Dehydrocostuslactone suppresses angiogenesis in vitro and in vivo through inhibition of AKT/GSK-3β and mtor signaling pathways

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Wang, Chih Ya ^a   Tsai, An Chi ^b   Peng, Chieh Yu ^c,d   Chang, Ya Ling ^a   Lee, Kuo Hsiung ^d,e   Teng, Che Ming ^a   Pan, Shiow Lin ^b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e UNC Hamner Institute for Drug Safety Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; CYCLIN A; CYCLIN D1; CYCLIN DEPENDENT KINASE 2; DEHYDROCOSTUSLACTONE; GLYCOGEN SYNTHASE KINASE 3BETA; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; DEHYDROCOSTUS LACTONE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; LACTONE; MTOR PROTEIN, HUMAN; SESQUITERPENE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER INHIBITION; CAPILLARY TUBE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY);

COSTUS; MUS MUSCULUS; SAUSSUREA;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; CELLS, CULTURED; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LACTONES; MICE; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEINS C-AKT; SESQUITERPENES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84863128252     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031195     Document Type: Article

References (44)

1. Folkman J, (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6: 273-286.
2. Bergers G, Benjamin LE, (2003) Tumorigenesis and the angiogenic switch. Nat Rev Cancer 3: 401-410.
3. Ingber D, Fujita T, Kishimoto S, Sudo K, Kanamaru T, et al. (1990) Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature 348: 555-557.
4. Shiojima I, Walsh K, (2002) Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90: 1243-1250.
5. Skurk C, Maatz H, Rocnik E, Bialik A, Force T, et al. (2005) Glycogen-Synthase Kinase3beta/beta-catenin axis promotes angiogenesis through activation of vascular endothelial growth factor signaling in endothelial cells. Circ Res 96: 308-318.
6. Kim HS, Skurk C, Thomas SR, Bialik A, Suhara T, et al. (2002) Regulation of angiogenesis by glycogen synthase kinase-3beta. J Biol Chem 277: 41888-41896.
7. Diehl JA, Zindy F, Sherr CJ, (1997) Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev 11: 957-972.
8. Diehl JA, Cheng M, Roussel MF, Sherr CJ, (1998) Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 12: 3499-3511.
9. Alt JR, Cleveland JL, Hannink M, Diehl JA, (2000) Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev 14: 3102-3114.
10. Giacinti C, Giordano A, (2006) RB and cell cycle progression. Oncogene 25: 5220-5227.
11. Sherr CJ, McCormick F, (2002) The RB and p53 pathways in cancer. Cancer Cell 2: 103-112.
12. Fu M, Wang C, Li Z, Sakamaki T, Pestell RG, (2004) Minireview: Cyclin D1: normal and abnormal functions. Endocrinology 145: 5439-5447.
13. Yasui M, Yamamoto H, Ngan CY, Damdinsuren B, Sugita Y, et al. (2006) Antisense to cyclin D1 inhibits vascular endothelial growth factor-stimulated growth of vascular endothelial cells: implication of tumor vascularization. Clin Cancer Res 12: 4720-4729.
14. Lee HJ, Kim NY, Jang MK, Son HJ, Kim KM, et al. (1999) A sesquiterpene, dehydrocostus lactone, inhibits the expression of inducible nitric oxide synthase and TNF-alpha in LPS-activated macrophages. Planta Med 65: 104-108.
15. Chen HC, Chou CK, Lee SD, Wang JC, Yeh SF, (1995) Active compounds from Saussurea lappa Clarks that suppress hepatitis B virus surface antigen gene expression in human hepatoma cells. Antiviral Res 27: 99-109.
16. Taniguchi M, Kataoka T, Suzuki H, Uramoto M, Ando M, et al. (1995) Costunolide and dehydrocostus lactone as inhibitors of killing function of cytotoxic T lymphocytes. Biosci Biotechnol Biochem 59: 2064-2067.
17. Yuuya S, Hagiwara H, Suzuki T, Ando M, Yamada A, et al. (1999) Guaianolides as immunomodulators. Synthesis and biological activities of dehydrocostus lactone, mokko lactone, eremanthin, and their derivatives. J Nat Prod 62: 22-30.
18. Matsuda H, Kageura T, Inoue Y, Morikawa T, Yoshikawa M, (2000) Absolute stereostructures and syntheses of saussureamines A, B, C, D and E, amino acid-sesquiterpene conjugates with gastroprotective effect, from the roots of Saussurea lappa. Tetrahedron 56: 7763-7777.
19. Choi EJ, Ahn WS, (2009) Antiproliferative effects of dehydrocostuslactone through cell cycle arrest and apoptosis in human ovarian cancer SK-OV-3 cells. Int J Mol Med 23: 211-216.
20. Oh GS, Pae HO, Chung HT, Kwon JW, Lee JH, et al. (2004) Dehydrocostus lactone enhances tumor necrosis factor-alpha-induced apoptosis of human leukemia HL-60 cells. Immunopharmacol Immunotoxicol 26: 163-175.
21. Hsu YL, Wu LY, Kuo PL, (2009) Dehydrocostuslactone, a medicinal plant-derived sesquiterpene lactone, induces apoptosis coupled to endoplasmic reticulum stress in liver cancer cells. J Pharmacol Exp Ther 329: 808-819.
22. Hung JY, Hsu YL, Ni WC, Tsai YM, Yang CJ, et al. (2010) Oxidative and endoplasmic reticulum stress signaling are involved in dehydrocostuslactone-mediated apoptosis in human non-small cell lung cancer cells. Lung Cancer 68: 355-365.
23. Kuo PL, Ni WC, Tsai EM, Hsu YL, (2009) Dehydrocostuslactone disrupts signal transducers and activators of transcription 3 through up-regulation of suppressor of cytokine signaling in breast cancer cells. Mol Cancer Ther 8: 1328-1339.
24. Burgering BM, Coffer PJ, (1995) Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 376: 599-602.
25. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, et al. (1995) The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81: 727-736.
26. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, et al. (1998) Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273: 30336-30343.
27. Hahn-Windgassen A, Nogueira V, Chen CC, Skeen JE, Sonenberg N, et al. (2005) Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 280: 32081-32089.
28. Gingras AC, Kennedy SG, O'Leary MA, Sonenberg N, Hay N, (1998) 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev 12: 502-513.
29. Rosenwald IB, Kaspar R, Rousseau D, Gehrke L, Leboulch P, et al. (1995) Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and post-transcriptional levels. J Biol Chem 270: 21176-21180.
30. Folkman J, (2002) Role of angiogenesis in tumor growth and metastasis. Semin Oncol 29: 15-18.
31. El Sayed KA, (2005) Natural products as angiogenesis modulators. Mini Rev Med Chem 5: 971-993.
32. Hanai J, Dhanabal M, Karumanchi SA, Albanese C, Waterman M, et al. (2002) Endostatin causes G1 arrest of endothelial cells through inhibition of cyclin D1. J Biol Chem 277: 16464-16469.
33. Skeen JE, Bhaskar PT, Chen CC, Chen WS, Peng XD, et al. (2006) Akt deficiency impairs normal cell proliferation and suppresses oncogenesis in a p53-independent and mTORC1-dependent manner. Cancer Cell 10: 269-280.
34. Kanda S, Hodgkin MN, Woodfield RJ, Wakelam MJ, Thomas G, et al. (1997) Phosphatidylinositol 3′-kinase-independent p70 S6 kinase activation by fibroblast growth factor receptor-1 is important for proliferation but not differentiation of endothelial cells. J Biol Chem 272: 23347-23353.
35. Jiang BH, Liu LZ, (2008) AKT signaling in regulating angiogenesis. Curr Cancer Drug Targets 8: 19-26.
36. Jiang BH, Zheng JZ, Aoki M, Vogt PK, (2000) Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc Natl Acad Sci U S A 97: 1749-1753.
37. Schnell CR, Stauffer F, Allegrini PR, O'Reilly T, McSheehy PM, et al. (2008) Effects of the dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor NVP-BEZ235 on the tumor vasculature: implications for clinical imaging. Cancer Res 68: 6598-6607.
38. Tsai AC, Pan SL, Liao CH, Guh JH, Wang SW, et al. (2010) Moscatilin, a bibenzyl derivative from the India orchid Dendrobrium loddigesii, suppresses tumor angiogenesis and growth in vitro and in vivo. Cancer Lett 292: 163-170.
39. Yuan TL, Choi HS, Matsui A, Benes C, Lifshits E, et al. (2008) Class 1A PI3K regulates vessel integrity during development and tumorigenesis. Proc Natl Acad Sci U S A 105: 9739-9744.
40. Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, et al. (2006) Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10: 159-170.
41. Hamada K, Sasaki T, Koni PA, Natsui M, Kishimoto H, et al. (2005) The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev 19: 2054-2065.
42. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM, (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science pp. 1098-1101.
43. Nelsen CJ, Rickheim DG, Tucker MM, Hansen LK, Albrecht JH, (2003) Evidence that cyclin D1 mediates both growth and proliferation downstream of TOR in hepatocytes. J Biol Chem 278: 3656-3663.
44. Engelman JA, (2009) Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 9: 550-562.