MLH1 deficiency enhances tumor cell sensitivity to ganciclovir

Cancer Gene Therapy

Volumn 16, Issue 9, 2009, Pages 683-692

  O'Konek, J J ^a   Boucher, P D ^a   Iacco, A A ^a   Wilson, T E ^a   Shewach, D S ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Ganciclovir; Mismatch repair; MLH1

Indexed keywords

GANCICLOVIR; PROTEIN MLH1; SMALL INTERFERING RNA; THYMIDINE KINASE;

ARTICLE; CELL SURVIVAL; COLON CARCINOMA; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG METABOLISM; DRUG SENSITIVITY; GLIOBLASTOMA; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; SUICIDE GENE THERAPY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE, TUMOR; CELL SURVIVAL; COLONIC NEOPLASMS; DNA DAMAGE; DNA MISMATCH REPAIR; GANCICLOVIR; GENE THERAPY; GLIOBLASTOMA; HUMANS; NUCLEAR PROTEINS; RNA, SMALL INTERFERING; SACCHAROMYCES CEREVISIAE;

SIMPLEXVIRUS;

EID: 68949220996     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2009.16     Document Type: Article

References (50)

1. Greco O, Dachs GU. Gene directed enzyme/prodrug therapy of cancer: historical appraisal and future prospectives. J Cell Physiol 2001; 187: 22-36.
2. O'Malley Jr BW, Chen SH, Schwartz MR, Woo SL. Adenovirus-mediated gene therapy for human head and neck squamous cell cancer in a nude mouse model. Cancer Res 1995; 55: 1080-1085.
3. Boucher PD, Ruch RJ, Shewach DS. Differential ganciclovir-mediated cytotoxicity and bystander killing in human colon carcinoma cell lines expressing herpes simplex virus thymidine kinase. Hum Gene Ther 1998; 9: 801-814.
4. Freytag SO, Paielli D, Wing M, Rogulski K, Brown S, Kolozsvary A et al. Efficacy and toxicity of replication-competent adenovirus-mediated double suicide gene therapy in combination with radiation therapy in an orthotopic mouse prostate cancer model. Int J Radiat Oncol Biol Phys 2002; 54: 873-885.
5. Roth JA, Cristiano RJ. Gene therapy for cancer: what have we done and where are we going? J Natl Cancer Inst 1997; 89: 21-39.
6. Trask TW, Trask RP, Aguilar-Cordova E, Shine HD, Wyde PR, Goodman JC et al. Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. Mol Ther 2000; 1: 195-203.
7. Smitt PS, Driesse M, Wolbers J, Kros M, Avezaat C. Treatment of relapsed malignant glioma with an adenoviral vector containing the herpes simplex thymidine kinase gene followed by ganciclovir. Mol Ther 2003; 7: 851-858.
8. Freytag SO, Stricker H, Pegg J, Paielli D, Pradhan DG, Peabody J et al. 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 2003; 63: 7497-7506.
9. Rubsam LZ, Davidson BL, Shewach DS. Superior cytotoxicity with ganciclovir compared with acyclovir and 1-beta-D-arabinofuranosylthymine in herpes simplex virus-thymidine kinase-expressing cells: a novel paradigm for cell killing. Cancer Res 1998; 58: 3873-3882.
10. Halloran PJ, Fenton RG. Irreversible G2-M arrest and cytoskeletal reorganization induced by cytotoxic nucleoside analogues. Cancer Res 1998; 58: 3855-3865.
11. Wei SJ, Chao Y, Hung YM, Lin WC, Yang DM, Shih YL et al. S- and G2-phase cell cycle arrests and apoptosis induced by ganciclovir in murine melanoma cells transduced with herpes simplex virus thymidine kinase. Exp Cell Res 1998; 241: 66-75.
12. Tomicic MT, Thust R, Kaina B. Ganciclovir-induced apoptosis in HSV-1 thymidine kinase expressing cells: critical role of DNA breaks, Bcl-2 decline and caspase-9 activation. Oncogene 2002; 21: 2141-2153.
13. Beltinger C, Fulda S, Kammertoens T, Meyer E, Uckert W, Debatin KM. Herpes simplex virus thymidine kinase/ganciclovir-induced apoptosis involves ligand-independent death receptor aggregation and activation of caspases. Proc Natl Acad Sci USA 1999; 96: 8699-8704.
14. Tomicic MT, Thust R, Sobol RW, Kaina B. DNA polymerase beta mediates protection of mammalian cells against ganciclovir-induced cytotoxicity and DNA breakage. Cancer Res 2001; 61: 7399-7403.
15. Boucher PD, Ostruszka LJ, Shewach DS. Synergistic enhancement of herpes simplex virus thymidine kinase/ganciclovir-mediated cytoxicity by hydroxyurea. Cancer Res 2000; 60: 1631-1636.
16. Boucher PD, Ostruszka LJ, Murphy PJ, Shewach DS. Hydroxyurea significantly enhances tumor growth delay in vivo with herpes simplex virus thymidine kinase/ganciclovir gene therapy. Gene Therapy 2002; 9: 1023-1030.
17. Gentry BG, Boucher PD, Shewach DS. Hydroxyurea induces bystander cytotoxicity in cocultures of herpes simplex virus thymidine kinase-expressing and nonexpressing HeLa cells incubated with ganciclovir. Cancer Res 2006; 66: 3845-3851.
18. Kunz BA. Genetic effects of deoxyribonucleotide pool imbalances. Environ Mutagen 1982; 4: 695-725.
19. Bebenek K, Roberts JD, Kunkel TA. The effects of dNTP pool imbalances on frameshift fidelity during DNA replication. J Biol Chem 1992; 267: 3589-3596.
20. Martomo SA, Mathews CK. Effects of biological DNA precursor pool asymmetry upon accuracy of DNA replication in vitro. Mutat Res 2002; 499: 197-211.
21. Carethers JM, Hawn MT, Chauhan DP, Luce MC, Marra G, Koi M et al. Competency in mismatch repair prohibits clonal expansion of cancer cells treated with N-methyl-N′-nitro-N-nitrosoguanidine. J Clin Invest 1996; 98: 199-206.
22. Jacob S, Aguado M, Fallik D, Praz F. The role of the DNA mismatch repair system in the cytotoxicity of the topoisomerase inhibitors camptothecin and etoposide to human colorectal cancer cells. Cancer Res 2001; 61: 6555-6562.
23. Wilson TE. A genomics-based screen for yeast mutants with an altered recombination/end-joining repair ratio. Genetics 2002; 162: 677-688.
24. Wilson TE, Lieber MR. Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J Biol Chem 1999; 274: 23599-23609.
25. Vance JR, Wilson TE. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc Natl Acad Sci USA 2002; 99: 13669-13674.
26. Gentry BG, Im M, Boucher PD, Ruch RJ, Shewach DS. GCV phosphates are transferred between HeLa cells despite lack of bystander cytotoxicity. Gene Therapy 2005; 12: 1033-1041.
27. Taverna P, Liu L, Hanson AJ, Monks A, Gerson SL. Characterization of MLH1 and MSH2 DNA mismatch repair proteins in cell lines of the NCI anticancer drug screen. Cancer Chemother Pharmacol 2000; 46: 507-516.
28. Simon JA, Szankasi P, Nguyen DK, Ludlow C, Dunstan HM, Roberts CJ et al. Differential toxicities of anticancer agents among DNA repair and checkpoint mutants of Saccharomyces cerevisiae. Cancer Res 2000; 60: 328-333.
29. Cejka P, Mojas N, Gillet L, Schar P, Jiricny J. Homologous recombination rescues mismatch-repair-dependent cytotoxicity of S(N)1-type methylating agents in S. cerevisiae. Curr Biol 2005; 15: 1395-1400.
30. Osman F, Whitby MC. Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair (Amst) 2007; 6: 1004-1017.
31. Natsume R, Eitoku M, Akai Y, Sano N, Horikoshi M, Senda T. Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4. Nature 2007; 446: 338-341.
32. O'Konek JJ, Boucher PD, Shewach DS. Activation of mismatch repair protects cells against ganciclovir cytotoxicity through decreasing errors in DNA replication. Proc Am Assoc Cancer Res 2007; 48.
33. Cortellino S, Turner D, Masciullo V, Schepis F, Albino D, Daniel R et al. The base excision repair enzyme MED1 mediates DNA damage response to antitumor drugs and is associated with mismatch repair system integrity. Proc Natl Acad Sci USA 2003; 100: 15071-15076.
34. Zhang H, Richards B, Wilson T, Lloyd M, Cranston A, Thorburn A et al. Apoptosis induced by overexpression of hMSH2 or hMLH1. Cancer Res 1999; 59: 3021-3027.
35. Fang Y, Tsao CC, Goodman BK, Furumai R, Tirado CA, Abraham RT et al. ATR functions as a gene dosage-dependent tumor suppressor on a mismatch repair-deficient background. EMBO J 2004; 23: 3164-3174.
36. Robinson BW, Im MM, Ljungman M, Praz F, Shewach DS. Enhanced radiosensitization with gemcitabine in mismatch repair-deficient HCT116 cells. Cancer Res 2003; 63: 6935-6941.
37. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411: 366-374.
38. Pouliot JJ, Yao KC, Robertson CA, Nash HA. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 1999; 286: 552-555.
39. Interthal H, Chen HJ, Kehl-Fie TE, Zotzmann J, Leppard JB, Champoux JJ. SCAN1 mutant Tdp1 accumulates the enzyme-DNA intermediate and causes camptothecin hypersensitivity. EMBO J 2005; 24: 2224-2233.
40. Thust R, Tomicic M, Klocking R, Wutzler P, Kaina B. Cytogenetic genotoxicity of anti-herpes purine nucleoside analogues in CHO cells expressing the thymidine kinase gene of herpes simplex virus type 1: comparison of ganciclovir, penciclovir and aciclovir. Mutagenesis 2000; 15: 177-184.
41. Tomicic MT, Bey E, Wutzler P, Thust R, Kaina B. Comparative analysis of DNA breakage, chromosomal aberrations and apoptosis induced by the anti-herpes purine nucleoside analogues aciclovir, ganciclovir and penciclovir. Mutat Res 2002; 505: 1-11.
42. Helleday T. Pathways for mitotic homologous recombination in mammalian cells. Mutat Res 2003; 532: 103-115.
43. Zhou Z, Elledge SJ. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 1993; 75: 1119-1127.
44. Huang M, Zhou Z, Elledge SJ. The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 1998; 94: 595-605.
45. Boucher PD, Shewach DS. In vitro and in vivo enhancement of ganciclovir-mediated bystander cytotoxicity with gemcitabine. Mol Ther 2005; 12: 1064-1071.
46. Parrilla-Castellar ER, Arlander SJ, Karnitz L. Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst) 2004; 3: 1009-1014.
47. Peltomaki P. Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 2003; 21: 1174-1179.
48. Freytag SO, Stricker H, Movsas B, Kim JH. Prostate cancer gene therapy clinical trials. Mol Ther 2007; 15: 1042-1052.
49. Sommadossi JP, Bevan R. High-performance liquid chromatographic method for the determination of 9-(1,3-dihydroxy-2-propoxymethyl)guanine in human plasma. J Chromatogr 1987; 414: 429-433.
50. Faulds D, Heel RC. Ganciclovir. A review of its antiviral activity, pharmacokinetic properties and therapeutic efficacy in cytomegalovirus infections. Drugs 1990; 39: 597-638.