Susceptibility of hepatoma-derived cells to histone deacetylase inhibitors is associated with ID2 expression

International Journal of Oncology

Volumn 42, Issue 4, 2013, Pages 1159-1166

  Tsunedomi, Ryouichi ^a   Iizuka, Norio ^a   Harada, Sawako ^a   Oka, Masaaki ^a  

^a YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Hepatocellular carcinoma; Histone deacethylase inhibitor; Inhibitor of DNA binding 2

Indexed keywords

4 PHENYLBUTYRIC ACID; ANTINEOPLASTIC AGENT; APICIDIN; BUTYRIC ACID; ENTINOSTAT; HISTONE DEACETYLASE INHIBITOR; INHIBITOR OF DIFFERENTIATION 2; LIPOCORTIN 5; MESSENGER RNA; PLASMID VECTOR; PROTEIN BCL 2; SMALL INTERFERING RNA; TRICHOSTATIN A; VORINOSTAT;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER PROGNOSIS; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE INDUCTION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MARKER GENE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TREATMENT RESPONSE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BUTYRATES; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL SURVIVAL; GENE EXPRESSION; HISTONE DEACETYLASE INHIBITORS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; LIVER NEOPLASMS;

EID: 84874631676     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2013.1811     Document Type: Article

References (50)

1. Thorgeirsson SS and Grisham JW: Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31:339-346, 2002.
2. Parkin DM, Bray F, Ferlay J and Pisani P: Global cancer statistics. CA Cancer J Clin 2005 55:74-108, 2002.
3. Bruix J, Boix L, Sala M and Llovet JM: Focus on hepatocellular carcinoma. Cancer Cell 5:215-219, 2004.
4. Iizuka N, Oka M, Yamada-Okabe H, Mori N, Tamesa T, Okada T, Takemoto N, Sakamoto K, Hamada K, Ishitsuka H, Miyamoto T, Uchimura S and Hamamoto Y: Self-organizing-map-based molecular signature representing the development of hepatocellular carcinoma. FEBS Lett 579:1089-1100, 2005.
5. Damdinsuren B, Nagano H, Kondo M, Yamamoto H, Hiraoka N, Yamamoto T, Marubashi S, Miyamoto A, Umeshita K, Dono K, Nakamori S, Wakasa K, Sakon M and Monden M: Expression of Id proteins in human hepatocellular carcinoma: relevance to tumor dedifferentiation. Int J Oncol 26:319-327, 2005.
6. Tsunedomi R, Iizuka N, Yamada-Okabe H, Tamesa T, Okada T, Sakamoto K, Takashima M, Hamaguchi T, Miyamoto T, Uchimura S, Hamamoto Y, Yamada M and Oka M: Identification of ID2 associated with invasion of hepatitis C virus-related hepatocellular carcinoma by gene expression profile. Int J Oncol 29:1445-1451, 2006.
7. Tsunedomi R, Iizuka N, Tamesa T, Sakamoto K, Hamaguchi T, Somura H, Yamada M and Oka M: Decreased ID2 promotes metastatic potentials of hepatocellular carcinoma by altering secretion of vascular endothelial growth factor. Clin Cancer Res 14:1025-1031, 2008.
8. Benezra R, Davis R, Lockshon D, Turner D and Weintraub H: The protein ID: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61:49-59, 1990.
9. Kadesch T: Consequences of heteromeric interactions among helix-loop-helix proteins. Cell Growth Differ 4:49-55, 1993.
10. Norton JD: ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 113:3897-3905, 2000.
11. Biggs J, Murphy EV and Israel MA: Id-like helix-loop-helix protein expressed during early development. Proc Natl Acad Sci USA 89:1512-1516, 1992.
12. Hara E, Yamaguchi T, Nojima H, Ide T, Campisi J, Okayama H and Oda K: Id-related genes encoding helix-loop-helix proteins are required for G1 progression and are repressed in senescent human fibroblasts. J Biol Chem 269:2139-2145, 1994.
13. Rivera R and Murre C: The regulation and function of the Id proteins inlymphocyte development. Oncogene 20:8308-8316, 2001.
14. Zebedee Z and Hara E: Id proteins in cell cycle control and cellular senescence. Oncogene 20:8317-8325, 2001.
15. Benezra R, Rafii S and Lyden D: The Id proteins and angiogenesis. Oncogene 20:8334-8341, 2001.
16. Ellmeier W, Aguzzi A, Kleiner E, Kurzbauer R and Weith A: Mutually exclusive expression of a helix-loop-helix gene and N-myc in human neuroblastomas and in normal development. EMBO J 11:2563-2571, 1992.
17. Israel MA, Hernandez MC, Florio M, Andres-Barquin PJ, Mantani A, Carter JH and Julin CM: Id gene expression as a key mediator of tumor cell biology. Cancer Res 59:1726s-1730s, 1999.
18. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K and Benezra R: Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401:670-677, 1999.
19. Maruyama H, Kleeff J, Wildi S, Friess H, Büchler MW, Israel MA and Korc M: Id-1 and Id-2 are overexpressed in pancreatic cancer and in dysplastic lesions in chronic pancreatitis. Am J Pathol 155:815-822, 1999.
20. Lin CQ, Singh J, Murata K, Itahana Y, Parrinello S, Liang SH, Gillett CE, Campisi J and Desprez PY: A role for Id-1 in the aggressive phenotype and steroid hormone response of human breast cancer cells. Cancer Res 60:1332-1340, 2000.
21. Langlands K, Down GA and Kealey T: Id proteins are dynamically expressed in normal epidermis and dysregulated in squamous cell carcinoma. Cancer Res 60:5929-5933, 2000.
22. Wilson JW, Deed RW, Inoue T, Balzi M, Becciolini A, Faraoni P, Potten CS and Norton JD: Expression of Id helix-loop-helix proteins in colorectal adenocarcinoma correlates with p53 expression and mitotic index. Cancer Res 61:8803-8810, 2001.
23. Schindl M, Schoppmann SF, Ströbel T, Heinzl H, Leisser C, Horvat R and Birner P: Level of Id-1protein expression correlates with poor differentiation, enhanced malignant potential and more aggressive clinical behavior of epithelial ovarian tumors. Clin Cancer Res 9:779-785, 2003.
24. Itahana Y, Singh J, Sumida T, Coppe JP, Parrinello S, Bennington JL and Desprez PY: Role of Id-2 in the maintenance of a differentiated and noninvasive phenotype in breast cancer cells. Cancer Res 63:7098-7105, 2003.
25. Coppe JP, Itahana Y, Moore DH, Bennington JL and Desprez PY: Id-1 and Id-2 proteins as molecular markers for human prostate cancer progression. Clin Cancer Res 10:2044-2051, 2004.
26. Umetani N, Takeuchi H, Fujimoto A, Shinozaki M, Bilchik AJ and Hoon DS: Epigenetic inactivation of ID4 in colorectal carcinomas correlates with poor differentiation and unfavorable prognosis. Clin Cancer Res 10:7475-7483, 2004.
27. de Candia P, Benera R and Solit DB: A role for Id proteins in mammary gland physiology and tumorigenesis. Adv Cancer Res 92:81-94, 2004.
28. Stighall M, Manetopoulos C, Axelson H and Landberg G: High ID2 protein expression correlates with a favourable prognosis in patients with primary breast cancer and reduces cellular invasiveness of breast cancer cells. Int J Cancer 115:403-411, 2005.
29. Umetani N, Mori T, Koyanagi K, Shinozaki M, Kim J, Giuliano AE and Hoon DS: Aberrant hypermethylation of ID4 gene promoter region increases risk of lymph node metastasis in T1 breast cancer. Oncogene 24:4721-4727, 2005.
30. Matsuda Y, Yamagiwa S, Takamura M, Honda Y, Ishimoto Y, Ichida T and Aoyagi Y: Overexpressed Id-1 is associated with a high risk of hepatocellular carcinoma development in patients with cirrhosis without transcriptional repression of p16. Cancer 104:1037-1044, 2005.
31. Lee TK, Poon RT, Yuen AP, Ling MT, Wang XH, Wong YC, Guan XY, Man K, Tang ZY and Fan ST: Regulation of angiogenesis by Id-1 through hypoxia-inducible factor-1a-mediated vascular endothelial growth factor up-regulation in hepatocellular carcinoma. Clin Cancer Res 12:6910-6919, 2006.
32. Drummond DC, Noble CO, Kirpotin DB, Guo Z, Scott GK and Benz CC: Clinical development of histone deacetylase inhibitors as anticancer agents. Annu Rev Pharmacol Toxicol 45:495-528, 2005.
33. Liu T, Kuljaca S, Tee A and Marshall GM: Histone deacetylase inhibitors: multifunctional anticancer agents. Cancer Treat Rev 32:157-165, 2006.
34. Khan O and La Thangue NB: HDAC inhibitors in cancer biology: Emerging mechanisms and clinical applications. Immunol Cell Biol 90:85-94, 2012.
35. Rosato RR, Almenara JA, Dai Y and Grant S: Simultaneous activation of the intrinsic and extrinsic pathways by histone deacetylase (HDAC) inhibitors and tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) synergistically induces mitochondrial damage and apoptosis in human leukemia cells. Mol Cancer Ther 2:1273-1284, 2003.
36. Emanuele S, Lauricella M and Tesoriere G: Histone deacetylase inhibitors: Apoptotic effects and clinical implications. Int J Oncol 33:637-646, 2008.
37. Zhang J, Kan S, Huang B, Hao Z, Mak TW and Zhong Q: Mule determines the apoptotic response to HDAC inhibitors by targeted ubiquitination and destruction of HDAC2. Genes Dev 25:2610-2618, 2011.
38. Vigushin DM and Coombes RC: Histone deacetylase inhibitors in cancer treatment. Anticancer Drugs 13:1-13, 2002.
39. Lin HY, Chen CS, Lin SP, Weng JR and Chen CS: Targeting histone deacetylase in cancer therapy. Med Res Rev 26:397-413, 2006.
40. Xu WS, Parmigiani RB and Marks PA: Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26:5541-5552, 2007.
41. Tsunedomi R, Ogawa Y, Iizuka N, Sakamoto K, Tamesa T, Moribe T and Oka M: The assessment of methylated BASP1 and SRD5A2 levels in the detection of early hepatocellular carcinoma. Int J Oncol 36:205-212, 2010.
42. Kouzarides T: Histone acetylases and deacetylases in cell proliferation. Curr Opin Genet Dev 9:40-48, 1999.
43. Marks PA, Richon VM and Rifkind RA: Histone deacetylase inhibitors: inducers of differentiation or apotosis of transformed cells. J Natl Cancer Inst 92:1210-1216, 2000.
44. Timmermann S, Lehrmann H, Polesskaya A and Harel-Bellan A: Histone acetylation and disease. Cell Mol Life Sci 58:728-736, 2001.
45. Ogawa K, Yasumura S, Atarashi Y, Minemura M, Miyazaki T, Iwamoto M, Higuchi K and Watanabe A: Sodium butyrate enhances Fas-mediated apoptosis of human hepatoma cells. J Hepatol 40:278-284, 2004.
46. Joseph J, Mudduluru G, Antony S, Vashistha S, Ajitkumar P, and Somasundaram K: Expression profiling of sodium butyrate (NaB)-treated cells: identification of regulation of genes related to cytokine signaling and cancer metastasis by NaB. Oncogene 23:6304-6315, 2004.
47. Chiba T, Yokosuka O, Arai M, Tada M, Fukai K, Imazeki F, Kato M, Seki N and Saisho H: Identification of genes up-regulated by histone deacetylase inhibition with cDNA microarray and exploration of epigenetic alterations on hepatoma cells. J Hepatol 41:436-445, 2004.
48. Chen J, Saha P, Kornbluth S, Dynlacht BD and Dutta A: Cyclin-binding motifs are essential for the function of p21CIP1. Mol Cell Biol 16:4673-4682, 1996.
49. Shin JY, Kim HS, Park J, Park JB and Lee JY: Mechanism for inactivation of the KIP family cyclin-dependent kinase inhibitor genes in gastric cancer cells. Cancer Res 60:262-265, 2000.
50. Han JW, Ahn SH, Kim YK, Bae GU, Yoon JW, Hong S, Lee HY, Lee YW and Lee HW: Activation of p21WAF1/Cip1 transcription through Sp1 sites by histone deacetylase inhibitor apicidin. J Biol Chem 276:42084-42090, 2001.