In vitro study on the schedule-dependency of the interaction between pemetrexed, gemcitabine and irradiation in non-small cell lung cancer and head and neck cancer cells

BMC Cancer

Volumn 10, Issue , 2010, Pages

  Wouters, An ^a   Pauwels, Bea ^a   Lardon, Filip ^a   Pattyn, Greet G O ^a   Lambrechts, Hilde A J ^a   Baay, Marc ^a   Meijnders, Paul ^a   Vermorken, Jan B ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GEMCITABINE; PEMETREXED; ANTINEOPLASTIC AGENT; DEOXYCYTIDINE; DRUG DERIVATIVE; GLUTAMIC ACID DERIVATIVE; GUANINE;

ARTICLE; CANCER CELL CULTURE; CANCER RADIOTHERAPY; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL SURVIVAL; CHRONOSEQUENCE; CHRONOTHERAPY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; HEAD AND NECK CANCER; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; RADIOSENSITIVITY; CELL CYCLE; CELL PROLIFERATION; DRUG EFFECT; DRUG INTERACTION; FLOW CYTOMETRY; HEAD AND NECK TUMOR; LUNG TUMOR; MULTIMODALITY CANCER THERAPY; PATHOLOGY; RADIATION DOSE; RADIATION EXPOSURE; SQUAMOUS CELL CARCINOMA; TUMOR CELL CULTURE;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; CELL CYCLE; CELL PROLIFERATION; COMBINED MODALITY THERAPY; DEOXYCYTIDINE; DRUG INTERACTIONS; DRUG SYNERGISM; FLOW CYTOMETRY; GLUTAMATES; GUANINE; HEAD AND NECK NEOPLASMS; HUMANS; LUNG NEOPLASMS; RADIOTHERAPY DOSAGE; TUMOR CELLS, CULTURED;

EID: 77955705494     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-10-441     Document Type: Article

References (55)

1. Seiwert TY, Salama JK, Vokes EE. The concurrent chemoradiation paradigm--general principles. Nat Clin Pract Oncol 2007, 4:86-100. 10.1038/ncponc0714, 17259930.
2. Peters GJ, van der Wilt CL, Van Moorsel CJA, Kroep JR, Bergman AM, Ackland SP. Basis for effective combination cancer chemotherapy with antimetabolites. Pharmacol Ther 2000, 87:227-253. 10.1016/S0163-7258(00)00086-3, 11008002.
3. Mackey JR, Mani RS, Selner M, Mowles D, Young JD, Belt JA, Crawford CR, Cass CE. Functional nucleoside transporters are required for gemcitabine influx and manifestation of toxicity in cancer cell lines. Cancer Res 1998, 58:4349-4357.
4. Huang P, Chubb S, Hertel LW, Grindey GB, Plunkett W. Action of 2',2'-difluorodeoxycytidine on DNA synthesis. Cancer Res 1991, 51:6110-6117.
5. Pauwels B, Korst A, Lardon F, Vermorken J. Combined modality therapy of gemcitabine and radiation. Oncologist 2005, 10:34-51. 10.1634/theoncologist.10-1-34, 15632251.
6. Robinson BW, Shewach DS. Radiosensitization by gemcitabine in p53 wild-type and mutant MCF-7 breast carcinoma cell lines. Clin Cancer Res 2001, 7:2581-2589.
7. Morgan M, Parsels L, Parsels J, Mesiwala A, Maybaum J, Lawrence T. Role of checkpoint kinase 1 in preventing premature mitosis in response to gemcitabine. Cancer Res 2005, 65:6835-42. 10.1158/0008-5472.CAN-04-2246, 16061666.
8. 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.
9. Wachters FM, van Putten JWG, Maring JG, Zdzienicka MZ, Groen HJM, Kampinga HH. Selective targeting of homologous DNA recombination repair by gemcitabine. Int J Rad Oncol Biol Phys 2003, 57:553-562.
10. Pauwels B, Vermorken JB, Wouters A, Ides J, Van LS, Lambrechts HA, Pattyn GG, Vermeulen K, Meijnders P, Lardon F. The role of apoptotic cell death in the radiosensitising effect of gemcitabine. Br J Cancer 2009, 101:628-636. 10.1038/sj.bjc.6605145, 2736812, 19672265.
11. van Putten JWG, Groen HJM, Smid K, Peters GJ, Kampinga HH. End-joining deficiency and radiosensitization induced by gemcitabine. Cancer Res 2001, 61:1585-1591.
12. Jensen A, Debus J, Weber KJ. S-phase cell-specific modification by gemcitabine of PFGE-analyzed radiation-induced DNA fragmentation and rejoining. Int J Radiat Biol 2008, 84:770-777. 10.1080/09553000802317752, 18821391.
13. Flanagan SA, Robinson BW, Krokosky CM, Shewach DS. Mismatched nucleotides as the lesions responsible for radiosensitization with gemcitabine: a new paradigm for antimetabolite radiosensitizers. Mol Cancer Ther 2007, 6:1858-1868. 10.1158/1535-7163.MCT-07-0068, 17575114.
14. Van Bree C, Rodermond H, de Vos J, Haveman J, Franken N. Mismatch repair proficiency is not required for radioenhancement by gemcitabine. Int J Radiat Oncol Biol Phys 2005, 62:1504-9.
15. Hanauske AR, Chen V, Paoletti P, Niyikiza C. Pemetrexed disodium: A novel Antifolate clinically active against multiple solid tumors. Oncologist 2001, 6:363-373. 10.1634/theoncologist.6-4-363, 11524555.
16. Vogelzang NJ, Rusthoven JJ, Symanowski J, Denham C, Kaukel E, Ruffie P, Gatzemeier U, Boyer M, Emri S, Manegold C, Niyikiza C, Paoletti P. Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J Clin Oncol 2003, 21:2636-2644. 10.1200/JCO.2003.11.136, 12860938.
17. Hanna N, Shepherd FA, Fossella FV, Pereira JR, De Marinis F, von Pawel J, Gatzemeier U, Tsao TCY, Pless M, Muller T, Lim HL, Desch C, Szondy K, Gervais R, Manegold C, Paul S, Paoletti P, Einhorn L, Bunn PA. Randomized phase III trial of pemetrexed versus docetaxel in patients with non-small-cell lung cancer previously treated with chemotherapy. J Clin Oncol 2004, 22:1589-1597. 10.1200/JCO.2004.08.163, 15117980.
18. Scagliotti GV, Parikh P, von PJ, Biesma B, Vansteenkiste J, Manegold C, Serwatowski P, Gatzemeier U, Digumarti R, Zukin M, Lee JS, Mellemgaard A, Park K, Patil S, Rolski J, Goksel T, De MF, Simms L, Sugarman KP, Gandara D. 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, 26:3543-3551. 10.1200/JCO.2007.15.0375, 18506025.
19. Belani CP, Brodowicz T, Ciuleanu T, Kim JH, Krzakowski M, Laack E, Wu YL, Peterson P, Krejcy K, Zielinski C. Maintenance pemetrexed (Pem) plus best supportive care (BSC) versus placebo (Plac) plus BSC: A randomized phase III study in advanced non-small cell lung cancer (NSCLC). J Clin Oncol 2009, 27:CRA8000.
20. Habeck LL, Mendelsohn LG, Shih C, Taylor EC, Colman PD, Gossett LS, Leitner TA, Schultz RM, Andis SL, Moran RG. Substrate specificity of mammalian folylpolyglutamate synthetase for 5,10-dideazatetrahydrofolate analogs. Mol Pharmacol 1995, 48:326-333.
21. Shih C, Chen VJ, Gossett LS, Gates SB, MacKellar WC, Habeck LL, Shackelford KA, Mendelsohn LG, Soose DJ, Patel VF, Andis SL, Bewley JR, Rayl EA, Moroson BA, Beardsley GP, Kohler W, Ratnam M, Schultz RM. LY231514, a pyrrolo[2,3-d]pyrimidine-based antifolate that inhibits multiple folate-requiring enzymes. Cancer Res 1997, 57:1116-1123.
22. Giovannetti E, Mey V, Nannizzi S, Pasqualetti G, Marini L, Del Tacca M, Danesi R. Cellular and pharmacogenetics foundation of synergistic interaction of pemetrexed and gemcitabine in human non-small-cell lung cancer cells. Mol Pharmacol 2005, 68:110-8.
23. Bischof M, Weber KJ, Blatter J, Wannenmacher M, Latz D. Interaction of pemetrexed disodium (Alimta, multitargeted antifolate) and irradiation in vitro. Int J Rad Oncol Biol Phys 2002, 52:1381-1388.
24. Teicher BA, Alvarez E, Liu PC, Lu K, Menon K, Dempsey J, Schultz RM. MTA (LY231514) in combination treatment regimens using human tumor xenografts and the EMT-6 murine mammary carcinoma. Sem in Oncol 1999, 26:55-62.
25. Teicher BA, Chen V, Shih C, Menon K, Forler PA, Phares VG, Amsrud T. Treatment regimens including the multitargeted antifolate LY231514 in human tumor xenografts. Clin Cancer Res 2000, 6:1016-1023.
26. Seiwert TY, Connell PP, Mauer AM, Hoffman PC, George CM, Szeto L, Salgia R, Posther KE, Nguyen B, Haraf DJ, Vokes EE. A phase I study of pemetrexed, carboplatin, and concurrent radiotherapy in patients with locally advanced or metastatic non-small cell lung or esophageal cancer. Clin Cancer Res 2007, 13:515-522. 10.1158/1078-0432.CCR-06-1058, 17255273.
27. Specenier PM, Van den Weyngaert D, Van LC, Weyler J, Van den Brande J, Huizing MT, Dyck J, Schrijvers D, Vermorken JB. Phase II feasibility study of concurrent radiotherapy and gemcitabine in chemonaive patients with squamous cell carcinoma of the head and neck: long-term follow up data. Ann Oncol 2007, 18:1856-1860. 10.1093/annonc/mdm346, 17823386.
28. Pauwels B, Korst AEC, De Pooter CMJ, Pattyn GGO, Lambrechts HAJ, Baay MFD, Lardon F, Vermorken JB. Comparison of the sulforhodamine B assay and the clonogenic assay for in vitro chemoradiation studies. Cancer Chemother Pharmacol 2003, 51:221-226.
29. Tonkinson JL, Worzalla JF, Teng CH, Mendelsohn LG. Cell cycle modulation by a multitargeted antifolate, LY231514, increases the cytotoxicity and antitumor activity of gemcitabine in HT29 colon carcinoma. Cancer Res 1999, 59:3671-3676.
30. Giovannetti E, Mey V, Danesi R, Mosca I, Del Tacca M. Synergistic cytotoxicity and pharmacogenetics of gemcitabine and pemetrexed combination in pancreatic cancer cell lines. Clin Cancer Res 2004, 10:2936-2943. 10.1158/1078-0432.CCR-03-0520, 15131028.
31. Dy GK, Suri A, Reid JM, Sloan JA, Pitot HC, Alberts SR, Goldberg RM, Atherton PJ, Hanson LJ, Burch PA, Rubin J, Erlichman C, Adjei AA. A phase IB study of the pharmacokinetics of gemcitabine and pemetrexed, when administered in rapid sequence to patients with advanced solid tumors. Cancer Chemother Pharmacol 2005, 55:522-30. 10.1007/s00280-004-0950-7, 15754203.
32. Treat J, Bonomi P, McCleod M, Christiansen NP, Mintzer DM, Monberg MJ, Ye Z, Chen R, Obasaju CK. Administration of pemetrexed immediately following gemcitabine as front-line therapy in advanced non-small cell lung cancer: a phase II trial. Lung Cancer 2006, 53:77-83. 10.1016/j.lungcan.2006.04.005, 16730854.
33. West HL, Wakelee HA, Perry MC, Belt RJ, Chen R, Obasaju C. Gemcitabine and pemetrexed administered in rapid sequence as front-line chemotherapy for advanced non-small-cell lung cancer: a phase II clinical trial. Ann Oncol 2009, 20:850-856. 10.1093/annonc/mdn715, 19150937.
34. Pauwels B, Korst AEC, Pattyn GGO, Lambrechts HAJ, Van Bockstaele DR, Vermeulen K, Lenjou M, De Pooter CMJ, Vermorken JB, Lardon F. Cell cycle effect of gemcitabine and its role in the radiosensitizing mechanism in vitro. Int J Radiat Oncol Biol Phys 2003, 57:1075-1083.
35. Watson JV, Chambers SH, Smith PJ. A pragmatic approach to the analysis of DNA histograms with a definable G1 peak. Cytometry 1987, 8:1-8. 10.1002/cyto.990080101, 3803091.
36. Fertil B, Dertinger H, Courdi A, Malaise EP. Mean inactivation dose: a useful concept for intercomparison of human cell survival curves. Radiation Res 1984, 99:73-84. 10.2307/3576448, 6739728.
37. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006, 58:621-681. 10.1124/pr.58.3.10, 16968952.
38. Bischof M, Abdollahi A, Gong P, Stoffregen C, Lip KE, Debus JU, Weber KJ, Huber PE. Triple combination of irradiation, chemotherapy (pemetrexed), and VEGFR inhibition (SU5416) in human endothelial and tumor cells. Int J Radiat Oncol Biol Phys 2004, 1220-32.
39. Pauwels B, Korst AEC, De Pooter CMJ, Lambrechts HAJ, Pattyn GGO, Lardon F, Vermorken JB. The radiosensitising effect of gemcitabine and the influence of the rescue agent amifostine in vitro. Eur J Cancer 2003, 39:838-846. 10.1016/S0959-8049(03)00002-9, 12651211.
40. Peters GJ, Clavel M, Noordhuis P, Geyssen GJ, Laan AC, Guastalla J, Edzes HT, Vermorken JB. Clinical phase I and pharmacology study of gemcitabine (2', 2'-difluorodeoxycytidine) administered in a two-weekly schedule. J Chemother 2007, 19:212-221.
41. Rinaldi DA, Kuhn JG, Burris HA, Dorr FA, Rodriguez G, Eckhardt SG, Jones S, Woodworth JR, Baker S, Langley C, Mascorro D, Abrahams T, Von Hoff DD. A phase I evaluation of multitargeted antifolate (MTA, LY231514), administered every 21 days, utilizing the modified continual reassessment method for dose escalation. Cancer Chemother Pharmacol 1999, 44:372-380. 10.1007/s002800050992, 10501910.
42. Nagai S, Takenaka K, Sonobe M, Wada H, Tanaka F. Schedule-dependent synergistic effect of pemetrexed combined with gemcitabine against malignant pleural mesothelioma and non-small cell lung cancer cell lines. Chemotherapy 2008, 54:166-175. 10.1159/000140360, 18560222.
43. Bischof M, Huber P, Stoffregen C, Wannenmacher M, Weber KJ. Radiosensitization by pemetrexed of human colon carcinoma cells in different cell cycle phases. Int J Radiat Oncol Biol Phys 2003, 57:289-292.
44. Tesei A, Ricotti L, De Paola F, Amadori D, Frassineti GL, Zoli W. In vitro schedule-dependent interactions between the multitargeted antifolate LY231514 and gemcitabine in human colon adenocarcinoma cell lines. Clin Cancer Res 2002, 8:233-239.
45. Rodenbach M, Eyol E, Seeli MH, Berger MR. Combination treatment of CC531-lac-Z rat liver metastases by chemoembolization with pemetrexed disodium and gemcitabine. J Cancer Res Clin Oncol 2005, 289-99. 10.1007/s00432-004-0643-y, 15657768.
46. Adjei AA, Erlichman C, Sloan JA, Reid JM, Pitot HC, Goldberg RM, Peethambaram P, Atherton P, Hanson LJ, Alberts SR, Jett J. Phase I and pharmacologic study of sequences of gemcitabine and the multitargeted antifolate agent in patients with advanced solid tumors. J Clin Oncol 2000, 18:1748-1757.
47. Ma CX, Nair S, Thomas S, Mandrekar SJ, Nikcevich DA, Rowland KM, Fitch TR, Windschitl HE, Hillman SL, Schild SE, Jett JR, Obasaju C, Adjei AA, Mayo C, . North Central Cancer Treatment Group, Eli Lilly & Company Randomized phase II trial of three schedules of pemetrexed and gemcitabine as front-line therapy for advanced non-small-cell lung cancer. J Clin Oncol 2005, 23:5929-37. 10.1200/JCO.2005.13.953, 16135464, North Central Cancer Treatment Group, Eli Lilly & Company.
48. Pauwels B, Korst AE, Pattyn GG, Lambrechts HA, Kamphuis JA, De Pooter CM, Peters GJ, Lardon F, Vermorken JB. The relation between deoxycytidine kinase activity and the radiosensitising effect of gemcitabine in eight different human tumour cell lines. BMC Cancer 2006, 6:142. 10.1186/1471-2407-6-142, 1513392, 16734894.
49. Gomez H, Santillana S, Vallejos C, Velarde R, Sanchez J, Wang X, Bauer N, Hockett R, Chen V, Niyikiza C, Hanauske A. A Phase II Trial of Pemetrexed in Advanced Breast Cancer: Clinical Response and Association with Molecular Target Expression. Clin Cancer Res 2006, 12:832-8. 10.1158/1078-0432.CCR-05-0295, 16467096.
50. Giovannetti E, Backus HH, Wouters D, Peters GJ. Functional inactivity and mutations of p53 differentially affect sensitivity to 5-fluorouracil and antifolate inhibitors of thymidylate synthase (TS) by altering TS levels in colorectal cancer cells. Nucleosides Nucleotides Nucleic Acids 2008, 27:740-745. 10.1080/15257770802145512, 18600534.
51. Tonkinson JL, Marder P, Andis SL, Schultz RM, Gossett LS, Shih C, Mendelsohn LG. Cell cycle effects of antifolate antimetabolites: implications for cytotoxicity and cytostasis. Cancer Chemother Pharmacol 1997, 39:521-531. 10.1007/s002800050608, 9118464.
52. Lu XH, Errington J, Curtin NJ, Lunec J, Newell DR. The impact of p53 status on cellular sensitivity to antifolate drugs. Clin Cancer Res 2001, 7:2114-2123.
53. Giovannetti E, Backus HH, Wouters D, Ferreira CG, van H, Brakenhoff RH, Poupon MF, Azzarello A, Pinedo HM, Peters GJ. Changes in the status of p53 affect drug sensitivity to thymidylate synthase (TS) inhibitors by altering TS levels. Br J Cancer 2007, 96:769-775. 10.1038/sj.bjc.6603639, 2360080, 17339891.
54. Pauwels B, Korst AEC, Andriessen V, Baay MFD, Pattyn GGO, Lambrechts HAJ, De Pooter CMJ, Lardon F, Vermorken JB. Unravelling the mechanism of radiosensitisation by gemcitabine: the role of p53. Radiation Research 2005, 164:642-50. 10.1667/RR3445.1, 16238441.
55. Chen M, Hough AM, Lawrence TS. The role of p53 in gemcitabine-mediated cytotoxicity and radiosensitization. Cancer Chemother Pharmacol 2000, 45:369-374. 10.1007/s002800051004, 10803919.