Antitumor effects of the benzophenanthridine alkaloid sanguinarine: Evidence and perspectives

World Journal of Gastrointestinal Oncology

Volumn 8, Issue 1, 2016, Pages 30-39

  Gaziano, Roberta ^a   Moroni, Gabriella ^a   Buè, Cristina ^a   Miele, Martino Tony ^a   Sinibaldi Vallebona, Paola ^a   Pica, Francesca ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Apoptosis; Cancer; Cell cycle; Chemotherapy; Sanguinarine

Indexed keywords

EID: 84976293800     PISSN: None     EISSN: 19485204     Source Type: Journal    
DOI: 10.4251/wjgo.v8.i1.30     Document Type: Article

References (109)

1. 1 Hanahan D, Weinberg RA. The hallmarks of cancer. Cell2000; 100: 57-70 [PMID: 10647931 DOI: 10.1016/S0092-8674(00)8168 3-9]
2. 2 Reddy L, Odhav B, Bhoola KD. Natural products for cancer prevention: a global perspective. Pharmacol Ther2003; 99: 1-13 [PMID: 12804695 DOI: 10.1016/S0163-7258(03)00042-1]
3. 3 Dvorak Z, Kuban V, Kledjus B, Hlavac J, Vicar J, Ulrichova J, Simanek V. Quaternary benzo[c]phenanthridines sanguinarine and chelerythrine: a review of investigations from chemical and biological studies. Heterocycles2006; 68: 2403-2422 [DOI: 10.1002/chin.200709233]
4. 4 Dostàl J, Slavik J. Some aspects of the chemistry of quaternary benzo[c]phenanthridines alkaloids. Stud Nat Prod Chem2002; 27155-184 [DOI: 10.1016/S1572-5995(02)80036-9]
5. 5 Psotova J, Vecera R, Zdarilova A, Anzebacherova E, Kosina P, Svobodova A, Hrbac J, Jirovsky D, Stiborova M, Lichnovsky V. Safety assessment of sanguitrin, alkaloid fraction of Macleaya cordata, in rats. Vet Med2006; 51: 145-155
6. 6 Kosina P, Walterová D, Ulrichová J, Lichnovský V, Stiborová M, Rýdlová H, Vicar J, Krecman V, Brabec MJ, Simánek V. Sanguinarine and chelerythrine: assessment of safety on pigs in ninety days feeding experiment. Food Chem Toxicol2004; 42: 85-91 [PMID: 14630132 DOI: 10.1007/s11101-013-9290-8]
7. 7 Slaninova I, Pencikova K, Urbanova J, Slanina J, Taborska E. Antitumor activities of sanguinarine and related alkaloids. Phytochem Rev2014; 13: 51-68 [DOI: 10.1007/s1101-013-9290-8]
8. 8 Miao F, Yang XJ, Zhou L, Hu HJ, Zheng F, Ding XD, Sun DM, Zhou CD, Sun W. Structural modification of sanguinarine and chelerythrine and their antibacterial activity. Nat Prod Res2011; 25: 863-875 [PMID: 21491327 DOI: 10.1080/14786419.2010.482055]
9. 9 Yang XJ, Miao F, Yao Y, Cao FJ, Yang R, Ma YN, Qin BF, Zhou L. In vitro antifungal activity of sanguinarine and chelerythrine derivatives against phytopathogenic fungi. Molecules2012; 17: 13026-13035 [PMID: 23124471 DOI: 10.3390/molecules1711130 26]
10. 10 Lenfeld J, Kroutil M, Marsálek E, Slavík J, Preininger V, Simánek V. Antiinflammatory activity of quaternary benzophenanthridine alkaloids from Chelidonium majus. Planta Med1981; 43: 161-165 [PMID: 7312984]
11. 11 Tan GT, Pezzuto JM, Kinghorn AD, Hughes SH. Evaluation of natural products as inhibitors of human immunodeficiency virus type 1 (HIV-1) reverse transcriptase. J Nat Prod1991; 54: 143-154 [PMID: 1710653]
12. 12 Tsai IL, Wun MF, Teng CM, Ishikawa T, Chen IS. Anti-platelet aggregation constituents from Formosan Toddalia asiatica. Phytochemistry1998; 48: 1377-1382 [PMID: 9720317 DOI: 10.1016/S0031-9422(97)00678-X]
13. 13 Eun JP, Koh GY. Suppression of angiogenesis by the plant alkaloid, sanguinarine. Biochem Biophys Res Commun2004; 317: 618-624 [PMID: 15063803 DOI: 10.1016/j.bbrc.2004.03.077]
14. 14 Miao F, Yang XJ, Ma YN, Zheng F, Song XP, Zhou L. Structural modification of sanguinarine and chelerythrine and their in vitro acaricidal activity against Psoroptes cuniculi. Chem Pharm Bull (Tokyo) 2012; 60: 1508-1513 [PMID: 23000953 DOI: 10.1248/cpb. c12-00618]
15. 15 Yao JY, Li XL, Shen JY, Pan XY, Hao GJ, Xu Y, Ying WL, Ru HS, Liu XL. Isolation of bioactive components from Chelidonium majus L. with activity against Trichodina sp. Aquaculture2011; 318: 235-238 [DOI: 10.1016/j.aquaculture.2011.04.035]
16. 16 Wang GX, Zhou Z, Jiang DX, Han J, Wang JF, Zhao LW, Li J. In vivo anthelmintic activity of five alkaloids from Macleaya microcarpa (Maxim) Fedde against Dactylogyrus intermedius in Carassius auratus. Vet Parasitol2010; 171: 305-313 [PMID: 20413222 DOI: 10.1016/j.vetpar.2010.03.032]
17. 17 Steller H. Mechanisms and genes of cellular suicide. Science1995; 267: 1445-1449 [PMID: 7878463 DOI: 10.1126/science.7878463]
18. 18 Meier P, Finch A, Evan G. Apoptosis in development. Nature2000; 407: 796-801 [PMID: 11048731 DOI: 10.1038/35037734]
19. 19 Ahsan H, Reagan-Shaw S, Breur J, Ahmad N. Sanguinarine induces apoptosis of human pancreatic carcinoma AsPC-1 and BxPC-3 cells via modulations in Bcl-2 family proteins. Cancer Lett2007; 249: 198-208 [PMID: 17005319 DOI: 10.1016/j.canlet.2006.08.018]
20. 20 Choi WY, Kim GY, Lee WH, Choi YH. Sanguinarine, a benzophenanthridine alkaloid, induces apoptosis in MDA-MB-231 human breast carcinoma cells through a reactive oxygen speciesmediated mitochondrial pathway. Chemotherapy2008; 54: 279-287 [PMID: 18667818 DOI: 10.1159/000149719]
21. 21 Han MH, Kim GY, Yoo YH, Choi YH. Sanguinarine induces apoptosis in human colorectal cancer HCT-116 cells through ROS-mediated Egr-1 activation and mitochondrial dysfunction. Toxicol Lett2013; 220: 157-166 [PMID: 23660334 DOI: 10.1016/j.toxlet.2013.04.020]
22. 22 Jang BC, Park JG, Song DK, Baek WK, Yoo SK, Jung KH, Park GY, Lee TY, Suh SI. Sanguinarine induces apoptosis in A549 human lung cancer cells primarily via cellular glutathione depletion. Toxicol In Vitro2009; 23: 281-287 [PMID: 19135517 DOI: 10.1016/j.tiv.2008.12.013]
23. 23 Ahmad N, Gupta S, Husain MM, Heiskanen KM, Mukhtar H. Differential antiproliferative and apoptotic response of sanguinarine for cancer cells versus normal cells. Clin Cancer Res2000; 6: 1524-1528 [PMID: 10778985]
24. 24 Adhami VM, Aziz MH, Mukhtar H, Ahmad N. Activation of prodeath Bcl-2 family proteins and mitochondrial apoptosis pathway by sanguinarine in immortalized human HaCaT keratinocytes. Clin Cancer Res2003; 9: 3176-3182 [PMID: 12912970]
25. 25 Reagan-Shaw S, Breur J, Ahmad N. Enhancement of UVB radiation-mediated apoptosis by sanguinarine in HaCaT human immortalized keratinocytes. Mol Cancer Ther2006; 5: 418-429 [PMID: 16505117 DOI: 10.1158/1535-7163.MCT-05-0250]
26. 26 Malíková J, Zdarilová A, Hlobilková A, Ulrichová J. The effect of chelerythrine on cell growth, apoptosis, and cell cycle in human normal and cancer cells in comparison with sanguinarine. Cell Biol Toxicol2006; 22: 439-453 [PMID: 16964588 DOI: 10.1007/s10565-006-0109-x]
27. 27 Adhami VM, Aziz MH, Reagan-Shaw SR, Nihal M, Mukhtar H, Ahmad N. Sanguinarine causes cell cycle blockade and apoptosis of human prostate carcinoma cells via modulation of cyclin kinase inhibitor-cyclin-cyclin-dependent kinase machinery. Mol Cancer Ther2004; 3: 933-940 [PMID: 15299076]
28. 28 Huh J, Liepins A, Zielonka J, Andrekopoulos C, Kalyanaraman B, Sorokin A. Cyclooxygenase 2 rescues LNCaP prostate cancer cells from sanguinarine-induced apoptosis by a mechanism involving inhibition of nitric oxide synthase activity. Cancer Res2006; 66: 3726-3736 [PMID: 16585199 DOI: 10.1158/0008-5472. CAN-05-4033]
29. 29 Ding Z, Tang SC, Weerasinghe P, Yang X, Pater A, Liepins A. The alkaloid sanguinarine is effective against multidrug resistance in human cervical cells via bimodal cell death. Biochem Pharmacol2002; 63: 1415-1421 [PMID: 11996882 DOI: 10.1016/S0006-2952 (02)00902-4]
30. 30 Debiton E, Madelmont JC, Legault J, Barthomeuf C. Sanguinarineinduced apoptosis is associated with an early and severe cellular glutathione depletion. Cancer Chemother Pharmacol2003; 51: 474-482 [PMID: 12700925]
31. 31 Holy J, Lamont G, Perkins E. Disruption of nucleocytoplasmic trafficking of cyclin D1 and topoisomerase II by sanguinarine. BMC Cell Biol2006; 7: 13 [PMID: 16512916 DOI: 10.1186/147-2121-7-13]
32. 32 Dong XZ, Zhang M, Wang K, Liu P, Guo DH, Zheng XL, Ge XY. Sanguinarine inhibits vascular endothelial growth factor release by generation of reactive oxygen species in MCF-7 human mammary adenocarcinoma cells. Biomed Res Int2013; 2013: 517698 [PMID: 23762849 DOI: 10.1155/2013/517698]
33. 33 Kalogris C, Garulli C, Pietrella L, Gambini V, Pucciarelli S, Lucci C, Tilio M, Zabaleta ME, Bartolacci C, Andreani C, Giangrossi M, Iezzi M, Belletti B, Marchini C, Amici A. Sanguinarine suppresses basal-like breast cancer growth through dihydrofolate reductase inhibition. Biochem Pharmacol2014; 90: 226-234 [PMID: 24875448 DOI: 10.1016/j.bcp.2014.05.014]
34. 34 Han MH, Yoo YH, Choi YH. Sanguinarine-induced apoptosis in human leukemia U937 cells via Bcl-2 downregulation and caspase-3 activation. Chemotherapy2008; 54: 157-165 [PMID: 18560221 DOI: 10.1159/000140359]
35. 35 Weerasinghe P, Hallock S, Tang SC, Liepins A. Role of Bcl-2 family proteins and caspase-3 in sanguinarine-induced bimodal cell death. Cell Biol Toxicol2001; 17: 371-381 [PMID: 11787859]
36. 36 Hussain AR, Al-Jomah NA, Siraj AK, Manogaran P, Al-Hussein K, Abubaker J, Platanias LC, Al-Kuraya KS, Uddin S. Sanguinarinedependent induction of apoptosis in primary effusion lymphoma cells. Cancer Res2007; 67: 3888-3897 [PMID: 17440103 DOI: 10.1158/0008-5472.CAN-06-3764]
37. 37 Burgeiro A, Bento AC, Gajate C, Oliveira PJ, Mollinedo F. Rapid human melanoma cell death induced by sanguinarine through oxidative stress. Eur J Pharmacol2013; 705: 109-118 [PMID: 23499690 DOI: 10.1016/j.ejphar.2013.02.035]
38. 38 Hammerová J, Uldrijan S, Táborská E, Slaninová I. Benzo[c] phenanthridine alkaloids exhibit strong anti-proliferative activity in malignant melanoma cells regardless of their p53 status. J Dermatol Sci2011; 62: 22-35 [PMID: 21324654 DOI: 10.1016/j. jdermsci.2011.01.006]
39. 39 Serafim TL, Matos JA, Sardão VA, Pereira GC, Branco AF, Pereira SL, Parke D, Perkins EL, Moreno AJ, Holy J, Oliveira PJ. Sanguinarine cytotoxicity on mouse melanoma K1735-M2 cells–nuclear vs. mitochondrial effects. Biochem Pharmacol2008; 76: 1459-1475 [PMID: 18692024 DOI: 10.1016/j.bcp.2008.07.013]
40. 40 Lee JS, Jung WK, Jeong MH, Yoon TR, Kim HK. Sanguinarine induces apoptosis of HT-29 human colon cancer cells via the regulation of Bax/Bcl-2 ratio and caspase-9-dependent pathway. Int J Toxicol2012; 31: 70-77 [PMID: 22215411 DOI: 10.1177/109158 1811423845]
41. 41 Matkar SS, Wrischnik LA, Hellmann-Blumberg U. Sanguinarine causes DNA damage and p53-independent cell death in human colon cancer cell lines. Chem Biol Interact2008; 172: 63-71 [PMID: 18243168 DOI: 10.1016/j.cbi.2007.12.006]
42. 42 Choi WY, Jin CY, Han MH, Kim GY, Kim ND, Lee WH, Kim SK, Choi YH. Sanguinarine sensitizes human gastric adenocarcinoma AGS cells to TRAIL-mediated apoptosis via down-regulation of AKT and activation of caspase-3. Anticancer Res2009; 29: 4457-4465 [PMID: 20032392]
43. 43 Larsson DE, Wickström M, Hassan S, Oberg K, Granberg D. The cytotoxic agents NSC-95397, brefeldin A, bortezomib and sanguinarine induce apoptosis in neuroendocrine tumors in vitro. Anticancer Res2010; 30: 149-156 [PMID: 20150630]
44. 44 Park H, Bergeron E, Senta H, Guillemette K, Beauvais S, Blouin R, Sirois J, Faucheux N. Sanguinarine induces apoptosis of human osteosarcoma cells through the extrinsic and intrinsic pathways. Biochem Biophys Res Commun2010; 399: 446-451 [PMID: 20678472 DOI: 10.1016/j.bbrc.2010.07.114]
45. 45 Cecen E, Altun Z, Ercetin P, Aktas S, Olgun N. Promoting effects of sanguinarine on apoptotic gene expression in human neuroblastoma cells. Asian Pac J Cancer Prev2014; 15: 9445-9451 [PMID: 25422239 DOI: 10.7314/APJCP.2014.15.21.9445]
46. 46 Deroussent A, Ré M, Hoellinger H, Cresteil T. Metabolism of sanguinarine in human and in rat: characterization of oxidative metabolites produced by human CYP1A1 and CYP1A2 and rat liver microsomes using liquid chromatography-tandem mass spectrometry. J Pharm Biomed Anal2010; 52: 391-397 [PMID: 19804952 DOI: 10.1016/j.jpba.2009.09.014]
47. 47 Lopez Lozano MJ, Rios Santos V, Bullon Fernandez P. [Effectiveness of chemical products as antiplaque agents]. Rev Eur Odontoestomatol1991; 3: 115-122 [PMID: 1867730]
48. 48 De Stefano I, Raspaglio G, Zannoni GF, Travaglia D, Prisco MG, Mosca M, Ferlini C, Scambia G, Gallo D. Antiproliferative and antiangiogenic effects of the benzophenanthridine alkaloid sanguinarine in melanoma. Biochem Pharmacol2009; 78: 1374-1381 [PMID: 19643088 DOI: 10.1016/j.bcp.2009.07.011]
49. 49 Pica F, Balestrieri E, Serafino A, Sorrentino R, Gaziano R, Moroni G, Moroni N, Palmieri G, Mattei M, Garaci E, Sinibaldi-Vallebona P. Antitumor effects of the benzophenanthridine alkaloid sanguinarine in a rat syngeneic model of colorectal cancer. Anticancer Drugs2012; 23: 32-42 [PMID: 21849887 DOI: 10.1097/CAD.0b013e32834a0c8e]
50. 50 Chaturvedi MM, Kumar A, Darnay BG, Chainy GB, Agarwal S, Aggarwal BB. Sanguinarine (pseudochelerythrine) is a potent inhibitor of NF-kappaB activation, IkappaBalpha phosphorylation, and degradation. J Biol Chem1997; 272: 30129-30134 [PMID: 9374492 DOI: 10.1074/jbc.272.48.30129]
51. 51 Malikova J, Zdarilova A, Hlobilkova A. Effects of sanguinarine and chelerythrine on the cell cycle and apoptosis. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub2006; 150: 5-12 [PMID: 16936897]
52. 52 Kim S, Lee TJ, Leem J, Choi KS, Park JW, Kwon TK. Sanguinarine-induced apoptosis: generation of ROS, down-regulation of Bcl-2, c-FLIP, and synergy with TRAIL. J Cell Biochem2008; 104: 895-907 [PMID: 18189268 DOI: 10.1002/jcb.21672]
53. 53 Xu JY, Meng QH, Chong Y, Jiao Y, Zhao L, Rosen EM, Fan S. Sanguinarine inhibits growth of human cervical cancer cells through the induction of apoptosis. Oncol Rep2012; 28: 2264-2270 [PMID: 22965493 DOI: 10.3892/or.2012.2024]
54. 54 Xu ZW, Friess H, Büchler MW, Solioz M. Overexpression of Bax sensitizes human pancreatic cancer cells to apoptosis induced by chemotherapeutic agents. Cancer Chemother Pharmacol2002; 49: 504-510 [PMID: 12107556 DOI: 10.1007/s00280-002-0435-5]
55. 55 Reed JC. Bcl-2: prevention of apoptosis as a mechanism of drug resistance. Hematol Oncol Clin North Am1995; 9: 451-473 [PMID: 7642473]
56. 56 Slaninová I, Slanina J, Táborská E. Quaternary benzo[c]phenanthridine alkaloids–novel cell permeant and red fluorescing DNA probes. Cytometry A2007; 71: 700-708 [PMID: 17549765 DOI: 10.1002/cyto.a.20423]
57. 57 Saran A, Srivastava S, Coutinho E, Maiti M. 1H NMR investigation of the interaction of berberine and sanguinarine with DNA. Indian J Biochem Biophys1995; 32: 74-77 [PMID: 7642203]
58. 58 Chang MC, Chan CP, Wang YJ, Lee PH, Chen LI, Tsai YL, Lin BR, Wang YL, Jeng JH. Induction of necrosis and apoptosis to KB cancer cells by sanguinarine is associated with reactive oxygen species production and mitochondrial membrane depolarization. Toxicol Appl Pharmacol2007; 218: 143-151 [PMID: 17196629 DOI: 10.1016/j.taap.2006.10.025]
59. 59 Carmody RJ, Cotter TG. Signalling apoptosis: a radical approach. Redox Rep2001; 6: 77-90 [PMID: 11450987 DOI: 10.1179/135100 001101536085]
60. 60 Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist Updat2004; 7: 97-110 [PMID: 15158766 DOI: 10.1016/j.drup.2004.01.004]
61. 61 Simon L, Szilágyi G, Bori Z, Telek G, Magyar K, Nagy Z. Low dose (-)deprenyl is cytoprotective: it maintains mitochondrial membrane potential and eliminates oxygen radicals. Life Sci2005; 78: 225-231 [PMID: 16242156 DOI: 10.1016/j.lfs.2005.04.078]
62. 62 Skulachev VP. Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis2006; 11: 473-485 [PMID: 16532373 DOI: 10.1007/s10495-006-5881-9]
63. 63 Kim IH, Kim SW, Kim SH, Lee SO, Lee ST, Kim DG, Lee MJ, Park WH. Parthenolide-induced apoptosis of hepatic stellate cells and anti-fibrotic effects in an in vivo rat model. Exp Mol Med2012; 44: 448-456 [PMID: 22581380 DOI: 10.3858/emm.2012.44.7.051]
64. 64 Karin M. NF-kappaB as a critical link between inflammation and cancer. Cold Spring Harb Perspect Biol2009; 1: a000141 [PMID: 20066113 DOI: 10.1101/cshperspect.a000141]
65. 65 Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell2002; 109 Suppl: S81-S96 [PMID: 11983155 DOI: 10.1016/S0092-8674(02)00703-1]
66. 66 Sun M, Liu C, Nadiminty N, Lou W, Zhu Y, Yang J, Evans CP, Zhou Q, Gao AC. Inhibition of Stat3 activation by sanguinarine suppresses prostate cancer cell growth and invasion. Prostate2012; 72: 82-89 [PMID: 21538419 DOI: 10.1002/pros.21409]
67. 67 Basini G, Bussolati S, Santini SE, Grasselli F. Sanguinarine inhibits VEGF-induced angiogenesis in a fibrin gel matrix. Biofactors2007; 29: 11-18 [PMID: 17611290]
68. 68 Xu JY, Meng QH, Chong Y, Jiao Y, Zhao L, Rosen EM, Fan S. Sanguinarine is a novel VEGF inhibitor involved in the suppression of angiogenesis and cell migration. Mol Clin Oncol2013; 1: 331-336 [PMID: 24649171 DOI: 10.3892/mco.2012.41]
69. 69 Basini G, Santini SE, Bussolati S, Grasselli F. The plant alkaloid sanguinarine is a potential inhibitor of follicular angiogenesis. J Reprod Dev2007; 53: 573-579 [PMID: 17310078]
70. 70 Ellis LM, Hicklin DJ. VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer2008; 8: 579-591 [PMID: 18596824 DOI: 10.1038/nrc2403]
71. 71 Lev DC, Ruiz M, Mills L, McGary EC, Price JE, Bar-Eli M. Dacarbazine causes transcriptional up-regulation of interleukin 8 and vascular endothelial growth factor in melanoma cells: a possible escape mechanism from chemotherapy. Mol Cancer Ther2003; 2753-763 [PMID: 12939465]
72. 72 Lev DC, Onn A, Melinkova VO, Miller C, Stone V, Ruiz M, McGary EC, Ananthaswamy HN, Price JE, Bar-Eli M. Exposure of melanoma cells to dacarbazine results in enhanced tumor growth and metastasis in vivo. J Clin Oncol2004; 22: 2092-2100 [PMID: 15123733 DOI: 10.1200/JCO.2004.11.070]
73. 73 Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell2010; 140: 883-899 [PMID: 20303878 DOI: 10.1016/j.cell.2010.01.025]
74. 74 Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol2001; 17: 463-516 [PMID: 11687497 DOI: 10.1146/annurev.cellbio.17.1.463]
75. 75 Jiang MC, Liao CF, Lee PH. Aspirin inhibits matrix metalloproteinase-2 activity, increases E-cadherin production, and inhibits in vitro invasion of tumor cells. Biochem Biophys Res Commun2001; 282: 671-677 [PMID: 11401513 DOI: 10.1006/bbrc.2001.4637]
76. 76 Cox TR, Erler JT. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech2011; 4: 165-178 [PMID: 21324931 DOI: 10.1242/dmm.004 077]
77. 77 Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev2006; 25: 9-34 [PMID: 16680569 DOI: 10.1007/s10555-006-7886-9]
78. 78 Jinga DC, Blidaru A, Condrea I, Ardeleanu C, Dragomir C, Szegli G, Stefanescu M, Matache C. MMP-9 and MMP-2 gelatinases and TIMP-1 and TIMP-2 inhibitors in breast cancer: correlations with prognostic factors. J Cell Mol Med2006; 10: 499-510 [PMID: 16796815 DOI: 10.1111/j.1582-4934.2006.tb00415.x]
79. 79 Scorilas A, Karameris A, Arnogiannaki N, Ardavanis A, Bassilopoulos P, Trangas T, Talieri M. Overexpression of matrixmetalloproteinase-9 in human breast cancer: a potential favourable indicator in node-negative patients. Br J Cancer2001; 84: 1488-1496 [PMID: 11384099 DOI: 10.1054/bjoc.2001.1810]
80. 80 Xu X, Wang Y, Chen Z, Sternlicht MD, Hidalgo M, Steffensen B. Matrix metalloproteinase-2 contributes to cancer cell migration on collagen. Cancer Res2005; 65: 130-136 [PMID: 15665288]
81. 81 Park SY, Jin ML, Kim YH, Lee SJ, Park G. Sanguinarine inhibits invasiveness and the MMP-9 and COX-2 expression in TPA-induced breast cancer cells by inducing HO-1 expression. Oncol Rep2014; 31: 497-504 [PMID: 24220687 DOI: 10.3892/or.2013.2843]
82. 82 Abdulghani J, Gu L, Dagvadorj A, Lutz J, Leiby B, Bonuccelli G, Lisanti MP, Zellweger T, Alanen K, Mirtti T, Visakorpi T, Bubendorf L, Nevalainen MT. Stat3 promotes metastatic progression of prostate cancer. Am J Pathol2008; 172: 1717-1728 [PMID: 18483213 DOI: 10.2353/ajpath.2008.071054]
83. 83 Itoh M, Murata T, Suzuki T, Shindoh M, Nakajima K, Imai K, Yoshida K. Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells. Oncogene2006; 25: 1195-1204 [PMID: 16205632 DOI: 10.1038/sj.onc.1209149]
84. 84 Silver DL, Naora H, Liu J, Cheng W, Montell DJ. Activated signal transducer and activator of transcription (STAT) 3: localization in focal adhesions and function in ovarian cancer cell motility. Cancer Res2004; 64: 3550-3558 [PMID: 15150111 DOI: 10.1158/0008-54 72.CAN-03-3959]
85. 85 Möller M, Weiss J, Wink M. Reduction of cytotoxicity of the alkaloid emetine through P-glycoprotein (MDR1/ABCB1) in human Caco-2 cells and leukemia cell lines. Planta Med2006; 72: 1121-1126 [PMID: 16783693 DOI: 10.1055/s-2006-941546]
86. 86 Ma Y, Wink M. Lobeline, a piperidine alkaloid from Lobelia can reverse P-gp dependent multidrug resistance in tumor cells. Phytomedicine2008; 15: 754-758 [PMID: 18222670 DOI: 10.1016/j.phymed.2007.11.028]
87. 87 El-Readi MZ, Hamdan D, Farrag N, El-Shazly A, Wink M. Inhibition of P-glycoprotein activity by limonin and other secondary metabolites from Citrus species in human colon and leukaemia cell lines. Eur J Pharmacol2010; 626: 139-145 [PMID: 19782062 DOI: 10.1016/j.ejphar.2009.09.040]
88. 88 Li S, Lei Y, Jia Y, Li N, Wink M, Ma Y. Piperine, a piperidine alkaloid from Piper nigrum re-sensitizes P-gp, MRP1 and BCRP dependent multidrug resistant cancer cells. Phytomedicine2011; 19: 83-87 [PMID: 21802927 DOI: 10.1016/j.phymed.2011.06.031]
89. 89 Wink M, Ashour ML, El-Readi MZ. Secondary Metabolites from Plants Inhibiting ABC Transporters and Reversing Resistance of Cancer Cells and Microbes to Cytotoxic and Antimicrobial Agents. Front Microbiol2012; 3: 130 [PMID: 22536197 DOI: 10.3389/fmicb.2012.00130]
90. 90 Li JH. [A study on treatment of lung cancer by combined therapy of traditional Chinese medicine and chemotherapy]. Zhongguo Zhong Xi Yi Jie He Za Zhi1996; 16: 136-138 [PMID: 9208532]
91. 91 Cai HB, Dai FG, Min QF, Shi M, Miao JX, Luo RC. [Clinical study of the effects of radiotherapy in combination with traditional Chinese medicine on non-small cell lung cancer]. Di Yi Jun Yi Da Xue Xue Bao2002; 22: 1112-1113 [PMID: 12480588]
92. 92 Efferth T, Davey M, Olbrich A, Rücker G, Gebhart E, Davey R. Activity of drugs from traditional Chinese medicine toward sensitive and MDR1-or MRP1-overexpressing multidrug-resistant human CCRF-CEM leukemia cells. Blood Cells Mol Dis2002; 28: 160-168 [PMID: 12064912 DOI: 10.1006/bcmd.2002.0492]
93. 93 Eid SY, El-Readi MZ, Wink M. Synergism of three-drug combinations of sanguinarine and other plant secondary metabolites with digitonin and doxorubicin in multi-drug resistant cancer cells. Phytomedicine2012; 19: 1288-1297 [PMID: 23146422 DOI: 10.1016/j.phymed.2012.08.010]
94. 94 Choy CS, Cheah KP, Chiou HY, Li JS, Liu YH, Yong SF, Chiu WT, Liao JW, Hu CM. Induction of hepatotoxicity by sanguinarine is associated with oxidation of protein thiols and disturbance of mitochondrial respiration. J Appl Toxicol2008; 28: 945-956 [PMID: 18548746 DOI: 10.1002/jat.1360]
95. 95 Hu CM, Cheng HW, Cheng YW, Kang JJ. Induction of skeletal muscle contracture and calcium release from isolated sarcoplasmic reticulum vesicles by sanguinarine. Br J Pharmacol2000; 130: 299-306 [PMID: 10807666 DOI: 10.1038/sj.bjp.0703279]
96. 96 Hu CM, Cheng HW, Cheng YW, Kan JJ. Mechanisms underlying the induction of vasorelaxation in rat thoracic aorta by sanguinarine. Jpn J Pharmacol2001; 85: 47-53 [PMID: 11243574]
97. 97 Hu CM, Cheng YW, Liao JW, Cheng HW, Kang JJ. Induction of contracture and extracellular Ca2+ influx in cardiac muscle by sanguinarine: a study on cardiotoxicity of sanguinarine. J Biomed Sci2005; 12: 399-407 [PMID: 15920678 DOI: 10.1007/s11373-005-3007-y]
98. 98 Chan WH. Embryonic toxicity of sanguinarine through apoptotic processes in mouse blastocysts. Toxicol Lett2011; 205: 285-292 [PMID: 21722720 DOI: 10.1016/j.toxlet.2011.06.018]
99. 99 Kaminskyy V, Lin KW, Filyak Y, Stoika R. Differential effect of sanguinarine, chelerythrine and chelidonine on DNA damage and cell viability in primary mouse spleen cells and mouse leukemic cells. Cell Biol Int2008; 32: 271-277 [PMID: 18029203 DOI: 10.1016/j.cellbi.2007.09.004]
100. 100 Das M, Khanna SK. Clinicoepidemiological, toxicological, and safety evaluation studies on argemone oil. Crit Rev Toxicol1997; 27: 273-297 [PMID: 9189656 DOI: 10.3109/10408449709089896]
101. 101 Hakim SA. Argemone oil, sanguinarine, and epidemic-dropsy glaucoma. Br J Ophthalmol1954; 38: 193-216 [PMID: 13149763 DOI: 10.1136/bjo.38.4.193]
102. 102 Hakim SA. Argemone oil, sanguinarine, dropsy, glaucoma and cancer. Indian Pract1967; 20: 129-141 [PMID: 6037511]
103. 103 Das M, Ansari KM, Dhawan A, Shukla Y, Khanna SK. Correlation of DNA damage in epidemic dropsy patients to carcinogenic potential of argemone oil and isolated sanguinarine alkaloid in mice. Int J Cancer2005; 117: 709-717 [PMID: 15981203 DOI: 10.1002/ijc.21234]
104. 104 Ansari KM, Dhawan A, Khanna SK, Das M. In vivo DNA damaging potential of sanguinarine alkaloid, isolated from argemone oil, using alkaline Comet assay in mice. Food Chem Toxicol2005; 43: 147-153 [PMID: 15582207 DOI: 10.1016/j.fct.2004.09.005]
105. 105 Anderson KM, Stoner GD, Fields HW, Chacon GE, Dohar AL, Gregg BR, Mallery SR. Immunohistochemical assessment of Viadent-associated leukoplakia. Oral Oncol2005; 41: 200-207 [PMID: 15695122 DOI: 10.1016/j.oraloncology.2004.08.008]
106. 106 Damm DD, Curran A, White DK, Drummond JF. Leukoplakia of the maxillary vestibule–an association with Viadent? Oral Surg Oral Med Oral Pathol Oral Radiol Endod1999; 87: 61-66 [PMID: 9927082 DOI: 10.1016/S1079-2104(99)70296-9]
107. 107 Karp JM, Rodrigo KA, Pei P, Pavlick MD, Andersen JD, McTigue DJ, Fields HW, Mallery SR. Sanguinarine activates polycyclic aromatic hydrocarbon associated metabolic pathways in human oral keratinocytes and tissues. Toxicol Lett2005; 158: 50-60 [PMID: 15993743 DOI: 10.1016/j.toxlet.2005.02.007]
108. 108 Wang M, Thanou M. Targeting nanoparticles to cancer. Pharmacol Res2010; 62: 90-99 [PMID: 20380880 DOI: 10.1016/j.phrs.2010.0 3.005]
109. 109 Li W, Li H, Yao H, Mu Q, Zhao G, Li Y, Hu H, Niu X. Pharmaco-kinetic and anti-inflammatory effects of sanguinarine solid lipid nanoparticles. Inflammation2014; 37: 632-638 [PMID: 24272172 DOI: 10.1007/s10753-013-9779-8]