Shikonin directly targets mitochondria and causes mitochondrial dysfunction in cancer cells

Evidence-based Complementary and Alternative Medicine

Volumn 2012, Issue , 2012, Pages

  Wiench, Benjamin ^a   Eichhorn, Tolga ^a   Paulsen, Malte ^b   Efferth, Thomas ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Armenia)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SHIKONIN; TRANSCRIPTOME;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CANCER CELL; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CELL CYCLE; CELL CYCLE ARREST; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; CYTOTOXICITY; DEREGULATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FLOW CYTOMETRY; FLUORESCENCE; HUMAN; HUMAN CELL; METABOLISM; MICROTUBULE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL;

EID: 84868705448     PISSN: 1741427X     EISSN: 17414288     Source Type: Journal    
DOI: 10.1155/2012/726025     Document Type: Article

References (53)

1. Jemal A., Bray F., Center M. M., Ferlay J., Ward E., Forman D., Global cancer statistics. CA: Cancer Journal for Clinicians 2011 61 2 69 90 2-s2.0-79952232216 10.3322/caac.20107
2. Hanahan D., Weinberg R. A., Hallmarks of cancer: the next generation. Cell 2011 144 5 646 674 2-s2.0-79952284127 10.1016/j.cell.2011.02.013
3. Fulda S., Debatin K. M., Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006 25 34 4798 4811 2-s2.0-33746886979 10.1038/sj.onc.1209608 (Pubitemid 44187627)
4. Li P., Nijhawan D., Budihardjo I., Srinivasula S. M., Ahmad M., Alnemri E. S., Wang X., Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997 91 4 479 489 2-s2.0-0030715323 (Pubitemid 27508237)
5. Fulda S., Galluzzi L., Kroemer G., Targeting mitochondria for cancer therapy. Nature Reviews Drug Discovery 2010 9 6 447 464 2-s2.0-77953131908 10.1038/nrd3137
6. Brookes P. S., Yoon Y., Robotham J. L., Anders M. W., Sheu S. S., Calcium, ATP, and ROS: a mitochondrial love-hate triangle. American Journal of PhysiologyCell Physiology 2004 287 4 C817 C833 2-s2.0-4544235673 10.1152/ajpcell.00139.2004 (Pubitemid 39238305)
7. Modica-Napolitano J. S., Singh K. K., Mitochondrial dysfunction in cancer. Mitochondrion 2004 4 5-6 755 762 2-s2.0-10644291664 10.1016/j.mito.2004. 07.027 (Pubitemid 39646820)
8. Gogvadze V., Orrenius S., Zhivotovsky B., Mitochondria in cancer cells: what is so special about them? Trends in Cell Biology 2008 18 4 165 173 2-s2.0-41149105722 10.1016/j.tcb.2008.01.006
9. Chen G., Wang F., Trachootham D., Huang P., Preferential killing of cancer cells with mitochondrial dysfunction by natural compounds. Mitochondrion 2010 10 6 614 625 2-s2.0-78149360700 10.1016/j.mito.2010.08.001
10. Kroemer G., Pouyssegur J., Tumor cell metabolism: cancer's achilles' heel. Cancer Cell 2008 13 6 472 482 2-s2.0-44449147036 10.1016/j.ccr.2008.05.005 (Pubitemid 351766797)
11. Brandon M., Baldi P., Wallace D. C., Mitochondrial mutations in cancer. Oncogene 2006 25 34 4647 4662 2-s2.0-33746466098 10.1038/sj.onc.1209607 (Pubitemid 44187615)
12. Guizzunti G., Theodorakis E. A., Yu A. L., Zurzolo C., Batova A., Cluvenone induces apoptosis via a direct target in mitochondria: a possible mechanism to circumvent chemo-resistance? Investigational New Drugs 2012 30 5 1841 1848
13. Chen X., Yang L., Oppenheim J. J., Howard O. M. Z., Cellular pharmacology studies of shikonin derivatives. Phytotherapy Research 2002 16 3 199 209 2-s2.0-0035990608 10.1002/ptr.1100 (Pubitemid 34534943)
14. Sankawa U., Ebizuka Y., Miyazaki T., Isomura Y., Otsuka H., Antitumor activity of shikonin and its derivatives. Chemical and Pharmaceutical Bulletin 1977 25 9 2392 2395 2-s2.0-0017697921 (Pubitemid 8196664)
15. Guo X. P., Zhang X. Y., Zhang S. D., Clinical trial on the effects of shikonin mixture on later stage lung cancer. Zhong Xi Yi Jie He Za Zhi 1991 11 10 598 580 2-s2.0-0026235940
16. Chen J., Xie J., Jiang Z., Wang B., Wang Y., Hu X., Shikonin and its analogs inhibit cancer cell glycolysis by targeting tumor pyruvate kinase-M2. Oncogene 2011 30 4297 4306 2-s2.0-79954986587 10.1038/onc.2011.137
17. Efferth T., Sauerbrey A., Olbrich A., Gebhart E., Rauch P., Weber H. O., Hengstler J. G., Halatsch M. E., Volm M., Tew K. D., Ross D. D., Funk J. O., Molecular modes of action of artesunate in tumor cell lines. Molecular Pharmacology 2003 64 2 382 394 2-s2.0-0042844638 10.1124/mol.64.2.382 (Pubitemid 36910002)
18. Thoma C. R., Matov A., Gutbrodt K. L., Hoerner C. R., Smole Z., Krek W., Danuser G., Quantitative image analysis identifies pVHL as a key regulator of microtubule dynamic instability. Journal of Cell Biology 2010 190 6 991 1003 2-s2.0-77957198722 10.1083/jcb.201006059
19. O'Brien J., Wilson I., Orton T., Pognan F., Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. European Journal of Biochemistry 2000 267 17 5421 5426 2-s2.0-0033856957 10.1046/j.1432-1327.2000.01606.x
20. Eberwine J., Yeh H., Miyashiro K., Cao Y., Nair S., Finnell R., Zettel M., Coleman P., Analysis of gene expression in single live neurons. Proceedings of the National Academy of Sciences of the United States of America 1992 89 7 3010 3014 2-s2.0-0026588147
21. Wiench B., Eichhorn T., Korn B., Paulsen M., Efferth T., Utilizing inherent fluorescence of therapeutics to analyze real-time uptake and multi-parametric effector kinetics. Methods 2012 57 3 376 382
22. Bass D. A., Parce J. W., Dechatelet L. R., Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. Journal of Immunology 1983 130 4 1910 1917 2-s2.0-0020625894 (Pubitemid 13091657)
23. Cossarizza A., Ferraresi R., Troiano L., Roat E., Gibellini L., Bertoncelli L., Nasi M., Pinti M., Simultaneous analysis of reactive oxygen species and reduced glutathione content in living cells by polychromatic flow cytometry. Nature Protocols 2009 4 12 1790 1797 2-s2.0-74949112458 10.1038/nprot.2009.189
24. Kohn K. W., Erickson L. C., Ewig R. A. G., Friedman C. A., Fractionation of DNA from mammalian cells by alkaline elution. Biochemistry 1976 15 21 4629 4637 2-s2.0-0017186787
25. Epe B., Pflaum M., Boiteux S., DNA damage induced by photosensitizers in cellular and cell-free systems. Mutation Research 1993 299 3-4 135 145 2-s2.0-0027408280 (Pubitemid 23115153)
26. Paredes R. M., Etzler J. C., Watts L. T., Zheng W., Lechleiter J. D., Chemical calcium indicators. Methods 2008 46 3 143 151 2-s2.0-56249126393 10.1016/j.ymeth.2008.09.025
27. Liang C. C., Park A. Y., Guan J. L., In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nature Protocols 2007 2 2 329 333 2-s2.0-34347218991 10.1038/nprot.2007.30 (Pubitemid 47040047)
28. Gebäck T., Schulz M. M. P., Koumoutsakos P., Detmar M., TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. BioTechniques 2009 46 4 265 274 2-s2.0-67650504966 10.2144/000113083
29. Kowaltowski A. J., de Souza-Pinto N. C., Castilho R. F., Vercesi A. E., Mitochondria and reactive oxygen species. Free Radical Biology and Medicine 2009 47 4 333 343 2-s2.0-67649866121 10.1016/j.freeradbiomed.2009.05.004
30. Chang I. C., Huang Y. J., Chiang T. I., Yeh C. W., Hsu L. S., Shikonin induces apoptosis through reactive oxygen species/extracellular signal-regulated kinase pathway in osteosarcoma cells. Biological and Pharmaceutical Bulletin 2010 33 5 816 824 2-s2.0-77952397814 10.1248/bpb.33.816
31. Henry T. R., Wallace K. B., Differential mechanisms of induction of the mitochondrial permeability transition by quinones of varying chemical reactivities. Toxicology and Applied Pharmacology 1995 134 2 195 203 2-s2.0-0028787907 10.1006/taap.1995.1184
32. Eiberger W., Volkmer B., Amouroux R., Dhérin C., Radicella J. P., Epe B., Oxidative stress impairs the repair of oxidative DNA base modifications in human skin fibroblasts and melanoma cells. DNA Repair 2008 7 6 912 921 2-s2.0-43849090978 10.1016/j.dnarep.2008.03.002
33. Oltra A. M., Carbonell F., Tormos C., Iradi A., Sáez G. T., Antioxidant enzyme activities and the production of MDA and 8-oxo-dG in chronic lymphocytic leukemia. Free Radical Biology and Medicine 2001 30 11 1286 1292 2-s2.0-0035371222 10.1016/S0891-5849(01)00521-4 (Pubitemid 32463939)
34. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M. A., Lassota P., Traganos F., Features of apoptotic cells measured by flow cytometry. Cytometry 1992 13 8 795 808 2-s2.0-0026492817 10.1002/cyto.990130802
35. Taylor R. C., Cullen S. P., Martin S. J., Apoptosis: controlled demolition at the cellular level. Nature Reviews Molecular Cell Biology 2008 9 3 231 241 2-s2.0-39749182234 10.1038/nrm2312 (Pubitemid 351301823)
36. Watanabe T., Noritake J., Kaibuchi K., Regulation of microtubules in cell migration. Trends in Cell Biology 2005 15 2 76 83 2-s2.0-13244269913 10.1016/j.tcb.2004.12.006 (Pubitemid 40188217)
37. Stepanova T., Slemmer J., Hoogenraad C. C., Lansbergen G., Dortland B., De Zeeuw C. I., Grosveld F., Van Cappellen G., Akhmanova A., Galjart N., Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). Journal of Neuroscience 2003 23 7 2655 2664 2-s2.0-0345701251 (Pubitemid 36418600)
38. Diehl M. R., Zhang K., Lee H. J., Tirrell D. A., Engineering cooperativity in biomotor-protein assemblies. Science 2006 311 5766 1468 1471 2-s2.0-33644856096 10.1126/science.1122125 (Pubitemid 43376702)
39. O'Brien E. T., Salmon E. D., Erickson H. P., How calcium causes microtubule depolymerization. Cell Motility and the Cytoskeleton 1997 36 125 135 (Pubitemid 27063205)
40. Han W., Li L., Qiu S., Lu Q., Pan Q., Gu Y., Luo J., Hu X., Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Molecular Cancer Therapeutics 2007 6 5 1641 1649 2-s2.0-34250748014 10.1158/1535-7163.MCT-06-0511 (Pubitemid 46954031)
41. Fujii N., Yamashita Y., Arima Y., Nagashima M., Nakano H., Induction of topoisomerase II-mediated DNA cleavage by the plant naphthoquinones plumbagin and shikonin. Antimicrobial Agents and Chemotherapy 1992 36 12 2589 2594 2-s2.0-0026458552
42. Cheng Y. W., Chang C. Y., Lin K. L., Hu C. M., Lin C. H., Kang J. J., Shikonin derivatives inhibited LPS-induced NOS in RAW 264.7 cells via downregulation of MAPK/NF- κ B signaling. Journal of Ethnopharmacology 2008 120 2 264 271 2-s2.0-55149114628 10.1016/j.jep.2008.09.002
43. Wu Z., Wu L., Li L., Tashiro S. I., Onodera S., Ikejima T., p53-mediated cell cycle arrest and apoptosis Induced by Shikonin via a Caspase-9-Dependent Mechanism in Human Malignant Melanoma A375-S2 Cells. Journal of Pharmacological Sciences 2004 94 2 166 176 2-s2.0-1642545128 10.1254/jphs.94.166 (Pubitemid 38405131)
44. Yang H., Zhou P., Huang H., Chen D., Ma N., Cui Q. C., Shen S., Dong W., Zhang X., Lian W., Wang X., Dou Q. P., Liu J., Shikonin exerts antitumor activity via proteasome inhibition and cell death induction in vitro and in vivo. International Journal of Cancer 2009 124 10 2450 2459 2-s2.0-64249097600 10.1002/ijc.24195
45. Chiu S. C., Yang N. S., Inhibition of tumor necrosis factor- α through selective blockade of Pre-mRNA splicing by shikonin. Molecular Pharmacology 2007 71 6 1640 1645 2-s2.0-34347378942 10.1124/mol.106.032821 (Pubitemid 47018066)
46. Buzzai M., Bauer D. E., Jones R. G., DeBerardinis R. J., Hatzivassiliou G., Elstrom R. L., Thompson C. B., The glucose dependence of Akt-transformed cells can be reversed by pharmacologic activation of fatty acid β -oxidation. Oncogene 2005 24 26 4165 4173 2-s2.0-20544449673 10.1038/sj.onc.1208622 (Pubitemid 40961771)
47. Chendong Y., Sudderth J., Tuyen D., Bachoo R. G., McDonald J. G., DeBerardinis R. J., Glioblastoma cells require glutamate dehydrogenase to survive impairments of glucose metabolism or Akt signaling. Cancer Research 2009 69 20 7986 7993 2-s2.0-70350217425 10.1158/0008-5472.CAN-09-2266
48. Ralph S. J., Neuzil J., Mitochondria as targets for cancer therapy. Molecular Nutrition & Food Research 2009 53 1 9 28 2-s2.0-65549144609 10.1002/mnfr.200800044
49. Iyanagi T., Yamazaki I., One-electron-transfer reactions in biochemical systems V. Difference in the mechanism of quinone reduction by the NADH dehydrogenase and the NAD(P)H dehydrogenase (DT-diaphorase). Biochimica et Biophysica Acta 1970 216 2 282 294 2-s2.0-0014842505
50. Criddle D. N., Gillies S., Baumgartner-Wilson H. K., Jaffar M., Chinje E. C., Passmore S., Chvanov M., Barrow S., Gerasimenko O. V., Tepikin A. V., Sutton R., Petersen O. H., Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells. Journal of Biological Chemistry 2006 281 52 40485 40492 2-s2.0-33845992232 10.1074/jbc.M607704200 (Pubitemid 46041851)
51. Jackson S. P., Bartek J., The DNA-damage response in human biology and disease. Nature 2009 461 7267 1071 1078 2-s2.0-70350504453 10.1038/nature08467
52. Kroemer G., Galluzzi L., Brenner C., Mitochondrial membrane permeabilization in cell death. Physiological Reviews 2007 87 1 99 163 2-s2.0-33845977959 10.1152/physrev.00013.2006 (Pubitemid 46209992)
53. Gong K., Li W., Shikonin, a Chinese plant-derived naphthoquinone, induces apoptosis in hepatocellular carcinoma cells through reactive oxygen species: a potential new treatment for hepatocellular carcinoma. Free Radical Biology & Medicine 2011 51 2259 2271