Genotoxic stress induces senescence-associated ADAM10-dependent release of NKG2D MIC ligands in multiple myeloma cells

Journal of Immunology

Volumn 195, Issue 2, 2015, Pages 736-748

  Zingoni, Alessandra ^a   Cecere, Francesca ^a   Vulpis, Elisabetta ^a   Fionda, Cinzia ^a   Molfetta, Rosa ^a   Soriani, Alessandra ^a   Petrucci, Maria Teresa ^b   Ricciardi, Maria Rosaria ^b   Fuerst, Daniel ^c,d   Amendola, Maria Giulia ^a   Mytilineos, Joannis ^c,d   Cerboni, Cristina ^a   Paolini, Rossella ^a   Cippitelli, Marco ^a   Santoni, Angela ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c German Red Cross Blood Transfusion Service Baden Württemberg Hessen and University Hospital Ulm   (Germany)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM10 ENDOPEPTIDASE; CD38 ANTIGEN; DOXORUBICIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MARIMASTAT; MELPHALAN; MHC CLASS I RELATED CHAIN A; NATURAL KILLER CELL RECEPTOR NKG2D; REACTIVE OXYGEN METABOLITE; SYNDECAN 1; UNCLASSIFIED DRUG; ADAM PROTEIN; ADAM10 PROTEIN, HUMAN; CD38 PROTEIN, HUMAN; CYTOTOXIN; HLA ANTIGEN CLASS 1; KLRK1 PROTEIN, HUMAN; MATRIX METALLOPROTEINASE INHIBITOR; MEMBRANE PROTEIN; MHC CLASS I-RELATED CHAIN A; MICB ANTIGEN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K; SDC1 PROTEIN, HUMAN; SECRETASE;

ARTICLE; CELL STRESS; CELL SURFACE; CONTROLLED STUDY; DEGRANULATION; DRUG SENSITIVITY; GENOTOXIC STRESS; HUMAN; HUMAN CELL; HUMAN TISSUE; MULTIPLE MYELOMA; MULTIPLE MYELOMA CELL LINE; NATURAL KILLER CELL; PLASMA CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; SENESCENCE; UPREGULATION; BONE MARROW CELL; CELL AGING; DNA DAMAGE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; PATHOLOGY; PRIMARY CELL CULTURE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANTIGENS, CD38; BONE MARROW CELLS; CELL AGING; CELL LINE, TUMOR; CYTOTOXINS; DNA DAMAGE; DOXORUBICIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; MATRIX METALLOPROTEINASE INHIBITORS; MELPHALAN; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MULTIPLE MYELOMA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PLASMA CELLS; PRIMARY CELL CULTURE; PROTEOLYSIS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SYNDECAN-1;

EID: 84936791354     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402643     Document Type: Article

References (60)

1. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
2. Dai, Z., C. J. Turtle, G. C. Booth, S. R. Riddell, T. A. Gooley, A. M. Stevens, T. Spies, and V. Groh. 2009. Normally occurring NKG2D+CD4+ T cells are immunosuppressive and inversely correlated with disease activity in juvenile-onset lupus. J. Exp. Med. 206: 793-805.
3. Bryceson, Y. T., and H. G. Ljunggren. 2008. Tumor cell recognition by the NK cell activating receptor NKG2D. Eur. J. Immunol. 38: 2957-2961.
4. Guerra, N., Y. X. Tan, N. T. Joncker, A. Choy, F. Gallardo, N. Xiong, S. Knoblaugh, D. Cado, N. M. Greenberg, and D. H. Raulet. 2008. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28: 571-580.
5. Raulet, D. H., S. Gasser, B. G. Gowen, W. Deng, and H. Jung. 2013. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 31: 413-441.
6. Champsaur, M., and L. L. Lanier. 2010. Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235: 267-285.
7. Cerboni, C., M. Ardolino, A. Santoni, and A. Zingoni. 2009. Detuning CD8+ T lymphocytes by down-regulation of the activating receptor NKG2D: role of NKG2D ligands released by activated T cells. Blood 113: 2955-2964.
8. Mincheva-Nilsson, L., O. Nagaeva, T. Chen, U. Stendahl, J. Antsiferova, I. Mogren, J. Hernestål, and V. Baranov. 2006. Placenta-derived soluble MHC class I chain-related molecules down-regulate NKG2D receptor on peripheral blood mononuclear cells during human pregnancy: A possible novel immune escape mechanism for fetal survival. J. Immunol. 176: 3585-3592.
9. Salih, H. R., H. G. Rammensee, and A. Steinle. 2002. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J. Immunol. 169: 4098-4102.
10. Salih, H. R., H. Antropius, F. Gieseke, S. Z. Lutz, L. Kanz, H. G. Rammensee, and A. Steinle. 2003. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 102: 1389-1396.
11. Groh, V., J. Wu, C. Yee, and T. Spies. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738.
12. Doubrovina, E. S., M. M. Doubrovin, E. Vider, R. B. Sisson, R. J. O'Reilly, B. Dupont, and Y. M. Vyas. 2003. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J. Immunol. 171: 6891-6899.
13. Chitadze, G., J. Bhat, M. Lettau, O. Janssen, and D. Kabelitz. 2013. Generation of soluble NKG2D ligands: proteolytic cleavage, exosome secretion and functional implications. Scand. J. Immunol. 78: 120-129.
14. Ashiru, O., P. Boutet, L. Fernández-Messina, S. Agüera-González, J. N. Skepper, M. Valés-Gómez, and H. T. Reyburn. 2010. 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. 70: 481-489.
15. Mahindra, A., T. Hideshima, and K. C. Anderson. 2010. Multiple myeloma: biology of the disease. Blood Rev. 24(Suppl. 1): S5-S11.
16. Godfrey, J., and D. M. Benson, Jr. 2012. The role of natural killer cells in immunity against multiple myeloma. Leuk. Lymphoma 53: 1666-1676.
17. Carbone, E., P. Neri, M. Mesuraca, M. T. Fulciniti, T. Otsuki, D. Pende, V. Groh, T. Spies, G. Pollio, D. Cosman, et al. 2005. HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells. Blood 105: 251-258.
18. El-Sherbiny, Y. M., J. L. Meade, T. D. Holmes, D. McGonagle, S. L. Mackie, A. W. Morgan, G. Cook, S. Feyler, S. J. Richards, F. E. Davies, et al. 2007. The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res. 67: 8444-8449.
19. Lu, X., A. Zhu, X. Cai, Z. Jia, W. Han, L. Ma, M. Zhou, K. Qian, L. Cen, and B. Chen. 2012. Role of NKG2D in cytokine-induced killer cells against multiple myeloma cells. Cancer Biol. Ther. 13: 623-629.
20. Rebmann, V., P. Schütt, D. Brandhorst, B. Opalka, T. Moritz, M. R. Nowrousian, and H. Grosse-Wilde. 2007. Soluble MICA as an independent prognostic factor for the overall survival and progression-free survival of multiple myeloma patients. Clin. Immunol. 123: 114-120.
21. Jinushi, M., M. Vanneman, N. C. Munshi, Y. T. Tai, R. H. Prabhala, J. Ritz, D. Neuberg, K. C. Anderson, D. R. Carrasco, and G. Dranoff. 2008. MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proc. Natl. Acad. Sci. USA 105: 1285-1290.
22. Soriani, A., A. Zingoni, C. Cerboni, M. L. Iannitto, M. R. Ricciardi, V. Di Gialleonardo, M. Cippitelli, C. Fionda, M. T. Petrucci, A. Guarini, et al. 2009. ATM-ATR-dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 113: 3503-3511.
23. Fionda, C., A. Soriani, G. Malgarini, M. L. Iannitto, A. Santoni, and M. Cippitelli. 2009. Heat shock protein-90 inhibitors increase MHC class I-related chain A and B ligand expression on multiple myeloma cells and their ability to trigger NK cell degranulation. J. Immunol. 183: 4385-4394.
24. Fionda, C., G. Malgarini, A. Soriani, A. Zingoni, F. Cecere, M. L. Iannitto, M. R. Ricciardi, V. Federico, M. T. Petrucci, A. Santoni, and M. Cippitelli. 2013. Inhibition of glycogen synthase kinase-3 increases NKG2D ligand MICA expression and sensitivity to NK cell-mediated cytotoxicity in multiple myeloma cells: role of STAT3. J. Immunol. 190: 6662-6672.
25. Wu, X., Y. Tao, J. Hou, X. Meng, and J. Shi. 2012. Valproic acid upregulates NKG2D ligand expression through an ERK-dependent mechanism and potentially enhances NK cell-mediated lysis of myeloma. Neoplasia 14: 1178-1189.
26. Soriani, A., M. L. Iannitto, B. Ricci, C. Fionda, G. Malgarini, S. Morrone, G. Peruzzi, M. R. Ricciardi, M. T. Petrucci, M. Cippitelli, and A. Santoni. 2014. Reactive oxygen species-and DNA damage response-dependent NK cell activating ligand upregulation occurs at transcriptional levels and requires the transcriptional factor E2F1. J. Immunol. 193: 950-960.
27. Molfetta, R., L. Quatrini, C. Capuano, F. Gasparrini, B. Zitti, A. Zingoni, R. Galandrini, A. Santoni, and R. Paolini. 2014. c-Cbl regulates MICA-but not ULBP2-induced NKG2D down-modulation in human NK cells. Eur. J. Immunol. 44: 2761-2770.
28. Zingoni, A., G. Palmieri, S. Morrone, M. Carretero, M. Lopez-Botel, M. Piccoli, L. Frati, and A. Santoni. 2000. CD69-triggered ERK activation and functions are negatively regulated by CD94/NKG2-A inhibitory receptor. Eur. J. Immunol. 30: 644-651.
29. Cerboni, C., A. Zingoni, M. Cippitelli, M. Piccoli, L. Frati, and A. Santoni. 2007. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK-cell lysis. Blood 110: 606-615.
30. Fürst, D., G. Solgi, K. Recker, D. Mytilineos, H. Schrezenmeier, and J. Mytilineos. 2011. Sequence-based typing of major histocompatibility complex class I chain-related gene A alleles by use of exons 2-5 information. Tissue Antigens 77: 201-205.
31. Ashiru, O., S. López-Cobo, L. Fernández-Messina, S. Pontes-Quero, R. Pandolfi, H. T. Reyburn, and M. Valés-Gómez. 2013. A GPI anchor explains the unique biological features of the common NKG2D-ligand allele MICA∗008. Biochem. J. 454: 295-302.
32. Boutet, P., S. Agüera-González, S. Atkinson, C. J. Pennington, D. R. Edwards, G. Murphy, H. T. Reyburn, and M. Valés-Gómez. 2009. Cutting edge: the metalloproteinase ADAM17/TNF-alpha-converting enzyme regulates proteo-lytic shedding of the MHC class I-related chain B protein. J. Immunol. 182: 49-53.
33. Chitadze, G., M. Lettau, J. Bhat, D. Wesch, A. Steinle, D. Fürst, J. Mytilineos, H. Kalthoff, O. Janssen, H. H. Oberg, and D. Kabelitz. 2013. Shedding of endogenous MHC class I-related chain molecules A and B from different human tumor entities: heterogeneous involvement of the "a disintegrin and metal-loproteases" 10 and 17. Int. J. Cancer 133: 1557-1566.
34. Waldhauer, I., D. Goehlsdorf, F. Gieseke, T. Weinschenk, M. Wittenbrink, A. Ludwig, S. Stevanovic, H. G. Rammensee, and A. Steinle. 2008. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 68: 6368-6376.
35. Ramani, V. C., A. Purushothaman, M. D. Stewart, C. A. Thompson, I. Vlodavsky, J. L. Au, and R. D. Sanderson. 2013. The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J. 280: 2294-2306.
36. Hoettecke, N., A. Ludwig, S. Foro, and B. Schmidt. 2010. Improved synthesis of ADAM10 inhibitor GI254023X. Neurodegener. Dis. 7: 232-238.
37. Rodier, F., and J. Campisi. 2011. Four faces of cellular senescence. J. Cell Biol. 192: 547-556.
38. Wu, J. D., L. M. Higgins, A. Steinle, D. Cosman, K. Haugk, and S. R. Plymate. 2004. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J. Clin. Invest. 114: 560-568.
39. Holdenrieder, S., P. Stieber, A. Peterfi, D. Nagel, A. Steinle, and H. R. Salih. 2006. Soluble MICB in malignant diseases: analysis of diagnostic significance and correlation with soluble MICA. Cancer Immunol. Immunother. 55: 1584-1589.
40. Holdenrieder, S., P. Stieber, A. Peterfi, D. Nagel, A. Steinle, and H. R. Salih. 2006. Soluble MICA in malignant diseases. Int. J. Cancer 118: 684-687.
41. Baragaño Raneros, A., B. Suarez-Alvarez, and C. López-Larrea. 2014. Secretory pathways generating immunosuppressive NKG2D ligands: New targets for therapeutic intervention. OncoImmunology 3: e28497.
42. Arreygue-Garcia, N. A., A. Daneri-Navarro, A. del Toro-Arreola, A. Cid-Arregui, O. Gonzalez-Ramella, L. F. Jave-Suarez, A. Aguilar-Lemarroy, R. Troyo-Sanroman, A. Bravo-Cuellar, V. Delgado-Rizo, et al. 2008. Augmented serum level of major histocompatibility complex class I-related chain A (MICA) protein and reduced NKG2D expression on NK and T cells in patients with cervical cancer and precursor lesions. BMC Cancer 8: 16.
43. Chaimowitz, N. S., D. J. Kang, L. M. Dean, and D. H. Conrad. 2012. ADAM10 regulates transcription factor expression required for plasma cell function. PLoS ONE 7: e42694.
44. Bret, C., D. Hose, T. Reme, A. Kassambara, A. Seckinger, T. Meissner, J. F. Schved, T. Kanouni, H. Goldschmidt, and B. Klein. 2011. Gene expression profile of ADAMs and ADAMTSs metalloproteinases in normal and malignant plasma cells and in the bone marrow environment. Exp. Hematol. 39: 546-557.e8.
45. Armanious, H., P. Gelebart, M. Anand, A. Belch, and R. Lai. 2011. Constitutive activation of metalloproteinase ADAM10 in mantle cell lymphoma promotes cell growth and activates the TNFa/NFkB pathway. Blood 117: 6237-6246.
46. Zocchi, M. R., S. Catellani, P. Canevali, S. Tavella, A. Garuti, B. Villaggio, A. Zunino, M. Gobbi, G. Fraternali-Orcioni, A. Kunkl, et al. 2012. High ERp5/ADAM10 expression in lymph node microenvironment and impaired NKG2D ligands recognition in Hodgkin lymphomas. Blood 119: 1479-1489.
47. Lizama, C., D. Rojas-Benitez, M. Antonelli, A. Ludwig, and R. D. Moreno. 2012. Involvement of TACE/ADAM17 and ADAM10 in etoposide-induced ap-optosis of germ cells in rat spermatogenesis. J. Cell. Physiol. 227: 829-838.
48. Kohga, K., T. Takehara, T. Tatsumi, T. Miyagi, H. Ishida, K. Ohkawa, T. Kanto, N. Hiramatsu, and N. Hayashi. 2009. Anticancer chemotherapy inhibits MHC class I-related chain a ectodomain shedding by downregulating ADAM10 expression in hepatocellular carcinoma. Cancer Res. 69: 8050-8057.
49. Fischer, O. M., S. Hart, A. Gschwind, N. Prenzel, and A. Ullrich. 2004. Oxi-dative and osmotic stress signaling in tumor cells is mediated by ADAM proteases and heparin-binding epidermal growth factor. Mol. Cell. Biol. 24: 5172-5183.
50. Vahdat, A. M., K. S. Reiners, V. L. Simhadri, D. A. Eichenauer, B. Böll, A. Chalaris, V. R. Simhadri, K. Wiegmann, H. W. Krell, S. Rose-John, et al. 2010. TNF-alpha-converting enzyme (TACE/ADAM17)-dependent loss of CD30 induced by proteasome inhibition through reactive oxygen species. Leukemia 24: 51-57.
51. Kyula, J. N., S. Van Schaeybroeck, J. Doherty, C. S. Fenning, D. B. Longley, and P. G. Johnston. 2010. Chemotherapy-induced activation of ADAM-17: A novel mechanism of drug resistance in colorectal cancer. Clin. Cancer Res. 16: 3378-3389.
52. Garbers, C., F. Kuck, S. Aparicio-Siegmund, K. Konzak, M. Kessenbrock, A. Sommerfeld, D. Häussinger, P. A. Lang, D. Brenner, T. W. Mak, et al. 2013. Cellular senescence or EGFR signaling induces Interleukin 6 (IL-6) receptor expression controlled by mammalian target of rapamycin (mTOR). Cell Cycle 12: 3421-3432.
53. Coppé, J. P., P. Y. Desprez, A. Krtolica, and J. Campisi. 2010. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 5: 99-118.
54. Kuilman, T., and D. S. Peeper. 2009. Senescence-messaging secretome: SMS-ing cellular stress. Nat. Rev. Cancer 9: 81-94.
55. Armeanu, S., M. Bitzer, U. M. Lauer, S. Venturelli, A. Pathil, M. Krusch, S. Kaiser, J. Jobst, I. Smirnow, A. Wagner, et al. 2005. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res. 65: 6321-6329.
56. Huang, B., R. Sikorski, P. Sampath, and S. H. Thorne. 2011. Modulation of NKG2D-ligand cell surface expression enhances immune cell therapy of cancer. J. Immunother. 34: 289-296.
57. Fridman, J. S., E. Caulder, M. Hansbury, X. Liu, G. Yang, Q. Wang, Y. Lo, B. B. Zhou, M. Pan, S. M. Thomas, et al. 2007. Selective inhibition of ADAM metalloproteases as a novel approach for modulating ErbB pathways in cancer. Clin. Cancer Res. 13: 1892-1902.
58. Zhou, B. B., M. Peyton, B. He, C. Liu, L. Girard, E. Caudler, Y. Lo, F. Baribaud, I. Mikami, N. Reguart, et al. 2006. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell 10: 39-50.
59. Duffy, M. J., M. Mullooly, N. O'Donovan, S. Sukor, J. Crown, A. Pierce, and P. M. McGowan. 2011. The ADAMs family of proteases: new biomarkers and therapeutic targets for cancer? Clin. Proteomics 8: 9.
60. Ramani, V. C., and R. D. Sanderson. 2014. Chemotherapy stimulates syndecan-1 shedding: A potentially negative effect of treatment that may promote tumor relapse. Matrix Biol. 35: 215-222.