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Brief Report

Platelet-mediated shedding of NKG2D ligands impairs NK cell immune-surveillance of tumor cells

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Article: e1364827 | Received 08 Feb 2017, Accepted 03 Aug 2017, Published online: 27 Nov 2017

References

  • Gasser S, Raulet DH. Activation and self-tolerance of natural killer cells. Immunol Rev. 2006;214:130-42. doi:10.1111/j.1600-065X.2006.00460.x. PMID:17100881
  • Caligiuri MA. Human natural killer cells. Blood. 2008;112:461-9. doi:10.1182/blood-2007-09-077438. PMID:18650461
  • Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell. 2010;142:847-56. doi:10.1016/j.cell.2010.08.031. PMID:20850008
  • Ullrich E, Koch J, Cerwenka A, Steinle A. New prospects on the NKG2D/NKG2DL system for oncology. Oncoimmunology. 2013;2:e26097. doi:10.4161/onci.26097. PMID:24353908
  • 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. doi:10.1073/pnas.201238598. PMID:11562472
  • Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature. 2001;413:165-71. doi:10.1038/35093109. PMID:11557981
  • Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol. 2002;169:4098-102. doi:10.4049/jimmunol.169.8.4098. PMID:12370336
  • 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. doi:10.1038/nature01112. PMID:12384702
  • Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 2013;31:413-41. doi:10.1146/annurev-immunol-032712-095951. PMID:23298206
  • Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, Stevanovic S, Rammensee HG, Steinle A. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68:6368-76. doi:10.1158/0008-5472.CAN-07-6768. PMID:18676862
  • Boutet P, Aguera-Gonzalez S, Atkinson S, Pennington CJ, Edwards DR, Murphy G, Reyburn HT, Vales-Gomez M. 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. doi:10.4049/jimmunol.182.1.49. PMID:19109134
  • Chitadze G, Lettau M, Bhat J, Wesch D, Steinle A, Furst D, Mytilineos J, Kalthoff H, Janssen O, Oberg HH, 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. 2013;133:1557-66. doi:10.1002/ijc.28174. PMID:23526433
  • Wolpert F, Tritschler I, Steinle A, Weller M, Eisele G. A disintegrin and metalloproteinases 10 and 17 modulate the immunogenicity of glioblastoma-initiating cells. Neuro Oncol. 2014;16:382-91. doi:10.1093/neuonc/not232. PMID:24327582
  • Blobel CP. ADAMs: key components in EGFR signalling and development. Nat Rev Mol Cell Biol. 2005;6:32-43. doi:10.1038/nrm1548. PMID:15688065
  • Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer. 2011;11:123-34. doi:10.1038/nrc3004. PMID:21258396
  • Labelle M, Begum S, Hynes RO. Direct signaling between platelets and cancer cells induces an epithelial-mesenchymal-like transition and promotes metastasis. Cancer Cell. 2011;20:576-90. doi:10.1016/j.ccr.2011.09.009. PMID:22094253
  • Placke T, Kopp HG, Salih HR. Modulation of natural killer cell anti-tumor reactivity by platelets. J Innate Immun. 2011;3:374-82. doi:10.1159/000323936. PMID:21411974
  • Gasic GJ, Gasic TB, Stewart CC. Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci U S A 1968;61:46-52. doi:10.1073/pnas.61.1.46. PMID:5246932
  • Camerer E, Qazi AA, Duong DN, Cornelissen I, Advincula R, Coughlin SR. Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood. 2004;104:397-401. doi:10.1182/blood-2004-02-0434. PMID:15031212
  • Nieswandt B, Hafner M, Echtenacher B, Mannel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 1999;59:1295-300. PMID:10096562
  • Kopp HG, Placke T, Salih HR. Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res. 2009;69:7775-83. doi:10.1158/0008-5472.CAN-09-2123. PMID:19738039
  • Placke T, Orgel M, Schaller M, Jung G, Rammensee HG, Kopp HG, Salih HR. Platelet-derived MHC class I confers a pseudonormal phenotype to cancer cells that subverts the antitumor reactivity of natural killer immune cells. Cancer Res. 2012;72:440-8. doi:10.1158/0008-5472.CAN-11-1872. PMID:22127925
  • Placke T, Salih HR, Kopp HG. GITR ligand provided by thrombopoietic cells inhibits NK cell antitumor activity. J Immunol. 2012;189:154-60. doi:10.4049/jimmunol.1103194. PMID:22649191
  • Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene. 2008;27:5944-58. doi:10.1038/onc.2008.272. PMID:18836475
  • Huergo-Zapico L, Acebes-Huerta A, Lopez-Soto A, Villa-Alvarez M, Gonzalez-Rodriguez AP, Gonzalez S. Molecular Bases for the Regulation of NKG2D Ligands in Cancer. Front Immunol. 2014;5:106. doi:10.3389/fimmu.2014.00106. PMID:24711808
  • Jung H, Hsiung B, Pestal K, Procyk E, Raulet DH. RAE-1 ligands for the NKG2D receptor are regulated by E2F transcription factors, which control cell cycle entry. J Exp Med. 2012;209:2409-22. doi:10.1084/jem.20120565. PMID:23166357
  • Henn V, Slupsky JR, Grafe M, Anagnostopoulos I, Forster R, Muller-Berghaus G, Kroczek RA. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 1998;391:591-4. doi:10.1038/35393. PMID:9468137
  • Colciaghi F, Marcello E, Borroni B, Zimmermann M, Caltagirone C, Cattabeni F, Padovani A, Di Luca M. Platelet APP, ADAM 10 and BACE alterations in the early stages of Alzheimer disease. Neurology. 2004;62:498-501. doi:10.1212/01.WNL.0000106953.49802.9C. PMID:14872043
  • Bergmeier W, Piffath CL, Cheng G, Dole VS, Zhang Y, von Andrian UH, Wagner DD. Tumor necrosis factor-alpha-converting enzyme (ADAM17) mediates GPIbalpha shedding from platelets in vitro and in vivo. Circ Res. 2004;95:677-83. doi:10.1161/01.RES.0000143899.73453.11. PMID:15345652
  • Fong KP, Barry C, Tran AN, Traxler EA, Wannemacher KM, Tang HY, Speicher KD, Blair IA, Speicher DW, Grosser T, et al. Deciphering the human platelet sheddome. Blood. 2011;117:e15−26. doi:10.1182/blood-2010-05-283838. PMID:20962327
  • Colciaghi F, Borroni B, Pastorino L, Marcello E, Zimmermann M, Cattabeni F, Padovani A, Di Luca M. [alpha]-Secretase ADAM10 as well as [alpha]APPs is reduced in platelets and CSF of Alzheimer disease patients. Mol Med. 2002;8:67-74. PMID: 12080182. PMID:12080182
  • 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. doi:10.1016/j.ejcb.2010.11.005. PMID:21194787
  • Wiesner T, Bugl S, Mayer F, Hartmann JT, Kopp HG. Differential changes in platelet VEGF, Tsp, CXCL12, and CXCL4 in patients with metastatic cancer. Clin Exp Metastasis. 2010;27:141-9. doi:10.1007/s10585-010-9311-6. PMID:20182908
  • Lin RJ, Afshar-Kharghan V, Schafer AI. Paraneoplastic thrombocytosis: the secrets of tumor self-promotion. Blood. 2014;124:184-7. doi:10.1182/blood-2014-03-562538. PMID:24868077
  • Meyer T, Amaya M, Desai H, Robles-Carrillo L, Hatfield M, Francis JL, Amirkhosravi A. Human platelets contain and release TWEAK. Platelets. 2010;21:571-4. doi:10.3109/09537104.2010.512403. PMID:20849210
  • Koerner SP, Andre MC, Leibold JS, Kousis PC, Kubler A, Pal M, Haen SP, Buhring HJ, Grosse-Hovest L, Jung G, et al. An Fc-optimized CD133 antibody for induction of NK cell reactivity against myeloid leukemia. Leukemia. 2017;31:459-69. doi:10.1038/leu.2016.194. PMID:27435001
  • Eisele G, Wischhusen J, Mittelbronn M, Meyermann R, Waldhauer I, Steinle A, Weller M, Friese MA. TGF-beta and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain. 2006;129:2416-25. doi:10.1093/brain/awl205. PMID:16891318
  • Weyrich AS, Zimmerman GA. Platelets: signaling cells in the immune continuum. Trends Immunol. 2004;25:489-95. doi:10.1016/j.it.2004.07.003. PMID:15324742
  • Deng W, Gowen BG, Zhang L, Wang L, Lau S, Iannello A, Xu J, Rovis TL, Xiong N, Raulet DH. Antitumor immunity. A shed NKG2D ligand that promotes natural killer cell activation and tumor rejection. Science. 2015;348:136-9. doi:10.1126/science.1258867
  • Hilpert J, Grosse-Hovest L, Grunebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol. 2012;189:1360-71. doi:10.4049/jimmunol.1200796. PMID:22730533
  • Salih HR, Goehlsdorf D, Steinle A. Release of MICB molecules by tumor cells: mechanism and soluble MICB in sera of cancer patients. Hum Immunol. 2006;67:188-95. doi:10.1016/j.humimm.2006.02.008. PMID:16698441
  • Salih HR, Antropius H, Gieseke F, Lutz SZ, Kanz L, Rammensee HG, Steinle A. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood. 2003;102:1389-96. doi:10.1182/blood-2003-01-0019. PMID:12714493
  • Raab S, Steinbacher J, Schmiedel BJ, Kousis PC, Steinle A, Jung G, Grosse-Hovest L, Salih HR. Fc-optimized NKG2D-Fc constructs induce NK cell antibody-dependent cellular cytotoxicity against breast cancer cells independently of HER2/neu expression status. J Immunol. 2014;193:4261-72. doi:10.4049/jimmunol.1400872. PMID:25217158

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