Yeast Cytosine Deaminase Mutants with Increased Thermostability Impart Sensitivity to 5-Fluorocytosine

Journal of Molecular Biology

Volumn 377, Issue 3, 2008, Pages 854-869

  Stolworthy, Tiffany S ^a   Korkegian, Aaron M ^b   Willmon, Candice L ^a   Ardiani, Andressa ^a   Cundiff, Jennifer ^a   Stoddard, Barry L ^b   Black, Margaret E ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

cytosine deaminase; prodrug gene therapy; random mutagenesis; structure; thermostability

Indexed keywords

CYTOSINE DEAMINASE; FLUCYTOSINE;

ANIMAL CELL; ARTICLE; CRYSTAL STRUCTURE; ENZYME KINETICS; HYDROPHOBICITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT; THERMOSTABILITY; TUMOR MODEL; YEAST;

ANIMALIA;

EID: 40649117959     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.01.002     Document Type: Article

References (55)

1. T. Nishiyama Y. Kawamura K. Kawamoto H. Matsumura N. Yamamoto T. Ito Antineoplastic effects in rats of 5-fluorocytosine in combination with cytosine deaminase capsules Cancer Res. 45 1985 1753 1761
2. G. Ireton G. McDermitt M.E. Black B.L. Stoddard The structure of Escherichia coli cytosine deaminase J. Mol. Biol. 315 2002 687 697
3. G.C. Ireton M.E. Black B.L. Stoddard The 1.14 Å crystal structure of yeast cytosine deaminase: evolution of nucleotide salvage enzymes and implications for genetic chemotherapy Structure (Camb.) 11 2003 961 972
4. B.E. Huber C.A. Richards T.A. Krenitsky Retroviral-mediated gene therapy for the treatment of hepatocellular carcinoma: an innovative approach for cancer therapy Proc. Natl Acad. Sci. USA 88 1991 8039 8043
5. R. Kanamaru H. Kakuta T. Sato C. Ishioka A. Wakui The inhibitory effects of 5-fluorouracil on the metabolism of preribosomal and ribosomal RNA in L-1210 cells in vitro Cancer Chemother. Pharmacol. 17 1986 43 46
6. H.M. Pinedo G.F. Peters Fluorouracil: biochemistry and pharmacology J. Clin. Oncol. 6 1988 1653 1664
7. D.M. Thomas J.R. Zalcberg 5-fluorouracil: a pharmacological paradigm in the use of cytotoxics Clin. Exp. Pharmacol. Physiol. 25 1998 887 895
8. S.A. Kaliberov J.M. Market G.Y. Gillespie V. Krendelchtchikova D. Della Manna J.C. Sellers Mutation of Escherichia coli cytosine deaminase significantly enhances molecular chemotherapy of human glioma Gene Ther. 14 2007 1111 1119
9. K. Hiraoka T. Kimura C.R. Logg C.K. Tai K. Haga G.W. Lawson N. Kasahara Therapeutic efficacy of replication-competent retrovirus vector-mediated suicide gene therapy in a multifocal colorectal cancer metastasis model Cancer Res. 67 2007 5345 5353
10. Y. Liu T. Ye J. Maynard H. Akbulut A. Deisseroth Engineering conditionally replication-competent adenoviral vectors carrying the cytosine deaminase gene increases the infectivity and therapeutic effect for breast cancer gene therapy Cancer Gene Ther. 13 2006 346 356
11. S.O. Freytag B. Movsas I. Aref H. Stricker J. Peabody J. Pegg Phase I trial of replication-competent adenovirus-mediated suicide gene therapy combined with IMRT for prostate cancer Mol. Ther. 15 2007 1016 1023
12. D.E. Post H. Shim E. Toussaint-Smith E.G. Van Meir Cancer Scene Investigation: how a cold virus became a tumor killer Future Oncol. 1 2005 247 258
13. K.N. Barton D. Paielli Y. Zhang S. Koul S.L. Brown M. Lu Second-generation replication-competent oncolytic adenovirus armed with improved suicide genes and ADP gene demonstrates greater efficacy without increased toxicity Mol. Ther. 13 2006 347 356
14. S.O. Freytag H. Stricker J. Pegg D. Paielli D.G. Pradhan J. Peabody Phase I study of replication-competent adenovirus-mediated double-suicide gene therapy in combination with conventional-dose three-dimensional conformal radiation therapy for the treatment of newly diagnosed, intermediate- to high-risk prostate cancer Cancer Res. 63 2003 7497 7506
15. S.O. Freytag M. Khil H. Stricker J. Peabody M. Menon M. DePeralta-Venturina Phase I study of replication-competent adenovirus-mediated double suicide gene therapy for the treatment of locally recurrent prostate cancer Cancer Res. 62 2002 4968 4976
16. R.B. Diasio D.E. Laking J.E. Bennett Evidence for conversion of 5-fluorocytosine to 5-fluorouracil in humans: possible factor in 5-fluorocytosine clinical toxicity Antimicrob. Agents Chemother. 14 1978 903 908
17. T.S. Lawrence A. Rehemtulla E.Y. Ng M. Wilson J.E. Trosko P.L. Stetson Preferential cytotoxicity of cells transduced with cytosine deaminase compared to bystander cells after treatment with 5-flucytosine Cancer Res. 58 1998 2588 2593
18. D.K. Hoganson R.K. Batra J.C. Olsen R.C. Boucher Comparison of the effects of three different toxin genes and their levels of expression on cell growth and bystander effect in lung adenocarcinoma Cancer Res. 56 1996 1315 1323
19. S. Kuriyama K. Masui T. Sakamoto T. Nakatani M. Kikukawa H. Tsujinoue Bystander effect caused by cytosine deaminase gene and 5-fluorocytosine in vitro is substantially mediated by generated 5-fluorouracil Anticancer Res. 18 1998 3399 3406
20. E. Nishihara Y. Nagayama M. Narimatsu H. Namba M. Watanabe M. Niwa S. Yamashita Treatment of thyroid carcinoma cells with four different suicide gene/prodrug combinations in vitro Anticancer Res. 18 1998 1521 1525
21. Q.T. Trinh E.A. Austin D.M. Murray V.C. Knick B.E. Huber 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. 55 1995 4808 4812
22. E. Kievit M.K. Nyati E. Ng L.D. Stegman J. Parsels B.D. Ross Yeast cytosine deaminase improves radiosensitization and bystander effect by 5-fluorocytosine of human colorectal cancer xenografts Cancer Res. 60 2000 6649 6655
23. T.S. Lawrence M.A. Davis J. Maybaum Dependence of 5-fluorouracil-mediated radiosensitization on DNA-directed effects Int. J. Radiat. Oncol., Biol., Phys. 29 1994 519 523
24. D.A. Hamstra D.J. Rice A. Pu D. Oyedijo B.D. Ross A. Rehemtulla Combined radiation and enzyme/prodrug treatment for head and neck cancer in an orthotopic animal model Radiat. Res. 152 1999 499 507
25. M.A. Stackhouse L.C. Pederson W.E. Grizzle D.T. Curiel J. Gebert K. Haack Fractionated radiation therapy in combination with adenoviral delivery of the cytosine deaminase gene and 5-fluorocytosine enhances cytotoxic and antitumor effects in human colorectal and cholangiocarcinoma models Gene Ther. 7 2000 1019 1026
26. L. Yao Y. Li Y. Wu A. Liu H. Yan Product release is rate-limiting in the activation of the prodrug 5-fluorocytosine by yeast cytosine deaminase Biochemistry 44 2005 5940 5947
27. E. Kievit E. Bershad E. Ng P. Sethna I. Dev T.S. Lawrence A. Rehemtulla Superiority of yeast over bacterial cytosine deaminase for enzyme/prodrug gene therapy in colon cancer xenografts Cancer Res. 59 1999 1417 1421
28. T. Katsuragi T. Sakai K. Tonomura Implantable enzyme capsules for cancer chemotherapy from bakers' yeast cytosine deaminase immobilized on epoxy–acrylic resin and urethane prepolymer Appl. Biochem. Biotechnol. 16 1987 61 69
29. A. Korkegian M.E. Black D. Baker B.L. Stoddard Computational thermostabilization of an enzyme Science 308 2005 857 860
30. G.J. Davies S.J. Gamblin J.A. Littlechild H.C. Watson The structure of a thermally stable 3-phosphoglycerate kinase and a comparison with its mesophilic equivalent Proteins: Struct. Funct. Genet. 15 1993 283 289
31. K.S. Yip T.J. Stillman K.L. Britton P.J. Artymiuk P.J. Baker S.E. Sedelnikova The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures Structure 3 1995 1147 1158
32. D.W. Rice K.S. Yip T.J. Stillman K.L. Britton A. Fuentes I. Connerton Insights into the molecular basis of thermal stability from the structure determination of Pyrococcus furiosus glutamate dehydrogenase FEMS Microbiol. Rev. 18 1996 105 117
33. G.W. Harris R.W. Pickersgill I. Connerton P. Debeire J.P. Touzel C. Breton S. Perez Structural basis of the properties of an industrially relevant thermophilic xylanase Proteins: Struct. Funct. Genet. 29 1997 77 86
34. G. Wallon G. Kryger S.T. Lovett T. Oshima D. Ringe G.A. Petsko Crystal structures of Escherichia coli and Salmonella typhimurium 3-isopropylmalate dehydrogenase and comparison with their thermophilic counterpart from Thermus thermophilus J. Mol. Biol. 266 1997 1016 1031
35. R.J. Russell J.M. Ferguson D.W. Hough M.J. Danson G.L. Taylor The crystal structure of citrate synthase from the hyperthermophilic archaeon Pyrococcus furiosus at 1.9 Å resolution Biochemistry 36 1997 9983 9994
36. D. Baker J.L. Sohl D.A. Agard A protein folding reaction under kinetic control Nature 356 1992 263 265
37. B.A. Kelch D.A. Agard Mesophile versus thermophile: insights into the structural mechanisms of kinetic stability J. Mol. Biol. 370 2007 784 795
38. G.U. Dachs J. Tupper G.M. Tozer From bench to bedside for gene-directed enzyme prodrug therapy of cancer Anticancer Drugs 16 2005 349 359
39. J.S. Norris K.L. Norris D.H. Holman A. El-Zawahry T.E. Keane J.Y. Dong M. Tavassoli The present and future for gene and viral therapy of directly accessible prostate and squamous cell cancers of the head and neck Future Oncol. 1 2005 115 123
40. M.E. Black M.S. Kokoris P. Sabo Herpes simplex virus-1 thymidine kinase mutants created by semi-random sequence mutagenesis improve prodrug-mediated tumor cell killing Cancer Res. 61 2001 3022 3026
41. R. Wiedrodt K. Amin M. Kiefer V.P. Jovanovic V. Kapoor S. Force Adenovirus-mediated gene transfer of enhanced herpes simplex virus thymidine kinase mutants improves prodrug-mediated tumor cell killing Cancer Gene Ther. 10 2003 353 364
42. K.R. Rogulski J.H. Kim S.H. Kim S.O. Freytag Glioma cells transduced with an Escherichia coli CD/HSV-1 TK fusion gene exhibit enhanced metabolic suicide and radiosensitivity Hum. Gene Ther. 8 1997 73 85
43. P. Erbs E. Regulier J. Kintz P. Leroy Y. Poitevin F. Exinger In vivo cancer gene therapy by adenovirus-mediated transfer of a bifunctional yeast cytosine deaminase/uracil phosphoribosyltransferase fusion gene Cancer Res. 60 2000 3813 3822
44. Y. Adachi T. Tamiya T. Ichikawa K. Terada Y. Ono K. Matsumoto Experimental gene therapy for brain tumors using adenovirus-mediated transfer of cytosine deaminase gene and uracil phosphoribosyltransferase gene with 5-fluorocytosine Hum. Gene Ther. 11 2000 77 89
45. C.L. Willmon E. Krabbenhoft M.E. Black A guanylate kinase/HSV-1 thymidine kinase fusion protein enhances prodrug-mediated cell killing Gene Ther. 13 2006 1309 1312
46. J.E. Kurtz M.E. Black Enhancement of suicide gene prodrug activation by random mutagenesis Methods Mol. Med. 90 2004 331 344
47. T.A. Kunkel J.D. Roberts R.A. Zakour Rapid and efficient site-specific mutagenesis without phenotypic selection Methods Enzymol. 154 1987 367 382
48. S.D. Mahan G.C. Ireton B.L. Stoddard M.E. Black Alanine-scanning mutagenesis reveals a cytosine deaminase mutant with altered substrate preference Biochemistry 43 2004 8957 8964
49. M.S. Kokoris P. Sabo E.T. Adman M.E. Black Enhancement of tumor ablation by a selected HSV-1 thymidine kinase mutant Gene Ther. 6 1999 1415 1426
50. G. Dantas B. Kuhlman D. Callender M. Wong D. Baker A large scale test of computational protein design: folding and stability of nine completely redesigned globular proteins J. Mol. Biol. 332 2003 449 460
51. Z. Otwinowski W. Minor Processing of x-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
52. C.R. Kissinger D.K. Gehlhaar D.B. Fogel Rapid automated molecular replacement by evolutionary search Acta Crystallogr., Sect. D: Biol. Crystallogr. 55 1999 484 491
53. A.T. Brunger Assessment of phase accuracy by cross validation: the free R value. Methods and applications Acta Crystallogr., Sect. D: Biol. Crystallogr. 49 1993 24 36
54. A.T. Brunger P.D. Adams G.M. Clore W.L. DeLano P. Gros R.W. Grosse-Kunstleve Crystallography & NMR System: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 1998 905 921
55. D.E. McRee A visual protein crystallographic software system for X11/XView J. Mol. Graphics 10 1992 44 46