ING1 and 5-azacytidine act synergistically to block breast cancer cell growth

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Thakur, Satbir ^a,b   Feng, Xiaolan ^a,b   Qiao Shi, Zhong ^b,c   Ganapathy, Amudha ^a,b   Kumar Mishra, Manoj ^c   Atadja, Peter ^d   Morris, Don ^b,c   Riabowol, Karl ^a,b  

^a UNIVERSITY OF CALGARY   (Canada)

^b Southern Alberta Cancer Research Institute   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d Novartis Institutes for Biomedical Research   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; AZACITIDINE; CASPASE 3; DNA METHYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE H2AX; INHIBITOR OF GROWTH 1 PROTEIN; INHIBITOR OF GROWTH 1B PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PANOBINOSTAT; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GENE THERAPY; CANCER INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DRUG POTENTIATION; DRUG TARGETING; EPIGENETICS; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; TUMOR REGRESSION; VIRAL GENE DELIVERY SYSTEM; VIRUS CONCENTRATION;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; AZACITIDINE; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; HUMANS; HYDROXAMIC ACIDS; INDOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, SCID; NUCLEAR PROTEINS; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84865165269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043671     Document Type: Article

References (53)

1. Kristensen LS, Nielsen HM, Hansen LL, ((2009)) Epigenetics and cancer treatment. Eur J Pharmacol 625: 131-142.
2. Garkavtsev I, Kazarov A, Gudkov A, Riabowol K, ((1996)) Suppression of the novel growth inhibitor p33ING1 promotes neoplastic transformation. Nat Genet 14: 415-420.
3. Nouman GS, Anderson JJ, Crosier S, Shrimankar J, Lunec J, et al. ((2003)) Downregulation of nuclear expression of the p33(ING1b) inhibitor of growth protein in invasive carcinoma of the breast. J Clin Pathol 56: 507-511.
4. Tokunaga E, Maehara Y, Oki E, Kitamura K, Kakeji Y, et al. ((2000)) Diminished expression of ING1 mRNA and the correlation with p53 expression in breast cancers. Cancer Lett 152: 15-22.
5. Toyama T, Iwase H, Watson P, Muzik H, Saettler E, et al. ((1999)) Suppression of ING1 expression in sporadic breast cancer. Oncogene 18: 5187-5193.
6. Maher SK, Helbing CC, ((2009)) Modulators of inhibitor of growth (ING) family expression in development and disease. Curr Drug Targets 10: 392-405.
7. Loewith R, Meijer M, Lees-Miller SP, Riabowol K, Young D, ((2000)) Three yeast proteins related to the human candidate tumor suppressor p33(ING1) are associated with histone acetyltransferase activities. Mol Cell Biol 20: 3807-3816.
8. Vieyra D, Toyama T, Hara Y, Boland D, Johnston R, et al. ((2002)) ING1 isoforms differentially affect apoptosis in a cell age-dependent manner. Cancer Res 62: 4445-4452.
9. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, et al. ((2006)) ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 21: 51-64.
10. Tallen G, Riabowol K, Wolff JE, ((2003)) Expression of p33ING1 mRNA and chemosensitivity in brain tumor cells. Anticancer Res 23: 1631-1635.
11. Zhu JJ, Liao WM, Li FB, Zhu XF, Zhou JM, et al. ((2004)) [p33(ING1b) enhances chemosensitivity of osteosarcoma cell U2OS to etoposide]. Ai Zheng 23: 640-644.
12. Sharma S, Kelly TK, Jones PA, ((2010)) Epigenetics in cancer. Carcinogenesis 31: 27-36.
13. Kim TY, Bang YJ, Robertson KD, ((2006)) Histone deacetylase inhibitors for cancer therapy. Epigenetics 1: 14-23.
14. Atadja PW, ((2011)) HDAC inhibitors and cancer therapy. Prog Drug Res 67: 175-195.
15. Candido EP, Reeves R, Davie JR, ((1978)) Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14: 105-113.
16. Atadja P, ((2009)) Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett 280: 233-241.
17. Smith KT, Martin-Brown SA, Florens L, Washburn MP, Workman JL, ((2010)) Deacetylase inhibitors dissociate the histone-targeting ING2 subunit from the Sin3 complex. Chem Biol 17: 65-74.
18. Szyf M, ((1994)) DNA methylation properties: consequences for pharmacology. Trends Pharmacol Sci 15: 233-238.
19. Kuendgen A, Lubbert M, ((2008)) Current status of epigenetic treatment in myelodysplastic syndromes. Ann Hematol 87: 601-611.
20. Wu JC, Santi DV, ((1985)) On the mechanism and inhibition of DNA cytosine methyltransferases. Prog Clin Biol Res 198: 119-129.
21. Oki Y, Aoki E, Issa JP, ((2007)) Decitabine-bedside to bench. Crit Rev Oncol Hematol 61: 140-152.
22. Soriano AO, Yang H, Faderl S, Estrov Z, Giles F, et al. ((2007)) Safety and clinical activity of the combination of 5-azacytidine, valproic acid, and all-trans retinoic acid in acute myeloid leukemia and myelodysplastic syndrome. Blood 110: 2302-2308.
23. Shimada H, Liu TL, Ochiai T, Shimizu T, Haupt Y, et al. ((2002)) Facilitation of adenoviral wild-type p53-induced apoptotic cell death by overexpression of p33(ING1) in T.Tn human esophageal carcinoma cells. Oncogene 21: 1208-1216.
24. Shinoura N, Muramatsu Y, Nishimura M, Yoshida Y, Saito A, et al. ((1999)) Adenovirus-mediated transfer of p33ING1 with p53 drastically augments apoptosis in gliomas. Cancer Res 59: 5521-5528.
25. Xie Y, Sheng W, Miao J, Xiang J, Yang J, ((2011)) Enhanced antitumor activity by combining an adenovirus harboring ING4 with cisplatin for hepatocarcinoma cells. Cancer Gene Ther 18: 176-188.
26. Xie Y, Zhang H, Sheng W, Xiang J, Ye Z, et al. ((2008)) Adenovirus-mediated ING4 expression suppresses lung carcinoma cell growth via induction of cell cycle alteration and apoptosis and inhibition of tumor invasion and angiogenesis. Cancer Lett 271: 105-116.
27. Zhao Y, Su C, Zhai H, Tian Y, Sheng W, et al. (2011) Synergistic antitumor effect of adenovirus-mediated hING4 gene therapy and (125)I radiation therapy on pancreatic cancer. Cancer Lett.
28. Zhu Y, Lv H, Xie Y, Sheng W, Xiang J, et al. ((2011)) Enhanced tumor suppression by an ING4/IL-24 bicistronic adenovirus-mediated gene cotransfer in human non-small cell lung cancer cells. Cancer Gene Ther 18: 627-636.
29. Zhang X, Xu LS, Wang ZQ, Wang KS, Li N, et al. ((2004)) ING4 induces G2/M cell cycle arrest and enhances the chemosensitivity to DNA-damage agents in HepG2 cells. FEBS Lett 570: 7-12.
30. Hackett AJ, Smith HS, Springer EL, Owens RB, Nelson-Rees WA, et al. ((1977)) Two syngeneic cell lines from human breast tissue: the aneuploid mammary epithelial (Hs578T) and the diploid myoepithelial (Hs578Bst) cell lines. J Natl Cancer Inst 58: 1795-1806.
31. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, et al. ((1998)) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95: 2509-2514.
32. Chou TC, Talalay P, ((1984)) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55.
33. Liu JY, Wu BQ, Zheng J, You JF, Zhong HH, et al. ((2003)) [Effects of two variants of ING1 expression on tumor cell growth regulation]. Zhonghua Bing Li Xue Za Zhi 32: 48-51.
34. Helbing CC, Veillette C, Riabowol K, Johnston RN, Garkavtsev I, ((1997)) A novel candidate tumor suppressor, ING1, is involved in the regulation of apoptosis. Cancer Res 57: 1255-1258.
35. Cheung KJ Jr, Li G, ((2002)) p33(ING1) enhances UVB-induced apoptosis in melanoma cells. Exp Cell Res 279: 291-298.
36. Nagashima M, Shiseki M, Miura K, Hagiwara K, Linke SP, et al. ((2001)) DNA damage-inducible gene p33ING2 negatively regulates cell proliferation through acetylation of p53. Proc Natl Acad Sci U S A 98: 9671-9676.
37. Nagashima M, Shiseki M, Pedeux RM, Okamura S, Kitahama-Shiseki M, et al. ((2003)) A novel PHD-finger motif protein, p47ING3, modulates p53-mediated transcription, cell cycle control, and apoptosis. Oncogene 22: 343-350.
38. Li Z, Xie Y, Sheng W, Miao J, Xiang J, et al. ((2010)) Tumor-suppressive effect of adenovirus-mediated inhibitor of growth 4 gene transfer in breast carcinoma cells in vitro and in vivo. Cancer Biother Radiopharm 25: 427-437.
39. Zhu Z, Lin J, Qu JH, Feitelson MA, Ni CR, et al. ((2005)) Inhibitory effect of tumor suppressor p33(ING1b) and its synergy with p53 gene in hepatocellular carcinoma. World J Gastroenterol 11: 1903-1909.
40. Scott M, Bonnefin P, Vieyra D, Boisvert FM, Young D, et al. ((2001)) UV-induced binding of ING1 to PCNA regulates the induction of apoptosis. J Cell Sci 114: 3455-3462.
41. Garkavtsev I, Grigorian IA, Ossovskaya VS, Chernov MV, Chumakov PM, et al. ((1998)) The candidate tumour suppressor p33ING1 cooperates with p53 in cell growth control. Nature 391: 295-298.
42. Toyama T, Iwase H, ((2004)) p33ING1b and estrogen receptor (ER) alpha. Breast Cancer 11: 33-37.
43. Toyama T, Iwase H, Yamashita H, Hara Y, Sugiura H, et al. ((2003)) p33(ING1b) stimulates the transcriptional activity of the estrogen receptor alpha via its activation function (AF) 2 domain. J Steroid Biochem Mol Biol 87: 57-63.
44. Ropero S, Esteller M, ((2007)) The role of histone deacetylases (HDACs) in human cancer. Mol Oncol 1: 19-25.
45. Garkavtsev I, Boucher Y, ((2005)) An intact ING1-P53 pathway can potentiate the cytotoxic effects of taxol. Cancer Biol Ther 4: 48-49.
46. Sanchez-Abarca LI, Gutierrez-Cosio S, Santamaria C, Caballero-Velazquez T, Blanco B, et al. ((2010)) Immunomodulatory effect of 5-azacytidine (5-azaC): potential role in the transplantation setting. Blood 115: 107-121.
47. Eastman A, Rigas JR (1999) Modulation of apoptosis signaling pathways and cell cycle regulation. Semin Oncol 26: 7-16; discussion 41-12.
48. Kiziltepe T, Hideshima T, Catley L, Raje N, Yasui H, et al. ((2007)) 5-Azacytidine, a DNA methyltransferase inhibitor, induces ATR-mediated DNA double-strand break responses, apoptosis, and synergistic cytotoxicity with doxorubicin and bortezomib against multiple myeloma cells. Mol Cancer Ther 6: 1718-1727.
49. Thalappilly S, Feng X, Pastyryeva S, Suzuki K, Muruve D, et al. ((2011)) The p53 tumor suppressor is stabilized by inhibitor of growth 1 (ING1) by blocking polyubiquitination. PLoS One 6: e21065.
50. Mandili G, Khadjavi A, Gallo V, Minero VG, Bessone L, et al. ((2012)) Characterization of the protein ubiquitination response induced by Doxorubicin. FEBS J 279: 2182-2191.
51. Han X, Feng X, Rattner JB, Smith H, Bose P, et al. ((2008)) Tethering by lamin A stabilizes and targets the ING1 tumour suppressor. Nat Cell Biol 10: 1333-1340.
52. Raguz S, Yague E, ((2008)) Resistance to chemotherapy: new treatments and novel insights into an old problem. Br J Cancer 99: 387-391.
53. Herman JG, Baylin SB, ((2003)) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349: 2042-2054.