The synergistic interaction of gemcitabine and cytosine arabinoside with the ribonucleotide reductase inhibitor triapine is schedule dependent

Biochemical Pharmacology

Volumn 73, Issue 10, 2007, Pages 1548-1557

  Sigmond, J ^a   Kamphuis, J A E ^a   Laan, A C ^a   Hoebe, E K ^a   Bergman, A M ^a   Peters, G J ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cytosine arabinoside; Deoxycytidine kinase; Gemcitabine; Ribonucleotide reductase; Synergistic interaction; Triapine

Indexed keywords

3 AMINOPICOLINALDEHYDE THIOSEMICARBAZONE; CYTARABINE; CYTARABINE TRIPHOSPHATE; DEOXYCYTIDINE KINASE; DNA; GEMCITABINE; GEMCITABINE TRIPHOSPHATE; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG CYTOTOXICITY; DRUG EXPOSURE; DRUG INHIBITION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; METABOLITE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; ARABINOFURANOSYLCYTOSINE TRIPHOSPHATE; CYTARABINE; DEOXYCYTIDINE; DNA; DRUG SYNERGISM; HUMANS; PYRIDINES; RIBONUCLEOTIDE REDUCTASES; THIOSEMICARBAZONES; TUMOR CELLS, CULTURED;

EID: 34047166367     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2007.01.025     Document Type: Article

References (48)

1. Toschi L., Finocchiaro G., Bartolini S., Gioia V., and Cappuzzo F. Role of gemcitabine in cancer therapy. Future Oncol 1 (2005) 7-17
2. Bergman A.M., Pinedo H.M., and Peters G.J. Determinants of resistance to 2′,2′-difluorodeoxycytidine (gemcitabine). Drug Resist Updat 5 (2002) 19-33
3. Ruiz van Haperen V.W., Veerman G., Vermorken J.B., and Peters G.J. 2′,2′-Difluoro-deoxycytidine (gemcitabine) incorporation into RNA and DNA of tumour cell lines. Biochem Pharmacol 46 (1993) 762-766
4. Heinemann V., Xu Y.Z., Chubb S., Sen A., Hertel L.W., Grindey G.B., et al. Inhibition of ribonucleotide reduction in CCRF-CEM cells by 2′2′-difluorodeoxycytidine. Mol Pharmacol 38 (1990) 567-572
5. Bergman A.M., Eijk P.P., Ruiz van Haperen V.W., Smid K., Veerman G., Hubeek I., et al. In vivo induction of resistance to gemcitabine results in increased expression of ribonucleotide reductase subunit M1 as the major determinant. Cancer Res 65 (2005) 9510-9516
6. Van Moorsel C.J., Smid K., Voorn D.A., Bergman A.M., Pinedo H.M., and Peters G.J. Effect of gemcitabine and cis-platinum combinations on ribonucleotide and deoxyribonucleotide pools in ovarian cancer cell lines. Int J Oncol 22 (2003) 201-207
7. Plunkett W., Huang P., Searcy C.E., and Gandhi V. Gemcitabine: preclinical pharmacology and mechanisms of action. Semin Oncol 23 (1996) 3-15
8. Grant S. Ara-C: cellular and molecular pharmacology. Adv Cancer Res 72 (1998) 197-233
9. Peters G.J., and Jansen G. Resistance to antimetabolites. In: Schilsky R.L., Milano G.A., and Ratain M.J. (Eds). Principles of antineoplastic drug development and pharmacology (1996), Marcel Dekker, Inc., New York 543-585
10. Thelander L., Graslund A., and Thelander M. Continual presence of oxygen and iron required for mammalian ribonucleotide reduction: possible regulation mechanism. Biochem Biophys Res Commun 110 (1983) 859-865
11. Thelander L., and Reichard P. Reduction of ribonucleotides. Annu Rev Biochem 48 (1979) 133-158
12. Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., et al. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 404 (2000) 42-49
13. Nakano K., Balint E., Ashcroft M., and Vousden K.H. A ribonucleotide reductase gene is a transcriptional target of p53 and p73. Oncogene 19 (2000) 4283-4289
14. Guittet O., Hakansson P., Voevodskaya N., Fridd S., Graslund A., Arakawa H., et al. Mammalian p53R2 protein forms an active ribonucleotide reductase in vitro with the R1 protein, which is expressed both in resting cells in response to DNA damage and in proliferating cells. J Biol Chem 276 (2001) 40647-40651
15. Xue L., Zhou B., Liu X., Qiu W., Jin Z., and Yen Y. Wild-type p53 regulates human ribonucleotide reductase by protein-protein interaction with p53R2 as well as hRRM2 subunits. Cancer Res 63 (2003) 980-986
16. Donehower R.C. An overview of the clinical experience with hydroxyurea. Semin Oncol 19 (1992) 11-19
17. Peters G.J., and Ackland S.P. New antimetabolites in preclinical and clinical development. Expert Opin Invest Drugs 5 (1996) 637-679
18. Creasey W.A., Agrawal K.C., Capizzi R.L., Stinson K.K., and Sartorelli A.C. Studies of the antineoplastic activity and metabolism of -(N)-heterocyclic carboxaldehyde thiosemicarbazones in dogs and mice. Cancer Res 32 (1972) 565-572
19. Krakoff I.H., Etcubanas E., Tan C., Mayer K., Bethune V., and Burchenal J.H. Clinical trial of 5-hydroxypicolinaldehyde thiosemicarbazone (5-HP; NSC-107392), with special reference to its iron-chelating properties. Cancer Chemother Rep 58 (1974) 207-212
20. Finch R.A., Liu M., Grill S.P., Rose W.C., Loomis R., Vasquez K.M., et al. Triapine (3-aminopyridine-2-carboxaldehyde-thiosemicarbazone): a potent inhibitor of ribonucleotide reductase activity with broad spectrum antitumor activity. Biochem Pharmacol 59 (2000) 983-991
21. Cory J.G., Cory A.H., Rappa G., Lorico A., Liu M.C., Lin T.S., et al. Inhibitors of ribonucleotide reductase. Comparative effects of amino- and hydroxy-substituted pyridine-2-carboxaldehyde thiosemicarbazones. Biochem Pharmacol 48 (1994) 335-344
22. Liu M.C., Lin T.S., and Sartorelli A.C. Synthesis and antitumor activity of amino derivatives of pyridine-2-carboxaldehyde thiosemicarbazone. J Med Chem 35 (1992) 3672-3677
23. Murren J., Modiano M., Clairmont C., Lambert P., Savaraj N., Doyle T., et al. Phase I and pharmacokinetic study of triapine, a potent ribonucleotide reductase inhibitor, administered daily for 5 days in patients with advanced solid tumors. Clin Cancer Res 9 (2003) 4092-4100
24. Wadler S., Makower D., Clairmont C., Lambert P., Fehn K., and Sznol M. Phase I and pharmacokinetic study of the ribonucleotide reductase inhibitor, 3-aminopyridine-2-carboxaldehyde thiosemicarbazone, administered by 96-hour intravenous continuous infusion. J Clin Oncol 22 (2004) 1553-1563
25. Kroep J.R., Loves W.J., van der Wilt C.L., Alvarez E., Talianidis I., Boven E., et al. Pretreatment deoxycytidine kinase levels predict in vivo gemcitabine sensitivity. Mol Cancer Ther 1 (2002) 371-376
26. Arner E.S., Spasokoukotskaja T., and Eriksson S. Selective assays for thymidine kinase 1 and 2 and deoxycytidine kinase and their activities in extracts from human cells and tissues. Biochem Biophys Res Commun 188 (1992) 712-718
27. Keepers Y.P., Pizao P.E., Peters G.J., van Ark-Otte J., Winograd B., and Pinedo H.M. Comparison of the sulforhodamine B protein and tetrazolium (MTT) assays for in vitro chemosensitivity testing. Eur J Cancer 27 (1991) 897-900
28. Chou T.C., and Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22 (1984) 27-55
29. Ruiz van Haperen V.W., Veerman G., Boven E., Noordhuis P., Vermorken J.B., and Peters G.J. Schedule dependence of sensitivity to 2′,2′-difluorodeoxycytidine (Gemcitabine) in relation to accumulation and retention of its triphosphate in solid tumour cell lines and solid tumours. Biochem Pharmacol 48 (1994) 1327-1339
30. Bergman A.M., Pinedo H.M., Talianidis I., Veerman G., Loves W.J., van der Wilt C.L., et al. Increased sensitivity to gemcitabine of P-glycoprotein and multidrug resistance-associated protein-overexpressing human cancer cell lines. Br J Cancer 88 (2003) 1963-1970
31. Huang P., and Plunkett W. Fludarabine- and gemcitabine-induced apoptosis: incorporation of analogs into DNA is a critical event. Cancer Chemother Pharmacol 36 (1995) 181-188
32. Bergman A.M., Pinedo H.M., Jongsma A.P., Brouwer M., Ruiz van Haperen V.W., Veerman G., et al. Decreased resistance to gemcitabine (2′,2′-difluorodeoxycitidine) of cytosine arabinoside-resistant myeloblastic murine and rat leukemia cell lines: role of altered activity and substrate specificity of deoxycytidine kinase. Biochem Pharmacol 57 (1999) 397-406
33. Stevens C., and La Thangue N.B. E2F and cell cycle control: a double-edged sword. Arch Biochem Biophys 412 (2003) 157-169
34. Johnson D.G., Schwarz J.K., Cress W.D., and Nevins J.R. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365 (1993) 349-352
35. Wang A., Li C.J., Reddy P.V., and Pardee A.B. Cancer chemotherapy by deoxynucleotide depletion and E2F-1 elevation. Cancer Res 65 (2005) 7809-7814
36. Duxbury M.S., Ito H., Zinner M.J., Ashley S.W., and Whang E.E. RNA interference targeting the M2 subunit of ribonucleotide reductase enhances pancreatic adenocarcinoma chemosensitivity to gemcitabine. Oncogene 23 (2004) 1539-1548
37. Hubeek I., Peters G.J., Broekhuizen A.J., Sargent J., Gibson B.E., Creutzig U., et al. Potentiation of in vitro ara-C cytotoxicity by ribonucleotide reductase inhibitors, cyclin-dependent kinase modulators and the DNA repair inhibitor aphidicolin in paediatric acute myeloid leukaemia. Br J Haematol 131 (2005) 219-222
38. Shao J., Zhou B., Zhu L., Qiu W., Yuan Y.C., Xi B., et al. In vitro characterization of enzymatic properties and inhibition of the p53R2 subunit of human ribonucleotide reductase. Cancer Res 64 (2004) 1-6
39. Fritzer-Szekeres M., Salamon A., Grusch M., Horvath Z., Hochtl T., Steinbrugger R., et al. Trimidox, an inhibitor of ribonucleotide reductase, synergistically enhances the inhibition of colony formation by Ara-C in HL-60 human promyelocytic leukemia cells. Biochem Pharmacol 64 (2002) 481-485
40. Nandy P., Lien E.J., and Avramis V.I. Inhibition of ribonucleotide reductase by a new class of isoindole derivatives: drug synergism with cytarabine (Ara-C) and induction of cellular apoptosis. Anticancer Res 19 (1999) 1625-1633
41. Madlener S., Illmer C., Horvath Z., Saiko P., Losert A., Herbacek I., et al. Gallic acid inhibits ribonucleotide reductase and cyclooxygenases in human HL-60 promyelocytic leukemia cells. Cancer Lett 245 (2006) 156-162
42. Tolis C., Peters G.J., Ferreira C.G., Pinedo H.M., and Giaccone G. Cell cycle disturbances and apoptosis induced by topotecan and gemcitabine on human lung cancer cell lines. Eur J Cancer 35 (1999) 796-807
43. Grusch M., Fritzer-Szekeres M., Fuhrmann G., Rosenberger G., Luxbacher C., Elford H.L., et al. Activation of caspases and induction of apoptosis by novel ribonucleotide reductase inhibitors amidox and didox. Exp Hematol 29 (2001) 623-632
44. Ferreira C.G., Span S.W., Peters G.J., Kruyt F.A., and Giaccone G. Chemotherapy triggers apoptosis in a caspase-8-dependent and mitochondria-controlled manner in the non-small cell lung cancer cell line NCI-H460. Cancer Res 60 (2000) 7133-7141
45. Murren J., Modiano M., Clairmont C., Lambert P., Savaraj N., Doyle T., et al. Phase I and pharmacokinetic study of triapine, a potent ribonucleotide reductase inhibitor, administered daily for five days in patients with advanced solid tumors. Clin Cancer Res 9 (2003) 4092-4100
46. Giles F.J., Fracasso P.M., Kantarjian H.M., Cortes J.E., Brown R.A., Vverstovsek S., et al. Phase I and pharmacodynamic study of Triapine, a novel ribonucleotide reductase inhibitor, in patients with advanced leukaemia. Leuk Res 12 (2003) 1077-1083
47. Yen Y., Margolin K., Doroshow J., Fishman M., Johnson B., Clairmont C., et al. A phase I trial of 3-aminopyridine-2-carboxaldehyde thiosemicarbazone in combination with gemcitabine for patients with advanced cancer. Cancer Chemother Pharmacol 54 (2004) 331-342
48. Yee K.W., Cortes J., Ferrajoli A., Garcia-Manero G., Verstovsek S., Wierda W., et al. Triapine and cytarabine is an active combination in patients with acute leukemia or myelodysplastic syndrome. Leuk Res 30 (2006) 813-822