Uracil-DNA glycosylase expression determines human lung cancer cell sensitivity to pemetrexed

Molecular Cancer Therapeutics

Volumn 12, Issue 10, 2013, Pages 2248-2260

  Weeks, Lachelle D ^a,c   Fu, Pingfu ^b,c   Gerson, Stanton L ^a,c  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; METHOXYAMINE; PEMETREXED; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; URACIL; URACIL DNA GLYCOSIDASE;

ARTICLE; CANCER CELL CULTURE; CANCER RESISTANCE; CONTROLLED STUDY; DNA REPLICATION; DNA STRAND BREAKAGE; DRUG SENSITIVITY; EXCISION REPAIR; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPLICATION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMATES; GUANINE; HUMANS; LUNG NEOPLASMS; RNA, SMALL INTERFERING; URACIL-DNA GLYCOSIDASE;

EID: 84885576391     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0172     Document Type: Article

References (50)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62: 10-29.
2. Felip E, Stahel RA, Pavlidis N, Force EGT. ESMO Minimum Clinical Recommendations for diagnosis, treatment and follow-up of non- small cell lung cancer (NSCLC). Ann Oncol 2005;16 Suppl 1:i28-9.
3. Hanna N, Shepherd FA, Fossella FV, Pereira JR, De Marinis F, von Pawel J, et al. Randomized phase III trial of pemetrexed versus docetaxel in patients with non-small cell lung cancer previously treated with chemotherapy. J Clin Oncol 2004;22: 1589-97.
4. Scagliotti GV, Parikh P, von Pawel J, Biesma B, Vansteenkiste J, Manegold C, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small cell lung cancer. J Clin Oncol 2008;26: 3543-51.
5. Ciuleanu T, Brodowicz T, Zielinski C, Kim JH, Krzakowski M, Laack E, et al. Maintenance pemetrexed plus best supportive care versus placebo plus best supportive care for non-small cell lung cancer: a randomised, double-blind, phase III study. Lancet 2009;374: 1432-40.
6. Shih C, Chen VJ, Gossett LS, Gates SB, MacKellar WC, Habeck LL, et al. LY231514, a pyrrolo[2,3-d]pyrimidine-based antifolate that inhibits multiple folate-requiring enzymes. Cancer Res 1997;57: 1116-23.
7. Curtin NJ, Hughes AN. Pemetrexed disodium, a novel antifolate with multiple targets. Lancet Oncol 2001;2: 298-306.
8. Van Triest B, Pinedo HM, Giaccone G, Peters GJ. Downstream molecular determinants of response to 5-fluorouracil and antifolate thymidylate synthase inhibitors. Ann Oncol 2000;11: 385-91.
9. Berger SH, Pittman DL, Wyatt MD. Uracil in DNA: consequences for carcinogenesis and chemotherapy. Biochem Pharmacol 2008;76: 697-706.
10. Assaraf YG. Molecular basis of antifolate resistance. Cancer Metastasis Rev 2007;26: 153-81.
11. Hanauske AR, Eismann U, Oberschmidt O, Pospisil H, Hoffmann S, Hanauske-Abel H, et al. In vitro chemosensitivity of freshly explanted tumor cells to pemetrexed is correlated with target gene expression. Invest New Drugs 2007;25: 417-23.
12. Ozasa H, Oguri T, Uemura T, Miyazaki M, Maeno K, Sato S, et al. Significance of thymidylate synthase for resistance to pemetrexed in lung cancer. Cancer Sci 2010;101: 161-6.
13. Zhang D, Ochi N, Takigawa N, Tanimoto Y, Chen Y, Ichihara E, et al. Establishment of pemetrexed-resistant non-small cell lung cancer cell lines. Cancer Lett 2011;309: 228-35.
14. Takezawa K, Okamoto I, Okamoto W, Takeda M, Sakai K, Tsukioka S, et al. Thymidylate synthase as a determinant of pemetrexed sensitivity in non-small cell lung cancer. Br J Cancer 2011;104: 1594-601.
15. Chen CY, Chang YL, Shih JY, Lin JW, Chen KY, Yang CH, et al. Thymidylate synthase and dihydrofolate reductase expression in non- small cell lung carcinoma: the association with treatment efficacy of pemetrexed. Lung Cancer 2011;74: 132-8.
16. Koehler SE, Ladner RD. Small interfering RNA-mediated suppression of dUTPase sensitizes cancer cell lines to thymidylate synthase inhibition. Mol Pharmacol 2004;66: 620-6.
17. Pulukuri SM, Knost JA, Estes N, Rao JS. Small interfering RNAdirected knockdown of uracil DNA glycosylase induces apoptosis and sensitizes human prostate cancer cells to genotoxic stress. Mol Cancer Res 2009;7: 1285-93.
18. el-Hajj HH, Wang L, Weiss B. Multiple mutant of Escherichia coli synthesizing virtually thymineless DNA during limited growth. J Bacteriol 1992;174: 4450-6.
19. Gadsden MH, McIntosh EM, Game JC, Wilson PJ, Haynes RH. dUTP pyrophosphatase is an essential enzyme in Saccharomyces cerevisiae. EMBO J 1993;12: 4425-31.
20. Bulgar AD, Weeks LD, Miao Y, Yang S, Xu Y, Guo C, et al. Removal of uracil by uracil DNA glycosylase limits pemetrexed cytotoxicity: overriding the limit with methoxyamine to inhibit base excision repair. Cell Death Dis 2012;3:e252.
21. Nakamura J, Walker VE, Upton PB, ChiangSY,KowYW, Swenberg JA. Highly sensitive apurinic/apyrimidinic site assay can detect spontaneous and chemically induced depurination under physiological conditions. Cancer Res 1998;58: 222-5.
22. Garber ME, Troyanskaya OG, Schluens K, Petersen S, Thaesler Z, Pacyna-Gengelbach M, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci U S A 2001;98: 13784-9.
23. Hou J, Aerts J, den Hamer B, van Ijcken W, den Bakker M, Riegman P, et al. Gene expression-based classification of non-small cell lung carcinomas and survival prediction. PLoS ONE 2010;5:e10312.
24. Bhattacharjee A, Richards WG, Staunton J, Li C, Monti S, Vasa P, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A 2001;98: 13790-5.
25. Jalal S, Ansari R, Govindan R, Bhatia S, Bruetman D, Fisher W, et al. Pemetrexed in second line and beyond small cell lung cancer: a Hoosier Oncology Group phase II study. J Thorac Oncol 2009;4: 93-6.
26. Socinski MA, Raju RN, Neubauer M, Smith DA, Richards DA, Savin M, et al. Pemetrexed in relapsed small-cell lung cancer and the impact of shortened vitamin supplementation lead-in time: results of a phase II trial Pemetrexed in second line and beyond small cell lung cancer: a Hoosier Oncology Group phase II study. J Thorac Oncol 2008;3: 1308-16.
27. Scagliotti G, Hanna N, Fossella F, Sugarman K, Blatter J, Peterson P, et al. The differential efficacy of pemetrexed according to NSCLC histology: a review of two phase III studies. Oncologist 2009;14: 253-63.
28. Beer DG, Kardia SL, Huang CC, Giordano TJ, Levin AM, Misek DE, et al. Gene-expression profiles predict survival of patients with lung adenocarcinoma. Nat Med 2002;8: 816-24.
29. Zhu CQ, Ding K, Strumpf D, Weir BA, Meyerson M, Pennell N, et al. Prognostic and predictive gene signature for adjuvant chemotherapy in resected non-small cell lung cancer. J Clin Oncol 2010;28: 4417-24.
30. Nilsen H, Rosewell I, Robins P, Skjelbred CF, Andersen S, Slupphaug G, et al. Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication. Mol Cell 2000;5: 1059-65.
31. Branzei D, Foiani M. The DNA damage response during DNA replication. Curr Opin Cell Biol 2005;17: 568-75.
32. Sabatinos SA. Recovering a stalled replication fork. Nat Educ 2010;3:31.
33. Montecucco A, Rossi R, Ferrari G, Scovassi AI, Prosperi E, Biamonti G. Etoposide induces the dispersal of DNA ligase I from replication factories. Mol Biol Cell 2001;12: 2109-18.
34. Franchitto A, Pirzio LM, Prosperi E, Sapora O, Bignami M, Pichierri P. Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81-dependent pathway. J Cell Biol 2008;183: 241-52.
35. Gordon M, Rosen L, Mendelson D, Ramanathan R, Goldman J, Liu L, et al. A phase 1 study of TRC102, an inhibitor of base excision repair, and pemetrexed in patients with advanced solid tumors. Invest New Drugs 2013;31: 714-23.
36. Yan L, Bulgar A, Miao Y, Mahajan V, Donze JR, Gerson SL, et al. Combined treatment with temozolomide and methoxyamine: blocking apurininc/pyrimidinic site repair coupled with targeting topoisomerase IIalpha. Clin Cancer Res 2007;13: 1532-9.
37. Saviozzi S, Ceppi P, Novello S, Ghio P, Lo Iacono M, Borasio P, et al. Non-small cell lung cancer exhibits transcript overexpression of genes associated with homologous recombination andDNAreplication pathways. Cancer Res 2009;69: 3390-6.
38. Houghton JA, Harwood FG, Houghton PJ. Cell cycle control processes determine cytostasis or cytotoxicity in thymineless death of colon cancer cells. Cancer Res 1994;54: 4967-73.
39. Longley DB, Harkin DP, Johnston PG. 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 2003;3: 330-8.
40. Ibe T, Shimizu K, Nakano T, Kakegawa S, Kamiyoshihara M, Nakajima T, et al. High-grade neuroendocrine carcinoma of the lung shows increased thymidylate synthase expression compared to other histotypes. J Surg Oncol 2010;102: 11-7.
41. Smit EF, Socinski MA, Mullaney BP, Myrand SP, Scagliotti GV, Lorigan P, et al. Biomarker analysis in a phase III study of pemetrexed- carboplatin versus etoposide-carboplatin in chemonaive patients with extensive-stage small-cell lung cancer. Ann Oncol 2012;23: 1723-9.
42. Chang MH, Ahn JS, Lee J, Kim KH, Park YH, Han J, et al. The efficacy of pemetrexed as a third- or fourth-line therapy and the significance of thymidylate synthase expression in patients with advanced non-small cell lung cancer. Lung Cancer 2010;69: 323-9.
43. Otterlei M, Warbrick E, Nagelhus TA, Haug T, Slupphaug G, Akbari M, et al. Post-replicative base excision repair in replication foci. EMBO J 1999;18: 3834-44.
44. Hagen L, Kavli B, Sousa MM, Torseth K, Liabakk NB, Sundheim O, et al. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J 2008;27: 51-61.
45. Visnes T, Akbari M, Hagen L, Slupphaug G, Krokan HE. The rate of base excision repair of uracil is controlled by the initiating glycosylase. DNA Repair 2008;7: 1869-81.
46. Ivarie R. Thymine methyls and DNA-protein interactions. Nucleic Acids Res 1987;15: 9975-83.
47. Nilsen H, Stamp G, Andersen S, Hrivnak G, Krokan HE, Lindahl T, et al. Gene-targeted mice lacking the Ung uracil-DNA glycosylase develop B-cell lymphomas. Oncogene 2003;22: 5381-6.
48. Andersen S, Heine T, Sneve R, Konig I, Krokan HE, Epe B, et al. Incorporation of dUMP into DNA is a major source of spontaneous DNA damage, while excision of uracil is not required for cytotoxicity of fluoropyrimidines in mouse embryonic fibroblasts. Carcinogenesis 2005;26: 547-55.
49. Wilson PM, Labonte MJ, Lenz HJ, Mack PC, Ladner RD. Inhibition of dUTPase induces synthetic lethality with thymidylate synthase-targeted therapies in non-small cell lung cancer. Mol Cancer Ther 2011;11: 616-28.
50. Luo Y, Walla M, Wyatt MD. Uracil incorporation into genomic DNA does not predict toxicity caused by chemotherapeutic inhibition of thymidylate synthase. DNA Repair 2008;7: 162-9.