Berberine inhibits human hepatoma cell invasion without cytotoxicity in healthy Hepatocytes

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Liu, Bing ^a   Wang, Genshu ^b   Yang, Jie ^c   Pan, Xuediao ^a   Yang, Zhicheng ^a   Zang, Linquan ^a  

^a GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c GUANGXI MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BERBERINE; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA;

ARTICLE; CELL INVASION; CELL VIABILITY; CONTROLLED STUDY; DENSITOMETRY; DOWN REGULATION; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG EFFICACY; FLOW CYTOMETRY; HEPATOMA CELL; HUMAN; HUMAN CELL; LIVER CELL; PROTEIN EXPRESSION; UPREGULATION; CELL LINE; CELL STRAIN HEPG2; CELL SURVIVAL; CYTOLOGY; DRUG EFFECT; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; WESTERN BLOTTING;

BERBERINE; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE; CELL SURVIVAL; HEP G2 CELLS; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING;

EID: 79959600879     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021416     Document Type: Article

References (48)

1. Sener SF, Grey N, (2005) The global burden of cancer. J Surg Oncol 92: 1-3.
2. Thomas MB, O'Beirne JP, Furuse J, Chan AT, Abou-Alfa G, et al. (2008) Systemic therapy for hepatocellular carcinoma: cytotoxic chemotherapy, targeted therapy and immunotherapy. Ann Surg Oncol 15: 1008-1014.
3. Pervaiz S, (2002) Anti-cancer drugs of today and tomorrow: are we close to making the turn from treating to curing cancer? Curr Pharm Des 8: 1723-1734.
4. Monvoisin A, Neaud V, De Ledinghen V, Dubuisson L, Balabaud C, et al. (1999) Direct evidence that hepatocyte growth factor-induced invasion of hepatocellular carcinoma cells is mediated by urokinase. J Hepatol 30: 511-518.
5. Chung TW, Lee YC, Kim CH, (2004) Hepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3K/AKT pathways: involvement of invasive potential. FASEB J 18: 1123-1125.
6. Kozuki Y, Miura Y, Yagasaki K, (2000) Inhibitory effects of carotenoids on the invasion of rat ascites hepatoma cells in culture. Cancer Lett 151: 111-115.
7. Zhang G, Miura Y, Yagasaki K, (2000) Suppression of adhesion and invasion of hepatoma cells in culture by tea compounds through antioxidative activity. Cancer Lett 159: 169-173.
8. Yagasaki K, Miura Y, Okauchi R, Furuse T, (2000) Inhibitory effects of chlorogenic acid and its related compounds on the invasion of hepatoma cells in culture. Cytotechnology 33: 229-235.
9. Kozuki Y, Miura Y, Yagasaki K, (2001) Resveratrol suppresses hepatoma cell invasion independently of its anti-proliferative action. Cancer Lett 167: 151-156.
10. Jantova S, Cipak L, Cernakova M, Kost'alova D, (2003) Effect of berberine on proliferation, cell cycle and apoptosis in HeLa and L1210 cells. J Pharm Pharmacol 55: 1143-1149.
11. Hwang JM, Kuo HC, Tseng TH, Liu JY, Chu CY, (2006) Berberine induces apoptosis through a mitochondria/caspases pathway in human hepatoma cells. Arch Toxicol 80: 62-73.
12. Lin TH, Kuo HC, Chou FP, Lu FJ, (2008) Berberine enhances inhibition of glioma tumor cell migration and invasiveness mediated by arsenic trioxide. BMC Cancer 8: 58.
13. Peng PL, Hsieh YS, Wang CJ, Hsu JL, Chou FP, (2006) Inhibitory effect of berberine on the invasion of human lung cancer cells via decreased productions of urokinase-plasminogen activator and matrix metalloproteinase-2. Toxicol Appl Pharmacol 214: 8-15.
14. Tang F, Wang D, Duan C, Huang D, Wu Y, et al. (2009) Berberine inhibits metastasis of nasopharyngeal carcinoma 5-8F cells by targeting Rho kinase-mediated Ezrin phosphorylation at threonine 567. J Biol Chem 284: 27456-27466.
15. Singh T, Vaid M, Katiyar N, Sharma S, Katiyar SK, (2011) Berberine, an isoquinoline alkaloid, inhibits melanoma cancer cell migration by reducing the expressions of cyclooxygenase-2, prostaglandin E2 and prostaglandin E2 receptors. Carcinogenesis 32: 86-92.
16. Weng CJ, Chau CF, Hsieh YS, Yang SF, Yen GC, (2008) Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF-kappaB and AP-1. Carcinogenesis 29: 147-156.
17. Kim WH, Chon CY, Moon YM, Kang JK, Park IS, et al. (1993) Effect of anticancer drugs and desferrioxamine in combination with radiation on hepatoma cell lines. Yonsei Med J 34: 45-56.
18. He B, Tong X, Wang L, Wang Q, Ye H, et al. (2009) Tramadol and flurbiprofen depress the cytotoxicity of cisplatin via their effects on gap junctions. Clin Cancer Res 15: 5803-5810.
19. Sanceau J, Truchet S, Bauvois B, (2003) Matrix metalloproteinase-9 silencing by RNA interference triggers the migratory-adhesive switch in Ewing's sarcoma cells. J Biol Chem 278: 36537-36546.
20. Deryugina EI, Zijlstra A, Partridge JJ, Kupriyanova TA, Madsen MA, et al. (2005) Unexpected effect of matrix metalloproteinase down-regulation on vascular intravasation and metastasis of human fibrosarcoma cells selected in vivo for high rates of dissemination. Cancer Res 65: 10959-10969.
21. Kamata H, Hirata H, (1999) Redox regulation of cellular signalling. Cell Signal 11: 1-14.
22. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, et al. (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404: 787-790.
23. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446.
24. Arii S, Mise M, Harada T, Furutani M, Ishigami S, et al. (1996) Overexpression of matrix metalloproteinase 9 gene in hepatocellular carcinoma with invasive potential. Hepatology 24: 316-322.
25. Oh SH, Lim SC, (2006) A rapid and transient ROS generation by cadmium triggers apoptosis via caspase-dependent pathway in HepG2 cells and this is inhibited through N-acetylcysteine-mediated catalase upregulation. Toxicol Appl Pharmacol 212: 212-223.
26. Kim JH, Lee SY, Oh SY, Han SI, Park HG, et al. (2004) Methyl jasmonate induces apoptosis through induction of Bax/Bcl-XS and activation of caspase-3 via ROS production in A549 cells. Oncol Rep 12: 1233-1238.
27. Meeran SM, Katiyar S, Katiyar SK, (2008) Berberine-induced apoptosis in human prostate cancer cells is initiated by reactive oxygen species generation. Toxicol Appl Pharmacol 229: 33-43.
28. Kim S, Choi JH, Kim JB, Nam SJ, Yang JH, et al. (2008) Berberine suppresses TNF-alpha-induced MMP-9 and cell invasion through inhibition of AP-1 activity in MDA-MB-231 human breast cancer cells. Molecules 13: 2975-2985.
29. Ho YT, Yang JS, Li TC, Lin JJ, Lin JG, et al. (2009) Berberine suppresses in vitro migration and invasion of human SCC-4 tongue squamous cancer cells through the inhibitions of FAK, IKK, NF-kappaB, u-PA and MMP-2 and-9. Cancer Lett 279: 155-162.
30. van Waveren C, Sun Y, Cheung HS, Moraes CT, (2006) Oxidative phosphorylation dysfunction modulates expression of extracellular matrix--remodeling genes and invasion. Carcinogenesis 27: 409-418.
31. Groth S, Schulze M, Kalthoff H, Fandrich F, Ungefroren H, (2005) Adhesion and Rac1-dependent regulation of biglycan gene expression by transforming growth factor-beta. Evidence for oxidative signaling through NADPH oxidase. J Biol Chem 280: 33190-33199.
32. Deem TL, Cook-Mills JM, (2004) Vascular cell adhesion molecule 1 (VCAM-1) activation of endothelial cell matrix metalloproteinases: role of reactive oxygen species. Blood 104: 2385-2393.
33. Wu WS, (2006) The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev 25: 695-705.
34. Takahra T, Smart DE, Oakley F, Mann DA, (2004) Induction of myofibroblast MMP-9 transcription in three-dimensional collagen I gel cultures: regulation by NF-kappaB, AP-1 and Sp1. Int J Biochem Cell Biol 36: 353-363.
35. Bahassi el M, Karyala S, Tomlinson CR, Sartor MA, Medvedovic M, et al. (2004) Critical regulation of genes for tumor cell migration by AP-1. Clin Exp Metastasis 21: 293-304.
36. Cheng JC, Chou CH, Kuo ML, Hsieh CY, (2006) Radiation-enhanced hepatocellular carcinoma cell invasion with MMP-9 expression through PI3K/Akt/NF-kappaB signal transduction pathway. Oncogene 25: 7009-7018.
37. Abiru S, Nakao K, Ichikawa T, Migita K, Shigeno M, et al. (2002) Aspirin and NS-398 inhibit hepatocyte growth factor-induced invasiveness of human hepatoma cells. Hepatology 35: 1117-1124.
38. Kohn EC, Liotta LA, (1995) Molecular insights into cancer invasion: strategies for prevention and intervention. Cancer Res 55: 1856-1862.
39. Itoh Y, Nagase H, (2002) Matrix metalloproteinases in cancer. Essays Biochem 38: 21-36.
40. Ito Y, Sasaki Y, Horimoto M, Wada S, Tanaka Y, et al. (1998) Activation of mitogen-activated protein kinases/extracellular signal-regulated kinases in human hepatocellular carcinoma. Hepatology 27: 951-958.
41. Xu G, Zhang W, Bertram P, Zheng XF, McLeod H, (2004) Pharmacogenomic profiling of the PI3K/PTEN-AKT-mTOR pathway in common human tumors. Int J Oncol 24: 893-900.
42. Scheving LA, Buchanan R, Krause MA, Zhang X, Stevenson MC, et al. (2007) Dexamethasone modulates ErbB tyrosine kinase expression and signaling through multiple and redundant mechanisms in cultured rat hepatocytes. Am J Physiol Gastrointest Liver Physiol 293: G552-559.
43. P Oc, Wongkajornsilp A, Rhys-Evans PH, Eccles SA, (2004) Signaling pathways required for matrix metalloproteinase-9 induction by betacellulin in head-and-neck squamous carcinoma cells. Int J Cancer 111: 174-183.
44. Thant AA, Nawa A, Kikkawa F, Ichigotani Y, Zhang Y, et al. (2000) Fibronectin activates matrix metalloproteinase-9 secretion via the MEK1-MAPK and the PI3K-Akt pathways in ovarian cancer cells. Clin Exp Metastasis 18: 423-428.
45. Ye M, Fu S, Pi R, He F, (2009) Neuropharmacological and pharmacokinetic properties of berberine: a review of recent research. J Pharm Pharmacol 61: 831-837.
46. Tsang CM, Lau EP, Di K, Cheung PY, Hau PM, et al. (2009) Berberine inhibits Rho GTPases and cell migration at low doses but induces G2 arrest and apoptosis at high doses in human cancer cells. Int J Mol Med 24: 131-138.
47. Gui SY, Wu L, Peng DY, Liu QY, Yin BP, et al. (2008) Preparation and evaluation of a microemulsion for oral delivery of berberine. Pharmazie 63: 516-519.
48. Tsai PL, Tsai TH, (2004) Hepatobiliary excretion of berberine. Drug Metab Dispos 32: 405-412.