Intratumoral natural killer cells show reduced effector and cytolytic properties and control the differentiation of effector Th1 cells

OncoImmunology

Volumn 5, Issue 12, 2016, Pages

  Paul, Sourav ^a   Kulkarni, Neeraja ^a   Shilpi, Neeraja ^a   Lal, Girdhari ^a  

^a NATIONAL CENTRE FOR CELL SCIENCE   (India)

Author keywords

Natural killer (NK) cells; NKG2D; Th1 cells; tolerance; tumor microenvironment

Indexed keywords

CD11B ANTIGEN; CD27 ANTIGEN; CD69 ANTIGEN; CELL THERAPY AGENT; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 21 RECEPTOR; INTERLEUKIN 6; NATURAL KILLER CELL RECEPTOR NKG2D;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL THERAPY; DEGRANULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HOUSEKEEPING GENE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH1 CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

EID: 85002406507     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1235106     Document Type: Article

References (55)

1. Hayakawa Y, Smyth MJ. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 2006; 176:1517-24; PMID:16424180; http://dx.doi.org/10.4049/jimmunol.176.3.1517
2. Fu B, Wang F, Sun R, Ling B, Tian Z, Wei H. CD11b and CD27 reflect distinct population and functional specialization in human natural killer cells. Immunol 2011; 133:350-9; PMID:21506999; http://dx.doi.org/10.1111/j.1365-2567.2011.03446.x
3. Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood 2009; 113:5488-96; PMID:19234143; http://dx.doi.org/10.1182/blood-2008-10-187179
4. Crouse J, Xu HC, Lang PA, Oxenius A. NK cells regulating T cell responses:mechanisms and outcome. Trends Immunol 2015; 36:49-58; PMID:25432489; http://dx.doi.org/10.1016/j.it.2014.11.001
5. Hayakawa Y, Sato-Matsushita M, Takeda K, Iwakura Y, Tahara H, Irimura T. Early activation and interferon-gamma production of tumor-infiltrating mature CD27 high natural killer cells. Cancer Sci 2011; 102:1967-71; PMID:21781225; http://dx.doi.org/10.1111/j.1349-7006.2011.02042.x
6. Ballas ZK, Buchta CM, Rosean TR, Heusel JW, Shey MR. Role of NK cell subsets in organ-specific murine melanoma metastasis. PLoS One 2013; 8:e65599; PMID:23776508; http://dx.doi.org/10.1371/journal.pone.0065599
7. Jin J, Fu B, Mei X, Yue T, Sun R, Tian Z, Wei H. CD11b(-)CD27(-) NK cells are associated with the progression of lung carcinoma. PLoS One 2013; 8:e61024; PMID:23565296; http://dx.doi.org/10.1371/journal.pone.0061024
8. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A, Balsamo M, Conte R, Benelli R, Minghelli S, et al. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res 2012; 72:1407-15; PMID:22258454; http://dx.doi.org/10.1158/0008-5472.CAN-11-2544
9. Balsamo M, Scordamaglia F, Pietra G, Manzini C, Cantoni C, Boitano M, Queirolo P, Vermi W, Facchetti F, Moretta A, et al. Melanoma-associated fibroblasts modulate NK cell phenotype and antitumor cytotoxicity. Proc Natl Acad Sci USA 2009; 106:20847-52; PMID:19934056; http://dx.doi.org/10.1073/pnas.0906481106
10. Cekic C, Day YJ, Sag D, Linden J. Myeloid expression of adenosine A2A receptor suppresses T and NK cell responses in the solid tumor microenvironment. Cancer Res 2014; 74:7250-9; PMID:25377469; http://dx.doi.org/10.1158/0008-5472.CAN-13-3583
11. + and NK lymphocytes in the direct cell-to-cell interaction. Clin Immunol 2004; 112:258-67; PMID:15308119; http://dx.doi.org/10.1016/j.clim.2004.04.003
12. 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-β 1. J Immunol 2009; 182:240-9; PMID:19109155; http://dx.doi.org/10.4049/jimmunol.182.1.240
13. Ardolino M, Azimi CS, Iannello A, Trevino TN, Horan L, Zhang L, Deng W, Ring AM, Fischer S, Garcia KC, et al. Cytokine therapy reverses NK cell anergy in MHC-deficient tumors. J Clin Invest 2014; 124:4781-94; PMID:25329698; http://dx.doi.org/10.1172/JCI74337
14. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence:an 11-year follow-up study of a general population. Lancet 2000; 356:1795-9; PMID:11117911; http://dx.doi.org/10.1016/S0140-6736(00)03231-1
15. Ljunggren HG, Malmberg KJ. Prospects for the use of NK cells in immunotherapy of human cancer. Nat Rev Immunol 2007; 7:329-39; PMID:17438573; http://dx.doi.org/10.1038/nri2073
16. Sutlu T, Alici E. Natural killer cell-based immunotherapy in cancer:current insights and future prospects. J Intern Med 2009; 266:154-81; PMID:19614820; http://dx.doi.org/10.1111/j.1365-2796.2009.02121.x
17. Huntington ND, Tabarias H, Fairfax K, Brady J, Hayakawa Y, Degli-Esposti MA, Smyth MJ, Tarlinton DM, Nutt SL. NK cell maturation and peripheral homeostasis is associated with KLRG1 upregulation. J Immunol 2007; 178:4764-70; PMID:17404256; http://dx.doi.org/10.4049/jimmunol.178.8.4764
18. Long EO, Kim HS, Liu D, Peterson ME, Rajagopalan S. Controlling natural killer cell responses:integration of signals for activation and inhibition. Ann Rev Immunol 2013; 31:227-58; PMID:23516982; http://dx.doi.org/10.1146/annurev-immunol-020711-075005
19. Mizutani T, Neugebauer N, Putz EM, Moritz N, Simma O, Zebedin-Brandl E, Gotthardt D, Warsch W, Eckelhart E, Kantner HP, et al. Conditional IFNAR1 ablation reveals distinct requirements of Type I IFN signaling for NK cell maturation and tumor surveillance. Oncoimmunol 2012; 1:1027-37; PMID:23170251; http://dx.doi.org/10.4161/onci.21284
20. Skak K, Frederiksen KS, Lundsgaard D. Interleukin-21 activates human natural killer cells and modulates their surface receptor expression. Immunology 2008; 123:575-83; PMID:18005035; http://dx.doi.org/10.1111/j.1365-2567.2007.02730.x
21. Brady J, Hayakawa Y, Smyth MJ, Nutt SL. IL-21 induces the functional maturation of murine NK cells. J Immunol 2004; 172:2048-58; PMID:14764669; http://dx.doi.org/10.4049/jimmunol.172.4.2048
22. Takaki R, Hayakawa Y, Nelson A, Sivakumar PV, Hughes S, Smyth MJ, Lanier LL. IL-21 enhances tumor rejection through a NKG2D-dependent mechanism. J Immunol 2005; 175:2167-73; PMID:16081783; http://dx.doi.org/10.4049/jimmunol.175.4.2167
23. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Xiangming C, Iwashige H, Aridome K, Hokita S, Aikou T. Clinical impact of intratumoral natural killer cell and dendritic cell infiltration in gastric cancer. Cancer Letters 2000; 159:103-8; PMID:10974412; http://dx.doi.org/10.1016/S0304-3835(00)00542-5
24. Villegas FR, Coca S, Villarrubia VG, Jimenez R, Chillon MJ, Jareno J, Zuil M, Callol L. Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 2002; 35:23-8; PMID:11750709; http://dx.doi.org/10.1016/S0169-5002(01)00292-6
25. Lakshmikanth T, Burke S, Ali TH, Kimpfler S, Ursini F, Ruggeri L, Capanni M, Umansky V, Paschen A, Sucker A, et al. NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J Clin Invest 2009; 119:1251-63; PMID:19349689; http://dx.doi.org/10.1172/JCI36022
26. Pedroza-Pacheco I, Madrigal A, Saudemont A. Interaction between natural killer cells and regulatory T cells:perspectives for immunotherapy. Cell Mol Immunol 2013; 10:222-9; PMID:23524654; http://dx.doi.org/10.1038/cmi.2013.2
27. Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, Lehner F, Manns MP, Greten TF, Korangy F. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009; 50:799-807; PMID:19551844; http://dx.doi.org/10.1002/hep.23054
28. Chen S, Kawashima H, Lowe JB, Lanier LL, Fukuda M. Suppression of tumor formation in lymph nodes by L-selectin-mediated natural killer cell recruitment. J Exp Med 2005; 202:1679-89; PMID:16352740; http://dx.doi.org/10.1084/jem.20051473
29. Wendel M, Galani IE, Suri-Payer E, Cerwenka A. Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res 2008; 68:8437-45; PMID:18922917; http://dx.doi.org/10.1158/0008-5472.CAN-08-1440
30. Lavergne E, Combadiere B, Bonduelle O, Iga M, Gao JL, Maho M, Boissonnas A, Murphy PM, Debré P, Combadière C. Fractalkine mediates natural killer-dependent antitumor responses in vivo. Cancer Res 2003; 63:7468-74; PMID:14612547
31. Esplugues E, Sancho D, Vega-Ramos J, Martinez C, Syrbe U, Hamann A, Engel P, Sánchez-Madrid F, Lauzurica P. Enhanced antitumor immunity in mice deficient in CD69. J Exp Med 2003; 197:1093-106; PMID:12732655; http://dx.doi.org/10.1084/jem.20021337
32. Esplugues E, Vega-Ramos J, Cartoixa D, Vazquez BN, Salaet I, Engel P, Lauzurica P. Induction of tumor NK-cell immunity by anti-CD69 antibody therapy. Blood 2005; 105:4399-406; PMID:15692061; http://dx.doi.org/10.1182/blood-2004-10-3854
33. + NK cells. Biomarkers 2009; 14:258-70; PMID:19489688; http://dx.doi.org/10.1080/13547500902814658
34. Markel G, Seidman R, Besser MJ, Zabari N, Ortenberg R, Shapira R, Treves AJ, Loewenthal R, Orenstein A, Nagler A, et al. Natural killer lysis receptor (NKLR)/NKLR-ligand matching as a novel approach for enhancing anti-tumor activity of allogeneic NK cells. PloS One 2009; 4:e5597; PMID:19440333; http://dx.doi.org/10.1371/journal.pone.0005597
35. Fregni G, Messaoudene M, Fourmentraux-Neves E, Mazouz-Dorval S, Chanal J, Maubec E, Marinho E, Scheer-Senyarich I, Cremer I, Avril MF, et al. Phenotypic and functional characteristics of blood natural killer cells from melanoma patients at different clinical stages. Plos One 2013; 8:e76928; PMID:24204708; http://dx.doi.org/10.1371/journal.pone.0076928
36. Messaoudene M, Fregni G, Fourmentraux-Neves E, Chanal J, Maubec E, Mazouz-Dorval S, Couturaud B, Girod A, Sastre-Garau X, Albert S, et al. Mature cytotoxic CD56(bright)/CD16(+) natural killer cells can infiltrate lymph nodes adjacent to metastatic melanoma. Cancer Res 2014; 74:81-92; PMID:24225017; http://dx.doi.org/10.1158/0008-5472.CAN-13-1303
37. Kadri N, Luu Thanh T, Hoglund P. Selection, tuning, and adaptation in mouse NK cell education. Immunol Rev 2015; 267:167-77; PMID:26284477; http://dx.doi.org/10.1111/imr.12330
38. Tu MM, Mahmoud AB, Wight A, Mottashed A, Belanger S, Rahim MM, Abou-Samra E, Makrigiannis AP. Ly49 family receptors are required for cancer immunosurveillance mediated by natural killer cells. Cancer Res 2014; 74:3684-94; PMID:24802191; http://dx.doi.org/10.1158/0008-5472.CAN-13-3021
39. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature 2009; 457:557-61; PMID:19136945; http://dx.doi.org/10.1038/nature07665
40. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 1998; 95:7556-61; PMID:9636188; http://dx.doi.org/10.1073/pnas.95.13.7556
41. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science 1996; 272:719-22; PMID:8614832; http://dx.doi.org/10.1126/science.272.5262.719
42. + T cells requires tumor responsiveness to IFN-gamma. J Immunol 2001; 166:2276-82; PMID:11160282; http://dx.doi.org/10.4049/jimmunol.166.4.2276
43. Chawla-Sarkar M, Lindner DJ, Liu YF, Williams BR, Sen GC, Silverman RH, Borden EC. Apoptosis and interferons:role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 2003; 8:237-49; PMID:12766484; http://dx.doi.org/10.1023/A:1023668705040
44. Crome SQ, Lang PA, Lang KS, Ohashi PS. Natural killer cells regulate diverse T cell responses. Trends Immunol 2013; 34:342-9; PMID:23601842; http://dx.doi.org/10.1016/j.it.2013.03.002
45. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004; 5:1260-5; PMID:15531883; http://dx.doi.org/10.1038/ni1138
46. Morandi B, Bougras G, Muller WA, Ferlazzo G, Munz C. NK cells of human secondary lymphoid tissues enhance T cell polarization via IFN-gamma secretion. Eur J Immunol 2006; 36:2394-400; PMID:16917961; http://dx.doi.org/10.1002/eji.200636290
47. Laouar Y, Sutterwala FS, Gorelik L, Flavell RA. Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat Immunol 2005; 6:600-7; PMID:15852008; http://dx.doi.org/10.1038/ni1197
48. + T cells in malignant pleural effusion. J Immunol 2010; 185:6348-54; PMID:20952674; http://dx.doi.org/10.4049/jimmunol.1001728
49. Gnerlich JL, Mitchem JB, Weir JS, Sankpal NV, Kashiwagi H, Belt BA, Porembka MR, Herndon JM, Eberlein TJ, Goedegebuure P, et al. Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. J Immunol 2010; 185:4063-71; PMID:20805420; http://dx.doi.org/10.4049/jimmunol.0902609
50. Martin-Orozco N, Muranski P, Chung Y, Yang XO, Yamazaki T, Lu S, Hwu P, Restifo NP, Overwijk WW, Dong C. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 2009; 31:787-98; PMID:19879162; http://dx.doi.org/10.1016/j.immuni.2009.09.014
51. Muranski P, Boni A, Antony PA, Cassard L, Irvine KR, Kaiser A, Paulos CM, Palmer DC, Touloukian CE, Ptak K, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 2008; 112:362-73; PMID:18354038; http://dx.doi.org/10.1182/blood-2007-11-120998
52. Smyth MJ, Crowe NY, Godfrey DI. NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 2001; 13:459-63; PMID:11282985; http://dx.doi.org/10.1093/intimm/13.4.459
53. Kaufman HL, Ruby CE, Hughes T, Slingluff CL, Jr. Current status of granulocyte-macrophage colony-stimulating factor in the immunotherapy of melanoma. J Immunother Cancer 2014; 2:11; PMID:24971166; http://dx.doi.org/10.1186/2051-1426-2-11
54. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 2002; 3:1150-5; PMID:12426564; http://dx.doi.org/10.1038/ni857
55. Spear P, Wu MR, Sentman ML, Sentman CL. NKG2D ligands as therapeutic targets. Cancer Immunity 2013; 13:8; PMID:23833565