Impact of polyglutamation on sensitivity to raltitrexed and methotrexate in relation to drug-induced inhibition of de novo thymidylate and purine biosynthesis in CCRF-CEM cell lines

Clinical Cancer Research

Volumn 5, Issue 9, 1999, Pages 2548-2558

  Barnes, Matthew J ^a   Estlin, Edward J ^b,e   Taylor, Gordon A ^a   Aherne, G Wynne ^c   Hardcastle, A ^c   McGuire, J J ^d   Calvete, Joanne A ^a   Lunec, John ^a   Pearson, Andrew D J ^b   Newell, David R ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b ROYAL VICTORIA INFIRMARY   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

^e BRISTOL ROYAL HOSPITAL FOR CHILDREN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LOMETREXOL; METHOTREXATE; NOLATREXED; PURINE; RALTITREXED; THYMIDINE PHOSPHATE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LEUKEMIA CELL; METABOLIC INHIBITION; PRIORITY JOURNAL; PURINE SYNTHESIS;

BIOLOGICAL TRANSPORT; CELL DIVISION; DRUG SCREENING ASSAYS, ANTITUMOR; FOLIC ACID ANTAGONISTS; GROWTH INHIBITORS; HUMANS; INHIBITORY CONCENTRATION 50; LEUKEMIA; METHOTREXATE; PEPTIDE SYNTHASES; PURINES; QUINAZOLINES; RNA, MESSENGER; THIOPHENES; THYMIDINE MONOPHOSPHATE; THYMIDYLATE SYNTHASE; TUMOR CELLS, CULTURED;

EID: 0032882886     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Jansen, G., Westerhof, G. R., Schornagel, J. H., Jackman, A. L., and Boyle, F. T. The reduced folate/methotrexate carrier and a membrane-associated folate binding protein as transport routes for novel antifolates: structure-activity relationships. Adv. Exp. Med. Biol., 338; 767-770, 1993.
2. Goldman, I. D., Lichtenstein, N. S., and Oliverio, V. T. Carrier-mediated transport of the folic acid analogue, methotrexate, in the L1210 leukemia cell. J. Biol. Chem., 243: 5007-5017, 1968.
3. McGuire, J. J., Hsieh, P., Coward, J. K., and Bertino, J. R. Enzymatic synthesis of the folylpolyglutamates. J. Biol. Chem., 255: 5776-5788, 1980.
4. Barredo, J., and Moran, R. G. Determinants of antifolate cytotoxicity: folylpolyglutamate synthetase activity during cellular proliferation and development. Mol. Pharmacol., 42: 687-694, 1992.
5. Galivan, J., Nimec, Z., and Balinska, M. Regulation of methotrexate polyglutamate accumulation in vitro: effects of cellular folate content. Biochem. Pharmacol., 32: 3244-3247, 1983.
6. Kimbell, R., Jackman, A. L., Boyle, F. T., Hardcastle, A., and Aherne, G. W. The duration of the inhibition of thymidylate synthase in intact L1210 cells exposed to two different classes of quinazoline analogues. Adv. Exp. Med. Biol., 338: 597-600, 1993.
7. Jolivet, J., Schilsky, R. L., Bailey, B. D., Drake J. C., and Chabner, B. A. Synthesis, retention, and biological activity of methotrexate polyglutamates in cultured human breast cancer cells. J. Clin. Invest., 70: 351-360, 1982.
8. Jackman, A. L., Taylor, G. A., Gibson, W., Kimbell, R., Brown, M., Calvert, A. H., Judson, I. R., and Hughes, L. R. ICI D1694, a quinazoline antifolate thymidylate synthase inhibitor that is a potent inhibitor of L1210 tumor cell growth in vitro and in vivo: a new agent for clinical study. Cancer Res., 51: 5579-5586, 1991.
9. Ward, W. H. J., Kimbell, R., and Jackman, A. L. Kinetic characteristics of ICI D1694: a quinazoline antifolate which inhibits thymidylate synthase. Biochem. Pharmacol., 43: 2029-2031, 1992.
10. Allegra, C. J., Chabner, B. A., Drake, J. C., Lutz, R., Rodbard D., and Jolivet, J. Enhanced inhibition of thymidylate synthase by methotrexate polyglutamates. J. Biol. Chem., 260: 9720-9726, 1985.
11. Kamen, B. A., Eibl, B., Cashmore, A., and Bertino, J. Uptake and efficacy of trimetrexate (TMQ, 2,4-diamino-5-methyl-6-[3,4,5-trimethoxyanilino)-methyl]quinazoline), a non-classical antifolate in methotrexate-resistant leukaemia cells in vitro. Biochem. Pharmacol., 33: 1697-1984, 1984.
12. Duch, D. S., Edelstein, M. P., Bowers, S. W., and Nichol, C. A. Biochemical and chemotherapeutic studies on 2,4-diamino-6-(2,5-dimethoxybenzyl)-5-methyl-pyridol[2,3-d]pyrimidine (BW301), a novel lipid soluble inhibitor of dihydrofolate reductase. Cancer Res., 42: 3987-3994, 1982.
13. Webber, S., Bartlett C. A., Boritzki, T. J., Hilliard, J. A., Howland, E. F., Johnston, A. L., Kosa, M., Margosiak, S. A., Morse, C. A., and Shetty, B. V. AG337, a novel lipophilic thymidylate synthase inhibitor: in vitro and in vivo preclinical studies. Cancer Chemother. Pharmacol., 37: 509-517, 1996.
14. Jackman, A. L., Kelland, I. R., Kimbell, R., Brown, M., Gibson, W., Aherne, G. W., Hardcastle, A., and Boyle, F. T. Mechanisms of acquired resistance to the quinazoline thymidylate synthase inhibitor ZD1694 (Tomudex) in one mouse and three human cell lines. Br. J. Cancer, 71: 914-924, 1995.
15. Rosowsky, A., Lazarus, H., Yuan, G. C., Beltz, W. R., Mangini, L., Abelson, H. T., Modest, E. J., and Frei, E. Effects of methotrexate esters and other lipophilic antifolates on methotrexate-resistant human leukaemic lymphoblasts. Biochem. Pharmacol., 29: 648-652, 1980.
16. Domin, B. A., Grill, S. P., and Cheng, Y-C. Establishment of dihydrofolate reductase-increased human cell lines and relationship between dihydrofolate reductase levels and gene copy. Cancer Res., 43: 2155-2158, 1983.
17. Jackson, R. C., Hart, L. I., and Harrap, K. R. Intrinsic resistance to methotrexate of cultured mammalian cells in relation to the inhibition kinetics of their dihydrofolate reductases. Cancer Res., 36: 1991-1997, 1976.
18. Goldie, J. H., Krystal, G., Hartley, D., Gudauskas, G., and Dedhar, S. A methotrexate insensitive variant of folate reductase present in two lines of methotrexate-resistant L5178Y cells. Eur. J. Cancer, 16: 1539-1546, 1980.
19. Fisher, T. C., Milner, A. E., Gregory, C. D., Jackman, A. L., Aherne, G. W., Hartley, J. A., Dive, C., and Hickman, J. A. bcl-2 Modulation of apoptosis induced by anticancer drugs: resistance to thymidylate stress is independent of classical resistance pathways. Cancer Res., 53: 3321-3326, 1993.
20. McCloskey, D. E., McGuire, J. J., Russell, C. A., Rowan, B. G., Bertino, J. R., Pizzorno, G., and Mini, E. Decreased folylpolyglutamate synthetase activity as a mechanism of methotrexate resistance in CCRF-CEM human leukemia sublines. J. Biol. Chem., 266: 6181-6187, 1991.
21. Lin, J. T., Tong, W. P., Trippett, T., Niedzwiecki, D., Tao, Y., Tan, C., Steinherz, P., Schweitzer, B. I., and Bertino, J. R. Basis for natural resistance to methotrexate in human acute non-lymphocytic leukemia. Leuk. Res., 15: 1191-1196, 1991.
22. Goker, E., Lin, J. T., Trippelt, T., Elisseyeff, Y., Tong, W. P., Niedzwiecki, D., Tan, C., Steinherz, P., Schweitzer, B. I., and Bertino, J. R. Decreased polyglutamation of methotrexate in acute lymphoblastic leukemia blasts in adults compared to children with this disease. Leukemia (Baltimore), 7: 1000-1004, 1993.
23. Rhee, M. S., Wang, Y., Nair, M. G., and Galivan, J. Acquisition of resistance to antifolates caused by enhanced γ-glutamyl hydrolase activity. Cancer Res., 53: 2227-2230, 1993.
24. Pizzorno, G., Chang, Y-M., McGuire, J. J., and Bertino, J. R. Inherent resistance of human squamous carcinoma cell lines to methotrexate as a result of decreased polyglutamation of this drug. Cancer Res., 49: 5275-5280, 1989.
25. Takemura, Y., Kobayashi, H., Gibson, W., Kimbell, R., Miyachi, H., and Jackman, A. L. The influence of drug-exposure conditions on the development of resistance to methotrexate or ZD1694 in cultured human leukaemia cell lines. Int. J. Cancer, 66: 29-36, 1996.
26. Curt, G. A., Jolivet, J., Carney, D. N., Bailey, B. D., Drake, J. C., Clendeninn, N. J., and Chabner, B. A. Determinants of the sensitivity of human small-cell lung cancer cell lines to methotrexate. J. Clin. Invest., 76: 1323-1329, 1985.
27. Whitehead, V. M., Rosenblatt, D. S., Vuchich, M-J., Shuster, J. J., Witte, A., and Beaulieu, D. Accumulation of methotrexate and methotrexate polyglutamates in lymphoblasts at diagnosis of childhood acute lymphoblastic leukemia: a pilot prognostic factor analysis. Blood, 76: 44-49, 1990.
28. Barnes, M. J., Estlin, E. J., Taylor, G. A., Calvete, J. A., Newell, D. R., Lunec, J., Hall, A. G., Pearson, A. D. J, Aherne, W., and Hardcastle, A. Impaired polyglutamation as a mechanism of Tomudex resistance in a CCRF-CEM cell line. Br. J. Cancer, 75 (Suppl. 1): 32, 1997.
29. Drake, J. C., Allegra, C. J., Moran, R. G., and Johnston, P. G. Resistance to Tomudex (ZD1694): multifactorial in human breast and colon carcinoma cell lines. Biochem. Pharmacol., 51: 1349-1355, 1996.
30. Cowan, K. H., and Jolivet, J. A. Methotrexate-resistant human breast cancer cell line with multiple defects, including diminished formation of methotrexate polyglutamates. J. Biol. Chem., 259: 10793-10800, 1984.
31. Estlin, E. J., Balmanno, K., Calvert, A. H., Hall, A. G., Lunec, J., Newell, D. R., Pearson, A. D. J., and Taylor, G. A. The relationship between intrinsic thymidylate synthase expression and sensitivity to THYMITAQ™ in human leukaemia and colorectal carcinoma cell lines. Br. J. Cancer, 76: 1579-1585, 1997.
32. Jansen, G., Schornagel, J. H., Westerhof, G. R., Rijksen, G., Newell, D. R., and Jackman, A. L. Multiple membrane transport systems for the uptake of folate-based thymidylate synthase inhibitors. Cancer Res., 50: 7544-7548, 1990.
33. Wohlhueter, R. M., Marz, R., Graff, J. C., and Plagemann, P. G. W. A rapid-mixing technique to measure transport in suspended animal cells: applications to nucleoside transport in Novikoff rat hepatoma cells. Methods Cell Biol., 20: 211-235, 1978.
34. Cheng, Y., and Prusoff, W. H. Relationship between the inhibition constant (Ki) and the concentration of inhibitor which causes 50% inhibition (150) of an enzymatic reaction. Biochem. Pharmacol., 22: 3099-3108, 1973.
35. Jansen, G., Schornagel, J. H., Kathman, I., Westerhof, G. R., Hordijk, G-J., and van der Laan, B. F. A. M. Measurement of folylpolyglutamate synthetase activity in head and neck squamous carcinoma cell lines and clinical samples using a new rapid separation procedure. Oncol. Res., 4: 299-305, 1992.
36. McGuire, J. J., and Russell, C. A. Folylpolyglutamate synthetase expression in antifolate-sensitive and resistant human cell lines. Oncol Res., 10: 193-200, 1998.
37. Aherne, G. W., Ward, E., Lawrence, N., Dobinson, D., Clarke, S. J., Musgrove, H., Sutcliffe, F., Stephens, T., and Jackman, A. L. Comparison of plasma and tissue levels of ZD1694 (Tomudex), a highly polyglutamable quinazoline thymidylate synthase inhibitor, in preclinical models. Br. J. Cancer, 77: 221-226, 1998.
38. Taylor, G. A., Jackman, A. J., Balmanno, K., Hughes, L. R., and Calvert, A. H. Estimation of the in vitro and in vivo inhibitory effects of antifolates upon thymidylate synthase (TS) in whole cells. In: K. Mikanagnagi, K. Nifhioka, and W. N. Kelley (eds.), Purine Metabolism in Man VI, pp. 383-388. New York: Plenum Publishing Corp., 1988.
39. Masson, E., Relling, M. V., Synold, T. W., Liu, Q., Schuetz, J. D., Sandlund, J. T., Pui, C-H., and Evans, W. E. Accumulation of methotrexate polyglutamates in lymphoblasts is a determinant of antileukemic effects in vivo. J. Clin. Invest., 97: 73-80, 1994.
40. McGuire, J. J., Haile, W. H., Russell, C. A., Galvin, J. M., and Shane, B. Evolution of drug resistance in CCRF-CEM human leukemia cells selected by intermittent methotrexate exposure. Oncol. Res., 7: 535-543, 1995.
41. Roy, K., Egan, M. G., Sirlin, S., and Sirotnak, F. M. Post-transcriptionally mediated decrease in folylpolyglutamate synthetase gene expression in some folate analogue-resistant variants of the L1210 cell. J. Biol. Chem., 272: 6903-6908, 1997.
42. Roy, K., and Sirotnak, F. M. A novel posttranscriptional mechanism of antifolate resistance in L1210 cells decreasing synthesis of folylpolyglutaniate synthetase. Proc. Am. Assoc. Cancer Res., 38: 659, 1997.
43. Allegra, C. J., Drake, J. C., Jolivet, J., and Chabner. B. A. Inhibition of phosphoribosylaminoimadazolecarboxamide transformylase by methotrexate and dihydrofolic acid polyglutamates. Proc. Natl. Acad. Sci. USA, 82: 4881-4885, 1985.
44. Whitehead, V. W. Synthesis of methotrexate polyglutamates in L1210 murine leukemia cells. Cancer Res., 37: 408-412, 1977.
45. Drake, J. C., Allegra, C. J., Baram, J., Kaufman, B. T., and Chabner, B. A. Effects of dihydrofolate reductase of methotrexate metabolites and intracellular folates formed following methotrexate exposure of human breast cancer cells. Biochem. Pharmacol., 36: 2416-2418, 1987.
46. Bokkerink, J. P. M., Bakker, M. A. H., Hulscher, T. W., De Abrew, R. R. A., Schretlen, E. D. A. M., van Laarhoven, J. P. R. M., and De Bruyn, C. H. M. M. Sequence-, time- and dose-dependent synergism of methotrexate and 6-mercaptopurine in malignant human T-lympho-blasts. Biochem. Pharmacol., 35: 3549-3555, 1986.
47. Benz, C., and Cadman, E. Modulation of 5-fluorouracil metabolism and cytotoxicity by antimetabolites in human colorectal adenocarcinoma HCT-8. Cancer Res., 41: 994-999, 1992.
48. McGuire, J. J., Heitzman, K. J., Haile, W. H., Russell, C. A., McCloskey, D. E., and Piper, J. R. Cross resistance studies of folylpolyglutamate synthetase-deficient, methotrexate-resistant CCRF-CEM human leukemia sublines. Leukemia (Baltimore), 7: 1996-2003, 1993.
49. Baldwin, S. W., Tse, A., Gossett, L. S., Taylor, E. C., Rosowsky, A., Shih, C., and Moran, R. G. Structural features of 5,10-dideaza-5,6,7,8-tetrahydrofolate that determines inhibition of mammalian glycinamide ribonucleotide formyltransferase. Biochemistry, 30: 1997-2006, 1991.
50. 10-substituted-5,8-didea-zafolates. Adv. Enzyme Regul., 31: 13-27, 1991.
51. Beardsley, G. P., Moroson, B. A., Taylor, E. C., and Moran, R. G. A new folate antimetabolite, 5,10-dideaza-5,6,7,8-tetrahydrofolate is a potent inhibitor of de novo purine synthesis. J. Biol. Chem., 264: 328-333, 1989.