Jaceosidin, Isolated from dietary mugwort (Artemisia princeps), Induces G2/M cell cycle arrest by inactivating cdc25C-cdc2 via ATM-Chk1/2 activation

Food and Chemical Toxicology

Volumn 55, Issue , 2013, Pages 214-221

  Lee, Jong Gyu ^a   Kim, Ji Hyun ^a   Ahn, Ji Hye ^a   Lee, Kyung Tae ^a   Baek, Nam In ^a   Choi, Jung Hye ^a  

^a Kyung Hee University   (South Korea)

Author keywords

ATM; Cdc25C; Chk1 2; Endometrial cancer; Jaceosidin; Mugwort

Indexed keywords

ANTIMITOTIC AGENT; ATM PROTEIN; CELL CYCLE PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CISPLATIN; CYCLIN B; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1; FLAVONOID; JACEOSIDIN; PROTEIN CDC25C; PROTEIN P21; PROTEIN TYROSINE PHOSPHATASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; ARTEMISIA VULGARIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL MEDIATED CYTOTOXICITY; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; ENDOMETRIUM CANCER; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; NONHUMAN; RNA INTERFERENCE;

ARTEMISIA; CDC25 PHOSPHATASES; CELL CYCLE PROTEINS; CELL DIVISION; CELL LINE, TUMOR; CYCLIN B; DNA-BINDING PROTEINS; FEMALE; FLAVONOIDS; G2 PHASE; HUMANS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84873563211     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.12.026     Document Type: Article

References (55)

1. Ando T., Kawabe T., Ohara H., Ducommun B., Itoh M., Okamoto T. Involvement of the interaction between p21 and proliferating cell nuclear antigen for the maintenance of G2/M arrest after DNA damage. J. Biol. Chem. 2001, 276:42971-42977.
2. Bartek J., Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 2003, 3:421-429.
3. Bates S., Ryan K.M., Phillips A.C., Vousden K.H. Cell cycle arrest and DNA endoreduplication following p21Waf1/Cip1 expression. Oncogene 1998, 17:1691-1703.
4. Bunz F., Dutriaux A., Lengauer C., Waldman T., Zhou S., Brown J.P., Sedivy J.M., Kinzler K.W., Vogelstein B. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 1998, 282:1497-1501.
5. Buolamwini J.K. Cell cycle molecular targets in novel anticancer drug discovery. Curr. Pharm. Des. 2000, 6:379-392.
6. Chang S.H., Jung E.J., Park Y.H., Lim D.G., Ko N.Y., Choi W.S., Her E., Kim S.H., Choi K.D., Bae J.H., Kim S.H., Kang C.D., Han D.J., Kim S.C. Anti-inflammatory effects of Artemisia princeps in antigen-stimulated T cells and regulatory T cells. J. Pharm. Pharmacol. 2009, 61:1043-1050.
7. Chaturvedi P., Eng W.K., Zhu Y., Mattern M.R., Mishra R., Hurle M.R., Zhang X., Annan R.S., Lu Q., Faucette L.F., Scott G.F., Li X., Carr S.A., Johnson R.K., Winkler J.D., Zhou B.B. Mammalian Chk2 is a downstream effector of the ATM-dependent DNA damage checkpoint pathway. Oncogene 1999, 18:4047-4054.
8. Cho J.H., Lee J.G., Yang Y.I., Kim J.H., Ahn J.H., Baek N.I., Lee K.T., Choi J.H. Eupatilin, a dietary flavonoid, induces G2/M cell cycle arrest in human endometrial cancer cells. Food Chem. Toxicol. 2011, 49:1737-1744.
9. Choi E.J., Oh H.M., Na B.R., Ramesh T.P., Lee H.J., Choi C.S., Choi S.C., Oh T.Y., Choi S.J., Chae J.R., Kim S.W., Jun C.D. Eupatilin protects gastric epithelial cells from oxidative damage and down-regulates genes responsible for the cellular oxidative stress. Pharm. Res. 2008, 25:1355-1364.
10. Choi J.Y., Shin S.K., Jeon S.M., Baek N.I., Chung H.G., Jeong T.S., Lee K.T., Lee M.K., Choi M.S. Dose-response study of sajabalssuk ethanol extract from Artemisia princeps Pampanini on blood glucose in subjects with impaired fasting glucose or mild type 2 diabetes. J. Med. Food 2011, 14:101-107.
11. Chon H.S., Marchion D.C., Xiong Y., Chen N., Bicaku E., Stickles X.B., Zgheib N.B., Judson P.L., Hakam A., Gonzalez-Bosquet J., Wenham R.M., Apte S.M., Lancaster J.M. The BCL2 antagonist of cell death pathway influences endometrial cancer cell sensitivity to cisplatin. Gynecol. Oncol. 2012, 124:119-124.
12. Collins K., Jacks T., Pavletich N.P. The cell cycle and cancer. Proc. Natl. Acad. Sci. USA 1997, 94:2776-2778.
13. Creasman W.T., Odicino F., Maisonneuve P., Beller U., Benedet J.L., Heintz A.P., Ngan H.Y., Sideri M., Pecorelli S. Carcinoma of the corpus uteri. J. Epidemiol. Biostat. 2001, 6:47-86.
14. Fernandez-Capetillo O., Mahadevaiah S.K., Celeste A., Romanienko P.J., Camerini-Otero R.D., Bonner W.M., Manova K., Burgoyne P., Nussenzweig A. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 2003, 4:497-508.
15. Frodin M., Peraldi P., Van Obberghen E. Cyclic AMP activates the mitogen-activated protein kinase cascade in PC12 cells. J. Biol. Chem. 1994, 269:6207-6214.
16. Garai J., Molnar V., Varga T., Koppan M., Torok A., Bodis J. Endometriosis: harmful survival of an ectopic tissue. Front. Biosci. 2006, 11:595-619.
17. Hajduch M., Havlieek L., Vesely J., Novotny R., Mihal V., Strnad M. Synthetic cyclin dependent kinase inhibitors. New generation of potent anti-cancer drugs. Adv. Exp. Med. Biol. 1999, 457:341-353.
18. Harper J.W., Adami G.R., Wei N., Keyomarsi K., Elledge S.J. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 1993, 75:805-816.
19. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics. CA Cancer J. Clin. 2009, 59:225-249.
20. Ju H.K., Lee H.W., Chung K.S., Choi J.H., Cho J.G., Baek N.I., Chung H.G., Lee K.T. Standardized flavonoid-rich fraction of Artemisia princeps Pampanini cv. Sajabal induces apoptosis via mitochondrial pathway in human cervical cancer HeLa cells. J. Ethnopharmacol. 2012, 141:460-468.
21. Jung U.J., Baek N.I., Chung H.G., Jeong T.S., Lee K.T., Lee M.K., Choi M.S. Antilipogenic and hypolipidemic effects of ethanol extracts from two variants of Artemisia princeps Pampanini in obese diabetic mice. J. Med. Food 2009, 12:1238-1244.
22. Khan M., Rasul A., Yi F., Zhong L., Ma T. Jaceosidin induces p53-dependent G2/M phase arrest in U87 glioblastoma cells. Asian Pac. J. Cancer Prev. 2011, 12:3235-3238.
23. Kim M.J., Kim D.H., Lee K.W., Yoon D.Y., Surh Y.J. Jaceosidin induces apoptosis in ras-transformed human breast epithelial cells through generation of reactive oxygen species. Ann. N. Y. Acad. Sci. 2007, 1095:483-495.
24. Kuo P.L., Hsu Y.L., Cho C.Y. Plumbagin induces G2-M arrest and autophagy by inhibiting the AKT/mammalian target of rapamycin pathway in breast cancer cells. Mol. Cancer Ther. 2006, 5:3209-3221.
25. Lee H.G., Yu K.A., Oh W.K., Baeg T.W., Oh H.C., Ahn J.S., Jang W.C., Kim J.W., Lim J.S., Choe Y.K., Yoon D.Y. Inhibitory effect of jaceosidin isolated from Artemisiaargyi on the function of E6 and E7 oncoproteins of HPV 16. J. Ethnopharmacol. 2005, 98:339-343.
26. Lee S.H., Bae E.A., Park E.K., Shin Y.W., Baek N.I., Han E.J., Chung H.G., Kim D.H. Inhibitory effect of eupatilin and jaceosidin isolated from Artemisia princeps in IgE-induced hypersensitivity. Int. Immunopharmacol. 2007, 7:1678-1684.
27. Lv W., Sheng X., Chen T., Xu Q., Xie X. Jaceosidin induces apoptosis in human ovary cancer cells through mitochondrial pathway. J. Biomed. Biotechnol. 2008, 2008:394802.
28. Matsuoka S., Huang M., Elledge S.J. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998, 282:1893-1897.
29. McKenzie F.R., Pouyssegur J. CAMP-mediated growth inhibition in fibroblasts is not mediated via mitogen-activated protein (MAP) kinase (ERK) inhibition. cAMP-dependent protein kinase induces a temporal shift in growth factor-stimulated MAP kinases. J. Biol. Chem. 1996, 271:13476-13483.
30. Medema R.H., Klompmaker R., Smits V.A., Rijksen G. P21waf1 can block cells at two points in the cell cycle, but does not interfere with processive DNA-replication or stress-activated kinases. Oncogene 1998, 16:431-441.
31. Melchionna R., Chen X.B., Blasina A., McGowan C.H. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat. Cell Biol. 2000, 2:762-765.
32. Min S.W., Kim N.J., Baek N.I., Kim D.H. Inhibitory effect of eupatilin and jaceosidin isolated from Artemisia princeps on carrageenan-induced inflammation in mice. J. Ethnopharmacol. 2009, 125:497-500.
33. Navo M.A., Smith J.A., Gaikwad A., Burke T., Brown J., Ramondetta L.M. In vitro evaluation of the growth inhibition and apoptosis effect of mifepristone (RU486) in human Ishikawa and HEC1A endometrial cancer cell lines. Cancer Chemother. Pharmacol. 2008, 62:483-489.
34. Niculescu A.B., Chen X., Smeets M., Hengst L., Prives C., Reed S.I. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol. Cell. Biol. 1998, 18:629-643.
35. Nugroho A., Lee K.R., Alam M.B., Choi J.S., Park H.J. Isolation and quantitative analysis of peroxynitrite scavengers from Artemisia princeps var. orientalis. Arch. Pharm. Res. 2010, 33:703-708.
36. Nurse P. Universal control mechanism regulating onset of M-phase. Nature 1990, 344:503-508.
37. Ouyang G., Yao L., Ruan K., Song G., Mao Y., Bao S. Genistein induces G2/M cell cycle arrest and apoptosis of human ovarian cancer cells via activation of DNA damage checkpoint pathways. Cell Biol. Int. 2009, 33:1237-1244.
38. Park E.Y., Lee K.W., Lee H.W., Cho Y.W., Baek N.I., Chung H.G., Jeong T.S., Choi M.S., Lee K.T. The ethanol extract from Artemisia princeps Pampanini induces p53-mediated G1 phase arrest in A172 human neuroblastoma cells. J. Med. Food 2008, 11:237-245.
39. Park I., Park K.K., Park J.H., Chung W.Y. Isoliquiritigenin induces G2 and M phase arrest by inducing DNA damage and by inhibiting the metaphase/anaphase transition. Cancer Lett. 2009, 277:174-181.
40. Qiu W., Zhuang S., von Lintig F.C., Boss G.R., Pilz R.B. Cell type-specific regulation of B-Raf kinase by cAMP and 14-3-3 proteins. J. Biol. Chem. 2000, 275:31921-31929.
41. Rabik C.A., Fishel M.L., Holleran J.L., Kasza K., Kelley M.R., Egorin M.J., Dolan M.E. Enhancement of cisplatin [cis-diammine dichloroplatinum (II)] cytotoxicity by O6-benzylguanine involves endoplasmic reticulum stress. J. Pharmacol. Exp. Ther. 2008, 327:442-452.
42. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., Bonner W. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 2002, 12:162-169.
43. Sanchez Y., Amran D., de Blas E., Aller P. Regulation of genistein-induced differentiation in human acute myeloid leukaemia cells (HL60, NB4) Protein kinase modulation and reactive oxygen species generation. Biochem. Pharmacol. 2009, 77:384-396.
44. Sanchez Y., Bachant J., Wang H., Hu F., Liu D., Tetzlaff M., Elledge S.J. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 1999, 286:1166-1171.
45. Sarath V.J., So C.S., Won Y.D., Gollapudi S. Artemisia princeps var orientalis induces apoptosis in human breast cancer MCF-7 cells. Anticancer Res. 2007, 27:3891-3898.
46. Sherr C.J. The Pezcoller lecture: cancer cell cycles revisited. Cancer Res. 2000, 60:3689-3695.
47. Shin S.Y., Hyun J., Yu J.R., Lim Y., Lee Y.H. 5-Methoxyflavanone induces cell cycle arrest at the G2/M phase, apoptosis and autophagy in HCT116 human colon cancer cells. Toxicol. Appl. Pharmacol. 2011, 254:288-298.
48. Stork P.J., Schmitt J.M. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol. 2002, 12:258-266.
49. Takai N., Narahara H. Human endometrial and ovarian cancer cells: histone deacetylase inhibitors exhibit antiproliferative activity, potently induce cell cycle arrest, and stimulate apoptosis. Curr. Med. Chem. 2007, 14:2548-2553.
50. Wei F., Xie Y., Tao L., Tang D. Both ERK1 and ERK2 kinases promote G2/M arrest in etoposide-treated MCF7 cells by facilitating ATM activation. Cell. Signal. 2010, 22:1783-1789.
51. Woerdenbag H.J., Merfort I., Passreiter C.M., Schmidt T.J., Willuhn G., van Uden W., Pras N., Kampinga H.H., Konings A.W. Cytotoxicity of flavonoids and sesquiterpene lactones from Arnica species against the GLC4 and the COLO 320 cell lines. Planta Med. 1994, 60:434-437.
52. Wong S.H., Shih R.S., Schoene N.W., Lei K.Y. Zinc-induced G2/M blockage is p53 and p21 dependent in normal human bronchial epithelial cells. Am. J. Physiol. Cell Physiol. 2008, 294:C1342-1349.
53. Yamamoto N., Kanemoto Y., Ueda M., Kawasaki K., Fukuda I., Ashida H. Anti-obesity and anti-diabetic effects of ethanol extract of Artemisia princeps in C57BL/6 mice fed a high-fat diet. Food Funct. 2011, 2:45-52.
54. Yan Y., Black C.P., Cowan K.H. Irradiation-induced G2/M checkpoint response requires ERK1/2 activation. Oncogene 2007, 26:4689-4698.
55. Young S.W., Dickens M., Tavare J.M. Differentiation of PC12 cells in response to a cAMP analogue is accompanied by sustained activation of mitogen-activated protein kinase. Comparison with the effects of insulin, growth factors and phorbol esters. FEBS Lett. 1994, 338:212-216.