(1S,2S,3E,7E,11E)-3,7,11,15-cembratetraen-17,2-olide, a cembrenolide diterpene from soft coral Lobophytum sp., inhibits growth and induces apoptosis in human colon cancer cells through reactive oxygen species generation

Biological and Pharmaceutical Bulletin

Volumn 35, Issue 7, 2012, Pages 1054-1063

  Hong, Ji Young ^a   Boo, Hye Jin ^a   Kang, Jung Il ^a   Kim, Min Kyoung ^a   Yoo, Eun Sook ^a   Hyun, Jin Won ^a   Koh, Young Sang ^a   Kim, Gi Young ^b   Maeng, Young Hee ^a   Hyun, Chang Lim ^a   Chang, Weon Young ^a   Kim, Young Ho ^c   Kim, Young Ree ^a   Kang, Hee Kyoung ^a  

^a Jeju National University School of Medicine   (South Korea)

^b Jeju National University   (South Korea)

^c Chungnam National University   (South Korea)

Author keywords

(1S,2S,3E,7E,11E) 3,7,11,15 cembratetraen 17,2 olide; Apoptosis; Cembrenolide diterpene; HT 29; Reactive oxygen species

Indexed keywords

3,7,11,15 CEMBRATETRAEN 17,2 OLIDE; ACETYLCYSTEINE; ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 8; CASPASE 9; CATALASE; CYTOCHROME C; GLUTATHIONE PEROXIDASE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN BID; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL DEATH; CELL STRAIN HT29; COLON CARCINOMA; CONCENTRATION RESPONSE; CORAL; DRUG CYTOTOXICITY; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; LOBOPHYTUM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOSIS INHIBITION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTHOZOA; ANTINEOPLASTIC AGENTS; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CASPASES; CATALASE; CELL PROLIFERATION; COLONIC NEOPLASMS; DITERPENES; GLUTATHIONE PEROXIDASE; HEME OXYGENASE-1; HT29 CELLS; HUMANS; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; STAT3 TRANSCRIPTION FACTOR; SUPEROXIDE DISMUTASE;

EID: 84863549044     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b11-00024     Document Type: Article

References (54)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J. Clin., 59, 225-249 (2009).
2. Espey DK, Wu XC, Swan J, Wiggins C, Jim MA, Ward E, Wingo PA, Howe HL, Ries LA, Miller BA, Jemal A, Ahmed F, Cobb N, Kaur JS, Edwards BK. Annual report to the nation on the status of cancer, 1975-2004, featuring cancer in American Indians and Alaska Natives. Cancer, 110, 2119-2152 (2007).
3. Ministry of Health and Welfare Republic of Korea. 2007 Annual Report of the Korea Central Cancer Registry, Korea Central Cancer Registry (2007).
4. Oh SY, Lee JH, Chang DK, Hoe SC, Kim HJ. Relationship of nutrients and food to colorectal cancer risk in Korean. Nutr. Res., 25, 805-813 (2005).
5. Longley DB, Harkin DP, Johnston PG. 5-Fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer, 3, 330-338 (2003).
6. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov., 8, 579-591 (2009).
7. Huang C, Zhang Z, Ding M, Li J, Ye J, Leonard SS, Shen HM, Butterworth L, Lu Y, Costa M, Rojanasakul Y, Castranova V, Vallyathan V, Shi X. Vanadate induces p53 transactivation through hydrogen peroxide and causes apoptosis. J. Biol. Chem., 275, 32516-32522 (2000).
8. Pelicano H, Feng L, Zhou Y, Carew JS, Hileman EO, Plunkett W, Keating MJ, Huang P. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Biol. Chem., 278, 37832-37839 (2003).
9. Fiers W, Beyaert R, Declercq W, Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene, 18, 7719-7730 (1999).
10. Simizu S, Takada M, Umezawa K, Imoto M. Requirement of caspase- 3(-like) protease-mediated hydrogen peroxide production for apoptosis induced by various anticancer drugs. J. Biol. Chem., 273, 26900-26907 (1998).
11. Blunt JW, Copp BR, Hu WP, Munro MH, Northcote PT, Prinsep MR. Marine natural products. Nat. Prod. Rep., 24, 31-86 (2007).
12. Higuchi R, Miyamoto T, Yamada K, Komori T. Cytotoxic and ichthyotoxic compounds from marine Opisthobranchia and soft coral. Toxicon, 36, 1703-1705 (1998).
13. Rashid MA, Gustafson KR, Boyd MR. HIV-inhibitory cembrane derivatives from a Philippines collection of the soft coral Lobophytum species. J. Nat. Prod., 63, 531-533 (2000).
14. Coll JC. The chemistry and the chemical ecology of octocorals (Coelenterata, Anthozoa, Octocorallia). Chem. Rev., 92, 613-631 (1992).
15. Chao CH, Wen ZH, Wu YC, Yeh HC, Sheu JH. Cytotoxic and anti-inflammatory cembranoids from the soft coral Lobophytum crassum. J. Nat. Prod., 71, 1819-1824 (2008).
16. Bonnard I, Jhaumeer-Laulloo SB, Bontemps N, Banaigs B, Aknin M. New lobane and cembrane diterpenes from two comorian soft corals. Mar Drugs, 8, 359-372 (2010).
17. Li LM, Li GY, Pu JX, Xiao WL, Ding LS, Sun HD. ent-Kaurane and cembrane diterpenoids from Isodon sculponeatus and their cytotoxicity. J. Nat. Prod., 72, 1851-1856 (2009).
18. Coval SJ, Patton RW, Petrin JM, James L, Rothofsky ML, Lin SL, Patel M, Reed JK, Mcphail AT, Bishop WR. A cembranolide diterpene farnesyl protein transferase inhibitor from the marine soft coral Lobophytum cristagalli. Bioorg. Med. Chem. Lett., 6, 909-912 (1996).
19. Nguyen HT, Chau VM, Phan VK, Hoang TH, Nguyen HN, Nguyen XC, Tran HQ, Nguyen XN, Hyun JH, Kang HK, Kim YH. Chemical components from the Vietnamese soft coral Lobophytum sp. Arch. Pharm. Res., 33, 503-508 (2010).
20. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of radiosensitivity. Cancer Res., 47, 943-946 (1987).
21. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal. Biochem., 150, 76-85 (1985).
22. Adler V, Yin Z, Tew KD, Ronai Z. Role of redox potential and reactive oxygen species in stress signaling. Oncogene, 18, 6104-6111 (1999).
23. Hei TK, Liu SX, Waldren C. Mutagenicity of arsenic in mammalian cells: role of reactive oxygen species. Proc. Natl. Acad. Sci. U.S.A., 95, 8103-8107 (1998).
24. Gao N, Ding M, Zheng JZ, Zhang Z, Leonard SS, Liu KJ, Shi X, Jiang BH. Vanadate-induced expression of hypoxia-inducible factor 1 α and vascular endothelial growth factor through phosphatidylinositol 3-kinase/Akt pathway and reactive oxygen species. J. Biol. Chem., 277, 31963-31971 (2002).
25. Irby RB, Yeatman TJ. Role of Src expression and activation in human cancer. Oncogene, 19, 5636-5642 (2000).
26. Kim LC, Song L, Haura EB. Src kinases as therapeutic targets for cancer. Nat. Rev. Clin. Oncol., 6, 587-595 (2009).
27. Nakashima I, Kato M, Akhand AA, Suzuki H, Takeda K, Hossain K, Kawamoto Y. Redox-linked signal transduction pathways for protein tyrosine kinase activation. Antioxid. Redox Signal., 4, 517-531 (2002).
28. Li WX. Canonical and non-canonical JAK-STAT signaling. Trends Cell Biol., 18, 545-551 (2008).
29. Kaur N, Lu B, Monroe RK, Ward SM, Halvorsen SW. Inducers of oxidative stress block ciliary neurotrophic factor activation of Jak/STAT signaling in neurons. J. Neurochem., 92, 1521-1530 (2005).
30. Su B, Karin M. Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol., 8, 402-411 (1996).
31. Kurata S. Selective activation of p38 MAPK cascade and mitotic arrest caused by low level oxidative stress. J. Biol. Chem., 275, 23413-23416 (2000).
32. Park SJ, Kim IS. The role of p38 MAPK activation in auranofin-induced apoptosis of human promyelocytic leukaemia HL-60 cells. Br. J. Pharmacol., 146, 506-513 (2005).
33. Kondoh M, Tasaki E, Araragi S, Takiguchi M, Higashimoto M, Watanabe Y, Sato M. Requirement of caspase and p38MAPK activation in zinc-induced apoptosis in human leukemia HL-60 cells. Eur. J. Biochem., 269, 6204-6211 (2002).
34. Tenhunen R, Marver HS, Schmid R. The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl. Acad. Sci. U.S.A., 61, 748-755 (1968).
35. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev., 86, 583-650 (2006).
36. Kietzmann T, Samoylenko A, Immenschuh S. Transcriptional regulation of heme oxygenase-1 gene expression by MAP kinases of the JNK and p38 pathways in primary cultures of rat hepatocytes. J. Biol. Chem., 278, 17927-17936 (2003).
37. Wu CC, Hsieh CW, Lai PH, Lin JB, Liu YC, Wung BS. Upregulation of endothelial heme oxygenase-1 expression through the activation of the JNK pathway by sublethal concentrations of acrolein. Toxicol. Appl. Pharmacol., 214, 244-252 (2006).
38. von Schwarzenberg K, Vollmar AM. Targeting apoptosis pathways by natural compounds in cancer: Marine compounds as lead structures and chemical tools for cancer therapy. Cancer Lett., (2010), in press.
39. Schumacker PT. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell, 10, 175-176 (2006).
40. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis, 12, 913-922 (2007).
41. Chen HM, Wu YC, Chia YC, Chang FR, Hsu HK, Hsieh YC, Chen CC, Yuan SS. Gallic acid, a major component of Toona sinensis leaf extracts, contains a ROS-mediated anti-cancer activity in human prostate cancer cells. Cancer Lett., 286, 161-171 (2009).
42. Trachootham D, Zhou Y, Zhang H, Demizu Y, Chen Z, Pelicano H, Chiao PJ, Achanta G, Arlinghaus RB, Liu J, Huang P. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell, 10, 241-252 (2006).
43. Singh SV, Srivastava SK, Choi S, Lew KL, Antosiewicz J, Xiao D, Zeng Y, Watkins SC, Johnson CS, Trump DL, Lee YJ, Xiao H, Herman-Antosiewicz A. Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species. J. Biol. Chem., 280, 19911-19924 (2005).
44. Crompton M, Barksby E, Johnson N, Capano M. Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie, 84, 143-152 (2002).
45. Green DR. Apoptotic pathways: ten minutes to dead. Cell, 121, 671-674 (2005).
46. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science, 281, 1305-1308 (1998).
47. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J., 14, 5579-5588 (1995).
48. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell, 91, 231-241 (1997).
49. Dolado I, Nebreda AR. AKT and oxidative stress team up to kill cancer cells. Cancer Cell, 14, 427-429 (2008).
50. 2 induces apoptosis by reactive oxygen species-mediated inactivation of Akt in leukemia and colorectal cancer cells and shows in vivo antitumor activity. Clin. Cancer Res., 15, 5414-5425 (2009).
51. Summy JM, Gallick GE. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev., 22, 337-358 (2003).
52. Aggarwal BB, Sethi G, Ahn KS, Sandur SK, Pandey MK, Kunnumakkara AB, Sung B, Ichikawa H. Targeting signal-transducer-andactivator-of-transcription-3 for prevention and therapy of cancer: modern target but ancient solution. Ann. N.Y. Acad. Sci., 1091, 151-169 (2006).
53. Park EJ, Lim JH, Nam SI, Park JW, Kwon TK. Rottlerin induces heme oxygenase-1 (HO-1) up-regulation through reactive oxygen species (ROS) dependent and PKC delta-independent pathway in human colon cancer HT29 cells. Biochimie, 92, 110-115 (2010).
54. Sharma V, Joseph C, Ghosh S, Agarwal A, Mishra MK, Sen E. Kaempferol induces apoptosis in glioblastoma cells through oxidative stress. Mol. Cancer Ther., 6, 2544-2553 (2007).