A short half-life of ULBP1 at the cell surface due to internalization and proteosomal degradation

Immunology and Cell Biology

Volumn 94, Issue 5, 2016, Pages 479-485

  Fernández Messina, Lola ^a,b   Reyburn, Hugh T ^a   Valés Gómez, Mar ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CD8 ANTIGEN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEASOME; PROTEIN; ULBP1 PROTEIN; ULBP2 PROTEIN; ULBP3 PROTEIN; UNCLASSIFIED DRUG; GLYCOSYLPHOSPHATIDYLINOSITOL; PROTEASOME INHIBITOR; SIGNAL PEPTIDE;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CELL DESTRUCTION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME MECHANISM; EXOSOME; HALF LIFE TIME; HUMAN; IMMUNE RESPONSE; NONHUMAN; PHOTOCHEMICAL INTERNALIZATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TRANSPORT; SURFACE PROPERTY; ANIMAL; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ENDOCYTOSIS; HAMSTER; LYSOSOME; METABOLISM;

ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; ENDOCYTOSIS; GLYCOSYLPHOSPHATIDYLINOSITOLS; HALF-LIFE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN STABILITY; PROTEOLYSIS;

EID: 84956907393     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2016.2     Document Type: Article

References (46)

1. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999; 285: 727-729
2. Radaev S, Rostro B, Brooks AG, Colonna M, Sun PD. Conformational plasticity revealed by the cocrystal structure of NKG2D and its class I MHC-like ligand ULBP3. Immunity 2001; 15: 1039-1049
3. Bahram S, Bresnahan M, Geraghty DE, Spies T. A second lineage of mammalian major histocompatibility complex class I genes. Proc Natl Acad Sci USA 1994; 91: 6259-6263
4. Chalupny NJ, Sutherland CL, Lawrence WA, Rein-Weston A, Cosman D. ULBP4 is a novel ligand for human NKG2D. Biochem Biophys Res Commun 2003; 305: 129-135
5. Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001; 14: 123-133
6. Eagle RA, Traherne JA, Hair JR, Jafferji I, Trowsdale J. ULBP6/RAET1L is an additional human NKG2D ligand. Eur J Immunol 2009; 39: 3207-3216
7. Das H, Groh V, Kuijl C, Sugita M, Morita CT, Spies T, et al. MICA engagement by human Vgamma2Vdelta2 T cells enhances their antigen-dependent effector function. Immunity 2001; 15: 83-93
8. Kuylenstierna C, Bjorkstrom NK, Andersson SK, Sahlstrom P, Bosnjak L, Paquin-Proulx D, et al. NKG2D performs two functions in invariant NKT cells: direct TCR-independent activation of NK-like cytolysis and co-stimulation of activation by CD1d. Eur J Immunol 2011; 41: 1913-1923
9. Boissel N, Rea D, Tieng V, Dulphy N, Brun M, Cayuela JM, et al. BCR/ABL oncogene directly controls MHC class I chain-related molecule A expression in chronic myelogenous leukemia. J Immunol 2006; 176: 5108-5116
10. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA 1996; 93: 12445-12450
11. Nedvetzki S, Sowinski S, Eagle RA, Harris J, Vely F, Pende D, et al. Reciprocal regulation of human natural killer cells and macrophages associated with distinct immune synapses. Blood 2007; 109: 3776-3785
12. Borchers MT, Harris NL, Wesselkamper SC, Vitucci M, Cosman D. NKG2D ligands are expressed on stressed human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2006; 291: L222-L231
13. Cerwenka A. New twist on the regulation of NKG2D ligand expression. J Exp Med 2009; 206: 265-268
14. Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 2013; 31: 413-441
15. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005; 436: 1186-1190
16. Vales-Gomez M, Chisholm SE, Cassady-Cain RL, Roda-Navarro P, Reyburn HT. Selective induction of expression of a ligand for the NKG2D receptor by proteasome inhibitors. Cancer Res 2008; 68: 1546-1554
17. Butler JE, Moore MB, Presnell SR, Chan HW, Chalupny NJ, Lutz CT. Proteasome regulation of ULBP1 transcription. J Immunol 2009; 182: 6600-6609
18. Stern-Ginossar N, Gur C, Biton M, Horwitz E, Elboim M, Stanietsky N, et al. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat Immunol 2008; 9: 1065-1073
19. Tang KF, Ren H, Cao J, Zeng GL, Xie J, Chen M, et al. Decreased Dicer expression elicits DNA damage and up-regulation of MICA and MICB. J Cell Biol 2008; 182: 233-239
20. Esteso G, Luzon E, Sarmiento E, Gomez-Caro R, Steinle A, Murphy G, et al. Altered microRNA expression after infection with human cytomegalovirus leads to TIMP3 downregulation and increased shedding of metalloprotease substrates, including MICA. J Immunol 2014; 193: 1344-1352
21. Waldhauer I, Steinle A. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res 2006; 66: 2520-2526
22. 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
23. 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: 8543-8551
24. 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 MICA008 that is shed by tumor cells in exosomes. Cancer Res 2010; 70: 481-489
25. Fernandez-Messina L, Reyburn HT, Vales-Gomez M. Human NKG2D-ligands: cell biology strategies to ensure immune recognition. Front Immunol 2012; 3: 299
26. Chitadze G, Bhat J, Lettau M, Janssen O, Kabelitz D. Generation of soluble NKG2D ligands: proteolytic cleavage, exosome secretion and functional implications. Scand J Immunol 2013; 78: 120-129
27. Aguera-Gonzalez S, Boutet P, Reyburn HT, Vales-Gomez M. Brief residence at the plasma membrane of the MHC class I-related chain B is due to clathrin-mediated cholesterol-dependent endocytosis and shedding. J Immunol 2009; 182: 4800-4808
28. Uhlenbrock F, Hagemann-Jensen M, Kehlet S, Andresen L, Pastorekova S, Skov S. The NKG2D ligand ULBP2 is specifically regulated through an invariant chain-dependent endosomal pathway. J Immunol 2014; 193: 1654-1665
29. Eagle RA, Trowsdale J. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 2007; 7: 737-744
30. Klausner RD, Donaldson JG, Lippincott-Schwartz J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 1992; 116: 1071-1080
31. Schneider CL, Hudson AW. The human herpesvirus-7 (HHV-7) U21 immunoevasin subverts NK-mediated cytoxicity through modulation of MICA and MICB. PLoS Pathogens 2011; 7: e1002362
32. Chatterjee S, Mayor S. The GPI-Anchor and protein sorting. Cell Mol Life Sci 2001; 58: 1969-1987
33. Mayor S, Riezman H. Sorting GPI-Anchored proteins. Nat Rev Mol Cell Biol 2004; 5: 110-120
34. Fujita M, Yoko OT, Jigami Y. Inositol deacylation by Bst1p is required for the quality control of glycosylphosphatidylinositol-Anchored proteins. Mol Biol Cell 2006; 17: 834-850
35. Field MC, Moran P, Li W, Keller GA, Caras IW. Retention and degradation of proteins containing an uncleaved glycosylphosphatidylinositol signal. J Biol Chem 1994; 269: 10830-10837
36. Nice TJ, Coscoy L, Raulet DH. Posttranslational regulation of the NKG2D ligand Mult1 in response to cell stress. J Exp Med 2009; 206: 287-298
37. Everett RD. The regulation of transcription of viral and cellular genes by herpesvirus immediate-early gene products (review). Anticancer Res 1987; 7: 589-604
38. Ashiru O, Lopez-Cobo S, Fernandez-Messina L, Pontes-Quero S, Pandolfi R, Reyburn HT, et al. A GPI anchor explains the unique biological features of the common NKG2D-ligand allele MICA008. Biochem J 2013; 454: 295-302
39. 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
40. Campbell TM, McSharry BP, Steain M, Slobedman B, Abendroth A. Varicella-Zoster virus and herpes simplex virus 1 differentially modulate NKG2D ligand expression during productive infection. J Virol 2015; 89: 7932-7943
41. Almond JB, Cohen GM. The proteasome: a novel target for cancer chemotherapy. Leukemia 2002; 16: 433-443
42. 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: 321-327
43. Apps R, Gardner L, Traherne J, Male V, Moffett A. Natural-killer cell ligands at the maternal-fetal interface: UL-16 binding proteins, MHC class-I chain related molecules, HLA-F and CD48. Hum Reprod 2008; 23: 2535-2548
44. Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 1986; 47: 333-348
45. Vales-Gomez M, Reyburn HT. Intracellular trafficking of the HCMV immunoevasin UL16 depends on elements present in both its cytoplasmic and transmembrane domains. J Mol Biol 2006; 363: 908-917
46. Vales-Gomez M, Winterhalter A, Roda-Navarro P, Zimmermann A, Boyle L, Hengel H, et al. The human cytomegalovirus glycoprotein UL16 traffics through the plasma membrane and the nuclear envelope. Cell Microbiol 2006; 8: 581-590