Electron transfer-based combination therapy of cisplatin with tetramethyl-p-phenylenediamine for ovarian, cervical, and lung cancers

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 26, 2012, Pages 10175-10180

  Luo, Ting ^a   Yu, Jianqing ^a,e   Nguyen, Jenny ^a   Wang, Chun Rong ^a   Bristow, Robert G ^b,c   Jaffray, David A ^b,c   Zhou, Xiao Zhen ^d   Lu, Kun Ping ^d   Lu, Qing Bin ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d HARVARD MEDICAL SCHOOL   (United States)

^e WUHAN UNIVERSITY   (China)

Author keywords

Biological chemistry; Biophysics; Chemical biology; Physical biology

Indexed keywords

CISPLATIN; DOUBLE STRANDED DNA; N,N,N',N' TETRAMETHYL 1,4 PHENYLENEDIAMINE;

APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CELL VIABILITY; CONTROLLED STUDY; DNA FRAGMENTATION; DOUBLE STRANDED DNA BREAK; DRUG POTENTIATION; ELECTRON TRANSFER BASED COMBINATION THERAPY; ELECTRON TRANSPORT; FEMALE; FLOW CYTOMETRY; FLUORESCENCE SPECTROSCOPY; HELA CELL; HUMAN; HUMAN CELL; LUNG CANCER; OVARY CANCER; PRIORITY JOURNAL; STEADY STATE; UTERINE CERVIX CANCER;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; ELECTRON TRANSPORT; FEMALE; FLOW CYTOMETRY; HUMANS; LUNG NEOPLASMS; OVARIAN NEOPLASMS; SPECTROMETRY, FLUORESCENCE; TETRAMETHYLPHENYLENEDIAMINE; UTERINE CERVICAL NEOPLASMS;

EID: 84862983611     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1203451109     Document Type: Article

References (49)

1. Kavarnos GJ, Turro NJ (1986) Photosensitization by reversible electron-transfer-theories, experimental-evidence, and examples. Chem Rev 86:401-449.
2. Marcus RA (1993) Electron transfer reactions in chemistry: Theory and experiment (Nobel Lecture). Rev Mod Phys 65:599-610.
3. Gray HB, Winkler JR (1996) Electron transfer in proteins. Ann Rev Biochem 65:537-561. (Pubitemid 26250619)
4. Wan C, Fiebig T, Schiemann O, Barton JK, Zewail AH (2000) Femtosecond direct observation of charge transfer between bases in DNA. Proc Natl Acad Sci USA 97:14052-14055. (Pubitemid 32016527)
5. Lu QB (2010) Cosmic-ray-driven electron-induced reactions of halogenated molecules adsorbed on ice surfaces: Implications for atmospheric ozone depletion and global climate change. Phys Rep 487:141-167.
6. Wang CR, Nguyen J, Lu QB (2009) Bond breaks of nucleotides by dissociative electron transfer of nonequilibrium prehydrated electrons: A new molecular mechanism for reductive DNAdamage. J Am Chem Soc 131:11320-11322.
7. Nguyen J, et al. (2011) Direct observation of ultrafast electron transfer reactions unravels high effectiveness of reductive DNA damage. Proc Natl Acad Sci USA 108:11778-11783.
8. Zewail AH (2000) Femtochemistry: Atomic-scale dynamics of the chemical bond using ultrafast lasers (Nobel Lecture). Angew Chem Int Ed 39:2587-2631.
9. Lu QB (2010) Effects of ultrashort-lived prehydrated electrons in radiation biology and their applications for radiotherapy of cancer. Mutat Res Rev Mutat Res 704:190-199.
10. Wang CR, Hu A, Lu QB (2006) Direct observation of the transition state of ultrafast electron transfer reaction of a radiosensitizing drug bromodeoxyuridine. J Chem Phys 124:241102.
11. Wang CR, Lu QB (2007) Real-time observation of a molecular reaction mechanism of aqueous 5-halo-2′-deoxyuridines under UV/ionizing radiation. Angew Chem Int Ed 46:6316-6321.
12. Wang CR, Lu QB (2010) Molecular mechanism of the DNA sequence selectivity of 5-halo-2′-deoxyuridines as potential radiosensitizers. J Am Chem Soc 132:14710-14713.
13. Lu QB (2007) Molecular reaction mechanisms of combination treatments of low-dose cisplatin with radiotherapy and photodynamic therapy. J Med Chem 50:2601-2604.
14. Lu QB, Kalantari S, Wang CR (2007) Electron transfer reaction mechanism of cisplatin with DNA at the molecular level. Mol Pharm 4:624-628. (Pubitemid 47310174)
15. Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics. CA Cancer J Clin 60:277-300.
16. Godwin AK, et al. (1992) High resistance to cisplatin in human ovarian cancer cell lines isassociated with marked increase of glutathione synthesis. Proc Natl Acad Sci USA 89:3070-3074.
17. Agarwal R, Kaye SB (2003) Ovarian cancer: Strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 3:502-516. (Pubitemid 37328838)
18. Sakai W, et al. (2008) Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 451:1116-1120. (Pubitemid 351317449)
19. Stewart JM, et al. (2011) Phenotypic heterogeneity and instability of human ovarian tumor-initiating cells. Proc Natl Acad Sci USA 108:6468-6473.
20. Cancer Genome Atlas Research Network (2011) Integrated genomic analyses of ovarian carcinoma. Nature 474:609-615.
21. Rosenberg B, van Camp L, Trosko JE, Mansour VH (1969) Platinum compounds: A new class of potent antitumor agents. Nature 222:385-386.
22. Reedijk J (2003) New clues for platinum antitumor chemistry: Kinetically controlled metal binding to DNA. Proc Natl Acad Sci USA 100:3611-3616.
23. Fuertes MA, Alonso C, Perez JM (2003) Biochemical modulation of cisplatin mechanisms of action: Enhancement of antitumor activity and circumvention of drug resistance. Chem Rev 103:645-662.
24. Wang D, Lippard SJ (2005) Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 4:307-320. (Pubitemid 41130944)
25. Kaiser J (2011) Combining target drugs to stop resistant tumors. Science 331:1542-1545.
26. Schaake-Koning C, et al. (1992) Effects of concomitant cisplatin and radiotherapy on inoperable non-small-cell lung cancer. N Engl J Med 326:524-530.
27. Rose PG, et al. (1999) Concurrent cisplatin-based radiotherapy and chemotherapy for locally advanced cervical cancer. N Engl J Med 340:1144-1153. (Pubitemid 29177873)
28. Peters GJ, et al. (2000) Basis for effective combination cancer chemotherapy with antimetabolites. Pharmacol Ther 87:227-253.
29. Berrada M, Yang Z, Lehnert S (2004) Tumor control by combined interstitial radio/chemotherapy. Radiat Res 162:64-70.
30. Seiwert TY, Salama JK, Vokes EE (2007) The chemoradiation paradigm in head and neck cancer. Nat Clin Prac Oncol 4:156-171. (Pubitemid 46358853)
31. Lehnert S (2007) Biomolecular Action of Ionizing Radiation (Taylor & Francis Ltd., New York).
32. Bristow RG, Hill RP (2008) Hypoxia DNA repair and genetic instability. Nat Rev Cancer 8:180-192.
33. Kopyra J, Koenig-Lehmann C, Bald I, Illenberger E (2009) A single slow electron triggers the loss of both chlorine atoms from the anticancer drug cisplatin: Implications for chemoradiationtherapy. Angew Chem Int Ed 48:7904-7907.
34. Kuduk-Jaworska J, Chojnacki H, Jański JJ (2011) Non-empirical quantum chemical studies on electron transferreactions in trans- and cis-diamminedichloroplatinum(II) complexes. J Mol Model 17:2411-2421.
35. Jurtshu KP, Jr., McQuitty DN, Riley WH (1979) Use of 3,3′- diaminobenzidine as a biochemical electron-donor for studies on terminal cytochrome-oxidase activity in azotobacter-vinelandii. Curr Microbiol 2:349-354. (Pubitemid 10213871)
36. Hamilton TC, et al. (1983) Characterization of a human ovarian carcinoma cell line (NIH:OVCAR-3) with androgen and estrogen receptors. Cancer Res 43:5379-5389. (Pubitemid 14230154)
37. Rogan AM, Hamilton TC, Young RC, Klecker RW, Ozols RF (1984) Reversal of Adriamycin resistance by verapamil in human ovarian cancer. Science 224:994-996. (Pubitemid 14105761)
38. Hamilton TC, Young RC, Ozols RF (1984) Experimental model systems of ovarian cancer: Applications to the design and evaluation of new treatment approaches. Semin Oncol 11:285-298. (Pubitemid 14013135)
39. Hamilton TC, et al. (1984) Characterization of a xenograft model of human ovarian carcinoma which produces ascites and intraabdominal carcinomatosis in mice. Cancer Res 44:5286-5290. (Pubitemid 15204502)
40. Hirata Y, Ichikawa M, Mataga N (1990) Monophotonic ionization from the vibrationally unrelaxed excited singlet state of N,N,N′,N′- tetramethyl-p-phenylenediamine in acetonitrile solution. J Phys Chem 94:3872-3874.
41. Shimamori H, Musasa H (1995) Spectroscopic observation of contact ion pairs formed from photolyzed TMPD and TMB in the presence of halogenated compounds in nonpolar solvents. J Phys Chem 99:14359-14364.
42. Egdell R, Green JC, Rao CNR (1975) Photoelectron spectra of substituted benzenes. Chem Phys Lett 33:600-607.
43. Fujiwara H, Fukumoto H, Fukumura H, Masuhara H (1998) Dynamics of excited and ionic states of N,N,N′,N′-tetramethyl-p-phenylenediaminein poly(methyl methacrylate) underablation condition. Res Chem Intermediat 24:879-892. (Pubitemid 128608701)
44. Nowosielska A, Marinus MG (2005) Cisplatin induces DNA double-strand break formation in Escherichia coli dam mutants. DNA Repair 4:773-781. (Pubitemid 40835849)
45. Frankenberg-Schwager M, et al. (2005) Cisplatin-mediated DNA double-strand breaks in replicating but not in quiescent cells of the yeast Saccharomyces cerevisiae. Toxicol 212:175-184. (Pubitemid 40981974)
46. Green JA, et al. (1984) Potentiation of melphalan cytotoxicity in human ovarian cancer cell lines by glutathione depletion. Cancer Res 44:5427-5431. (Pubitemid 15204523)
47. Rudin CM, et al. (2003) Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res 63:312-318. (Pubitemid 36152486)
48. Pompella A, Visvikis A, Paolicchi A, De Tata V, Casini AF (2003) The changing faces of glutathione, a cellular protagonist. Biochem Pharmacol 66:1499-1503. (Pubitemid 38373339)
49. Brown JM (1999) The hypoxic cell: A target for selective cancer therapy (18th Bruce F Cain Memorial Award Lecture). Cancer Res 59:5863-5870.