Synergistic activity of histone deacetylase and proteasome inhibition against pancreatic and hepatocellular cancer cell lines

Anticancer Research

Volumn 31, Issue 4, 2011, Pages 1093-1103

  Spratlin, Jennifer L ^a,c   Pitts, T M ^a   Kulikowski, G N ^a   Morelli, M P ^a   Tentler, J J ^a   Serkova, N J ^b   Eckhardt, S G ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Apoptosis; Belinostat; Bortezomib; Hepatocellular cancer; Histone deacetylase inhibitor; Metabolomics; Pancreas cancer; Proteasome inhibitor

Indexed keywords

BELINOSTAT; BORTEZOMIB; CASPASE 3; CASPASE 7; HISTONE DEACETYLASE; HISTONE H3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEASOME; PROTEIN P21; SULFORHODAMINE B;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENCY; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME INHIBITION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIVER CELL CARCINOMA; METABOLOMICS; NUCLEAR MAGNETIC RESONANCE; PANCREAS CANCER; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; UPREGULATION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BORONIC ACIDS; CARCINOMA, HEPATOCELLULAR; CASPASE 3; CELL LINE, TUMOR; DRUG SYNERGISM; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; IMMUNOBLOTTING; LIVER NEOPLASMS; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOMICS; PANCREATIC NEOPLASMS; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES;

EID: 79956071947     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J and Thun MJ: Cancer statistics, 2009. CA Cancer J Clin 59: 225-249, 2009.
2. Burris HA 3rd, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, Cripps MC, Portenoy RK, Storniolo AM, Tarassoff P, Nelson R, Dorr FA, Stephens CD and Von Hoff DD: 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: 2403-2413, 1997. (Pubitemid 27251144)
3. Moore MJ, Goldstein D, Hamm J, Figer A, Hecht JR, Gallinger S, Au HJ, Murawa P, Walde D, Wolff RA, Campos D, Lim R, Ding K, Clark G, Voskoglou-Nomikos T, Ptasynski M and Parulekar W: Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 25: 1960-1966, 2007.
4. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc J F, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Haussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D and Bruix J: Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359: 378-390, 2008.
5. Monneret C: Histone deacetylase inhibitors for epigenetic therapy of cancer. Anticancer Drugs 18: 363-370, 2007.
6. Mehnert JM and Kelly WK: Histone deacetylase inhibitors: biology and mechanism of action. Cancer J 13: 23-29, 2007.
7. Marks PA, Richon VM, Breslow R and Rifkind RA: Histone deacetylase inhibitors as new cancer drugs. Curr Opin Oncol 13: 477-483, 2001. (Pubitemid 33027900)
8. Wang J, Saunthararajah Y, Redner RL and Liu JM: Inhibitors of histone deacetylase relieve ETO-mediated repression and induce differentiation of AML1-ETO leukemia cells. Cancer Res 59: 2766-2769, 1999. (Pubitemid 29283104)
9. Borrow J, Stanton VP Jr., Andresen JM, Becher R, Behm FG, Chaganti RS, Civin CI, Disteche C, Dube I, Frischauf AM, Horsman D, Mitelman F, Volinia S, Watmore AE and Housman DE: The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nat Genet 14: 33-41, 1996.
10. Johnstone RW: Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat Rev Drug Discov 1: 287-299, 2002.
11. Xu WS, Parmigiani RB and Marks PA: Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26: 5541-5552, 2007.
12. Mann BS, Johnson JR, Cohen MH, Justice R and Pazdur R: FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12: 1247-1252, 2007. (Pubitemid 350106355)
13. Glaser KB: HDAC inhibitors: clinical update and mechanism-based potential. Biochem Pharmacol 74: 659-671, 2007.
14. Odenike O, Green M, Larson R, Rich E, Ott J, Ratain M and Stock W: Phase I study of belinostat (PXD101) plus azacitidine (AZC) in patients with advanced myeloid neoplasms. J Clin Oncol 26, 2008.
15. Mackay H, Hirte HW, Covens A, MacAlpine K, Wang L, Tsao MS, Pan J, Zwiebel JA and Oza AM: A phase II trial of the histone deacetylase inhibitor belinostat (PXD101) in patients with platinum resistant epithelial ovarian tumors and micropapillary/borderline (LMP) ovarian tumors. A PMH phase II consortium trial. J Clin Oncol 26, 2008.
16. Kelly WK, Yap T, Lee J, Lassen U, Crowley E, Clarke A, Hawthorne T, Buhl-Jensen P and Bono JD: A phase I study of oral belinostat (PXD101) in patients with advanced solid tumors. J Clin Oncol 25: 14092, 2007.
17. Yeo W, Lim R, MA BB, Hui P, Chan L, Mo FK, Yu SC, Ho SS, Koh J, Chan AT and Goh B: A phase I/II study of belinostat (PXD101) in patients with unresectable hepatocellular carcinoma. J Clinical Oncol 25: 15081, 2007.
18. Sinha R, Moliffe R, Scurr M, Vidal L, Engelholm SA, Jensen PB, Normann A, Li S, Bono JD and Lassen U: A phase I/II study of the safety and anticancer activity of IV-administered belinostat (PXD101) plus carboplatin (C) or paclitaxel (P), or both in patients with advanced solid tumors. J Clinical Oncol 25: 3574, 2007.
19. O'Bryant C, Leong S, Camidge D, Gore L, Diab S, Call J, Spratlin J, Zwiebel J and Eckhardt SG: A phase 1 study of belinostat (PXD101) in combination with bortezomib in patients with advanced solid tumors and lymphoma. In: Proceedings of Annual AACR Meeting, San Francisco, California, 2007.
20. Milano A, Iaffaioli RV and Caponigro F: The proteasome: a worthwhile target for the treatment of solid tumours? Eur J Cancer 43: 1125-1133, 2007.
21. Landis-Piwowar KR, Milacic V, Chen D, Yang H, Zhao Y, Chan TH, Yan B and Dou QP: The proteasome as a potential target for novel anticancer drugs and chemosensitizers. Drug Resist Updat 9: 263-273, 2006. (Pubitemid 46357634)
22. Boccadoro M, Morgan G and Cavenagh J: Preclinical evaluation of the proteasome inhibitor bortezomib in cancer therapy. Cancer Cell Int 5: 18, 2005.
23. Papazisis KT, Geromichalos GD, Dimitriadis KA and Kortsaris AH: Optimization of the sulforhodamine B colorimetric assay. J Immunol Methods 208: 151-158, 1997. (Pubitemid 28015342)
24. Chou TC and Talalay P: Analysis of combined drug effects: A new look at a very old problem. Trends Pharmacol Sci 4: 450-454, 1983.
25. Serkova NJ and Glunde K: Metabolomics of cancer. Methods Mol Biol 520: 273-295, 2009.
26. Kominsky DJ, Klawitter J, Brown JL, Boros LG, Melo JV, Eckhardt SG and Serkova NJ: Abnormalities in glucose uptake and metabolism in imatinib-resistant human BCR-ABL-positive cells. Clin Cancer Res 15: 3442-3450, 2009.
27. Klawitter J, Kominsky DJ, Brown JL, Klawitter J, Christians U, Leibfritz D, Melo JV, Eckhardt SG and Serkova NJ: Metabolic characteristics of imatinib resistance in chronic myeloid leukaemia cells. Br J Pharmacol 158: 588-600, 2009.
28. Serkova NJ, Christians U and Benet LZ: Biochemical mechanisms of cyclosporine neurotoxicity. Mol Interv 4: 97-107, 2004.
29. Pitts TM, Morrow M, Kaufman SA, Tender JJ and Eckhardt SG: Vorinostat and bortezomib exert synergistic antiproliferative and proapoptotic effects in colon cancer cell models. Mol Cancer Ther 8: 342-349, 2009.
30. Villar-Garea A and Esteller M: Histone deacetylase inhibitors: understanding a new wave of anticancer agents. Int J Cancer 112: 171-178, 2004. (Pubitemid 39244355)
31. Dokmanovic M and Marks PA: Prospects: histone deacetylase inhibitors. J Cell Biochem 96: 293-304, 2005.
32. Lin HY, Chen CS, Lin SP, Weng JR and Chen CS: Targeting histone deacetylase in cancer therapy. Med Res Rev 26: 397-413, 2006.
33. Liu T, Kuljaca S, Tee A and Marshall GM: Histone deacetylase inhibitors: multifunctional anticancer agents. Cancer Treat Rev 32: 157-165, 2006.
34. Marks PA, Richon VM, Kelly WK, Chiao JH and Miller T: Histone deacetylase inhibitors: development as cancer therapy. Novartis Found Symp 259: 269-281; discussion 281-268, 2004.
35. Amiri KI, Horton LW, LaFleur BJ, Sosman JA and Richmond A: Augmenting chemosensitivity of malignant melanoma tumors via proteasome inhibition: implication for bortezomib (VELCADE, PS-341) as a therapeutic agent for malignant melanoma. Cancer Res 64: 4912-4918, 2004. (Pubitemid 38924537)
36. Teicher BA, Ara G, Herbst R, Palombella VJ and Adams J: The proteasome inhibitor PS-341 in cancer therapy. Clin Cancer Res 5: 2638-2645, 1999. (Pubitemid 29437352)
37. Williams S, Pettaway C, Song R, Papandreou C, Logothetis C and McConkey DJ: Differential effects of the proteasome inhibitor bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther 2: 835-843, 2003.
38. Adams J, Palombella VJ, Sausville EA, Johnson J, Destree A, Lazarus DD, Maas J, Pien CS, Prakash S and Elliott PJ: Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res 59: 2615-2622, 1999. (Pubitemid 29269108)
39. Satou Y, Nosaka K, Koya Y, Yasunaga JI, Toyokuni S and Matsuoka M: Proteasome inhibitor, bortezomib, potently inhibits the growth of adult T-cell leukemia cells both in vivo and in vitro. Leukemia 18: 1357-1363, 2004. (Pubitemid 39136745)
40. Tan C and Waldmann TA: Proteasome inhibitor PS-341, a potential therapeutic agent for adult T-cell leukemia. Cancer Res 62: 1083-1086, 2002. (Pubitemid 34160291)
41. Cusack JC Jr., Liu R, Houston M, Abendroth K, Elliott PJ, Adams J and Baldwin AS Jr.: Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition. Cancer Res 61: 3535-3540, 2001.
42. Bae SH, Ryoo HM, Kim MK, Lee KH, Sin JI and Hyun MS: Effects of the proteasome inhibitor bortezomib alone and in combination with chemotherapeutic agents in gastric cancer cell lines. Oncol Rep 19: 1027-1032, 2008. (Pubitemid 351802676)
43. Wagenblast J, Hambek M, Baghi M, Gstottner W, Strebhardt K, Ackermann H and Knecht R: Antiproliferative activity of bortezomib alone and in combination with cisplatin or docetaxel in head and neck squamous cell carcinoma cell lines. J Cancer Res Clin Oncol 134: 323-330, 2008. (Pubitemid 351170053)
44. Jung CS, Zhou Z, Khuri FR and Sun SY: Assessment of apoptosis-inducing effects of docetaxel combined with the proteasome inhibitor PS-341 in human lung cancer cells. Cancer Biol Ther 6: 749-754, 2007. (Pubitemid 47328357)
45. Glaser KB, Staver MJ, Waring JF, Stender J, Ulrich RG and Davidsen SK: 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: 151-163, 2003.
46. Yin D, Ong JM, Hu J, Desmond JC, Kawamata N, Konda BM, Black KL and Koeffler HP: Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 13: 1045-1052, 2007. (Pubitemid 46340384)
47. Kumagai T, Wakimoto N, Yin D, Gery S, Kawamata N, Takai N, Komatsu N, Chumakov A, Imai Y and Koeffler HP: Histone deacetylase inhibitor, suberoylanilide hydroxamic acid (Vorinostat, SAHA) profoundly inhibits the growth of human pancreatic cancer cells. Int J Cancer 121: 656-665, 2007. (Pubitemid 46986501)
48. Rajkumar SV, Richardson PG, Hideshima T and Anderson KC: Proteasome inhibition as a novel therapeutic target in human cancer. J Clin Oncol 23: 630-639, 2005. (Pubitemid 46224241)
49. Buckley MT, Yoon J, Yee H, Chiriboga L, Liebes L, Ara G, Qian X, Bajorin DF, Sun TT, Wu XR and Osman I: The histone deacetylase inhibitor belinostat (PXD101) suppresses bladder cancer cell growth in vitro and in vivo. J Transi Med 5: 49, 2007.
50. Qian X, Ara G, Mills E, LaRochelle WJ, Lichenstein HS and Jeffers M: Activity of the histone deacetylase inhibitor belinostat (PXD101) in preclinical models of prostate cancer. Int J Cancer 122: 1400-1410, 2008. (Pubitemid 351287242)
51. Plumb JA, Finn PW, Williams RJ, Bandara MJ, Romero MR, Watkins CJ, La Thangue NB and Brown R: Pharmacodynamic response and inhibition of growth of human tumor xenografts by the novel histone deacetylase inhibitor PXD101. Mol Cancer Ther 2: 721-728, 2003.
52. Qian X, LaRochelle WJ, Ara G, Wu F, Petersen KD, Thougaard A, Sehested M, Lichenstein HS and Jeffers M: Activity of PXD101, a histone deacetylase inhibitor, in preclinical ovarian cancer studies. Mol Cancer Ther 5: 2086-2095, 2006. (Pubitemid 44336581)
53. + immature phenotype. Haematologica 93: 57-66, 2008. (Pubitemid 351156152)
54. Servida F, Soligo D, Delia D, Henderson C, Brancolini C, Lombardi L and Deliliers GL: Sensitivity of human multiple myelomas and myeloid leukemias to the proteasome inhibitor I. Leukemia 19: 2324-2331, 2005. (Pubitemid 41741629)
55. Dai Y, Chen S, Kramer LB, Funk VL, Dent P and Grant S: Interactions between bortezomib and romidepsin and belinostat in chronic lymphocytic leukemia cells. Clin Cancer Res 14: 549-558, 2008.
56. Feng R, Oton A, Mapara MY, Anderson G, Belani C and Lentzsch S: The histone deacetylase inhibitor, PXD101, potentiates bortezomib-induced anti-multiple myeloma effect by induction of oxidative stress and DNA damage. Br J Haematol 139: 385-397, 2007. (Pubitemid 47512171)
57. Heider U, von Metzler I, Kaiser M, Rosche M, Sterz J, Rotzer S, Rademacher J, Jakob C, Fleissner C, Kuckelkorn U, Kloetzel PM and Sezer O: Synergistic interaction of the histone deacetylase inhibitor SAHA with the proteasome inhibitor bortezomib in mantle cell lymphoma. Eur J Haematol 80: 133-142, 2008.
58. Baradari V, Hopfner M, Huether A, Schuppan D and Scherubl H: Histone deacetylase inhibitor MS-275 alone or combined with bortezomib or sorafenib exhibits strong antiproliferative action in human cholangiocarcinoma cells. World J Gastroenterol 13: 4458-4466, 2007. (Pubitemid 47412408)
59. Del Bello B, Valentini MA, Mangiavacchi P, Comporti M and Maellaro E: Role of caspases-3 and -7 in Apaf-1 proteolytic cleavage and degradation events during cisplatin-induced apoptosis in melanoma cells. Exp Cell Res 293: 302-310, 2004. (Pubitemid 38083220)
60. Janicke RU, Ng P, Sprengart ML and Porter AG: Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem 273: 15540-15545, 1998.
61. Lee JS, Chu IS, Heo J, Calvisi DF, Sun Z, Roskams T, Durnez A, Demetris AJ and Thorgeirsson SS: Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 40: 667-676, 2004. (Pubitemid 39265589)
62. Tischoff I and Tannapfe A: DNA methylation in hepatocellular carcinoma. World J Gastroenterol 14: 1741-1748, 2008.
63. Tai DI, Tsai SL, Chang YH, Huang SN, Chen TC, Chang KS and Liaw YF: Constitutive activation of nuclear factor kappaB in hepatocellular carcinoma. Cancer 89: 2274-2281, 2000.
64. Rayet B and Gelinas C: Aberrant REL/NFKB genes and activity in human cancer. Oncogene 18: 6938-6947, 1999.
65. Dolcet X, Llobet D, Encinas M, Pallares J, Cabero A, Schoenenberger JA, Comella JX and Matias-Guiu X: Proteasome inhibitors induce death but activate NF-kappaB on endometrial carcinoma cell lines and primary culture explants. J Biol Chem 281: 22118-22130, 2006. (Pubitemid 44181916)
66. Spratlin JL, Serkova NJ and Eckhardt SG: Clinical applications of metabolomics in oncology: a review. Clin Cancer Res 15: 431-440, 2009.
67. Serkova NJ, Spratlin JL and Eckhardt SG: NMR-based metabolomics: translational application and treatment of cancer. Curr Opin Mol Ther 9: 572-585, 2007. (Pubitemid 350179097)
68. Marin S, Lee WN, Bassilian S, Lim S, Boros LG, Centelles JJ, FernAndez-Novell JM, Guinovart JJ and Cascante M: Dynamic profiling of the glucose metabolic network in fasted rat hepatocytes using [1,2-13C2]glucose. Biochem J 381: 287-294, 2004. (Pubitemid 38932235)