Antitumor effects of the combination of cholesterol reducing drugs

Oncology Reports

Volumn 26, Issue 1, 2011, Pages 169-176

  Issat, Tadeusz ^a,b   Nowis, Dominika ^a   Bil, Jacek ^a   Winiarska, Magdalena ^a   Jakobisiak, Marek ^a   Golab, Jakub ^a,c  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF MOTHER AND CHILD   (Poland)

^c INSTITUTE OF PHYSICAL CHEMISTRY   (Poland)

Author keywords

Berberine; Lovastatin; Prenylation; Tumor

Indexed keywords

BERBERINE; MEVINOLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DOSE RESPONSE; DRUG CYTOTOXICITY; DRUG POTENTIATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VIVO STUDY; MONOTHERAPY; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN FARNESYLATION; PROTEIN GERANYLGERANYLATION; PROTEIN MODIFICATION; PROTEIN PRENYLATION;

ANIMALS; ANTICHOLESTEREMIC AGENTS; ANTINEOPLASTIC AGENTS; BERBERINE; CELL CYCLE; CELL LINE, TUMOR; DRUG THERAPY, COMBINATION; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LOVASTATIN; MEVALONIC ACID; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; NEOPLASMS;

EID: 79955866863     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2011.1261     Document Type: Article

References (64)

1. Pedersen TR, Kjekshus J, Berg K, Haghfelt T, Faergeman O, Faergeman G, Pyörälä K, Miettinen T, Wilhelmsen L, Olsson AG and Wedel H; Scandinavian Simvastatin Survival Study Group: Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4S). Atheroscler Suppl 5: 81-87, 2004
2. Sacks FM, Pfeffer MA, Moye LA, Rouleau JL, Rutherford JD, Cole TG, Brown L, Warnica JW, Arnold JM, Wun CC, Davis BR and Braunwald E: The effect of pravastatin on coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events Trial investigators. N Engl J Med 335: 1001-1009, 1996. (Pubitemid 26338729)
3. Velasco JA: After 4S, CARE and LIPID - is evidence-based medicine being practised? Atherosclerosis 9: 147, 1999.
4. Kusama T, Mukai M, Iwasaki T, Tatsuta M, Matsumoto Y, Akedo H, Inoue M and Nakamura H: 3-Hydroxy-3-methylglutaryl-coenzyme a reductase inhibitors reduce human pancreatic cancer cell invasion and metastasis. Gastroenterology 122: 308-317, 2002. (Pubitemid 34116983)
5. Denoyelle C, Vasse M, Körner M, Mishal Z, Ganné F, Vannier JP, Soria J and Soria C: Cerivastatin, an inhibitor of HMG-CoA reductase, inhibits the signaling pathways involved in the invasiveness and metastatic properties of highly invasive breast cancer cell lines: an in vitro study. Carcinogenesis 22: 1139-1148, 2001. (Pubitemid 32737327)
6. Williams TM and Lisanti MP: Caveolin-1 in oncogenic transfor-mation, cancer, and metastasis. Am J Physiol Cell Physiol 288: C494-C506, 2005. (Pubitemid 40229478)
7. Nissen SE, Tuzcu EM, Schoenhagen P, Brown BG, Ganz P, Vogel RA, Crowe T, Howard G, Cooper CJ, Brodie B, Grines CL, DeMaria AN and REVERSAL Investigators: Effect of intensive compared with moderate lipid-lowering therapy on progression of coronary atherosclerosis: a randomized controlled trial. JAMA 291: 1071-1080, 2004. (Pubitemid 38541684)
8. Waters D, Schwartz GG and Olsson AG: The myocardial ischemia reduction with acute cholesterol lowering (MIRACL) trial: a new frontier for statins? Curr Control Trials Cardiovasc Med 2: 111-114, 2001. (Pubitemid 32600514)
9. Lamprecht J, Wójcik C, Jakóbisiak M, Stoehr M, Schrorter D and Paweletz N: Lovastatin induces mitotic abnormalities in various cell lines. Cell Biol Int 23: 51-60, 1999. (Pubitemid 29516353)
10. MacDonald JS, Gerson RJ, Kornbrust DJ, Kloss MW, Prahalada S, Berry PH, Alberts AW and Bokelman DL: Preclinical evaluation of lovastatin. Am J Cardiol 62: J16-J27, 1988.
11. Newman TB and Hulley SB: Carcinogenicity of lipid-lowering drugs. JAMA 275: 55-60, 1996.
12. Downs JR, Clearfield M, Weis S, Whitney E, Shapiro DR, Beere PA, Langendorfer A, Stein EA, Kruyer W and Gotto AM Jr: Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS. Air Force/Texas Coronary Atherosclerosis Prevention Study. JAMA 279: 1615-1622, 1998.
13. Reid IR, Hague W, Emberson J, Baker J, Tonkin A, Hunt D, MacMahon S and Sharpe N: Effect of pravastatin on frequency of fracture in the LIPID study: secondary analysis of a randomised controlled trial. Long-term Intervention with Pravastatin in Ischaemic Disease. Lancet 357: 509-512, 2001. (Pubitemid 32173587)
14. Kaye JA, Meier CR, Walker AM and Jick H: Statin use, hyperlipidaemia, and the risk of breast cancer. Br J Cancer 86: 1436-1439, 2002. (Pubitemid 34548066)
15. Poynter JN, Gruber SB, Higgins PD, Almog R, Bonner JD, Rennert HS, Low M, Greenson JK and Rennert G: Statins and the risk of colorectal cancer. N Engl J Med 352: 2184-2192, 2005.
16. Clearfield M, Downs JR, Weis S, Whitney EJ, Kruyer W, Shapiro DR, Stein EA, Langendorfer A, Beere PA and Gotto AM: Air Force/Texas Coronary Atherosclerosis Prevention Study (AFCAPS/TexCAPS): efficacy and tolerability of long-term treatment with lovastatin in women. J Womens Health Gend Based Med 10: 971-981, 2001. (Pubitemid 34065628)
17. Graaf MR, Beiderbeck AB, Egberts AC, Richel DJ and Guchelaar HJ: The risk of cancer in users of statins. J Clin Oncol 22: 2388-2394, 2004. (Pubitemid 41115396)
18. Coogan PF, Rosenberg L, Palmer JR, Strom BL, Zauber AG and Shapiro S: Statin use and the risk of breast and prostate cancer. Epidemiology 13: 262-267, 2002. (Pubitemid 34415845)
19. Ivanovska N and Philipov S: Study on the anti-inflammatory action of Berberis vulgaris root extract, alkaloid fractions and pure alkaloids. Int J Immunopharmacol 18: 553-561, 1996. (Pubitemid 27105918)
20. Yeşilada E and Küpeli E: Berberis crataegina root exhibits potent anti-inflammatory, analgesic and febrifuge effects in mice and rats. J Ethnopharmacol 79: 237-248, 2002.
21. Kong W, Wei J, Abidi P, Lin M, Inaba S, Li C, Wang Y, Wang Z, Si S, Pan H, Wang S, Wu J, Wing Y, Li Z, Liu J and Jiang JD: Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 10: 1344-1351, 2004. (Pubitemid 40022716)
22. Youn MJ, So HS, Cho HJ, Kim HJ, Kim Y, Lee JH, Sohn JS, Kim YK, Chung SY and Park R: Berberine, a natural product, combined with cisplatin enhanced apoptosis through a mitochondria/caspase-mediated pathway in HeLa cells. Biol Pharm Bull 31: 789-795, 2008. (Pubitemid 351731963)
23. Lin HL, Liu TY, Wu CW and Chi CW: Berberine modulates expression of mdr1 gene product and the responses of digestive track cancer cells to Paclitaxel. Br J Cancer 81: 416-422, 1999.
24. Wang XN, Han X, Xu LN, Yin LH, Xu YW, Qi Y and Peng JY: Enhancement of apoptosis of human hepatocellular carcinoma SMMC-7721 cells through synergy of berberine and evodiamine. Phytomedicine 15: 1062-1068, 2008.
25. Gołab J, Stokłosa T, Zagozdzon R, Kaca A, Giermasz A, Pojda Z, Machaj E, Dabrowska A, Feleszko W, Lasek W, Iwan-Osiecka A and Jakóbisiak M: G-CSF prevents the suppression of bone marrow hematopoiesis induced by IL-12 and augments its antitumor activity in a melanoma model in mice. Ann Oncol 9: 63-69, 1998.
26. Chou TC and Talalay P: Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55, 1984.
27. Issat T, Jakóbisiak M and Golab J: Berberine, a natural cholesterol reducing product, exerts antitumor cytostatic/cytotoxic effects independently from the mevalonate pathway. Oncol Rep 16: 1273-1276, 2006.
28. Dimitroulakos J, Nohynek D, Backway KL, Hedley DW, Yeger H, Freedman MH, Minden MD and Penn LZ: Increased sensitivity of acute myeloid leukemias to lovastatin-induced apoptosis: a potential therapeutic approach. Blood 93: 1308-1318, 1999. (Pubitemid 29076146)
29. Agarwal B, Rao CV, Bhendwal S, Ramey WR, Shirin H, Reddy BS and Holt PR: Lovastatin augments sulindac-induced apoptosis in colon cancer cells and potentiates chemopreventive effects of sulindac. Gastroenterology 117: 838-847, 1999. (Pubitemid 29468226)
30. Feleszko W, Młynarczuk I, Olszewska D, Jalili A, Grzela T, Lasek W, Hoser G, Korczak-Kowalska G and Jakóbisiak M: Lovastatin potentiates antitumor activity of doxorubicin in murine melanoma via an apoptosis-dependent mechanism. Int J Cancer 100: 111-118, 2002. (Pubitemid 34602074)
31. Jakóbisiak M, Bruno S, Skierski JS and Darzynkiewicz Z: Cell cycle-specific effects of lovastatin. Proc Natl Acad Sci USA 88: 3628-3632, 1991.
32. Rao S, Porter DC, Chen X, Herliczek T, Lowe M and Keyomarsi K: Lovastatin-mediated G1 arrest is through inhibition of the proteasome, independent of hydroxymethyl glutaryl-CoA reductase. Proc Natl Acad Sci USA 96: 7797-7802, 1999. (Pubitemid 29328361)
33. Bouterfa HL, Sattelmeyer V, Czub S, Vordermark D, Roosen K and Tonn JC: Inhibition of Ras farnesylation by lovastatin leads to down-regulation of proliferation and migration in primary cultured human glioblastoma cells. Anticancer Res 20: 2761-2771, 2000. (Pubitemid 30614496)
34. DeClue JE, Vass WC, Papageorge AG, Lowy DR and Willumsen BM: Inhibition of cell growth by lovastatin is independent of ras function. Cancer Res 51: 712-717, 1991.
35. Crick DC, Andres DA, Danesi R, Macchia M and Waechter CJ: Geranylgeraniol overcomes the block of cell proliferation by lovastatin in C6 glioma cells. J Neurochem 70: 2397-2405, 1998. (Pubitemid 28252365)
36. Rao S, Lowe M, Herliczek TW and Keyomarsi K: Lovastatin mediated G1 arrest in normal and tumor breast cells is through inhibition of CDK2 activity and redistribution of p21 and p27, independent of p53. Oncogene 17: 2393-2402, 1998. (Pubitemid 28515393)
37. Gray-Bablin J, Rao S and Keyomarsi K: Lovastatin induction of cyclin-dependent kinase inhibitors in human breast cells occurs in a cell cycle-independent fashion. Cancer Res 57: 604-669, 1997.
38. Park WH, Lee YY, Kim ES, Seol JG, Jung CW, Lee CC and Kim BK: Lovastatin-induced inhibition of HL-60 cell proliferation via cell cycle arrest and apoptosis. Anticancer Res 19: 3133-3140, 1999. (Pubitemid 30042600)
39. Oda H, Kasiske BL, O'Donnell MP and Keane WF: Effects of lovastatin on expression of cell cycle regulatory proteins in vascular smooth muscle cells. Kidney Int (Suppl) 71: S202-S205, 1999. (Pubitemid 29304852)
40. Naderi S, Blomhoff R, Myklebust J, Smeland EB, Erikstein B, Norum KR and Blomhoff HK: Lovastatin inhibits G1/S transition of normal human B-lymphocytes independent of apoptosis. Exp Cell Res 252: 144-153, 1999. (Pubitemid 29485134)
41. Feleszko W, Mlynarczuk I, Balkowiec-Iskra EZ, Czajka A, Switaj T, Stoklosa T, Giermasz A and Jakóbisiak M: Lovastatin potentiates antitumor activity and attenuates cardiotoxicity of doxorubicin in three tumor models in mice. Clin Cancer Res 6: 2044-2052, 2000. (Pubitemid 30305104)
42. Rozados VR, Hinrichsen LI, Binda MM, Gervasoni SI, Matar P, Bonfil RD and Scharovsky OG: Lovastatin enhances the antitumoral and apoptotic activity of doxorubicin in murine tumor models. Oncol Rep 19: 1205-1211, 2008.
43. Werner M, Sacher J and Hohenegger M: Mutual amplification of apoptosis by statin-induced mitochondrial stress and doxorubicin toxicity in human rhabdomyosarcoma cells. Br J Pharmacol 143: 715-724, 2004. (Pubitemid 39611607)
44. Feleszko W, Zagozdzon R, Gołab J and Jakóbisiak M: Potentiated antitumour effects of cisplatin and lovastatin against MmB16 melanoma in mice. Eur J Cancer 34: 406-411, 1998. (Pubitemid 28183843)
45. Kozar K, Kaminski R, Legat M, Kopec M, Nowis D, Skierski JS, Koronkiewicz M, Jakóbisiak M and Golab J: Cerivastatin demonstrates enhanced antitumor activity against human breast cancer cell lines when used in combination with doxorubicin or cisplatin. Int J Oncol 24: 1149-1157, 2004.
46. Mantha AJ, McFee KE, Niknejad N, Goss G, Lorimer IA and Dimitroulakos J: Epidermal growth factor receptor-targeted therapy potentiates lovastatin-induced apoptosis in head and neck squamous cell carcinoma cells. J Cancer Res Clin Oncol 129: 631-641, 2003. (Pubitemid 37452629)
47. Wang W, Collie-Duguid E and Cassidy J: Cerivastatin enhances the cytotoxicity of 5-fluorouracil on chemosensitive and resistant colorectal cancer cell lines. FEBS Lett 531: 415-420, 2002. (Pubitemid 35336061)
48. Orfila L, Rodríguez M, Colman T, Hasegawa M, Merentes E and Arvelo F: Structural modification of berberine alkaloids in relation to cytotoxic activity in vitro. J Ethnopharmacol 71: 449-456, 2000. (Pubitemid 30642868)
49. Eom KS, Hong JM, Youn MJ, So HS, Park R, Kim JM and Kim TY: Berberine induces G1 arrest and apoptosis in human glioblastoma T98G cells through mitochondrial/caspases pathway. Biol Pharm Bull 31: 558-562, 2008. (Pubitemid 351500476)
50. Piyanuch R, Sukhthankar M, Wandee G and Back SJ: Berberine, a natural isoquinoline alkaloid, induces NAG-1 and ATF3 expression in human colorectal cancer cells. Cancer Lett 258: 230-240, 2007. (Pubitemid 350110378)
51. Meeran SM, Katiyar S and Katiyar SK: Berberine-induced apoptosis in human prostate cancer cells is initiated by reactive oxygen species generation. Toxicol Appl Pharmacol 229: 33-43, 2008.
52. Lin JP, Yang JS, Lee JH, Hsieh WT and Chung JG: Berberine induces cell cycle arrest and apoptosis in human gastric carcinoma SNU-5 cell line. World J Gastroenterol 12: 21-28, 2006.
53. Katiyar SK, Meeran SM, Katiyar N and Akhtar S: 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 Carcinogenesis 48: 24-37, 2009.
54. Lin S, Tsai SC, Lee CC, Wang BW, Liou JY and Shyu KG: Berberine inhibits HIF-1alpha expression via enhanced proteolysis. Mol Pharmacol 66: 612-619, 2004. (Pubitemid 39329260)
55. Lin JP, Yang JS, Wu CC, Lin SS, Hsieh WT, Lin ML, Yu FS, Yu CS, Chen GW, Chang YH and Chung JG: Berberine induced down-regulation of matrix metalloproteinase-1, -2 and -9 in human gastric cancer cells (SNU-5) in vitro. In Vivo 22: 223-230, 2008.
56. Kim S, Choi JH, Kim JB, Nam SJ, Yang JH, Kim JH and Lee JE: 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, 2008.
57. Ho YT, Yang JS, Li TC, Lin JJ, Lin JG, Lai KC, Ma CY, Wood WG and Chung JG: Berberine suppresses in vitro migration and invasion of human SCC-4 tongue squamous cancer cells through the inhibitions of FAK, IKK, NF-κB, u-PA and MMP-2 and -9. Cancer Lett 279: 155-162, 2009.
58. Peng PL, Hsieh YS, Wang CJ, Hsu JL and Chou FP: 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.
59. Mitani N and Murakami K: Inhibitory effect of berberine on the mediastinal lymph node metastasis. Cancer Lett 165: 35-42, 2001.
60. Li H, Guo L, Jie S, Liu W, Zhu J, Du W, Fan L, Wang X, Fu B and Huang S: 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: 573-578, 2008.
61. Kong WJ, Wei J, Zuo ZY, Wang YM, Song DQ, You XF, Zhao LX, Pan HN and Jiang JD: Combination of simvastatin with berberine improves the lipid-lowering efficacy. Metabolism 57: 1029-1037, 2008. (Pubitemid 351978060)
62. Bjerre LM and LeLorier J: Do statins cause cancer? A meta-analysis of large randomized clinical trials. Am J Med 110: 716-723, 2001. (Pubitemid 32524321)
63. Dale KM, Coleman CL, Henyan NN, Kluger J and White CM: Statins and cancer risk: a meta-analysis. JAMA 295: 74-80, 2006. (Pubitemid 43042692)
64. Winiarska M, Bil J, Wilczek E, Wilczynski GM, Lekka M, Engelberts PJ, Mackus WJ, Gorska E, Bojarski L, Stoklosa T, Nowis D, Kurzaj Z, Makowski M, Glodkowska E, Issat T, Mrowka P, Lasek W, Dabrowska-Iwanicka A, Basak GW, Wasik M, Warzocha K, Sinski M, Gaciong Z, Jakobisiak M, Parren PW and Golab J: Statins impair antitumor effects of rituximab by inducing conformational changes of CD20. PLoS Med 5: e64, 2008.