Gene expression profiling after treatment with the histone deacetylase inhibitor trichostatin A reveals altered expression of both pro- and anti-apoptotic genes in pancreatic adenocarcinoma cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1693, Issue 3, 2004, Pages 167-176

  Moore, Patrick S ^a   Barbi, Stefano ^a   Donadelli, Massimo ^b   Costanzo, Chiara ^b   Bassi, Claudio ^a   Palmieri, Marta ^b   Scarpa, Aldo ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b Section of Biochemistry   (Italy)

Author keywords

Expression profiling; Pancreatic cancer; Trichostatin A

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; PROTEIN BCL W; PROTEIN BCL XL; TRICHOSTATIN A;

APOPTOSIS; ARTICLE; BCL W GENE; BCL XL GENE; BINDING SITE; CANCER CELL CULTURE; CELL FUNCTION; CELL LINE; CELL PROLIFERATION; CELL RESPIRATION; DOWN REGULATION; DRUG EFFECT; GENE; GENE CONTROL; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; MAXIMUM ALLOWABLE CONCENTRATION; PANCREAS ADENOCARCINOMA; PANCREAS CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

ADENOCARCINOMA; APOPTOSIS; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; PANCREATIC NEOPLASMS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR CELLS, CULTURED;

EID: 4444223456     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2004.07.001     Document Type: Article

References (62)

1. E. Rozenblum, M. Schutte, M. Goggins, S.A. Hahn, S. Panzer, M. Zahurak, S.N. Goodman, T.A. Sohn, R.H. Hruban, C.J. Yeo, and S.E. Kern Tumor-suppressive pathways in pancreatic carcinoma Cancer Res. 57 1997 1731 1734
2. P.S. Moore, S. Orlandini, G. Zamboni, P. Capelli, G. Rigaud, M. Falconi, C. Bassi, N.R. Lemoine, and A. Scarpa Pancreatic tumours: molecular pathways implicated in ductal cancer are involved in ampullary but not in exocrine nonductal or endocrine tumorigenesis Br. J. Cancer 84 2001 253 262
3. C. Sorio, A. Baron, S. Orlandini, G. Zamboni, P. Pederzoli, K. Huebner, and A. Scarpa The FHIT gene is expressed in pancreatic ductular cells and is altered in pancreatic cancers Cancer Res. 59 1999 1308 1314
4. J.R. Dobosy, and E.U. Selker Emerging connections between DNA methylation and histone acetylation Cell. Mol. Life Sci. 58 2001 721 727
5. G. Leone, L. Teofili, M.T. Voso, and M. Lubbert DNA methylation and demethylating drugs in myelodysplastic syndromes and secondary leukemias Haematologica 87 2002 1324 1341
6. A. Aparicio, and J.S. Weber Review of the clinical experience with 5-azacytidine and 5-aza-2′ -deoxycytidine in solid tumors Curr. Opin. Investig. Drugs 3 2002 627 633
7. V.M. Richon, T.W. Sandhoff, R.A. Rifkind, and P.A. Marks Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation Proc. Natl. Acad. Sci. U. S. A. 97 2000 10014 10019
8. U. Dressel, R. Renkawitz, and A. Baniahmad Promoter specific sensitivity to inhibition of histone deacetylases: implications for hormonal gene control, cellular differentiation and cancer Anticancer Res. 20 2000 1017 1022
9. B. Eickhoff, L. Germeroth, C. Stahl, G. Kohler, S. Ruller, M. Schlaak, and J. van der Bosch Trichostatin A-mediated regulation of gene expression and protein kinase activities: reprogramming tumor cells for ribotoxic stress-induced apoptosis Biol. Chem. 381 2000 1127 1132
10. M. Muraoka, M. Konishi, R. Kikuchi-Yanoshita, K. Tanaka, N. Shitara, J.M. Chong, T. Iwama, and M. Miyaki p300 gene alterations in colorectal and gastric carcinomas Oncogene 12 1996 1565 1569
11. R.W. Johnstone Histone-deacetylase inhibitors: novel drugs for the treatment of cancer Nat. Rev., Drug Discov. 1 2002 287 299
12. W.K. Kelly, O.A. O'Connor, and P.A. Marks Histone deacetylase inhibitors: from target to clinical trials Expert Opin. Investig. Drugs 11 2002 1695 1713
13. U.H. Weidle, and A. Grossmann Inhibition of histone deacetylases: a new strategy to target epigenetic modifications for anticancer treatment Anticancer Res. 20 2000 1471 1485
14. M. Donadelli, C. Costanzo, L. Faggioli, M.T. Scupoli, P.S. Moore, C. Bassi, A. Scarpa, and M. Palmieri Trichostatin A, an inhibitor of histone deacetylases, strongly suppresses growth of pancreatic adenocarcinoma cells Mol. Carcinog. 38 2003 59 69
15. A. Batova, L.E. Shao, M.B. Diccianni, A.L. Yu, T. Tanaka, A. Rephaeli, A. Nudelman, and J. Yu The histone deacetylase inhibitor AN-9 has selective toxicity to acute leukemia and drug-resistant primary leukemia and cancer cell lines Blood 100 2002 3319 3324
16. M. Fournel, M.C. Trachy-Bourget, P.T. Yan, A. Kalita, C. Bonfils, C. Beaulieu, S. Frechette, S. Leit, E. Abou-Khalil, S.H. Woo, D. Delorme, A.R. MacLeod, J.M. Besterman, and Z. Li Sulfonamide anilides, a novel class of histone deacetylase inhibitors, are antiproliferative against human tumors Cancer Res. 62 2002 4325 4330
17. D.M. Vigushin, S. Ali, P.E. Pace, N. Mirsaidi, K. Ito, I. Adcock, and R.C. Coombes Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo Clin. Cancer Res. 7 2001 971 976
18. C. Nervi, U. Borello, F. Fazi, V. Buffa, P.G. Pelicci, and G. Cossu Inhibition of histone deacetylase activity by trichostatin A modulates gene expression during mouse embryogenesis without apparent toxicity Cancer Res. 61 2001 1247 1249
19. D.D. Von Hoff, and D. Bearss New drugs for patients with pancreatic cancer Curr. Opin. Oncol. 14 2002 621 627
20. S.A. Rummel, A.J. Kraker, R.W. Steinkampf, K.E. Hook, and W.D. Klohs Role of a small molecular weight phosphoprotein in the mechanism of action of CI-994 (N-acetyldinaline) Int. J. Cancer 62 1995 636 642
21. M.J. Peart, K.M. Tainton, A.A. Ruefli, A.E. Dear, K.A. Sedelies, L.A. O'Reilly, N.J. Waterhouse, J.A. Trapani, and R.W. Johnstone Novel mechanisms of apoptosis induced by histone deacetylase inhibitors Cancer Res. 63 2003 4460 4471
22. K.B. Glaser, M.J. Staver, J.F. Waring, J. Stender, R.G. Ulrich, and S.K. Davidsen Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines Mol. Cancer Ther. 2 2003 151 163
23. C. Van Lint The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation Gene Expr. 5 1996 245 253
24. H. Suzuki, E. Gabrielson, W. Chen, R. Anbazhagan, M. van Engel, M.P. Weijenberg, J.G. Herman, and S.B. Baylin A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer Nat. Genet. 31 2002 141 149
25. N. Sato, N. Fukushima, A. Maitra, H. Matsubayashi, C.J. Yeo, J.L. Cameron, R.H. Hruban, and M. Goggins Discovery of novel targets for aberrant methylation in pancreatic carcinoma using high-throughput microarrays Cancer Res. 63 2003 3735 3742
26. J.M. Mariadason, G.A. Corner, and L.H. Augenlicht Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer Cancer Res. 60 2000 4561 4572
27. P. Moore, B. Sipos, S. Orlandini, C. Sorio, F. Real, N. Lemoine, T. Gress, C. Bassi, K. G, H. Kalthoff, H. Ungefroren, M. Lühr, and A. Scarpa Genetic profile of 22 pancreatic carcinoma cell lines: analysis of K-ras, p53, p16 and DPC4/Smad4 Virchows Arch. 439 2001 798 802
28. G. Liu, A.E. Loraine, R. Shigeta, M. Cline, J. Cheng, V. Valmeekam, S. Sun, D. Kulp, and M.A. Siani-Rose NetAffx: affymetrix probesets and annotations Nucleic Acids Res. 31 2003 82 86
29. T. Hubbard, D. Barker, E. Birney, G. Cameron, Y. Chen, L. Clark, T. Cox, J. Cuff, V. Curwen, T. Down, R. Durbin, E. Eyras, J. Gilbert, M. Hammond, L. Huminiecki, A. Kasprzyk, H. Lehvaslaiho, P. Lijnzaad, C. Melsopp, E. Mongin, R. Pettett, M. Pocock, S. Potter, A. Rust, E. Schmidt, S. Searle, G. Slater, J. Smith, W. Spooner, A. Stabenau, J. Stalker, E. Stupka, A. Ureta-Vidal, I. Vastrik, and M. Clamp The Ensembl genome database project Nucleic Acids Res. 30 2002 38 41
30. K. Quandt, K. Frech, H. Karas, E. Wingender, and T. Werner MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data Nucleic Acids Res. 23 1995 4878 4884
31. E. Wingender, P. Dietze, H. Karas, and R. Knuppel TRANSFAC: a database on transcription factors and their DNA binding sites Nucleic Acids Res. 24 1996 238 241
32. L.M. Butler, D.B. Agus, H.I. Scher, B. Higgins, A. Rose, C. Cordon-Cardo, H.T. Thaler, R.A. Rifkind, P.A. Marks, and V.M. Richon Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo Cancer Res. 60 2000 5165 5170
33. Z. Hodny, R. Li, P. Barath, and B.D. Nelson Sp1 and chromatin environment are important contributors to the formation of repressive chromatin structures on the transfected human adenine nucleotide translocase-2 promoter Biochem. J. 346 Pt 1 2000 93 97
34. L. Huang, Y. Sowa, T. Sakai, and A.B. Pardee Activation of the p21WAF1/CIP1 promoter independent of p53 by the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) through the Sp1 sites Oncogene 19 2000 5712 5719
35. G.E. Walker, E.M. Wilson, D. Powell, and Y. Oh Butyrate, a histone deacetylase inhibitor, activates the human IGF binding protein-3 promoter in breast cancer cells: molecular mechanism involves an Sp1/Sp3 multiprotein complex Endocrinology 142 2001 3817 3827
36. J. Yang, Y. Kawai, R.W. Hanson, and I.J. Arinze Sodium butyrate induces transcription from the G alpha(i2) gene promoter through multiple Sp1 sites in the promoter and by activating the MEK-ERK signal transduction pathway J. Biol. Chem. 276 2001 25742 25752
37. A.J. de Ruijter, A.H. van Gennip, H.N. Caron, S. Kemp, and A.B. van Kuilenburg Histone deacetylases (HDACs): characterization of the classical HDAC family Biochem. J. 370 2003 737 749
38. P.A. Wade, and A.P. Wolffe Histone acetyltransferases in control Curr. Biol. 7 1997 R82 R84
39. Y. Zhang, G. LeRoy, H.P. Seelig, W.S. Lane, and D. Reinberg The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities Cell 95 1998 279 289
40. H. Xiao, T. Hasegawa, and K. Isobe p300 collaborates with Sp1 and Sp3 in p21(waf1/cip1) promoter activation induced by histone deacetylase inhibitor J. Biol. Chem. 275 2000 1371 1376
41. A. Doetzlhofer, H. Rotheneder, G. Lagger, M. Koranda, V. Kurtev, G. Brosch, E. Wintersberger, and C. Seiser Histone deacetylase 1 can repress transcription by binding to Sp1 Mol. Cell. Biol. 19 1999 5504 5511
42. J. Won, J. Yim, and T.K. Kim Sp1 and Sp3 recruit histone deacetylase to repress transcription of human telomerase reverse transcriptase (hTERT) promoter in normal human somatic cells J. Biol. Chem. 277 2002 38230 38238
43. S. Ammanamanchi, J.W. Freeman, and M.G. Brattain Acetylated sp3 is a transcriptional activator J. Biol. Chem. 278 2003 35775 35780
44. Z.Y. Huang, Y. Wu, N. Hedrick, and D.H. Gutmann T-cadherin-mediated cell growth regulation involves G2 phase arrest and requires p21(CIP1/WAF1) expression Mol. Cell. Biol. 23 2003 566 578
45. V. Della Valle, D. Duro, O. Bernard, and C.J. Larsen The human protein p19ARF is not detected in hemopoietic human cell lines that abundantly express the alternative beta transcript of the p16INK4a/MTS1 gene Oncogene 15 1997 2475 2481
46. K. Tsuji, K. Mizumoto, H. Sudo, K. Kouyama, E. Ogata, and M. Matsuoka p53-independent apoptosis is induced by the p19ARF tumor suppressor Biochem. Biophys. Res. Commun. 295 2002 621 629
47. Y. Hashimoto, K. Kohri, Y. Kaneko, H. Morisaki, T. Kato, K. Ikeda, and M. Nakanishi Critical role for the 310 helix region of p57(Kip2) in cyclin-dependent kinase 2 inhibition and growth suppression J. Biol. Chem. 273 1998 16544 16550
48. F. Baus, V. Gire, D. Fisher, J. Piette, and V. Dulic Permanent cell cycle exit in G2 phase after DNA damage in normal human fibroblasts EMBO J. 22 2003 3992 4002
49. M. Kasten, and A. Giordano Cdk10, a Cdc2-related kinase, associates with the Ets2 transcription factor and modulates its transactivation activity Oncogene 20 2001 1832 1838
50. L. O'Connor, A. Strasser, L.A. O'Reilly, G. Hausmann, J.M. Adams, S. Cory, and D.C. Huang Bim: a novel member of the Bcl-2 family that promotes apoptosis EMBO J. 17 1998 384 395
51. M. Marani, T. Tenev, D. Hancock, J. Downward, and N.R. Lemoine Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis Mol. Cell. Biol. 22 2002 3577 3589
52. M. Strasberg Rieber, U. Zangemeister-Wittke, and M. Rieber p53-Independent induction of apoptosis in human melanoma cells by a bcl-2/bcl-xL bispecific antisense oligonucleotide Clin. Cancer Res. 7 2001 1446 1451
53. Z. Jiang, X. Zheng, and K.M. Rich Down-regulation of Bcl-2 and Bcl-xL expression with bispecific antisense treatment in glioblastoma cell lines induce cell death J. Neurochem. 84 2003 273 281
54. S. Hopkins-Donaldson, R. Cathomas, A.P. Simoes-Wust, S. Kurtz, L. Belyanskaya, R.A. Stahel, and U. Zangemeister-Wittke Induction of apoptosis and chemosensitization of mesothelioma cells by Bcl-2 and Bcl-xL antisense treatment Int. J. Cancer 106 2003 160 166
55. H. Friess, Z. Lu, A. Andren-Sandberg, P. Berberat, A. Zimmermann, G. Adler, R. Schmid, and M.W. Buchler Moderate activation of the apoptosis inhibitor bcl-xL worsens the prognosis in pancreatic cancer Ann. Surg. 228 1998 780 787
56. A.J. Minn, C.M. Rudin, L.H. Boise, and C.B. Thompson Expression of bcl-xL can confer a multidrug resistance phenotype Blood 86 1995 1903 1910
57. Z. Xu, H. Friess, M. Solioz, S. Aebi, M. Korc, J. Kleeff, and M.W. Buchler Bcl-x(L) antisense oligonucleotides induce apoptosis and increase sensitivity of pancreatic cancer cells to gemcitabine Int. J. Cancer 94 2001 268 274
58. J.F. Mirjolet, M. Barberi-Heyob, C. Didelot, J.P. Peyrat, J. Abecassis, R. Millon, and J.L. Merlin Bcl-2/Bax protein ratio predicts 5-fluorouracil sensitivity independently of p53 status Br. J. Cancer 83 2000 1380 1386
59. D.J. Van Antwerp, S.J. Martin, I.M. Verma, and D.R. Green Inhibition of TNF-induced apoptosis by NF-kappa B Trends Cell Biol. 8 1998 107 111
60. P. Hersey, and X.D. Zhang Overcoming resistance of cancer cells to apoptosis J. Cell. Physiol. 196 2003 9 18
61. R.R. Rosato, J.A. Almenara, Y. Dai, and S. Grant 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 2003 1273 1284
62. S. Janjua, A. Stephanou, and D.S. Latchman The C-terminal activation domain of the STAT-1 transcription factor is necessary and sufficient for stress-induced apoptosis Cell Death Differ. 9 2002 1140 1146