A disintegrin and metalloproteinases 10 and 17 modulate the immunogenicity of glioblastoma-initiating cells

Neuro-Oncology

Volumn 16, Issue 3, 2014, Pages 382-391

  Wolpert, Fabian ^a   Tritschler, Isabel ^a   Steinle, Alexander ^b   Weller, Michael ^a   Eisele, Günter ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

a disintegrin and metalloproteinase (ADAM); glioblastoma; immunotherapy; NK cell; NKG2D; stem cell

Indexed keywords

A DISINTEGRIN AND METALLOPROTEINASE (ADAM); GLIOBLASTOMA; IMMUNOTHERAPY; NK CELL; NKG2D; STEM CELL;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; DIPEPTIDES; GLIOBLASTOMA; GPI-LINKED PROTEINS; HUMANS; HYDROXAMIC ACIDS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEOPLASTIC STEM CELLS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA;

EID: 84894271474     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/not232     Document Type: Article

References (37)

1. Johnson DR,MaDJ, Buckner JC,Hammack JE. Conditional probability of long-term survival in glioblastoma: A population-based analysis. Cancer. 2012;118(22):5608-5613.
2. Mitchell DA, Sampson JH. Toward effective immunotherapy for the treatment of malignant brain tumors. Neurotherapeutics. 2009;6(3): 527-538.
3. Ogbomo H, Cinatl J Jr., Mody CH, Forsyth PA. Immunotherapy in gliomas: limitations and potential of natural killer (NK) cell therapy. Trends Mol Med. 2011;17(8):433-441.
4. Friese MA, Steinle A, Weller M. The innate immune response in the central nervous system and its role in glioma immune surveillance. Onkologie. 2004;27(5):487-491.
5. Pegram HJ, Andrews DM, Smyth MJ, Darcy PK, Kershaw MH. Activating and inhibitory receptors of natural killer cells. Immunol Cell Biol. 2011; 89(2):216-224.
6. Fernandez-Messina L, Reyburn HT, Vales-Gomez M. Human NKG2D-ligands: cell biology strategies to ensure immune recognition. Front Immunol. 2012;3:299.
7. Friese MA, Platten M, Lutz SZ, et al. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res. 2003; 63(24):8996-9006.
8. Eisele G, Wischhusen J, Mittelbronn M, et al. TGF-beta and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain. 2006;129(Pt 9): 2416-2425.
9. Duffy MJ, Mullooly M, O'Donovan N, et al. The ADAMs family of proteases: new biomarkers and therapeutic targets for cancer? Clin Proteomics. 2011;8(1):9.
10. Zheng X, Jiang F, Katakowski M, Lu Y, Chopp M. ADAM17 promotes glioma cell malignant phenotype. Mol Carcinog. 2012;51(2):150-164.
11. Kohutek ZA, diPierro CG, Redpath GT, Hussaini IM. ADAM-10-mediated N-cadherin cleavage is protein kinase C-alpha dependent and promotes glioblastoma cell migration. J Neurosci. 2009;29(14): 4605-4615.
12. Bulstrode H, Jones LM, Siney EJ, et al. A-Disintegrin and Metalloprotease (ADAM) 10 and 17 promote self-renewal of brain tumor sphere forming cells. Cancer Lett. 2012;326(1):79-87.
13. Chitadze G, Lettau M, Bhat J, et al. Shedding of endogenous MHC class I-related chain moleculesAandBfromdifferenthumantumorentities: Heterogeneous involvement of the "a disintegrin and metalloproteases" 10 and 17. Int J Cancer. 2013;133(7):1557-1566.
14. Waldhauer I, Goehlsdorf D, Gieseke F, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68(15):6368-6376.
15. Singh SK, Clarke ID, Hide T, Dirks PB.Cancer stemcells in nervous system tumors. Oncogene. 2004;23(43):7267-7273.
16. Tabatabai G, Weller M. Glioblastoma stem cells. Cell Tissue Res. 2011; 343(3):459-465.
17. Park DM, Rich JN. Biology of glioma cancer stem cells. Mol Cells. 2009; 28(1):7-12.
18. Castriconi R, Daga A, DonderoA, et al.NK cells recognize and killhuman glioblastoma cells with stem cell-like properties. J Immunol. 2009; 182(6):3530-3539.
19. Di Tomaso T, Mazzoleni S, Wang E, et al. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin Cancer Res. 2010;16(3):800-813.
20. Wei J, Barr J, Kong LY, et al. Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal trans-ducers and activators of transcription 3 pathway. Mol Cancer Ther. 2010; 9(1):67-78.
21. Wei J, Barr J, Kong LY, et al. Glioma-associated cancer-initiating cells induce immunosuppression. Clin Cancer Res. 2010;16(2):461-473.
22. Wolpert F, Roth P, Lamszus K, Tabatabai G, Weller M, Eisele G. HLA-E contributes to an immune-inhibitory phenotype of glioblastoma stem-like cells. J Neuroimmunol. 2012;250(1-2):27-34.
23. Gunther HS, Schmidt NO, Phillips HS, et al. Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene. 2008;27(20):2897-2909.
24. Robertson MJ, Cochran KJ, Cameron C, Le JM, Tantravahi R, Ritz J. Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia. Exp Hematol. 1996;24(3):406-415.
25. Ludwig A, Hundhausen C, Lambert MH, et al. Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb Chem High Throughput Screen. 2005;8(2):161-171.
26. UhlM, AulwurmS,Wischhusen J, et al. SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res. 2004;64(21): 7954-7961.
27. Welte SA, Sinzger C, Lutz SZ, et al. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur J Immunol. 2003;33(1):194-203.
28. Schreiner B, Voss J, Wischhusen J, et al. Expression of toll-like receptors by human muscle cells in vitro and in vivo: TLR3 is highly expressed in inflammatory and HIV myopathies, mediates IL-8 release and up-regulation of NKG2D-ligands. FASEB J. 2005;20(1):118-120.
29. Lee-MacAry AE, Ross EL, Davies D, et al. Development of a novel flow cytometric cell-mediated cytotoxicity assay using the fluorophores PKH-26 and TO-PRO-3 iodide. J Immunol Methods. 2001;252(1-2): 83-92.
30. Raulet DH, Gasser S, Gowen BG, DengW, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 2013;31: 413-441.
31. Waldhauer I, Steinle A. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res. 2006;66(5):2520-2526.
32. Boutet P, Aguera-Gonzalez S, Atkinson S, et al. Cutting edge: the metalloproteinase ADAM17/TNF-alpha-converting enzyme regulates proteolytic shedding of the MHC class I-related chain B protein. J Immunol. 2009;182(1):49-53.
33. Lu Y, Jiang F, Zheng X, et al. TGF-beta1 promotes motility and invasiveness of glioma cells through activation of ADAM17. Oncol Rep. 2011;25(5):1329-1335.
34. Ray A, Dhar S, Ray BK. Transforming growth factor-beta1-mediated activation of NF-kappaB contributes to enhanced ADAM-12 expression in mammary carcinoma cells. Mol Cancer Res. 2010;8(9):1261-1270.
35. Ashiru O, Boutet P, Fernandez-Messina L, et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res. 2010; 70(2):481-489.
36. Kaiser BK, Yim D, Chow IT, et al. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature. 2007; 447(7143):482-486.
37. Hundhausen C, Misztela D, Berkhout TA, et al. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood. 2003;102(4):1186-1195.