Genistein induces G2/M arrest in gastric cancer cells by increasing the tumor suppressor PTEN expression

Nutrition and Cancer

Volumn 65, Issue 7, 2013, Pages 1034-1041

  Liu, Yan Long ^a   Zhang, Guo Qiang ^a   Yang, Yue ^a   Zhang, Chun Yan ^a   Fu, Rong Xia ^b   Yang, Yan Mei ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b TIANJIN AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GENISTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CONTROLLED STUDY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; STOMACH CANCER; UPREGULATION;

GLYCINE MAX;

CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL DIVISION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN B; DOWN-REGULATION; G2 PHASE; GENISTEIN; HUMANS; NUCLEAR PROTEINS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RNA, SMALL INTERFERING; STOMACH NEOPLASMS; UP-REGULATION;

EID: 84888350043     PISSN: 01635581     EISSN: 15327914     Source Type: Journal    
DOI: 10.1080/01635581.2013.810290     Document Type: Article

References (54)

1. Messina M, Nagata C, and Wu AH: Estimated Asian adult soy protein and isoflavone intakes. Nutr Cancer 55, 1-12, 2006.
2. Banerjee S, Li Y,Wang Z, and Sarkar FH: Multi-targeted therapy of cancer by genistein. Cancer Lett 269, 226-242, 2008.
3. Li Y and Sarkar FH: Inhibition of nuclear factor kappaB activation in PC3 cells by genistein is mediated via Akt signaling pathway. Clin Cancer Res 8, 2369-2377, 2002.
4. Yuan-Jing F, Nan-Shan H, and Lian X: Genistein synergizes with RNA interference inhibiting survivin for inducing DU-145 of prostate cancer cells to apoptosis. Cancer Lett 284, 189-197, 2009.
5. Frey RS, Li J, and Singletary KW: Effects of genistein on cell proliferation and cell cycle arrest in nonneoplastic human mammary epithelial cells: involvement of Cdc2, p21(waf/cip1), p27(kip1), and Cdc25C expression. Biochem Pharmacol 61, 979-989, 2001.
6. Chang KL, Kung ML, Chow NH, and Su SJ: Genistein arrests hepatoma cells at G2/M phase: involvement of ATM activation and upregulation of p21waf1/cip1 and Wee1. Biochem Pharmacol 67, 717-726, 2004.
7. Ouyang G, Yao L, Ruan K, Song G, Mao Y, et al.: Genistein induces G2/M cell cycle arrest and apoptosis of human ovarian cancer cells via activation of DNA damage checkpoint pathways. Cell Biol Int 33, 1237-1244, 2009.
8. Zhao R, Xiang N, Domann FE, and Zhong W: Effects of selenite and genistein on G2/M cell cycle arrest and apoptosis in human prostate cancer cells. Nutr Cancer 61, 397-407, 2009.
9. Park CE, Yun H, Lee EB, Min BI, Bae H, et al.: The antioxidant effects of genistein are associated with AMP-activated protein kinase activation and PTEN induction in prostate cancer cells. J Med Food 13, 815-820, 2010.
10. Rahal OM and Simmen RC: PTEN and p53 cross-regulation induced by soy isoflavone genistein promotes mammary epithelial cell cycle arrest and lobuloalveolar differentiation. Carcinogenesis 31, 1491-1500, 2010.
11. Elledge SJ: Cell cycle checkpoints: preventing an identity crisis. Science 274, 1664-1672, 1996.
12. Nigg EA: Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2, 21-32, 2001.
13. Okumura E, Fukuhara T, Yoshida H, Hanada Si S, Kozutsumi R, et al.: Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat Cell Biol 4, 111-116, 2002.
14. McGowan CHand Russell P: Cell cycle regulation of human WEE1.EMBO J 14, 2166-2175, 1995.
15. Gautier J, Solomon MJ, Booher RN, Bazan JF, and Kirschner MW: cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67, 197-211, 1991.
16. Chu EC and Tarnawski AS: PTEN regulatory functions in tumor suppression and cell biology. Med Sci Monit 10, RA235-RA241, 2004.
17. Xu X, Zhang Y, Qu D, Jiang T, and Li S: Osthole induces G2/M arrest and apoptosis in lung cancer A549 cells by modulating PI3K/Akt pathway. J Exp Clin Cancer Res 30, 33, 2011.
18. Lim WT, Zhang WH, Miller CR, Watters JW, Gao F, et al.: PTEN and phosphorylated AKT expression and prognosis in early-and late-stage non-small cell lung cancer. Oncol Rep 17, 853-857, 2007.
19. Sawai H, Yasuda A, Ochi N, Ma J, Matsuo Y, et al.: Loss of PTEN expression is associated with colorectal cancer liver metastasis and poor patient survival. BMC Gastroenterol 8, 56, 2008.
20. Pandolfi PP: Breast cancer-loss of PTEN predicts resistance to treatment. N Engl J Med 351, 2337-2338, 2004.
21. Warde N: Prostate cancer: loss of PTEN promotes progression of prostate cancer in an androgen-independent manner. Nat Rev Urol 8, 412, 2011.
22. Chow LM and Baker SJ: PTEN function in normal and neoplastic growth. Cancer Lett 241, 184-196, 2006.
23. Kandel ES, Skeen J, Majewski N, Di Cristofano A, Pandolfi PP, et al.: Activation of Akt/protein kinase B overcomes a G(2)/m cell cycle checkpoint induced by DNA damage. Mol Cell Biol 22, 7831-7841, 2002.
24. Arafa el SA, Zhu Q, Shah ZI, Wani G, Barakat BM, et al.: Thymoquinone up-regulates PTEN expression and induces apoptosis in doxorubicinresistant human breast cancer cells. Mutat Res 706, 28-35, 2011.
25. Saito Y, Swanson X, Mhashilkar AM, Oida Y, Schrock R, et al.: Adenovirus-mediated transfer of the PTEN gene inhibits human colorectal cancer growth in vitro and in vivo. Gene Ther 10, 1961-1969, 2003.
26. Hang Y, Zheng YC, Cao Y, Li QS, and Sui YJ: Suppression of gastric cancer growth by adenovirus-mediated transfer of the PTEN gene. World J Gastroenterol 11, 2224-2229, 2005.
27. Zhang Y, Chen LH, Wang L, Wang HM, Zhang YW, et al.: Radiationinducible PTEN expression radiosensitises hepatocellular carcinoma cells. Int J Radiat Biol 86, 964-974, 2010.
28. KatayamaK, Fujita N, and Tsuruo T:Akt/protein kinase B-dependent phosphorylation and inactivation ofWEE1Hu promote cell cycle progression at G2/M transition. Mol Cell Biol 25, 5725-5737, 2005.
29. Weir NM, Selvendiran K, Kutala VK, Tong L, Vishwanath S, et al.: Curcumin induces G2/M arrest and apoptosis in cisplatin-resistant human ovarian cancer cells by modulating Akt and p38 MAPK. Cancer Biol Ther 6, 178-184, 2007.
30. Du HP, Shen JK, Yang M, Wang YQ, Yuan XQ, et al.: 4-Chlorobenzoyl berbamine induces apoptosis and G2/M cell cycle arrest through the PI3K/Akt and NF-kappaB signal pathway in lymphoma cells. Oncol Rep 23, 709-716, 2010.
31. Huang SM, Yang JS, Tsai SC, Chen MH, Hsu MH, et al.: The novel synthesized 2-(3-(methylamino)phenyl)-6-(pyrrolidin-1-yl)quinolin-4-one (Smh-3) compound induces G2/M phase arrest and mitochondrial-dependent apoptotic cell death through inhibition of CDK1 and AKT activity in HL-60 human leukemia cells. Int J Oncol 38, 1357-1364, 2011.
32. Zhou HB, Chen JJ, Wang WX, Cai JT, and Du Q: Apoptosis of human primary gastric carcinoma cells induced by genistein.World J Gastroenterol 10, 1822-1825, 2004.
33. Cui HB, Na XL, Song DF, and Liu Y: Blocking effects of genistein on cell proliferation and possible mechanism in human gastric carcinoma. World J Gastroenterol 11, 69-72, 2005.
34. Zhou HB, Chen JM, Cai JT, Du Q and Wu CN: Anticancer activity of genistein on implanted tumor of human SG7901 cells in nude mice. World J Gastroenterol 14, 627-631, 2008.
35. Kim HJ, Chang WK, Kim MK, Lee SS, and Choi BY: Dietary factors and gastric cancer in Korea: a case-control study. Int J Cancer 97, 531-535, 2002.
36. Wu AH, Yang D, and Pike MC: A meta-analysis of soyfoods and risk of stomach cancer: the problem of potential confounders. Cancer Epidemiol Biomarkers Prev 9, 1051-1058, 2000.
37. Nagata C, Takatsuka N, Kawakami N, and Shimizu H: A prospective cohort study of soy product intake and stomach cancer death. Br J Cancer 87, 31-36, 2002.
38. Ito LS, Inoue M, Tajima K, Yamamura Y, Kodera Y, et al.: Dietary factors and the risk of gastric cancer among Japanese women: a comparison between the differentiated and non-differentiated subtypes. Ann Epidemiol 13, 24-31, 2003.
39. Sauvaget C, Lagarde F, Nagano J, Soda M, Koyama K, et al.: Lifestyle factors, radiation and gastric cancer in atomic-bomb survivors (Japan). Cancer Causes Control 16, 773-780, 2005.
40. Bowey E,Adlercreutz H, and Rowland I:Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human flora associated rats. Food Chem Toxicol 41, 631-636, 2003.
41. Ko KP, Park SK, Park B, Yang JJ, Cho LY, et al.: Isoflavones from phytoestrogens and gastric cancer risk: a nested case-control study within the Korean Multicenter Cancer Cohort. Cancer Epidemiol Biomarkers Prev 19, 1292-1300, 2010.
42. Touny LH and Banerjee PP: Identification of both Myt-1 and Wee-1 as necessary mediators of the p21-independent inactivation of the cdc-2/cyclin B1 complex and growth inhibition of TRAMP cancer cells by genistein. Prostate 66, 1542-1555, 2006.
43. Li Z, Li J, Mo B, Hu C, Liu H, et al.: Genistein induces G2/M cell cycle arrest via stable activation of ERK1/2 pathway in MDA-MB-231 breast cancer cells. Cell Biol Toxicol 24, 401-409, 2008.
44. Mukherjee S, Acharya BR, Bhattacharyya B, and Chakrabarti G: Genistein arrests cell cycle progression of A549 cells at the G(2)/M phase and depolymerizes interphase microtubules through binding to a unique site of tubulin. Biochemistry 49, 1702-1712, 2010.
45. Han H, Zhong C, Zhang X, Liu R, Pan M, et al.: Genistein induces growth inhibition and G2/M arrest in nasopharyngeal carcinoma cells. Nutr Cancer 62, 641-647, 2010.
46. Selvendiran K, Tong L, Vishwanath S, Bratasz A, Trigg NJ, et al.: EF24 induces G2/M arrest and apoptosis in cisplatin-resistant human ovarian cancer cells by increasing PTEN expression. J Biol Chem 282, 28609-28618, 2007.
47. Cao F, Jin TY, and Zhou YF: Inhibitory effect of isoflavones on prostate cancer cells and PTEN gene. Biomed Environ Sci 19, 35-41, 2006.
48. Wu DD, Feng C, Xu XY, Xiao JY, Liu C, et al.: Protein kinase B/Akt may regulate G2/M transition in the fertilized mouse egg by changing the localization of p21(Cip1/WAF1). Cell Biochem Funct 29, 265-271, 2011.
49. Tonic I, Yu WN, Park Y, Chen CC, and Hay N: Akt activation emulates Chk1 inhibition and Bcl2 overexpression and abrogates G2 cell cycle checkpoint by inhibiting BRCA1 foci. J Biol Chem 285, 23790-23798, 2010.
50. McGowan CH and Russell P: Human Wee1 kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15. EMBO J 12, 75-85, 1993.
51. Taylor WR and Stark GR: Regulation of the G2/M transition by p53. Oncogene 20, 1803-1815, 2001.
52. Ismail IA, Kang KS, Lee HA, Kim JW, and Sohn YK: Genistein-induced neuronal apoptosis and G2/M cell cycle arrest is associated with MDC1 up-regulation and PLK1 down-regulation. Eur J Pharmacol 575, 12-20, 2007.
53. Raffoul JJ, Wang Y, Kucuk O, Forman JD, Sarkar FH, et al.: Genistein inhibits radiation-induced activation of NF-kappaB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer 6, 107, 2006.
54. Kikuno N, Shiina H, Urakami S, Kawamoto K, Hirata H, et al.: Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells. Int J Cancer 123, 552-560, 2008.