Eradication of metastatic melanoma through cooperative expression of RNA-based HDAC1 inhibitor and p73 by oncolytic adenovirus

Oncotarget

Volumn 5, Issue 15, 2014, Pages 5893-5907

  Schipper, Holger ^a   Alla, Vijay ^a   Meier, Claudia ^a   Nettelbeck, Dirk M ^b   Herchenröder, Ottmar ^a   Pützer, Brigitte M ^a  

^a ROSTOCK UNIVERSITY MEDICAL CENTER   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Apoptosis; Autophagy; Chemoresistance; HDAC1; Malignant melanoma; Oncolytic adenovirus; P73

Indexed keywords

HISTONE DEACETYLASE 1; ONCOLYTIC ADENOVIRUS; PROTEIN P73; SHORT HAIRPIN RNA; DNA BINDING PROTEIN; HDAC1 PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOLYTIC VIRUS; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN P73;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CYTOTOXICITY; DEACETYLATION; EPIGENETICS; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTATIC MELANOMA; MOUSE; NONHUMAN; TUMOR GROWTH; TUMOR REGRESSION; VIRUS REPLICATION; ADENOVIRIDAE; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; GENE SILENCING; GENETICS; HEK293 CELL LINE; MELANOMA; ONCOLYTIC VIROTHERAPY; PROCEDURES; TRANSGENE; TUMOR CELL LINE; VIROLOGY;

ADENOVIRIDAE; CELL LINE, TUMOR; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HISTONE DEACETYLASE 1; HUMANS; MELANOMA; NUCLEAR PROTEINS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; RNA, SMALL INTERFERING; TRANSGENES; TUMOR SUPPRESSOR PROTEINS;

EID: 84906247811     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1839     Document Type: Article

References (66)

1. Garbe C, Peris K, Hauschild A, Saiag P, Middleton M, Spatz A, Grob JJ, Malvehy J, Newton-Bishop J, Stratigos A, Pehamberger H, Eggermont AM. Diagnosis and treatment of melanoma. European consensus-based interdisciplinary guideline -Update 2012. Eur J Cancer. 2012; 48:2375-90.
2. Pützer BM, Steder M, Alla V. Predicting and preventing melanoma invasiveness: advances in clarifying E2F1 function. Expert Rev Anticancer Ther. 2010; 10:1707-20.
3. Dahl C, Guldberg P. The genome and epigenome of malignant melanoma. APMIS. 2007; 115:1161-76.4. Vazquez A, Bond EE, Levine AJ, Bond GL. The genetics of the p53 pathway, apoptosis and cancer therapy. Nat Rev Drug Discov. 2008; 7:979-87.
4. Vazquez A, Bond EE, Levine AJ, Bond GL. The genetics of the p53 pathway, apoptosis and cancer therapy. Nat Rev Drug Discov. 2008; 7:979-87
5. Terzian T, Torchia EC, Dai D, Robinson SE, Murao K, Stiegmann RA, Gonzalez V, Boyle GM, Powell MB, Pollock PM, Lozano G, Robinson WA, Roop DR et al. p53 prevents progression of nevi to melanoma predominantly through cell cycle regulation. Pigment Cell Melanoma Res. 2010; 23:781-94.
6. Gray-Schopfer V, Wellbrock C, Marais R. Melanoma biology and new targeted therapy. Nature. 2007; 445:851-7.
7. Hoon DS, Spugnardi M, Kuo C, Huang SK, Morton DL, Taback B. Profiling epigenetic inactivation of tumor suppressor genes in tumors and plasma from cutaneous melanoma patients. Oncogene. 2004; 23:4014-22.
8. Bostick M, Kim JK, Estève PO, Clark A, Pradhan S, Jacobsen SE. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science. 2007; 317:1760-4.
9. Schinke C, Mo Y, Yu Y, Amiri K, Sosman J, Greally J, Verma A. Aberrant DNA methylation in malignant melanoma. Melanoma Res. 2010; 20:253-65.
10. Soengas MS, Capodieci P, Polsky D, Mora J, Esteller M, Opitz-Araya X, McCombie R, Herman JG, Gerald WL, Lazebnik YA, Cordón-Cardó C, Lowe SW. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature. 2001; 409:207-11.
11. Stiewe T, Theseling CC, Pützer BM. Transactivationdeficient Delta TA-p73 inhibits p53 by direct competition for DNA binding: implications for tumorigenesis. J Biol Chem. 2002; 277:14177-85.
12. Tomasini R, Mak TW, Melino G. The impact of p53 and p73 on aneuploidy and cancer. Trends Cell Biol. 2008; 5:244-52.
13. Buhlmann S, Pützer BM. DNp73 a matter of cancer: mechanisms and clinical implications. Biochim Biophys Acta. 2008; 1785:207-16.
14. Dötsch V, Bernassola F, Coutandin D, Candi E, Melino G. p63 and p73, the ancestors of p53. Cold Spring Harb Perspect Biol. 2010; 9:a004887.
15. Tuve S, Wagner SN, Schittek B, Pützer BM. Alterations of DeltaTA-p 73 splice transcripts during melanoma development and progression. Int J Cancer. 2004; 108:162-6.
16. Steder M, Alla V, Meier C, Spitschak A, Pahnke J, Fürst K, Kowtharapu BS, Engelmann D, Petigk J, Egberts F, Schäd-Trcka SG, Gross G, Nettelbeck DM et al. DNp73 exerts function in metastasis initiation by disconnecting the inhibitory role of EPLIN on IGF1R-AKT/STAT3 signaling. Cancer Cell. 2013; 24:512-27.
17. Alla V, Kowtharapu BS, Engelmann D, Emmrich S, Schmitz U, Steder M, Pützer BM. E2F1 confers anticancer drug resistance by targeting ABC transporter family members and Bcl-2 via the p73/DNp73-miR-205 circuitry.Cell Cycle. 2012; 11:3067-78.
18. Emmrich S, Wang W, John K, Li W, Pützer BM. Antisense gapmers selectively suppress individual oncogenic p73 splice isoforms and inhibit tumor growth in vivo. Mol Cancer. 2009; 8:61.
19. Musselman CA, Lalonde ME, Côté J, Kutateladze TG. Perceiving the epigenetic landscape through histone readers. Nat Struct Mol Biol. 2012; 19:1218-27.
20. Boyle GM, Martyn AC, Parsons PG. Histone deacetylase inhibitors and malignant melanoma. Pigment Cell Res. 2005; 18:160-6.
21. Bandyopadhyay D, Mishra A, Medrano EE. Overexpression of histone deacetylase 1 confers resistance to sodium butyrate-mediated apoptosis in melanoma cells through a p53-mediated pathway. Cancer Res. 2004; 64:7706-10.
22. Valentini A, Gravina P, Federici G, Bernardini S. Valproic acid induces apoptosis, p16INK4A upregulation and sensitization to chemotherapy in human melanoma cells. Cancer Biol Ther. 2007; 6:185-91.
23. Gowda R, Madhunapantula SV, Desai D, Amin S, Robertson GP. Selenium-containing histone deacetylase inhibitors for melanoma management. Cancer Biol Ther. 2012; 13:756-65.
24. Groselj B, Sharma NL, Hamdy FC, Kerr M, Kiltie AE. Histone deacetylase inhibitors as radiosensitisers: effects on DNA damage signalling and repair. Br J Cancer. 2013; 108:748-54.
25. Finzer P, Krueger A, Stöhr M, Brenner D, Soto U, Kuntzen C, Krammer PH, Rösl F. HDAC inhibitors trigger apoptosis in HPV-positive cells by inducing the E2F-p73 pathway. Oncogene. 2004; 23:4807-17.
26. Wong HH, Lemoine NR, WangY. Oncolytic Viruses for Cancer Therapy: Overcoming the Obstacles. Viruses. 2010; 2:78-106.
27. Kaufmann JK, Nettelbeck DM. Virus chimeras for gene therapy, vaccination, and oncolysis: adenoviruses and beyond. Trends Mol Med. 2012; 18:365-76.
28. Fueyo J, Gomez-Manzano C, Alemany R, Lee PS, McDonnell TJ, Mitlianga P, Shi YX, Levin VA, Yung WK, Kyritsis AP. A mutant oncolytic adenovirus targeting the Rb pathway produces anti-glioma effect in vivo. Oncogene. 2000; 19:2-12.
29. Vasey PA, Shulman LN, Campos S, Davis J, Gore M, Johnston S, Kirn DH, O'Neill V, Siddiqui N, Seiden MV, Kaye SB. Phase I trial of intraperitoneal injection of the E1B-55-kd-gene-deleted adenovirus ONYX-015 (dl1520) given on days 1 through 5 every 3 weeks in patients with recurrent/refractory epithelial ovarian cancer. J Clin Oncol. 2002; 20:1562-9.
30. Zhang J, Xu E, Chen X. TAp73 protein stability is controlled by histone deacetylase 1 via regulation of Hsp90 chaperone function. J Biol Chem. 2013; 288:7727-37.
31. Suzuki K, Alemany R, Yamamoto M, Curiel DT. The presence of the adenovirus E3 region improves the oncolytic potency of conditionally replicative adenoviruses. Clin Cancer Res. 2002; 8:3348-59.
32. Tuve S, Racek T, Niemetz A, Schultz J, Soengas MS, Pützer BM. Adenovirus-mediated TA-p73beta gene transfer increases chemosensitivity of human malignant melanomas. Apoptosis. 2006; 11:235-43.
33. Schreiner S. Wimmer P, Dobner T. Adenovirus degradation of cellular proteins. Future Microbiol. 2012; 7:211-25.
34. Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy. Nat Cell Biol. 2013; 15:713-20.
35. Rodriguez-Rocha H, Gomez-Gutierrez JG, Garcia-Garcia A, Rao XM, Chen L, McMasters KM, Zhou HS. Adenoviruses induce autophagy to promote virus replication and oncolysis. Virology. 2011; 416:9-15.
36. Jiang H, White EJ, Ríos-Vicil CI, Xu J, Gomez-Manzano C, Fueyo J. Human adenovirus type 5 induces cell lysis through autophagy and autophagy-triggered caspase activity. J Virol. 2011; 85:4720-9.
37. Soengas MS, Lowe SW. Apoptosis and melanoma chemoresistance. Oncogene. 2003; 22:3138-51.
38. Grossmann D, Altieri DC. Drug resistance in melanoma: Mechanisms, apoptosis, and new potential therapeutic targets. Cancer Metastasis Rev. 2001; 20:3-11.
39. Nikolaou VA, Stratigos AJ, Flaherty KT, Tsao H. Melanoma: new insights and new therapies. J Invest Dermatol. 2012; 132:854-63.
40. Houben R, Hesbacher S, Schmid CP, Kauczok CS, Flohr U, Haferkamp S, Müller CS, Schrama D, Wischhusen J, Becker JC. High-level expression of wild-type p53 in melanoma cells is frequently associated with inactivity in p53 reporter gene assays. PLoS One. 2011;6(7):e22096.
41. Avery-Kiejda KA, Bowden NA, Croft AJ, Scurr LL, Kairupan CF, Ashton KA, Talseth-Palmer BA, Rizos H, Zhang XD, Scott RJ, Hersey P. P53 in human melanoma fails to regulate target genes associated with apoptosis and the cell cycle and may contribute to proliferation. BMC Cancer. 2011; 11:203.
42. Lu M, Breyssens H, Salter V, Zhong S, Hu Y, Baer C, Ratnayaka I, Sullivan A, Brown NR, Endicott J, Knapp S, Kessler BM, Middleton MR et al. Restoring p53 function in human melanoma cells by inhibiting MDM2 and cyclin B1/ CDK1-phosphorylated nuclear iASPP. Cancer Cell. 2013; 23:618-33.
43. Uramoto H, Wetterskog D, Hackzell A, Matsumoto Y, Funa K. p73 competes with co-activators and recruits histone deacetylase to NF-Y in the repression of PDGF betareceptor. J Cell Sci. 2004; 117:5323-31.
44. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov. 2006; 5:769-84.
45. Costanzo A, Merlo P, Pediconi N, Fulco M, Sartorelli V, Cole PA, Fontemaggi G, Fanciulli M, Schiltz L, Blandino G, Balsano C, Levrero M. DNA damage-dependent acetylation of p73 dictates the selective activation of apoptotic target genes. Mol Cell. 2002; 9:175-186.
46. Kato Y, Yoshimura K, Shin T, Verheul H, Hammers H, Sanni TB, Salumbides BC, Van Erp K, Schulick R, Pili R. Synergistic in vivo antitumor effect of the histone deacetylase inhibitor MS-275 in combination with interleukin 2 in a murine model of renal cell carcinoma. Clin Cancer Res. 2007; 13:4538-46.
47. Kulesz-Martin M, Lagowski J, Fei S, Pelz C, Sears R, Powell MB, Halaban R, Johnson J. Melanocyte and keratinocyte carcinogenesis: p53 family protein activities and intersecting mRNA expression profiles. J Investig Dermatol Symp Proc. 2005; 2:142-52.
48. Vera J, Schmitz U, Lai X, Engelmann D, Khan FM, Wolkenhauer O, Pützer BM. Kinetic modeling-based detection of genetic signatures that provide chemoresistance via the E2F1-p73/DNp73-miR-205 network. Cancer Res. 2013; 73:3511-24.
49. Liu TC, Galanis E, Kirn D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat Clin Pract Oncol. 2007; 4:101-17.
50. Cody JJ, Douglas JT. Armed replicating adenoviruses for cancer virotherapy. Cancer Gene Ther. 2009; 16:473-88.
51. Höti N, Chowdhury W, Hsieh JT, Sachs MD, Lupold SE, Rodriguez R. Valproic acid, a histone deacetylase inhibitor, is an antagonist for oncolytic adenoviral gene therapy. Mol Ther. 2006; 14:768-78.
52. Eberle J, Fecker LF, Forschner T, Ulrich C, Röwert-Huber J, Stockfleth E. Apoptosis pathways as promising targets for skin cancer therapy. Br J Dermatol. 2007; 156 Suppl 3:18-24.
53. Crighton D, O'Prey J, Bell HS, Ryan KM. Crighton p73 regulates DRAM-independent autophagy that does not contribute to programmed cell death. Cell Death Differ. 2007; 14:1071-9.
54. Gammoh N, Lam D, Puente C, Ganley I, Marks PA, Jiang X. Role of autophagy in histone deacetylase inhibitorinduced apoptotic and nonapoptotic cell death. Proc Natl Acad Sci U S A. 2012; 109:6561-5.
55. Wong SW, Tiong KH, Kong WY, Yue YC, Chua CH, Lim JY, Lee CY, Quah SI, Fow C, Chung C, So I, Tan BS, Choo HL, Rosli R, Cheong SK, Leong CO. Rapamycin synergizes cisplatin sensitivity in basal-like breast cancer cells through up-regulation of p73. Breast Cancer Res Treat. 2011; 2:301-13.
56. Bisso A, Collavin L, Del Sal G. p73 as a pharmaceutical target for cancer therapy. Curr Pharm Des. 2011; 6:578-90.
57. Maas AM, Bretz AC, Mack E, Stiewe T. Targeting p73 in cancer. Cancer Lett. 2013; 2:229-36.
58. Zeng X, Overmeyer JH, Maltese WA. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J Cell Sci. 2006; 119:259-70.
59. Tong Y, You L, Liu H, Li L, Meng H, Qian Q, Qian W. Potent antitumor activity of oncolytic adenovirus expressing Beclin-1 via induction of autophagic cell death in leukemia. Oncotarget. 2013; 4:860-74.
60. Botta G, Passaro C, Libertini S, Abagnale A, Barbato S, Maione AS, Hallden G, Beguinot F, Formisano P, Portella G. Inhibition of autophagy enhances the effects of E1Adefective oncolytic adenovirus dl922-947 against glioma cells in vitro and in vivo. Hum Gene Ther. 2012; 23:623-34.
61. Tormo D, Checinska A, Alonso-Curbelo D, Pérez-Guijarro E, Cañón E, Riveiro-Falkenbach E, Calvo TG, Larribere L, Megías D, Mulero F, Piris MA, Dash R, Barral PM et al. Targeted activation of innate immunity for therapeutic induction of autophagy and apoptosis in melanoma cells. Cancer Cell. 2009; 16:103-14.
62. Rivera AA, Wang M, Suzuki K, Uil TG, Krasnykh V, Curiel DT, Nettelbeck DM. Mode of transgene expression after fusion to early or late viral genes of a conditionally replicating adenovirus via an optimized internal ribosome entry site in vitro and in vivo. Virology. 2004; 320:121-34.
63. Quirin C, Rohmer S, Fernández-Ulibarri I, Behr M, Hesse A, Engelhardt S, Erbs P, Enk AH, Nettelbeck DM. Selectivity and efficiency of late transgene expression by transcriptionally targeted oncolytic adenoviruses are dependent on the transgene insertion strategy. Hum Gene Ther. 2011; 22:389-404.
64. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc. 2007; 2:1236-47.
65. Harms KL, Chen X. Histone deacetylase 2 modulates p53 transcriptional activities through regulation of p53-DNA binding activity. Cancer Res. 2007; 67:3145-52.
66. John K, Alla V, Meier C, Pützer BM. GRAMD4 mimics p53 and mediates the apoptotic function of p73 at mitochondria. Cell Death Differ. 2011; 18:874-86.