A conditionally replicating adenovirus targeted to tumor cells through activated RAS/P-MAPK-selective mRNA stabilization

Nature Biotechnology

Volumn 21, Issue 7, 2003, Pages 771-777

  Ahmed, Atique ^a   Thompson, Jill ^a   Emiliusen, Lisa ^a   Murphy, Stephen ^a   Beauchamp, R Daniel ^b   Suzuki, Kaori ^a   Alemany, Ramon ^c   Harrington, Kevin ^d   Vile, Richard G ^a  

^a MAYO CLINIC   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; PATHOLOGY; PROTEINS; RNA; TUMORS; VIRUSES;

GENE EXPRESSION;

BIOTECHNOLOGY;

ADENOVIRUS VECTOR; CONDITIONALLY REPLICATING ADENOVIRUS; CYCLOOXYGENASE 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHORYLATED MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN ENDOPEROXIDE SYNTHASE 2; PROSTAGLANDIN SYNTHASE; RAS PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADENOVIRAL EARLY REGION 1A; ARTICLE; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; EXPRESSION VECTOR; GENE; GENE EXPRESSION REGULATION; GENE INDUCTION; HUMAN; HUMAN CELL; INFLAMMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA STABILITY; TUMOR CELL CULTURE; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS REPLICATION;

ADENOVIRIDAE; CELL DIVISION; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TARGETING; GENE TRANSFER TECHNIQUES; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASMS; RAS PROTEINS; RNA STABILITY; RNA, MESSENGER; TRANSFECTION; VIRUS REPLICATION;

ADENOVIRIDAE; UNIDENTIFIED BACTERIOPHAGE; VECTORS;

EID: 0038496739     PISSN: 10870156     EISSN: None     Source Type: Journal    
DOI: 10.1038/nbt835     Document Type: Article

References (48)

1. Biederer, C., Ries, S., Brandts, C.H. & McCormick, F. Replication-selective viruses for cancer therapy. J. Mol. Med. 80, 163-175 (2002).
2. Verma, I. & Somia, N. Gene therapy-promises, problems and prospects. Nature 389, 239-242 (1997).
3. Vile, R.G., Russell, S.J. & Lemoine, N.R. Cancer gene therapy: hard lessons and new courses. Gene Ther. 7, 2-8 (2000).
4. Alemany. R., Balague, C. & Curiel, D.T. Replicative adenoviruses for cancer therapy. Nat. Biotechnol. 18, 723-727 (2000).
5. Kirn, D., Martuza, R.L. & Zwiebel, J. Replication-selective virotherapy for cancer: biological principles, risk management and future directions. Nat. Med. 7, 781-787 (2001).
6. Krasnykh, V., Belousova, N., Korokhov, N., Mikheeva, G. & Curiel, D.T. Genetic targeting of an adenovirus vector via replacement of the fiber protein with the phage T4 fibritin. J. Virol. 75, 4176-4183 (2001).
7. Rodriguez, R. et al. Prostate attenuated replication competent adenovirus (ARCA) CN706: a selective cytotoxic for prostate-specific antigen-positive prostate cancer cells. Cancer Res. 57, 2559-2563 (1997).
8. Bischoff, J. et al. An adenovirus mutant that replicates selectively in p53-deficient human tumor cells. Science 274, 373-376 (1996).
9. Ramachandra, M. et al. Reengineering adenovirus regulatory pathways to enhance oncolytic specificity and efficacy. Nat. Biotechnol. 19, 1035-1041 (2001).
10. Hallenbeck, P.L. et al. A novel tumor-specific replication-restricted adenoviral vector for gene therapy of hepatocellular carcinoma. Hum. Gene Ther. 10, 1721-1733 (1999).
11. Kurihara, T., Brough, D.E., Kovesdi, I. & Kufe, D.W. Selectivity of a replication-competent adenovirus for human breast carcinoma cells expressing the MUC1 antigen. J. Clin. Invest. 106, 763-771 (2000).
12. Siders, W.M., Halloran, P.J. & Fenton, R.G. Transcriptional targeting of recombinant adenoviruses to human and murine melanoma cells. Cancer Res. 56, 5638-5646 (1996).
13. Blackburn, R.V., Galoforo, S.S., Corry, P.M. & Lee, Y.J. Adenoviral-mediated transfer of a heat-inducible double suicide gene into prostate carcinoma cells. Cancer Res. 58, 1358-1362 (1998).
14. Ring, C.J.A., Harris, J.D., Hurst, H.C. & Lemoine, N.R. Suicide gene expression induced in tumour cells transduced with recombinant adenoviral, retroviral and plasmid vectors containing the ERBB2 promoter. Gene Ther. 3, 1094-1103 (1996).
15. Doyle, G.A., Bourdeau-Heller, J.M., Coulthard, S., Meisner, L.F. & Ross, J. Amplification in human breast cancer of a gene encoding a c-myc mRNA-binding protein. Cancer Res. 60, 2756-2759 (2000).
16. Bauer, S.R. et al. Altered myc gene transcription and intron-induced stabilization of myc RNAs in two mouse plasmacytomas. Oncogene 4, 615-623 (1989).
17. Ross, J. mRNA stability in mammalian cells. Microbiol. Rev. 59, 423-450 (1995).
18. Derrigo, M., Cestelli, A., Savettieri, G. & Di Liegro, I. RNA-protein interactions in the control of stability and localization of messenger RNA (review). Int. J. Mol. Med. 5, 111-123 (2000).
19. Chen, C.Y. & Shyu, A.B. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470 (1995).
20. Caput, D. et al. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA 83, 1670-1674 (1986).
21. Shaw, G. & Kamen, R. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659-667 (1986).
22. Brook, M., Sully, G., Clark, A.R. & Saklatvala, J. Regulation of tumour necrosis factor alpha mRNA stability by the mitogen-activated protein kinase p38 signalling cascade. FEBS Lett. 483, 57-61 (2000).
23. Maity, A., McKenna, W.G. & Muschel, R.J. Evidence for post-transcriptional regulation of cyclin B1 mRNA in the cell cycle and following irradiation in HeLa cells. EMBO J. 14, 603-609 (1995).
24. Maity, A., McKenna, W.G. & Muschel, R.J. Cyclin A message stability varies with the cell cycle. Cell Growth Differ. 8, 311-318 (1997).
25. Lindsten, T., June, C.H., Ledbetter, J.A., Stella, G. & Thompson, C.B. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244, 339-343 (1989).
26. Sheng, H., Shao, J. & Dubois, R.N. K-Ras-mediated increase in cyclooxygenase 2 mRNA stability involves activation of the protein kinase B1. Cancer Res. 61, 2670-2675 (2001).
27. Claffey, K.P. et al. Identification of a human VPF/VEGF 3′ untranslated region mediating hypoxia-induced mRNA stability. Mol. Biol. Cell 9, 469-481 (1998).
28. Chen, C.Y., Xu, N. & Shyu, A.B. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol. Cell Biol. 15, 5777-5788 (1995).
29. Ross, H.J., Sato, N., Ueyama, Y. & Koeffler, H.P. Cytokine messenger RNA stability is enhanced in tumor cells. Blood 77, 1787-1795 (1991).
30. Lee, C.H., Bradley, G. & Ling, V. Increased P-glycoprotein messenger RNA stability in rat liver tumors in vivo. J. Cell Physiol. 177, 1-12 (1998).
31. Sidransky, H., Murty, C.N. & Verney, E. Turnover of messenger RNA in transplantable hepatomas and host liver of rats. Cancer Res. 38, 1645-1653 (1978).
32. Cao, Y. & Prescott, S.M. Many actions of cyclooxygenase-2 in cellular dynamics and in cancer. J. Cell Physiol. 190, 279-286 (2002).
33. Bakhle, Y.S. COX-2 and cancer: a new approach to an old problem. Br. J. Pharmacol. 134, 1137-1150 (2001).
34. Turini, M.E. & DuBois, R.N. Cyclooxygenase-2: a therapeutic target. Annu. Rev. Med. 53, 35-57 (2002).
35. Sheng, H. et al. Cyclooxygenase-2 induction and transforming growth factor β growth inhibition in rat intestinal epithelial cells. Cell Growth Differ. 8, 463-470 (1997).
36. Sheng, G.G. et al. A selective cyclooxygenase 2 inhibitor suppresses the growth of H-ras-transformed rat intestinal epithelial cells. Gastroenterology 113, 1883-1891 (1997).
37. Sheng, H. et al. Induction of cyclooxygenase-2 by activated Ha-ras oncogene in Rat-1 fibroblasts and the role of mitogen-activated protein kinase pathway. J. Biol. Chem. 273, 22120-22127 (1998).
38. Heasley, L.E. et al. Induction of cytosolic phospholipase A2 by oncogenic Ras in human non-small cell lung cancer. J. Biol. Chem. 272, 14501-14504 (1997).
39. Sheng, H. et al. Transforming growth factor-β1 enhances Ha-ras-induced expression of cyclooxygenase-2 in intestinal epithelial cells via stabilization of mRNA. J. Biol. Chem. 275, 6628-6635 (2000).
40. Dixon, D.A., Kaplan, C.D., McIntyre, T.M., Zimmerman, G.A. & Prescott, S.M. Posttranscriptional control of cyclooxygenase-2 gene expression. The role of the 3′-untranslated region. J. Biol. Chem. 275, 11750-11757 (2000).
41. Montero, L. & Nagamine, Y. Regulation by p38 mitogen-activated protein kinase of adenylate- and uridylate-rich element-mediated urokinase-type plasminogen activator (uPA) messenger RNA stability and uPA-dependent in vitro cell invasion. Cancer Res. 59, 5286-5293 (1999).
42. Gallouzi, I.E. et al. A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell Biol. 18, 3956-3965 (1998).
43. Chong, H., Ruchatz, A., Clackson, T., Rivera, V.M. & Vile, R.G. A system for small-molecule control of conditionally replication-competent adenoviral vectors. Mol. Ther. 5, 195-203 (2002).
44. Maity, A. & Solomon, D. Both increased stability and transcription contribute to the induction of the urokinase plasminogen activator receptor (uPAR) message by hypoxia. Exp. Cell Res. 255, 250-257 (2000).
45. Henderson, B.R., Tansey, W.P., Phillips, S.M., Ramshaw, I.A. & Kefford, R.F. Transcriptional and posttranscriptional activation of urokinase plasminogen activator gene expression in metastatic tumor cells. Cancer Res. 52, 2489-2496 (1992).
46. Li, Y.C. & Lieberman, M.W. Two genes associated with liver cancer are regulated by different mechanisms in rasT24 transformed liver epithelial cells. Oncogene 4, 795-798 (1989).
47. Stauber, C. & Schumperli, D. 3′ processing of pre-mRNA plays a major role in proliferation-dependent regulation of histone gene expression. Nucleic Acids Res. 16, 9399-9414 (1988).
48. Yamamoto, M., Alemany, R., Adachi, Y., Grizzle, W.E. & Curiel, D.T. Characterization of the cyclooxygenase-2 promoter in an adenoviral vector and its application for the mitigation of toxicity in suicide gene therapy of gastrointestinal cancers. Mol. Ther. 3, 385-394 (2001).