A gene expression signature-based approach reveals the mechanisms of action of the Chinese herbal medicine berberine

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Lee, Kuen Haur ^a   Lo, Hsiang Ling ^a   Tang, Wan Chun ^a   Hsiao, Heidi Hao Yun ^a   Yang, Pei Ming ^a  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BERBERINE; HERBACEOUS AGENT; HISTONE DEACETYLASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; TUBULIN; TUMOR MARKER;

APOPTOSIS; BREAST NEOPLASMS; CELL CYCLE; CELL MOTION; CELL PROLIFERATION; DNA MICROARRAY; DRUG EFFECTS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

AMP-ACTIVATED PROTEIN KINASES; APOPTOSIS; BERBERINE; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DRUGS, CHINESE HERBAL; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASES; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUBULIN; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 84923324365     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06394     Document Type: Article

References (59)

1. Tillhon, M., Guaman Ortiz, L. M., Lombardi, P. & Scovassi, A. I. Berberine: new perspectives for old remedies. Biochem. Pharmacol. 84, 1260-1267 (2012).
2. Iizuka, N. et al. Inhibitory effect of Coptidis Rhizoma and berberine on the proliferation of human esophageal cancer cell lines. Cancer Lett. 148, 19-25 (2000).
3. Liu, B. et al. Berberine inhibits human hepatoma cell invasion without cytotoxicity in healthy hepatocytes. PLoS One 6, e21416 (2011).
4. Mantena, S. K., Sharma, S. D. &Katiyar, S. K. Berberine, a natural product, induces G1-phase cell cycle arrest and caspase-3-dependent apoptosis in human prostate carcinoma cells. Mol. Cancer Ther. 5, 296-308 (2006).
5. Peng, P. L., Hsieh, Y. S., Wang, C. J., Hsu, J. L. & Chou, F. P. 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 (2006).
6. Wang, L. et al. Berberine inhibits proliferation and down-regulates epidermal growth factor receptor through activation of Cbl in colon tumor cells. PLoS One 8, e56666 (2013).
7. Lee, Y. S. et al. Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55, 2256-2264 (2006).
8. Kim, H. S. et al. Berberine-induced AMPK activation inhibits the metastatic potential of melanoma cells via reduction of ERK activity and COX-2 protein expression. Biochem. Pharmacol. 83, 385-394 (2012).
9. Park, J. J. et al. Berberine inhibits human colon cancer cell migration via AMPactivated protein kinase-mediated downregulation of integrin beta1 signaling. Biochem. Biophys. Res. Commun. 426, 461-467 (2012).
10. Yang, X. & Huang, N. Berberine induces selective apoptosis through the AMPKmediated mitochondrial/caspase pathway in hepatocellular carcinoma. Mol Med Rep 8, 505-510 (2013).
11. Lehrmann, H., Pritchard, L. L. & Harel-Bellan, A. Histone acetyltransferases and deacetylases in the control of cell proliferation and differentiation. Adv. Cancer Res. 86, 41-65 (2002).
12. Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074-1080 (2001).
13. Xu, W. S., Parmigiani, R. B. & Marks, P. A. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26, 5541-5552 (2007).
14. Campas-Moya, C. Romidepsin for the treatment of cutaneous T-cell lymphoma. Drugs Today (Barc) 45, 787-795 (2009).
15. Mann, B. S., Johnson, J. R., Cohen, M. H., Justice, R. & Pazdur, R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12, 1247-1252 (2007).
16. Lamb, J. et al. The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 313, 1929-1935 (2006).
17. Fayad, W. et al. Identification of a novel topoisomerase inhibitor effective in cells overexpressing drug efflux transporters. PLoS One 4, e7238 (2009).
18. Gheeya, J. et al. Expression profiling identifies epoxy anthraquinone derivative as a DNA topoisomerase inhibitor. Cancer Lett. 293, 124-131 (2010).
19. Hieronymus, H. et al. Gene expression signature-based chemical genomic prediction identifies a novel class of HSP90 pathway modulators. Cancer Cell 10, 321-330 (2006).
20. Wen, Z. et al. Discovery of molecular mechanisms of traditional Chinese medicinal formula Si-Wu-Tang using gene expression microarray and connectivity map. PLoS One 6, e18278 (2011).
21. Lo, T. F., Tsai, W. C. & Chen, S. T. MicroRNA-21-3p, a berberine-induced miRNA, directly down-regulates humanmethionine adenosyltransferases 2A and 2B and inhibits hepatoma cell growth. PLoS One 8, e75628 (2013).
22. Kuhn, M. et al. STITCH 4: integration of protein-chemical interactions with user data. Nucleic Acids Res. 42, D401-407 (2014).
23. de Haro, C., Mendez, R. & Santoyo, J. The eIF-2alpha kinases and the control of protein synthesis. FASEB J. 10, 1378-1387 (1996).
24. Hoyer-Hansen, M. & Jaattela, M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ. 14, 1576-1582 (2007).
25. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544 (2012).
26. Mizushima, N. et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657-668 (2001).
27. Mizushima, N. et al. Aprotein conjugation system essential for autophagy. Nature 395, 395-398 (1998).
28. Meijer, A. J. & Dubbelhuis, P. F. Amino acid signalling and the integration of metabolism. Biochem. Biophys. Res. Commun. 313, 397-403 (2004).
29. Inoki, K., Zhu, T. & Guan, K. L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115, 577-590 (2003).
30. Matsui, Y. et al. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ. Res. 100, 914-922 (2007).
31. Manning, B. D. &Cantley, L. C. United at last: the tuberous sclerosis complex gene products connect the phosphoinositide 3-kinase/Akt pathway to mammalian target of rapamycin (mTOR) signalling. Biochem. Soc. Trans. 31, 573-578 (2003).
32. Sangeetha, S., Ranjitha, S., Murugan, K. & Kumar, G. R. Breast Cancer Specific Histone Deacetylase Inhibitors and Lead Discovery using Molecular Docking and Descriptor Study. Trends in Bioinformatics 6 (2013).
33. Dokmanovic, M., Clarke, C. & Marks, P. A. Histone deacetylase inhibitors: overview and perspectives. Mol. Cancer Res. 5, 981-989 (2007).
34. Sauve, A. A., Wolberger, C., Schramm, V. L. & Boeke, J. D. The biochemistry of sirtuins. Annu. Rev. Biochem. 75, 435-465 (2006).
35. Hubbert, C. et al. HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458 (2002).
36. Krishnakumar, R. & Kraus, W. L. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 39, 8-24 (2010).
37. Li, C. Specific cell cycle synchronization with butyrate and cell cycle analysis. Methods Mol. Biol. 761, 125-136 (2011).
38. Kuo, L. J. & Yang, L. X. Gamma-H2AX-a novel biomarker for DNA doublestrand breaks. In Vivo 22, 305-309 (2008).
39. Jabbarzadeh Kaboli, P., Rahmat, A., Ismail, P. & Ling, K. H. Targets and mechanisms of berberine, a natural drug with potential to treat cancer with special focus on breast cancer. Eur. J. Pharmacol. 740C, 584-595 (2014).
40. Wen, C. J. et al. Genomic screening for targets regulated by berberine in breast cancer cells. Asian Pac. J. Cancer Prev. 14, 6089-6094 (2013).
41. Chou, H. C. et al. Proteomic and redox-proteomic analysis of berberine-induced cytotoxicity in breast cancer cells. J. Proteomics 75, 3158-3176 (2012).
42. Li, S., Zhang, B., Jiang, D.,Wei, Y. &Zhang, N. Herb network construction and comodule analysis for uncovering the combination rule of traditional Chinese herbal formulae. BMC Bioinformatics 11 Suppl 11, S6 (2010).
43. Liang, X., Li, H. & Li, S. A novel network pharmacology approach to analyse traditional herbal formulae: the Liu-Wei-Di-Huang pill as a case study. Mol Biosyst 10, 1014-1022 (2014).
44. Zhang, B. et al. Vitexicarpin acts as a novel angiogenesis inhibitor and its target network. Evid. Based Complement. Alternat. Med. 2013, 278405 (2013).
45. Zhang, B., Wang, X. & Li, S. An Integrative Platform of TCM Network Pharmacology and Its Application on a Herbal Formula, Qing-Luo-Yin. Evid. Based Complement. Alternat. Med. 2013, 456747 (2013).
46. Paolini, G. V., Shapland, R. H., van Hoorn, W. P., Mason, J. S. & Hopkins, A. L. Global mapping of pharmacological space. Nat. Biotechnol. 24, 805-815 (2006).
47. Hopkins, A. L. Network pharmacology: the next paradigm in drug discovery. Nat. Chem. Biol. 4, 682-690 (2008).
48. Yildirim, M. A., Goh, K. I., Cusick, M. E., Barabasi, A. L. & Vidal, M. Drug-target network. Nat. Biotechnol. 25, 1119-1126 (2007).
49. Ennis, H. L. & Lubin, M. Cycloheximide: Aspects of Inhibition of Protein Synthesis in Mammalian Cells. Science 146, 1474-1476 (1964).
50. Nandi, R., Debnath, D. & Maiti, M. Interactions of berberine with poly(A) and tRNA. Biochim. Biophys. Acta 1049, 339-342 (1990).
51. Khan, M. et al. Berberine and a Berberis lycium extract inactivate Cdc25A and induce alpha-tubulin acetylation that correlate with HL-60 cell cycle inhibition and apoptosis. Mutat. Res. 683, 123-130 (2010).
52. Marcus, A. I. et al. The synergistic combination of the farnesyl transferase inhibitor lonafarnib and paclitaxel enhances tubulin acetylation and requires a functional tubulin deacetylase. Cancer Res. 65, 3883-3893 (2005).
53. Piperno, G., LeDizet, M. & Chang, X. J. Microtubules containing acetylated alphatubulin in mammalian cells in culture. J. Cell Biol. 104, 289-302 (1987).
54. Liu, Y. L. et al. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy 6, 1057-1065 (2010).
55. Yang, P. M. et al. Inhibition of autophagy enhances anticancer effects of atorvastatin in digestive malignancies. Cancer Res. 70, 7699-7709 (2010).
56. Yang, P. M. & Chen, C. C. Life or death? Autophagy in anticancer therapies with statins and histone deacetylase inhibitors. Autophagy 7, 107-108 (2011).
57. Jones, K. R. et al. p53-Dependent accelerated senescence induced by ionizing radiation in breast tumour cells. Int. J. Radiat. Biol. 81, 445-458 (2005).
58. Wang, N. et al. Berberine induces autophagic cell death and mitochondrial apoptosis in liver cancer cells: the cellular mechanism. J. Cell. Biochem. 111, 1426-1436 (2010).
59. Yu, R. et al. Berberine-induced apoptotic and autophagic death of HepG2 cells requires AMPK activation. Cancer Cell Int. 14, 49 (2014).