Fusion of the HSV-1 tegument protein vp22 to cytosine deaminase confers enhanced bystander effect and increased therapeutic benefit

Gene Therapy

Volumn 13, Issue 2, 2006, Pages 127-137

  Lee, K C ^a   Hamstra, D A ^a   Bullarayasamudram, S ^a   Bhojani, M S ^a   Moffat, B A ^a   Dornfeld, K J ^a   Ross, B D ^a   Rehemtulla, A ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Bystander effect; Cytosine deaminase; GDEPT; Magnetic resonance spectroscopy; vp22

Indexed keywords

ADENOVIRUS VECTOR; CYTOSINE DEAMINASE; FLUCYTOSINE; FLUOROURACIL; PROTEIN VP22;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BYSTANDER EFFECT; CANCER CELL CULTURE; CANCER INHIBITION; COLONY FORMATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG METABOLISM; DRUG POTENTIATION; DRUG SENSITIVITY; GENE EXPRESSION; GENETIC TRANSDUCTION; GLIOSARCOMA; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WILD TYPE;

ADENOVIRIDAE; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BYSTANDER EFFECT; CELL LINE; CYTOSINE DEAMINASE; FLUCYTOSINE; FLUOROURACIL; GENE FUSION; GENE THERAPY; GENETIC ENGINEERING; HUMANS; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, NUDE; SACCHAROMYCES CEREVISIAE; TRANSDUCTION, GENETIC; TRANSLOCATION, GENETIC; VIRAL STRUCTURAL PROTEINS;

ADENOVIRIDAE; ANIMALIA; HUMAN HERPESVIRUS 1; SACCHAROMYCES CEREVISIAE;

EID: 29944440529     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/sj.gt.3302631     Document Type: Article

References (47)

1. Kerr DJ, Young LS, Searle PF, McNeish IA. Gene directed enzyme prodrug therapy for cancer. Adv Drug Deliv Rev 1997; 26: 173-184.
2. Lawrence TS, Rehemtulla A, Ng EY, Wilson M, Trosko JE, Stetson PL. Preferential cytotoxicity of cells transduced with cytosine deaminase compared to bystander cells after treatment with 5-flucytosine. Cancer Res 1998; 58: 2588-2593.
3. Trinh QT, Austin EA, Murray DM, Knick VC, Huber BE. Enzyme/prodrug gene therapy: Comparison of cytosine deaminase/5-fluorocytosine versus thymidine kinase/ganciclovir enzyme/prodrug systems in a human colorectal carcinoma cell line. Cancer Res 1995; 55: 4808-4812.
4. Mesnil M, Piccoli C, Tiraby G, Willecke K, Yamasaki H. Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins. Proc Natl Acad Sci USA 1996; 93: 1831-1835.
5. Kievit E, Bershad E, Ng E, Sethna P, Dev I, Lawrence TS et al. Superiority of yeast over bacterial cytosine deaminase for enzyme/ prodrug gene therapy in colon cancer xenografts. Cancer Res 1999; 59: 1417-1421.
6. Hamstra DA, Rice DJ, Fahmy S, Ross BD, Rehemtulla A. Enzyme/prodrug therapy for head and neck cancer using a catalytically superior cytosine deaminase. Hum Gene Ther 1999; 10: 1993-2003.
7. Erbs P, Regulier E, Kintz J, Leroy P, Poitevin Y, Exinger F et al. In vivo cancer gene therapy by adenovirus-mediated transfer of a bifunctional yeast cytosine deaminase/uracil phosphoribosyltransferase fusion gene. Cancer Res 2000; 60: 3813-3822.
8. Hamstra DA, Lee KC, Tychewicz JM, Schepkin VD, Moffat BA, Chen M et al. The use of (19)F spectroscopy and diffusion-weighted MRI to evaluate differences in gene-dependent enzyme prodrug therapies. Mol Ther 2004; 10: 916-928.
9. Kambara H, Tamiya T, Ono Y, Ohtsuka S, Terada K, Adachi Y et al. Combined radiation and gene therapy for brain tumors with adenovirus-mediated transfer of cytosine deaminase and uracil phosphoribosyltransferase genes. Cancer Gene Ther 2002; 9: 840-845.
10. Miyagi T, Koshida K, Hori O, Konaka H, Katoh H, Kitagawa Y et al. Gene therapy for prostate cancer using the cytosine deaminase/uracil phosphoribosyltransferase suicide system. J Gene Med 2003; 5: 30-37.
11. Tiraby M, Cazaux C, Baron M, Drocourt D, Reynes JP, Tiraby G. Concomitant expression of E. coli cytosine deaminase and uracil phosphoribosyltransferase improves the cytotoxicity of 5-fluorocytosine. FEMS Microbiol Lett 1998; 167: 41-49.
12. Verma IM, Somia N. Gene therapy - promises, problems and prospects. Nature 1997; 389: 239-242.
13. Somia N, Verma IM. Gene therapy: Trials and tribulations. Nat Rev Genet 2000; 1: 91-99.
14. McCormick F. Cancer gene therapy: Fringe or cutting edge? Nat Rev Cancer 2001; 1: 130-141.
15. Greco O, Scott SD, Marples B, Dachs GU. Cancer gene therapy: 'delivery, delivery, delivery'. Front Biosci 2002; 7: D1516-d1524.
16. Dachs GU, Dougherty GJ, Stratford IJ, Chaplin DJ. Targeting gene therapy to cancer: A review. Oncol Res 1997; 9: 313-325.
17. Huber BE, Austin EA, Richards CA, Davis ST, Good SS. Metabolism of 5-fluorocytosine to 5-fluorouracil in human colorectal tumor cells transduced with the cytosine deaminase gene: Significant antitumor effects when only a small percentage of tumor cells express cytosine deaminase. Proc Natl Acad Sci USA 1994; 91: 8302-8306.
18. Luft FC. Can VP22 resurrect gene therapy? J Mol Med 1999; 77: 575-576.
19. Lundberg P, Langel U. A brief introduction to cell-penetrating peptides. J Mol Recognit 2003; 16: 227-233.
20. Snyder EL, Dowdy SF. Cell penetrating peptides in drug delivery. Pharm Res 2004; 21: 389-393.
21. Trehin R, Merkle HP. Chances and pitfalls of cell penetrating peptides for cellular drug delivery. Eur J Pharm Biopharm 2004; 58: 209-223.
22. Elliott G, O'Hare P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 1997; 88: 223-233.
23. Martin A, O'Hare P, McLauchlan J, Elliott G. Herpes simplex virus tegument protein VP22 contains overlapping domains for cytoplasmic localization, microtubule interaction, and chromatin binding. J Virol 2002; 76: 4961-4970.
24. Aints A, Dilber MS, Smith CI. Intercellular spread of GFP-VP22. J Gene Med 1999; 1: 275-279.
25. Cashman SM, Sadowski SL, Morris DJ, Frederick J, Kumar-Singh R. Intercellular trafficking of adenovirus-delivered HSV VP22 from the retinal pigment epithelium to the photoreceptors - implications for gene therapy. Mol Ther 2002; 6: 813-823.
26. Elliott G, O'Hare P. Intercellular trafficking of VP22-GFP fusion proteins. Gene Therapy 1999; 6: 149-151.
27. Elliott G, O'Hare P. Live-cell analysis of a green fluorescent protein-tagged herpes simplex virus infection. J Virol 1999; 73: 4110-4119.
28. Wybranietz WA, Prinz F, Spiegel M, Schenk A, Bitzer M, Gregor M et al. Quantification of VP22-GFP spread by direct fluorescence in 15 commonly used cell lines. J GeneMed 1999; 1: 265-274.
29. Phelan A, Elliott G, O'Hare P. Intercellular delivery of functional p53 by the herpesvirus protein VP22. Nat Biotechnol 1998; 16: 440-443.
30. Dilber MS, Phelan A, Aints A, Mohamed AJ, Elliott G, Smith CI et al. Intercellular delivery of thymidine kinase prodrug activating enzyme by the herpes simplex virus protein, VP22. Gene Therapy 1999; 6: 12-21.
31. Liu CS, Kong B, Xia HH, Ellem KA, Wei MQ. VP22 enhanced intercellular trafficking of HSV thymidine kinase reduced the level of ganciclovir needed to cause suicide cell death. J Gene Med 2001; 3: 145-152.
32. Wybranietz WA, Gross CD, Phelan A, O'Hare P, Spiegel M, Graepler F et al. Enhanced suicide gene effect by adenoviral transduction of a VP22-cytosine deaminase (CD) fusion gene. Gene Therapy 2001; 8: 1654-1664.
33. Kong BH, Wang WX, Liu CS, Ma DX, Qu X. Tegument viral protein 22 enhanced cell-killing effect of the herpes simplex virus thymidine kinase/ganciclovir system on ovarian cancer in vivo. Zhonghua Fu Chan Ke Za Zhi 2003; 38: 195-198.
34. Qiu Z, Harms JS, Zhu J, Splitter GA. Bovine herpesvirus tegument protein VP22 enhances thymidine kinase/ganciclovir suicide gene therapy for neuroblastomas compared to herpes simplex virus VP22. J Virol 2004; 78: 4224-4233.
35. Stegman LD, Rehemtulla A, Beattie B, Kievit E, Lawrence TS, Blasberg RG et al. Noninvasive quantitation of cytosine deaminase transgene expression in human tumor xenografts with in vivo magnetic resonance spectroscopy. Proc Natl Acad Sci USA 1999; 96: 9821-9826.
36. Stevens AN, Morris PG, Iles RA, Sheldon PW, Griffiths JR. 5-fluorouracil metabolism monitored in vivo by 19F NMR. Br J Cancer 1984; 50: 113-117.
37. Stegman LD, Rehemtulla A, Hamstra DA, Rice DJ, Jonas SJ, Stout KL et al. Diffusion MRI detects early events in the response of a glioma model to the yeast cytosine deaminase gene therapy strategy. Gene Therapy 2000; 7: 1005-1010.
38. Kievit E, Nyati MK, Ng E, Stegman LD, Parsels J, Ross BD et al. Yeast cytosine deaminase improves radiosensitization and bystander effect by 5-fluorocytosine of human colorectal cancer xenografts. Cancer Res 2000; 60: 6649-6655.
39. Segota E, Bukowski RM. The promise of targeted therapy: Cancer drugs become more specific. Cleve Clin J Med 2004; 71: 551-560.
40. Aghi M, Hochberg F, Breakefield XO. Prodrug activation enzymes in cancer gene therapy. J Gene Med 2000; 2: 148-164.
41. Greco O, Dachs GU. Gene directed enzyme/prodrug therapy of cancer: historical appraisal and future prospectives. J Cell Physiol 2001; 187: 22-36.
42. Freeman SM, Abboud CN, Whartenby KA, Packman CH, Koeplin DS, Moolten FL et al. The 'bystander effect': Tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 1993; 53: 5274-5283.
43. Rehemtulla A, Hamstra DA, Kievit E, Davis MA, Ng EY, Dornfeld K et al. Extracellular expression of cytosine deaminase results in increased 5-FU production for enhanced enzyme/prodrug therapy. Anticancer Res 2004; 24: 1393-1399.
44. Mullen CA, Kilstrup M, Blaese RM. Transfer of the bacterial gene for cytosine deaminase to mammalian cells confers lethal sensitivity to 5-fluorocytosine: A negative selection system. Proc Natl Acad Sci USA 1992; 89: 33-37.
45. Wygoda MR, Wilson MR, Davis MA, Trosko JE, Rehemtulla A, Lawrence TS. Protection of herpes simplex virus thymidine kinase-transduced cells from ganciclovir-mediated cytotoxicity by bystander cells: The Good Samaritan effect. Cancer Res 1997; 57: 1699-1703.
46. Rehemtulla A, Hall DE, Stegman LD, Prasad U, Chen G, Bhojani MS et al. Molecular imaging of gene expression and efficacy following adenoviral-mediated brain tumor gene therapy. Mol Imaging 2002; 1: 43-55.
47. Lawrence TS. Reduction of doxorubicin cytotoxicity by ouabain: correlation with topoisomerase-induced DNA strand breakage in human and hamster cells. Cancer Res 1988; 48: 725-730.