Collateral sensitivity to novel thymidylate synthase inhibitors correlates with folate cycle enzymes impairment in cisplatin-resistant human ovarian cancer cells

European Journal of Pharmacology

Volumn 615, Issue 1-3, 2009, Pages 17-26

  Marverti, Gaetano ^a   Ligabue, Alessio ^a   Paglietti, Giuseppe ^b   Corona, Paola ^b   Piras, Sandra ^b   Vitale, Gabriella ^b   Guerrieri, Davide ^a   Luciani, Rosaria ^a   Costi, Maria Paola ^a   Frassineti, Chiara ^a   Moruzzi, Maria Stella ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY OF SASSARI   (Italy)

Author keywords

Cisplatin resistance; Folate cycle inhibitor; Ovarian cancer; Quinoxaline

Indexed keywords

3 METHYL 7 TRIFLUOROMETHYL (3,4,5 TRIMETHOXYANILO)QUINOXALINE; 3 PIPERAZINILMETHYL 2 [4 (OXYMETHYL)PHENOXY]QUINOXALINE; CISPLATIN; DIHYDROFOLATE REDUCTASE; THYMIDYLATE SYNTHASE; THYMIDYLATE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER RESISTANCE; CHEMOSENSITIVITY; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; CYSTADENOCARCINOMA, SEROUS; DRUG RESISTANCE, NEOPLASM; FEMALE; FLUOROURACIL; FOLIC ACID ANTAGONISTS; HUMANS; OVARIAN NEOPLASMS; QUINOXALINES; TETRAHYDROFOLATE DEHYDROGENASE; THYMIDYLATE SYNTHASE;

EID: 67449146884     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2009.04.062     Document Type: Article

References (53)

1. Andrews P.A., and Albright K.D. Mitochondrial defects in cis-diamminedichloroplatinum(II)-resistant human ovarian carcinoma cells. Cancer Res. 52 (1992) 1895-1901
2. - ΔΔCt calculation as an alternate method of data analysis for quantitative PCR of BCR-ABL P210 transcripts. Diagn. Mol. Pathol. 15 (2006) 56-61
3. Banerjee D., Mayer-Kuckuk P., Capiaux G., Budak-Alpdogan T., Gorlick R., and Bertino J.R. Novel aspects of resistance to drugs targeted to dihydrofolate reductase and thymidylate synthase. Biochim. Biophys. Acta 1587 (2002) 164-173
4. Bedford P., Shellard S.A., Walker M.C., Whelan R.D.H., Masters J.R.W., and Hill B.T. Differential expression of collateral sensitivity or resistance to cisplatin in human bladder carcinoma cell lines pre-exposed in vitro to either X-irradiation or cisplatin. Int. J. Cancer 40 (2006) 681-686
5. Bradford M.M. A rapid and sensitive method for quantification of microgram quantities of protein utilising the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
6. Bystroff C., and Kraut J. Crystal structure of unliganded Escherichia coli dihydrofolate reductase. Ligand-induced conformational changes and cooperativity in binding. Biochemistry 30 (1991) 2227-2239
7. Carreras C.W., and Santi D.V. The catalytic mechanism and structure of thymidylate synthase. Ann. Rev. Biochem. 64 (1995) 721-762
8. Chou T.C., and Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. In: Weber G. (Ed). Advances in Enzyme Regulation (1984), Pergamon Press, New York, NY 27-55
9. Chu E., Koeller D.M., Casey J.L., Drake J.C., Chabner B.A., Elwood P.C., Zinn S., and Allegra C.J. Autoregulation of human thymidylate synthase messenger RNA translation by thymidilate synthase. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 8977-8981
10. Chu E., Koeller D.M., Johnston P., Zinn S., and Allegra C.J. Regulation of thymidylate synthase in human colon cancer cells treated with 5-fluorouracil and interferon-gamma. Mol. Pharmacol. 43 (1993) 527-533
11. Chu E., and Allegra C.J. The role of thymidylate synthase as an RNA binding protein. Bioessays. 18 (1996) 191-198
12. Costi P., and Ferrari S. Update on antifolate drugs targets. Curr. Drug Targets 2 (2001) 135-166
13. Fram R.J., Woda B.A., Wilson J.M., and Robichaud N. Characterization of acquired resistance to cis-diamminedichloroplatinum(II) in BE human colon carcinoma cells. Cancer Res. 50 (1990) 72-77
14. Gangjee A., Qiu Y., Li W., and Kisliuk R.L. Potent dual thymidylate synthase and dihydrofolate reductase inhibitors: classical and nonclassical 2-amino-4-oxo-5-arylthio-substituted-6-methylthieno[2,3-d]pyrimidine antifolates. J. Med. Chem. 51 (2008) 5789-5797
15. Goker E., Walthman M.C., Kheradpour A., Trippett T., Majumdar M., Elisseyeff Y., Schneiders B., Steinherz P., Tan C., and Berman E. Amplification of the dihydrofolate reductase gene is a mechanism of acquired resistance to methotrexate in patients with acute lymphoblastic leukemia and is correlated with p53 gene mutations. Blood 86 (1995) 677-684
16. Gonçalves E.M., Ventura C.A., Yano T., Rodrigues Macero M.L., and Genari S.C. Morphological and growth alterations in Vero cells transformed by cisplatin. Cell Biol. Int. 30 (2006) 485-494
17. Kelland L.R., Kimbell R., Hardcastle A., Aherne G.W., and Jackman A.L. Relationship between resistance to cisplatin and antifolates in sensitive and resistant tumour cell lines. Eur. J. Cancer 31A (1995) 981-986
18. Keyomarsi K., Samet J., Molnar G., and Pardee A.B. The thymidylate synthase inhibitor, ICI D1694, overcomes translational detainment of the enzyme. J. Biol. Chem. 268 (1993) 15142-15149
19. Kitchens M.E., Forsthoefel A.M., Barbour K.W., Spencer H.T., and Berger F.G. Mechanisms of acquired resistance to thymidylate synthase inhibitors: the role of enzyme stability. Mol. Pharmacol. 56 (1999) 1063-1070
20. Kitchens M.E., Forsthoefel A.M., Rafique Z., Spencer H.T., and Berger F.G. Ligand-mediated induction of thymidilate occurs by enzyme stabilization. J. Biol. Chem. 274 (1999) 12544-12547
21. Kueng W., Siber E., and Eppenberger U. Quantification of cells cultured on 96-well plates. Anal. Biochem. 182 (1989) 16-19
22. Lai G.M., Ozols R.F., Smyth J.F., Young R.C., and Hamilton T.C. Enhanced DNA repair and resistance to cisplatin in human ovarian cancer. Biochem. Pharmacol. 37 (1988) 4597-4600
23. Leamon C.P. Folate-targeted drug strategies for the treatment of cancer. Curr. Opin. Investig. Drugs 9 (2008) 1277-1286
24. Longley D.B., Ferguson P.R., Boyer J., Latif T., Lynch M., Maxwell P., Harkin D.P., and Johnston P.G. Characterization of a thymidilate synthase (TS)-inducible cell line: a model system for studying sensitivity to TS- and non-TS-targeted chemotherapies. Clin. Cancer Res. 7 (2001) 3533-3539
25. Loriga M., Fiore M., Sanna P., and Paglietti G. Quinoxaline chemistry. Part 4. 2-(R)-anilinoquinoxalines as non classic antifolate agents. Synthesis, structure elucidation and evaluation of in vitro anticancer activity. Il Farmaco 50 (1995) 289-301
26. Loriga M., Moro P., Sanna P., and Paglietti G. Quinoxaline chemistry. Part 8. 2-[Anilino]-3-[Carboxy]-6(7)-substituted quinoxalines as non classical antifolate agents. Synthesis and evaluation of in vitro anticancer, anti-HIV and antifungal activity. Il Farmaco 52 (1997) 531-537
27. Loriga M., Piras S., Paglietti G., Costi M.P., and Venturelli A. Quinoxaline chemistry. Part 15. 4-[2-Quinoxalylmethylenimino]benzoylglutamates and -benzoates, 4-[2-quinoxalylmethyl-N-methylamino]-benzoylglutamates as analogues of classical antifolate agents. Synthesis, elucidation of structures and in vitro evaluation of antifolate and anticancer activities. Il Farmaco 58 (2003) 51-61
28. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folic phenol reagent. J. Biol. Chem. 193 (1951) 265-275
29. Lu Y., Han J., and Scanlon K.J. Biochemical and molecular properties of cisplatin-resistant A2780 cells grown in folinic acid. J. Biol. Chem. 263 (1988) 4891-4894
30. Mann S.C., Andrews P.A., and Howell S.B. Short-term cis-diamminedichloroplatinum(II) accumulation in sensitive and resistant human ovarian carcinoma cells. Cancer Chemother. Pharmacol. 25 (1990) 236-240
31. 12-bis(ethyl)spermine effect on growth of cis-diamminedichloroplatinum(II)-sensitive and -resistant human ovarian carcinoma cell lines. Int. J. Cancer 78 (1998) 33-40
32. Masuda H., Ozols R.F., Lai G., Fojo A., Rothembert M., and Hamilton T.C. Increased DNA repair as a mechanism of acquired resistance to cis-diamminedichloroplatinum (II) in human ovarian carcinoma cells. Cancer Res. 48 (1988) 5713-5716
33. Mohsen A.W., Aull J.L., Payne D., and Daron H.H. Ligand-induced conformational changes of thymidylate synthase detected by limited proteolysis. Biochemistry 34 (1995) 1669-1677
34. Morgan R.J., Braly P., Leong L., Shibata S., Margolin K., Somlo G., McNamara M., Longmate J., Schinke S., Raschko J., Nagasawa S., Kogut N., Najera L., Johnson D., and Doroshow J.H. Phase II trial of combination intraperitoneal cisplatin and 5-fluorouracil in previously treated patients with advanced ovarian cancer: long-term follow-up. Gynecol. Oncol. 77 (2000) 433-438
35. Muggia F. Platinum compounds 30 years after the introduction of cisplatin: implications for the treatment of ovarian cancer. Gynecol. Oncol. 112 (2009) 275-281
36. Newman E.M., Lu Y., Kashani-Sabet M., Kesavan V., and Scanlon K.J. Mechanisms of cross-resistance to methotrexate and 5-fluorouracil in an A2780 human ovarian carcinoma cell subline resistant to cisplatin. Biochem. Pharmacol. 37 (1988) 443-447
37. Ohe Y., Sugimoto Y., and Saijo N. Collateral sensitivity of cisplatin-resistant human lung cancer cell lines to thymidylate synthase inhibitors. Cancer J. 3 (1990) 332-336
38. Pinedo H.M., and Peters G.J. Fluorouracil: biochemistry and pharmacology. J. Clin. Oncol. 6 (1988) 1653-1664
39. Piras S., Loriga M., and Paglietti G. Quinoxaline chemistry. Part 17. 4[3,6(7)disubstituted-2-quinoxalinyl-oxy]phenylacetate and phenylacetylglutamate analogues of methotrexate. Synthesis and evaluation of in vitro anticancer activity. Il Farmaco 59 (2004) 185-194
40. Piras S., Loriga M., Carta A., Paglietti G., Costi M.P., and Ferrari S. Novel 3 benzoyl-2-piperazinylquinoxaline derivatives as potential antitumor agents. J. Heterocycl. Chem. 43 (2006) 541-551
41. Porter J., Lumb S., Lecomte F., Reuberson J., Foley A., Calmiano M., le Riche K., Edwards H., Delgado J., Franklin R.J., Gascon-Simorte J.M., Maloney A., Meier C., and Batchelor M. Discovery of a novel series of quinoxalines as inhibitors of c-Met kinase. Bioorg. Med. Chem. Lett. 19 (2009) 397-400
42. Qing L., Boyer C., Lee J.Y., and Shepard H.M. A novel approach to thymidylate synthase as a target for cancer chemotherapy. Mol. Pharmacol. 59 (2001) 446-452
43. Rossi T., Coppi A., Bruni E., Ruberto A., Santachiara S., and Baggio G. Effects of anti-malarial drugs on MCF-7 and Vero cell replication. Anticancer Res. 27 (2007) 2555-2560
44. 3H]dihydrofolate. Anal. Biochem. 103 (1980) 152-156
45. Scanlon K.J., and Kashani-Sabet M. Elevated expression of thymidylate synthase cycle genes in cisplatin-resistant human ovarian carcinoma A2780 cells. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 650-653
46. Scanlon K.J., Newman E.M., Lu Y., and Priest D.G. Biochemical basis for cisplatin and 5-fluorouracil synergism in human ovarian carcinoma cells. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 8923-8925
47. Schmitz J.C., Chen T., and Chu E. Small interfering double-stranded RNAs as therapeutic molecules to restore chemosensitivity to thymidylate synthase inhibitor compounds. Cancer Res. 64 (2004) 1431-1435
48. Shirasaki T., Maruya S., Mizukami H., Kakehata S., Kurotaki H., Yagihashi S., and Shinkawa H. Effects of small interfering RNA targeting thymidylate synthase on survival of ACC3 cells from salivary adenoid cystic carcinoma. BMC Cancer 8 (2008) 348-360
49. Stewart D.J. Mechanisms of resistance to cisplatin and carboplatin. Crit. Rev. Oncol./Hematol. 63 (2007) 12-31
50. Theisen J., Danenberg K., Ott K., Becker K., Danenberg P., Stein H.J., and Siewert J.-R. Predictors of response and survival for neoadjuvant treated patients with esophageal adenocarcinoma. Dis. Esophagus 21 (2008) 601-606
51. van Triest B., Pinedo H.M., van Hensbergen Y., Smid K., Telleman F., Schoenmakers P.S., van der Wilt C.L., van Laar J.A.M., Noordhuis P., Jansen G., and Peters G.J. Thymidylate synthase level as the main predictive parameter for sensitivity to 5-fluorouracil, but not for folate-based thymidilate synthase inhibitors, in 13 nonselected colon cancer cell lines. Clin. Cancer Res. 5 (1999) 643-654
52. Yasumatsu R., Nakashima T., Uryu H., Ayada T., Wakasaki T., Kogo R., Masuda M., Fukushima M., and Komune S. Correlation between thymidylate synthase expression and chemosensitivity to 5-fluorouracil, cell proliferation and clinical outcome in head and neck squamous cell carcinoma. Chemotherapy 55 (2009) 36-41
53. Wang L., Liu B., Wang T., Ding Y., Qian X., and Zhao Y. Detection of cell-free ERCC1 and thymidylate synthase (TS) mRNA in malignant effusions and its association with anticancer drug sensitivity. Anticancer Res. 28 (2008) 1085-1091