The lignan, (-)-sesamin reveals cytotoxicity toward cancer cells: Pharmacogenomic determination of genes associated with sensitivity or resistance

Phytomedicine

Volumn 21, Issue 5, 2014, Pages 689-696

  Saeed, Mohamed ^a   Khalid, Hassan ^b   Sugimoto, Yoshikazu ^c   Efferth, Thomas ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b National Center for Research Sudan   (Sudan)

^c KEIO UNIVERSITY   (Japan)

Author keywords

ABC transporters; ABCB1; ABCB5; Chemotherapy; Lignan, ( ) sesamin; Multidrug resistance; Pharmacogenomics; Phytotherapy

Indexed keywords

ABC TRANSPORTER B5; MESSENGER RNA; MITOCHONDRIAL PROTEIN; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; RIBOSOME PROTEIN; SESAMIN; 1,3 DIOXOLANE DERIVATIVE; ABCB1 PROTEIN, HUMAN; ABCB5 PROTEIN, HUMAN; LIGNAN; PLANT EXTRACT;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL STRAIN HEK293; CYTOTOXICITY; DRUG SENSITIVITY; FATTY ACID METABOLISM; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IC 50; MULTIDRUG RESISTANCE; PHARMACOGENOMICS; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA METABOLISM; CLUSTER ANALYSIS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETICS; HEK293 CELL LINE; NEOPLASMS; PHYTOTHERAPY; TUMOR CELL LINE;

CELL LINE, TUMOR; CLUSTER ANALYSIS; DIOXOLES; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; GENE EXPRESSION PROFILING; HEK293 CELLS; HUMANS; LIGNANS; NEOPLASMS; P-GLYCOPROTEIN; P-GLYCOPROTEINS; PHYTOTHERAPY; PLANT EXTRACTS;

EID: 84898059591     PISSN: 09447113     EISSN: 1618095X     Source Type: Journal    
DOI: 10.1016/j.phymed.2014.01.006     Document Type: Article

References (71)

1. M.C. Alley, D.A. Scudiero, A. Monks, M.L. Hursey, M.J. Czerwinski, D.L. Fine, B.J. Abbott, J.G. Mayo, R.H. Shoemaker, and M.R. Boyd Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay Cancer Res. 48 1988 589 601
2. J. Bertram, K. Palfner, W. Hiddemann, and M. Kneba Overexpression of ribosomal proteins L4 and L5 and the putative alternative elongation factor PTI-1 in the doxorubicin resistant human colon cancer cell line LoVoDxR Eur. J. Cancer 34 1998 731 736
3. T.J. Buckley, J.M. Waldman, R. Dhara, A. Greenberg, Z. Ouyang, and P.J. Lioy An assessment of a urinary biomarker for total human environmental exposure to benzo[a]pyrene Int. Arch. Occup. Environ. Health 67 1995 257 266
4. E.B. Butler, Y. Zhao, C. Munoz-Pinedo, J. Lu, and M. Tan Stalling the engine of resistance: targeting cancer metabolism to overcome therapeutic resistance Cancer Res. 73 2013 2709 2717
5. X.L. Cao, J. Xu, G. Bai, H. Zhang, Y. Liu, J.F. Xiang, and Y.L. Tang Isolation of anti-tumor compounds from the stem bark of Zanthoxylum ailanthoides Sieb. & Zucc. by silica gel column and counter-current chromatography J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 929 2013 6 10
6. K.G. Chen, J.C. Valencia, J.P. Gillet, V.J. Hearing, and M.M. Gottesman Involvement of ABC transporters in melanogenesis and the development of multidrug resistance of melanoma Pigment Cell Melanoma Res. 22 2009 740 749
7. S.T. Cheung, P.F. Cheung, C.K. Cheng, N.C. Wong, and S.T. Fan Granulin-epithelin precursor and ATP-dependent binding cassette (ABC)B5 regulate liver cancer cell chemoresistance Gastroenterology 140 2011 344 355
8. S. Childs, and V. Ling The MDR superfamily of genes and its biological implications Important Adv. Oncol. 1994 21 36
9. C. Cordon-Cardo, J.P. O'Brien, J. Boccia, D. Casals, J.R. Bertino, and M.R. Melamed Expression of the multidrug resistance gene product (P-glycoprotein) in human normal and tumor tissues J. Histochem. Cytochem. 38 1990 1277 1287
10. E. Dassa, and P. Bouige The ABC of ABCS: a phylogenetic and functional classification of ABC systems in living organisms Res. Microbiol. 152 2001 211 229
11. P. Deng, C. Wang, L. Chen, C. Wang, Y. Du, X. Yan, M. Chen, G. Yang, and G. He Sesamin induces cell cycle arrest and apoptosis through the inhibition of signal transducer and activator of transcription 3 signalling in human hepatocellular carcinoma cell line HepG2 Biol. Pharm. Bull. 36 2013 1540 1548
12. J. Du, Y. Shi, Y. Pan, X. Jin, C. Liu, N. Liu, Q. Han, Y. Lu, T. Qiao, and D. Fan Regulation of multidrug resistance by ribosomal protein l6 in gastric cancer cells Cancer Biol. Ther. 4 2005 242 247
13. T. Efferth The human ATP-binding cassette transporter genes: from the bench to the bedside Curr. Mol. Med. 1 2001 45 65
14. T. Efferth Personalized cancer medicine: from molecular diagnostics to targeted therapy with natural products Planta Med. 76 2010 1143 1154
15. T. Efferth Stem cells, cancer stem-like cells, and natural products Planta Med. 78 2012 935 942
16. T. Efferth, and E. Koch Complex interactions between phytochemicals. The multi-target therapeutic concept of phytotherapy Curr. Drug Targets 12 2011 122 132
17. T. Efferth, V.B. Konkimalla, Y.F. Wang, A. Sauerbrey, S. Meinhardt, F. Zintl, J. Mattern, and M. Volm Prediction of broad spectrum resistance of tumors towards anticancer drugs Clin. Cancer Res. 14 2008 2405 2412
18. T. Efferth, and R. Osieka Clinical relevance of the MDR-a gene and it's gene product, P-glycoprotein, for cancer chemotherapy Tumor Diagn. Ther. 14 1993 238 243
19. T. Efferth, A. Sauerbrey, A. Olbrich, E. Gebhart, P. Rauch, H.O. Weber, J.G. Hengstler, M.E. Halatsch, M. Volm, K.D. Tew, D.D. Ross, and J.O. Funk Molecular modes of action of artesunate in tumor cell lines Mol. Pharmacol. 64 2003 382 394
20. A. Evans, V. Bates, H. Troy, S. Hewitt, S. Holbeck, Y.L. Chung, R. Phillips, M. Stubbs, J. Griffiths, and R. Airley Glut-1 as a therapeutic target: increased chemoresistance and HIF-1-independent link with cell turnover is revealed through COMPARE analysis and metabolomic studies Cancer Chemother. Pharmacol. 61 2008 377 393
21. V. Fagan, S. Bonham, M.P. Carty, P. Saenz-Mendez, L.A. Eriksson, and F. Aldabbagh COMPARE analysis of the toxicity of an iminoquinone derivative of the imidazo[5,4-f]benzimidazoles with NAD(P)H:quinone oxidoreductase 1 (NQO1) activity and computational docking of quinones as NQO1 substrates Bioorg. Med. Chem. 20 2012 3223 3232
22. J.M. Ford, J.M. Yang, and W.N. Hait P-glycoprotein-mediated multidrug resistance: experimental and clinical strategies for its reversal Cancer Treat. Res. 87 1996 3 38
23. N.Y. Frank, A. Margaryan, Y. Huang, T. Schatton, A.M. Waaga-Gasser, M. Gasser, M.H. Sayegh, W. Sadee, and M.H. Frank ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma Cancer Res. 65 2005 4320 4333
24. F.R. Garcez, W.S. Garcez, M. Martins, M.F. Matos, Z.R. Guterres, M.S. Mantovani, C.K. Misu, and S.T. Nakashita Cytotoxic and genotoxic butanolides and lignans from Aiouea trinervis Planta Med. 71 2005 923 927
25. P. Gazzaniga, E. Cigna, V. Panasiti, V. Devirgiliis, U. Bottoni, B. Vincenzi, C. Nicolazzo, A. Petracca, and A. Gradilone CD133 and ABCB5 as stem cell markers on sentinel lymph node from melanoma patients Eur. J. Surg. Oncol. 36 2010 1211 1214
26. J.P. Gillet, T. Efferth, and J. Remacle Chemotherapy-induced resistance by ATP-binding cassette transporter genes Biochim. Biophys. Acta 1775 2007 237 262
27. J.P. Gillet, T. Efferth, D. Steinbach, J. Hamels, F. de Longueville, V. Bertholet, and J. Remacle Microarray-based detection of multidrug resistance in human tumor cells by expression profiling of ATP-binding cassette transporter genes Cancer Res. 64 2004 8987 8993
28. M.M. Gottesman, T. Fojo, and S.E. Bates Multidrug resistance in cancer: role of ATP-dependent transporters Nat. Rev. Cancer 2 2002 48 58
29. M. Grimm, M. Krimmel, J. Polligkeit, D. Alexander, A. Munz, S. Kluba, C. Keutel, J. Hoffmann, S. Reinert, and S. Hoefert ABCB5 expression and cancer stem cell hypothesis in oral squamous cell carcinoma Eur. J. Cancer 48 2012 3186 3197
30. H. Hibasami, T. Fujikawa, H. Takeda, S. Nishibe, T. Satoh, T. Fujisawa, and K. Nakashima Induction of apoptosis by Acanthopanax senticosus HARMS and its component, sesamin in human stomach cancer KATO III cells Oncol. Rep. 7 2000 1213 1216
31. N. Hirose, F. Doi, T. Ueki, K. Akazawa, K. Chijiiwa, M. Sugano, K. Akimoto, S. Shimizu, and H. Yamada Suppressive effect of sesamin against 7,12-dimethylbenz[a]-anthracene induced rat mammary carcinogenesis Anticancer Res. 12 1992 1259 1265
32. Z.B. Hu, M.D. Minden, E.A. McCulloch, and J. Stahl Regulation of drug sensitivity by ribosomal protein S3a Blood 95 2000 1047 1055
33. M. Jang, S.S. Kim, and J. Lee Cancer cell metabolism: implications for therapeutic targets Exp. Mol. Med. 45 2013 e45
34. L. Jia, P.D. Allen, M.G. Macey, M.F. Grahn, A.C. Newland, and S.M. Kelsey Mitochondrial electron transport chain activity, but not ATP synthesis, is required for drug-induced apoptosis in human leukaemic cells: a possible novel mechanism of regulating drug resistance Br. J. Haematol. 98 1997 686 698
35. A. Johnsson, I. Zeelenberg, Y. Min, J. Hilinski, C. Berry, S.B. Howell, and G. Los Identification of genes differentially expressed in association with acquired cisplatin resistance Br. J. Cancer 83 2000 1047 1054
36. A. Kamal-Eldin, A. Moazzami, and S. Washi Sesame seed lignans: potent physiological modulators and possible ingredients in functional foods & nutraceuticals Recent Pat. Food Nutr. Agric. 3 2011 17 29
37. A. Kamal-Eldin, G. Yousif, and L.A. Appelqvist Thin-layer chromatographic separations of seed oil unsaponifiables from four sesamum species JAOCS 68 11 1991 844 847
38. T. Kawanobe, S. Kogure, S. Nakamura, M. Sato, K. Katayama, J. Mitsuhashi, K. Noguchi, and Y. Sugimoto Expression of human ABCB5 confers resistance to taxanes and anthracyclines Biochem. Biophys. Res. Commun. 418 2012 736 741
39. A. Kimmig, V. Gekeler, M. Neumann, G. Frese, R. Handgretinger, G. Kardos, H. Diddens, and D. Niethammer Susceptibility of multidrug-resistant human leukemia cell lines to human interleukin 2-activated killer cells Cancer Res. 50 1990 6793 6799
40. D.G. Kingston, M.M. Rao, and W.V. Zucker Plant anticancer agents. IX. Constituents of Hyptis tomentosa J. Nat. Prod. 42 1979 496 499
41. S. Kozaki, Y. Takenaka, Y. Mizushina, T. Yamaura, and T. Tanahashi Three acetophenones from Acronychia pedunculata J. Nat. Med. 2013 2013 [epub ahead of print]
42. V. Kuete, B. Wiench, M.E. Hegazy, T.A. Mohamed, A.G. Fankam, A.A. Shahat, and T. Efferth Antibacterial activity and cytotoxicity of selected Egyptian medicinal plants Planta Med. 78 2012 193 199
43. J.S. Lee, J. Kim, Y.U. Yu, and Y.C. Kim Inhibition of phospholipase Cgamma1 and cancer cell proliferation by lignans and flavans from Machilus thunbergii Arch. Pharm. Res. 27 2004 1043 1047
44. Z. Liu, N.M. Saarinen, and L.U. Thompson Sesamin is one of the major precursors of mammalian lignans in sesame seed (Sesamum indicum) as observed in vitro and in rats J. Nutr. 136 2006 906 912
45. Y. Luo, L.Z. Ellis, K. Dallaglio, M. Takeda, W.A. Robinson, S.E. Robinson, W. Liu, K.D. Lewis, M.D. McCarter, R. Gonzalez, D.A. Norris, D.R. Roop, R.A. Spritz, N.G. Ahn, and M. Fujita Side population cells from human melanoma tumors reveal diverse mechanisms for chemoresistance J. Invest. Dermatol. 132 2012 2440 2450
46. E.L. Luzina, and A.V. Popov Synthesis, evaluation of anticancer activity and COMPARE analysis of N-bis(trifluoromethyl)alkyl-N′-substituted ureas with pharmacophoric moieties Eur. J. Med. Chem. 53 2012 364 373
47. V. Kuete, and T. Efferth Molecular determinants of cancer cell sensitivity and resistance towards the sesquiterpene farnesol Pharmazie 68 2013 608 615
48. Y. Miyahara, T. Komiya, H. Katsuzaki, K. Imai, M. Nakagawa, Y. Ishi, and H. Hibasami Sesamin and episesamin induce apoptosis in human lymphoid leukemia Molt 4B cells Int. J. Mol. Med. 6 2000 43 46
49. T. Nabekura, T. Yamaki, K. Ueno, and S. Kitagawa Inhibition of P-glycoprotein and multidrug resistance protein 1 by dietary phytochemicals Cancer Chemother. Pharmacol. 62 2008 867 873
50. J. O'Brien, I. Wilson, T. Orton, and F. Pognan Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity Eur. J. Biochem. 267 2000 5421 5426
51. C.R. Oliva, S.E. Nozell, A. Diers, S.G. McClugage 3rd, J.N. Sarkaria, J.M. Markert, V.M. Darley-Usmar, S.M. Bailey, G.Y. Gillespie, A. Landar, and C.E. Griguer Acquisition of temozolomide chemoresistance in gliomas leads to remodeling of mitochondrial electron transport chain J. Biol. Chem. 285 2010 39759 39767
52. K.D. Paull, R.H. Shoemaker, L. Hodes, A. Monks, D.A. Scudiero, L. Rubinstein, J. Plowman, and M.R. Boyd Display and analysis of patterns of differential activity of drugs against human tumor cell lines: development of mean graph and COMPARE algorithm J. Natl. Cancer Inst. 81 1989 1088 1092
53. J.L. Penalvo, S.M. Heinonen, A.M. Aura, and H. Adlercreutz Dietary sesamin is converted to enterolactone in humans J. Nutr. 135 2005 1056 1062
54. N. Rangkaew, R. Suttisri, M. Moriyasu, and K. Kawanishi A new acyclic diterpene acid and bioactive compounds from Knema glauca Arch. Pharm. Res. 32 2009 685 692
55. A. Roesch, A. Vultur, I. Bogeski, H. Wang, K.M. Zimmermann, D. Speicher, C. Korbel, M.W. Laschke, P.A. Gimotty, S.E. Philipp, E. Krause, S. Patzold, J. Villanueva, C. Krepler, M. Fukunaga-Kalabis, M. Hoth, B.C. Bastian, T. Vogt, and M. Herlyn Overcoming intrinsic multidrug resistance in melanoma by blocking the mitochondrial respiratory chain of slow-cycling JARID1B(high) cells Cancer Cell 23 2013 811 825
56. L.V. Rubinstein, R.H. Shoemaker, K.D. Paull, R.M. Simon, S. Tosini, P. Skehan, D.A. Scudiero, A. Monks, and M.R. Boyd Comparison of in vitro anticancer-drug-screening data generated with a tetrazolium assay versus a protein assay against a diverse panel of human tumor cell lines J. Natl. Cancer Inst. 82 1990 1113 1118
57. L.A. Sanchez, D. Olmedo, J.L. Lopez-Perez, T.D. Williams, and M.P. Gupta Two new alkylresorcinols from Homalomena wendlandii and their cytotoxic activity Nat. Prod. Commun. 7 2012 1043 1046
58. A.H. Schinkel, and J.W. Jonker Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview Adv. Drug Deliv. Rev. 55 2003 3 29
59. Y. Shi, H. Zhai, X. Wang, Z. Han, C. Liu, M. Lan, J. Du, C. Guo, Y. Zhang, K. Wu, and D. Fan Ribosomal proteins S13 and L23 promote multidrug resistance in gastric cancer cells by suppressing drug-induced apoptosis Exp. Cell Res. 296 2004 337 346
60. S. Trifunovic, V. Vajs, Z. Juranic, Z. Zizak, V. Tesevic, S. Macura, and S. Milosavljevic Cytotoxic constituents of Achillea clavennae from Montenegro Phytochemistry 67 2006 887 893
61. J.S. Truan, J.M. Chen, and L.U. Thompson Comparative effects of sesame seed lignan and flaxseed lignan in reducing the growth of human breast tumors (MCF-7) at high levels of circulating estrogen in athymic mice Nutr. Cancer 64 2012 65 71
62. M. Volm, R. Koomägi, and T. Efferth Prediction of drug sensitivity and resistance of cancer by protein expression profiling Cancer Genomics Proteomics 1 2004 157 166
63. Z. Walther, and J. Sklar Molecular tumor profiling for prediction of response to anticancer therapies Cancer J. 17 2011 71 79
64. H.M. Wang, K.C. Cheng, C.J. Lin, S.W. Hsu, W.C. Fang, T.F. Hsu, C.C. Chiu, H.W. Chang, C.H. Hsu, and A.Y. Lee Obtusilactone A and (-)-sesamin induce apoptosis in human lung cancer cells by inhibiting mitochondrial Lon protease and activating DNA damage checkpoints Cancer Sci. 101 2010 2612 2620
65. B.J. Wilson, T. Schatton, Q. Zhan, M. Gasser, J. Ma, K.R. Saab, R. Schanche, A.M. Waaga-Gasser, J.S. Gold, Q. Huang, G.F. Murphy, M.H. Frank, and N.Y. Frank ABCB5 identifies a therapy-refractory tumor cell population in colorectal cancer patients Cancer Res. 71 2011 5307 5316
66. I.G. Wool Extraribosomal functions of ribosomal proteins Trends Biochem. Sci. 21 1996 164 165
67. I.G. Wool, Y.L. Chan, and A. Gluck Structure and evolution of mammalian ribosomal proteins Biochem. Cell Biol. 73 1995 933 947
68. K. Wosikowski, J.A. Silverman, P. Bishop, J. Mendelsohn, and S.E. Bates Reduced growth rate accompanied by aberrant epidermal growth factor signaling in drug resistant human breast cancer cells Biochim. Biophys. Acta 1497 2000 215 226
69. S. Xu, N. Li, M.M. Ning, C.H. Zhou, Q.R. Yang, and M.W. Wang Bioactive compounds from Peperomia pellucida J. Nat. Prod. 69 2006 247 250
70. M. Yang, W. Li, D. Fan, Y. Yan, X. Zhang, Y. Zhang, and D. Xiong Expression of ABCB5 gene in hematological malignances and its significance Leuk. Lymphoma 53 2012 1211 1215
71. T. Yokota, Y. Matsuzaki, M. Koyama, T. Hitomi, M. Kawanaka, M. Enoki-Konishi, Y. Okuyama, J. Takayasu, H. Nishino, A. Nishikawa, T. Osawa, and T. Sakai Sesamin, a lignan of sesame, down-regulates cyclin D1 protein expression in human tumor cells Cancer Sci. 98 2007 1447 1453