Melatonin induces transcriptional regulation of Bim by FoxO3a in HepG2 cells

British Journal of Cancer

Volumn 108, Issue 2, 2013, Pages 442-449

  Carbajo Pescador, S ^a   Steinmetz, C ^b   Kashyap, A ^b   Lorenz, S ^b   Mauriz, J L ^a   Heise, M ^b   Galle, P R ^b   Gonzalez Gallego J ^a   Strand, S ^b  

^a UNIVERSITY OF LEÓN   (Spain)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Bim; FoxO3a; Hepatocellular carcinoma; Melatonin

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; MELATONIN; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHRL1;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL STRAIN HEPG2; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG CYTOTOXICITY; GENE SILENCING; HEPATOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VITRO STUDY; LIVER CANCER; LIVER CELL; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSACTIVATION; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BINDING SITES; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; FORKHEAD TRANSCRIPTION FACTORS; HEP G2 CELLS; HEPATOCYTES; HUMANS; MELATONIN; MEMBRANE PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84873743356     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2012.563     Document Type: Article

References (60)

1. Anton S, Melville L, Rena G (2007) Epigallocatechin gallate (EGCG) mimics insulin action on the transcription factor FOXO1a and elicits cellular responses in the presence and absence of insulin. Cell Signal 19: 378-383. (Pubitemid 44969987)
2. Barthel A, Schmoll D, Unterman TG (2005) FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab 16: 183-189. (Pubitemid 40603098)
3. Bhalla S, Evens AM, Dai B, Prachand S, Gordon LI, Gartenhaus RB (2011) The novel anti-MEK small molecule AZD6244 induces BIM-dependent and AKT-independent apoptosis in diffuse large B-cell lymphoma. Blood 118: 1052-1061.
4. Boreddy SR, Pramanik KC, Srivastava SK (2011) Pancreatic tumour suppression by benzyl isothiocyanate is associated with inhibition of PI3K/AKT/FOXO pathway. Clin Cancer Res 17: 1784-1795.
5. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, HüLS, Anderson MJ, Arden KC, Blenis J, Greenberg ME (1999) Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96: 857-868. (Pubitemid 29165088)
6. Burgering BM, Kops GJ (2002) Cell cycle and death control: Long live forkheads. Trends Biochem Sci 27: 352-360. (Pubitemid 34756518)
7. Cabrera J, Negrin G, Estevez F, Loro J, Reiter RJ, Quintana J (2010) Melatonin decreases cell proliferation and induces melanogenesis in human melanoma SK-MEL-1 cells. J Pineal Res 49: 45-54.
8. Calnan DR, Brunet A (2008) The FoxO code. Oncogene 27: 2276-2288. (Pubitemid 351501779)
9. Carbajo-Pescador S, Garcia-Palomo A, Martin-Renedo J, Piva M, Gonzalez-Gallego J, Mauriz JL (2011) Melatonin modulation of intracellular signaling pathways in hepatocarcinoma HepG2 cell line: Role of the MT1 receptor. J Pineal Res 51: 463-471.
10. Carbajo-Pescador S, Martin-Renedo J, Garcia-Palomo A, Tunon MJ, Mauriz JL, Gonzalez-Gallego J (2009) Changes in the expression of melatonin receptors induced by melatonin treatment in hepatocarcinoma HepG2 cells. J Pineal Res 47: 330-338.
11. Chen Q, Ganapathy S, Singh KP, Shankar S, Srivastava RK (2010) Resveratrol induces growth arrest and apoptosis through activation of FOXO transcription factors in prostate cancer cells. PLoS One 5: E15288.
12. ChiüCC, Chen JY, Lin KL, Huang CJ, Lee JC, Chen BH, Chen WY, Lo YH, Chen YL, Tseng CH, Chen YL, Lin SR (2010) p38 MAPK and NF-kappaB pathways are involved in naphtho[1,2-b] furan-4,5-dione induced antiproliferation and apoptosis of human hepatoma cells. Cancer Lett 295: 92-99.
13. Cini G, Neri B, Pacini A, Cesati V, Sassoli C, Quattrone S, D'Apolito M, Fazio A, Scapagnini G, Provenzani A, Quattrone A (2005) Antiproliferative activity of melatonin by transcriptional inhibition of cyclin D1 expression: A molecular basis for melatonin-induced oncostatic effects. J Pineal Res 39: 12-20. (Pubitemid 40966457)
14. Cornella H, Alsinet C, Villanueva A (2011) Molecular Pathogenesis of Hepatocellular Carcinoma. Alcohol Clin Exp Res 35: 821-825.
15. Cutando A, Aneiros-Fernandez J, Aneiros-Cachaza J, Arias-Santiago S (2011) Melatonin and cancer: Current knowledge and its application to oral cavity tumours. J Oral Pathol Med 40: 593-597.
16. Denizot F, Lang R (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89: 271-277. (Pubitemid 16080782)
17. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ (2000) Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 10: 1201-1204.
18. El-Serag HB (2011) Hepatocellular carcinoma. N Engl J Med 365: 1118-1127.
19. Ewings KE, Wiggins CM, Cook SJ (2007) Bim and the pro-survival Bcl-2 proteins: Opposites attract, ERK repels. Cell Cycle 6: 2236-2240. (Pubitemid 47547699)
20. Fan LL, Sun GP, Wei W, Wang ZG, Ge L, FüWZ, Wang H (2010) Melatonin and doxorubicin synergistically induce cell apoptosis in human hepatoma cell lines. World J Gastroenterol 16: 1473-1481.
21. Farriol M, Venereo Y, Orta X, Castellanos JM, Segovia-Silvestre T (2000) In vitro effects of melatonin on cell proliferation in a colon adenocarcinoma line. J Appl Toxicol 20: 21-24. (Pubitemid 30093182)
22. Fei M, Zhao Y, Wang Y, LüM, Cheng C, Huang X, Zhang D, LüJ, He S, Shen A (2009) Low expression of Foxo3a is associated with poor prognosis in ovarian cancer patients. Cancer Invest 27: 52-59.
23. Fernandez de Mattos S, Villalonga P, Clardy J, Lam EW (2008) FOXO3a mediates the cytotoxic effects of cisplatin in colon cancer cells. Mol Cancer Ther 7: 3237-3246.
24. Futagami M, Sato S, Sakamoto T, Yokoyama Y, Saito Y (2001) Effects of melatonin on the proliferation and cis-diamminedichloroplatinum (CDDP) sensitivity of cultured human ovarian cancer cells. Gynecol Oncol 82: 544-549. (Pubitemid 32826457)
25. Garcia-Navarro A, Gonzalez-Puga C, Escames G, Lopez LC, Lopez A, Lopez-Cantarero M, Camacho E, Espinosa A, Gallo MA, Acuna-Castroviejo D (2007) Cellular mechanisms involved in the melatonin inhibition of HT-29 human colon cancer cell proliferation in culture. J Pineal Res 43: 195-205. (Pubitemid 47078925)
26. Garcia-Santos G, Antolin I, Herrera F, Martin V, Rodriguez-Blanco J, del Pilar Carrera M, Rodriguez C (2006) Melatonin induces apoptosis in human neuroblastoma cancer cells. J Pineal Res 41: 130-135. (Pubitemid 44141747)
27. Gonzalez A, Del Castillo-Vaquero A, Miro-Moran A, Tapia JA, Salido GM (2010) Melatonin reduces pancreatic tumour cell viability by altering mitochondrial physiology. J Pineal Res 50: 250-260.
28. Hill SM, Blask DE (1988) Effects of the pineal hormone melatonin on the proliferation and morphological characteristics of human breast cancer cells (MCF-7) in culture. Cancer Res 48: 6121-6126. (Pubitemid 18266811)
29. Hong ZY, Lee HJ, Shin DY, Kim SK, Seo M, Lee EJ (2012) Inhibition of Akt/FOXO3a signaling by constitutively active FOXO3a suppresses growth of follicular thyroid cancer cell lines. Cancer Lett 314: 34-40.
30. Hsieh TC, Wang Z, Hamby CV, WüJM (2005) Inhibition of melanoma cell proliferation by resveratrol is correlated with upregulation of quinone reductase 2 and p53. Biochem Biophys Res Commun 334: 223-230. (Pubitemid 40978529)
31. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
32. Jin GS, Kondo E, Miyake T, Shibata M, Takashima T, LiüYX, Hayashi K, Akagi T, Yoshino T (2004) Expression and intracellular localization of FKHRL1 in mammary gland neoplasms. Acta Med Okayama 58: 197-205. (Pubitemid 39277936)
33. Leja-Szpak A, Jaworek J, Pierzchalski P, Reiter RJ (2010) Melatonin induces pro-apoptotic signaling pathway in human pancreatic carcinoma cells (PANC-1). J Pineal Res 49: 248-255.
34. Lin K, Dorman JB, Rodan A, Kenyon C (1997) Daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319-1322. (Pubitemid 27495748)
35. Martin-Renedo J, Mauriz JL, Jorquera F, Ruiz-Andres O, Gonzalez P, Gonzalez-Gallego J (2008) Melatonin induces cell cycle arrest and apoptosis in hepatocarcinoma HepG2 cell line. J Pineal Res 45: 532-540.
36. Mu?ller M, Strand S, Hug H, Heinemann EM, Walczak H, Hofmann WJ, Stremmel W, Krammer PH, Galle PR (1997) Drug-induced apoptosis in hepatoma cells is mediated by the CD95 (APO-1/Fas) receptor/ligand system and involves activation of wild-type p53. J Clin Invest 99: 403-413. (Pubitemid 27414797)
37. Notas G, Nifli AP, Kampa M, Vercauteren J, Kouroumalis E, Castanas E (2006) Resveratrol exerts its antiproliferative effect on HepG2 hepatocellular carcinoma cells, by inducing cell cycle arrest, and NOS activation. Biochim Biophys Acta 1760: 1657-1666. (Pubitemid 44667277)
38. Oz E, Ilhan MN (2006) Effects of melatonin in reducing the toxic effects of doxorubicin. Mol Cell Biochem 286: 11-15.
39. Pan M, Song YL, XüJM, Gan HZ (2006) Melatonin ameliorates nonalcoholic fatty liver induced by high-fat diet in rats. J Pineal Res 41: 79-84. (Pubitemid 43980699)
40. Papazisis KT, Kouretas D, Geromichalos GD, Sivridis E, Tsekreli OK, Dimitriadis KA, Kortsaris AH (1998) Effects of melatonin on proliferation of cancer cell lines. J Pineal Res 25: 211-218. (Pubitemid 29029898)
41. Paroni G, Fratelli M, Gardini G, Bassano C, Flora M, Zanetti A, Guarnaccia V, Ubezio P, Centritto F, Terao M, Garattini E (2011) Synergistic antitumor activity of lapatinib and retinoids on a novel subtype of breast cancer with coamplification of ERBB2 and RARA. Oncogene.
42. Petranka J, Baldwin W, Biermann J, Jayadev S, Barrett JC, Murphy E (1999) The oncostatic action of melatonin in an ovarian carcinoma cell line. J Pineal Res 26: 129-136. (Pubitemid 29183115)
43. Ren D, TüHC, Kim H, Wang GX, Bean GR, Takeuchi O, Jeffers JR, Zambetti GP, Hsieh JJ, Cheng EH (2010) BID, BIM, and PUMA are essential for activation of the BAX- and BAK-dependent cell death program. Science 330: 1390-1393.
44. Rena G, Woods YL, Prescott AR, Peggie M, Unterman TG, Williams MR, Cohen P (2002) Two novel phosphorylation sites on FKHR that are critical for its nuclear exclusion. EMBO J 21: 2263-2271. (Pubitemid 34516785)
45. Roy SK, Chen Q, FüJ, Shankar S, Srivastava RK (2011) Resveratrol inhibits growth of orthotopic pancreatic tumours through activation of FOXO transcription factors. PLoS One 6: E25166.
46. Schneider-Jakob S, Corazza N, Badmann A, Sidler D, Stuber-Roos R, Keogh A, Frese S, Tschan M, Brunner T (2010) Synergistic induction of cell death in liver tumour cells by TRAIL and chemotherapeutic drugs via the BH3-only proteins Bim and Bid. Cell Death Dis 1: E86.
47. Sharma G, Kar S, Palit S, Das PK (2011) 18Beta-glycyrrhetinic acid induces apoptosis through modulation of Akt/FOXO3a/Bim pathway in human breast cancer MCF-7 cells. J Cell Physiol 227: 1923-1931.
48. ShiüSY, Li L, XüJN, Pang CS, Wong JT, Pang SF (1999) Melatonin-induced inhibition of proliferation and G1/S cell cycle transition delay of human choriocarcinoma JAr cells: Possible involvement of MT2 (MEL1B) receptor. J Pineal Res 27: 183-192. (Pubitemid 29487963)
49. Srinivasan V, Pandi-Perumal SR, Brzezinski A, Bhatnagar KP, Cardinali DP (2011) Melatonin, immune function and cancer. Recent Pat Endocr Metab Immune Drug Discov 5: 109-123.
50. SüJL, Cheng X, Yamaguchi H, Chang YW, HoüCF, Lee DF, Ko HW, Hua KT, Wang YN, Hsiao M, Chen PB, HsüJM, Bast Jr RC, Hortobagyi GN, Hung MC (2011) FOXO3a-dependent mechanism of E1A-induced chemosensitization. Cancer Res 71: 6878-6887.
51. Subramanian P, Mirunalini S, Pandi-Perumal SR, Trakht I, Cardinali DP (2007) Melatonin treatment improves the antioxidant status and decreases lipid content in brain and liver of rats. Eur J Pharmacol 571: 116-119. (Pubitemid 47385902)
52. Sunters A, Fernandez de Mattos S, Stahl M, Brosens JJ, ZoumpoulidoüG, Saunders CA, Coffer PJ, Medema RH, Coombes RC, Lam EW (2003) FoxO3a transcriptional regulation of Bim controls apoptosis in paclitaxeltreated breast cancer cell lines. J Biol Chem 278: 49795-49805. (Pubitemid 37548813)
53. Tahan V, Atug O, Akin H, Eren F, Tahan G, Tarcin O, Uzun H, Ozdogan O, Tarcin O, Imeryuz N, Ozguner F, Celikel C, Avsar E, Tozun N (2009) Melatonin ameliorates methionine- and choline-deficient diet-induced nonalcoholic steatohepatitis in rats. J Pineal Res 46: 401-407.
54. Thong-Ngam D, Samuhasaneeto S, Kulaputana O, Klaikeaw N (2007) Nacetylcysteine attenuates oxidative stress and liver pathology in rats with non-alcoholic steatohepatitis. World J Gastroenterol 13: 5127-5132. (Pubitemid 47527351)
55. Tran H, Brunet A, Grenier JM, Datta SR, Fornace Jr AJ, DiStefano PS, Chiang LW, Greenberg ME (2002) DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296: 530-534. (Pubitemid 34408672)
56. Tzivion G, Dobson M, Ramakrishnan G (2011) FoxO transcription factors: Regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta 1813: 1938-1945.
57. Weidinger C, Krause K, Mueller K, Klagge A, Fuhrer D (2011) FOXO3 is inhibited by oncogenic PI3K/Akt signaling but can be reactivated by the NSAID sulindac sulfide. J Clin Endocrinol Metab 96: E1361-E1371.
58. Yang JY, Xia W, HüMC (2006) Ionizing radiation activates expression of FOXO3a, Fas ligand, and Bim, and induces cell apoptosis. Int J Oncol 29: 643-648.
59. Yuan Z, Wang F, Zhao Z, Zhao X, QiüJ, Nie C, Wei Y (2011) BIM-mediated AKT phosphorylation is a key modulator of arsenic trioxide-induced apoptosis in cisplatin-sensitive and -resistant ovarian cancer cells PLoS One 6: E20586.
60. Zanella F, Link W, Carnero A (2010) Understanding FOXO, new views on old transcription factors. Curr Cancer Drug Targets 10: 135-146.