Matrine activates PTEN to induce growth inhibition and apoptosis in V600EBRAF harboring melanoma cells

International Journal of Molecular Sciences

Volumn 14, Issue 8, 2013, Pages 16040-16057

  Jin, Hui ^a   Sun, Yu ^b   Wang, Shuiying ^b   Cheng, Xiaodong ^a,b  

^a TONGJI UNIVERSITY   (China)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

V600EBRAF melanoma; Apoptosis; Cell cycle arrest; Matrine; PTEN

Indexed keywords

B RAF KINASE; CASPASE 3; CYCLIN D; DNA NUCLEOTIDYLEXOTRANSFERASE; MATRINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN P21;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE CHECKPOINT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; ENZYME ACTIVATION; FLOW CYTOMETRY; G0 G1 CELL CYCLE ARREST; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MELANOMA CELL; NICK END LABELING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ALKALOIDS; ANTHELMINTICS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOWN-REGULATION; ENZYME ACTIVATION; G1 PHASE CELL CYCLE CHECKPOINTS; HUMANS; MAP KINASE SIGNALING SYSTEM; MELANOMA; MITOCHONDRIA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; QUINOLIZINES; RNA, MESSENGER;

EID: 84881165246     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140816040     Document Type: Article

References (53)

1. Li, J.; Yen, C.; Liaw, D.; Podsypanina, K.; Bose, S.; Wang, S.I.; Puc, J.; Miliaresis, C.; Rodgers, L.; McCombie, R.; et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997, 275, 1943-1947.
2. Steck, P.A.; Pershouse, M.A.; Jasser, S.A.; Yung, W.K.; Lin, H.; Ligon, A.H.; Langford, L.A.; Baumgard, M.L.; Hattier, T.; Davis, T.; et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 1997, 15, 356-362.
3. Furnari, F.B.; Huang, H.J.; Cavenee, W.K. The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res. 1998, 58, 5002-5008.
4. Georgescu, M.M.; Kirsch, K.H.; Kaloudis, P.; Yang, H.; Pavletich, N.P.; Hanafusa, H. Stabilization and productive positioning roles of the C2 domain of PTEN tumor suppressor. Cancer Res. 2000, 60, 7033-7038.
5. Chalhoub, N.; Baker, S.J. PTEN and the PI3-kinase pathway in cancer. Annu. Rev. Pathol. 2009, 4, 127-150.
6. Garcia-Echeverria, C.; Sellers, W. Drug discovery approaches targeting the PI3K/Akt pathway in cancer. Oncogene 2008, 27, 5511-5526.
7. Lim, Y.; Han, I.; Kwon, H.; Oh, E. Trichostatin a-induced detransformation correlates with decreased focal adhesion kinase phosphorylation at tyrosine 861 inras-transformed fibroblasts. J. Biol. Chem. 2002, 277, 12735-12740.
8. Bali, P.; George, P.; Cohen, P.; Tao, J.; Guo, F.; Sigua, C.; Vishvanath, A.; Scuto, A.; Annavarapu, S.; Fiskus, W.; et al. Superior activity of the combination of histone deacetylase inhibitor LAQ824 and the FLT-3 kinase inhibitor PKC412 against human acute myelogenous leukemia cells with mutant FLT-3. Clin. Cancer Res. 2004, 10, 4991-4997.
9. Gan, Y.H.; Zhang, S. PTEN/AKT pathway involved in histone deacetylases inhibitor induced cell growth inhibition and apoptosis of oral squamous cell carcinoma cells. Oral Oncol. 2009, 45, e150-e154.
10. Stambolic, V.; MacPherson, D.; Sas, D.; Lin, Y.; Snow, B.; Jang, Y.; Benchimol, S.; Mak, T. Regulation of PTEN transcription by p53. Mol. Cell 2001, 8, 317-325.
11. Baron, V.; Adamson, E.D.; Calogero, A.; Ragona, G.; Mercola, D. The transcription factor Egr1 is a direct regulator of multiple tumor suppressors including TGFβ1, PTEN, p53, and fibronectin. Cancer Gene Ther. 2005, 13, 115-124.
12. Kim, S.; Domon-Dell, C.; Kang, J.; Chung, D.H.; Freund, J.N.; Evers, B.M. Down-regulation of the tumor suppressor PTEN by the tumor necrosis factor-α/nuclear factor-κB (NF-κB)-inducing kinase/NF-κB pathway is linked to a default IκB-α autoregulatory loop. J. Biol. Chem. 2004, 279, 4285-4291.
13. Ishola, T.A.; Kang, J.H.; Qiao, J.; Evers, B.M.; Chung, D.H. Phosphatidylinositol 3-kinase regulation of gastrin-releasing peptide-induced cell cycle progression in neuroblastoma cells. Biochim. Biophys. Acta (BBA) 2007, 1770, 927-932.
14. Vredeveld, L.C.; Possik, P.A.; Smit, M.A.; Meissl, K.; Michaloglou, C.; Horlings, H.M.; Ajouaou, A.; Kortman, P.C.; Dankort, D.; McMahon, M.; et al. Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Genes Dev. 2012, 26, 1055-1069.
15. Yajima, I.; Kumasaka, M.Y.; Thang, N.D.; Goto, Y.; Takeda, K.; Yamanoshita, O.; Iida, M.; Ohgami, N.; Tamura, H.; Kawamoto, Y.; et al. RAS/RAF/MEK/ERK and PI3K/PTEN/AKT signaling in malignant melanoma progression and therapy. Dermatol. Res. Pract. 2012, 354191:1-354191:5.
16. Jemal, A.; Siegel, R.; Ward, E.; Hao, Y.; Xu, J.; Thun, M.J. Cancer statistics, 2009. CA Cancer J. Clin. 2009, 59, 225-249.
17. Siegel, R.; Naishadham, D.; Jemal, A. Cancer statistics, 2012. CA Cancer J. Clin. 2012, 62, 10-29.
18. V600EBRAF. Oncogene 2012, 31, 446-457.
19. Daud, A.; Bastian, B.C. Beyond BRAF in melanoma. Curr. Top. Microbiol. Immunol. 2012, 355, 99-117.
20. Mehnert, J.M.; Kluger, H.M. Driver mutations in melanoma: Lessons learned from bench-to-bedside studies. Curr. Oncol. Rep. 2012, 14, 449-457.
21. Song, M.S.; Salmena, L.; Pandolfi, P.P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 2012, 13, 283-296.
22. Jiang, H.; Hou, C.; Zhang, S.; Xie, H.; Zhou, W.; Jin, Q.; Cheng, X.; Qian, R.; Zhang, X. Matrine upregulates the cell cycle protein E2F-1 and triggers apoptosis via the mitochondrial pathway in K562 cells. Eur. J. Pharmacol. 2007, 559, 98-108.
23. Yang, Y.; Xiu, J.; Zhang, X.; Zhang, L.; Yan, K.; Qin, C.; Liu, J. Antiviral effect of matrine against human enterovirus 71. Molecules 2012, 17, 10370-10376.
24. Suo, Z.; Liu, Y.; Ferreri, M.; Zhang, T.; Liu, Z.; Mu, X.; Han, B. Impact of matrine on inflammation related factors in rat intestinal microvascular endothelial cells. J. Ethnopharmacol. 2009, 125, 404-409.
25. Gao, H.Y.; Li, G.Y.; Lou, M.M.; Li, X.Y.; Wei, X.Y.; Wang, J.H. Hepatoprotective effect of Matrine salvianolic acid B salt on carbon tetrachloride-induced hepatic fibrosis. J. Inflamm. 2012, 9, 16:1-16:9.
26. Li, X.; Chu, W.; Liu, J.; Xue, X.; Lu, Y.; Shan, H.; Yang, B. Antiarrhythmic properties of long-term treatment with matrine in arrhythmic rat induced by coronary ligation. Biol. Pharm. Bull. 2009, 32, 1521-1526.
27. Zheng, H.; Chen, G.; Shi, L.; Lou, Z.; Chen, F.; Hu, J. Determination of oxymatrine and its metabolite matrine in rat blood and dermal microdialysates by high throughput liquid chromatography/tandem mass spectrometry. J. Pharm. Biomed. Anal. 2009, 49, 427-433.
28. Dai, Z.J.; Gao, J.; Ji, Z.Z.; Wang, X.J.; Ren, H.T.; Liu, X.X.; Wu, W.Y.; Kang, H.F.; Guan, H.T. Matrine induces apoptosis in gastric carcinoma cells via alteration of Fas/FasL and activation of caspase-3. J. Ethnopharmacol. 2009, 123, 91-96.
29. Han, Y.; Zhang, S.; Wu, J.; Yu, K.; Zhang, Y.; Yin, L.; Bi, L. Matrine induces apoptosis of human multiple myeloma cells via activation of the mitochondrial pathway. Leuk. Lymphoma 2010, 51, 1337-1346.
30. Li, H.; Tan, G.; Jiang, X.; Qiao, H.; Pan, S.; Jiang, H.; Kanwar, J.R.; Sun, X. Therapeutic effects of matrine on primary and metastatic breast cancer. Am. J. Chin. Med. 2010, 38, 1115-1130.
31. Zhang, J.Q.; Li, Y.M.; Liu, T.; He, W.T.; Chen, Y.T.; Chen, X.H.; Li, X.; Zhou, W.C.; Yi, J.F.; Ren, Z.J. Antitumor effect of matrine in human hepatoma G2 cells by inducing apoptosis and autophagy. World J. Gastroenterol. 2010, 16, 4281-4290.
32. Zhang, Z.; Wang, X.; Wu, W.; Wang, J.; Wang, Y.; Wu, X.; Fei, X.; Li, S.; Zhang, J.; Dong, P.; et al. Effects of matrine on proliferation and apoptosis in gallbladder carcinoma cells (GBC-SD). Phytother. Res. 2012, 26, 932-937.
33. Yang, C.L.; Liu, S.S.; Ma, Y.G.; Liu, Y.Y.; Xue, Y.X.; Huang, B. The influence of intraoperative pleural perfusion with matrine-cisplatin or cisplatin on stromal cell-derived factor-1 in non-small cell lung cancer patients with subclinical pleural metastasis. Med. Oncol. 2012, 29, 574-581.
34. Luo, C.; Zhong, H.J.; Zhu, L.M.; Wu, X.G.; Ying, J.E.; Wang, X.H.; Lu, W.X.; Xu, Q.; Zhu, Y.L.; Huang, J. Inhibition of matrine against gastric cancer cell line MNK45 growth and its anti-tumor mechanism. Mol. Biol. Rep. 2012, 39, 5459-5464.
35. Solit, D.B.; Garraway, L.A.; Pratilas, C.A.; Sawai, A.; Getz, G.; Basso, A.; Ye, Q.; Lobo, J.M.; She, Y.; Osman, I.; et al. BRAF mutation predicts sensitivity to MEK inhibition. Nature 2006, 439, 358-362.
36. Curtin, J.A.; Fridlyand, J.; Kageshita, T.; Patel, H.N.; Busam, K.J.; Kutzner, H.; Cho, K.H.; Aiba, S.; Brocker, E.B.; LeBoit, P.E.; et al. Distinct sets of genetic alterations in melanoma. N. Engl. J. Med. 2005, 353, 2135-2147.
37. Basile, K.J.; Aplin, A.E. Downregulation of Noxa by RAF/MEK inhibition counteracts cell death response in mutant B-RAF melanoma cells. Am. J. Cancer Res. 2012, 2, 726-735.
38. Heneberg, P. Dabrafenib: The new inhibitor of hyperactive B-RAF kinase. Klin. Onkol. 2012, 25, 333-339.
39. Kim, Y.K.; Ahn, S.K.; Lee, M. Differential sensitivity of melanoma cell lines with differing B-Raf mutational status to the new oncogenic B-Raf kinase inhibitor UI-152. Cancer Lett. 2012, 320, 215-224.
40. Konjevic, G.; Mirjacic Martinovic, K.; Vuletic, A.; Babovic, N. In-vitro IL-2 or IFN-α-induced NKG2D and CD161 NK cell receptor expression indicates novel aspects of NK cell activation in metastatic melanoma patients. Melanoma Res. 2010, 20, 459-467.
41. Trepiakas, R.; Berntsen, A.; Hadrup, S.R.; Bjorn, J.; Geertsen, P.F.; Straten, P.T.; Andersen, M.H.; Pedersen, A.E.; Soleimani, A.; Lorentzen, T.; et al. Vaccination with autologous dendritic cells pulsed with multiple tumor antigens for treatment of patients with malignant melanoma: Results from a phase I/II trial. Cytotherapy 2010, 12, 721-734.
42. Li, L.Q.; Li, X.L.; Wang, L.; Du, W.J.; Guo, R.; Liang, H.H.; Liu, X.; Liang, D.S.; Lu, Y.J.; Shan, H.L.; et al. Matrine inhibits breast cancer growth via miR-21/PTEN/Akt pathway in MCF-7 cells. Cell. Physiol. Biochem. 2012, 30, 631-641.
43. Liu, X.Y.; Fang, H.; Yang, Z.G.; Wang, X.Y.; Ruan, L.M.; Fang, D.R.; Ding, Y.G.; Wang, Y.N.; Zhang, Y.; Jiang, X.L.; et al. Matrine inhibits invasiveness and metastasis of human malignant melanoma cell line A375 in vitro. Int. J. Dermatol. 2008, 47, 448-456.
44. Dhawan, P.; Singh, A.B.; Ellis, D.L.; Richmond, A. Constitutive activation of Akt/protein kinase B in melanoma leads to up-regulation of nuclear factor-κB and tumor progression. Cancer Res. 2002, 62, 7335-7342.
45. Tsao, H.; Zhang, X.; Fowlkes, K.; Haluska, F.G. Relative reciprocity of NRAS and PTEN/MMAC1 alterations in cutaneous melanoma cell lines. Cancer Res. 2000, 60, 1800-1804.
46. Tsao, H.; Goel, V.; Wu, H.; Yang, G.; Haluska, F.G. Genetic interaction between NRAS and BRAF mutations and PTEN/MMAC1 inactivation in melanoma. J. Invest. Dermatol. 2004, 122, 337-341.
47. Conde-Perez, A.; Larue, L. PTEN and melanomagenesis. Future Oncol. 2012, 8, 1109-1120.
48. Deng, W.; Gopal, Y.N.; Scott, A.; Chen, G.; Woodman, S.E.; Davies, M.A. Role and therapeutic potential of PI3K-mTOR signaling in de novo resistance to BRAF inhibition. Pigment Cell Melanoma Res. 2012, 25, 248-258.
49. Paraiso, K.H.; Xiang, Y.; Rebecca, V.W.; Abel, E.V.; Chen, Y.A.; Munko, A.C.; Wood, E.; Fedorenko, I.V.; Sondak, V.K.; Anderson, A.R.; et al. PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res. 2011, 71, 2750-2760.
50. Wang, X.; Wang, Y.; Yu, L.; Sakakura, K.; Visus, C.; Schwab, J.H.; Ferrone, C.R.; Favoino, E.; Koya, Y.; Campoli, M.R.; et al. CSPG4 in cancer: Multiple roles. Curr. Mol. Med. 2010, 10, 419-429.
51. Gopal, Y.N.; Deng, W.; Woodman, S.E.; Komurov, K.; Ram, P.; Smith, P.D.; Davies, M.A. Basal and treatment-induced activation of AKT mediates resistance to cell death by AZD6244 (ARRY-142886) in Braf-mutant human cutaneous melanoma cells. Cancer Res. 2010, 70, 8736-8747.
52. Liu, X.-S.; Jiang, J.; Jiao, X.-Y.; Wu, Y.-E.; Lin, J.-H. Matrine-induced apoptosis in leukemia U937 cells: Involvement of caspases activation and MAPK-independent pathways. Planta Med. 2006, 72, 501-506.
53. Jin, H.; Liang, L.; Liu, L.; Deng, W.; Liu, J. HDAC inhibitor DWP0016 activates p53 transcription and acetylation to inhibit cell growth in U251 glioblastoma cells. J. Cell. Biochem. 2013, 114, 1498-1509.