EGR1 reactivation by histone deacetylase inhibitors promotes synovial sarcoma cell death through the PTEN tumor suppressor

Oncogene

Volumn 29, Issue 30, 2010, Pages 4352-4361

  Su, L ^a   Cheng, H ^a   Sampaio, A V ^a   Nielsen, T O ^a   Underhill, T M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

apoptosis; EGR1; HDAC inhibitors; PTEN; synovial sarcoma

Indexed keywords

BELINOSTAT; COMPLEMENTARY DNA; DEPSIPEPTIDE; HISTONE DEACETYLASE INHIBITOR; HYBRID PROTEIN; MESSENGER RNA; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RIBOSOME RNA; RNA 18S; ROMIDEPSIN; SMALL INTERFERING RNA; SS18 SSX ONCOPROTEIN; TRANSCRIPTION FACTOR EGR 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL STRAIN HEK293; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SARCOMA CELL; SYNOVIAL SARCOMA; WESTERN BLOTTING;

APOPTOSIS; CELL LINE, TUMOR; EARLY GROWTH RESPONSE PROTEIN 1; HISTONE DEACETYLASE INHIBITORS; HUMANS; PTEN PHOSPHOHYDROLASE; SARCOMA, SYNOVIAL;

EID: 77955177292     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.204     Document Type: Article

References (48)

1. Archer SY, Meng S, Shei A, Hodin RA. (1998). p21(WAF1) is required for butyrate-mediated growth inhibition of human colon cancer cells. Proc Natl Acad Sci USA 95: 6791-6796.
2. Bolden JE, Peart MJ, Johnstone RW. (2006). Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784.
3. Bozzi F, Ferrari A, Negri T, Conca E, Luca da R, Losa M et al. (2008). Molecular characterization of synovial sarcoma in children and adolescents: evidence of akt activation. Transl Oncol 1: 95-101.
4. Brett D, Whitehouse S, Antonson P, Shipley J, Cooper C, Goodwin G. (1997). The SYT protein involved in the t(X;18) synovial sarcoma translocation is a transcriptional activator localised in nuclear bodies. Hum Mol Genet 6: 1559-1564.
5. Calogero A, Cuomo L, DOnofrio M, de Grazia U, Spinsanti P, Mercola D et al. (1996). Expression of Egr-1 correlates with the transformed phenotype and the type of viral latency in EBV genome positive lymphoid cell lines. Oncogene 13: 2105-2112.
6. Calogero A, Lombari V, De Gregorio G, Porcellini A, Ucci S, Arcella A et al. (2004). Inhibition of cell growth by EGR-1 in human primary cultures from malignant glioma. Cancer Cell Int 4: 1.
7. Condorelli F, Gnemmi I, Vallario A, Genazzani AA, Canonico PL. (2008). Inhibitors of histone deacetylase (HDAC) restore the p53 pathway in neuroblastoma cells. Br J Pharmacol 153: 657-668.
8. de Bruijn DR, Allander SV, van Dijk AH, Willemse MP, Thijssen J, van Groningen JJ et al. (2006). The synovial-sarcoma-associated SS18-SSX2 fusion protein induces epigenetic gene (de)regulation. Cancer Res 66: 9474-9482.
9. Downes CP, Bennett D, McConnachie G, Leslie NR, Pass I, MacPhee C et al. (2001). Antagonism of PI 3-kinase-dependent signalling pathways by the tumour suppressor protein, PTEN. Biochem Soc Trans 29: 846-851.
10. Gan YH, Zhang S. (2009). PTEN/AKT pathway involved in histone deacetylases inhibitor induced cell growth inhibition and apoptosis of oral squamous cell carcinoma cells. Oral Oncol 45: e150-e154.
11. Gashler A, Sukhatme VP. (1995). Early growth response protein 1 (Egr-1): prototype of a zinc-finger family of transcription factors. Prog Nucleic Acid Res Mol Biol 50: 191-224.
12. Habold C, Poehlmann A, Bajbouj K, Hartig R, Korkmaz KS, Roessner A et al. (2008). Trichostatin A causes p53 to switch oxidative-damaged colorectal cancer cells from cell cycle arrest into apoptosis. J Cell Mol Med 12: 607-621.
13. Huang RP, Darland T, Okamura D, Mercola D, Adamson ED. (1994). Suppression of v-sis-dependent transformation by the transcription factor, Egr-1. Oncogene 9:1367-1377.
14. Huang RP, Fan Y, de Belle I, Niemeyer C, Gottardis MM, Mercola D et al. (1997). Decreased Egr-1 expression in human, mouse and rat mammary cells and tissues correlates with tumor formation. Int J Cancer 72: 102-109.
15. Huang RP, Liu C, Fan Y, Mercola D, Adamson ED. (1995). Egr-1 negatively regulates human tumor cell growth via the DNA-binding domain. Cancer Res 55: 5054-5062.
16. Italiano A, Penel N, Robin YM, Bui B, Le Cesne A, Piperno-Neumann S et al. (2009). Neo/adjuvant chemotherapy does not improve outcome in resected primary synovial sarcoma: a study of the French Sarcoma Group. Ann Oncol 20: 425-430.
17. Ito T, Ouchida M, Morimoto Y, Yoshida A, Jitsumori Y, Ozaki T et al. (2005). Significant growth suppression of synovial sarcomas by the histone deacetylase inhibitor FK228 in vitro and in vivo. Cancer Lett 224: 311-319.
18. Khan O, La Thangue NB. (2008). Drug Insight: histone deacetylase inhibitor-based therapies for cutaneous T-cell lymphomas. Nat Clin Pract Oncol 5: 714-726.
19. Kim J, Lee YH, Kwon TK, Chang JS, Chung KC, Min DS. (2006). Phospholipase D prevents etoposide-induced apoptosis by inhibiting the expression of early growth response-1 and phosphatase and tensin homologue deleted on chromosome 10. Cancer Res 66: 784-793.
20. Krones-Herzig A, Mittal S, Yule K, Liang H, English C, Urcis R et al. (2005). Early growth response 1 acts as a tumor suppressor in vivo and in vitro via regulation of p53. Cancer Res 65: 5133-5143.
21. Le Beau MM, Espinosa 3rd R, Neuman WL, Stock W, Roulston D, Larson RA et al. (1993). Cytogenetic and molecular delineation of the smallest commonly deleted region of chromosome 5 in malignant myeloid diseases. Proc Natl Acad Sci USA 90: 5484-5488.
22. Levin WJ, Press MF, Gaynor RB, Sukhatme VP, Boone TC, Reissmann PT et al. (1995). Expression patterns of immediate early transcription factors in human non-small cell lung cancer. The Lung Cancer Study Group. Oncogene 11: 1261-1269.
23. Lim FL, Soulez M, Koczan D, Thiesen HJ, Knight JC. (1998). A KRAB-related domain and a novel transcription repression domain in proteins encoded by SSX genes that are disrupted in human sarcomas. Oncogene 17: 2013-2018.
24. Liu C, Adamson E, Mercola D. (1996). Transcription factor EGR-1 suppresses the growth and transformation of human HT-1080 fibrosarcoma cells by induction of transforming growth factor beta 1. Proc Natl Acad Sci USA 93: 11831-11836.
25. Liu C, Yao J, de Belle I, Huang RP, Adamson E, Mercola D. (1999). The transcription factor EGR-1 suppresses transformation of human fibrosarcoma HT1080 cells by coordinated induction of transforming growth factor-beta1, fibronectin, and plasminogen activator inhibitor-1. J Biol Chem 274: 4400-4411.
26. Liu J, Grogan L, Nau MM, Allegra CJ, Chu E, Wright JJ. (2001). Physical interaction between p53 and primary response gene Egr-1. Int J Oncol 18: 863-870.
27. Lubieniecka JM, de Bruijn DR, Su L, van Dijk AH, Subramanian S, van de Rijn M et al. (2008). Histone deacetylase inhibitors reverse SS18-SSX-mediated polycomb silencing of the tumor suppressor early growth response 1 in synovial sarcoma. Cancer Res 68: 4303-4310.
28. Ma DZ, Xu Z, Liang YL, Su JM, Li ZX, Zhang W et al. (2005). Down-regulation of PTEN expression due to loss of promoter activity in human hepatocellular carcinoma cell lines. World J Gastroenterol 11: 4472-4477.
29. Medina V, Edmonds B, Young GP, James R, Appleton S, Zalewski PD. (1997). Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res 57: 3697-3707.
30. Moradei O, Vaisburg A, Martell RE. (2008). Histone deacetylase inhibitors in cancer therapy: new compounds and clinical update of benzamide-type agents. Curr Top Med Chem 8: 841-858.
31. Nagai M, Tanaka S, Tsuda M, Endo S, Kato H, Sonobe H et al. (2001). Analysis of transforming activity of human synovial sarcoma-associated chimeric protein SYT-SSX1 bound to chroma-tin remodeling factor hBRM/hSNF2 alpha. Proc Natl Acad Sci USA 98: 3843-3848.
32. Nair P, Muthukkumar S, Sells SF, Han SS, Sukhatme VP, Rangnekar VM. (1997). Early growth response-1-dependent apoptosis is mediated by p53. J Biol Chem 272: 20131-20138.
33. Okcu MF, Munsell M, Treuner J, Mattke A, Pappo A, Cain A et al. (2003). Synovial sarcoma of childhood and adolescence: a multicenter, multivariate analysis of outcome. J Clin Oncol 21: 1602-1611.
34. Pan L, Lu J, Wang X, Han L, Zhang Y, Han S et al. (2007). Histone deacetylase inhibitor trichostatin a potentiates doxorubicin-induced apoptosis by up-regulating PTEN expression. Cancer 109: 1676-1688.
35. Roeb W, Boyer A, Cavenee WK, Arden KC. (2007). PAX3-FOXO1 controls expression of the p57Kip2 cell-cycle regulator through degradation of EGR1. Proc Natl Acad Sci USA 104: 18085-18090.
36. Roeb W, Boyer A, Cavenee WK, Arden KC. (2008). Guilt by association: PAX3-FOXO1 regulates gene expression through selective destabilization of the EGR1 transcription factor. Cell Cycle 7: 837-841.
37. Roy S, Tenniswood M. (2007). Site-specific acetylation of p53 directs selective transcription complex assembly. J Biol Chem 282: 4765-4771.
38. Soulez M, Saurin AJ, Freemont PS, Knight JC. (1999). SSX and the synovial-sarcoma-specific chimaeric protein SYT-SSX co-localize with the human Polycomb group complex. Oncogene 18: 2739-2746.
39. Stimson L, Wood V, Khan O, Fotheringham S, La Thangue NB. (2009). HDAC inhibitor-based therapies and haematological malignancy. Ann Oncol 20: 1293-1302.
40. Sukhatme VP. (1990). Early transcriptional events in cell growth: the Egr family. J Am Soc Nephrol 1: 859-866.
41. Sukhatme VP, Kartha S, Toback FG, Taub R, Hoover RG, Tsai-Morris CH. (1987). A novel early growth response gene rapidly induced by fibroblast, epithelial cell and lymphocyte mitogens. Oncogene Res 1: 343-355.
42. Thaete C, Brett D, Monaghan P, Whitehouse S, Rennie G, Rayner E et al. (1999). Functional domains of the SYT and SYT-SSX synovial sarcoma translocation proteins and co-localization with the SNF protein BRM in the nucleus. Hum Mol Genet 8: 585-591.
43. Virolle T, Adamson ED, Baron V, Birle D, Mercola D, Mustelin T et al. (2001). The Egr-1 transcription factor directly activates PTEN during irradiation-induced signalling. Nat Cell Biol 3: 1124-1128.
44. Virolle T, Krones-Herzig A, Baron V, De Gregorio G, Adamson ED, Mercola D. (2003). Egr1 promotes growth and survival of prostate cancer cells. Identification of novel Egr1 target genes. J Biol Chem 278: 11802-11810.
45. Yu J, Baron V, Mercola D, Mustelin T, Adamson ED. (2007). A network of p73, p53 and Egr1 is required for efficient apoptosis in tumor cells. Cell Death Differ 14: 436-446.
46. Yu J, de Belle I, Liang H, Adamson ED. (2004). Coactivating factors p300 and CBP are transcriptionally crossregulated by Egr1 in prostate cells, leading to divergent responses. Mol Cell 15: 83-94.
47. Yu J, Zhang SS, Saito K, Williams S, Arimura Y, Ma Y et al. (2009). PTEN regulation by Akt-EGR1-ARF-PTEN axis. EMBO J 28: 21-33.
48. Zhao Y, Lu S, Wu L, Chai G, Wang H, Chen Y et al. (2006). Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol Cell Biol 26: 2782-2790.