Synergistic inhibition of pancreatic adenocarcinoma cell growth by trichostatin A and gemcitabine

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 7, 2007, Pages 1095-1106

  Donadelli, Massimo ^a   Costanzo, Chiara ^a   Beghelli, Stefania ^a   Scupoli, Maria Teresa ^a   Dandrea, Mario ^a   Bonora, Antonio ^a   Piacentini, Paolo ^a   Budillon, Alfredo ^b   Caraglia, Michele ^b   Scarpa, Aldo ^a   Palmieri, Marta ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Apoptosis; Gemcitabine; Oxidative stress; Pancreatic cancer; RNA interference; Trichostatin A

Indexed keywords

5' NUCLEOTIDASE; ACETYLCYSTEINE; BIM PROTEIN; CYTIDINE DEAMINASE; DEOXYCYTIDINE KINASE; GEMCITABINE; HISTONE DEACETYLASE; NUCLEOTIDE TRANSPORTER; REACTIVE OXYGEN METABOLITE; RIBONUCLEOTIDE REDUCTASE; SCAVENGER; TRICHOSTATIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER RESISTANCE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; DRUG EFFICACY; DRUG POTENTIATION; DRUG SENSITIVITY; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO CULTURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA INTERFERENCE; TUMOR VOLUME; TUMOR XENOGRAFT;

5'-NUCLEOTIDASE; ADENOCARCINOMA; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DEOXYCYTIDINE; ENZYME INHIBITORS; GLYCOPROTEINS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; MEMBRANE PROTEINS; MICE; PANCREATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; REACTIVE OXYGEN SPECIES;

MUS MUSCULUS;

EID: 34250200750     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.05.002     Document Type: Article

References (44)

1. Li D., Xie K., Wolff R., and Abbruzzese J.L. Pancreatic cancer. Lancet 363 (2004) 1049-1057
2. Neoptolemos J.P., Cunningham D., Friess H., Bassi C., Stocken D.D., Tait D.M., Dunn J.A., Dervenis C., Lacaine F., Hickey H., Raraty M.G., Ghaneh P., and Buchler M.W. Adjuvant therapy in pancreatic cancer: historical and current perspectives. Ann. Oncol. 14 (2003) 675-692
3. Haller D.G. New perspectives in the management of pancreas cancer. Semin. Oncol. 30 (2003) 3-10
4. Burris III H.A., Moore M.J., Andersen J., Green M.R., Rothenberg M.L., Modiano M.R., Cripps M.C., Portenoy R.K., Storniolo A.M., Tarassoff P., Nelson R., Dorr F.A., Stephens C.D., and Von Hoff D.D. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J. Clin. Oncol. 15 (1997) 2403-2413
5. Clarke M.L., Mackey J.R., Baldwin S.A., Young J.D., and Cass C.E. The role of membrane transporters in cellular resistance to anticancer nucleoside drugs. Cancer Treat. Res. 112 (2002) 27-47
6. Ruiz van Haperen V.W., Veerman G., Eriksson S., Stegmann A.P., and Peters G.J. Induction of resistance to 2′,2′-difluorodeoxycytidine in the human ovarian cancer cell line A2780. Semin. Oncol. 22 (1995) 35-41
7. Neff T., and Blau C.A. Forced expression of cytidine deaminase confers resistance to cytosine arabinoside and gemcitabine. Exp. Hematol. 24 (1996) 1340-1346
8. Dumontet C., Fabianowska-Majewska K., Mantincic D., Callet Bauchu E., Tigaud I., Gandhi V., Lepoivre M., Peters G.J., Rolland M.O., Wyczechowska D., Fang X., Gazzo S., Voorn D.A., Vanier-Viornery A., and MacKey J. Common resistance mechanisms to deoxynucleoside analogues in variants of the human erythroleukaemic line K562. Br. J. Haematol. 106 (1999) 78-85
9. Goan Y.G., Zhou B., Hu E., Mi S., and Yen Y. Overexpression of ribonucleotide reductase as a mechanism of resistance to 2,2-difluorodeoxycytidine in the human KB cancer cell line. Cancer Res. 59 (1999) 4204-4207
10. Galmarini C.M., Clarke M.L., Falette N., Puisieux A., Mackey J.R., and Dumontet C. Expression of a non-functional p53 affects the sensitivity of cancer cells to gemcitabine. Int. J. Cancer 97 (2002) 439-445
11. Moore P.S., Sipos B., Orlandini S., Sorio C., Real F.X., Lemoine N.R., Gress T., Bassi C., Kloppel G., Kalthoff H., Ungefroren H., Lohr M., and Scarpa A. Genetic profile of 22 pancreatic carcinoma cell lines. Analysis of K-ras, p53, p16 and DPC4/Smad4. Virchows Arch. 439 (2001) 798-802
12. Cascallo M., Calbo J., Gelpi J.L., and Mazo A. Modulation of drug cytotoxicity by reintroduction of wild-type p53 gene (Ad5CMV-p53) in human pancreatic cancer. Cancer Gene Ther. 7 (2000) 545-556
13. Cascallo M., Calbo J., Capella G., Fillat C., Pastor-Anglada M., and Mazo A. Enhancement of gemcitabine-induced apoptosis by restoration of p53 function in human pancreatic tumors. Oncology 68 (2005) 179-189
14. Maehara S., Tanaka S., Shimada M., Shirabe K., Saito Y., Takahashi K., and Maehara Y. Selenoprotein P, as a predictor for evaluating gemcitabine resistance in human pancreatic cancer cells. Int. J. Cancer 112 (2004) 184-189
15. Ducasse M., and Brown M.A. Epigenetic aberrations and cancer. Mol. Cancer 5 (2006) 60
16. Marks P.A., and Dokmanovic M. Histone deacetylase inhibitors: discovery and development as anticancer agents. Expert Opin. Investig. Drugs 14 (2005) 1497-1511
17. Fournel M., Trachy-Bourget M.C., Yan P.T., Kalita A., Bonfils C., Beaulieu C., Frechette S., Leit S., Abou-Khalil E., Woo S.H., Delorme D., MacLeod A.R., Besterman J.M., and Li Z. Sulfonamide anilides, a novel class of histone deacetylase inhibitors, are antiproliferative against human tumors. Cancer Res. 62 (2002) 4325-4330
18. Batova A., Shao L.E., Diccianni M.B., Yu A.L., Tanaka T., Rephaeli A., Nudelman A., and Yu J. 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
19. Nervi C., Borello U., Fazi F., Buffa V., Pelicci P.G., and Cossu G. Inhibition of histone deacetylase activity by trichostatin A modulates gene expression during mouse embryogenesis without apparent toxicity. Cancer Res. 61 (2001) 1247-1249
20. Vigushin D.M., Ali S., Pace P.E., Mirsaidi N., Ito K., Adcock I., and Coombes R.C. Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo. Clin. Cancer Res. 7 (2001) 971-976
21. Henderson C., Mizzau M., Paroni G., Maestro R., Schneider C., and Brancolini C. Role of caspases, Bid, and p53 in the apoptotic response triggered by histone deacetylase inhibitors trichostatin-A (TSA) and suberoylanilide hydroxamic acid (SAHA). J. Biol. Chem. 278 (2003) 12579-12589
22. Sawa H., Murakami H., Ohshima Y., Sugino T., Nakajyo T., Kisanuki T., Tamura Y., Satone A., Ide W., Hashimoto I., and Kamada H. Histone deacetylase inhibitors such as sodium butyrate and trichostatin A induce apoptosis through an increase of the bcl-2-related protein Bad. Brain Tumor Pathol. 18 (2001) 109-114
23. Donadelli M., Costanzo C., Faggioli L., Scupoli M.T., Moore P.S., Bassi C., Scarpa A., and Palmieri M. Trichostatin A, an inhibitor of histone deacetylases, strongly suppresses growth of pancreatic adenocarcinoma cells. Mol. Carcinog. 38 (2003) 59-69
24. Moore P.S., Barbi S., Donadelli M., Costanzo C., Bassi C., Palmieri M., and Scarpa A. 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. Biochim. Biophys. Acta 1693 (2004) 167-176
25. Zhao Y., Tan J., Zhuang L., Jiang X., Liu E.T., and Yu Q. Inhibitors of histone deacetylases target the Rb-E2F1 pathway for apoptosis induction through activation of proapoptotic protein Bim. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 16090-16095
26. Piacentini P., Donadelli M., Costanzo C., Moore P.S., Palmieri M., and Scarpa A. Trichostatin A enhances the response of chemotherapeutic agents in inhibiting pancreatic cancer cell proliferation. Virchows Arch. 448 (2006) 797-804
27. Chou T.C., and Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 22 (1984) 27-55
28. Bruzzese F., Di Gennaro E., Avallone A., Pepe S., Arra C., Caraglia M., Tagliaferri P., and Budillon A. Synergistic antitumor activity of epidermal growth factor receptor tyrosine kinase inhibitor gefitinib and IFN-alpha in head and neck cancer cells in vitro and in vivo. Clin. Cancer Res. 12 (2006) 617-625
29. Leach J.K., Van Tuyle G., Lin P.S., Schmidt-Ullrich R., and Mikkelsen R.B. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res. 61 (2001) 3894-3901
30. Puthalakath H., and Strasser A. Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ. 9 (2002) 505-512
31. Marani M., Tenev T., Hancock D., Downward J., and Lemoine N.R. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol. Cell. Biol. 22 (2002) 3577-3589
32. Pelicano H., Carney D., and Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 7 (2004) 97-110
33. Schirmer M., Stegmann A.P., Geisen F., and Konwalinka G. Lack of cross-resistance with gemcitabine and cytarabine in cladribine-resistant HL60 cells with elevated 5′-nucleotidase activity. Exp. Hematol. 26 (1998) 1223-1228
34. Schniewind B., Christgen M., Kurdow R., Haye S., Kremer B., Kalthoff H., and Ungefroren H. Resistance of pancreatic cancer to gemcitabine treatment is dependent on mitochondria-mediated apoptosis. Int. J. Cancer 109 (2004) 182-188
35. Shi X., Liu S., Kleeff J., Friess H., and Buchler M.W. Acquired resistance of pancreatic cancer cells towards 5-Fluorouracil and gemcitabine is associated with altered expression of apoptosis-regulating genes. Oncology 62 (2002) 354-362
36. Xu Z., Friess H., Solioz M., Aebi S., Korc M., Kleeff J., and Buchler M.W. Bcl-x(L) antisense oligonucleotides induce apoptosis and increase sensitivity of pancreatic cancer cells to gemcitabine. Int. J. Cancer 94 (2001) 268-274
37. Xu Z.W., Friess H., Buchler M.W., and Solioz M. Overexpression of Bax sensitizes human pancreatic cancer cells to apoptosis induced by chemotherapeutic agents. Cancer Chemother. Pharmacol. 49 (2002) 504-510
38. Chinery R., Brockman J.A., Peeler M.O., Shyr Y., Beauchamp R.D., and Coffey R.J. Antioxidants enhance the cytotoxicity of chemotherapeutic agents in colorectal cancer: a p53-independent induction of p21WAF1/CIP1 via C/EBPbeta. Nat. Med. 3 (1997) 1233-1241
39. Laurent A., Nicco C., Chereau C., Goulvestre C., Alexandre J., Alves A., Levy E., Goldwasser F., Panis Y., Soubrane O., Weill B., and Batteux F. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res. 65 (2005) 948-956
40. Ammerpohl O., Trauzold A., Schniewind B., Griep U., Pilarsky C., Grutzmann R., Saeger H.D., Janssen O., Sipos B., Kloppel G., and Kalthoff H. Complementary effects of HDAC inhibitor 4-PB on gap junction communication and cellular export mechanisms support restoration of chemosensitivity of PDAC cells. Br. J. Cancer 96 (2007) 73-81
41. Arnold N.B., Arkus N., Gunn J., and Korc M. The histone deacetylase inhibitor suberoylanilide hydroxamic acid induces growth inhibition and enhances gemcitabine-induced cell death in pancreatic cancer. Clin. Cancer Res. 13 (2007) 18-26
42. Oliani C., Padovani M., Manno P., Barana D., Falconi M., Bassi C., Cavallini G., Pederzoli P., and Cetto G.L. Gemcitabine and continuous infusion of 5-fluorouracil in locally advanced and metastatic pancreatic cancer: a phase I-II study. Anticancer Res. 24 (2004) 2107-2112
43. Berlin J.D., Catalano P., Thomas J.P., Kugler J.W., Haller D.G., and Benson III A.B. Phase III study of gemcitabine in combination with fluorouracil versus gemcitabine alone in patients with advanced pancreatic carcinoma: Eastern Cooperative Oncology Group Trial E2297. J. Clin. Oncol. 20 (2002) 3270-3275
44. Raraty M.G., Magee C.J., Ghaneh P., and Neoptolemos J.P. New techniques and agents in the adjuvant therapy of pancreatic cancer. Acta Oncol. 41 (2002) 582-595