Increased sMICA and TGFβ1 levels in HNSCC patients impair NKG2D-dependent functionality of activated NK cells

OncoImmunology

Volumn 4, Issue 11, 2015, Pages

  Klöß, Stephan ^a   Chambron, Nicole ^b   Gardlowski, Tanja ^a   Arseniev, Lubomir ^a   Koch, Joachim ^c   Esser, Ruth ^a   Glienke, Wolfgang ^a   Seitz, Oliver ^b   Köhl, Ulrike ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Klinikum Hanau GmbH   (Germany)

^c INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

HNSCC; NK cell cytotoxicity; NKG2D; soluble MICA; TGF 1; tumor immune escape mechanisms

Indexed keywords

CASPASE 3; CD123 ANTIGEN; CD14 ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; CD3 ANTIGEN; CD36 ANTIGEN; CD4 ANTIGEN; CYTOKINE; GLYCOPHORIN A; HLA DR ANTIGEN; INTERLEUKIN 2; NATURAL KILLER CELL RECEPTOR NKG2D; TRANSFORMING GROWTH FACTOR BETA1;

ADULT; AGED; ARTICLE; CANCER STAGING; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOFLUOROMETRY; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW UP; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOMAGNETIC SEPARATION; IMMUNOTHERAPY; MAJOR CLINICAL STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; NATURAL KILLER CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TIME-LAPSE VIDEO MICROSCOPY; TUMOR ESCAPE; TUMOR GROWTH;

EID: 84941756515     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1055993     Document Type: Article

References (51)

1. K.Shibuya, C.D.Mathers, C.Boschi-Pinto, A.D.Lopez, C.J.Murray. Global and regional estimates of cancer mortality and incidence by site: II. Results for the global burden of disease 2000. BMC Cancer 2002; 2:37; PMID:12502432
2. C.C.Ragin, F.Modugno, S.M.Gollin. The epidemiology and risk factors of head and neck cancer: a focus on human papillomavirus. J Dent Res 2007; 86:104–14; PMID:17251508; http://dx.doi.org/10.1177/154405910708600202
3. H.P.Howaldt, M.Kainz, B.Euler, H.Vorast. Proposal for modification of the TNM staging classification for cancer of the oral cavity. DOSAK. J Craniomaxillofac Surg 1999; 27:275-88; PMID:10717829; http://dx.doi.org/10.1054/jcms.1999.0070
4. C.McLarnon, P.Kulloo, H.Mehanna, C.Kelly, V.Paleri. Quality-of-life considerations in treatment of unresectable, recurrent head and neck cancer. Expert Rev Anticancer Ther 2010; 10:345-52; PMID:20214516; http://dx.doi.org/10.1586/era.10.13
5. L.M.Akst, J.Chan, P.Elson, J.Saxton, M.Strome, D.Adelstein. Functional outcomes following chemoradiotherapy for head and neck cancer. Otolaryngol Head Neck Surg 2004; 131:950-7; PMID:15577796; http://dx.doi.org/10.1016/j.otohns.2004.05.020
6. A.Bose, T.Chakraborty, K.Chakraborty, S.Pal, R.Baral. Dysregulation in immune functions is reflected in tumor cell cytotoxicity by peripheral blood mononuclear cells from head and neck squamous cell carcinoma patients. Cancer Immun 2008; 8:10; PMID:18547033
7. S.S.Farag, M.A.Caligiuri. Human natural killer cell development and biology. Blood Rev 2006; 20:123-37; PMID:16364519; http://dx.doi.org/10.1016/j.blre.2005.10.001
8. S.Kloss, K.Bochennek, S.Huenecke, S.Y.Zimmermann, S.Kuci, T.Muller, W.S.Wels, T.Klingebiel, R.Esser, U.Koehl. A novel five-colour flow cytometric assay to determine NK cell cytotoxicity against neuroblastoma and other adherent tumour cells. J Immunol Methods 2007; 325:140-7; PMID:17663991; http://dx.doi.org/10.1016/j.jim.2007.06.013
9. S.Huenecke, S.Y.Zimmermann, S.Kloess, R.Esser, A.Brinkmann, L.Tramsen, M.Koenig, S.Erben, C.Seidl, T.Tonn, et al. IL-2-driven regulation of NK cell receptors with regard to the distribution of CD16+ and CD16- subpopulations and in vivo influence after haploidentical NK cell infusion. J Immunother 2010; 33:200-10; PMID:20145545; http://dx.doi.org/10.1097/CJI.0b013e3181bb46f7
10. J.D.Coudert, W.Held. The role of the NKG2D receptor for tumor immunity. Semin Cancer Biol 2006; 16:333-43; PMID:16914326; http://dx.doi.org/10.1016/j.semcancer.2006.07.008
11. H.R.Salih, H.Antropius, F.Gieseke, S.Z.Lutz, L.Kanz, H.G.Rammensee, A.Steinle. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003; 102:1389-96; PMID:12714493; http://dx.doi.org/10.1182/blood-2003-01-0019
12. Y.T.Bryceson, H.G.Ljunggren. Tumor cell recognition by the NK cell activating receptor NKG2D. Eur J Immunol 2008; 38(11):2957-61; PMID:18979516
13. V.Groh, J.Wu, C.Yee, T.Spies. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002; 419:734-8; PMID:12384702; http://dx.doi.org/10.1038/nature01112
14. S.Tamaki, N.Sanefuzi, M.Kawakami, K.Aoki, Y.Imai, Y.Yamanaka, K.Yamamoto, A.Ishitani, K.Hatake, T.Kirita. Association between soluble MICA levels and disease stage IV oral squamous cell carcinoma in Japanese patients. Hum Immunol 2008; 69:88-93; PMID:18361932; http://dx.doi.org/10.1016/j.humimm.2008.01.010
15. A.Duray, S.Demoulin, P.Hubert, P.Delvenne, S.Saussez. Immune suppression in head and neck cancers: a review. Clin Dev Immunol 2010; 2010:701657; PMID:21437225; http://dx.doi.org/10.1155/2010/701657
16. S.Dasgupta, M.Bhattacharya-Chatterjee, B.W.O'Malley, Jr., S.K.Chatterjee. Inhibition of NK cell activity through TGF-beta 1 by down-regulation of NKG2D in a murine model of head and neck cancer. J Immunol 2005; 175:5541-50; PMID:16210663; http://dx.doi.org/10.4049/jimmunol.175.8.5541
17. L.Raffaghello, I.Prigione, I.Airoldi, M.Camoriano, I.Levreri, C.Gambini, D.Pende, A.Steinle, S.Ferrone, V.Pistoia. Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 2004; 6:558-68; PMID:15548365; http://dx.doi.org/10.1593/neo.04316
18. J.D.Wu, L.M.Higgins, A.Steinle, D.Cosman, K.Haugk, S.R.Plymate. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J Clin Investig 2004; 114:560-8; PMID:15314693; http://dx.doi.org/10.1172/JCI200422206
19. E.S.Doubrovina, M.M.Doubrovin, E.Vider, R.B.Sisson, R.J.O'Reilly, B.Dupont, Y.M.Vyas. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J Immunol 2003; 171:6891-9; PMID:14662896; http://dx.doi.org/10.4049/jimmunol.171.12.6891
20. S.Kloess, S.Huenecke, D.Piechulek, R.Esser, J.Koch, C.Brehm, J.Soerensen, T.Gardlowski, A.Brinkmann, P.Bader, et al. IL-2-activated haploidentical NK cells restore NKG2D-mediated NK-cell cytotoxicity in neuroblastoma patients by scavenging of plasma MICA. Eur J Immunol 2010; 40:3255-67; PMID:21061445; http://dx.doi.org/10.1002/eji.201040568
21. W.Zou. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 2006; 6:295-307; PMID:16557261; http://dx.doi.org/10.1038/nri1806
22. N.W.Zwirner, M.B.Fuertes, M.V.Girart, C.I.Domaica, L.E.Rossi. Cytokine-driven regulation of NK cell functions in tumor immunity: role of the MICA-NKG2D system. Cytokine Growth Factor Rev 2007; 18:159-70; PMID:17324607; http://dx.doi.org/10.1016/j.cytogfr.2007.01.013
23. T.Walzer, M.Dalod, S.H.Robbins, L.Zitvogel, E.Vivier. Natural-killer cells and dendritic cells: “l'union fait la force”. Blood 2005; 106:2252-8; PMID:15933055; http://dx.doi.org/10.1182/blood-2005-03-1154
24. S.Wulff, R.Pries, K.Borngen, T.Trenkle, B.Wollenberg. Decreased levels of circulating regulatory NK cells in patients with head and neck cancer throughout all tumor stages. Anticancer Res 2009; 29:3053-7; PMID:19661315
25. R.Mukhopadhyaya, R.J.Tatake, N.Krishnan, R.S.Rao, A.R.Fakih, S.L.Naik, S.G.Gangal. Immunoreactivity of lymphocytes from draining lymph nodes, peripheral blood and tumor infiltrates from oral cancer patients. J Clin Lab Immunol 1989; 30:21-5; PMID:2641790
26. N.F.Watson, I.Spendlove, Z.Madjd, R.McGilvray, A.R.Green, I.O.Ellis, J.H.Scholefield, L.G.Durrant. Expression of the stress-related MHC class I chain-related protein MICA is an indicator of good prognosis in colorectal cancer patients. Int J cancer J Int du Cancer 2006; 118:1445-52; PMID:16184547; http://dx.doi.org/10.1002/ijc.21510
27. S.Girlanda, C.Fortis, D.Belloni, E.Ferrero, P.Ticozzi, C.Sciorati, M.Tresoldi, A.Vicari, T.Spies, V.Groh, et al. MICA expressed by multiple myeloma and monoclonal gammopathy of undetermined significance plasma cells Costimulates pamidronate-activated gammadelta lymphocytes. Cancer Res 2005; 65:7502-8; PMID:16103105; http://dx.doi.org/10.1158/0008-5472.CAN-05-0731
28. S.Holdenrieder, P.Stieber, A.Peterfi, D.Nagel, A.Steinle, H.R.Salih. Soluble MICB in malignant diseases: analysis of diagnostic significance and correlation with soluble MICA. Cancer Immunol Immunother 2006; 55:1584-9; PMID:16636811; http://dx.doi.org/10.1007/s00262-006-0167-1
29. A.Franchi, M.Santucci, E.Masini, I.Sardi, M.Paglierani, O.Gallo. Expression of matrix metalloproteinase 1, matrix metalloproteinase 2, and matrix metalloproteinase 9 in carcinoma of the head and neck. Cancer 2002; 95:1902-10; PMID:12404284; http://dx.doi.org/10.1002/cncr.10916
30. G.Chitadze, M.Lettau, J.Bhat, D.Wesch, A.Steinle, D.Furst, J.Mytilineos, H.Kalthoff, O.Janssen, H.H.Oberg, et al. Shedding of endogenous MHC class I-related chain molecules A and B from different human tumor entities: heterogeneous involvement of the “a disintegrin and metalloproteases” 10 and 17. Int J Cancer J Int du Cancer 2013; 133:1557-66; PMID:23526433; http://dx.doi.org/10.1002/ijc.28174
31. C.Badoual, G.Bouchaud, H.Agueznay Nel, E.Mortier, S.Hans, A.Gey, F.Fernani, S.Peyrard, P.L.Puig, P.Bruneval, et al. The soluble alpha chain of interleukin-15 receptor: a proinflammatory molecule associated with tumor progression in head and neck cancer. Cancer Res 2008; 68:3907-14; PMID:18483276; http://dx.doi.org/10.1158/0008-5472.CAN-07-6842
32. D.Pende, C.Cantoni, P.Rivera, M.Vitale, R.Castriconi, S.Marcenaro, M.Nanni, R.Biassoni, C.Bottino, A.Moretta, et al. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur J Immunol 2001; 31:1076-86; PMID:11298332; http://dx.doi.org/10.1002/1521-4141(200104)31:4%3c1076::AID-IMMU1076%3e3.0.CO;2-Y
33. J.R.Ostberg, B.E.Dayanc, M.Yuan, E.Oflazoglu, E.A.Repasky. Enhancement of natural killer (NK) cell cytotoxicity by fever-range thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells. J leukoc Biol 2007; 82:1322-31; PMID:17711975; http://dx.doi.org/10.1189/jlb.1106699
34. S.Tamaki, M.Kawakami, A.Ishitani, W.Kawashima, S.Kasuda, Y.Yamanaka, H.Shimomura, Y.Imai, Y.Nakagawa, K.Hatake, et al. Soluble MICB serum levels correlate with disease stage and survival rate in patients with oral squamous cell carcinoma. Anticancer Res 2010; 30:4097-101; PMID:21036725
35. V.Rebmann, P.Schutt, D.Brandhorst, B.Opalka, T.Moritz, M.R.Nowrousian, H.Grosse-Wilde. Soluble MICA as an independent prognostic factor for the overall survival and progression-free survival of multiple myeloma patients. Clin Immunol 2007; 123:114-20; PMID:17218152; http://dx.doi.org/10.1016/j.clim.2006.11.007
36. S.Tamaki, M.Kawakami, Y.Yamanaka, H.Shimomura, Y.Imai, J.Ishida, K.Yamamoto, A.Ishitani, K.Hatake, T.Kirita. Relationship between soluble MICA and the MICA A5.1 homozygous genotype in patients with oral squamous cell carcinoma. Clin Immunol 2009; 130:331-7; PMID:18951065; http://dx.doi.org/10.1016/j.clim.2008.09.004
37. L.E.Rossi, D.E.Avila, R.G.Spallanzani, A.Ziblat, M.B.Fuertes, L.Lapyckyj, D.O.Croci, G.A.Rabinovich, C.I.Domaica, N.W.Zwirner. Histone deacetylase inhibitors impair NK cell viability and effector functions through inhibition of activation and receptor expression 2012; 91(2):321-31; Epub 2011 Nov 28; http://dx.doi.org/10.1189/jlb.0711339
38. A.Marten, M.von Lilienfeld-Toal, M.W.Buchler, J.Schmidt. Soluble MIC is elevated in the serum of patients with pancreatic carcinoma diminishing gammadelta T cell cytotoxicity. Int J Cancer J Int du Cancer 2006; 119:2359-65; PMID:16929491; http://dx.doi.org/10.1002/ijc.22186
39. C.A.Crane, S.J.Han, J.J.Barry, B.J.Ahn, L.L.Lanier, A.T.Parsa. TGF-beta downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro-oncology 2010; 12:7-13; PMID:20150362; http://dx.doi.org/10.1093/neuonc/nop009
40. M.Ghio, P.Contini, S.Negrini, S.Boero, A.Musso, A.Poggi. Soluble HLA-I-mediated secretion of TGF-beta1 by human NK cells and consequent down-regulation of anti-tumor cytolytic activity. Eur J Immunol 2009; 39:3459-68; PMID:19830740; http://dx.doi.org/10.1002/eji.200939728
41. E.B.Wilson, J.J.El-Jawhari, A.L.Neilson, G.D.Hall, A.A.Melcher, J.L.Meade, G.P.Cook. Human tumour immune evasion via TGF-beta blocks NK cell activation but not survival allowing therapeutic restoration of anti-tumour activity. PloS one 2011; 6:e22842
42. S.Lyford-Pike, S.Peng, G.D.Young, J.M.Taube, W.H.Westra, B.Akpeng, T.C.Bruno, J.D.Richmon, H.Wang, J.A.Bishop, et al. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res 2013; 73:1733-41; PMID:23288508; http://dx.doi.org/10.1158/0008-5472.CAN-12-2384
43. D.M.Benson, Jr., C.E.Bakan, A.Mishra, C.C.Hofmeister, Y.Efebera, B.Becknell, R.A.Baiocchi, J.Zhang, J.Yu, M.K.Smith, et al. The PD-1/PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood 2010; 116:2286-94; PMID:20460501; http://dx.doi.org/10.1182/blood-2010-02-271874
44. C.Badoual, S.Hans, N.Merillon, C.Van Ryswick, P.Ravel, N.Benhamouda, E.Levionnois, M.Nizard, A.Si-Mohamed, N.Besnier, et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-associated head and neck cancer. Cancer Res 2013; 73:128-38; PMID:23135914; http://dx.doi.org/10.1158/0008-5472.CAN-12-2606
45. Baragano A.Raneros, B.Suarez-Alvarez, C.Lopez-Larrea. Secretory pathways generating immunosuppressive NKG2D ligands: New targets for therapeutic intervention. Oncoimmunology 2014; 3:e28497; PMID:25050215; http://dx.doi.org/10.4161/onci.28497
46. E.Ullrich, J.Koch, A.Cerwenka, A.Steinle. New prospects on the NKG2D/NKG2DL system for oncology. Oncoimmunology 2013; 2:e26097; PMID:24353908; http://dx.doi.org/10.4161/onci.26097
47. U.Koehl, C.Brehm, S.Huenecke, S.Y.Zimmermann, S.Kloess, M.Bremm, E.Ullrich, J.Soerensen, A.Quaiser, S.Erben, et al. Clinical grade purification and expansion of NK cell products for an optimized manufacturing protocol. Front Oncol 2013; 3:118; PMID:23730623; http://dx.doi.org/10.3389/fonc.2013.00118
48. S.Huenecke, M.Behl, C.Fadler, S.Y.Zimmermann, K.Bochennek, L.Tramsen, R.Esser, D.Klarmann, M.Kamper, A.Sattler, et al. Age-matched lymphocyte subpopulation reference values in childhood and adolescence: application of exponential regression analysis. Eur J Haematol 2008; 80:532-9; PMID:18284628
49. J.G.Rheinwald, M.A.Beckett. Tumorigenic keratinocyte lines requiring anchorage and fibroblast support cultures from human squamous cell carcinomas. Cancer research 1981; 41:1657-63; PMID:7214336
50. J.G.Rheinwald, M.A.Beckett. Defective terminal differentiation in culture as a consistent and selectable character of malignant human keratinocytes. Cell 1980; 22:629-32; PMID:6160916; http://dx.doi.org/10.1016/0092-8674(80)90373-6
51. S.Y.Zimmermann, R.Esser, E.Rohrbach, T.Klingebiel, U.Koehl. A novel four-colour flow cytometric assay to determine natural killer cell or T-cell-mediated cellular cytotoxicity against leukaemic cells in peripheral or bone marrow specimens containing greater than 20% of normal cells. J Immunol Methods 2005; 296:63-76; PMID:15680151