Melatonin inhibits AP-2β/hTERT, NF-κB/COX-2 and Akt/ERK and activates caspase/Cyto C signaling to enhance the antitumor activity of berberine in lung cancer cells

Oncotarget

Volumn 7, Issue 3, 2016, Pages 2985-3001

  Lu, Jian Jun ^a   Fu, Lingyi ^b,c   Tang, Zhipeng ^d   Zhang, Changlin ^b   Qin, Lijun ^a   Wang, Jingshu ^b   Yu, Zhenlong ^d   Shi, Dingbo ^b   Xiao, Xiangsheng ^b   Xie, Fangyun ^b   Huang, Wenlin ^b,e   Deng, Wuguo ^b,e  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^c GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

^d DALIAN MEDICAL UNIVERSITY   (China)

^e Guangzhou Double Bioproduct Inc   (China)

Author keywords

Berberine; COX 2; HTERT; Lung cancer; Melantonin

Indexed keywords

BERBERINE; CASPASE; CASPASE 3; CASPASE 9; CYCLOOXYGENASE 2; CYTOCHROME C; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MELATONIN; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 2 BETA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BCL2 PROTEIN, HUMAN; CYCLOOXYGENASE 2 INHIBITOR; DNA BINDING PROTEIN; PTGS2 PROTEIN, HUMAN; TELOMERASE; TERT PROTEIN, HUMAN; TRANSCRIPTION FACTOR AP 2;

A549 CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIVITY; ENZYME ACTIVATION; H1299 CELL LINE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; LUNG CANCER CELL LINE; MALE; MIGRATION INHIBITION; MONOTHERAPY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PROMOTER REGION; PROTEIN CLEAVAGE; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN SECRETION; TUMOR VOLUME; TUMOR XENOGRAFT; ACTIVE TRANSPORT; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; DRUG EFFECTS; DRUG SCREENING; GENETICS; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BERBERINE; CASPASE 9; CELL LINE, TUMOR; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; CYTOCHROMES C; DNA-BINDING PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; LUNG NEOPLASMS; MALE; MELATONIN; MICE; MICE, INBRED BALB C; MICE, NUDE; NF-KAPPA B; POLY(ADP-RIBOSE) POLYMERASES; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; TELOMERASE; TRANSCRIPTION FACTOR AP-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962319977     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6407     Document Type: Article

References (57)

1. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG et al: Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. New Engl J Med 2004, 350:2129-2139.
2. Stehle JH, Saade A, Rawashdeh O, Ackermann K, Jilg A, Sebesteny T, Maronde E: A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. J Pineal Res 2011, 51:17-43.
3. Detterbeck FC, Postmus PE, Tanoue LT: The stage classification of lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013, 143:e191S-210S.
4. Venegas C, Garcia JA, Escames G, Ortiz F, Lopez A, Doerrier C, Garcia-Corzo L, Lopez LC, Reiter RJ, Acuna-Castroviejo D: Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. J Pineal Res 2012, 52:217-227.
5. Reiter RJ, Melchiorri D, Sewerynek E, Poeggeler B, Barlow-Walden L, Chuang J, Ortiz GG, Acuna-Castroviejo D: A review of the evidence supporting melatonin's role as an antioxidant. J Pineal Res 1995, 18:1-11.
6. Rodriguez C, Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Reiter RJ: Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004, 36:1-9.
7. Tan DX, Reiter RJ, Manchester LC, Yan MT, El-Sawi M, Sainz RM, Mayo JC, Kohen R, Allegra M, Hardeland R: Chemical and physical properties and potential mechanisms: melatonin as a broad spectrum antioxidant and free radical scavenger. Curr Top Med Chem 2002, 2:181-197.
8. Mukherjee D, Roy SG, Bandyopadhyay A, Chattopadhyay A, Basu A, Mitra E, Ghosh AK, Reiter RJ, Bandyopadhyay D: Melatonin protects against isoproterenol-induced myocardial injury in the rat: antioxidative mechanisms. J Pineal Res 2010, 48:251-262.
9. Galano A, Tan DX, Reiter RJ: Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011, 51:1-16.
10. Shi D, Xiao X, Wang J, Liu L, Chen W, Fu L, Xie F, Huang W, Deng W: Melatonin suppresses proinflammatory mediators in lipopolysaccharide-stimulated CRL1999 cells via targeting MAPK, NF-kappaB, c/EBPbeta, and p300 signaling. J Pineal Res 2012, 53:154-165.
11. Carrillo-Vico A, Lardone PJ, Naji L, Fernandez-Santos JM, Martin-Lacave I, Guerrero JM, Calvo JR: Beneficial pleiotropic actions of melatonin in an experimental model of septic shock in mice: regulation of pro-/anti-inflammatory cytokine network, protection against oxidative damage and anti-apoptotic effects. J Pineal Res 2005, 39:400-408.
12. Deng WG, Tang ST, Tseng HP, Wu KK: Melatonin suppresses macrophage cyclooxygenase-2 and inducible nitric oxide synthase expression by inhibiting p52 acetylation and binding. Blood 2006, 108:518-524.
13. Reiter RJ: The pineal gland and melatonin in relation to aging: a summary of the theories and of the data. Exp Gerontol 1995, 30:199-212.
14. Petrosillo G, Moro N, Paradies V, Ruggiero FM, Paradies G: Increased susceptibility to Ca(2+)-induced permeability transition and to cytochrome c release in rat heart mitochondria with aging: effect of melatonin. J Pineal Res 2010, 48:340-346.
15. Mao LL, Yuan L, Slakey LM, Jones FE, Burow ME, Hill SM: Inhibition of breast cancer cell invasion by melatonin is mediated through regulation of the p38 mitogen-activated protein kinase signaling pathway. Breast Cancer Res 2010, 12:R107.
16. Gonzalez A, del Castillo-Vaquero A, Miro-Moran A, Tapia JA, Salido GM: Melatonin reduces pancreatic tumor cell viability by altering mitochondrial physiology. J Pineal Res 2011, 50:250-260.
17. Um HJ, Park JW, Kwon TK: Melatonin sensitizes Caki renal cancer cells to kahweol-induced apoptosis through CHOP-mediated up-regulation of PUMA. J Pineal Res 2011, 50:359-366.
18. Proietti S, Cucina A, D'Anselmi F, Dinicola S, Pasqualato A, Lisi E, Bizzarri M: Melatonin and vitamin D3 synergistically down-regulate Akt and MDM2 leading to TGFbeta-1-dependent growth inhibition of breast cancer cells. J Pineal Res 2011, 50:150-158.
19. Martinez-Campa CM, Alonso-Gonzalez C, Mediavilla MD, Cos S, Gonzalez A, Sanchez-Barcelo EJ: Melatonin down-regulates hTERT expression induced by either natural estrogens (17 beta-estradiol) or metalloestrogens (cadmium) in MCF-7 human breast cancer cells. Cancer Lett 2008, 268:272-277.
20. Dai M, Cui P, Yu M, Han J, Li H, Xiu R: Melatonin modulates the expression of VEGF and HIF-1 alpha induced by CoCl2 in cultured cancer cells. J Pineal Res 2008, 44:121-126.
21. Zha LX, Fan LL, Sun GP, Wang H, Ma T, Zhong F, Wei W: Melatonin sensitizes human hepatoma cells to endoplasmic reticulum stress-induced apoptosis. J Pineal Res 2012, 52:322-331.
22. Cabrera J, Negrin G, Estevez F, Loro J, Reiter RJ, Quintana J: Melatonin decreases cell proliferation and induces melanogenesis in human melanoma SK-MEL-1 cells. J Pineal Res 2010, 49:45-54.
23. Joo SS, Yoo YM: Melatonin induces apoptotic death in LNCaP cells via p38 and JNK pathways: therapeutic implications for prostate cancer. J Pineal Res 2009, 47:8-14.
24. Pizarro JG, Yeste-Velasco M, Esparza JL, Verdaguer E, Pallas M, Camins A, Folch J: The antiproliferative activity of melatonin in B65 rat dopaminergic neuroblastoma cells is related to the downregulation of cell cycle-related genes. J Pineal Res 2008, 45:8-16.
25. Sanchez-Hidalgo M, Lee M, de la Lastra CA, Guerrero JM, Packham G: Melatonin inhibits cell proliferation and induces caspase activation and apoptosis in human malignant lymphoid cell lines. J Pineal Res 2012, 53:366-373.
26. Hevia D, Sainz RM, Blanco D, Quiros I, Tan DX, Rodriguez C, Mayo JC: Melatonin uptake in prostate cancer cells: intracellular transport versus simple passive diffusion. J Pineal Res 2008, 45:247-257.
27. Lissoni P, Barni S, Mandala M, Ardizzoia A, Paolorossi F, Vaghi M, Longarini R, Malugani F, Tancini G: Decreased toxicity and increased efficacy of cancer chemotherapy using the pineal hormone melatonin in metastatic solid tumour patients with poor clinical status. European Journal of Cancer 1999, 35:1688-1692.
28. Ram PT, Dai J, Yuan L, Dong C, Kiefer TL, Lai L, Hill SM: Involvement of the mt1 melatonin receptor in human breast cancer. Cancer Lett 2002, 179:141-150.
29. Mao LL, Cheng Q, Guardiola-Lemaitre B, Schuster-Klein C, Dong CM, Lai L, Hill SM: In vitro and in vivo antitumor activity of melatonin receptor agonists. J Pineal Res 2010, 49:210-221.
30. Kuo HP, Chuang TC, Tsai SC, Tseng HH, Hsu SC, Chen YC, Kuo CL, Kuo YH, Liu JY, Kao MC: Berberine, an Isoquinoline Alkaloid, Inhibits the Metastatic Potential of Breast Cancer Cells via Akt Pathway Modulation. J Agr Food Chem 2012, 60:9649-9658.
31. Park JJ, Seo SM, Kim EJ, Lee YJ, Ko YG, Ha J, Lee M: Berberine inhibits human colon cancer cell migration via AMP-activated protein kinase-mediated downregulation of integrin beta 1 signaling. Biochem Bioph Res Co 2012, 426:461-467.
32. Choi MS, Oh JH, Kim SM, Jung HY, Yoo HS, Lee YM, Moon DC, Han SB, Hong JT: Berberine inhibits p53-dependent cell growth through induction of apoptosis of prostate cancer cells. Int J Oncol 2009, 34:1221-1230.
33. Tong NN, Zhang J, Chen YR, Li ZB, Luo YH, Zuo H, Zhao XY: Berberine sensitizes mutliple human cancer cells to the anticancer effects of doxorubicin in vitro. Oncol Lett 2012, 3:1263-1267.
34. Hwang JM, Kuo HC, Tseng TH, Liu JY, Chu CY: Berberine induces apoptosis through a mitochondria/caspases pathway in human hepatoma cells. Arch Toxicol 2006, 80:62-73.
35. Mantena SK, Sharma SD, Katiyar SK: Berberine inhibits growth, induces G1 arrest and apoptosis in human epidermoid carcinoma A431 cells by regulating Cdki-Cdk-cyclin cascade, disruption of mitochondrial membrane potential and cleavage of caspase 3 and PARP. Carcinogenesis 2006, 27:2018-2027.
36. Lin JP, Yang JS, Lee JH, Hsieh WT, Chung JG: Berberine induces cell cycle arrest and apoptosis in human gastric carcinoma SNU-5 cell line. World J Gastroentero 2006, 12:21-28.
37. Murthy KNC, Jayaprakasha GK, Patil BS: The natural alkaloid berberine targets multiple pathways to induce cell death in cultured human colon cancer cells. Eur J Pharmacol 2012, 688:14-21.
38. Wang LH, Liu LP, Shi Y, Cao HW, Chaturvedi R, Calcutt MW, Hu TH, Ren XB, Wilson KT, Polk DB et al: Berberine Induces Caspase-Independent Cell Death in Colon Tumor Cells through Activation of Apoptosis-Inducing Factor. PLoS One 2012, 7:e36418.
39. Wang Y, Liu Q, Liu ZJ, Li BX, Sun ZL, Zhou HB, Zhang XY, Gong YQ, Shao CS: Berberine, a genotoxic alkaloid, induces ATM-Chk1 mediated G2 arrest in prostate cancer cells. Mutat Res-Fund Mol M 2012, 734:20-29.
40. Fu L, Chen W, Guo W, Wang J, Tian Y, Shi D, Zhang X, Qiu H, Xiao X, Kang T et al: Berberine Targets AP-2/hTERT, NF-kappaB/COX-2, HIF-1alpha/VEGF and Cytochrome-c/Caspase Signaling to Suppress Human Cancer Cell Growth. PLoS One 2013, 8:e69240.
41. Kong WJ, Wei J, Abidi P, Lin MH, Inaba S, Li C, Wang YL, Wang ZZ, Si SY, Pan HN et al: Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 2004, 10:1344-1351.
42. Liu JC, Chan P, Chen YJ, Tomlinson B, Hong SH, Cheng JT: The antihypertensive effect of the berberine derivative 6-protoberberine in spontaneously hypertensive rats. Pharmacology 1999, 59:283-289.
43. Yu HH, Kim KJ, Cha JD, Kim HK, Lee YE, Choi NY, You YO: Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillin-resistant Staphylococcus aureus. J Med Food 2005, 8:454-461.
44. Kong WJ, Xing XY, Xiao XH, Zhao YL, Wei JH, Wang JB, Yang RC, Yang MH: Effect of berberine on Escherichia coli, Bacillus subtilis, and their mixtures as determined by isothermal microcalorimetry. Appl Microbiol Biot 2012, 96:503-510.
45. Kuo CL, Chi CW, Liu TY: The anti-inflammatory potential of berberine in vitro and in vivo. Cancer Lett 2004, 203:127-137.
46. Kupeli E, Kosar M, Yesilada E, Husnu K, Baser KHC: A comparative study on the anti-inflammatory, antinociceptive and antipyretic effects of isoquinoline alkaloids from the roots of Turkish Berberis species. Life Sci 2002, 72:645-657.
47. Yesilada E, Kupeli E: Berberis crataegina DC. root exhibits potent anti-inflammatory, analgesic and febrifuge effects in mice and rats. J Ethnopharmacol 2002, 79:237-248.
48. Jeong HW, Hsu KC, Lee JW, Ham M, Huh JY, Shin HJ, Kim WS, Kim JB: Berberine suppresses proinflammatory responses through AMPK activation in macrophages. Am J Physiol-Endoc M 2009, 296:E955-E964.
49. Deng WG, Jayachandran G, Wu G, Xu K, Roth JA, Ji L: Tumor-specific activation of human telomerase reverses transcriptase promoter activity by activating enhancer-binding protein-2 beta in human lung cancer cells. J Biol Chem 2007, 282:26460-26470.
50. Kajita S, Ruebel KH, Casey MB, Nakamura N, Lloyd RV: Role of COX-2, thromboxane A(2) synthase, and prostaglandin I-2 synthase in papillary thyroid carcinoma growth. Modern Pathol 2005, 18:221-227.
51. Wang D, DuBois RN: The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene 2010, 29:781-788.
52. Wenzel U, Nickel A, Daniel H: Melatonin potentiates flavone-induced apoptosis in human colon cancer cells by increasing the level of glycolytic end products. Int J Cancer 2005, 116:236-242.
53. Stewart SA, Hahn WC, O'Connor BF, Banner EN, Lundberg AS, Modha P, Mizuno H, Brooks MW, Fleming M, Zimonjic DB et al: Telomerase contributes to turnorigenesis by a telomere length-independent mechanism. P Natl Acad Sci USA 2002, 99:12606-12611.
54. Saretzki G, Petersen S, Petersen I, Kolble K, von Zglinicki T: hTERT gene dosage correlates with telomerase activity in human lung cancer cell lines. Cancer Lett 2002, 176:81-91.
55. Wang J, Xiao X, Zhang Y, Shi D, Chen W, Fu L, Liu L, Xie F, Kang T, Huang W et al: Simultaneous modulation of COX-2, p300, Akt, and Apaf-1 signaling by melatonin to inhibit proliferation and induce apoptosis in breast cancer cells. J Pineal Res 2012, 53:77-90.
56. Deng WG, Zhu Y, Wu KK: Up-regulation of p300 binding and p50 acetylation in tumor necrosis factor-alpha-induced cyclooxygenase-2 promoter activation. J Biol Chem 2003, 278:4770-4777.
57. Deng WG, Zhu Y, Wu KK: Role of p300 and PCAF in regulating cyclooxygenase-2 promoter activation by inflammatory mediators. Blood 2004, 103:2135-2142.