Maintaining the Balance: Regulation of NK Cell Activity
Abstract
:1. Introduction
2. NK Cell Receptors and Activation
2.1. Activating Receptors
2.2. Inhibitory Receptors
3. Regulation of NK Cell Activity
3.1. Regulation of NK Cell Responsiveness during Development
3.1.1. Education through Inhibitory Receptors
3.1.2. Education through Activating Receptors
3.2. Regulation of NK Cell Responsiveness in the Periphery
3.3. Tipping the Balance
4. Memory NK Cells
5. Therapeutic Implications of NK Cells
6. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Seillet, C.; Brossay, L.; Vivier, E. Natural killers or ILC1s? That is the question. Curr. Opin. Immunol. 2021, 68, 48–53. [Google Scholar] [CrossRef]
- Ebbo, M.; Crinier, A.; Vely, F.; Vivier, E. Innate lymphoid cells: Major players in inflammatory diseases. Nat. Rev. Immunol. 2017, 17, 665–678. [Google Scholar] [CrossRef]
- Mattiola, I.; Diefenbach, A. Innate lymphoid cells and cancer at border surfaces with the environment. Semin. Immunol. 2019, 41, 101278. [Google Scholar] [CrossRef] [PubMed]
- Klose, C.S.N.; Flach, M.; Mohle, L.; Rogell, L.; Hoyler, T.; Ebert, K.; Fabiunke, C.; Pfeifer, D.; Sexl, V.; Fonseca-Pereira, D.; et al. Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell 2014, 157, 340–356. [Google Scholar] [CrossRef] [PubMed]
- Vivier, E.; Artis, D.; Colonna, M.; Diefenbach, A.; Di Santo, J.P.; Eberl, G.; Koyasu, S.; Locksley, R.M.; McKenzie, A.N.J.; Mebius, R.E.; et al. Innate Lymphoid Cells: 10 Years On. Cell 2018, 174, 1054–1066. [Google Scholar] [CrossRef]
- Poli, A.; Michel, T.; Theresine, M.; Andres, E.; Hentges, F.; Zimmer, J. CD56bright natural killer (NK) cells: An important NK cell subset. Immunology 2009, 126, 458–465. [Google Scholar] [CrossRef]
- Abel, A.M.; Yang, C.; Thakar, M.S.; Malarkannan, S. Natural Killer Cells: Development, Maturation, and Clinical Utilization. Front. Immunol. 2018, 9, 1869. [Google Scholar] [CrossRef]
- Prager, I.; Watzl, C. Mechanisms of natural killer cell-mediated cellular cytotoxicity. J. Leukoc. Biol. 2019, 105, 1319–1329. [Google Scholar] [CrossRef] [PubMed]
- Prager, I.; Liesche, C.; van Ooijen, H.; Urlaub, D.; Verron, Q.; Sandstrom, N.; Fasbender, F.; Claus, M.; Eils, R.; Beaudouin, J.; et al. NK cells switch from granzyme B to death receptor-mediated cytotoxicity during serial killing. J. Exp. Med. 2019, 216, 2113–2127. [Google Scholar] [CrossRef]
- Piersma, S.J.; Brizic, I. Natural killer cell effector functions in antiviral defense. FEBS J. 2022, 289, 3982–3999. [Google Scholar] [CrossRef]
- Coenon, L.; Villalba, M. From CD16a Biology to Antibody-Dependent Cell-Mediated Cytotoxicity Improvement. Front. Immunol. 2022, 13, 913215. [Google Scholar] [CrossRef]
- Paul, S.; Lal, G. The Molecular Mechanism of Natural Killer Cells Function and Its Importance in Cancer Immunotherapy. Front. Immunol. 2017, 8, 1124. [Google Scholar] [CrossRef] [PubMed]
- Bajénoff, M.; Breart, B.; Huang, A.Y.C.; Qi, H.; Cazareth, J.; Braud, V.M.; Germain, R.N.; Glaichenhaus, N. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J. Exp. Med. 2006, 203, 619–631. [Google Scholar] [CrossRef] [PubMed]
- He, Y.K.; Tian, Z.G. NK cell education via nonclassical MHC and non-MHC ligands. Cell Mol. Immunol. 2017, 14, 321–330. [Google Scholar] [CrossRef]
- Vivier, E.; Tomasello, E.; Baratin, M.; Walzer, T.; Ugolini, S. Functions of natural killer cells. Nat. Immunol. 2008, 9, 503–510. [Google Scholar] [CrossRef]
- Chan, C.J.; Smyth, M.J.; Martinet, L. Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ. 2014, 21, 5–14. [Google Scholar] [CrossRef] [PubMed]
- Gabor, F.; Jahn, G.; Sedmak, D.D.; Sinzger, C. In vivo Downregulation of MHC Class I Molecules by HCMV Occurs During All Phases of Viral Replication but Is Not Always Complete. Front. Cell Infect. Microbiol. 2020, 10, 283. [Google Scholar] [CrossRef] [PubMed]
- Campbell, A.E.; Slater, J.S. Down-regulation of major histocompatibility complex class I synthesis by murine cytomegalovirus early gene expression. J. Virol. 1994, 68, 1805–1811. [Google Scholar] [CrossRef]
- Goepel, J.R.; Rees, R.C.; Rogers, K.; Stoddard, C.J.; Thomas, W.E.; Shepherd, L. Loss of monomorphic and polymorphic HLA antigens in metastatic breast and colon carcinoma. Br. J. Cancer 1991, 64, 880–883. [Google Scholar] [CrossRef]
- McDougall, C.J.; Ngoi, S.S.; Goldman, I.S.; Godwin, T.; Felix, J.; DeCosse, J.J.; Rigas, B. Reduced expression of HLA class I and II antigens in colon cancer. Cancer Res. 1990, 50, 8023–8027. [Google Scholar]
- Vitale, M.; Rezzani, R.; Rodella, L.; Zauli, G.; Grigolato, P.; Cadei, M.; Hicklin, D.J.; Ferrone, S. HLA class I antigen and transporter associated with antigen processing (TAP1 and TAP2) down-regulation in high-grade primary breast carcinoma lesions. Cancer Res. 1998, 58, 737–742. [Google Scholar] [PubMed]
- Cathro, H.P.; Smolkin, M.E.; Theodorescu, D.; Jo, V.Y.; Ferrone, S.; Frierson, H.F., Jr. Relationship between HLA class I antigen processing machinery component expression and the clinicopathologic characteristics of bladder carcinomas. Cancer Immunol. Immunother. 2010, 59, 465–472. [Google Scholar] [CrossRef]
- Cristiani, C.M.; Garofalo, C.; Passacatini, L.C.; Carbone, E. New avenues for melanoma immunotherapy: Natural Killer cells? Scand. J. Immunol. 2020, 91, e12861. [Google Scholar] [CrossRef] [PubMed]
- Yokoyama, W.M.; Kim, S. How do natural killer cells find self to achieve tolerance? Immunity 2006, 24, 249–257. [Google Scholar] [CrossRef] [PubMed]
- Karre, K.; Ljunggren, H.G.; Piontek, G.; Kiessling, R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986, 319, 675–678. [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]
- Arase, H.; Mocarski, E.S.; Campbell, A.E.; Hill, A.B.; Lanier, L.L. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002, 296, 1323–1326. [Google Scholar] [CrossRef]
- Smith, H.R.; Heusel, J.W.; Mehta, I.K.; Kim, S.; Dorner, B.G.; Naidenko, O.V.; Iizuka, K.; Furukawa, H.; Beckman, D.L.; Pingel, J.T.; et al. Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA 2002, 99, 8826–8831. [Google Scholar] [CrossRef]
- Lanier, L.L. Up on the tightrope: Natural killer cell activation and inhibition. Nat. Immunol. 2008, 9, 495–502. [Google Scholar] [CrossRef]
- Huntington, N.D.; Vosshenrich, C.A.; Di Santo, J.P. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nature reviews. Immunology 2007, 7, 703–714. [Google Scholar]
- Hasan, M.; Krmpotic, A.; Ruzsics, Z.; Bubic, I.; Lenac, T.; Halenius, A.; Loewendorf, A.; Messerle, M.; Hengel, H.; Jonjic, S.; et al. Selective down-regulation of the NKG2D ligand H60 by mouse cytomegalovirus m155 glycoprotein. J. Virol. 2005, 79, 2920–2930. [Google Scholar] [CrossRef]
- Krmpotic, A.; Busch, D.H.; Bubic, I.; Gebhardt, F.; Hengel, H.; Hasan, M.; Scalzo, A.A.; Koszinowski, U.H.; Jonjic, S. MCMV glycoprotein gp40 confers virus resistance to CD8+ T cells and NK cells in vivo. Nat. Immunol. 2002, 3, 529–535. [Google Scholar] [CrossRef] [PubMed]
- Krmpotic, A.; Hasan, M.; Loewendorf, A.; Saulig, T.; Halenius, A.; Lenac, T.; Polic, B.; Bubic, I.; Kriegeskorte, A.; Pernjak-Pugel, E.; et al. NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J. Exp. Med. 2005, 201, 211–220. [Google Scholar] [CrossRef]
- Diefenbach, A.; Jensen, E.R.; Jamieson, A.M.; Raulet, D.H. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001, 413, 165–171. [Google Scholar] [CrossRef] [PubMed]
- Cerwenka, A.; Baron, J.L.; Lanier, L.L. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc. Natl. Acad. Sci. USA 2001, 98, 11521–11526. [Google Scholar] [CrossRef] [PubMed]
- Guerra, N.; Tan, Y.X.; Joncker, N.T.; Choy, A.; Gallardo, F.; Xiong, N.; Knoblaugh, S.; Cado, D.; Greenberg, N.M.; Raulet, D.H. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008, 28, 571–580. [Google Scholar] [CrossRef] [PubMed]
- Zafirova, B.; Mandaric, S.; Antulov, R.; Krmpotic, A.; Jonsson, H.; Yokoyama, W.M.; Jonjic, S.; Polic, B. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity 2009, 31, 270–282. [Google Scholar] [CrossRef]
- Rehermann, B. Natural Killer Cells in Viral Hepatitis. Cell Mol. Gastroenterol. Hepatol. 2015, 1, 578–588. [Google Scholar] [CrossRef]
- Glasner, A.; Ghadially, H.; Gur, C.; Stanietsky, N.; Tsukerman, P.; Enk, J.; Mandelboim, O. Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1. J. Immunol. 2012, 188, 2509–2515. [Google Scholar] [CrossRef]
- Elhaik-Goldman, S.; Kafka, D.; Yossef, R.; Hadad, U.; Elkabets, M.; Vallon-Eberhard, A.; Hulihel, L.; Jung, S.; Ghadially, H.; Braiman, A.; et al. The natural cytotoxicity receptor 1 contribution to early clearance of Streptococcus pneumoniae and to natural killer-macrophage cross talk. PLoS ONE 2011, 6, e23472. [Google Scholar] [CrossRef]
- Halfteck, G.G.; Elboim, M.; Gur, C.; Achdout, H.; Ghadially, H.; Mandelboim, O. Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1. J. Immunol. 2009, 182, 2221–2230. [Google Scholar] [CrossRef]
- Iguchi-Manaka, A.; Kai, H.; Yamashita, Y.; Shibata, K.; Tahara-Hanaoka, S.; Honda, S.; Yasui, T.; Kikutani, H.; Shibuya, K.; Shibuya, A. Accelerated tumor growth in mice deficient in DNAM-1 receptor. J. Exp. Med. 2008, 205, 2959–2964. [Google Scholar] [CrossRef]
- Deng, W.; Gowen, B.G.; Zhang, L.; Wang, L.; Lau, S.; Iannello, A.; Xu, J.; Rovis, T.L.; Xiong, N.; Raulet, D.H. Antitumor immunity. A shed NKG2D ligand that promotes natural killer cell activation and tumor rejection. Science 2015, 348, 136–139. [Google Scholar] [CrossRef]
- Barrow, A.D.; Edeling, M.A.; Trifonov, V.; Luo, J.; Goyal, P.; Bohl, B.; Bando, J.K.; Kim, A.H.; Walker, J.; Andahazy, M.; et al. Natural Killer Cells Control Tumor Growth by Sensing a Growth Factor. Cell 2018, 172, 534–548 e519. [Google Scholar] [CrossRef] [PubMed]
- Rahim, M.M.; Tu, M.M.; Mahmoud, A.B.; Wight, A.; Abou-Samra, E.; Lima, P.D.; Makrigiannis, A.P. Ly49 receptors: Innate and adaptive immune paradigms. Front. Immunol. 2014, 5, 145. [Google Scholar] [CrossRef] [PubMed]
- Raulet, D.H.; Vance, R.E.; McMahon, C.W. Regulation of the natural killer cell receptor repertoire. Annu. Rev. Immunol. 2001, 19, 291–330. [Google Scholar] [CrossRef] [PubMed]
- Jelencic, V.; Sestan, M.; Kavazovic, I.; Lenartic, M.; Marinovic, S.; Holmes, T.D.; Prchal-Murphy, M.; Lisnic, B.; Sexl, V.; Bryceson, Y.T.; et al. NK cell receptor NKG2D sets activation threshold for the NCR1 receptor early in NK cell development. Nat. Immunol. 2018, 19, 1083–1092. [Google Scholar] [CrossRef] [PubMed]
- Long, E.O.; Kim, H.S.; Liu, D.; Peterson, M.E.; Rajagopalan, S. Controlling natural killer cell responses: Integration of signals for activation and inhibition. Annu. Rev. Immunol. 2013, 31, 227–258. [Google Scholar] [CrossRef]
- Elliott, J.M.; Yokoyama, W.M. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol. 2011, 32, 364–372. [Google Scholar] [CrossRef]
- Liao, N.S.; Bix, M.; Zijlstra, M.; Jaenisch, R.; Raulet, D. MHC class I deficiency: Susceptibility to natural killer (NK) cells and impaired NK activity. Science 1991, 253, 199–202. [Google Scholar] [CrossRef]
- Bix, M.; Liao, N.S.; Zijlstra, M.; Loring, J.; Jaenisch, R.; Raulet, D. Rejection of class I MHC-deficient haemopoietic cells by irradiated MHC-matched mice. Nature 1991, 349, 329–331. [Google Scholar] [CrossRef] [PubMed]
- Belanger, S.; Tu, M.M.; Rahim, M.M.; Mahmoud, A.B.; Patel, R.; Tai, L.H.; Troke, A.D.; Wilhelm, B.T.; Landry, J.R.; Zhu, Q.; et al. Impaired natural killer cell self-education and “missing-self” responses in Ly49-deficient mice. Blood 2012, 120, 592–602. [Google Scholar] [CrossRef]
- Zhang, X.; Feng, J.; Chen, S.; Yang, H.; Dong, Z. Synergized regulation of NK cell education by NKG2A and specific Ly49 family members. Nat. Commun. 2019, 10, 5010. [Google Scholar] [CrossRef] [PubMed]
- Elliott, J.M.; Wahle, J.A.; Yokoyama, W.M. MHC class I-deficient natural killer cells acquire a licensed phenotype after transfer into an MHC class I-sufficient environment. J. Exp. Med. 2010, 207, 2073–2079. [Google Scholar] [CrossRef] [PubMed]
- Anfossi, N.; Andre, P.; Guia, S.; Falk, C.S.; Roetynck, S.; Stewart, C.A.; Breso, V.; Frassati, C.; Reviron, D.; Middleton, D.; et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity 2006, 25, 331–342. [Google Scholar] [CrossRef]
- Cooley, S.; Xiao, F.; Pitt, M.; Gleason, M.; McCullar, V.; Bergemann, T.L.; McQueen, K.L.; Guethlein, L.A.; Parham, P.; Miller, J.S. A subpopulation of human peripheral blood NK cells that lacks inhibitory receptors for self-MHC is developmentally immature. Blood 2007, 110, 578–586. [Google Scholar] [CrossRef] [PubMed]
- Parham, P.; Moffett, A. Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution. Nat. Rev. Immunol. 2013, 13, 133–144. [Google Scholar] [CrossRef]
- Manser, A.R.; Weinhold, S.; Uhrberg, M. Human KIR repertoires: Shaped by genetic diversity and evolution. Immunol. Rev. 2015, 267, 178–196. [Google Scholar] [CrossRef]
- Mahaweni, N.M.; Ehlers, F.A.I.; Bos, G.M.J.; Wieten, L. Tuning Natural Killer Cell Anti-multiple Myeloma Reactivity by Targeting Inhibitory Signaling via KIR and NKG2A. Front. Immunol. 2018, 9, 2848. [Google Scholar] [CrossRef]
- Leijonhufvud, C.; Reger, R.; Segerberg, F.; Theorell, J.; Schlums, H.; Bryceson, Y.T.; Childs, R.W.; Carlsten, M. LIR-1 educates expanded human NK cells and defines a unique antitumor NK cell subset with potent antibody-dependent cellular cytotoxicity. Clin. Transl. Immunol. 2021, 10, e1346. [Google Scholar] [CrossRef]
- Highton, A.J.; Diercks, B.P.; Mockl, F.; Martrus, G.; Sauter, J.; Schmidt, A.H.; Bunders, M.J.; Korner, C.; Guse, A.H.; Altfeld, M. High Metabolic Function and Resilience of NKG2A-Educated NK Cells. Front. Immunol. 2020, 11, 559576. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.C.; Stanton, R.J.; Banat, J.J.; Wills, M.R. Leukocyte Immunoglobulin-Like Receptor 1-Expressing Human Natural Killer Cell Subsets Differentially Recognize Isolates of Human Cytomegalovirus through the Viral Major Histocompatibility Complex Class I Homolog UL18. J. Virol. 2016, 90, 3123–3137. [Google Scholar] [CrossRef] [PubMed]
- Boudreau, J.E.; Hsu, K.C. Natural killer cell education in human health and disease. Curr. Opin. Immunol. 2018, 50, 102–111. [Google Scholar] [CrossRef] [PubMed]
- Stanietsky, N.; Mandelboim, O. Paired NK cell receptors controlling NK cytotoxicity. FEBS Lett. 2010, 584, 4895–4900. [Google Scholar] [CrossRef] [PubMed]
- Lopez-Botet, M.; Bellon, T.; Llano, M.; Navarro, F.; Garcia, P.; de Miguel, M. Paired inhibitory and triggering NK cell receptors for HLA class I molecules. Hum. Immunol. 2000, 61, 7–17. [Google Scholar] [CrossRef]
- Almeida, C.R.; Davis, D.M. Segregation of HLA-C from ICAM-1 at NK cell immune synapses is controlled by its cell surface density. J. Immunol. 2006, 177, 6904–6910. [Google Scholar] [CrossRef] [PubMed]
- Jonjic, S.; Babic, M.; Polic, B.; Krmpotic, A. Immune evasion of natural killer cells by viruses. Curr. Opin. Immunol. 2008, 20, 30–38. [Google Scholar] [CrossRef]
- Latchman, Y.; McKay, P.F.; Reiser, H. Identification of the 2B4 molecule as a counter-receptor for CD48. J. Immunol. 1998, 161, 5809–5812. [Google Scholar] [CrossRef]
- Yokoyama, S.; Staunton, D.; Fisher, R.; Amiot, M.; Fortin, J.J.; Thorley-Lawson, D.A. Expression of the Blast-1 activation/adhesion molecule and its identification as CD48. J. Immunol. 1991, 146, 2192–2200. [Google Scholar] [CrossRef]
- Tangye, S.G.; Phillips, J.H.; Lanier, L.L.; Nichols, K.E. Functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. J. Immunol. 2000, 165, 2932–2936. [Google Scholar] [CrossRef]
- Roncagalli, R.; Taylor, J.E.; Zhang, S.; Shi, X.; Chen, R.; Cruz-Munoz, M.E.; Yin, L.; Latour, S.; Veillette, A. Negative regulation of natural killer cell function by EAT-2, a SAP-related adaptor. Nat. Immunol. 2005, 6, 1002–1010. [Google Scholar] [CrossRef] [PubMed]
- Chlewicki, L.K.; Velikovsky, C.A.; Balakrishnan, V.; Mariuzza, R.A.; Kumar, V. Molecular basis of the dual functions of 2B4 (CD244). J. Immunol. 2008, 180, 8159–8167. [Google Scholar] [CrossRef] [PubMed]
- Clarkson, N.G.; Simmonds, S.J.; Puklavec, M.J.; Brown, M.H. Direct and indirect interactions of the cytoplasmic region of CD244 (2B4) in mice and humans with FYN kinase. J. Biol. Chem. 2007, 282, 25385–25394. [Google Scholar] [CrossRef] [PubMed]
- Imsirovic, V.; Lenartic, M.; Wensveen, F.M.; Polic, B.; Jelencic, V. Largely preserved functionality after the combined loss of NKG2D, NCR1 and CD16 demonstrates the remarkable plasticity of NK cell responsiveness. Front. Immunol. 2023, 14, 1191884. [Google Scholar] [CrossRef] [PubMed]
- Sheppard, S.; Triulzi, C.; Ardolino, M.; Serna, D.; Zhang, L.; Raulet, D.H.; Guerra, N. Characterization of a novel NKG2D and NKp46 double-mutant mouse reveals subtle variations in the NK cell repertoire. Blood 2013, 121, 5025–5033. [Google Scholar] [CrossRef]
- Huntington, N.D.; Xu, Y.; Nutt, S.L.; Tarlinton, D.M. A requirement for CD45 distinguishes Ly49D-mediated cytokine and chemokine production from killing in primary natural killer cells. J. Exp. Med. 2005, 201, 1421–1433. [Google Scholar] [CrossRef] [PubMed]
- Lowin-Kropf, B.; Kunz, B.; Schneider, P.; Held, W. A role for the src family kinase Fyn in NK cell activation and the formation of the repertoire of Ly49 receptors. Eur. J. Immunol. 2002, 32, 773–782. [Google Scholar] [CrossRef]
- Sheppard, S.; Sun, J.C. Virus-specific NK cell memory. J. Exp. Med. 2021, 218, e20201731. [Google Scholar] [CrossRef] [PubMed]
- Romee, R.; Schneider, S.E.; Leong, J.W.; Chase, J.M.; Keppel, C.R.; Sullivan, R.P.; Cooper, M.A.; Fehniger, T.A. Cytokine activation induces human memory-like NK cells. Blood 2012, 120, 4751–4760. [Google Scholar] [CrossRef] [PubMed]
- Brillantes, M.; Beaulieu, A.M. Memory and Memory-Like NK Cell Responses to Microbial Pathogens. Front. Cell Infect. Microbiol. 2020, 10, 102. [Google Scholar] [CrossRef]
- Cerwenka, A.; Lanier, L.L. Natural killer cell memory in infection, inflammation and cancer. Nat. Rev. Immunol. 2016, 16, 112–123. [Google Scholar] [CrossRef]
- Sun, J.C.; Beilke, J.N.; Lanier, L.L. Adaptive immune features of natural killer cells. Nature 2009, 457, 557–561. [Google Scholar] [CrossRef] [PubMed]
- Keppel, M.P.; Yang, L.; Cooper, M.A. Murine NK cell intrinsic cytokine-induced memory-like responses are maintained following homeostatic proliferation. J. Immunol. 2013, 190, 4754–4762. [Google Scholar] [CrossRef]
- Cooper, M.A.; Elliott, J.M.; Keyel, P.A.; Yang, L.; Carrero, J.A.; Yokoyama, W.M. Cytokine-induced memory-like natural killer cells. Proc. Natl. Acad. Sci. USA 2009, 106, 1915–1919. [Google Scholar] [CrossRef]
- Lee, J.; Zhang, T.; Hwang, I.; Kim, A.; Nitschke, L.; Kim, M.; Scott, J.M.; Kamimura, Y.; Lanier, L.L.; Kim, S. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity 2015, 42, 431–442. [Google Scholar] [CrossRef] [PubMed]
- Schlums, H.; Cichocki, F.; Tesi, B.; Theorell, J.; Beziat, V.; Holmes, T.D.; Han, H.; Chiang, S.C.; Foley, B.; Mattsson, K.; et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity 2015, 42, 443–456. [Google Scholar] [CrossRef] [PubMed]
- Luetke-Eversloh, M.; Hammer, Q.; Durek, P.; Nordstrom, K.; Gasparoni, G.; Pink, M.; Hamann, A.; Walter, J.; Chang, H.D.; Dong, J.; et al. Human cytomegalovirus drives epigenetic imprinting of the IFNG locus in NKG2Chi natural killer cells. PLoS Pathog. 2014, 10, e1004441. [Google Scholar] [CrossRef] [PubMed]
- Laskowski, T.J.; Biederstadt, A.; Rezvani, K. Natural killer cells in antitumour adoptive cell immunotherapy. Nat. Rev. Cancer 2022, 22, 557–575. [Google Scholar] [CrossRef]
- Molgora, M.; Bonavita, E.; Ponzetta, A.; Riva, F.; Barbagallo, M.; Jaillon, S.; Popovic, 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, 110–114. [Google Scholar] [CrossRef]
- Andre, P.; Denis, C.; Soulas, C.; Bourbon-Caillet, C.; Lopez, J.; Arnoux, T.; Blery, M.; Bonnafous, C.; Gauthier, L.; Morel, A.; et al. Anti-NKG2A mAb Is a Checkpoint Inhibitor that Promotes Anti-tumor Immunity by Unleashing Both T and NK Cells. Cell 2018, 175, 1731–1743 e1713. [Google Scholar] [CrossRef]
- van Montfoort, N.; Borst, L.; Korrer, M.J.; Sluijter, M.; Marijt, K.A.; Santegoets, S.J.; van Ham, V.J.; Ehsan, I.; Charoentong, P.; Andre, P.; et al. NKG2A Blockade Potentiates CD8 T Cell Immunity Induced by Cancer Vaccines. Cell 2018, 175, 1744–1755 e1715. [Google Scholar] [CrossRef]
- Cao, Y.; Wang, X.; Jin, T.; Tian, Y.; Dai, C.; Widarma, C.; Song, R.; Xu, F. Immune checkpoint molecules in natural killer cells as potential targets for cancer immunotherapy. Signal Transduct. Target. Ther. 2020, 5, 250. [Google Scholar] [CrossRef] [PubMed]
- Khan, M.; Arooj, S.; Wang, H. NK Cell-Based Immune Checkpoint Inhibition. Front. Immunol. 2020, 11, 167. [Google Scholar] [CrossRef]
- Poggi, A.; Zocchi, M.R. Natural killer cells and immune-checkpoint inhibitor therapy: Current knowledge and new challenges. Mol. Ther. Oncolytics 2022, 24, 26–42. [Google Scholar] [CrossRef] [PubMed]
- Hsu, J.; Hodgins, J.J.; Marathe, M.; Nicolai, C.J.; Bourgeois-Daigneault, M.C.; Trevino, T.N.; Azimi, C.S.; Scheer, A.K.; Randolph, H.E.; Thompson, T.W.; et al. Contribution of NK cells to immunotherapy mediated by PD-1/PD-L1 blockade. J. Clin. Investig. 2018, 128, 4654–4668. [Google Scholar] [CrossRef]
- Quatrini, L.; Mariotti, F.R.; Munari, E.; Tumino, N.; Vacca, P.; Moretta, L. The Immune Checkpoint PD-1 in Natural Killer Cells: Expression, Function and Targeting in Tumour Immunotherapy. Cancers 2020, 12, 3285. [Google Scholar] [CrossRef]
- Rezvani, K.; Rouce, R.; Liu, E.; Shpall, E. Engineering Natural Killer Cells for Cancer Immunotherapy. Mol. Ther. 2017, 25, 1769–1781. [Google Scholar] [CrossRef] [PubMed]
- Sterner, R.C.; Sterner, R.M. CAR-T cell therapy: Current limitations and potential strategies. Blood Cancer J. 2021, 11, 69. [Google Scholar] [CrossRef] [PubMed]
- Ahmad, A. CAR-T Cell Therapy. Int. J. Mol. Sci. 2020, 21, 4303. [Google Scholar] [CrossRef]
- Sullivan, M.R.; Finocchiaro, M.; Yang, Y.; Thomas, J.; Ali, A.; Kaplan, I.; Abdulhamid, Y.; Bobilev, E.; Sheffer, M.; Romee, R.; et al. An innovative single-cell approach for phenotyping and functional genotyping of CAR NK cells. J. Immunother. Cancer 2024, 12, e008912. [Google Scholar] [CrossRef]
- Liu, E.; Tong, Y.; Dotti, G.; Shaim, H.; Savoldo, B.; Mukherjee, M.; Orange, J.; Wan, X.; Lu, X.; Reynolds, A.; et al. Cord blood NK cells engineered to express IL-15 and a CD19-targeted CAR show long-term persistence and potent antitumor activity. Leukemia 2018, 32, 520–531. [Google Scholar] [CrossRef]
- Li, L.; Mohanty, V.; Dou, J.; Huang, Y.; Banerjee, P.P.; Miao, Q.; Lohr, J.G.; Vijaykumar, T.; Frede, J.; Knoechel, B.; et al. Loss of metabolic fitness drives tumor resistance after CAR-NK cell therapy and can be overcome by cytokine engineering. Sci. Adv. 2023, 9, eadd6997. [Google Scholar] [CrossRef]
- Childs, R.W.; Carlsten, M. Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: The force awakens. Nat. Rev. Drug Discov. 2015, 14, 487–498. [Google Scholar] [CrossRef] [PubMed]
- Tay, S.S.; Carol, H.; Biro, M. TriKEs and BiKEs join CARs on the cancer immunotherapy highway. Hum. Vaccin. Immunother. 2016, 12, 2790–2796. [Google Scholar] [CrossRef]
- Gleason, M.K.; Verneris, M.R.; Todhunter, D.A.; Zhang, B.; McCullar, V.; Zhou, S.X.; Panoskaltsis-Mortari, A.; Weiner, L.M.; Vallera, D.A.; Miller, J.S. Bispecific and trispecific killer cell engagers directly activate human NK cells through CD16 signaling and induce cytotoxicity and cytokine production. Mol. Cancer Ther. 2012, 11, 2674–2684. [Google Scholar] [CrossRef]
- Vallera, D.A.; Ferrone, S.; Kodal, B.; Hinderlie, P.; Bendzick, L.; Ettestad, B.; Hallstrom, C.; Zorko, N.A.; Rao, A.; Fujioka, N.; et al. NK-Cell-Mediated Targeting of Various Solid Tumors Using a B7-H3 Tri-Specific Killer Engager In Vitro and In Vivo. Cancers 2020, 12, 2659. [Google Scholar] [CrossRef] [PubMed]
- Demaria, O.; Gauthier, L.; Vetizou, M.; Blanchard Alvarez, A.; Vagne, C.; Habif, G.; Batista, L.; Baron, W.; Belaid, N.; Girard-Madoux, M.; et al. Antitumor immunity induced by antibody-based natural killer cell engager therapeutics armed with not-alpha IL-2 variant. Cell Rep. Med. 2022, 3, 100783. [Google Scholar] [CrossRef]
- Klein, C.; Waldhauer, I.; Nicolini, V.G.; Freimoser-Grundschober, A.; Nayak, T.; Vugts, D.J.; Dunn, C.; Bolijn, M.; Benz, J.; Stihle, M.; et al. Cergutuzumab amunaleukin (CEA-IL2v), a CEA-targeted IL-2 variant-based immunocytokine for combination cancer immunotherapy: Overcoming limitations of aldesleukin and conventional IL-2-based immunocytokines. Oncoimmunology 2017, 6, e1277306. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Imširović, V.; Wensveen, F.M.; Polić, B.; Jelenčić, V. Maintaining the Balance: Regulation of NK Cell Activity. Cells 2024, 13, 1464. https://doi.org/10.3390/cells13171464
Imširović V, Wensveen FM, Polić B, Jelenčić V. Maintaining the Balance: Regulation of NK Cell Activity. Cells. 2024; 13(17):1464. https://doi.org/10.3390/cells13171464
Chicago/Turabian StyleImširović, Vanna, Felix M. Wensveen, Bojan Polić, and Vedrana Jelenčić. 2024. "Maintaining the Balance: Regulation of NK Cell Activity" Cells 13, no. 17: 1464. https://doi.org/10.3390/cells13171464