NK cell viability and antibody dependent cellular cytotoxicity. Cancer Immunol Immunother. 2022;71:237–49.
pubmed: 34110453
doi: 10.1007/s00262-021-02976-7
Shimizu J, Yamazaki S, Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity1. J Immunol. 1999;163:5211–8.
pubmed: 10553041
doi: 10.4049/jimmunol.163.10.5211
Wolf AM, Wolf D, Steurer M, Gastl G, Gunsilius E, Grubeck-Loebenstein B. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res J Am Assoc Cancer Res. 2003;9:606–12.
Trzonkowski P, Szmit E, Myśliwska J, Myśliwski A. CD4+CD25+ T regulatory cells inhibit cytotoxic activity of CTL and NK cells in humans—impact of immunosenescence. Clin Immunol. 2006;119:307–16.
pubmed: 16545982
doi: 10.1016/j.clim.2006.02.002
Ghiringhelli F, Ménard C, Terme M, Flament C, Taieb J, Chaput N, et al. CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor–β–dependent manner. J Exp Med. 2005;202:1075–85.
pubmed: 16230475
pmcid: 2213209
doi: 10.1084/jem.20051511
Wong JL, Berk E, Edwards RP, Kalinski P. IL-18–primed helper NK cells collaborate with dendritic cells to promote recruitment of effector CD8+ T cells to the tumor microenvironment. Cancer Res. 2013;73:4653–62.
pubmed: 23761327
pmcid: 3780558
doi: 10.1158/0008-5472.CAN-12-4366
Iraolagoitia XLR, Spallanzani RG, Torres NI, Araya RE, Ziblat A, Domaica CI, et al. NK cells restrain spontaneous antitumor CD8+ T cell priming through PD-1/PD-L1 interactions with dendritic cells. J Immunol. 2016;197:953–61.
pubmed: 27342842
doi: 10.4049/jimmunol.1502291
Bai L, Peng H, Hao X, Tang L, Sun C, Zheng M, et al. CD8+ T cells promote maturation of liver‐resident NK cells through the CD70‐CD27 axis. Hepatology. 2019;70:1804–15.
pubmed: 31077406
doi: 10.1002/hep.30757
Somersalo K, Carpén O, Saksela E. Stimulated natural killer cells secrete factors with chemotactic activity, including NAP‐1/IL‐8, which supports VLA‐4‐ and VLA‐5‐mediated migration of T lymphocytes. Eur J Immunol. 1994;24:2957–65.
pubmed: 7805722
doi: 10.1002/eji.1830241206
Roda JM, Parihar R, Magro C, Nuovo GJ, Tridandapani S, Carson WE. Natural killer cells produce T cell-recruiting chemokines in response to antibody-coated tumor cells. Cancer Res. 2006;66:517–26.
pubmed: 16397268
doi: 10.1158/0008-5472.CAN-05-2429
Shanker A, Verdeil G, Buferne M, Inderberg-Suso EM, Puthier D, Joly F, et al. CD8 T cell help for innate antitumor immunity. J Immunol Balt Md 1950. 2007;179:6651–62.
Villalba M, Alexia C, Bellin-Robert A, Fayd’herbe de Maudave A, Gitenay D. Non-genetically improving the natural cytotoxicity of natural killer (NK) cells. Front Immunol. 2019;10:3026.
pubmed: 31998309
doi: 10.3389/fimmu.2019.03026