Ribonucleotide reductase inhibition restores platinum-sensitivity in platinum-resistant ovarian cancer: A Gynecologic Oncology Group Study

Journal of Translational Medicine

Volumn 10, Issue 1, 2012, Pages

  Kunos, Charles ^a   Radivoyevitch, Tomas ^b   Abdul Karim, Fadi W ^a   Fanning, James ^c   Abulafia, Ovadia ^d   Bonebrake, Albert J ^e   Usha, Lydia ^f  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

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

^c PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^d SUNY DOWNSTATE MEDICAL CENTER   (United States)

^e Division of Gynecologic Oncology   (United States)

^f RUSH MEDICAL COLLEGE   (United States)

Author keywords

Methemoglobinemia; Ovarian cancer; Ribonucleotide reductase; Triapine

Indexed keywords

3 AMINOPYRIDINE 2 CARBOXYALDEHYDE THIOSEMICARBAZONE; CISPLATIN; METHYLENE BLUE; OXIDOREDUCTASE INHIBITOR; RIBONUCLEOTIDE REDUCTASE; UNCLASSIFIED DRUG; 2'-DEOXYCYTIDINE 5'-TRIPHOSPHATE; 3 AMINOPICOLINALDEHYDE THIOSEMICARBAZONE; 3-AMINOPYRIDINE-2-CARBOXALDEHYDE THIOSEMICARBAZONE; DEOXYCYTIDINE PHOSPHATE; DEOXYCYTIDINE TRIPHOSPHATE; ENZYME INHIBITOR; H2AFX PROTEIN, HUMAN; HISTONE; PLATINUM; PYRIDINE DERIVATIVE; THIOSEMICARBAZONE DERIVATIVE;

ADULT; ANEMIA; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CANCER PATIENT; CELL SURVIVAL; CLINICAL ARTICLE; CONTINUOUS INFUSION; CONTROLLED STUDY; DNA DAMAGE; DRUG EFFICACY; DRUG HYPERSENSITIVITY; DRUG SAFETY; DYSPNEA; ENZYME ACTIVITY; FEMALE; GASTROINTESTINAL DISEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LEUKOPENIA; LUNG DISEASE; METABOLIC DISORDER; METHEMOGLOBINEMIA; MULTIPLE CYCLE TREATMENT; NAUSEA; NEUROLOGIC DISEASE; NEUTROPENIA; OVARY CANCER; OXYGEN THERAPY; PAIN; PROTEIN EXPRESSION; SKIN DISEASE; THROMBOCYTOPENIA; TREATMENT RESPONSE; VOMITING; AGED; CLINICAL TRIAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; ENZYMOLOGY; GYNECOLOGY; IMMUNOBLOTTING; METABOLISM; MIDDLE AGED; ONCOLOGY; OVARY TUMOR; PATHOLOGY; TREATMENT OUTCOME; TUMOR CELL LINE;

ADULT; AGED; CELL LINE, TUMOR; CELL SURVIVAL; DEOXYCYTOSINE NUCLEOTIDES; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; FEMALE; GYNECOLOGY; HISTONES; HUMANS; IMMUNOBLOTTING; MEDICAL ONCOLOGY; MIDDLE AGED; OVARIAN NEOPLASMS; PLATINUM; PYRIDINES; RIBONUCLEOTIDE REDUCTASES; THIOSEMICARBAZONES; TREATMENT OUTCOME;

EID: 84862165672     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-10-79     Document Type: Article

References (35)

1. Armstrong D, Bundy B, Wenzel L, Huang HQ, Baergen R, Lele S, Copeland LJ, Walker JL, Burger RA, . Gynecologic Oncology Group Intraperitoneal cisplatin and paclitaxel in ovarian cancer. N Engl J Med 2006, 354:34-43. 10.1056/NEJMoa052985, 16394300, Gynecologic Oncology Group.
2. Markman M, Kennedy A, Webster K, Peterson G, Kulp B, Belinson J. Combination chemotherapy with carboplatin and docetaxel in the treatment of cancers of the ovary and fallopian tube and primary carcinoma of the peritoneum. J Clin Oncol 2001, 19:1901-1905.
3. Ozols RF, Bundy BN, Greer BE, Fowler JM, Clarke-Pearson D, Burger RA, Mannel RS, DeGeest K, Hartenbach EM, Baergen R. Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study. J Clin Oncol 2003, 21:3194-3200. 10.1200/JCO.2003.02.153, 12860964.
4. du Bois A, Herrstedt J, Hardy-Bessard AC, Muller HH, Harter P, Kristensen G, Joly F, Huober J, Avall-Lundquist E, Weber B, Kurzeder C, Jelic S, Pujade-Lauraine E, Burges A, Pfisterer J, Gropp M, Staehle A, Wimberger P, Jackisch C, Sehouli J. Phase III trial of carboplatin plus paclitaxel with or without gemcitabine in first-line treatment of epithelial ovarian cancer. J Clin Oncol 2010, 28:4162-4169. 10.1200/JCO.2009.27.4696, 20733132.
5. Brewer CA, Blessing JA, Nagourney RA, Morgan M, Hanjani P. Cisplatin plus gemcitabine in platinum-refractory ovarian or peritoneal cancer: a phase II study of the Gynecologic Oncology Group. Gynecol Oncol 2006, 103:446-450. 10.1016/j.ygyno.2006.03.018, 16643994.
6. Peng P, Shen K, Yang JX, Wu M, Huang HF, Pan LY, Lang JH. Phase II study of gemcitabine combined with platinum chemotherapy for recurrent epithelial ovarian cancer. Chin Med Sci J 2007, 22:177-182.
7. Kunos CA, Waggoner S, Von Gruenigen V, Eldermire E, Pink J, Dowlati A, Kinsella TJ. Phase I trial of intravenous 3-aminopyridine-2-carboxaldehyde thiosemicarbazone (3-AP, NSC #663249) in combination with pelvic radiation therapy and weekly cisplatin chemotherapy for locally advanced cervical cancer. Clin Cancer Res 2010, 16:1298-1306. 10.1158/1078-0432.CCR-09-2469, 2822897, 20145183.
8. Dueñas-González A, Zárba J, Patel F, Alcedo JC, Beslija S, Casanova L, Pattaranutaporn P, Hameed S, Blair JM, Barraclough H, Orlando M. A phase III, open-label, randomized study comparing concurrent gemcitabine plus cisplatin and radiation followed by adjuvant gemcitabine and cisplatin versus concurrent cisplatin and radiation in patients with stage IIB to IVA carcinoma of the cervix. J Clin Oncol 2011, 29:1678-1685. 10.1200/JCO.2009.25.9663, 21444871.
9. Rose P, DeGeest K, McMeekin S, Fusco N. A phase I study of gemcitabine followed by cisplatin concurrent with whole pelvic radiation therapy in locally advanced cervical cancer: A Gynecologic Oncology Group study. Gynecol Oncol 2007, 107:274-279. 10.1016/j.ygyno.2007.06.012, 17688925.
10. Kunos C, Radivoyevitch T, Pink J, Chiu SM, Stefan T, Jacobberger J, Kinsella TJ. Ribonucleotide reductase inhibition enhances chemoradiosensitivity of human cervical cancers. Radiation Res 2010, 174:574-581. 10.1667/RR2273.1, 20954859.
11. Kunos CA, Chiu SM, Pink J, Kinsella TJ. Modulating radiation resistance by inhibiting tribonucleotide reductase in cancers with virally or mutationally silenced p53 protein. Radiation Res 2009, 172:666-676. 10.1667/RR1858.1, 2818576, 19929413.
12. Kunos C, Ferris G, Pyatka N, Pink J, Radivoyevitch T. Deoxynucleoside salvage facilitates DNA repair during tibonucleotide reductase blockade in human cervical cancers. Radiat Res 2011, 176:425-433. 10.1667/RR2556.1, 21756082.
13. Schöndorf T, Neumann R, Benz C, Becker M, Riffelmann M, Göhring UJ, Sartorius J, von König CH, Breidenbach M, Valter MM, Hoopman M, Di Nicolantonio F, Kurbacher CM. Cisplatin, doxorubicin and paclitaxel induce mdr1 gene transcription in ovarian cancer cell lines. Recent Results Cancer Res 2003, 161:111-116. 10.1007/978-3-642-19022-3_10, 12528803.
14. Lemos C, Kathmann I, Giovannetti E, Beliën JAM, Scheffer GL, Calhau C, Jansen G, Peters GJ. Cellular folate status modulates the expression of BCRP and MRP multidrug transporters in cancer cell lines from different origins. Mol Cancer Ther 2009, 8:655-664. 10.1158/1535-7163.MCT-08-0768, 19240161.
15. Yen Y, Margolin K, Doroshow J, Fishman M, Johnson B, Clairmont C, Sullivan D, Sznol M. A phase I trial of 3-aminopyridine-2-carboxaldehyde thiosemicarbazone in combination with gemcitabine for patients with advanced cancer. Cancer Chemother Pharmacol 2004, 54:331-342.
16. Murren J, Modiano M, Clairmont C, Lambert P, Savaraj N, Doyle T, Sznol M. 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 2003, 9:4092-4100.
17. Feun L, Modiano M, Lee K, Mao J, Marini A, Savaraj N, Plezia P, Almassian B, Colacino E, Fischer J, MacDonald S. Phase I and pharmacokinetic study of 3-aminopyridine-2-carboxaldehyde thiosemicarbazone (3-AP) using a single intravenous dose schedule. Cancer Chemother Pharmacol 2002, 50:223-229. 10.1007/s00280-002-0480-0, 12203104.
18. Wadler S, Makower D, Clairmont C, Lambert P, Fehn K, 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 2004, 22:1553-1563. 10.1200/JCO.2004.07.158, 15117978.
19. Olive P, Banáth J. Kinetics of H2AX phosphorylation after exposure to cisplatin. Cytometry B Clin Cytol 2009, 76:79-90.
20. Olive P, Banáth J. Phosphorylation of histone H2AX as a measure of radiosensitivity. Int J Radiation Oncol Biol Phys 2004, 58:331-335.
21. Mansouri A, Lurie AA. Concise review: methemoglobinemia. Amer J Hematol 1993, 42:7-12.
22. Radivoyevitch T, Taverna P, Schupp J, et al. The linear-quadratic log-survival radiation dose response model: Confidence ellipses, drug-drug interactions, and brachytherapeutic gains. Med Hypotheses Res 2004, 1:23-28.
23. Reece SY, Hodgkiss JM, Stubbe J, Nocera DG. Proton-coupled electron transfer: the mechanisitc underpinning for radical transport and catalysis in biology. Phil Trans R Soc B 2006, 361:1351-1364. 10.1098/rstb.2006.1874, 1647304, 16873123.
24. Hreshchyshyn MM, Aron BS, Boronow RC, Franklin EW, Shingleton HM, Blessing JA. Hydroxyurea or placebo combined with radiation to treat stages IIIB and IV cervical cancer confined to the pelvis. Int J Radiat Oncol Biol Phys 1979, 5:317-322. 10.1016/0360-3016(79)91209-4, 110744.
25. Whitney CW, Sause W, Bundy BN, Malfetano JH, Hannigan EV, Fowler WC, Clarke-Pearson DL, Liao SY. Randomized comparison of fluorouracil plus cisplatin versus hydroxyurea as an adjunct to radiation therapy in stage IIB-IVA carcinoma of the cervix with negative para-aortic lymph nodes: a Gynecologic Oncology Group and Southwest Oncology Group study. J Clin Oncol 1999, 17:1339-1348.
26. Rose P, Ali S, Watkins E, Thigpen JT, Deppe G, Clarke-Pearson DL, Insalaco S, . Gynecologic Oncology Group Long-term follow-up of a randomized trial comparing concurrent single agent cisplatin, cisplatin-based combination chemotherapy, or hydroxyurea during pelvic irradiation for locally advanced cervical cancer: A Gynecologic Oncology Group Study. J Clin Oncol 2007, 25:2804-2810. 10.1200/JCO.2006.09.4532, 17502627, Gynecologic Oncology Group.
27. Schelman W, Morgan-Meadows S, Marnocha R, Lee F, Eickhoff J, Huang W, Pomplun M, Jiang Z, Alberti D, Kolesar JM, Ivy P, Wilding G, Traynor AM. A phase I study of Triapine in combination with doxorubicin in patients with advanced solid tumors. Cancer Chemother Pharmacol 2009, 63:1147-1156. 10.1007/s00280-008-0890-8, 3050713, 19082825.
28. Traynor AM, Lee JW, Bayer GK, Tate JM, Thomas SP, Mazurczak M, Graham DL, Kolesar JM, Schiller JH. A phase II trial of triapine (NSC #663249) and gemcitabine as second line treatment of advanced non-small cell lung cancer: Eastern Cooperative Oncology Group Study 1503. Invest New Drugs 2010, 28:91-97. 10.1007/s10637-009-9230-z, 3045859, 19238328.
29. Swinnen LJ, Rankin C, Carraway H, Albain KS, Townsend JJ, Budd GT, Kish JA, Rivkin SE, Blumenthal DT. A phase II study of cisplatin preceded by a 12-h continuous infusion of concurrent hydroxyurea and cytosine arabinoside (Ara-C) for adult patients with malignant gliomas (Southwest Oncology Group S9149). J Neurooncol 2008, 86:353-358. 10.1007/s11060-007-9483-3, 18175205.
30. Piver M, Khalil M, Emrich L. Hydroxyurea plus pelvic irradiation versus placebo plus pelvic irradiation in nonsurgically staged stage IIIB cervical cancer. J Surg Oncol 1989, 42:120-125. 10.1002/jso.2930420211, 2796346.
31. Chabes A, Thelander L. Controlled protein degradation regulates ribonucleotide reductase activity in proliferating mammalian cells during the normal cell cycle and in response to DNA damage and replication blocks. J Biol Chem 2000, 275:17747-17753. 10.1074/jbc.M000799200, 10747958.
32. Wang D, Lippard SJ. Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 2005, 4:307-320. 10.1038/nrd1691, 15789122.
33. Chaston TB, Lovejoy DB, Watts RN, Richardson DR. Examination of the antiproliferative activity of iron chelators: multiple cellular targets and the different mechanism of action of triapine compared with desferrioxamine and the potent pyridoxal isonicotinoyl hydrazone analogue 311. Clin Cancer Res 2003, 9(1):402-414.
34. Popović-Bijelić A, Kowol CR, Lind ME, Luo J, Himo F, Enyedy EA, Arion VB, Gräslund A. Ribonucleotide reductase inhibition by metal complexes of Triapine (3-aminopyridine-2-carboxaldehyde thiosemicarbazone): A combined experimental and theoretical study. J Inorg Biochem 2011, 105(11):1422-1431. 10.1016/j.jinorgbio.2011.07.003, 3374975, 21955844.
35. do Nascimento TS, Pereira RO, de Mello HL, Costa J. Methemoglobinemia: from diagnosis to treatment. Rev Bras Anestesiol 2008, 58:651-64. 10.1590/S0034-70942008000600011, 19082413.