Phytochemicals as anticancer and chemopreventive topoisomerase II poisons

Phytochemistry Reviews

Volumn 13, Issue 1, 2014, Pages 19-35

  Ketron, Adam C ^a   Osheroff, Neil ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bioflavonoids; Catechins; Curcumin; Demethyl epipodophyllotoxins; Isothiocyanates

Indexed keywords

ANTINEOPLASTIC AGENT; CATECHIN; CURCUMIN; DNA TOPOISOMERASE (ATP HYDROLYSING); EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; EPIPODOPHYLLOTOXIN DERIVATIVE; ETOPOSIDE; FLAVONE DERIVATIVE; FLAVONOL DERIVATIVE; GENISTEIN; ISOFLAVONE DERIVATIVE; ISOTHIOCYANIC ACID DERIVATIVE; MIXED LINEAGE LEUKEMIA PROTEIN; PLANT MEDICINAL PRODUCT; SULFORAPHANE; TENIPOSIDE;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; CANCER PREVENTION; CHROMOSOME 11Q; CHROMOSOME TRANSLOCATION; DNA CLEAVAGE; DNA DAMAGE; DNA STRAND BREAKAGE; DRUG BIOAVAILABILITY; DRUG SELECTIVITY; DRUG STRUCTURE; GENOMIC INSTABILITY; GENOTOXICITY; GERM CELL TUMOR; HUMAN; LEUKEMIA; LUNG SMALL CELL CANCER; LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; REVIEW; SARCOMA;

EID: 84896699533     PISSN: 15687767     EISSN: 1572980X     Source Type: Journal    
DOI: 10.1007/s11101-013-9291-7     Document Type: Review

References (146)

1. Adlercreutz H, Markkanen H, Watanabe S (1993) Plasma concentrations of phyto-oestrogens in Japanese men. Lancet 342:1209-1210 (Pubitemid 23331713)
2. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262:5592-5595
3. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB (2007) Bioavailability of curcumin: problems and promises. Mol Pharm 4:807-818
4. Anand P, Thomas SG, Kunnumakkara AB, Sundaram C, Harikumar KB, Sung B, Tharakan ST, Misra K, Priyadarsini IK, Rajasekharan KN, Aggarwal BB (2008) Biological activities of curcumin and its analogues (Congeners) made by man and Mother Nature. Biochem Pharmacol 76:1590-1611
5. Andoh T, Ishida R (1998) Catalytic inhibitors of DNA topoisomerase II. Biochim Biophys Acta 1400:155-171 (Pubitemid 28475101)
6. Annereau JP, Brel V, Dumontet C, Guminski Y, Imbert T, Broussas M, Vispe S, Breand S, Guilbaud N, Barret JM, Bailly C (2008) A fluorescent biomarker of the polyamine transport system to select patients with AML for F14512 treatment. Leuk Res 34:1383-1389
7. Austin CA, Marsh KL (1998) Eukaryotic DNA topoisomerase II b. BioEssays 20:215-226
8. Austin CA, Patel S, Ono K, Nakane H, Fisher LM (1992) Sitespecific DNA cleavage by mammalian DNA topoisomerase II induced by novel flavone and catechin derivatives. Biochem J 282:883-889
9. Bailly C (2012) Contemporary challenges in the design of topoisomerase II inhibitors for cancer chemotherapy. Chem Rev 112:3611-3640
10. Baker NM, Rajan R, Mondragon A (2009) Structural studies of type I topoisomerases. Nucleic Acids Res 37:693-701
11. Baldwin EL, Osheroff N(2005) Etoposide, topoisomerase II and cancer. Curr Med Chem Anti-Cancer Agents 5:363-372 (Pubitemid 40974810)
12. Bandele OJ, Osheroff N (2007) Bioflavonoids as poisons of human topoisomerase IIα and IIβ. Biochemistry 46:6097-6108
13. Bandele OJ, Osheroff N (2008) (-)-Epigallocatechin gallate, a major constituent of green tea, poisons human type II topoisomerases. Chem Res Toxicol 21:936-943 (Pubitemid 351644572)
14. Bandele OJ, Clawson SJ, OsheroffN(2008) Dietary polyphenols as topoisomerase II poisons: B ring and C ring substituents determine the mechanism of enzyme-mediated DNA cleavage enhancement. Chem Res Toxicol 21:1253-1260 (Pubitemid 351967390)
15. Barret JM, Kruczynski A, Vispe S, Annereau JP, Brel V, Guminski Y, Delcros JG, Lansiau A, Guilbaud N, Imbert T, Bailly C (2008) F14512, a potent antitumor agent targeting topoisomerase II vectored into cancer cells via the polyamine transport system. Cancer Res 68:9845-9853
16. Bates AD, Maxwell A (2005) DNA topology. Oxford University Press, New York
17. Bender RP, Osheroff N (2008) DNA topoisomerases as targets for the chemotherapeutic treatment of cancer. In: Dai W (ed) Checkpoint responses in cancer therapy. Humana Press, Totowa, pp 57-91
18. Bender RP, Lehmler HJ, Robertson LW, Ludewig G, Osheroff N (2006) Polychlorinated biphenyl quinone metabolites poison human topoisomerase IIa: altering enzyme function by blocking the N-terminal protein gate. Biochemistry 45:10140-10152 (Pubitemid 44257408)
19. Bender RP, Ham AJ, Osheroff N (2007) Quinone-induced enhancement of DNA cleavage by human topoisomerase IIα: adduction of cysteine residues 392 and 405. Biochemistry 46:2856-2864 (Pubitemid 46420241)
20. Bender RP, Jablonksy MJ, Shadid M, Romaine I, Dunlap N, Anklin C, Graves DE, Osheroff N (2008) Substituents on etoposide that interact with human topoisomerase IIα in the binary enzyme-drug complex: contributions to etoposide binding and activity. Biochemistry 47:4501-4509 (Pubitemid 351522100)
21. Burden DA, Kingma PS, Froelich-Ammon SJ, Bjornsti M-A, Patchan MW, Thompson RB, Osheroff N (1996) Topoisomerase II-etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. J Biol Chem 271:29238-29244 (Pubitemid 26382636)
22. Byl JA, Cline SD, Utsugi T, Kobunai T, Yamada Y, Osheroff N (2001) DNA topoisomerase II as the target for the anticancer drug TOP-53: mechanistic basis for drug action. Biochemistry 40:712-718 (Pubitemid 32096856)
23. Champoux JJ (1994) Mechanism of catalysis by eukaryotic DNA topoisomerase I. Adv Pharmacol 29:71-82
24. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369-413
25. Chen GL, Yang L, Rowe TC, Halligan BD, Tewey KM, Liu LF (1984) Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J Biol Chem 259:13560-13566 (Pubitemid 15221834)
26. Chen W, Qiu J, Shen YM (2012) Topoisomerase IIα, rather than IIβ, is a promising target in development of anti-cancer drugs. Drug Discov Ther 6:230-237
27. Chung FL, Conaway CC, Rao CV, Reddy BS (2000) Chemoprevention of colonic aberrant crypt foci in Fischer rats by sulforaphane and phenethyl isothiocyanate. Carcinogenesis 21:2287-2291 (Pubitemid 32049237)
28. Collin F, Karkare S, Maxwell A (2011) Exploiting bacterial DNA gyrase as a drug target: current state and perspectives. Appl Microbiol Biotechnol 92:479-497
29. Constantinou A, Mehta R, Runyan C, Rao K, Vaughan A, Moon R (1995) Flavonoids as DNA topoisomerase antagonists and poisons: structure-activity relationships. J Nat Prod 58:217-225
30. Corbett KD, Berger JM (2004) Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu Rev Biophys Biomol Struct 33:95-118 (Pubitemid 38829953)
31. Cowell IG, Austin CA (2012) Mechanism of generation of therapy related leukemia in response to anti-topoisomerase II agents. Int J Environ Res Public Health 9:2075-2091
32. Cushman M, Nagarathnam D, Burg DL, Geahlen RL (1991) Synthesis and protein-tyrosine kinase inhibitory activities of flavonoid analogues. J Med Chem 34:798-806
33. D'Arpa P, Beardmore C, Liu LF (1990) Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons. Cancer Res 50:6919-6924 (Pubitemid 20361091)
34. Deweese JE, Osheroff N (2009) The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res 37:738-748
35. Deweese JE, Osheroff N (2010) The use of divalent metal ions by type II topoisomerases. Metallomics 2:450-459
36. Deweese JE, Osheroff MA, Osheroff N (2008) DNA topology and topoisomerases: teaching a "knotty" subject. Biochem Mol Biol Educ 37:2-10
37. Deweese JE, Burch AM, Burgin AB, Osheroff N (2009) Use of divalent metal ions in the DNA cleavage reaction of human type II topoisomerases. Biochemistry 48:1862-1869
38. DhillonN,Aggarwal BB, Newman RA, Wolff RA, Kunnumakkara AB, Abbruzzese JL, Ng CS, Badmaev V, Kurzrock R (2008) Phase II trial of curcumin in patientswith advanced pancreatic cancer. Clin Cancer Res 14:4491-4499
39. Dong KC, Berger JM (2007) Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450:1201-1205
40. Dragsted LO (2003) Antioxidant actions of polyphenols in humans. Int J Vitam Nutr Res 73:112-119
41. Felix CA, Lange BJ, Hosler MR, Fertala J, Bjornsti M-A (1995) Chromosome band 11q23 translocation breakpoints are DNA topoisomerase II cleavage sites. Cancer Res 55:4287-4292
42. Felix CA, Kolaris CP, Osheroff N (2006) Topoisomerase II and the etiology of chromosomal translocations. DNA Repair (Amst) 5:1093-1108 (Pubitemid 44291622)
43. Fortune JM, Osheroff N (1998) Merbarone inhibits the catalytic activity of human topoisomerase IIα by blocking DNA cleavage. J Biol Chem 273:17643-17650 (Pubitemid 28355102)
44. Fortune JM, Osheroff N (2000) Topoisomerase II as a target for anticancer drugs: when enzymes stop being nice. Prog Nucleic Acid Res Mol Biol 64:221-253
45. Fresco P, Borges F, Diniz C, Marques MP (2006) New insights on the anticancer properties of dietary polyphenols. Med Res Rev 26:747-766 (Pubitemid 44735552)
46. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM Press, Washington, DC
47. Galati G, O'Brien PJ (2004) Potential toxicity of flavonoids and other dietary phenolics: significance for their chemopreventive and anticancer properties. Free Radic Biol Med 37:287-303 (Pubitemid 38833996)
48. Geahlen RL, Koonchanok NM, McLaughlin JL, Pratt DE (1989) Inhibition of protein-tyrosine kinase activity by flavanoids and related compounds. J Nat Prod 52:982-986 (Pubitemid 19270608)
49. Gentry AC, Pitts SL, Jablonsky MJ, Bailly C, Graves DE, Osheroff N (2011) Interactions between the etoposide derivative F14512 and human type II topoisomerases: implications for the C4 spermine moiety in promoting enzyme-mediated DNA cleavage. Biochemistry 50:3240-3249
50. Goel A, Kunnumakkara AB, Aggarwal BB (2008) Curcumin as "curecumin": from kitchen to clinic. Biochem Pharmacol 75:787-809
51. Greaves MF (1997) Aetiology of acute leukaemia. Lancet 349:344-349
52. Griesser M, Pistis V, Suzuki T, Tejera N, Pratt DA, Schneider C (2011) Autoxidative and cyclooxygenase-2 catalyzed transformation of the dietary chemopreventive agent curcumin. J Biol Chem 286:1114-1124
53. Gupta SC, Sung B, Kim JH, Prasad S, Li S, Aggarwal BB (2012) Multitargeting by turmeric, the golden spice: from kitchen to clinic. Mol Nutr Food Res. doi: 10.1002/mnfr.201100741
54. Hagiwara M, Inoue S, Tanaka T, Nunoki K, Ito M, Hidaka H (1988) Differential effects of flavonoids as inhibitors of tyrosine protein kinases and serine/threonine protein kinases. Biochem Pharmacol 37:2987-2992
55. Haince JF, Rouleau M, Poirier GG (2006) Transcription. Gene expression needs a break to unwind before carrying on. Science 312:1752-1753 (Pubitemid 43962879)
56. Hande KR (1998a) Clinical applications of anticancer drugs targeted to topoisomerase II. Biochim Biophys Acta 1400: 173-184
57. Hande KR (1998b) Etoposide: four decades of development of a topoisomerase II inhibitor. Eur J Cancer 34:1514-1521
58. Hardin AH, Sarkar SK, Seol Y, Liou GF, Osheroff N, Neuman KC (2011) Direct measurement of DNA bending by type IIA topoisomerases: implications for non-equilibrium topology simplification. Nucleic Acids Res 39:5729-5743
59. Hatcher H, Planalp R, Cho J, Torti FM, Torti SV (2008) Curcumin: from ancient medicine to current clinical trials. Cell Mol Life Sci 65:1631-1652
60. Herr I, Buchler MW(2010) Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. Cancer Treat Rev 36:377-383
61. Hollosy F, Keri G (2004) Plant-derived protein tyrosine kinase inhibitors as anticancer agents. Curr Med Chem Anticancer Agents 4:173-197 (Pubitemid 38410597)
62. Ireson C, Orr S, Jones DJ, Verschoyle R, Lim CK, Luo JL, Howells L, Plummer S, Jukes R, Williams M, Steward WP, Gescher A (2001) Characterization of metabolites of the chemopreventive agent curcumin in human and rat hepatocytes and in the rat in vivo, and evaluation of their ability to inhibit phorbol ester-induced prostaglandin E2 production. Cancer Res 61:1058-1064 (Pubitemid 32174425)
63. Isaacs RJ, Davies SL, Sandri MI, Redwood C, Wells NJ, Hickson ID (1998) Physiological regulation of eukaryotic topoisomerase II. Biochim Biophys Acta 1400:121-137 (Pubitemid 28475099)
64. Isbrucker RA, Bausch J, Edwards JA, Wolz E (2006a) Safety studies on epigallocatechin gallate (EGCG) preparations. Part 1: genotoxicity. Food Chem Toxicol 44:626-635
65. Isbrucker RA, Edwards JA, Wolz E, Davidovich A, Bausch J (2006b) Safety studies on epigallocatechin gallate (EGCG) preparations. Part 2: dermal, acute and short-term toxicity studies. Food Chem Toxicol 44:636-650
66. Ishino N, Yanase E, Nakatsuka S (2010) Epimerization of tea catechins under weakly acidic and alkaline conditions. Biosci Biotechnol Biochem 74:875-877
67. Joannides M, Grimwade D (2010) Molecular biology of therapy-related leukaemias. Clin Transl Oncol 12:8-14
68. Joannides M, Mays AN, Mistry AR, Hasan SK, Reiter A, Wiemels JL, Felix CA, Coco FL, Osheroff N, Solomon E, Grimwade D (2011) Molecular pathogenesis of secondary acute promyelocytic leukemia. Mediterr J Hematol Infect Dis 3:e2011045
69. Ju BG, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW, Glass CK, Rosenfeld MG (2006) A topoisomerase IIb-mediated dsDNA break required for regulated transcription. Science 312:1798-1802 (Pubitemid 43962898)
70. Kandaswami C, Lee LT, Lee PP, Hwang JJ, Ke FC, Huang YT, Lee MT (2005) The antitumor activities of flavonoids. In Vivo 19:895-909
71. Kanwar J, Taskeen M, Mohammad I, Huo C, Chan TH, Dou QP (2012) Recent advances on tea polyphenols. Front Biosci (Elite Ed) 4:111-131
72. Kaufmann SH (1998) Cell death induced by topoisomerasetargeted drugs: more questions than answers. Biochim Biophys Acta 1400:195-211
73. Ketron AC, Osheroff N (2013) DNA Topology and topoisomerases. Encycl Mol Life Sci (in press)
74. Ketron AC, Gordon ON, Schneider C, Osheroff N (2013) Oxidative metabolites of curcumin poison human type II topoisomerases. Biochemistry 52:221-227
75. Kingma PS, Burden DA, Osheroff N (1999) Binding of etoposide to topoisomerase II in the absence of DNA: decreased affinity as a mechanism of drug resistance. Biochemistry 38:3457-3461 (Pubitemid 29149463)
76. Kitamura R, Bandoh T, Tsuda M, Satoh T (1997) Determination of a new podophyllotoxin derivative, TOP-53, and its metabolite in rat plasma and urine by high-performance liquid chromatography with electrochemical detection. J Chromatogr B Biomed Sci Appl 7:283-288 (Pubitemid 27136480)
77. 13C NMR and X-ray studies of genistein complexes with amines. Potential biological function of the C-7, C-5, and C4′-OH groups. Org Biomol Chem 1:3578-3585
78. Kruczynski A, Vandenberghe I, Pillon A, Pesnel S, Goetsch L, Barret JM, Guminski Y, Le Pape A, Imbert T, Bailly C, Guilbaud N (2009) Preclinical activity of F14512, designed to target tumors expressing an active polyamine transport system. Invest New Drugs 29:9-21
79. Kurzer MS, Xu X (1997) Dietary phytoestrogens. Annu Rev Nutr 17:353-381 (Pubitemid 27328805)
80. Lamartiniere CA (2000) Protection against breast cancer with genistein: a component of soy. Am J Clin Nutr 71:1705S-1707S
81. 2+-mediated dynamic bending of gate-DNA. Proc Natl Acad Sci USA 109:2925-2930
82. Leppard JB, Champoux JJ (2005) Human DNA topoisomerase I: relaxation, roles, and damage control. Chromosoma 114:75-85 (Pubitemid 41030970)
83. Lin RK, Zhou N, Lyu YL, Tsai YC, Lu CH, Kerrigan J, Chen YT, Guan Z, Hsieh TS, Liu LF (2011) Dietary isothiocy-anate-induced apoptosis via thiol modification of DNA topoisomerase IIa. J Biol Chem 286:33591-33600
84. Lindsey RH Jr, Bromberg KD, Felix CA, Osheroff N (2004) 1,4-Benzoquinone is a topoisomerase II poison. Biochemistry 43:7563-7574 (Pubitemid 38745772)
85. Linka RM, Porter AC, Volkov A, Mielke C, Boege F, Christensen MO (2007) C-terminal regions of topoisomerase IIα and IIβ determine isoform-specific functioning of the enzymes in vivo. Nucleic Acids Res 35:3810-3822 (Pubitemid 47244673)
86. Liu Z, Deibler RW, Chan HS, Zechiedrich L (2009) The why and how of DNA unlinking. Nucleic Acids Res 37:661-671
87. Loike JD, Horwitz SB (1976) Effects of podophyllotoxin and VP-16-213 on microtubule assembly in vitro and nucleoside transport in HeLa cells. Biochemistry 15:5435-5443 (Pubitemid 8004251)
88. Lopez-Lazaro M, Willmore E, Austin CA (2007a) Cells lacking DNA topoisomerase IIβ are resistant to genistein. J Nat Prod 70:763-767 (Pubitemid 46953596)
89. Lopez-Lazaro M, Willmore E, Jobson A, Gilroy KL, Curtis H, Padget K, Austin CA (2007b) Curcumin induces high levels of topoisomerase I- and II-DNA complexes in K562 leukemia cells. J Nat Prod 70:1884-1888
90. Lopez-Lazaro M, Willmore E, Austin CA (2010) The dietary flavonoids myricetin and fisetin act as dual inhibitors of DNA topoisomerases I and II in cells. Mutat Res 696:41-47
91. Lovett BD, Lo Nigro L, Rappaport EF, Blair IA, Osheroff N, Zheng N, Megonigal MD, Williams WR, Nowell PC, Felix CA (2001a) Near-precise interchromosomal recombination and functional DNA topoisomerase II cleavage sites at MLL and AF-4 genomic breakpoints in treatment-related acute lymphoblastic leukemia with t(4;11) translocation. Proc Natl Acad Sci USA 98:9802-9807 (Pubitemid 32769384)
92. Lovett BD, Strumberg D, Blair IA, Pang S, Burden DA, Megonigal MD, Rappaport EF, Rebbeck TR, Osheroff N, Pommier YG, Felix CA (2001b) Etoposide metabolites enhance DNA topoisomerase II cleavage near leukemia-associated MLL translocation breakpoints. Biochemistry 40:1159-1170 (Pubitemid 32142877)
93. Mahady GB, Pendland SL, Yun G, Lu ZZ (2002) Turmeric (Curcuma longa) and curcumin inhibit the growth of Helicobacter pylori, a group 1 carcinogen. Anticancer Res 22:4179-4181 (Pubitemid 36134453)
94. Markovits J, Junqua S, Goldwasser F, Venuat AM, Luccioni C, Beaumatin J, Saucier JM, Bernheim A, Jacquemin-Sablon A (1995) Genistein resistance in human leukaemic CCRFCEM cells: selection of a diploid cell line with reduced DNA topoisomerase IIβ isoform. Biochem Pharmacol 50:177-186
95. McClendon AK, Osheroff N (2007) DNA topoisomerase II, genotoxicity, and cancer. Mutat Res 623:83-97 (Pubitemid 47368578)
96. Nitiss JL (2009a) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 9:327-337
97. Nitiss JL (2009b) Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 9:338-350
98. Osheroff N (1989) Effect of antineoplastic agents on the DNA cleavage/religation reaction of eukaryotic topoisomerase II: inhibition of DNA religation by etoposide. Biochemistry 28:6157-6160
99. Patel VB, Misra S, Patel BB, Majumdar AP (2010) Colorectal cancer: chemopreventive role of curcumin and resveratrol. Nutr Cancer 62:958-967
100. Pfeiffer E, Heoehle SI, Solyom AM, Metzler M (2003) Studies on the stability of turmeric constituents. J Food Eng 56:257-259 (Pubitemid 35384659)
101. Pitts SL, Jablonksy MJ, Duca M, Dauzonne D, Monneret C, Arimondo PB, Anklin C, Graves DE, Osheroff N (2011) Contributions of the D-ring to the activity of etoposide against human topoisomerase IIα: potential interactions with DNA in the ternary enzyme-drug-DNA complex. Biochemistry 50:5058-5066
102. Pommier Y (2009) DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem Rev 109:2894-2902
103. Pommier Y (2013) Drugging topoisomerases: lessons and challenges. ACS Chem Biol 8:82-95
104. Pommier Y, Marchand C (2005) Interfacial inhibitors of protein-nucleic acid interactions. Curr Med Chem Anti-Cancer Agents 5:421-429 (Pubitemid 40974814)
105. Pommier Y, Leo E, Zhang H, Marchand C (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 17:421-433
106. Ren W, Qiao Z, Wang H, Zhu L, Zhang L (2003) Flavonoids: promising anticancer agents. Med Res Rev 23:519-534 (Pubitemid 36706514)
107. Robinson BW, Cheung NK, Kolaris CP, Jhanwar SC, Choi JK, Osheroff N, Felix CA (2008) Prospective tracing of MLLFRYL clone with low MEIS1 expression from emergence during neuroblastoma treatment to diagnosis of myelodysplastic syndrome. Blood 111:3802-3812
108. Ross W, Rowe T, Glisson B, Yalowich J, Liu L (1984) Role of topoisomerase II in mediating epipodophyllotoxin-induced DNA cleavage. Cancer Res 44:5857-5860 (Pubitemid 15183602)
109. Ross JA, Potter JD, Robison LL (1994) Infant leukemia, topoisomerase II inhibitors, and the MLL gene. J Natl Cancer Inst 86:1678-1680
110. Sang S, Hou Z, Lambert JD, Yang CS (2005a) Redox properties of tea polyphenols and related biological activities. Antioxid Redox Signal 7:1704-1714 (Pubitemid 41768003)
111. Sang S, Lee MJ, Hou Z, Ho CT, Yang CS (2005b) Stability of tea polyphenol (-)-epigallocatechin-3-gallate and formation of dimers and epimers under common experimental conditions. J Agric Food Chem 53:9478-9484 (Pubitemid 41784153)
112. Sarkar FH, Li Y (2004) The role of isoflavones in cancer chemoprevention. Front Biosci 9:2714-2724
113. Sarkar FH, Adsule S, Padhye S, Kulkarni S, Li Y (2006) The role of genistein and synthetic derivatives of isoflavone in cancer prevention and therapy. Mini Rev Med Chem 6:401-407
114. Satoskar RR, Shah SJ, Shenoy SG (1986) Evaluation of anti-inflammatory property of curcumin (diferuloyl methane) in patients with postoperative inflammation. Int J Clin Pharmacol Ther Toxicol 24:651-654 (Pubitemid 17205963)
115. Scalbert A, Williamson G (2000) Dietary intake and bioavailability of polyphenols. J Nutr 130:2073S-2085S (Pubitemid 30619386)
116. Schmidt BH, Burgin AB, Deweese JE, Osheroff N, Berger JM (2010) A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 465:641-644
117. Sharma RA, McLelland HR, Hill KA, Ireson CR, Euden SA, Manson MM, Pirmohamed M, Marnett LJ, Gescher AJ, Steward WP (2001) Pharmacodynamic and pharmacokinetic study of oral Curcuma extract in patients with colorectal cancer. Clin Cancer Res 7:1894-1900 (Pubitemid 32994823)
118. Shen L, Ji HF (2009) Contribution of degradation products to the anticancer activity of curcumin. Clin Cancer Res 15:7108
119. Shen L, Ji HF (2012) The pharmacology of curcumin: is it the degradation products? Trends Mol Med 18:138-144
120. Siddiqui IA, Adhami VM, Saleem M, Mukhtar H (2006) Beneficial effects of tea and its polyphenols against prostate cancer. Mol Nutr Food Res 50:130-143 (Pubitemid 43325654)
121. Singh AV, Xiao D, Lew KL, Dhir R, Singh SV (2004) Sulforaphane induces caspase-mediated apoptosis in cultured PC-3 human prostate cancer cells and retards growth of PC-3 xenografts in vivo. Carcinogenesis 25:83-90 (Pubitemid 38128621)
122. Sissi C, PalumboM(2010) In front of and behind the replication fork: bacterial type IIA topoisomerases. Cell Mol Life Sci 67:2001-2024
123. Spector LG, Xie Y, Robison LL, Heerema NA, Hilden JM, Lange B, Felix CA, Davies SM, Slavin J, Potter JD, Blair CK, Reaman GH, Ross JA (2005) Maternal diet and infant leukemia: the DNA topoisomerase II inhibitor hypothesis: a report from the children's oncology group. Cancer Epidemiol Biomarkers Prev 14:651-655 (Pubitemid 40489210)
124. Stahelin HF, von Wartburg A (1991) The chemical and biological route from podophyllotoxin glucoside to etoposide: ninth Cain memorial Award lecture. Cancer Res 51:5-15
125. Stan SD, Kar S, Stoner GD, Singh SV (2008) Bioactive food components and cancer risk reduction. J Cell Biochem 104:339-356
126. Strick R, Strissel PL, Borgers S, Smith SL, Rowley JD (2000) Dietary bioflavonoids induce cleavage in the MLL gene and may contribute to infant leukemia. Proc Natl Acad Sci USA 97:4790-4795
127. Timmel MA, Byl JA, Osheroff N (2013) Epimerization of green tea catechins during brewing does not affect the ability to poison human type II topoisomerases. Chem Res Toxicol (in press)
128. Tonnesen HH, Karlsen J (1985) Studies on curcumin and curcuminoids. VI. Kinetics of curcumin degradation in aqueous solution. Z Lebensm Unters Forsch 180:402-404
129. Valcic S, Muders A, Jacobsen NE, Liebler DC, Timmermann BN (1999) Antioxidant chemistry of green tea catechins. Identification of products of the reaction of (-)-epigallocatechin gallate with peroxyl radicals. Chem Res Toxicol 12:382-386 (Pubitemid 29193915)
130. Valcic S, Burr JA, Timmermann BN, Liebler DC (2000) Antioxidant chemistry of green tea catechins. New oxidation products of (-)-epigallocatechin gallate and (-)-epigallocatechin from their reactions with peroxyl radicals. Chem Res Toxicol 13:801-810
131. Von Low EC, Perabo FG, Siener R, Muller SC (2007) Facts and fiction of phytotherapy for prostate cancer: a critical assessment of preclinical and clinical data. In Vivo 21:189-204 (Pubitemid 46534271)
132. Vos SM, Tretter EM, Schmidt BH, Berger JM (2011) All tangled up: how cells direct, manage and exploit topoisomerase function. Nat Rev Mol Cell Biol 12:827-841
133. Wang JC (1991) DNA topoisomerases: why so many? J Biol Chem 266:6659-6662
134. Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430-440
135. Wang YJ, Pan MH, Cheng AL, Lin LI, Ho YS, Hsieh CY, Lin JK (1997) Stability of curcumin in buffer solutions and characterization of its degradation products. J Pharm Biomed Anal 15:1867-1876
136. Wang H, Mao Y, Chen AY, Zhou N, LaVoie EJ, Liu LF (2001) Stimulation of topoisomerase II-mediated DNA damage via a mechanism involving protein thiolation. Biochemistry 40:3316-3323 (Pubitemid 32221633)
137. Warin R, Chambers WH, Potter DM, Singh SV (2009) Prevention of mammary carcinogenesis in MMTV-neu mice by cruciferous vegetable constituent benzyl isothiocyanate. Cancer Res 69:9473-9480
138. Whitmarsh RJ, Saginario C, Zhuo Y, Hilgenfeld E, Rappaport EF, Megonigal MD, Carroll M, Liu M, Osheroff N, Cheung NK, Slater DJ, Ried T, Knutsen T, Blair IA, Felix CA (2003) Reciprocal DNA topoisomerase II cleavage events at 5′-TATTA-3′ sequences in MLL and AF-9 create homologous single-stranded overhangs that anneal to form der(11) and der(9) genomic breakpoint junctions in treatment-related AML without further processing. Oncogene 22:8448-8459 (Pubitemid 37523897)
139. Williams RJ, Spencer JP, Rice-Evans C (2004) Flavonoids: antioxidants or signalling molecules? Free Radic Biol Med 36:838-849 (Pubitemid 38352901)
140. Wilstermann AM, Bender RP, Godfrey M, Choi S, Anklin C, Berkowitz DB, Osheroff N, Graves DE (2007) Topoisomerase II-drug interaction domains: identification of substituents on etoposide that interact with the enzyme. Biochemistry 46:8217-8225 (Pubitemid 47075961)
141. Wu CC, Li TK, Farh L, Lin LY, Lin TS, Yu YJ, Yen TJ, Chiang CW, Chan NL (2011) Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide. Science 333:459-462
142. Yang L, Rowe TC, Liu LF (1985) Identification of DNA topoisomerase II as an intracellular target of antitumor epipodophyllotoxins in Simian Virus 40-infected monkey cells. Cancer Res 45:5872-5876 (Pubitemid 16218602)
143. Yang X, Li W, Prescott ED, Burden SJ, Wang JC (2000) DNA topoisomerase IIβ and neural development. Science 287:131-134
144. Yang EB, Guo YJ, Zhang K, Chen YZ, Mack P (2001) Inhibition of epidermal growth factor receptor tyrosine kinase by chalcone derivatives. Biochim Biophys Acta 1550:144-152 (Pubitemid 34038000)
145. Yang CS, Lambert JD, Ju J, Lu G, Sang S (2007) Tea and cancer prevention: molecular mechanisms and human relevance. Toxicol Appl Pharmacol 224:265-273 (Pubitemid 47592860)
146. Yao LH, Jiang YM, Shi J, Tomas-Barberan FA, Datta N, Singanusong R, Chen SS (2004) Flavonoids in food and their health benefits. Plant Foods Hum Nutr 59:113-122 (Pubitemid 40172010)