Histone deacetylase inhibitors interact with melanoma differentiation associated-7/interleukin-24 to kill primary human glioblastoma cells

Molecular Pharmacology

Volumn 84, Issue 2, 2013, Pages 171-181

  Hamed, Hossein A ^a   Yacoub, Adly ^a   Park, Margaret A ^b   Archer, Kellie ^b   Das, Swadesh K ^b   Sarkar, Devanand ^a,b   Grant, Steven ^a,b   Fisher, Paul B ^a,b   Dent, Paul ^a  

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

^b Department of Medicine ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM ION; CERAMIDE GLUCOSYLTRANSFERASE; HISTONE DEACETYLASE INHIBITOR; INTERLEUKIN 24; ONCOLYTIC ADENOVIRUS; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPHAGY; CANCER SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYRIAN HAMSTER; VIRAL GENE DELIVERY SYSTEM; VIRUS REPLICATION;

ADENOVIRIDAE; ANIMALS; BRAIN NEOPLASMS; CALCIUM; CELL LINE, TUMOR; CRICETINAE; FEMALE; GENETIC THERAPY; GLIOBLASTOMA; HISTONE DEACETYLASE INHIBITORS; HUMANS; INTERLEUKINS; MEMBRANE PROTEINS; MICE; MICE, NUDE; REACTIVE OXYGEN SPECIES; SPHINGOSINE N-ACYLTRANSFERASE;

EID: 84880587509     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.086553     Document Type: Article

References (50)

1. Azab B, Dash R, Das SK, Bhutia SK, Shen XN, Quinn BA, Sarkar S, Wang XY, Hedvat M, and Dmitriev IP et al. (2012) Enhanced delivery of mda-7/IL-24 using a serotype chimeric adenovirus (Ad.5/3) in combination with the Apogossypol derivative BI-97C1 (Sabutoclax) improves therapeutic efficacy in low CAR colorectal cancer cells. J Cell Physiol 227:2145-2153.
2. Bhutia SK, Das SK, Azab B, Dash R, Su ZZ, Lee SG, Dent P, Curiel DT, Sarkar D, and Fisher PB (2011) Autophagy switches to apoptosis in prostate cancer cells infected with melanoma differentiation associated gene-7/interleukin-24 (mda-7/IL-24). Autophagy 7:1076-1077.
3. Chinnaiyan P, Chowdhary S, Potthast L, Prabhu A, Tsai YY, Sarcar B, Kahali S, Brem S, Yu HM, and Rojiani A et al. (2012) Phase I trial of vorinostat combined with bevacizumab and CPT-11 in recurrent glioblastoma. Neuro-oncol 14:93-100.
4. Cunningham CC, Chada S, Merritt JA, Tong A, Senzer N, Zhang Y, Mhashilkar A, Parker K, Vukelja S, and Richards D et al. (2005) Clinical and local biological effects of an intratumoral injection of mda-7 (IL24; INGN 241) in patients with advanced carcinoma: a phase I study. Mol Ther 11:149-159.
5. Curiel DT and Fisher PB eds. (2012) Applications of Viruses for Cancer Therapy, Advances in Cancer Research, vol 115, pp 1-334, Academic Press, Waltham, MA, ISBN: 9780123983428.
6. Dai Y, Rahmani M, Dent P, and Grant S (2005) Blockade of histone deacetylase inhibitor-induced RelA/p65 acetylation and NF-kB activation potentiates apoptosis in leukemia cells through a process mediated by oxidative damage, XIAP downregulation, and c-Jun N-terminal kinase 1 activation. Mol Cell Biol 25:5429-5444.
7. Dash R, Bhutia SK, Azab B, Su ZZ, Quinn BA, Kegelmen TP, Das SK, Kim K, Lee SG, and Park MA et al. (2010a) mda-7/IL-24: a unique member of the IL-10 gene family promoting cancer-targeted toxicity. Cytokine Growth Factor Rev 21:381-391.
8. Dash R, Azab B, Quinn BA, Shen X, Wang XY, Das SK, Rahmani M, Wei J, Hedvat M, and Dent P et al. (2011) Apogossypol derivative BI-97C1 (Sabutoclax) targeting Mcl-1 sensitizes prostate cancer cells to mda-7/IL-24-mediated toxicity. Proc Natl Acad Sci USA 108:8785-8790.
9. Dash R, Dmitriev I, Su ZZ, Bhutia SK, Azab B, Vozhilla N, Yacoub A, Dent P, Curiel DT, and Sarkar D et al. (2010b) Enhanced delivery of mda-7/IL-24 using a serotype chimeric adenovirus (Ad.5/3) improves therapeutic efficacy in low CAR prostate cancer cells. Cancer Gene Ther 17:447-456.
10. Dhar D, Toth K, and Wold WS (2012) Syrian hamster tumor model to study oncolytic Ad5-based vectors. Methods Mol Biol 797:53-63.
11. Dent P, Yacoub A, Hamed HA, Park MA, Dash R, Bhutia SK, Sarkar D, Wang XY, Gupta P, and Emdad L et al. (2010a) The development of MDA-7/IL-24 as a cancer therapeutic. Pharmacol Ther 128:375-384.
12. Dent P, Yacoub A, Hamed HA, Park MA, Dash R, Bhutia SK, Sarkar D, Gupta P, Emdad L, and Lebedeva IV et al. (2010b) MDA-7/IL-24 as a cancer therapeutic: from bench to bedside. Anticancer Drugs 21:725-731.
13. Ekmekcioglu S, Ellerhorst J, Mhashilkar AM, Sahin AA, Read CM, Prieto VG, Chada S, and Grimm EA (2001) Down-regulated melanoma differentiation associated gene (mda-7) expression in human melanomas. Int J Cancer 94:54-59.
14. Ellerhorst JA, Prieto VG, Ekmekcioglu S, Broemeling L, Yekell S, Chada S, and Grimm EA (2002) Loss of MDA-7 expression with progression of melanoma. J Clin Oncol 20:1069-1074.
15. Ellis L and Pili R (2010) Histone deacetylase inhibitors: advancing therapeutic strategies in hematological and solid malignancies. Pharmaceuticals (Basel) 3: 2411-2469.
16. Emanuele S, Lauricella M, Carlisi D, Vassallo B, D'Anneo A, Di Fazio P, Vento R, and Tesoriere G (2007) SAHA induces apoptosis in hepatoma cells and synergistically interacts with the proteasome inhibitor Bortezomib. Apoptosis 12: 1327-1338.
17. Emdad L, Lebedeva IV, Su ZZ, Gupta P, Sauane M, Dash R, Grant S, Dent P, Curiel DT, and Sarkar D et al. (2009) Historical perspective and recent insights into our understanding of the molecular and biochemical basis of the antitumor properties of mda-7/IL-24. Cancer Biol Ther 8:391-400.
18. Fisher PB, Gopalkrishnan RV, Chada S, Ramesh R, Grimm EA, Rosenfeld MR, Curiel DT, and Dent P (2003) mda-7/IL-24, a novel cancer selective apoptosis inducing cytokine gene: from the laboratory into the clinic. Cancer Biol Ther 2(Suppl 1)S23-S37.
19. Fisher PB (2005) Is mda-7/IL-24 a "magic bullet" for cancer? Cancer Res 65: 10128-10138.
20. Frew AJ, Johnstone RW, and Bolden JE (2009) Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Lett 280:125-133.
21. Friday BB, Anderson SK, Buckner J, Yu C, Giannini C, Geoffroy F, Schwerkoske J, Mazurczak M, Gross H, and Pajon E et al. (2012) Phase II trial of vorinostat in combination with bortezomib in recurrent glioblastoma: a north central cancer treatment group study. Neuro-oncol 14:215-221.
22. Galanis E, Jaeckle KA, Maurer MJ, Reid JM, Ames MM, Hardwick JS, Reilly JF, Loboda A, Nebozhyn M, and Fantin VR et al. (2009) Phase II trial of vorinostat in recurrent glioblastoma multiforme: a north central cancer treatment group study. J Clin Oncol 27:2052-2058.
23. Gupta P, Su ZZ, Lebedeva IV, Sarkar D, Sauane M, Emdad L, Bachelor MA, Grant S, Curiel DT, and Dent P et al. (2006a) mda-7/IL-24: multifunctional cancer-specific apoptosis-inducing cytokine. Pharmacol Ther 111:596-628.
24. Gupta P, Walter MR, Su ZZ, Lebedeva IV, Emdad L, Randolph A, Valerie K, Sarkar D, and Fisher PB (2006b) BiP/GRP78 is an intracellular target for MDA-7/IL-24 induction of cancer-specific apoptosis. Cancer Res 66:8182-8191.
25. Hamed HA, Yacoub A, Park MA, Eulitt PJ, Dash R, Sarkar D, Dmitriev IP, Lesniak MS, Shah K, and Grant S et al. (2010) Inhibition of multiple protective signaling pathways and Ad.5/3 delivery enhances mda-7/IL-24 therapy of malignant glioma. Mol Ther 18:1130-1142.
26. Jiang H, Lin JJ, Su ZZ, Goldstein NI, and Fisher PB (1995) Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 11: 2477-2486.
27. Kahali S, Sarcar B, Fang B, Williams ES, Koomen JM, Tofilon PJ, and Chinnaiyan P (2010) Activation of the unfolded protein response contributes toward the antitumor activity of vorinostat. Neoplasia 12:80-86.
28. Lebedeva IV, Sauane M, Gopalkrishnan RV, Sarkar D, Su ZZ, Gupta P, Nemunaitis J, Cunningham C, Yacoub A, and Dent P et al. (2005) mda-7/IL-24: exploiting cancer's Achilles' heel. Mol Ther 11:4-18.
29. Lee EQ, Puduvalli VK, Reid JM, Kuhn JG, Lamborn KR, Cloughesy TF, Chang SM, Drappatz J, Yung WK, and Gilbert MR et al. (2012) Phase I study of vorinostat in combination with temozolomide in patients with high-grade gliomas: North American Brain Tumor Consortium Study 04-03. Clin Cancer Res 18:6032-6039.
30. Park MA, Walker T, Martin AP, Allegood J, Vozhilla N, Emdad L, Sarkar D, Rahmani M, Graf M, and Yacoub A et al. (2009) MDA-7/IL-24-induced cell killing in malignant renal carcinoma cells occurs by a ceramide/CD95/PERK-dependent mechanism. Mol Cancer Ther 8:1280-1291.
31. Paul CP, Everts M, Glasgow JN, Dent P, Fisher PB, Ulasov IV, Lesniak MS, Stoff-Khalili MA, Roth JC, and Preuss MA et al. (2008) Characterization of infectivity of knob-modified adenoviral vectors in glioma. Cancer Biol Ther 7:786-793.
32. Robins HI, Chang S, Butowski N, and Mehta M (2007) Therapeutic advances for glioblastoma multiforme: current status and future prospects. Curr Oncol Rep 9: 66-70.
33. Rosato RR and Grant S (2004) Histone deacetylase inhibitors in clinical development. Expert Opin Investig Drugs 13:21-38.
34. Ruefli AA, Ausserlechner MJ, Bernhard D, Sutton VR, Tainton KM, Kofler R, Smyth MJ, and Johnstone RW (2001) The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc Natl Acad Sci USA 98:10833-10838.
35. Sarkar D, Lebedeva IV, Su ZZ, Park ES, Chatman L, Vozhilla N, Dent P, Curiel DT, and Fisher PB (2007) Eradication of therapy-resistant human prostate tumors using a cancer terminator virus. Cancer Res 67:5434-5442.
36. Sarkar D, Su ZZ, Park ES, Vozhilla N, Dent P, Curiel DT, and Fisher PB (2008) A cancer terminator virus eradicates both primary and distant human melanomas. Cancer Gene Ther 15:293-302.
37. Sarkar D, Su ZZ, Vozhilla N, Park ES, Gupta P, and Fisher PB (2005) Dual cancerspecific targeting strategy cures primary and distant breast carcinomas in nude mice. Proc Natl Acad Sci USA 102:14034-14039.
38. Sauane M, Su ZZ, Dash R, Liu X, Norris JS, Sarkar D, Lee SG, Allegood JC, Dent P, and Spiegel S et al. (2010) Ceramide plays a prominent role in MDA-7/IL-24-induced cancer-specific apoptosis. J Cell Physiol 222:546-555.
39. Sauane M, Su ZZ, Gupta P, Lebedeva IV, Dent P, Sarkar D, and Fisher PB (2008) Autocrine regulation of mda-7/IL-24 mediates cancer-specific apoptosis. Proc Natl Acad Sci USA 105:9763-9768.
40. Spiegel S, Milstien S, and Grant S (2012) Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene 31:537-551.
41. Su Z, Lebedeva IV, Gopalkrishnan RV, Goldstein NI, Stein CA, Reed JC, Dent P, and Fisher PB (2001) A combinatorial approach for selectively inducing programmed cell death in human pancreatic cancer cells. Proc Natl Acad Sci USA 98: 10332-10337.
42. Su ZZ, Madireddi MT, Lin JJ, Young CS, Kitada S, Reed JC, Goldstein NI, and Fisher PB (1998) The cancer growth suppressor gene mda-7 selectively induces apoptosis in human breast cancer cells and inhibits tumor growth in nude mice. Proc Natl Acad Sci USA 95:14400-14405.
43. Su ZZ, Sarkar D, Emdad L, Duigou GJ, Young CS, Ware J, Randolph A, Valerie K, and Fisher PB (2005) Targeting gene expression selectively in cancer cells by using the progression-elevated gene-3 promoter. Proc Natl Acad Sci USA 102: 1059-1064.
44. Tang Y, Yacoub A, Hamed HA, Poklepovic A, Tye G, Grant S, and Dent P (2012) Sorafenib and HDAC inhibitors synergize to kill CNS tumor cells. Cancer Biol Ther 13:567-574.
45. Ungerstedt JS, Sowa Y, Xu WS, Shao Y, Dokmanovic M, Perez G, Ngo L, Holmgren A, Jiang X, and Marks PA (2005) Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci USA 102: 673-678.
46. Yacoub A, Hamed HA, Allegood J, Mitchell C, Spiegel S, Lesniak MS, Ogretmen B, Dash R, Sarkar D, and Broaddus WC et al. (2010a) PERK-dependent regulation of ceramide synthase 6 and thioredoxin play a key role in mda-7/IL-24-induced killing of primary human glioblastoma multiforme cells. Cancer Res 70:1120-1129.
47. Yacoub A, Park MA, Gupta P, Rahmani M, Zhang G, Hamed H, Hanna D, Sarkar D, Lebedeva IV, and Emdad L et al. (2008a) Caspase-, cathepsin-, and PERK dependent regulation of MDA-7/IL-24-induced cell killing in primary human glioma cells. Mol Cancer Ther 7:297-313.
48. Yacoub A, Gupta P, Park MA, Rhamani M, Hamed H, Hanna D, Zhang G, Sarkar D, Lebedeva IV, and Emdad L et al. (2008b) Regulation of GST-MDA-7 toxicity in human glioblastoma cells by ERBB1, ERK1/2, PI3K, and JNK1-3 pathway signaling. Mol Cancer Ther 7:314-329.
49. Yacoub A, Hamed H, Emdad L, Dos Santos W, Gupta P, Broaddus WC, Ramakrishnan V, Sarkar D, Shah K, and Curiel DT et al. (2008c) MDA-7/IL-24 plus radiation enhance survival in animals with intracranial primary human GBM tumors. Cancer Biol Ther 7:917-933.
50. Yacoub A, Liu R, Park MA, Hamed HA, Dash R, Schramm DN, Sarkar D, Dimitriev IP, Bell JK, and Grant S et al. (2010b) Cisplatin enhances protein kinase R-like endoplasmic reticulum kinase-and CD95-dependent melanoma differentiation-associated gene-7/interleukin-24-induced killing in ovarian carcinoma cells. Mol Pharmacol 77:298-310. and Digestive and Kidney Diseases