Vorinostat and sorafenib increase CD95 activation in gastrointestinal tumor cells through a CA2+-de novo ceramide-PP2A-reactive oxygen species-dependent signaling pathway

Cancer Research

Volumn 70, Issue 15, 2010, Pages 6313-6324

  Park, Margaret A ^a   Mitchell, Clint ^a   Zhang, Guo ^a   Yacoub, Adly ^a   Allegood, Jeremy ^a   Häussinger, Dieter ^e   Reinehr, Roland ^e   Larner, Andrew ^a   Spiegel, Sarah ^a   Fisher, Paul B ^b,c   Voelkel Johnson, Christina ^d   Ogretmen, Besim ^d   Grant, Steven ^a,b   Dent, Paul ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CERAMIDE; FAS ANTIGEN; PHOSPHOPROTEIN PHOSPHATASE 2; PLACEBO; REACTIVE OXYGEN METABOLITE; SORAFENIB; SPHINGOMYELIN PHOSPHODIESTERASE; VORINOSTAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CELL KILLING; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; DRUG EFFECT; ENZYME INHIBITION; GASTROINTESTINAL TUMOR; LIVER CANCER; LOW DRUG DOSE; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RADIOSENSITIZATION; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; ANTIGENS, CD95; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BENZENESULFONATES; CALCIUM; CARBOXYLIC ESTER HYDROLASES; CELL LINE, TUMOR; CERAMIDES; GASTROINTESTINAL NEOPLASMS; HUMANS; HYDROXAMIC ACIDS; PYRIDINES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 77955393899     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0999     Document Type: Article

References (46)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
2. Bilimoria KY, Bentrem DJ, Lillemoe KD, Talamonti MS, Ko CY, Pancreatic Cancer Quality Indicator Development Expert Panel, American College of Surgeons. Assessment of pancreatic cancer care in the United States based on formally developed quality indicators. J Natl Cancer Inst 2009;101: 848-59.
3. Dent P. MAP kinase pathways in the control of hepatocyte growth, metabolism and survival. In: Dufour JF, Clavien P-A, editors. Signaling Pathways in Liver Diseases. New York: Springer Press; 2005. Chapter 19, p. 223-38.
4. Dent P, Yacoub A, Fisher PB, Hagan MP, Grant S. MAPK pathways in radiation responsesOncogene 2003;22:5885-96.
5. Valerie K, Yacoub A, Hagan MP, et al. Radiation-induced cell signaling: inside-out and outside-in. Mol Cancer Ther 2007;6: 789-801.
6. Grant S, Dent P. Kinase inhibitors and cytotoxic drug resistance. Clin Cancer Res 2004;10:2205-7.
7. Allan LA, Morrice N, Brady S, Magee G, Pathak S, Clarke PR. Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK. Nat Cell Biol 2003;5:647-54.
8. Mori M, Uchida M, Watanabe T, et al. Activation of extracellular signal-regulated kinases ERK1 and ERK2 induces Bcl-xL up-regulation via inhibition of caspase activities in erythropoietin signaling. J Cell Physiol 2003;195:290-7.
9. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ. Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J Biol Chem 2003;278:18811-6.
10. Wang YF, Jiang CC, Kiejda KA, Gillespie S, Zhang XD, Hersey P. Apoptosis induction in human melanoma cells by inhibition of MEK is caspase-independent and mediated by the Bcl-2 family members PUMA, Bim, and Mcl-1. Clin Cancer Res 2007;13: 4934-42.
11. Qiao L, Han SI, Fang Y, et al. Bile acid regulation of C/EBPaβ CREB, c-Jun function, via the extracellular signal-regulated kinase and c-Jun NH2-terminal kinase pathways, modulates the apoptotic response of hepatocytes. Mol Cell Biol 2003;23: 3052-66.
12. Li N, Batt D, Warmuth M. B-Raf kinase inhibitors for cancer treatment. Curr Opin Investig Drugs 2007;8:452-6.
13. Davies BR, Logie A, McKay JS, et al. AZD6244 (ARRY-142886), a potent inhibitor of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1/2 kinases: mechanism of action in vivo, pharmacokinetic/ pharmacodynamic relationship, and potential for combination in preclinical models. Mol Cancer Ther 2007;6:2209-19.
14. Flaherty KT. Sorafenib: delivering a targeted drug to the right targets. Expert Rev Anticancer Ther 2007;7:617-26.
15. Rini BI. Sorafenib. Expert Opin Pharmacother 2006;7:453-61.
16. Strumberg D. Preclinical and clinical development of the oral multikinase inhibitor sorafenib in cancer treatment. Drugs Today (Barc) 2005;41:773-84.
17. Gollob JA. Sorafenib: scientific rationales for single-agent and combination therapy in clear-cell renal cell carcinoma. Clin Genitourin Cancer 2005;4:167-74.
18. Rahmani M, Davis EM, Bauer C, Dent P, Grant S. Apoptosis induced by the kinase inhibitor BAY 43-9006 in human leukemia cells involves down-regulation of Mcl-1 through inhibition of translation. J Biol Chem 2005;280:35217-27.
19. Rahmani M, Nguyen TK, Dent P, Grant S. The multikinase inhibitor sorafenib induces apoptosis in highly imatinib mesylateresistant bcr/abl+ human leukemia cells in association with signal transducer and activator of transcription 5 inhibition and myeloid cell leukemia-1 down-regulation. Mol Pharmacol 2007; 72:788-95.
20. Dasmahapatra G, Yerram N, Dai Y, Dent P, Grant S. Synergistic interactions between vorinostat and sorafenib in chronic myelogenous leukemia cells involve Mcl-1 and p21CIP1 down-regulation. Clin Cancer Res 2007;13:4280-90.
21. Rahmani M, Davis EM, Crabtree TR, et al. The kinase inhibitor sorafenib induces cell death through a process involving induction of endoplasmic reticulum stress. Mol Cell Biol 2007;27:5499-513.
22. Gregory PD, Wagner K, Horz W. Histone acetylation and chromatin remodeling. Exp Cell Res 2001;265:195-202.
23. Marks PA, Miller T, Richon VM. Histone deacetylases. Curr Opin Pharmacol 2003;3:344-51.
24. Bali P, Pranpat M, Swaby R, et al. Activity of suberoylanilide hydroxamic Acid against human breast cancer cells with amplification of her-2. Clin Cancer Res 2005;11:6382-9.
25. Kwon SH, Ahn SH, Kim YK, et al. Apicidin, a histone deacetylase inhibitor, induces apoptosis and Fas/Fas ligand expression in human acute promyelocytic leukemia cells. J Biol Chem 2002;277: 2073-80.
26. Pang RW, Poon RT. From molecular biology to targeted therapies for hepatocellular carcinoma: the future is now. Oncology 2007;72 Suppl 1:30-44.
27. Venturelli S, Armeanu S, Pathil A, et al. Epigenetic combination therapy as a tumor-selective treatment approach for hepatocellular carcinoma. Cancer 2007;109:2132-41.
28. Wise LD, Turner KJ, Kerr JS. Assessment of developmental toxicity of vorinostat, a histone deacetylase inhibitor, in Sprague-Dawley rats and Dutch Belted rabbits. Birth Defects Res Part B Dev Reprod Toxicol 2007;80:57-68.
29. Zhang G, Park MA, Mitchell C, et al. Vorinostat and sorafenib synergistically kill tumor cells via FLIP suppression and CD95 activation. Clin Cancer Res 2008;14:5385-99.
30. Park MA, Zhang G, Martin AP, et al. Vorinostat and sorafenib increase ER stress, autophagy and apoptosis via ceramide-dependent CD95 and PERK activation. Cancer Biol Ther 2008;7: 1648-62.
31. Park MA, Zhang G, Mitchell C, et al. Mitogen-activated protein kinase kinase 1/2 inhibitors and 17-allylamino-17-demethoxygeldanamycin synergize to kill human gastrointestinal tumor cells in vitro via suppression of c-FLIP-s levels and activation of CD95. Mol Cancer Ther 2008;7:2633-48.
32. Yacoub A, Park MA, Gupta P, et al. Caspase-, cathepsin- and PERKdependent regulation of MDA-7/IL-24-induced cell killing in primary human glioma cells. Mol Cancer Ther 2008;7:297-313. (Pubitemid 351302524)
33. Mitchell C, Park MA, Zhang G, et al. 17-Allylamino-17- demethoxygeldanamycin enhances the lethality of deoxycholic acid in primary rodent hepatocytes and established cell lines. Mol Cancer Ther 2007;6:618-32.
34. Gupta S, Natarajan R, Payne SG, et al. Deoxycholic acid activates the c-Jun N-terminal kinase pathway via FAS receptor activation in primary hepatocytes. Role of acidic sphingomyelinase-mediated ceramide generation in FAS receptor activation. J Biol Chem 2001; 279:5821-8.
35. Qiao L, Studer E, Leach K, et al. Deoxycholic acid (DCA) causes ligand-independent activation of epidermal growth factor receptor (EGFR) and FAS receptor in primary hepatocytes: inhibition of EGFR/mitogen-activated protein kinase-signaling module enhances DCA-induced apoptosis. Mol Biol Cell 2001; 12:2629-45.
36. Zhang G, Park MA, Mitchell C, et al. Multiple cyclin kinase inhibitors promote bile acid-induced apoptosis and autophagy in primary hepatocytes via p53 -CD95-dependent signaling. J Biol Chem 2008; 283:24343-58.
37. Mukhopadhyay A, Saddoughi SA, Song P, et al. Direct interaction between the inhibitor 2 and ceramide via sphingolipid-protein binding is involved in the regulation of protein phosphatase 2A activity and signaling. FASEB J 2009;23:751-63.
38. Wegrzyn J, Potla R, Chwae YJ, et al. Function of mitochondrial Stat3 in cellular respiration. Science 2009;323:793-7.
39. Reinehr R, Häussinger D. Hyperosmotic activation of the CD95 system. Methods Enzymol 2007;428:145-60.
40. Pewzner-Jung Y, Ben-Dor S, Futerman AH. When do Lasses (longevity assurance genes) become CerS (ceramide synthases)?: insights into the regulation of ceramide synthesis. J Biol Chem 2006;281:25001-5.
41. Rosato RR, Almenara JA, Maggio SC, et al. Role of histone deacetylase inhibitor-induced reactive oxygen species and DNA damage in LAQ-824/fludarabine antileukemic interactions. Mol Cancer Ther 2008;7:3285-97.
42. Mikkelsen RB, Wardman P. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 2003;22:5734-54.
43. 2+-dependent cell survival and death. Mol Cell 2009;33:377-88.
44. White-Gilbertson S, Mullen T, Senkal C, et al. Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene 2009;28:1132-41.
45. Walker T, Mitchell C, Park MA, et al. Sorafenib and vorinostat kill colon cancer cells by CD95-dependent and -independent mechanisms. Mol Pharmacol 2009;76:342-55.
46. Martin AP, Park MA, Mitchell C, et al. BCL-2 family inhibitors enhance histone deacetylase inhibitor and sorafenib lethality via autophagy and overcome blockade of the extrinsic pathway to facilitate killing. Mol Pharmacol 2009;76:327-41.