Metalloprotease-mediated tumor cell shedding of B7-H6, the ligand of the natural killer cell-activating receptor NKp30

Cancer Research

Volumn 74, Issue 13, 2014, Pages 3429-3440

  Schlecker, Eva ^a   Fiegler, Nathalie ^a   Arnold, Annette ^a   Altevogt, Peter ^b   Rose John, Stefan ^c   Moldenhauer, Gerhard ^b   Sucker, Antje ^d   Paschen, Annette ^d   Von Strandmann, Elke Pogge ^e   Textor, Sonja ^a   Cerwenka, Adelheid ^a  

^a Innate Immunity ^*  (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e University of Cologne   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; ADAM10 ENDOPEPTIDASE; ADAM17 PROTEIN; B7 H6 PROTEIN; BATIMASTAT; MEMBRANE PROTEIN; MESSENGER RNA; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; UNCLASSIFIED DRUG;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; DEGRANULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MELANOMA; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; TUMOR CELL; TUMOR ESCAPE; UPREGULATION;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; B7 ANTIGENS; CELL LINE, TUMOR; DIPEPTIDES; HCT116 CELLS; HELA CELLS; HUMANS; HYDROXAMIC ACIDS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MCF-7 CELLS; MELANOMA; MEMBRANE PROTEINS; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; PHENYLALANINE; PROTEASE INHIBITORS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; THIOPHENES; TUMOR ESCAPE; UP-REGULATION;

EID: 84903954045     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3017     Document Type: Article

References (55)

1. Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol 2001;1:41-9.
2. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity. The example of natural killer cells. Science 2011;331:44-9.
3. Gasser S, Raulet DH. Activation and self-tolerance of natural killer cells. Immunol Rev 2006;214:130-42.
4. Raulet DH, Guerra N. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 2009;9:568-80.
5. Soriani A, Zingoni A, Cerboni C, Iannitto ML, Ricciardi MR, Di Gialleonardo V, et al. 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 2009;113:3503-11.
6. Textor S, Durst M, Jansen L, Accardi R, Tommasino M, Trunk MJ, et al. Activating NK cell receptor ligands are differentially expressed during progression to cervical cancer. Int J Cancer 2008;123:2343-53.
7. Pende D, Parolini S, Pessino A, Sivori S, Augugliaro R, Morelli L, et al. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J Exp Med 1999;190:1505-16.
8. Byrd A, Hoffmann SC, Jarahian M, Momburg F, Watzl C. Expression analysis of the ligands for the Natural Killer cell receptors NKp30 and NKp44. PLoS ONE 2007;2:e1339.
9. Brandt CS, BaratinM, Yi EC, Kennedy J, Gao Z, Fox B, et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med 2009;206; 1495-503.
10. Li Y, Wang Q, Mariuzza RA. Structure of the human activating natural cytotoxicity receptor NKp30 bound to its tumor cell ligand B7-H6. J Exp Med 208:703-14.
11. Kaifu T, Escaliere B, Gastinel LN, Vivier E, Baratin M. B7-H6/NKp30 interaction: a mechanism of alerting NK cells against tumors. Cell Mol Life Sci 2011;68:3531-9.
12. Matta J, Baratin M, Chiche L, Forel JM, Cognet C, Thomas G, et al. Induction of B7-H6, a ligand for the natural killer cell activating receptor NKp30, in inflammatory conditions. Blood;122:394-404.
13. Salih HR, Holdenrieder S, Steinle A. Soluble NKG2D ligands: prevalence, release, and functional impact. Front Biosci 2008;13:3448-56.
14. Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev 2010;235:267-85.
15. Ashiru O, Boutet P, Fernandez-Messina L, Aguera-Gonzalez S, Skepper JN, Vales-Gomez M, 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;70:481-9.
16. Fernandez-Messina L, Ashiru O, Boutet P, Aguera-Gonzalez S, Skepper JN, Reyburn HT, et al. Differential mechanisms of shedding of the glycosylphosphatidylinositol (GPI)-anchored NKG2D ligands. J Biol Chem 2010;285:8543-51.
17. Kaiser BK, Yim D, Chow IT, Gonzalez S, Dai Z, Mann HH, et al. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 2007;447:482-6.
18. Liu G, Atteridge CL,WangX, Lundgren AD,WuJD. The membrane type matrix metalloproteinase MMP14 mediates constitutive shedding of MHCclass I chain-related molecule A independent of A disintegrin and metalloproteinases. J Immunol 2010;184:3346-50.
19. Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 2002;169: 4098-102.
20. 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.
21. Waldhauer I, Steinle A. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res 2006;66:2520-6.
22. Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002;419: 734-8.
23. Hilpert J, Grosse-Hovest L, Grunebach F, Buechele C, Nuebling T, Raum T, et al. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol 189:1360-71.
24. Wu JD, Higgins LM, Steinle A, Cosman D, Haugk K, Plymate SR. Prevalent expression of the immunostimulatory MHC class I chainrelated molecule is counteracted by shedding in prostate cancer. J Clin Invest 2004;114:560-8.
25. Holdenrieder S, Stieber P, Peterfi A, Nagel D, Steinle A, Salih HR. Soluble MICB in malignant diseases: analysis of diagnostic significance and correlation with soluble MICA. Cancer Immunol Immunother 2006;55:1584-9.
26. Holdenrieder S, Stieber P, Peterfi A, Nagel D, Steinle A, Salih HR. Soluble MICA in malignant diseases. Int J Cancer 2006;118:684-7.
27. 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.
28. Tessarz AS, Weiler S, Zanzinger K, Angelisova P, Horejsi V, Cerwenka A. Non-T cell activation linker (NTAL) negatively regulates TREM-1/ DAP12-induced inflammatory cytokine production in myeloid cells. J Immunol 2007;178:1991-9.
29. Jarahian M, Watzl C, Fournier P, Arnold A, Djandji D, Zahedi S, et al. Activation of natural killer cells by newcastle disease virus hemagglutinin- neuraminidase. J Virol 2009;83:8108-21.
30. Textor S, Fiegler N, Arnold A, Porgador A, Hofmann TG, Cerwenka A. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res 2011;71:5998-6009.
31. Duffy MJ, McKiernan E, O'Donovan N, McGowan PM. Role of ADAMs in cancer formation and progression. Clin Cancer Res 2009;15: 1140-4.
32. Zanzinger K, Schellack C, Nausch N, Cerwenka A. Regulation of triggering receptor expressed on myeloid cells 1 expression on mouse inflammatory monocytes. Immunology 2009;128:185-95.
33. Raffaghello L, Prigione I, Airoldi I, Camoriano M, Levreri I, Gambini C, et al. Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 2004;6:558-68.
34. Giavazzi R, Garofalo A, Ferri C, Lucchini V, Bone EA, Chiari S, et al. Batimastat, a synthetic inhibitor of matrix metalloproteinases, potentiates the antitumor activity of cisplatin in ovarian carcinoma xenografts. Clin Cancer Res 1998;4:985-92.
35. Fiegler N, Textor S, Arnold A, Rolle A, Oehme I, Breuhahn K, et al. Downregulation of the activating NKp30 ligand B7-H6 by HDAC inhibitors impairs tumor cell recognition by NK cells. Blood 2013;122: 684-93.
36. Boutet P, Aguera-Gonzalez S, Atkinson S, Pennington CJ, Edwards DR, Murphy G, 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: 49-53.
37. Stoeck A, Keller S, Riedle S, Sanderson MP, Runz S, Le Naour F, et al.A role for exosomes in the constitutive and stimulus-induced ectodomain cleavage of L1 and CD44, Biochem J 2006;393:609-18.
38. Sanderson MP, Erickson SN, Gough PJ, Garton KJ, Wille PT, Raines EW, et al. ADAM10 mediates ectodomain shedding of the b-cellulin precursor activated by p-aminophenylmercuric acetate and extracellular calcium influx. J Biol Chem 2005;280:1826-37.
39. Hooper NM, Karran EH, Turner AJ. Membrane protein secretases. Biochem J 1997;321(Pt 2):265-79.
40. Blobel CP. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol 2005;6:32-43.
41. Wu J, Lanier LL. Natural killer cells and cancer. Adv Cancer Res 2003;90:127-56.
42. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, et al. Transforming growth factor b1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci U S A 2003;100: 4120-5.
43. Moretta L, Bottino C, Pende D, Castriconi R, Mingari MC, Moretta A. Surface NK receptors and their ligands on tumor cells. Semin Immunol 2006;18:151-8.
44. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A, 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.
45. Reiners KS, Topolar D, Henke A, Simhadri VR, Kessler J, Sauer M, et al. Soluble ligands for NK cell receptors promote evasion of chronic lymphocytic leukemia cells from NK cell anti-tumor activity. Blood 2013;121:3658-65.
46. Cesaro A, Abakar-Mahamat A, Brest P, Lassalle S, Selva E, Filippi J, et al. Differential expression and regulation of ADAM17 and TIMP3 in acute inflamed intestinal epithelia. Am J Physiol Gastrointest Liver Physiol 2009;296:G1332-43.
47. Horiuchi K, Kimura T, Miyamoto T, Takaishi H, Okada Y, Toyama Y, et al. Cutting edge: TNF-a-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J Immunol 2007;179:2686-9.
48. Ohta S, Harigai M, Tanaka M, Kawaguchi Y, Sugiura T, Takagi K, et al. Tumor necrosis factor-alpha (TNF-alpha) converting enzyme contributes to production of TNF-a in synovial tissues from patients with rheumatoid arthritis. J Rheumatol 2001;28:1756-63.
49. Wu E, Croucher PI, McKie N. Expression of members of the novel membrane linked metalloproteinase family ADAM in cells derived from a range of haematological malignancies. Biochem Biophys Res Commun 1997;235:437-42.
50. Ding X, Yang LY, Huang GW, Wang W, Lu WQ. ADAM17 mRNA expression and pathological features of hepatocellular carcinoma. World J Gastroenterol 2004;10:2735-9.
51. Lendeckel U, Kohl J, Arndt M, Carl-McGrath S, Donat H, Rocken C. Increased expression ofADAMfamilymembers inhuman breast cancer and breast cancer cell lines. J Cancer Res Clin Oncol 2005;131:41-8.
52. Ohtsuka T, Shiomi T, Shimoda M, Kodama T,Amour A, Murphy G, et al. ADAM28 is overexpressed in human non-small cell lung carcinomas and correlates with cell proliferation and lymph node metastasis. Int J Cancer 2006;118:263-73.
53. McGowan PM, McKiernan E, Bolster F, Ryan BM, Hill AD, McDermott EW, et al. ADAM-17 predicts adverse outcome in patients with breast cancer. Ann Oncol 2008;19:1075-81.
54. Lee SB, Schramme A, Doberstein K, Dummer R, Abdel-Bakky MS, Keller S, et al. ADAM10 is upregulated in melanoma metastasis compared with primary melanoma. J Invest Dermatol 2010;130: 763-73.
55. Saftig P, Reiss K. The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17: novel drug targets with therapeutic potential. Eur J Cell Biol 2011;90:527-35.