Inducible but not constitutive expression of PD-L1 in human melanoma cells is dependent on activation of NF-κB

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Gowrishankar, Kavitha ^a   Gunatilake, Dilini ^a   Gallagher, Stuart J ^a   Tiffen, Jessamy ^a   Rizos, Helen ^b   Hersey, Peter ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b MACQUARIE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 AMINOETHYLAMINO) 1,8 DIMETHYLIMIDAZO[1,2 A]QUINOXALINE; 7 (3,5 DIMETHYL 4 ISOXAZOLYL) 1,3 DIHYDRO 8 METHOXY 1 [1 (2 PYRIDINYL)ETHYL] 2H IMIDAZO[4,5 C]QUINOLIN 2 ONE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN C JUN; RAF PROTEIN; SMALL INTERFERING RNA; STAT3 PROTEIN; TRANSCRIPTION FACTOR AP 1; VEMURAFENIB; 4(2'-AMINOETHYL)AMINO-1,8-DIMETHYLIMIDAZO(1,2-A)QUINOXALINE; CD274 PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; QUINOXALINE DERIVATIVE; SULFONAMIDE;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG RESPONSE; FLOW CYTOMETRY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MELANOMA CELL LINE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; MELANOMA; METABOLISM; TIME FACTOR; TUMOR CELL LINE;

ANTIGENS, CD274; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMIDAZOLES; INDOLES; INTERFERON-GAMMA; MELANOMA; NF-KAPPA B; QUINOXALINES; SULFONAMIDES; TIME FACTORS;

EID: 84927539299     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123410     Document Type: Article

References (43)

1. Topalian SL SM, Brahmer JR. Nivolumab(Anti-PD1) inpatients with advanced solid tumors.: Survival and long term safety in a phase 1 trial. J Clin Oncol 31, 2013(suppl:; abstr3002). 2013.
2. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013; 369(2):134-44. doi: 10.1056/NEJMoa1305133 PMID: 23724846.
3. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus Ipilimumab in Advanced Melanoma. The New England journal of medicine. 2013; 2:2.
4. Kamphorst AO, Ahmed R. Manipulating the PD-1 pathway to improve immunity. Curr Opin Immunol. 2013; 25(3):381-8. Epub 2013/04/16. doi: 10.1016/j.coi.2013.03.003 PMID: 23582509.
5. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nature medicine. 2002; 8(8):793- 800. Epub 2002/07/02. PMID: 12091876.
6. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annual review of immunology. 2008; 26:677-704. Epub 2008/01/05. doi: 10.1146/annurev.immunol.26.021607. 090331 PMID: 18173375.
7. Hamid O, Carvajal RD. Anti-programmed death-1 and anti-programmed death-ligand 1 antibodies in cancer therapy. Expert opinion on biological therapy. 2013; 13(6):847-61. doi: 10.1517/14712598. 2013.770836 PMID: 23421934.
8. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012; 366(26):2443-54. Epub 2012/06/05. doi: 10.1056/NEJMoa1200690 PMID: 22658127.
9. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2014; 32 (10):1020-30. Epub 2014/03/05.
10. Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nature medicine. 2007; 13(1):84-8. PMID: 17159987.
11. Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci U S A. 2008; 105(52):20852-7. Epub 2008/12/18. doi: 10.1073/pnas.0810958105 PMID: 19088198.
12. Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, et al. Activation of the PD- 1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer discovery. 2013; 3 (12):1355-63. doi: 10.1158/2159-8290.CD-13-0310 PMID: 24078774.
13. Lee SJ, Jang BC, Lee SW, Yang YI, Suh SI, Park YM, et al. Interferon regulatory factor-1 is prerequisite to the constitutive expression and IFN-gamma-induced upregulation of B7-H1 (CD274). FEBS letters. 2006; 580(3):755-62. PMID: 16413538.
14. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012; 4(127):127-37. Epub 2012/03/31. doi: 10.1126/scitranslmed.3003689 PMID: 22461641.
15. Taube JM, Klein AP, Brahmer JR, Xu H, Pan X, Kim JH, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res. 2014. Epub 2014/04/10.
16. Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT, et al. Up-regulation of PD-L1, IDO, and T (regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Science translational medicine. 2013; 5(200):200-116. Epub 2013/08/30. doi: 10.1126/scitranslmed.3006504 PMID: 23986400.
17. Jiang X, Zhou J, Giobbie-Hurder A, Wargo J, Hodi FS. The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clinical cancer research: An official journal of the American Association for Cancer Research. 2013; 19 (3):598-609. doi: 10.1158/1078-0432.CCR-12-2731 PMID: 23095323.
18. Mijatov BSK, Jin L, gallagher S, Hersey P. Cytokines and the NF-kB pathwayin resistance of melanoma to BRAF inhibitors. Pigment cell and Melanoma research. 2012; 25(6):875-. Epub November 2012.
19. Lee SK, Seo SH, Kim BS, Kim CD, Lee JH, Kang JS, et al. IFN-gamma regulates the expression of B7- H1 in dermal fibroblast cells. J Dermatol Sci. 2005; 40(2):95-103. PMID: 16085391.
20. Hayden MS, Ghosh S. NF-kappaB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012; 26(3):203-34. Epub 2012/02/04. doi: 10.1101/gad.183434.111 PMID: 22302935.
21. DiDonato JA, Mercurio F, Karin M. NF-kappaB and the link between inflammation and cancer. Immunological reviews. 2012; 246(1):379-400. doi: 10.1111/j.1600-065X.2012.01099.x PMID: 22435567.
22. Ueda Y, Richmond A. NF-kappaB activation in melanoma. Pigment Cell Res. 2006; 19(2):112-24. PMID: 16524427.
23. Smale ST. Dimer-specific regulatory mechanisms within the NF-kappaB family of transcription factors. Immunological reviews. 2012; 246(1):193-204. doi: 10.1111/j.1600-065X.2011.01091.x PMID: 22435556.
24. Perkins ND. The diverse and complex roles of NF-kappaB subunits in cancer. Nature reviews Cancer. 2012; 12(2):121-32. doi: 10.1038/nrc3204 PMID: 22257950.
25. Burke JR, Pattoli MA, Gregor KR, Brassil PJ, MacMaster JF, McIntyre KW, et al. BMS-345541 is a highly selective inhibitor of I kappa B kinase that binds at an allosteric site of the enzyme and blocks NFkappa B-dependent transcription in mice. The Journal of biological chemistry. 2003; 278(3):1450-6. PMID: 12403772.
26. Gallagher SJ, Mijatov B, Gunatilake D, Gowrishankar K, Tiffen J, James W, et al. Control of NF-kB activity in human melanoma by bromodomain and extra-terminal protein inhibitor I-BET151. Pigment Cell Melanoma Res. 2014. Epub 2014/06/14.
27. Belkina AC, Denis GV. BET domain co-regulators in obesity, inflammation and cancer. Nature reviews Cancer. 2012; 12(7):465-77. Epub 2012/06/23. doi: 10.1038/nrc3256 PMID: 22722403.
28. Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S, Chung CW, et al. Suppression of inflammation by a synthetic histone mimic. Nature. 2010; 468(7327):1119-23. Epub 2010/11/12. doi: 10.1038/nature09589 PMID: 21068722.
29. Zhang XD, Franco A, Myers K, Gray C, Nguyen T, Hersey P. Relation of TNF-related apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer research. 1999; 59(11):2747-53. PMID: 10364001.
30. Franco AV, Zhang XD, Van Berkel E, Sanders JE, Zhang XY, Thomas WD, et al. The role of NF-kappa B in TNF-related apoptosis-inducing ligand (TRAIL)-induced apoptosis of melanoma cells. Journal of immunology (Baltimore, Md: 1950). 2001; 166(9):5337-45. PMID: 11313369.
31. Lai F, Jiang CC, Farrelly ML, Zhang XD, Hersey P. Evidence for upregulation of Bim and the splicing factor SRp55 in melanoma cells from patients treated with selective BRAF inhibitors. Melanoma Res. 2012; 22(3):244-51. Epub 2012/04/21. doi: 10.1097/CMR.0b013e328353eff2 PMID: 22516966.
32. Irvine M, Philipsz S, Frausto M, Mijatov B, Gallagher SJ, Fung C, et al. Amino terminal hydrophobic import signals target the p14(ARF) tumor suppressor to the mitochondria. Cell cycle. 2010; 9(4):829-39. PMID: 20107316.
33. Gallagher SJ, Mijatov B, Gunatilake D, Tiffen JC, Gowrishankar K, Jin L, et al. The Epigenetic Regulator I-BET151 Induces BIM-Dependent Apoptosis and Cell Cycle Arrest of Human Melanoma Cells. J Invest Dermatol. 2014. Epub 2014/06/07.
34. Gowrishankar K, Snoyman S, Pupo GM, Becker TM, Kefford RF, Rizos H. Acquired resistance to BRAF inhibition can confer cross-resistance to combined BRAF/MEK inhibition. J Invest Dermatol. 2012; 132(7):1850-9. Epub 2012/03/23. doi: 10.1038/jid.2012.63 PMID: 22437314.
35. He XH, Xu LH, Liu Y. Identification of a novel splice variant of human PD-L1 mRNA encoding an isoform- lacking Igv-like domain. Acta Pharmacol Sin. 2005; 26(4):462-8. PMID: 15780196.
36. Yang J, Amiri KI, Burke JR, Schmid JA, Richmond A. BMS-345541 targets inhibitor of kappaB kinase and induces apoptosis in melanoma: Involvement of nuclear factor kappaB and mitochondria pathways. Clin Cancer Res. 2006; 12(3 Pt 1):950-60. PMID: 16467110.
37. Huang G, Wen Q, Zhao Y, Gao Q, Bai Y. NF-kappaB plays a key role in inducing CD274 expression in human monocytes after lipopolysaccharide treatment. PLoS One. 2013; 8(4):61602. doi: 10.1371/journal.pone.0061602 PMID: 23585913.
38. Chen J, Li G, Meng H, Fan Y, Song Y, Wang S, et al. Upregulation of B7-H1 expression is associated with macrophage infiltration in hepatocellular carcinomas. Cancer Immunol Immunother. 2012; 61 (1):101-8. Epub 2011/08/20. doi: 10.1007/s00262-011-1094-3 PMID: 21853301.
39. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: An overview of signals, mechanisms and functions. J Leukoc Biol. 2004; 75(2):163-89. PMID: 14525967.
40. Atefi M, Avramis E, Lassen A, Wong DJ, Robert L, Foulad D, et al. Effects of MAPK and PI3K Pathways on PD-L1 Expression in Melanoma. Clin Cancer Res. 2014; 20(13):3446-57. Epub 2014/05/09. doi: 10.1158/1078-0432.CCR-13-2797 PMID: 24812408.
41. Li N, Grivennikov SI, Karin M. The unholy trinity: Inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell. 2011; 19(4):429-31. doi: 10.1016/j.ccr.2011.03.018 PMID: 21481782.
42. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine & growth factor reviews. 2010; 21(1):11-9.
43. Azuma K, Ota K, Kawahara A, Hattori S, Iwama E, Harada T, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected non-small cell lung cancer. Annals of oncology: official journal of the European Society for Medical Oncology/ESMO. 2014. Epub 2014/07/11.