Human anaplastic thyroid carcinoma cells are sensitive to NK cell-mediated lysis via ULBP2/5/6 and chemoattract NK cells

Clinical Cancer Research

Volumn 20, Issue 22, 2014, Pages 5733-5744

  Wennerberg, Erik ^a   Pfefferle, Aline ^a   Ekblad, Lars ^b   Yoshimoto, Yuya ^a   Kremer, Veronika ^a   Kaminskyy, Vitaliy O ^a   Juhlin, C Christofer ^a   Höög, Anders ^a   Bodin, Inger ^a   Svjatoha, Vitalijs ^a   Larsson, Catharina ^a   Zedenius, Jan ^a   Wennerberg, Johan ^b   Lundqvist, Andreas ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHEMOATTRACTANT; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10; NATURAL KILLER CELL RECEPTOR NKG2D; PROSTAGLANDIN E2; PROTEIN ULBP2; PROTEIN ULBP5; PROTEIN ULBP6; UNCLASSIFIED DRUG; BLOCKING ANTIBODY; CYCLOOXYGENASE 2; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; MONOCLONAL ANTIBODY; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; SIGNAL PEPTIDE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; ULBP2 PROTEIN, HUMAN;

ANAPLASTIC THYROID CANCER; ARTICLE; BLOOD SAMPLING; CELL EXPANSION; CELL INFILTRATION; CELL INTERACTION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOLYSIS; DOWN REGULATION; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NATURAL KILLER CELL; PHENOTYPE; PROTEIN EXPRESSION; THYROID CANCER CELL LINE; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHEMOTAXIS; CYTOTOXICITY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; THYROID CARCINOMA; TUMOR CELL LINE;

ANTIBODIES, BLOCKING; ANTIBODIES, MONOCLONAL; CELL LINE, TUMOR; CHEMOKINE CXCL10; CHEMOTAXIS; CYCLOOXYGENASE 2; CYTOTOXICITY, IMMUNOLOGIC; DINOPROSTONE; GENE EXPRESSION; GPI-LINKED PROTEINS; HUMANS; IMMUNOPHENOTYPING; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PHENOTYPE; RECEPTORS, CXCR3; THYROID CARCINOMA, ANAPLASTIC; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84918591544     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-0291     Document Type: Article

References (50)

1. Green LD, Mack L, Pasieka JL. Anaplastic thyroid cancer and primary thyroid lymphoma: a review of these rare thyroid malignancies. J Surg Oncol 2006;94:725-36.
2. Yu GP, Li JC, Branovan D, McCormick S, Schantz SP. Thyroid cancer incidence and survival in the national cancer institute surveillance, epidemiology, and end results race/ethnicity groups. Thyroid 2010;20:465-73.
3. Papewalis C, Wuttke M, Jacobs B, Domberg J, Willenberg H, Baehring T, et al. Dendritic cell vaccination induces tumor epitope-specific Th1 immune response in medullary thyroid carcinoma. Horm Metab Res 2008;40:108-16.
4. Papewalis C, Ehlers M, Schott M. Advances in cellular therapy for the treatment of thyroid cancer. J Oncol 2010;2010:179491.
5. Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 2005;105:3051-7.
6. Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res 2011;17:6287-97.
7. Lundqvist A, Berg M, Smith A, Childs RW. Bortezomib treatment to potentiate the anti-tumor immunity of ex-vivo expanded adoptively infused autologous natural killer cells. J Cancer 2011;2:383-5.
8. 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.
9. Li C, Ge B, Nicotra M, Stern JN, Kopcow HD, Chen X, et al. JNK MAP kinase activation is required for MTOC and granule polarization in NKG2D-mediated NK cell cytotoxicity. Proc Natl Acad Sci U S A 2008;105:3017-22.
10. Li H, Lakshmikanth T, Garofalo C, Enge M, Spinnler C, Anichini A, et al. Pharmacological activation of p53 triggers anticancer innate immune response through induction of ULBP2. Cell Cycle 2011;10:3346-58.
11. Takanami I, Takeuchi K, Giga M. The prognostic value of natural killer cell infiltration in resected pulmonary adenocarcinoma. J Thorac Cardiovasc Surg 2001;121:1058-63.
12. Ishigami S, Natsugoe S, Tokuda K, Nakajo A, Che X, Iwashige H, et al. Prognostic value of intratumoral natural killer cells in gastric carcinoma. Cancer 2000;88:577-83.
13. Maghazachi AA. Role of chemokines in the biology of natural killer cells. Curr Top Microbiol Immunol 2010;341:37-58.
14. 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.
15. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, Berger A, et al. Biomolecular network reconstruction identifies T-cell homing factors associated with survival in colorectal cancer. Gastroenterology 2010;138:1429-40.
16. Vitale M, Cantoni C, Pietra G, Mingari MC, Moretta L. Effect of tumor cells and tumor microenvironment on NK-cell function. Eur J Immunol 2014;44:1582-92.
17. Berg M, Lundqvist A, McCoy P Jr, Samsel L, Fan Y, Tawab A, et al. Clinical-grade ex vivo -expanded human natural killer cells upregulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy 2009;11:341-55.
18. Sutlu T, Alici E. Ex vivo expansion of natural killer cells: a question of function. Cytotherapy 2011;13:767-8.
19. Besana C, Sabbadini MG, Corti C, Di Lucca G, Foppoli M, Marcatti M, et al. Autoimmune thyroiditis following interleukin-2 and LAK cell therapy for metastatic renal cell carcinoma: correlation with tumor regression. Tumori 1991;77:339-42.
20. Steegmann JL, Requena MJ, Martin-Regueira P, De La Camara R, Casado F, Salvanes FR, et al. High incidence of autoimmune alterations in chronic myeloid leukemia patients treated with interferon-alpha. Am J Hematol 2003;72:170-6.
21. Bronstein Y, Ng CS, Hwu P, Hwu WJ. Radiologic manifestations of immune-related adverse events in patients with metastatic melanoma undergoing anti-CTLA-4 antibody therapy. AJR Am J Roentgenol 2011;197:W992-1000.
22. Bernardo SG, Moskalenko M, Pan M, Shah S, Sidhu HK, Sicular S, et al. Elevated rates of transaminitis during ipilimumab therapy for metastatic melanoma. Melanoma Res 2013;23:47-54.
23. Hidaka Y, Amino N, Iwatani Y, Kaneda T, Nasu M, Mitsuda N, et al. Increase in peripheral natural killer cell activity in patients with autoimmune thyroid disease. Autoimmunity 1992;11:239-46.
24. Godal R, Keilholz U, Uharek L, Letsch A, Asemissen AM, Busse A, et al. Lymphomas are sensitive to perforin-dependent cytotoxic pathways despite expression of PI-9 and overexpression of bcl-2. Blood 2006;107:3205-11.
25. Carlsten M, Bjorkstrom NK, Norell H, Bryceson Y, van Hall T, Baumann BC, et al. DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells. Cancer Res 2007;67:1317-25.
26. Carbone E, Neri P, Mesuraca M, Fulciniti MT, Otsuki T, Pende D, et al. HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells. Blood 2005;105:251-8.
27. Cerwenka A, Baron JL, Lanier LL. 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 U S A 2001;98:11521-6.
28. Fernandez-Messina L, Ashiru O, Aguera-Gonzalez S, Reyburn HT, Vales-Gomez M. The human NKG2D ligand ULBP2 can be expressed at the cell surface with or without a GPI anchor and both forms can activate NK cells. J Cell Sci 2011;124:321-7.
29. Paschen A, Sucker A, Hill B, Moll I, Zapatka M, Nguyen XD, et al. Differential clinical significance of individual NKG2D ligands in melanoma: soluble ULBP2 as an indicator of poor prognosis superior to S100B. Clin Cancer Res 2009;15:5208-15.
30. Kawashima A, Yamazaki K, Hara T, Akama T, Yoshihara A, Sue M, et al. Demonstration of innate immune responses in the thyroid gland: potential to sense danger and a possible trigger for autoimmune reactions. Thyroid 2013;23:477-87.
31. Antonelli A, Fallahi P, Rotondi M, Ferrari SM, Serio M, Miccoli P. Serum levels of the interferon-gamma-inducible alpha chemokine CXCL10 in patients with active Graves' disease, and modulation by methimazole therapy and thyroidectomy. Br J Surg 2006;93:1226-31.
32. Antonelli A, Ferrari SM, Mancusi C, Mazzi V, Pupilli C, Centanni M, et al. Interferon-alpha, -beta and -gamma induce CXCL11 secretion in human thyrocytes: modulation by peroxisome proliferator-activated receptor gamma agonists. Immunobiology 2013;218:690-5.
33. Antonelli A, Ferrari SM, Fallahi P, Frascerra S, Piaggi S, Gelmini S, et al. Dysregulation of secretion of CXC alpha-chemokine CXCL10 in papillary thyroid cancer: modulation by peroxisome proliferator-activated receptor-gamma agonists. Endocr Relat Cancer 2009;16:1299-311.
34. Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410:1107-11.
35. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004;5:1260-5.
36. Li Z, Pradera F, Kammertoens T, Li B, Liu S, Qin Z. Cross-talk between T cells and innate immune cells is crucial for IFN-gamma-dependent tumor rejection. J Immunol 2007;179:1568-76.
37. Ohmori Y, Hamilton TA. The interferon-stimulated response element and a kappa B site mediate synergistic induction of murine IP-10 gene transcription by IFN-gamma and TNF-alpha. J Immunol 1995;154:5235-44.
38. Gogali F, Paterakis G, Rassidakis GZ, Liakou CI, Liapi C. CD3(-)CD16(-) CD56(bright) immunoregulatory NK cells are increased in the tumor microenvironment and inversely correlate with advanced stages in patients with papillary thyroid cancer. Thyroid 2013;23:1561-8.
39. Bauernhofer T, Kuss I, Henderson B, Baum AS, Whiteside TL. Preferential apoptosis of CD56dim natural killer cell subset in patients with cancer. Eur J Immunol 2003;33:119-24.
40. Harlin H, Hanson M, Johansson CC, Sakurai D, Poschke I, Norell H, et al. The CD16- CD56(bright) NK cell subset is resistant to reactive oxygen species produced by activated granulocytes and has higher antioxidative capacity than the CD16+ CD56(dim) subset. J Immunol 2007;179:4513-9.
41. Morandi F, Ferretti E, Castriconi R, Dondero A, Petretto A, Bottino C, et al. Soluble HLA-G dampens CD94/NKG2A expression and function and differentially modulates chemotaxis and cytokine and chemokine secretion in CD56bright and CD56dim NK cells. Blood 2011;118:5840-50.
42. Eisenhardt M, Glassner A, Kramer B, Korner C, Sibbing B, Kokordelis P, et al. The CXCR3(+)CD56Bright phenotype characterizes a distinct NK cell subset with anti-fibrotic potential that shows dys-regulated activity in hepatitis C. PLoS One 2012;7:e38846.
43. Sancho D, Gomez M, Sanchez-Madrid F. CD69 is an immunoregulatory molecule induced following activation. Trends Immunol 2005;26:136-40.
44. Esplugues E, Sancho D, Vega-Ramos J, Martinez C, Syrbe U, Hamann A, et al. Enhanced antitumor immunity in mice deficient in CD69. J Exp Med 2003;197:1093-106.
45. Benson DM Jr, Bakan CE, Mishra A, Hofmeister CC, Efebera Y, Becknell B, 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.
46. Funk CD. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 2001;294:1871-5.
47. Wolff H, Saukkonen K, Anttila S, Karjalainen A, Vainio H, Ristimaki A. Expression of cyclooxygenase-2 in human lung carcinoma. Cancer Res 1998;58:4997-5001.
48. Eberhart CE, Coffey RJ, Radhika A, Giardiello FM, Ferrenbach S, DuBois RN. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 1994;107:1183-8.
49. Martinet L, Jean C, Dietrich G, Fournie JJ, Poupot R. PGE2 inhibits natural killer and gamma delta T cell cytotoxicity triggered by NKR and TCR through a cAMP-mediated PKA type I-dependent signaling. Biochem Pharmacol 2010;80:838-45.
50. Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res 2008;68:6368-76.