Proteasome regulation of ULBP1 transcription

Journal of Immunology

Volumn 182, Issue 10, 2009, Pages 6600-6609

  Butler, James E ^a   Moore, Mikel B ^a,d   Presnell, Steven R ^a   Chan, Huei Wei ^a   Jan Chalupny, N ^c   Lutz, Charles T ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c AMGEN INC   (United States)

^d CARGILL INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; ATM PROTEIN; ATR PROTEIN; BLEOMYCIN; BORTEZOMIB; CAFFEINE; CELL SURFACE PROTEIN; CISPLATIN; HYDROXYUREA; MESSENGER RNA; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN ULBP 1; RNA; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CANCER CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; GAMMA RADIATION; GENE CONTROL; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; IONIZING RADIATION; KERATINOCYTE; LOW DRUG DOSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEINASE INHIBITION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TRANSCRIPTION REGULATION; ULTRAVIOLET RADIATION; UPREGULATION;

ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CARCINOMA, SQUAMOUS CELL; CELL CYCLE PROTEINS; CELL LINE, TUMOR; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; HEAD AND NECK NEOPLASMS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 77950636009     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0801214     Document Type: Article

References (77)

1. Long, E. O., and S. Rajagopalan. 2002. Stress signals activate natural killer cells. J. Exp. Med. 196: 1399-1402. (Pubitemid 35424934)
2. Raulet, D. H. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3: 781-790.
3. Gleimer, M., and P. Parham. 2003. Stress management: MHC class I and class I-like molecules as reporters of cellular stress. Immunity 19: 469-477. (Pubitemid 37311429)
4. Upshaw, J. L., and P. J. Leibson. 2006. NKG2D-mediated activation of cytotoxic lymphocytes: unique signaling pathways and distinct functional outcomes. Semin. Immunol. 18: 167-175.
5. Guerra, N., Y. X. Tan, N. T. Joncker, A. Choy, F. Gallardo, N. Xiong, S. Knoblaugh, D. Cado, N. R. Greenberg, and D. H. Raulet. 2008. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28: 571-580.
6. Eagle, R. A., and J. Trowsdale. 2007. Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7: 737-744.
7. Mistry, A. R., and C. A. O'Callaghan. 2007. Regulation of ligands for the activating receptor NKG2D. Immunology 121: 439-447.
8. Schrambach, S., M. Ardizzone, V. Leymarie, J. Sibilia, and S. Bahram. 2007. In vivo expression pattern of MICA and MICB and its relevance to auto-immunity and cancer. PLoS ONE 2: e518.
9. McFarland, B. J., T. Kortemme, S. F. Yu, D. Baker, and R. K. Strong. 2003. Symmetry recognizing asymmetry: analysis of the interactions between the C-type lectin-like immunoreceptor NKG2D and MHC class I-like ligands. Structure 11: 411-422.
10. Eagle, R. A., J. A. Traherne, O. Ashiru, M. R. Wills, and J. Trowsdale. 2006. Regulation of NKG2D ligand gene expression. Hum. Immunol. 67: 159-169. (Pubitemid 43673921)
11. Kriegeskorte, A. K., F. E. Gebhardt, S. Porcellini, M. Schiemann, C. Stemberger, T. J. Franz, K. M. Huster, L. N. Carayannopoulos, W. M. Yokoyama, M. Colonna, et al. 2005. NKG2D-independent suppression of T cell proliferation by H60 and MICA. Proc. Natl. Acad. Sci. USA 102: 11805-11810.
12. Cerwenka, A., J. L. Baron, and L. L. Lanier. 2001. 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. USA 98: 11521-11526. (Pubitemid 32928761)
13. Diefenbach, A., E. R. Jensen, A. M. Jamieson, and D. H. Raulet. 2001. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413: 165-171. (Pubitemid 32867877)
14. Friese, M. A., M. Platten, S. Z. Lutz, U. Naumann, S. Aulwurm, F. Bischof, H. J. Buhring, J. Dichgans, H. G. Rammensee, A. Steinle, and M. Weller. 2003. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res. 63: 8996-9006. (Pubitemid 38064081)
15. Smyth, M. J., J. Swann, J. M. Kelly, E. Cretney, W. M. Yokoyama, A. Diefenbach, T. J. Sayers, and Y. Hayakawa. 2004. NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J. Exp. Med. 200: 1325-1335.
16. 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. (Pubitemid 35177960)
17. 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.
18. Lee, J.-C., K.-M. Lee, D.-W. Kim, and D. S. Heo. 2004. Elevated TGF-β1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J. Immunol. 172: 7335-7340.
19. Oppenheim, D. E., S. J. Roberts, S. L. Clarke, R. Filler, J. M. Lewis, R. E. Tigelaar, M. Girardi, and A. C. Hayday. 2005. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat. Immunol. 6: 928-937.
20. Vetter, C. S., W. Lieb, E.-B. Brocker, and J. C. Becker. 2004. Loss of nonclassical MHC molecules MIC-A/B expression during progression of uveal melanoma. Br. J. Cancer 91: 1495-1499.
21. Madjd, Z., I. Spendlove, R. Moss, S. Bevin, S. E. Pinder, N. F. S. Watson, I. Ellis, and L. G. Durrant. 2007. Upregulation of MICA on high-grade invasive operable breast carcinoma. Cancer Immun. 7: 17. (Pubitemid 350021808)
22. Pende, D., C. Cantoni, P. Rivera, M. Vitale, R. Castriconi, S. Marcenaro, M. Nanni, R. Biassoni, C. Bottino, A. Moretta, and L. Moretta. 2001. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur. J. Immunol. 31: 1076-1086.
23. Vetter, C. S., V. Groh, P. T. Straten, T. Spies, E.-B. Bröcker, and J. C. Becker. 2002. Expression of stress-induced MHC class I related chain molecules on human melanoma. J. Invest. Dermatol. 118: 600-605.
24. Pende, D., P. Rivera, S. Marcenaro, C. C. Chang, R. Biassoni, R. Conte, M. Kubin, D. Cosman, S. Ferrone, L. Moretta, and A. Moretta. 2002. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res. 62: 6178-6186. (Pubitemid 35244469)
25. Maccalli, C., D. Pende, C. Castelli, M. C. Mingari, P. F. Robbins, and G. Parmiani. 2003. NKG2D engagement of colorectal cancer-specific T cells strengthens TCR-mediated antigen stimulation and elicits TCR independent antitumor activity. Eur. J. Immunol. 33: 2033-2043. (Pubitemid 37120876)
26. - antitumor T cells. Cancer Res. 64: 2175-2182.
27. Wrobel, P., H. Shojaei, B. Schittek, F. Gieseler, B. Wollenberg, H. Kalthoff, D. Kabelitz, and D. Wesch. 2007. Lysis of a broad range of epithelial tumour cells by human γδ T cells: involvement of NKG2D ligands and T-cell receptorversus NKG2D-dependent recognition. Scand. J. Immunol. 66: 320-328. (Pubitemid 47063194)
28. Gustin, D. M. 2004. Chemoprevention of head and neck cancer. Semin. Oncol. 31: 769-777.
29. Liu, C.-J., M.-T. Lui, H.-L. Chen, S.-C. Lin, and K.-W. Chang. 2007. MICA and MICB overexpression in oral squamous cell carcinoma. J. Oral Pathol. Med. 36: 43-47. (Pubitemid 44973987)
30. Reinders, J., E. H. Rozemuller, P. van der Weide, A. Oka, P. J. Slootweg, H. Inoko, and M. G. J. Tilanus. 2007. Genes in the HLA region indicative for head and neck squamous cell carcinoma. Mol. Immunol. 44: 848-855. (Pubitemid 44415008)
31. Li, D., B. Ronson, M. Guo, S. Liu, J. S. Bishop, D. A. Van Echo, and B. W. O'Malley, Jr. 2002. Interleukin 2 gene transfer prevents NKG2D suppression and enhances antitumor efficacy in combination with cisplatin for head and neck squamous cell cancer. Cancer Res. 62: 4023-4028. (Pubitemid 34791069)
32. Cosman, D., J. Müllberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14: 123-133. (Pubitemid 32206515)
33. Chalupny, N. J., C. L. Sutherland, W. A. Lawrence, A. Rein Weston, and D. Cosman. 2003. ULBP4 is a novel ligand for human NKG2D. Biochem. Biophys. Res. Commun. 305: 129-135.
34. Darzynkiewicz, Z., and X. Huang. 2004. Analysis of cellular DNA content by flow cytometry. In Current Protocols in Immunology. J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, and W. Strober, eds. Wiley, New York pp. 5.7.1-5.7.18.
35. Chan, H. W., J. S. Miller, M. B. Moore, and C. T. Lutz. 2005. Epigenetic control of highly homologous killer Ig-like receptor gene alleles. J. Immunol. 175: 5966-5974.
36. Bacon, L., R. A. Eagle, M. Meyer, N. Easom, N. T. Young, and J. Trowsdale. 2004. Two human ULBP/RAET1 molecules with transmembrane regions are ligands for NKG2D. J. Immunol. 173: 1078-1084. (Pubitemid 38924282)
37. Presnell, S. R., L. Zhang, C. A. Ramilo, H.-W. Chan, and C. T. Lutz. 2006. Functional redundancy of transcription factor-binding sites in the killer cell Iglike receptor (KIR) gene promoter. Int. Immunol. 18: 1221-1232.
38. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254.
39. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Lab. Press, Cold Spring Harbor, NY.
40. Forastiere, A. A., H. Goepfert, M. Maor, T. F. Pajak, R. Weber, W. Morrison, B. Glisson, A. Trotti, J. A. Ridge, C. Chao, et al. 2003. Concurrent chemotherapy and radiotherapy for organ preservation in advanced laryngeal cancer. N. Engl. J. Med. 349: 2091-2098. (Pubitemid 37464533)
41. Adema, A. D., J. Cloos, R. H. Verheijen, B. J. Braakhuis, and P. E. Bryant. 2003. Comparison of bleomycin and radiation in the G2 assay of chromatid breaks. Int. J. Radiat. Biol. 79: 655-661.
42. Myung, J., K. B. Kim, and C. M. Crews. 2001. The ubiquitin-proteasome pathway and proteasome inhibitors. Med. Res. Rev. 21: 245-273.
43. Armeanu, S., M. Krusch, K. M. Baltz, T. S. Weiss, I. Smirnow, A. Steinle, U. M. Lauer, M. Bitzer, and H. R. Salih. 2008. Direct and natural killer cell-mediated antitumor effects of low-dose bortezomib in hepatocellular carcinoma. Clin. Cancer Res. 14: 3520-3528.
44. Valés-Gómez, M., S. E. Chisholm, R. L. Cassady-Cain, P. Roda-Navarro, and H. T. Reyburn. 2008. Selective induction of expression of a ligand for the NKG2D receptor by proteasome inhibitors. Cancer Res. 68: 1546-1554. (Pubitemid 351346864)
45. Bruno, M. E. C., and C. S. Kaetzel. 2005. Long-term exposure of the HT-29 human intestinal epithelial cell line to TNF causes sustained up-regulation of the polymeric Ig receptor and proinflammatory genes through transcriptional and posttranscriptional mechanisms. J. Immunol. 174: 7278-7284.
46. López-Soto, A., A. Quinones-Lombrana, R. López- Arbesú, C. López-Larrea, and S. González. 2006. Transcriptional regulation of ULBP1, a human ligand of the NKG2D receptor. J. Biol. Chem. 281: 30419-30430. (Pubitemid 44582098)
47. Gasser, S., S. Orsulic, E. J. Brown, and D. H. Raulet. 2005. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436: 1186-1190. (Pubitemid 41232299)
48. 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 NKcell lysis. Blood 110: 606-615. (Pubitemid 47105399)
49. Sarkaria, J. N., R. S. Tibbetts, E. C. Busby, A. P. Kennedy, D. E. Hill, and R. T. Abraham. 1998. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res. 58: 4375-4382.
50. Kurz, E. U., and S. P. Lees-Miller. 2004. DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst.) 3: 889-900.
51. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506.
52. Criswell, T., K. Leskov, S. Miyamoto, G. Luo, and D. A. Boothman. 2003. Transcription factors activated in mammalian cells after clinically relevant doses of ionizing radiation. Oncogene 22: 5813-5827. (Pubitemid 37176702)
53. Tibbetts, R. S., K. M. Brumbaugh, J. M. Williams, J. N. Sarkaria, W. A. Cliby, S.-Y. Shieh, Y. Taya, C. Prives, and R. T. Abraham. 1999. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13: 152-157. (Pubitemid 29061945)
54. Bolt, J., Q. N. Vo, W.-J. Kim, A. J. McWhorter, J. Thomson, M. E. Hagensee, P. Friedlander, K. D. Brown, and J. Gilbert. 2005. The ATM/p53 pathway is commonly targeted for inactivation in squamous cell carcinoma of the head and neck (SCCHN) by multiple molecular mechanisms. Oral Oncol. 41: 1013-1020. (Pubitemid 41434067)
55. McGowan, C. H., and P. Russell. 2004. The DNA damage response: sensing and signaling. Curr. Opin. Cell Biol. 16: 629-633. (Pubitemid 39463112)
56. Friese, M. A., J. Wischhusen, W. Wick, M. Weiler, G. Eisele, A. Steinle, and M. Weller. 2004. RNA interference targeting transforming growth factor-β enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Res. 64: 7596-7603.
57. Borchers, M. T., N. L. Harris, S. C. Wesselkamper, M. Vitucci, and D. Cosman. 2006. NKG2D ligands are expressed on stressed human airway epithelial cells. Am. J. Physiol. 291: L222-L231.
58. Groh, V., R. Rhinehart, H. Secrist, S. Bauer, K. H. Grabstein, and T. Spies. 1999. Broad tumor-associated expression and recognition by tumor-derived γδ T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96: 6879-6884. (Pubitemid 29274978)
59. Groh, V., A. Steinle, S. Bauer, and T. Spies. 1998. Recognition of stress-induced MHC molecules by intestinal epithelial γδ T cells. Science 279: 1737-1740. (Pubitemid 28164472)
60. Nowbakht, P., M.-C. S. Ionescu, A. Rohner, C. P. Kalberer, E. Rossy, L. Mori, D. Cosman, G. De Libero, and A. Wodnar-Filipowicz. 2005. Ligands for natural killer cell-activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias. Blood 105: 3615-3622. (Pubitemid 40628208)
61. Laroia, G., R. Cuesta, G. Brewer, and R. J. Schneider. 1999. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284: 499-502. (Pubitemid 29289625)
62. Nice, T. J., L. Coscoy, and D. H. Raulet. 2009. Posttranslational regulation of the NKG2D ligand Mult1 in response to cell stress. J. Exp. Med. 206: 287-298.
63. Unni, A. M., T. Bondar, and R. Medzhitov. 2008. Intrinsic sensor of oncogenic transformation induces a signal for innate immunosurveillance. Proc. Natl. Acad. Sci. USA 105: 1686-1691.
64. Yamamoto, K., Y. Fujiyama, A. Andoh, T. Bamba, and H. Okabe. 2001. Oxidative stress increases MICA and MICB gene expression in the human colon carcinoma cell line (CaCo-2). Biochim. Biophys. Acta 1526: 10-12. (Pubitemid 32245765)
65. Pappworth, I. Y., E. C. Wang, and M. Rowe. 2007. The switch from latent to productive infection in Epstein-Barr virus-infected B cells is associated with sensitization to NK cell killing. J. Virol. 81: 474-482.
66. Vankayalapati, R., A. Garg, A. Porgador, D. E. Griffith, P. Klucar, H. Safi, W. M. Girard, D. Cosman, T. Spies, and P. F. Barnes. 2005. Role of NK cell-activating receptors and their ligands in the lysis of mononuclear phagocytes infected with an intracellular bacterium. J. Immunol. 175: 4611-4617. (Pubitemid 41362000)
67. Sirén, J., T. Sareneva, J. Pirhonen, M. Strengell, V. Veckman, I. Julkunen, and S. Matikainen. 2004. Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J. Gen. Virol. 85: 2357-2364. (Pubitemid 39162608)
68. Lodoen, M., K. Ogasawara, J. A. Hamerman, H. Arase, J. P. Houchins, E. S. Mocarski, and L. L. Lanier. 2003. NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J. Exp. Med. 197: 1245-1253. (Pubitemid 36617771)
69. Hamerman, J. A., K. Ogasawara, and L. L. Lanier. 2004. Cutting edge: Toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. J. Immunol. 172: 2001-2005.
70. Hideshima, T., C. Mitsiades, M. Akiyama, T. Hayashi, D. Chauhan, P. Richardson, R. Schlossman, K. Podar, N. C. Munshi, N. Mitsiades, and K. C. Anderson. 2003. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 101: 1530-1534. (Pubitemid 36182530)
71. Molinero, L. L., M. B. Fuertes, M. V. Girart, L. Fainboim, G. A. Rabinovich, M. A. Costas, and N. W. Zwirner. 2004. NF-κB regulates expression of the MHC class I-related chain A gene in activated T lymphocytes. J. Immunol. 173: 5583-5590.
72. Perkins, N. D. 2007. Integrating cell-signalling pathways with NF-κB and IKK function. Nat. Rev. Mol. Cell Biol. 8: 49-62.
73. Venkataraman, G. M., D. Suciu, V. Groh, J. M. Boss, and T. Spies. 2007. Promoter region architecture and transcriptional regulation of the genes for the MHC class I-related chain A and B ligands of NKG2D. J. Immunol. 178: 961-969.
74. Li, M., Y. Wang, M.-C. Hung, and P. Kannan. 2006. Inefficient proteasomaldegradation pathway stabilizes AP-2α and activates HER-2/neu gene in breast cancer. Int. J. Cancer 118: 802-811. (Pubitemid 43157655)
75. Mathew, A., S. K. Mathur, and R. I. Morimoto. 1998. Heat shock response and protein degradation: regulation of HSF2 by the ubiquitin-proteasome pathway. Mol. Cell. Biol. 18: 5091-5098. (Pubitemid 28388092)
76. Murray-Zmijewski, F., D. P. Lane, and J.-C. Bourdon. 2006. p53/p63/p73 isoforms: an orchestra of isoforms to harmonise cell differentiation and response to stress. Cell Death Differ. 13: 962-972. (Pubitemid 43753487)
77. DeYoung, M. P., C. M. Johannessen, C.-O. Leong, W. Faquin, J. W. Rocco, and L. W. Ellisen. 2006. Tumor-specific p73 up-regulation mediates p63 dependence in squamous cell carcinoma. Cancer Res. 66: 9362-9368. (Pubitemid 44623630)