Differential response of p53 and p21 on HDAC inhibitor-mediated apoptosis in HCT116 colon cancer cells in vitro and in vivo

International Journal of Oncology

Volumn 31, Issue 6, 2007, Pages 1391-1402

  Zopf, Steffen ^a   Neureiter, Daniel ^b   Bouralexis, Steve ^c   Abt, Tobias ^a   Glaser, Keith B ^d   Okamoto, Kinya ^a   Ganslmayer, Marion ^a   Hahn, Eckhart G ^a   Herold, Christoph ^a   Ocker, Matthias ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

^c ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d ABBOTT LABORATORIES   (United States)

Author keywords

Apoptosis; Colon carcinoma; HCT116; Histone deacetylase inhibitor; p53; TRAIL

Indexed keywords

A 423378.0; A-423378.0; CASPASE; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; ENZYME INHIBITOR; HISTONE DEACETYLASE; MESSENGER RNA; PROTEIN BAX; PROTEIN P53; THIAZOLE DERIVATIVE; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL; APOPTOSIS; ARTICLE; CELL MEMBRANE POTENTIAL; CELL PROLIFERATION; CELL STRAIN HCT116; COLON TUMOR; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HUMAN; MALE; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASES; CELL PROLIFERATION; COLONIC NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; ENZYME INHIBITORS; HCT116 CELLS; HISTONE DEACETYLASES; HUMANS; MALE; MEMBRANE POTENTIALS; MICE; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; RNA, MESSENGER; THIAZOLES; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR SUPPRESSOR PROTEIN P53;

EID: 38449087548     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.31.6.1391     Document Type: Article

References (52)

1. Boyle P and Langman JS: ABC of colorectal cancer: Epidemiology. BMJ 321: 805-808, 2000.
2. Alberts DS: Reducing the risk of colorectal cancer by intervening in the process of carcinogenesis: a status report. Cancer J 8: 208-221, 2002.
3. Neureiter D, Herold C and Ocker M: Gastrointestinal cancer - only a deregulation of stem cell differentiation? (Review). Int J Mol Med 17: 483-489, 2006.
4. Kopelovich L, Crowell JA and Fay JR: The epigenome as a target for cancer chemoprevention. J Natl Cancer Inst 95: 1747-1757, 2003.
5. Csordas A: On the biological role of histone acetylation. Biochem J 265: 23-38, 1990.
6. Johnstone RW: Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 1: 287-299, 2002.
7. Grunstein M: Histone acetylation in chromatin structure and transcription. Nature 389: 349-352, 1997.
8. Jenuwein T and Allis CD: Translating the histone code. Science 293: 1074-1080, 2001.
9. Villar-Garea A and Esteller M: Histone deacetylase inhibitors: understanding a new wave of anticancer agents. Int J Cancer 112: 171-178, 2004.
10. Donadelli M, Costanzo C, Faggioli L, Scupoli MT, Moore PS, Bassi C, Scarpa A and Palmieri M: Trichostatin A, an inhibitor of histone deacetylases, strongly suppresses growth of pancreatic adenocarcinoma cells. Mol Carcinog 38: 59-69, 2003.
11. Herold C, Ganslmayer M, Ocker M, Hermann M, Geerts A, Hahn EG and Schuppan D: The histone-deacetylase inhibitor Trichostatin A blocks proliferation and triggers apoptotic programs in hepatoma cells. J Hepatol 36: 233-240, 2002. (Pubitemid 34146430)
12. Richon VM, Sandhoff TW, Rifkind RA and Marks PA: Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc Natl Acad Sci USA 97: 10014-10019, 2000.
13. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW and Vogelstein B: Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501, 1998. (Pubitemid 28538613)
14. Waldman T, Kinzler KW and Vogelstein B: p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 55: 5187-5190, 1995.
15. Wagner S and Roemer K: Retinoblastoma protein is required for efficient colorectal carcinoma cell apoptosis by histone deacetylase inhibitors in the absence of p21Waf. Biochem Pharmacol 69: 1059-1067, 2005.
16. Waldman T, Lengauer C, Kinzler KW and Vogelstein B: Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381: 713-716, 1996.
17. Waldman T, Zhang Y, Dillehay L, Yu J, Kinzler K, Vogelstein B and Williams J: Cell-cycle arrest vs. cell death in cancer therapy. Nat Med 3: 1034-1036, 1997.
18. Ashkenazi A and Dixit VM: Death receptors: signaling and modulation. Science 281: 1305-1308, 1998.
19. Kim K, Fisher MJ, Xu SQ and El-Deiry WS: Molecular determinants of response to TRAIL in killing of normal and cancer cells. Clin Cancer Res 6: 335-346, 2000.
20. Glaser KB, Li J, Pease LJ, Staver MJ, Marcotte PA, Guo J, Frey RR, Garland RB, Heyman HR, Wada CK, Vasudevan A, Michaelides MR, Davidsen SK and Curtin ML: Differential protein acetylation induced by novel histone deacetylase inhibitors. Biochem Biophys Res Commun 325: 683-690, 2004.
21. Sionov RV and Haupt Y: The cellular response to p53: the decision between life and death. Oncogene 18: 6145-6157, 1999.
22. Bukholm IK and Nesland JM: Protein expression of p53, p21 (WAF1/CIP1), bcl-2, Bax, cyclin D1 and pRb in human colon carcinomas. Virchows Arch 436: 224-228, 2000.
23. Russo A, Bazan V, Iacopetta B, Kerr D, Soussi T and Gebbia N: The TP53 colorectal cancer international collaborative study on the prognostic and predictive significance of p53 mutation: influence of tumor site, type of mutation, and adjuvant treatment. J Clin Oncol 23: 7518-7528, 2005. (Pubitemid 46291815)
24. Prives C and Manley JL: Why is p53 acetylated? Cell 107: 815-818, 2001.
25. Ocker M, Alajati A, Ganslmayer M, Zopf S, Luders M, Neureiter D, Hahn EG, Schuppan D and Herold C: The histone-deacetylase inhibitor SAHA potentiates proapoptotic effects of 5-fluorouracil and irinotecan in hepatoma cells. J Cancer Res Clin Oncol 131: 385-394, 2005.
26. Ganslmayer M, Ocker M, Kraemer G, Zopf S, Hahn EG, Schuppan D and Herold C: The combination of tamoxifen and 9cis retinoic acid exerts overadditive anti-tumoral efficacy in rat hepatocellular carcinoma. J Hepatol 40: 952-956, 2004.
27. Neureiter D, Zopf S, Leu T, Dietze O, Hauser-Kronberger C, Hahn EG, Herold C and Ocker M: Apoptosis, proliferation and differentiation patterns are influenced by Zebularine and SAHA in pancreatic cancer models. Scand J Gastroenterol 42: 103-116, 2007.
28. Hasel C, Durr S, Rau B, Strater J, Schmid RM, Walczak H, Bachem MG and Moller P: In chronic pancreatitis, widespread emergence of TRAIL receptors in epithelia coincides with neoexpression of TRAIL by pancreatic stellate cells of early fibrotic areas. Lab Invest 83: 825-836, 2003.
29. Butler LM, Liapis V, Bouralexis S, Welldon K, Hay S, Thai le M, Labrinidis A, Tilley WD, Findlay DM and Evdokiou A: The histone deacetylase inhibitor, suberoylanilide hydroxamic acid, overcomes resistance of human breast cancer cells to Apo2L/ TRAIL. Int J Cancer 119: 944-954, 2006.
30. Han Z, Wei W, Dunaway S, Darnowski JW, Calabresi P, Sedivy J, Hendrickson EA, Balan KV, Pantazis P and Wyche JH: Role of p21 in apoptosis and senescence of human colon cancer cells treated with camptothecin. J Biol Chem 277: 17154-17160, 2002.
31. Ocker M and Schneider-Stock R: Histone deacetylase inhibitors: Signalling towards p21(cip1/waf1). Int J Biochem Cell Biol 39: 1367-1374, 2007.
32. Javelaud D and Besancon F: Inactivation of p21WAF1 sensitizes cells to apoptosis via an increase of both p14ARF and p53 levels and an alteration of the Bax/Bcl-2 ratio. J Biol Chem 277: 37949-37954, 2002.
33. Maier S, Reich E, Martin R, Bachem M, Altug V, Hautmann RE and Gschwend JE: Tributyrin induces differentiation, growth arrest and apoptosis in androgen-sensitive and androgen-resistant human prostate cancer cell lines. Int J Cancer 88: 245-251, 2000.
34. Nakano K, Mizuno T, Sowa Y, Orita T, Yoshino T, Okuyama Y, Fujita T, Ohtani-Fujita N, Matsukawa Y, Tokino T, Yamagishi H, Oka T, Nomura H and Sakai T: Butyrate activates the WAF1/ Cip1 gene promoter through Sp1 sites in a p53-negative human colon cancer cell line. J Biol Chem 272: 22199-22206, 1997.
35. Park KS, Jeon SH, Oh JW and Choi KY: p21Cip/WAF1 activation is an important factor for the ERK pathway dependent anti-proliferation of colorectal cancer cells. Exp Mol Med 36: 557-562, 2004.
36. Sewing A, Wiseman B, Lloyd AC and Land H: High-intensity Raf signal causes cell cycle arrest mediated by p21Cip1. Mol Cell Biol 17: 5588-5597, 1997. (Pubitemid 27357655)
37. Huang L, Sowa Y, Sakai T and Pardee AB: Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites. Oncogene 19: 5712-5719, 2000.
38. Mahyar-Roemer M and Roemer K: p21 Waf1/Cip1 can protect human colon carcinoma cells against p53-dependent and p53- independent apoptosis induced by natural chemopreventive and therapeutic agents. Oncogene 20: 3387-3398, 2001. (Pubitemid 32588987)
39. Bai S and Goodrich DW: Different DNA lesions trigger distinct cell death responses in HCT116 colon carcinoma cells. Mol Cancer Ther 3: 613-619, 2004.
40. Kim K, Takimoto R, Dicker DT, Chen Y, Gazitt Y and El-Deiry WS: Enhanced TRAIL sensitivity by p53 overexpression in human cancer but not normal cell lines. Int J Oncol 18: 241-247, 2001.
41. Wu GS, Kim K and El-Deiry WS: KILLER/DR5, a novel DNA-damage inducible death receptor gene, links the p53-tumor suppressor to caspase activation and apoptotic death. Adv Exp Med Biol 465: 143-151, 2000.
42. Gliniak B and Le T: Tumor necrosis factor-related apoptosisinducing ligand's antitumor activity in vivo is enhanced by the chemotherapeutic agent CPT-11. Cancer Res 59: 6153-6158, 1999.
43. Kelley SK and Ashkenazi A: Targeting death receptors in cancer with Apo2L/TRAIL. Curr Opin Pharmacol 4: 333-339, 2004.
44. Ravi R, Jain AJ, Schulick RD, Pham V, Prouser TS, Allen H, Mayer EG, Yu H, Pardoll DM, Ashkenazi A and Bedi A: Elimination of hepatic metastases of colon cancer cells via p53- independent cross-talk between irinotecan and Apo2 ligand/ TRAIL. Cancer Res 64: 9105-9114, 2004. (Pubitemid 39665525)
45. Van Oosten RL, Moore JM, Karacay B and Griffith TS: Histone deacetylase inhibitors modulate renal cell carcinoma sensitivity to TRAIL/Apo-2L-induced apoptosis by enhancing TRAIL-R2 expression. Cancer Biol Ther 4: 1104-1112, 2005.
46. Moll UM, Wolff S, Speidel D and Deppert W: Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 17: 631-636, 2005.
47. Garcia-Morales P, Gomez-Martinez A, Carrato A, Martinez- Lacaci I, Barbera VM, Soto JL, Carrasco-Garcia E, Menendez- Gutierrez MP, Castro-Galache MD, Ferragut JA and Saceda M: Histone deacetylase inhibitors induced caspase-independent apoptosis in human pancreatic adenocarcinoma cell lines. Mol Cancer Ther 4: 1222-1230, 2005.
48. Bolden JE, Peartm MJ and Johnstone RW: Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 5: 769-784, 2006.
49. Chiba T, Yokosuka O, Fukai K, Kojima H, Tada M, Arai M, Imazeki F and Saisho H: Cell growth inhibition and gene expression induced by the histone deacetylase inhibitor, trichostatin A, on human hepatoma cells. Oncology 66: 481-491, 2004.
50. Zigrino P, Loffek S and Mauch C: Tumor-stroma interactions: their role in the control of tumor cell invasion. Biochimie 87: 321-328, 2005. (Pubitemid 40387611)
51. Bouralexis S, Findlay DM and Evdokiou A: Death to the bad guys: targeting cancer via Apo2L/TRAIL. Apoptosis 10: 35-51, 2005.
52. Vinyals A, Peinado MA, Gonzalez-Garrigues M, Monzo M, Bonfil RD and Fabra A: Failure of wild-type p53 gene therapy in human cancer cells expressing a mutant p53 protein. Gene Ther 6: 22-33, 1999.