Kaempferol induces G2/M cell cycle arrest via checkpoint kinase 2 and promotes apoptosis via death receptors in human ovarian carcinoma A2780/CP70 Cells

Molecules

Volumn 23, Issue 5, 2018, Pages

  Gao, Ying ^a   Yin, Junfeng ^a   Rankin, Gary O ^b   Chen, Yi Charlie ^c  

^a BEIJING HOSPITAL   (China)

^b MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Alderson Broaddus College   (United States)

Author keywords

Apoptosis; Cell cycle arrest; Chk2; DR5; Fas; Kaempferol

Indexed keywords

ANTINEOPLASTIC AGENT; CASP8 PROTEIN, HUMAN; CASPASE 8; CDC25C PROTEIN, HUMAN; CDK1 PROTEIN, HUMAN; CHECKPOINT KINASE 2; CHEK2 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DEATH RECEPTOR; FADD PROTEIN, HUMAN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; KAEMPFEROL; KAEMPFEROL DERIVATIVE; PROTEIN TYROSINE PHOSPHATASE;

APOPTOSIS; DRUG EFFECT; EPITHELIUM CELL; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; OVARY; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CASPASE 8; CDC2 PROTEIN KINASE; CDC25 PHOSPHATASES; CELL LINE, TUMOR; CHECKPOINT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P21; EPITHELIAL CELLS; FAS-ASSOCIATED DEATH DOMAIN PROTEIN; FEMALE; G2 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KAEMPFEROLS; OVARY; RECEPTORS, DEATH DOMAIN; SIGNAL TRANSDUCTION;

EID: 85046634267     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules23051095     Document Type: Article

References (44)

1. Calderon-Montano, J.M.; Burgos-Moron, E.; Perez-Guerrero, C.; Lopez-Lazaro, M. A review on the dietary flavonoid kaempferol. Mini. Rev. Med. Chem. 2011, 11, 298–344. [CrossRef] [PubMed]
2. Gates, M.A.; Tworoger, S.S.; Hecht, J.L.; De Vivo, I.; Rosner, B.; Hankinson, S.E. A prospective study of dietary flavonoid intake and incidence of epithelial ovarian cancer. Int. J Cancer 2007, 121, 2225–2232. [CrossRef] [PubMed]
3. Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer statistics, 2018. CA Cancer J. Clin. 2018, 68, 7–30. [CrossRef] [PubMed]
4. Mizuno, T.; Suzuki, N.; Makino, H.; Furui, T.; Morii, E.; Aoki, H.; Kunisada, T.; Yano, M.; Kuji, S.; Hirashima, Y.; et al. Cancer stem-like cells of ovarian clear cell carcinoma are enriched in the aldh-high population associated with an accelerated scavenging system in reactive oxygen species. Gynecol. Oncol. 2015, 137, 299–305. [CrossRef] [PubMed]
5. Kao, Y.L.; Kuo, Y.M.; Lee, Y.R.; Yang, S.F.; Chen, W.R.; Lee, H.J. Apple polyphenol induces cell apoptosis, cell cycle arrest at g2/m phase, and mitotic catastrophe in human bladder transitional carcinoma cells. J. Funct. Foods 2015, 14, 384–394. [CrossRef]
6. Ravishankar, D.; Rajora, A.K.; Greco, F.; Osborn, H.M. Flavonoids as prospective compounds for anti-cancer therapy. Int. J. Biochem. Cell Biol. 2013, 45, 2821–2831. [CrossRef] [PubMed]
7. Romagnolo, D.F.; Selmin, O.I. Flavonoids and cancer prevention: A review of the evidence. J. Nutr. Gerontol. Geriatr. 2012, 31, 206–238. [CrossRef] [PubMed]
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. [CrossRef] [PubMed]
9. Hsu, Y.L.; Uen, Y.H.; Chen, Y.; Liang, H.L.; Kuo, P.L. Tricetin, a dietary flavonoid, inhibits proliferation of human breast adenocarcinoma mcf-7 cells by blocking cell cycle progression and inducing apoptosis. J. Agric. Food Chem. 2009, 57, 8688–8695. [CrossRef] [PubMed]
10. Hung, J.Y.; Hsu, Y.L.; Ko, Y.C.; Tsai, Y.M.; Yang, C.J.; Huang, M.S.; Kuo, P.L. Didymin, a dietary flavonoid glycoside from citrus fruits, induces fas-mediated apoptotic pathway in human non-small-cell lung cancer cells in vitro and in vivo. Lung Cancer 2010, 68, 366–374. [CrossRef] [PubMed]
11. Horinaka, M.; Yoshida, T.; Shiraishi, T.; Nakata, S.; Wakada, M.; Nakanishi, R.; Nishino, H.; Matsui, H.; Sakai, T. Luteolin induces apoptosis via death receptor 5 upregulation in human malignant tumor cells. Oncogene 2005, 24, 7180–7189. [CrossRef] [PubMed]
12. Bartek, J.; Lukas, J. Chk1 and chk2 kinases in checkpoint control and cancer. Cancer Cell 2003, 3, 421–429. [CrossRef]
13. Hirao, A.; Cheung, A.; Duncan, G.; Girard, P.M.; Elia, A.J.; Wakeham, A.; Okada, H.; Sarkissian, T.; Wong, J.A.; Sakai, T.; et al. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (atm)-dependent and an atm-independent manner. Mol. Cell. Biol. 2002, 22, 6521–6532. [CrossRef] [PubMed]
14. Stolz, A.; Ertych, N.; Bastians, H. Tumor suppressor chk2: Regulator of DNA damage response and mediator of chromosomal stability. Clin. Cancer Res. 2011, 17, 401–405. [CrossRef] [PubMed]
15. Guicciardi, M.E.; Gores, G.J. Life and death by death receptors. FASEB J. 2009, 23, 1625–1637. [CrossRef] [PubMed]
16. Lavrik, I.; Golks, A.; Krammer, P.H. Death receptor signaling. J. Cell Sci. 2005, 118, 265–267. [CrossRef] [PubMed]
17. Debatin, K.M.; Krammer, P.H. Death receptors in chemotherapy and cancer. Oncogene 2004, 23, 2950–2966. [CrossRef] [PubMed]
18. Friesen, C.; Herr, I.; Krammer, P.H.; Debatin, K.M. Involvement of the cd95 (apo-1/fas) receptor/ligand system in drug-induced apoptosis in leukemia cells. Nat. Med. 1996, 2, 574–577. [CrossRef] [PubMed]
19. Parajuli, B.; Shin, S.J.; Kwon, S.H.; Cha, S.D.; Chung, R.; Park, W.J.; Lee, H.G.; Cho, C.H. Salinomycin induces apoptosis via death receptor-5 up-regulation in cisplatin-resistant ovarian cancer cells. Anticancer Res. 2013, 33, 1457–1462. [PubMed]
20. Shankar, S.; Ganapathy, S.; Chen, Q.; Srivastava, R.K. Curcumin sensitizes trail-resistant xenografts: Molecular mechanisms of apoptosis, metastasis and angiogenesis. Mol. Cancer 2008, 7, 16. [CrossRef] [PubMed]
21. Luo, H.; Rankin, G.O.; Li, Z.; Depriest, L.; Chen, Y.C. Kaempferol induces apoptosis in ovarian cancer cells through activating p53 in the intrinsic pathway. Food Chem. 2011, 128, 513–519. [CrossRef] [PubMed]
22. Luo, H.; Rankin, G.O.; Juliano, N.; Jiang, B.H.; Chen, Y.C. Kaempferol inhibits vegf expression and in vitro angiogenesis through a novel erk-nfkappab-cmyc-p21 pathway. Food Chem. 2012, 130, 321–328. [CrossRef] [PubMed]
23. Aliouat-Denis, C.M.; Dendouga, N.; van den Wyngaert, I.; Goehlmann, H.; Steller, U.; van de Weyer, I.; van Slycken, N.; Andries, L.; Kass, S.; Luyten, W.; et al. P53-independent regulation of p21waf1/cip1 expression and senescence by chk2. Mol. Cancer Res. 2005, 3, 627–634. [CrossRef] [PubMed]
24. Yu, D.; Jing, T.; Liu, B.; Yao, J.; Tan, M.; McDonnell, T.J.; Hung, M.C. Overexpression of erbb2 blocks taxol-induced apoptosis by upregulation of p21cip1, which inhibits p34cdc2 kinase. Mol. Cell 1998, 2, 581–591. [CrossRef]
25. Renehan, A.G.; Booth, C.; Potten, C.S. What is apoptosis, and why is it important? BMJ 2001, 322, 1536–1538. [CrossRef] [PubMed]
26. Hirao, A.; Kong, Y.Y.; Matsuoka, S.; Wakeham, A.; Ruland, J.; Yoshida, H.; Liu, D.; Elledge, S.J.; Mak, T.W. DNA damage-induced activation of p53 by the checkpoint kinase chk2. Science 2000, 287, 1824–1827. [CrossRef] [PubMed]
27. Jack, M.T.; Woo, R.A.; Hirao, A.; Cheung, A.; Mak, T.W.; Lee, P.W. Chk2 is dispensable for p53-mediated g1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA 2002, 99, 9825–9829. [CrossRef] [PubMed]
28. Hollstein, M.; Sidransky, D.; Vogelstein, B.; Harris, C.C. P53 mutations in human cancers. Science 1991, 253, 49–53. [CrossRef] [PubMed]
29. Nevanlinna, H.; Bartek, J. The chek2 gene and inherited breast cancer susceptibility. Oncogene 2006, 25, 5912–5919. [CrossRef] [PubMed]
30. Zannini, L.; Delia, D.; Buscemi, G. Chk2 kinase in the DNA damage response and beyond. J. Mol. Cell Biol. 2014, 6, 442–457. [CrossRef] [PubMed]
31. Huang, H.; Hu, M.; Zhao, R.; Li, P.; Li, M. Dihydromyricetin suppresses the proliferation of hepatocellular carcinoma cells by inducing g2/m arrest through the chk1/chk2/cdc25c pathway. Oncol. Rep. 2013, 30, 2467–2475. [CrossRef] [PubMed]
32. Choi, Y.H.; Zhang, L.; Lee, W.H.; Park, K.Y. Genistein-induced g2/m arrest is associated with the inhibition of cyclin b1 and the induction of p21 in human breast carcinoma cells. Int. J. Oncol. 1998, 13, 391–396. [CrossRef] [PubMed]
33. Kim, K.Y.; Jang, W.Y.; Lee, J.Y.; Jun, D.Y.; Ko, J.Y.; Yun, Y.H.; Kim, Y.H. Kaempferol activates g(2)-checkpoint of the cell cycle resulting in g(2)-arrest and mitochondria-dependent apoptosis in human acute leukemia jurkat t cells. J. Microbiol. Biotechnol. 2016, 26, 287–294. [CrossRef] [PubMed]
34. Camidge, D.R.; Herbst, R.S.; Gordon, M.S.; Eckhardt, S.G.; Kurzrock, R.; Durbin, B.; Ing, J.; Tohnya, T.M.; Sager, J.; Ashkenazi, A.; et al. A phase i safety and pharmacokinetic study of the death receptor 5 agonistic antibody pro95780 in patients with advanced malignancies. Clin. Cancer Res. 2010, 16, 1256–1263. [CrossRef] [PubMed]
35. LaVallee, T.M.; Zhan, X.H.; Johnson, M.S.; Herbstritt, C.J.; Swartz, G.; Williams, M.S.; Hembrough, W.A.; Green, S.J.; Pribluda, V.S. 2-methoxyestradiol up-regulates death receptor 5 and induces apoptosis through activation of the extrinsic pathway. Cancer Res. 2003, 63, 468–475. [PubMed]
36. Wilson, N.S.; Yang, A.; Yang, B.; Couto, S.; Stern, H.; Gogineni, A.; Pitti, R.; Marsters, S.; Weimer, R.M.; Singh, M.; et al. Proapoptotic activation of death receptor 5 on tumor endothelial cells disrupts the vasculature and reduces tumor growth. Cancer Cell 2012, 22, 80–90. [CrossRef] [PubMed]
37. Oh, Y.T.; Yue, P.; Wang, D.; Tong, J.S.; Chen, Z.G.; Khuri, F.R.; Sun, S.Y. Suppression of death receptor 5 enhances cancer cell invasion and metastasis through activation of caspase-8/traf2-mediated signaling. Oncotarget 2015, 6, 41324–41338. [CrossRef] [PubMed]
38. Xu, L.H.; Deng, C.S.; Zhu, Y.Q.; Liu, S.Q.; Liu, D.Z. Synergistic antitumor effect of trail and doxorubicin on colon cancer cell line sw480. World J. Gastroenterol. 2003, 9, 1241–1245. [CrossRef] [PubMed]
39. Li, Y.; Fan, X.; Goodwin, C.R.; Laterra, J.; Xia, S. Hepatocyte growth factor enhances death receptor-induced apoptosis by up-regulating dr5. BMC Cancer 2008, 8, 325. [CrossRef] [PubMed]
40. Lee, H.S.; Cho, H.J.; Yu, R.; Lee, K.W.; Chun, H.S.; Park, J.H. Mechanisms underlying apoptosis-inducing effects of kaempferol in ht-29 human colon cancer cells. Int. J. Mol. Sci. 2014, 15, 2722–2737. [CrossRef] [PubMed]
41. Yoshida, T.; Konishi, M.; Horinaka, M.; Yasuda, T.; Goda, A.E.; Taniguchi, H.; Yano, K.; Wakada, M.; Sakai, T. Kaempferol sensitizes colon cancer cells to trail-induced apoptosis. Biochem. Biophys. Res. Commun. 2008, 375, 129–133. [CrossRef] [PubMed]
42. Lee, C.F.; Yang, J.S.; Tsai, F.J.; Chiang, N.N.; Lu, C.C.; Huang, Y.S.; Chen, C.; Chen, F.A. Kaempferol induces atm/p53-mediated death receptor and mitochondrial apoptosis in human umbilical vein endothelial cells. Int. J. Oncol. 2016, 48, 2007–2014. [CrossRef] [PubMed]
43. Zhao, Y.; Tian, B.; Wang, Y.; Ding, H. Kaempferol sensitizes human ovarian cancer cells-ovcar-3 and skov-3 to tumor necrosis factor-related apoptosis-inducing ligand (trail)-induced apoptosis via jnk/erk-chop pathway and up-regulation of death receptors 4 and 5. Med. Sci. Monit. 2017, 23, 5096–5105. [CrossRef] [PubMed]
44. Gao, Y.; Rankin, G.O.; Tu, Y.; Chen, Y.C. Theaflavin-3, 3’-digallate decreases human ovarian carcinoma ovcar-3 cell-induced angiogenesis via akt and notch-1 pathways, not via mapk pathways. Int. J. Oncol. 2016, 48, 281–292. [CrossRef] [PubMed]