Armoring CRAds with p21/Waf-1 shRNAs: The next generation of oncolytic adenoviruses

Cancer Gene Therapy

Volumn 17, Issue 8, 2010, Pages 585-597

  Hoti N ^a   Chowdhury, W H ^a   Mustafa, S ^a   Ribas, J ^a   Castanares, M ^a   Johnson, T ^a   Liu, M ^a   Lupold, S E ^a   Rodriguez, R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenovirus; CRAd; P21 Waf 1; Prostate cancer; ShRNA

Indexed keywords

ANDROGEN; CONDITIONALLY REPLICATING ADENOVIRUS; CYCLIN DEPENDENT KINASE INHIBITOR 1; DOXORUBICIN; E1A PROTEIN; ONCOLYTIC ADENOVIRUS; SHORT HAIRPIN RNA; ANDROGEN RECEPTOR; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; ONCOLYTIC VIRUS; SMALL INTERFERING RNA;

ADENOVIRUS; ANDROGEN RESPONSIVE ELEMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CONTROLLED STUDY; GENE EXPRESSION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; LIFE CYCLE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN INDUCTION; RNA INTERFERENCE; SURVIVAL TIME; TISSUE SPECIFICITY; TUMOR GROWTH; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS ATTENUATION; VIRUS INHIBITION; VIRUS REPLICATION; ADENOVIRIDAE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; DOWN REGULATION; GENE SILENCING; GENE VECTOR; GENETICS; METABOLISM; NUDE MOUSE; PHYSIOLOGY; PROSTATIC NEOPLASMS; TUMOR CELL LINE; VIROLOGY;

ADENOVIRIDAE; ANIMALS; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOWN-REGULATION; DOXORUBICIN; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GENETIC VECTORS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; ONCOLYTIC VIRUSES; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; RNA INTERFERENCE; RNA, SMALL INTERFERING; VIRUS REPLICATION;

ADENOVIRIDAE; MUS;

EID: 77954816343     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2010.15     Document Type: Article

References (48)

1. Imai E, Isaka Y. Strategies of gene transfer to the kidney. Kidney Int 1998; 53: 264-272.
2. Greber UF, Willetts M, Webster P, Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993; 75: 477-486.
3. Pombo A, Ferreira J, Bridge E, Carmo-Fonseca M. Adenovirus replication and transcription sites are spatially separated in the nucleus of infected cells. EMBO J 1994; 13: 5075-5085. (Pubitemid 24341089)
4. Ben-Israel H, Kleinberger T. Adenovirus and cell cycle control. Front Biosci 2002; 7: d1369-d1395.
5. Morimoto K, Gosselink J, Kartono A, Hogg JC, Hayashi S, Ogawa E. Adenovirus E1a regulates lung epithelial Icam-1 expression by interacting with transcriptional regulators at its promoter. Am J Physiol Lung Cell Mol Physiol 2009; 296: L361-L371.
6. Horwitz GA, Zhang K, McBrian MA, Grunstein M, Kurdistani SK, Berk AJ. Adenovirus small e1a alters global patterns of histone modification. Science 2008; 321: 1084-1085.
7. Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ, Kurdistani SK. Epigenetic reprogramming by adenovirus e1a. Science 2008; 321: 1086-1088.
8. Miller DL, Myers CL, Rickards B, Coller HA, Flint SJ. Adenovirus type 5 exerts genome-wide control over cellular programs governing proliferation, quiescence, and survival. Genome Biol 2007; 8: R58.
9. Jones N, Shenk T. An adenovirus type 5 early gene function regulates expression of other early viral genes. Proc Natl Acad Sci USA 1979; 76: 3665-3669.
10. Rodriguez R, Schuur ER, Lim HY, Henderson GA, Simons JW, Henderson DR. Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostate-specific antigen-positive prostate cancer cells. Cancer Res 1997; 57: 2559-2563.
11. Dilley J, Reddy S, Ko D, Nguyen N, Rojas G, Working P et al. Oncolytic adenovirus CG7870 in combination with radiation demonstrates synergistic enhancements of antitumor efficacy without loss of specificity. Cancer Gene Ther 2005; 12: 715-722.
12. Hoti 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: 768-778.
13. Shiina M, Lacher MD, Christian C, Korn WM. RNA interference-mediated knockdown of p21(WAF1) enhances anti-tumor cell activity of oncolytic adenoviruses. Cancer Gene Ther 2009; 16: 810-819.
14. Niculescu III AB, Chen X, Smeets M, Hengst L, Prives C, Reed SI. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplica-tion. Mol Cell Biol 1998; 18: 629-643.
15. Fuse T, Yamada K, Asai K, Kato T, Nakanishi M. Heat shock-mediated cell cycle arrest is accompanied by induction of p21 CKI. Biochem Biophys Res Commun 1996; 225: 759-763.
16. Gehen SC, Vitiello PF, Bambara RA, Keng PC, O'Reilly MA. Downregulation of PCNA potentiates p21-mediated growth inhibition in response to hyperoxia. Am J Physiol Lung Cell Mol Physiol 2007; 292: L716-L724.
17. Suzuki A, Kawano H, Hayashida M, Hayasaki Y, Tsutomi Y, Akahane K. Procaspase 3/p21 complex formation to resist fas-mediated cell death is initiated as a result of the phosphorylation of p21 by protein kinase A. Cell Death Differ 2000; 7: 721-728. (Pubitemid 30599253)
18. Cayrol C, Knibiehler M, Ducommun B. p21 binding to PCNA causes G1 and G2 cell cycle arrest in p53-deficient cells. Oncogene 1998; 16: 311-320.
19. van Beusechem VW, Mastenbroek DC, van den Doel PB, Lamfers ML, Grill J, Wurdinger T et al. Conditionally replicative adenovirus expressing a targeting adapter molecule exhibits enhanced oncolytic potency on CAR-deficient tumors. Gene Therapy 2003; 10: 1982-1991.
20. Nebbioso A, Clarke N, Voltz E, Germain E, Ambrosino C, Bontempo P et al. Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nat Med 2005; 11: 77-84.
21. Hoti N, Li Y, Chen CL, Chowdhury WH, Johns DC, Xia Q et al. Androgen receptor attenuation of Ad5 replication: implications for the development of conditionally replication competent adenoviruses. Mol Ther 2007; 15: 1495-1503.
22. Yu DC, Chen Y, Seng M, Dilley J, Henderson DR. The addition of adenovirus type 5 region E3 enables calydon virus 787 to eliminate distant prostate tumor xenografts. Cancer Res 1999; 59: 4200-4203.
23. Li Y, McCadden J, Ferrer F, Kruszewski M, Carducci M, Simons J et al. Prostate-specific expression of the diphtheria toxin A chain (DT-A): studies of inducibility and specificity of expression of prostate-specific antigen promoter-driven DT-A adenoviral-mediated gene transfer. Cancer Res 2002; 62: 2576-2582.
24. Lupold SE, Kudrolli TA, Chowdhury WH, Wu P, Rodriguez R. A novel method for generating and screening peptides and libraries displayed on adenovirus fiber. Nucleic Acids Res 2007; 35: e138.
25. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 1998; 95: 2509-2514.
26. Sachs MD, Ramamurthy M, Poel H, Wickham TJ, Lamfers M, Gerritsen W et al. Histone deacetylase inhibitors upregulate expression of the coxsackie adenovirus receptor (CAR) preferentially in bladder cancer cells. Cancer Gene Ther 2004; 11: 477-486.
27. Huang B, Kochanek S. Adenovirus-mediated silencing of huntingtin expression by shRNA. Hum Gene Ther 2005; 16: 618-626.
28. Chattopadhyay D, Ghosh MK, Mal A, Harter ML. Inactivation of p21 by E1A leads to the induction of apoptosis in DNA-damaged cells. J Virol 2001; 75: 9844-9856.
29. Nettelbeck DM, Rivera AA, Balague C, Alemany R, Curiel DT. Novel oncolytic adenoviruses targeted to melanoma: specific viral replication and cytolysis by expression of E1A mutants from the tyrosinase enhancer/promoter. Cancer Res 2002; 62: 4663-4670.
30. Bischoff JR, Kirn DH, Williams A, Heise C, Horn S, Muna M et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 1996; 274: 373-376.
31. Leitner S, Sweeney K, Oberg D, Davies D, Miranda E, Lemoine NR et al. Oncolytic adenoviral mutants with E1B19K gene deletions enhance gemcitabine-induced apop-tosis in pancreatic carcinoma cells and anti-tumor efficacy in vivo. Clin Cancer Res 2009; 15: 1730-1740.
32. Satoh M, Wang H, Ishidoya S, Abe H, Moriya T, Hamada H et al. Oncolytic virotherapy for prostate cancer by E1A, E1B mutant adenovirus. Urology 2007; 70: 1243-1248.
33. Raponi M, Arndt GM. Double-stranded RNA-mediated gene silencing in fission yeast. Nucleic Acids Res 2003; 31: 4481-4489.
34. Graat HC, Witlox MA, Schagen FH, Kaspers GJ, Helder MN, Bras J et al. Different susceptibility of osteosarcoma cell lines and primary cells to treatment with oncolytic adenovirus and doxorubicin or cisplatin. Br J Cancer 2006; 94: 1837-1844.
35. Mike S, Harrison C, Coles B, Staffurth J, Wilt TJ, Mason MD. Chemotherapy for hormone-refractory prostate cancer. Cochrane Database Syst Rev 2006; 4: CD005247.
36. DeWeese TL, van der Poel H, Li S, Mikhak B, Drew R, Goemann M et al. A phase I trial of CV706, a replication-competent, PSA selective oncolytic adenovirus, for the treatment of locally recurrent prostate cancer following radiation therapy. Cancer Res 2001; 61: 7464-7472.
37. Small EJ, Carducci MA, Burke JM, Rodriguez R, Fong L, van Ummersen L et al. A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol Ther 2006; 14: 107-117.
38. Cooper MP, Balajee AS, Bohr VA. The C-terminal domain of p21 inhibits nucleotide excision repair In vitro and In vivo. Mol Biol Cell 1999; 10: 2119-2129.
39. Wang LG, Ossowski L, Ferrari AC. Overexpressed androgen receptor linked to p21WAF1 silencing may be responsible for androgen independence and resistance to apoptosis of a prostate cancer cell line. Cancer Res 2001; 61: 7544-7551.
40. Yoo JY, Kim JH, Kim J, Huang JH, Zhang SN, Kang YA et al. Short hairpin RNA-expressing oncolytic adenovirus-mediated inhibition of IL-8: effects on antiangiogenesis and tumor growth inhibition. Gene Therapy 2008; 15: 635-651.
41. Chu L, Gu J, Sun L, Qian Q, Qian C, Liu X. Oncolytic adenovirus-mediated shRNA against Apollon inhibits tumor cell growth and enhances antitumor effect of 5-fluorouracil. Gene Therapy 2008; 15: 484-494.
42. Mathews MB, Shenk T. Adenovirus virus-associated RNA and translation control. J Virol 1991; 65: 5657-5662.
43. Lu S, Cullen BR. Adenovirus VA1 noncoding RNA can inhibit small interfering RNA and MicroRNA biogenesis. J Virol 2004; 78: 12868-12876.
44. Koshiji M, Kageyama Y, Pete EA, Horikawa I, Barrett JC, Huang LE. HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. EMBO J 2004; 23: 1949-1956.
45. Schmaltz C, Hardenbergh PH, Wells A, Fisher DE. Regulation of proliferation-survival decisions during tumor cell hypoxia. Mol Cell Biol 1998; 18: 2845-2854.
46. Shen BH, Hermiston TW. Effect of hypoxia on Ad5 infection, transgene expression and replication. Gene Therapy 2005; 12: 902-910.
47. Wang YA, Elson A, Leder P. Loss of p21 increases sensitivity to ionizing radiation and delays the onset of lymphoma in atm-deficient mice. Proc Natl Acad Sci USA 1997; 94: 14590-14595.
48. Park SH, Park JY, Weiss RH. Antisense attenuation of p21 sensitizes kidney cancer to apoptosis in response to conventional DNA damaging chemotherapy associated with enhancement of phospho-p53. J Urol 2008; 180: 352-360.