Berberine: New perspectives for old remedies

Biochemical Pharmacology

Volumn 84, Issue 10, 2012, Pages 1260-1267

  Tillhon, Micol ^a   Guamán Ortiz, Luis M ^a,b   Lombardi, Paolo ^c   Scovassi, A Ivana ^a  

^a CNR   (Italy)

^b UNIVERSIDAD TÉCNICA PARTICULAR DE LOJA   (Ecuador)

^c Naxospharma   (Italy)

Author keywords

Apoptosis; Autophagy; Berberine; Cancer; Isoquinoline alkaloid

Indexed keywords

ANTINEOPLASTIC AGENT; ARSENIC TRIOXIDE; BERBERINE; CASPASE 3; CASPASE 8; CASPASE 9; CATHEPSIN; CISPLATIN; CYCLOOXYGENASE 2 INHIBITOR; CYTOCHROME C; DNA TOPOISOMERASE; EVODIAMINE; FAS ANTIGEN; GELATINASE A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROSTAGLANDIN E; PROSTAGLANDIN E2; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P21; PROTEIN P27; PROTEIN P53; PUMA PROTEIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG;

ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ASPERGILLUS; AUTOPHAGY; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANDIDA; COLORECTAL CANCER; CRYPTOCOCCUS; DNA FRAGMENTATION; DRUG STRUCTURE; GLIOBLASTOMA; HUMAN; LIVER CELL CARCINOMA; LUNG CANCER; METASTASIS; MYCOBACTERIUM TUBERCULOSIS; NASOPHARYNX CARCINOMA; NEUROBLASTOMA; NEUROBLASTOMA CELL; NONHUMAN; OSTEOSARCOMA; PENICILLIUM; PRIORITY JOURNAL; PROSTATE CARCINOMA; REVIEW; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; AUTOPHAGY; BERBERINE; HUMANS; HYPOGLYCEMIC AGENTS; NEOPLASM METASTASIS;

EID: 84867846281     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.07.018     Document Type: Review

References (113)

1. V.C. Chung, P.H. Ma, C.H. Lau, and S.M. Griffiths Developing policy for integrating biomedicine and traditional Chinese medical practice using focus groups and the Delphi technique Evid Based Complement Alternat Med 2012 2012 149512
2. N.K. Quartey, P.H. Ma, V.C. Chung, and S.M. Griffiths Complementary and alternative medicine education for medical profession: systematic review Evid Based Complement Alternat Med 2012 2012 656812
3. WHO monographs on: Medicinal plants commonly used in the Newly Independent Stases (NIS). WHO 2010; p. 1-441.
4. W.C. McClatcheya, G.B. Mahadyb, B.C. Bennettc, L. Shielsa, and V. Savod Ethnobotany as a pharmacological research tool and recent developments in CNS-active natural products from ethnobotanical sources Pharmacol Ther 123 2009 239 254
5. W.H. Lewis Pharmaceutical discoveries based on ethnomedicinal plants: 1985 to 2000 and beyond Econ Bot 57 2003 126 134
6. WHO monographs on: Traditional medicines: global situation, issues and challenges. WHO 2011; p. 1-12.
7. B. Patwardhan, and A.D. Vaidya Natural products drug discovery: accelerating the clinical candidate development using reverse pharmacology approaches Indian J Exp Biol 48 2010 220 227
8. D.J. Newman, and G.M. Cragg Natural products as sources of new drugs over the last 25 years J Nat Prod 70 2007 461 477
9. S. Beg, S. Swain, H. Hasan, M.A. Barkat, and M.S. Hussain Systematic review of herbals as potential anti-inflammatory agents: recent advances, current clinical status and future perspectives Pharmacogn Rev 5 2011 120 137
10. H. Jiang, A.C. Torregrossa, D.K. Parthasarathy, and N.S. Bryan Natural product nitric oxide chemistry: new activity of old medicines Evid Based Complement Alternat Med 2012 2012 873210
11. M. Imanshahidi, and H. Hosseinzadeh Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine Phytother Res 22 2008 999 1012
12. G.A. Cordell, M.L. Quinn-Beattle, and N.R. Farnsworth The potential of alkaloids in drug discovery Phytother Res 15 2001 183 205
13. Y. Kobayashi, Y. Yamashita, N. Fujii, K. Takaboshi, T. Kawakami, and M. Kawamura Inhibitors of DNA topoisomerase I and II isolated from the Coptis rhizomes Planta Med 61 1995 414 418
14. W.H. Chen, J.Y. Pang, Y. Qin, Q. Peng, Z. Cai, and Z.H. Jiang Synthesis of lined berberine dimers and their remarkably enhanced DNA-binding affinities Bioorg Med Chem Lett 15 2005 2689 2692
15. P. Krishnan, and K. Bastow The 9-position in berberine analogs is an important determinant of DNA topoisomerase II inhibition Anti-Cancer Drug Des 15 2000 255 264
16. J.Y. Pang, Y. Qin, W.H. Chen, G.A. Luo, and Z.H. Jiangb Synthesis and DNA-binding affinities of monomodified berberines Bioorg Med Chem 13 2005 5835 5840
17. W.J. Zhang, T.M. Ou, Y.J. Lu, Y.Y. Huang, W.B. Wu, and Z.S. Huang 9-Substituted berberine derivatives as G-quadruplex stabilizing ligands in telomeric DNA Bioorg Med Chem 15 2007 5493 5501
18. J.Y. Pang, Y.H. Long, W.H. Chen, and Z.H. Jiang Amplification of DNA-binding affinities of protoberberine alkaloids by appended polyamines Bioorg Med Chem Lett 17 2007 1018 1021
19. Y. Ma, T.M. Ou, J.H. Tan, J.Q. Hou, S.L. Shi-Liang Huang, and L.Q. Gu Synthesis and evaluation of 9-O-substituted berberine derivatives containing aza-aromatic terminal group as highly selective telomeric G-quadruplex stabilizing ligands Bioorg Med Chem Lett 19 2009 3414 3417
20. J.S. Cui, F. Xu, J.Y. Pang, W.H. Chen, and Z.H. Jiang Synthesis and DNA-binding affinities of protoberberine-based multivalent agents Chem Biodivers 7 2010 2908 2916
21. L. Huang, Z. Luo, F. He, A. Shi, F. Qin, and X. Li Berberine derivatives, with substituted amino groups linked at the 9-position, as inhibitors of acetylcholinesterase/butyrylcholinesterase Bioorg Med Chem Lett 20 2010 6649 6652
22. M. Shamma The protoberberines and retroprotoberberines M. Shamma, The isoquinoline alkaloids 1972 Academic Press New York, London 268 314
23. K. Iwasa, D.U. Lee, S.I. Kang, and W. Wiegrebe Antimicrobial activity of 8-alkyl- and 8-phenyl-substituted berberines and their 12-bromo derivatives J Nat Prod 6 1998 1150 1153
24. Y. Yang, X.L. Ye, J. Zheng, B.S. Zhang, and X.G. Li Synthesis of 8-alkylberberine J Org Chem 11 2007 1438 1440
25. K. Iwasa, M. Kamigauchi, M. Ueki, and M. Taniguchi Antibacterial activity and structure-activity relationships of berberine analogs Eur J Med Chem 31 1996 469 478
26. K.D. Park, J.H. Lee, S.H. Kim, T.H. Kang, J.S. Moon, and S.U. Kim Synthesis of 13-(substituted benzyl) berberine and berberrubine derivatives as antifungal agents Bioorg Med Chem Lett 16 2006 3913 3916
27. Kim JH, Jhong TN, Paik YK, Park JS, Kim ED, Lee YS, et al. 13,13a-Didehydroberberine derivatives. US Patent 2001;6,239,139B1.
28. S.K. Kulkarni, and A. Dhir Berberine: a plant alkaloid with therapeutic potential for central nervous system disorders Phytother Res 24 2010 317 324
29. P.R. Vuddanda, S. Chakraborty, and S. Singh Berberine: a potential phytochemical with multispectrum therapeutic activities Expert Opin Invest Drugs 19 2010 1297 1307
30. J.M. Boberek, J. Stach, and L. Good Genetic evidence for inhibition of bacterial division protein FtsZ by berberine PLoS One 5 2010 e13745
31. K.A. Ettefagh, J.T. Burns, H.A. Junio, G.W. Kaatz, and N.B. Cech Goldenseal (Hydrastis canadensis L.) extracts synergistically enhance the antibacterial activity of berberine via efflux pump inhibition Planta Med 77 2011 835 840
32. S. Samosorn, B. Tanwirat, N. Muhamad, G. Casadei, D. Tomkiewicz, and K. Lewis Antibacterial activity of berberine-NorA pump inhibitor hybrids with a methylene ether linking group Bioorg Med Chem 17 2009 3866 3872
33. A. Remppis, F. Bea, H.J. Greten, A. Buttler, H. Wang, and Q. Zhou Rhizoma coptidis inhibits LPS-induced MCP-1/CCL2 production in murine macrophages via an AP-1 and NFkappaB-dependent pathway Mediators Inflamm 2010 2010 194896
34. J. Yin, H. Zhang, and J. Ye Traditional chinese medicine in treatment of metabolic syndrome Endocr Metab Immune Disord Drug Targets 8 2008 99 111
35. H. Hui, G. Tang, V. Liang, and W. Go Hypoglycemic herbs and their action mechanisms Chin Med 4 2009 11
36. Y. Chen, Y. Wang, J. Zhang, C. Sun, and A. Lopez Berberine improves glucose homeostasis in streptozotocin-induced diabetic rats in association with multiple factors of insulin resistance ISRN Endocrinol 2011 519371
37. X. Xia, J. Yan, Y. Shen, K. Tang, J. Yin, and Y. Zhang Berberine improves glucose metabolism in diabetic rats by inhibition of hepatic gluconeogenesis PLoS One 6 2011 e16556
38. J. Yin, H. Xing, and J. Ye Efficacy of berberine in patients with type 2 diabetes mellitus Metabolism 57 2008 712 717
39. J. Yang, J. Yin, H. Gao, L. Xu, Y. Wang, and L. Xu Berberine improves insulin sensitivity by inhibiting fat store and adjusting adipokines profile in human preadipocytes and metabolic syndrome patients Evid Based Complement Alternat Med 2012 363845
40. P. Giri, and G.S. Kumar Isoquinoline alkaloids and their binding with polyadenylic acid: potential basis of therapeutic action Mini Rev Med Chem 10 2010 568 577
41. K. Bhadra, and G.S. Kumar Therapeutic potential of nucleic acid-binding isoquinoline alkaloids: binding aspects and implications for drug design Med Res Rev 31 2011 821 862
42. K. Bhadra, and G.S. Kumar Isoquinoline alkaloids and their binding with DNA: calorimetry and thermal analysis applications Mini Rev Med Chem 10 2010 1235 1247
43. M. Maiti, and G.S. Kumar Polymorphic nucleic Acid binding of bioactive isoquinoline alkaloids and their role in cancer J Nucleic Acids 2010 2010:593408
44. N. Xu, H. Yang, M. Cui, F. Song, Z. Liu, and S. Liu Evaluation of alkaloids binding to the parallel quadruplex structure [d(TGGGGT)](4) by electrospray ionization mass spectrometry J Mass Spectrom 47 2012 694 700
45. Y. Qin, J.Y. Pang, W.H. Chen, Z.Z. Zhao, L. Liu, and Z.H. Jiang Inhibition of DNA topoisomerase I by natural and synthetic mono- and dimeric protoberberine alkaloids Chem Biodivers 4 2007 481 487
46. S.A. Kim, Y. Kwon, J.H. Kim, M.T. Muller, and I.K. Chung Induction of topoisomerase II-mediated DNA cleavage by a protoberberine alkaloid, berberrubine Biochemistry 37 1998 16316 16324
47. B. Gatto, M.M. Sanders, C. Yu, H.Y. Wu, D. Makhey, and E.J. LaVoie Identification of topoisomerase I as the cytotoxic target of the protoberberine alkaloid coralyne Cancer Res 56 1996 2795 2800
48. M.R. Kang, and I.K. Chung Down-regulation of DNA topoisomerase II alpha in human colorectal carcinoma cells resistant to a protoberberine alkaloid, berberrubine Mol Pharmacol 61 2002 879 884
49. Y. Kobayashi, Y. Yamashita, N. Fujii, K. Takaboshi, T. Kawakami, and M. Kawamura Inhibitors of DNA topoisomerase I and II isolated from the Coptis rhizomes Planta Med 61 1995 414 418
50. D.S. Pilch, C. Yu, D. Makhey, E.J. LaVoie, A.R. Srinivasan, and W.K. Olson Minor groove-directed and intercalative ligand-DNA interactions in the poisoning of human DNA topoisomerase I by protoberberine analogs Biochemistry 36 1997 12542 12553
51. M.M. Sanders, A.A. Liu, T.K. Li, H.Y. Wu, S.D. Desai, and Y. Mao Selective cytotoxicity of topoisomerase-directed protoberberines against glioblastoma cells Biochem Pharmacol 56 1998 1157 1166
52. J.B. Kim, J.H. Yu, E. Ko, K.W. Lee, A.K. Song, and S.Y. Park The alkaloid berberine inhibits the growth of Anoikis-resistant MCF-7 and MDA-MB-231 breast cancer cell lines by inducing cell cycle arrest Phytomedicine 17 2010 436 440
53. K.S. Park, J.B. Kim, J. Bae, S.Y. Park, H.G. Jee, and K.E. Lee Berberine inhibited the growth of thyroid cancer cell lines 8505C and TPC1 Yonsei Med J 53 2012 346 351
54. K.S. Park, J.B. Kim, S.J. Lee, and J. Bae Berberine-induced growth inhibition of epithelial ovarian carcinoma cell lines J Obstet Gynaecol Res 38 2012 535 540
55. M.A. James, H. Fu, Y. Liu, D.R. Chen, and M. You Dietary administration of berberine or Phellodendron amurense extract inhibits cell cycle progression and lung tumorigenesis Mol Carcinog 50 2011 1 7
56. T.L. Serafim, P.J. Oliveira, V.A. Sardao, E. Perkins, D. Parke, and J. Holy Different concentrations of berberine result in distinct cellular localization patterns and cell cycle effects in a melanoma cell line Cancer Chemother Pharmacol 61 2008 1007 1018
57. Z. Liu, Q. Liu, B. Xu, J. Wu, C. Guo, and F. Zhu Berberine induces p53-dependent cell cycle arrest and apoptosis of human osteosarcoma cells by inflicting DNA damage Mutat Res 662 2009 75 83
58. J.P. Lin, J.S. Yang, N.W. Chang, T.H. Chiu, C.C. Su, and K.W. Lu GADD153 mediates berberine-induced apoptosis in human cervical cancer Ca ski cells Anticancer Res 27 2007 3379 3386
59. C.L. Kuo, C.W. Chi, and T.Y. Liu Modulation of apoptosis by berberine through inhibition of cyclooxygenase-2 and Mcl-1 expression in oral cancer cells In Vivo 19 2005 247 252
60. H.L. Wu, C.Y. Hsu, W.H. Liu, and B.Y. Yung Berberine-induced apoptosis of human leukemia HL-60 cells is associated with down-regulation of nucleophosmin/B23 and telomerase activity Int J Cancer 81 1999 923 929
61. W. Tan, J. Lu, M. Huang, Y. Li, M. Chen, and G. Wu Anti-cancer natural products isolated from Chinese medicinal herbs Chin Med 6 2011 27
62. Y. Sun, K. Xun, Y. Wang, and X. Chen A systematic review of the anticancer properties of berberine, a natural product from Chinese herbs Anticancer Drugs 20 2009 757 769
63. J. Tang, Y. Feng, S. Tsao, N. Wang, R. Curtain, and Y. Wang Berberine and Coptidis rhizoma as novel antineoplastic agents: a review of traditional use and biomedical investigations J Ethnopharmacol 126 2009 5 17
64. W. Tan, Y. Li, M. Chen, and Y. Wang Berberine hydrochloride: anticancer activity and nanoparticulate delivery system Int J Nanomed 6 2011 1773 1777
65. M.S. Choi, D.Y. Yuk, J.H. Oh, H.Y. Jung, S.B. Han, and D.C. Moon Berberine inhibits human neuroblastoma cell growth through induction of p53-dependent apoptosis Anticancer Res 28 2008 3777 3784
66. K.S. Eom, J.M. Hong, M.J. Youn, H.S. So, R. Park, and J.M. Kim Berberine induces G1 arrest and apoptosis in human glioblastoma T98G cells through mitochondrial/caspases pathway Biol Pharm Bull 31 2008 558 562
67. C.M. Tsang, E.P. Lau, K. Di, P.Y. Cheung, P.M. Hau, and Y.P. Ching 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 2009 131 138
68. Y.T. Ho, C.C. Lu, J.S. Yang, J.H. Chiang, T.C. Li, and S.W. Ip Berberine induced apoptosis via promoting the expression of caspase-8, -9 and -3, apoptosis-inducing factor and endonuclease G in SCC-4 human tongue squamous carcinoma cancer cells Anticancer Res 29 2009 4063 4070
69. S.K. Katiyar, S.M. Meeran, N. Katiyar, and S. Akhtar p53 Cooperates berberine-induced growth inhibition and apoptosis of non-small cell human lung cancer cells in vitro and tumor xenograft growth in vivo Mol Carcinog 48 2009 24 37
70. J.B. Patil, J. Kim, and G.K. Jayaprakasha Berberine induces apoptosis in breast cancer cells (MCF-7) through mitochondrial-dependent pathway Eur J Pharmacol 645 2010 70 78
71. J.M. Hwang, H.C. Kuo, T.H. Tseng, J.Y. Liu, and C.Y. Chu Berberine induces apoptosis through a mitochondria/caspases pathway in human hepatoma cells Arch Toxicol 80 2006 62 73
72. L. Wang, L. Liu, Y. Shi, H. Cao, R. Chaturvedi, and M.W. Calcutt Berberine induces caspase-independent cell death in colon tumor cells through activation of apoptosis-inducing factor PLoS One 7 2012 e36418
73. R. Piyanuch, M. Sukhthankar, G. Wandee, and S.J. Baek Berberine, a natural isoquinoline alkaloid, induces NAG-1 and ATF3 expression in human colorectal cancer cells Cancer Lett 258 2007 230 240
74. W.H. Hsu, Y.S. Hsieh, H.C. Kuo, C.Y. Teng, H.I. Huang, and C.J. Wang Berberine induces apoptosis in SW620 human colonic carcinoma cells through generation of reactive oxygen species and activation of JNK/p38 MAPK and FasL Arch Toxicol 81 2007 719 728
75. M.S. Choi, J.H. Oh, S.M. Kim, H.Y. Jung, H.S. Yoo, and Y.M. Lee Berberine inhibits p53-dependent cell growth through induction of apoptosis of prostate cancer cells Int J Oncol 34 2009 1221 1230
76. S.M. Meeran, S. Katiyar, and S.K. Katiyar Berberine-induced apoptosis in human prostate cancer cells is initiated by reactive oxygen species generation Toxicol Appl Pharmacol 229 2008 33 43
77. S.K. Mantena, S.D. Sharma, and S.K. Katiyar Berberine, a natural product, induces G1-phase cell cycle arrest and caspase-3-dependent apoptosis in human prostate carcinoma cells Mol Cancer Ther 5 2006 296 308
78. S.K. Mantena, S.D. Sharma, and S.K. Katiyar 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 27 2006 2018 2027
79. S. Letasiova, S. Jantova, L. Cipak, and M. Muckova Berberine- antiproliferative activity in vitro and induction of apoptosis/necrosis of the U937 and B16 cells Cancer Lett 239 2006 254 262
80. S. Jantova, L. Cipak, and S. Letasiova Berberine induces apoptosis through a mitochondrial/caspase pathway in human promonocytic U937 cells Toxicol In Vitro 21 2007 25 31
81. C.C. Lin, S.T. Kao, G.W. Chen, H.C. Ho, and J.G. Chung Apoptosis of human leukemia HL-60 cells and murine leukemia WEHI-3 cells induced by berberine through the activation of caspase-3 Anticancer Res 26 2006 227 242
82. H.P. Kuo, T.C. Chuang, M.H. Yeh, S.C. Hsu, T.D. Way, and P.Y. Chen Growth suppression of HER2-overexpressing breast cancer cells by berberine via modulation of the HER2/PI3K/Akt signaling pathway J Agric Food Chem 59 2011 8216 8224
83. B. Liu, G. Wang, J. Yang, X. Pan, Z. Yang, and L. Zang Berberine inhibits human hepatoma cell invasion without cytotoxicity in healthy hepatocytes PLoS One 6 2011 e21416
84. M.K. Pandey, B. Sung, A.B. Kunnumakkara, G. Sethi, M.M. Chaturvedi, and B.B. Aggarwal Berberine modifies cysteine 179 of IkappaBalpha kinase, suppresses nuclear factor-kappaB-regulated antiapoptotic gene products, and potentiates apoptosis Cancer Res 68 2008 5370 5379
85. K. Fukuda, Y. Hibiya, M. Mutoh, M. Koshiji, S. Akao, and H. Fujiwara Inhibition of activator protein 1 activity by berberine in human hepatoma cells Planta Med 65 1999 381 383
86. C.L. Kuo, C.W. Chi, and T.Y. Liu The anti-inflammatory potential of berberine in vitro and in vivo Cancer Lett 203 2004 127 137
87. S. Kim, J.H. Choi, J.B. Kim, S.J. Nam, J.H. Yang, and J.H. Kim 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 2008 2975 2985
88. K. Fukuda, Y. Hibiya, M. Mutoh, M. Koshiji, S. Akao, and H. Fujiwara Inhibition by berberine of cyclooxygenase-2 transcriptional activity in human colon cancer cells J Ethnopharmacol 66 1999 227 233
89. N. Xiao, S. Chen, Y. Ma, J. Qiu, J.H. Tan, and T.M. Ou Interaction of berberine derivative with protein POT1 affect telomere function in cancer cells Biochem Biophys Res Commun 419 2012 567 572
90. J.P. Lin, J.S. Yang, C.C. Wu, S.S. Lin, W.T. Hsieh, and M.L. Lin Berberine induced down-regulation of matrix metalloproteinase-1, -2 and -9 in human gastric cancer cells (SNU-5) in vitro In Vivo 22 2008 223 230
91. T.H. Lin, H.C. Kuo, F.P. Chou, and F.J. Lu Berberine enhances inhibition of glioma tumor cell migration and invasiveness mediated by arsenic trioxide BMC Cancer 8 2008 58
92. D.W. Kim, S.H. Ahan, and T.Y. Kim Enhancement of arsenic trioxide (As(2)O(3))-mediated apoptosis using berberine in human neuroblastoma SH-SY5Y cells J Korean Neurosurg Soc 42 2007 392 399
93. M.J. Youn, H.S. So, H.J. Cho, H.J. Kim, Y. Kim, and J.H. Lee Berberine, a natural product, combined with cisplatin enhanced apoptosis through a mitochondria/caspase-mediated pathway in HeLa cells Biol Pharm Bull 31 2008 789 795
94. X.N. Wang, X. Han, L.N. Xu, L.H. Yin, Y.W. Xu, and Y. Qi Enhancement of apoptosis of human hepatocellular carcinoma SMMC-7721 cells through synergy of berberine and evodiamine Phytomedicine 15 2008 1062 1068
95. J. Liu, C. He, K. Zhou, J. Wang, and J.X. Kang Coptis extracts enhance the anticancer effect of estrogen receptor antagonists on human breast cancer cells Biochem Biophys Res Commun 378 2009 174 178
96. P.L. Peng, W.H. Kuo, H.C. Tseng, and F.P. Chou Synergistic tumor-killing effect of radiation and berberine combined treatment in lung cancer: the contribution of autophagic cell death Int J Radiat Oncol Biol Phys 70 2008 529 542
97. J.M. Hur, M.S. Hyun, S.Y. Lim, W.Y. Lee, and D. Kim The combination of berberine and irradiation enhances anti-cancer effects via activation of p38 MAPK pathway and ROS generation in human hepatoma cells J Cell Biochem 107 2009 955 964
98. T. Singh, M. Vaid, N. Katiyar, S. Sharma, and S.K. Katiyar Berberine, an isoquinoline alkaloid, inhibits melanoma cancer cell migration by reducing the expressions of cyclooxygenase-2, prostaglandin E(2) and prostaglandin E(2) receptors Carcinogenesis 32 2011 86 92
99. F. Tang, D. Wang, C. Duan, D. Huang, Y. Wu, and Y. Chen Berberine inhibits metastasis of nasopharyngeal carcinoma 5-8F cells by targeting Rho kinase-mediated Ezrin phosphorylation at threonine 567 J Biol Chem 284 2009 27456 27466
100. P.L. Peng, Y.S. Hsieh, C.J. Wang, J.L. Hsu, and F.P. Chou 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 2006 8 15
101. Y.T. Ho, J.S. Yang, C.C. Lu, J.H. Chiang, T.C. Li, and J.J. Lin Berberine inhibits human tongue squamous carcinoma cancer tumor growth in a murine xenograft model Phytomedicine 16 2009 887 890
102. H. Li, L. Guo, S. Jie, W. Liu, J. Zhu, and W. Du Berberine inhibits SDF-1-induced AML cells and leukemic stem cells migration via regulation of SDF-1 level in bone marrow stromal cells Biomed Pharmacother 62 2008 573 578
103. H.S. Kim, M.J. Kim, E.J. Kim, Y. Yang, M.S. Lee, and J.S. Lim Berberine-induced AMPK activation inhibits the metastatic potential of melanoma cells via reduction of ERK activity and COX-2 protein expression Biochem Pharmacol 83 2012 385 394
104. T.P. Hamsa, and G. Kuttan Berberine inhibits pulmonary metastasis through down-regulation of MMP in metastatic B16F-10 melanoma cells Phytother Res 26 2012 568 578
105. M. Hoare, A.R. Young, and M. Narita Autophagy in cancer: having your cake and eating it Semin Cancer Biol 21 2011 397 404
106. N. Mizushima, and B. Levine Autophagy in mammalian development and differentiation Nat Cell Biol 12 2010 823 830
107. A. Eisenberg-Lerner, and A. Kimchi The paradox of autophagy and its implication in cancer etiology and therapy Apoptosis 14 2009 376 391
108. H.M. Shen, and P. Codogno Autophagic cell death: Loch Ness monster or endangered species Autophagy 7 2011 457 465
109. D. Denton, S. Nicholson, and S. Kumar Cell death by autophagy: facts and apparent artifacts Cell Death Differ 19 2012 87 95
110. V. Giansanti, M. Tillhon, G. Mazzini, E. Prosperi, P. Lombardi, and A.I. Scovassi Killing of tumor cells: a drama in two acts Biochem Pharmacol 82 2011 1304 1310
111. N. Wang, Y. Feng, M. Zhu, C.M. Tsang, K. Man, and Y. Tong Berberine induces autophagic cell death and mitochondrial apoptosis in liver cancer cells: the cellular mechanism J Cell Biochem 111 2010 1426 1436
112. Q. Hou, X. Tang, H. Liu, J. Tang, Y. Yang, and X. Jing Berberine induces cell death in human hepatoma cells in vitro by downregulating CD147 Cancer Sci 102 2011 1287 1292
113. V. Giansanti, A. Torriglia, and A.I. Scovassi Conversation between apoptosis and autophagy: "Is it your turn or mine?" Apoptosis 16 2011 321 333