Cracking the cytotoxicity code: Apoptotic induction of 10- acetylirciformonin B is mediated through ROS generation and mitochondrial dysfunction

Marine Drugs

Volumn 12, Issue 5, 2014, Pages 3072-3090

  Shih, Huei Chuan ^a   El Shazly, Mohamed ^b   Juan, Yung Shun ^c,d,e   Chang, Chao Yuan ^d   Su, Jui Hsin ^f,g   Chen, Yu Cheng ^f   Shih, Shou Ping ^f   Chen, Huei Mei ^h   Wu, Yang Chang ⁱ   Lu, Mei Chin ^f,g  

^a MEIHO UNIVERSITY   (Taiwan)

^b African Union Organization St Abbassia   (Egypt)

^c KAOHSIUNG MUNICIPAL HSIAO KANG HOSPITAL   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^f NATIONAL DONG HWA UNIVERSITY   (Taiwan)

^g NATIONAL MUSEUM OF MARINE BIOLOGY AND AQUARIUM   (Taiwan)

^h KAOHSIUNG VETERANS GENERAL HOSPITAL   (Taiwan)

ⁱ CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

10 Acetylirciformonin B; Apoptosis; Hexokinase; Mitochondria; Reactive oxygen species (ROS); Topoisomerase

Indexed keywords

10 ACETYLIRCIFORMONIN B; CYTOTOXIC AGENT; DNA TOPOISOMERASE (ATP HYDROLYSING); HEXOKINASE; HEXOKINASE ISOENZYME; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; SURVIVIN; TERPENOID DERIVATIVE; TOPOISOMERASE IIALPHA; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; 10-ACETYLIRCIFORMONIN B; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; GYRASE INHIBITOR; TERPENE;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECTS; METABOLISM; MITOCHONDRION; SPONGE (PORIFERA); TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL LINE, TUMOR; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; PORIFERA; REACTIVE OXYGEN SPECIES; TERPENES; TOPOISOMERASE II INHIBITORS;

EID: 84901452007     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12053072     Document Type: Article

References (52)

1. Cairns, R.A.; Harris, I.S.; Mak, T.W. Regulation of cancer cell metabolism. Nat. Rev. Cancer 2011, 11, 85-95.
2. Tatarkova, Z.; Kuka, S.; Petras, M.; Racay, P.; Lehotsky, J.; Dobrota, D.; Kaplan, P. Why mitochondria are excellent targets for cancer therapy. Klin. Onkol. 2012, 25, 421-426.
3. Gall, J.M.; Wong, V.; Pimental, D.R.; Havasi, A.; Wang, Z.; Pastorino, J.G.; Bonegio, R.G.; Schwartz, J.H.; Borkan, S.C. Hexokinase regulates Bax-mediated mitochondrial membrane injury following ischemic stress. Kidney Int. 2011, 79, 1207-1216.
4. Gogvadze, V.; Orrenius, S.; Zhivotovsky, B. Mitochondria as targets for chemotherapy. Apoptosis 2009, 14, 624-640.
5. Fogg, V.C.; Lanning, N.J.; Mackeigan, J.P. Mitochondria in cancer: At the crossroads of life and death. Chin. J. Cancer 2011, 30, 526-539.
6. Gasparre, G.; Porcelli, A.M.; Lenaz, G.; Romeo, G. Relevance of mitochondrial genetics and metabolism in cancer development. Cold Spring Harb. Persp. Biol. 2013, 5, doi:10.1101/cshperspect.a011411.
7. Patra, K.C.; Wang, Q.; Bhaskar, P.T.; Miller, L.; Wang, Z.; Wheaton, W.; Chandel, N.; Laakso, M.; Muller, W.J.; Allen, E.L.; et al. Hexokinase 2 is required for tumor initiation and maintenance and its systemic deletion is therapeutic in mouse models of cancer. Cancer Cell 2013, 24, 213-228.
8. Wenner, C.E. Cell signaling and cancer-possible targets for therapy. J. Cell. Physiol. 2010, 223, 299-308.
9. Arora, K.K.; Pedersen, P.L. Functional significance of mitochondrial bound hexokinase in tumor cell metabolism. Evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. J. Biol. Chem. 1988, 263, 17422-17428. (Pubitemid 19029327)
10. Shulga, N.; Wilson-Smith, R.; Pastorino, J.G. Hexokinase II detachment from the mitochondria potentiates cisplatin induced cytotoxicity through a caspase-2 dependent mechanism. Cell Cycle 2009, 8, 3355-3364.
11. Mathupala, S.P.; Ko, Y.H.; Pedersen, P.L. The pivotal roles of mitochondria in cancer: Warburg and beyond and encouraging prospects for effective therapies. Biochim. Biophys. Acta 2010, 1797, 1225-1230.
12. Murphy, M.P.; Holmgren, A.; Larsson, N.G.; Halliwell, B.; Chang, C.J.; Kalyanaraman, B.; Rhee, S.G.; Thornalley, P.J.; Partridge, L.; Gems, D.; et al. Unraveling the biological roles of reactive oxygen species. Cell. Metab. 2011, 13, 361-366.
13. Kim, K.Y.; Yu, S.N.; Lee, S.Y.; Chun, S.S.; Choi, Y.L.; Park, Y.M.; Song, C.S.; Chatterjee, B.; Ahn, S.C. Salinomycin-induced apoptosis of human prostate cancer cells due to accumulated reactive oxygen species and mitochondrial membrane depolarization. Biochem. Biophys. Res. Commun. 2011, 413, 80-86.
14. Circu, M.L.; Aw, T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48, 749-762.
15. Bauer, G. Tumor cell-protective catalase as a novel target for rational therapeutic approaches based on specific intercellular ROS signaling. Anticancer Res. 2012, 32, 2599-2624.
16. Martindale, J.L.; Holbrook, N.J. Cellular response to oxidative stress: Signaling for suicide and survival. J. Cell. Physiol. 2002, 192, 1-15. (Pubitemid 34587382)
17. Mates, J.M.; Segura, J.A.; Alonso, F.J.; Marquez, J. Oxidative stress in apoptosis and cancer: An update. Arch. Toxicol 2012, 86, 1649-1665.
18. Azad, N.; Iyer, A.; Vallyathan, V.; Wang, L.; Castranova, V.; Stehlik, C.; Rojanasakul, Y. Role of oxidative/nitrosative stress-mediated Bcl-2 regulation in apoptosis and malignant transformation. Ann. N. Y. Acad. Sci. 2010, 1203, 1-6.
19. Clement, M.V.; Hirpara, J.L.; Pervaiz, S. Decrease in intracellular superoxide sensitizes Bcl-2-overexpressing tumor cells to receptor and drug-induced apoptosis independent of the mitochondria. Cell Death Differ. 2003, 10, 1273-1285. (Pubitemid 37407129)
20. Macip, S.; Igarashi, M.; Berggren, P.; Yu, J.; Lee, S.W.; Aaronson, S.A. Influence of induced reactive oxygen species in p53-mediated cell fate decisions. Mol. Cell. Biol. 2003, 23, 8576-8585. (Pubitemid 37433363)
21. Llovet, J.M.; Di Bisceglie, A.M.; Bruix, J.; Kramer, B.S.; Lencioni, R.; Zhu, A.X.; Sherman, M.; Schwartz, M.; Lotze, M.; Talwalkar, J.; et al. Design and endpoints of clinical trials in hepatocellular carcinoma. J. Natl. Cancer Inst. 2008, 100, 698-711.
22. Yap, T.A.; Workman, P. Exploiting the cancer genome: Strategies for the discovery and clinical development of targeted molecular therapeutics. Ann. Rev. Pharmacol. Toxicol. 2012, 52, 549-573.
23. Su, J.H.; Tseng, S.W.; Lu, M.C.; Liu, L.L.; Chou, Y.; Sung, P.J. Cytotoxic C21 and C22 terpenoid-derived metabolites from the sponge Ircinia sp. J. Nat. Prod. 2011, 74, 2005-2009.
24. Su, J.H.; Chang, W.B.; Chen, H.M.; El-Shazly, M.; Du, Y.C.; Kung, T.H.; Chen, Y.C.; Sung, P.J.; Ho, Y.S.; Kuo, F.W.; et al. 10-Acetylirciformonin B, a sponge furanoterpenoid, induces DNA damage and apoptosis in leukemia cells. Molecules 2012, 17, 11839-11848.
25. Du, Y.C.; Chang, F.R.; Wu, T.Y.; Hsu, Y.M.; El-Shazly, M.; Chen, C.F.; Sung, P.J.; Lin, Y.Y.; Lin, Y.H.; Wu, Y.C.; et al. Antileukemia component, dehydroeburicoic acid from Antrodia camphorata induces DNA damage and apoptosis in vitro and in vivo models. Phytomedicine 2012, 19, 788-796.
26. Su, J.H.; Chen, Y.C.; El-Shazly, M.; Du, Y.C.; Su, C.W.; Tsao, C.W.; Liu, L.L.; Chou, Y.; Chang, W.B.; Su, Y.D.; et al. Towards the Small and the Beautiful: A Small Dibromotyrosine Derivative from Pseudoceratina sp. Sponge Exhibits Potent Apoptotic Effect through Targeting IKK/NFkappaB Signaling Pathway. Mar. Drugs 2013, 11, 3168-3185.
27. Nitiss, J.L. Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer 2009, 9, 338-350.
28. 3) induces apoptosis through activation of Bax in hematopoietic cells. Oncogene 2005, 24, 3339-3347.
29. Gardai, S.J.; Hildeman, D.A.; Frankel, S.K.; Whitlock, B.B.; Frasch, S.C.; Borregaard, N.; Marrack, P.; Bratton, D.L.; Henson, P.M. Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J. Biol. Chem. 2004, 279, 21085-21095. (Pubitemid 38656511)
30. Zhou, H.; Xu, M.; Gao, Y.; Deng, Z.; Cao, H.; Zhang, W.; Wang, Q.; Zhang, B.; Song, G.; Zhan, Y. Matrine induces caspase-independent program cell death in hepatocellular carcinoma through bid-mediated nuclear translocation of apoptosis inducing factor. Mol. Cancer 2014, 13, doi:10.1186/1476-4598-13-59.
31. Pang, B.; Qiao, X.; Janssen, L.; Velds, A.; Groothuis, T.; Kerkhoven, R.; Nieuwland, M.; Ovaa, H.; Rottenberg, S.; van Tellingen, O.; et al. Drug-induced histone eviction from open chromatin contributes to the chemotherapeutic effects of doxorubicin. Nat. Commun. 2013, 4, doi:10.1038/ncomms2921.
32. Wu, C.C.; Li, T.K.; Farh, L.; Lin, L.Y.; Lin, T.S.; Yu, Y.J.; Yen, T.J.; Chiang, C.W.; Chan, N.L. Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide. Science 2011, 333, 459-462.
33. Ratain, M.J.; Rowley, J.D. Therapy-related acute myeloid leukemia secondary to inhibitors of topoisomerase II: From the bedside to the target genes. Ann. Oncol. 1992, 3, 107-111.
34. Roulston, D.; Anastasi, J.; Rudinsky, R.; Nucifora, G.; Zeleznik-Le, N.; Rowley, J.D.; McGavran, L.; Tsuchida, M.; Hayashi, Y. Therapy-related acute leukemia associated with t(11q23) after primary acute myeloid leukemia with t(8;21): A report of two cases. Blood 1995, 86, 3613-3614.
35. Kudo, K.; Yoshida, H.; Kiyoi, H.; Numata, S.; Horibe, K.; Naoe, T. Etoposide-related acute promyelocytic leukemia. Leukemia 1998, 12, 1171-1175. (Pubitemid 28395977)
36. Pedersen-Bjergaard, J.; Philip, P.; Larsen, S.O.; Andersson, M.; Daugaard, G.; Ersboll, J.; Hansen, S.W.; Hou-Jensen, K.; Nielsen, D.; Sigsgaard, T.C.; et al. Therapy-related myelodysplasia and acute myeloid leukemia. Cytogenetic characteristics of 115 consecutive cases and risk in seven cohorts of patients treated intensively for malignant diseases in the Copenhagen series. Leukemia 1993, 7, 1975-1986.
37. Chiara, A.D.; Pederzoli-Ribeil, M.; Burgel, P.R.; Danel, C.; Witko-Sarsat, V. Targeting cytosolic proliferating cell nuclear antigen in neutrophil-dominated inflammation. Front. Immunol. 2012, 3, doi:10.3389/fimmu. 2012.00311.
38. Liebermann, D.A.; Hoffman, B. Gadd45 in the response of hematopoietic cells to genotoxic stress. Blood Cells Mol. Dis. 2007, 39, 329-335. (Pubitemid 47484472)
39. Liebermann, D.A.; Tront, J.S.; Sha, X.; Mukherjee, K.; Mohamed-Hadley, A.; Hoffman, B. Gadd45 stress sensors in malignancy and leukemia. Crit. Rev. Oncog. 2011, 16, 129-140.
40. Barreto, G.; Schafer, A.; Marhold, J.; Stach, D.; Swaminathan, S.K.; Handa, V.; Doderlein, G.; Maltry, N.; Wu, W.; Lyko, F.; et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445, 671-675.
41. Wadhwa, S.; Mumper, R.J. D-Penicillamine and other low molecular weight thiols: Review of anticancer effects and related mechanisms. Cancer Lett. 2013, 337, 8-21.
42. Gillies, L.A.; Kuwana, T. Apoptosis regulation at the mitochondrial outer membrane. J. Cell. Biochem. 2014, 115, 632-640.
43. Chiara, F.; Gambalunga, A.; Sciacovelli, M.; Nicolli, A.; Ronconi, L.; Fregona, D.; Bernardi, P.; Rasola, A.; Trevisan, A. Chemotherapeutic induction of mitochondrial oxidative stress activates GSK-3alpha/beta and Bax, leading to permeability transition pore opening and tumor cell death. Cell Death Dis. 2012, 3, e444.
44. Wang, Q.; Sun, S.-Y.; Khuri, F.; Curran, W.J.; Deng, X. Mono-or double-site phosphorylation distinctly regulates the proapoptotic function of Bax. PLoS One 2010, 5, e13393.
45. An, J.; Chen, Y.; Huang, Z. Critical upstream signals of cytochrome c release induced by a novel Bcl-2 inhibitor. J. Biol. Chem. 2004, 279, 19133-19140. (Pubitemid 38623344)
46. Steelman, L.S.; Franklin, R.A.; Abrams, S.L.; Chappell, W.; Kempf, C.R.; Basecke, J.; Stivala, F.; Donia, M.; Fagone, P.; Nicoletti, F.; et al. Roles of the Ras/Raf/MEK/ERK pathway in leukemia therapy. Leukemia 2011, 25, 1080-1094.
47. Palorini, R.; Simonetto, T.; Cirulli, C.; Chiaradonna, F. Mitochondrial complex I inhibitors and forced oxidative phosphorylation synergize in inducing cancer cell death. Int. J. Cell. Biol. 2013, 2013, doi: 10.1155/2013/243876.
48. Kim, J.S.; Ahn, K.J.; Kim, J.A.; Kim, H.M.; Lee, J.D.; Lee, J.M.; Kim, S.J.; Park, J.H. Role of reactive oxygen species-mediated mitochondrial dysregulation in 3-bromopyruvate induced cell death in hepatoma cells : ROS-mediated cell death by 3-BrPA. J. Bioenerg. Biomembr. 2008, 40, 607-618.
49. Wei, L.; Dai, Q.; Zhou, Y.; Zou, M.; Li, Z.; Lu, N.; Guo, Q. Oroxylin A sensitizes non-small cell lung cancer cells to anoikis via glucose-deprivation- like mechanisms: c-Src and hexokinase II. Biochim. Biophys. Acta 2013, 1830, 3835-3845.
50. Sebastian, S.; Kenkare, U.W. Expression of two type II-like tumor hexokinase RNA transcripts in cancer cell lines. Tumor Biol. 1998, 19, 253-260. (Pubitemid 28318435)
51. Marin-Hernandez, A.; Rodriguez-Enriquez, S.; Vital-Gonzalez, P.A.; Flores-Rodriguez, F.L.; Macias-Silva, M.; Sosa-Garrocho, M.; Moreno-Sanchez, R. Determining and understanding the control of glycolysis in fast-growth tumor cells. Flux control by an over-expressed but strongly product-inhibited hexokinase. FEBS J. 2006, 273, 1975-1988.
52. Liu, C.X.; Zhou, H.C.; Yin, Q.Q.; Wu, Y.L.; Chen, G.Q. Targeting peroxiredoxins against leukemia. Exp. Cell Res. 2013, 319, 170-176.