Bioactive tanshinones in Salvia miltiorrhiza inhibit the growth of prostate cancer cells in vitro and in mice

International Journal of Cancer

Volumn 129, Issue 5, 2011, Pages 1042-1052

  Gong, Yi ^a   Li, Yanli ^a   Lu, Yin ^a,b   Li, Linglin ^a   Abdolmaleky, Hamid ^a   Blackburn, George L ^a   Zhou, Jin Rong ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

angiogenesis; apoptosis; Aurora A; chemoprevention; proliferation; prostate cancer; tanshinones

Indexed keywords

AURORA A KINASE; CRYPTOTANSHINONE; TANSHINONE I; TANSHINONE IIA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL CYCLE ARREST; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; SALVIA MILTIORRHIZA;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BLOTTING, WESTERN; CELL ADHESION; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; DITERPENES, ABIETANE; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MICE; MICE, SCID; PHENANTHRENES; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SALVIA MILTIORRHIZA; TUMOR CELLS, CULTURED;

EID: 79959767855     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25678     Document Type: Article

References (49)

1. Eisenberg DM, Davis RB, Ettner SL,. Trends in alternative medicine use in the United States, 1990-1997: results of a follow-up national survey. JAMA 1998; 280: 1569-75. (Pubitemid 28520643)
2. Zhou L, Zuo Z, Chow MS,. Danshen: an overview of its chemistry, pharmacology, pharmacokinetics, and clinical use. J Clin Pharmacol 2005; 45: 1345-59. (Pubitemid 41643896)
3. Mosaddik MA,. In vitro cytotoxicity of tanshinones isolated from Salvia miltiorrhiza Bunge against P388 lymphocytic leukemia cells. Phytomedicine 2003; 10: 682-5. (Pubitemid 37500097)
4. Song Y, Yuan SL, Yang YM, Wang XJ, Huang GQ,. Alteration of activities of telomerase in tanshinone IIA inducing apoptosis of the leukemia cells. Zhongguo Zhong Yao Za Zhi 2005; 30: 207-11. (Pubitemid 44366792)
5. Sung HJ, Choi SM, Yoon Y, An KS,. Tanshinone IIA, an ingredient of Salvia miltiorrhiza BUNGE, induces apoptosis in human leukemia cell lines through the activation of caspase-3. Exp Mol Med 1999; 31: 174-8. (Pubitemid 30021333)
6. Yoon Y, Kim YO, Jeon WK, Park HJ, Sung HJ,. Tanshinone IIA isolated from Salvia miltiorrhiza BUNGE induced apoptosis in HL60 human premyelocytic leukemia cell line. J Ethnopharmacol 1999; 68: 121-7. (Pubitemid 29502468)
7. Lee CY, Sher HF, Chen HW, Liu CC, Chen CH, Lin CS, Yang PC, Tsay HS, Chen JJ,. Anticancer effects of tanshinone I in human non-small cell lung cancer. Mol Cancer Ther 2008; 7: 3527-38.
8. Nizamutdinova IT, Lee GW, Son KH, Jeon SJ, Kang SS, Kim YS, Lee JH, Seo HG, Chang KC, Kim HJ,. Tanshinone I effectively induces apoptosis in estrogen receptor-positive (MCF-7) and estrogen receptor-negative (MDA-MB-231) breast cancer cells. Int J Oncol 2008; 33: 485-91.
9. Wang X, Wei Y, Yuan S, Liu G, Lu Y, Zhang J, Wang W,. Potential anticancer activity of tanshinone IIA against human breast cancer. Int J Cancer 2005; 116: 799-807. (Pubitemid 41099713)
10. Su CC, Lin YH,. Tanshinone IIA inhibits human breast cancer cells through increased Bax to Bcl-xL ratios. Int J Mol Med 2008; 22: 357-61.
11. Yuan S, Wang Y, Chen X, Song Y, Yang Y,. A study on apoptosis of nasopharyngeal carcinoma cell line induced by Tanshinone II A and its molecular mechanism. Hua Xi Yi Ke Da Xue Xue Bao 2002; 33: 84-6, 90.
12. Wang J, Wang X, Jiang S, Yuan S, Lin P, Zhang J, Lu Y, Wang Q, Xiong Z, Wu Y, Ren J, Yang H,. Growth inhibition and induction of apoptosis and differentiation of tanshinone IIA in human glioma cells. J Neurooncol 2007; 82: 11-21.
13. Liu JJ, Zhang Y, Lin DJ, Xiao RZ,. Tanshinone IIA inhibits leukemia THP-1 cell growth by induction of apoptosis. Oncol Rep 2009; 21: 1075-81.
14. Yuan SL, Wei YQ, Wang XJ, Xiao F, Li SF, Zhang J,. Growth inhibition and apoptosis induction of tanshinone II-A on human hepatocellular carcinoma cells. World J Gastroenterol 2004; 10: 2024-8. (Pubitemid 39106951)
15. Wang X, Yuan S, Huang R, Song Y,. An observation of the effect of tanshinone on cancer cell proliferation by Brdu and PCNA labeling. Hua Xi Yi Ke Da Xue Xue Bao 1996; 27: 388-91. (Pubitemid 27028572)
16. Wang X, Yuan S, Wang C,. A preliminary study of the anti-cancer effect of tanshinone on hepatic carcinoma and its mechanism of action in mice. Zhonghua Zhong Liu Za Zhi 1996; 18: 412-4.
17. Zhang P, Pei Y, Qi Y,. Influence of blood-activating drugs on adhesion and invasion of cells in lung cancer patients. Zhongguo Zhong Xi Yi Jie He Za Zhi 1999; 19: 103-5.
18. Lee WY, Chiu LC, Yeung JH,. Cytotoxicity of major tanshinones isolated from Danshen (Salvia miltiorrhiza) on HepG2 cells in relation to glutathione perturbation. Food Chem Toxicol 2008; 46: 328-38. (Pubitemid 350235777)
19. Singh AV, Franke AA, Blackburn GL, Zhou JR,. Soy phytochemicals prevent orthotopic growth and metastasis of bladder cancer in mice by alterations of cancer cell proliferation and apoptosis and tumor angiogenesis. Cancer Res 2006; 66: 1851-8. (Pubitemid 43259972)
20. Zhou J-R, Mukherjee P, Gugger ET, Tanaka T, Blackburn GL, Clinton SK,. The inhibition of murine bladder tumorigenesis by soy isoflavones via alterations in the cell cycle, apoptosis, and angiogenesis. Cancer Res 1998; 58: 5231-8. (Pubitemid 28521187)
21. Mai Z, Blackburn GL, Zhou JR,. Genistein sensitizes inhibitory effect of tamoxifen on the growth of estrogen receptor-positive and HER2-overexpressing human breast cancer cells. Mol Carcinog 2007; 46: 534-42. (Pubitemid 47068072)
22. Lentini L, Amato A, Schillaci T, Insalaco L, Di Leonardo A,. Aurora-A transcriptional silencing and vincristine treatment show a synergistic effect in human tumor cells. Oncol Res 2008; 17: 115-25. (Pubitemid 352006265)
23. Huh JE, Lee EO, Kim MS, Kang KS, Kim CH, Cha BC, Surh YJ, Kim SH,. Penta-O-galloyl-beta-D-glucose suppresses tumor growth via inhibition of angiogenesis and stimulation of apoptosis: roles of cyclooxygenase-2 and mitogen-activated protein kinase pathways. Carcinogenesis 2005; 26: 1436-45.
24. Zhou J-R, Yu L, Zerbini LF, Libermann TA, Blackburn GL,. Progression to androgen-independent LNCaP human prostate tumors: cellular and molecular alterations. Int J Cancer 2004; 81: 800-6. (Pubitemid 38758504)
25. Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, Ford LG, Parnes HL, Minasian LM, Gaziano JM, Hartline JA, Parsons JK, Bearden JD, III, et al. Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 2009; 301: 39-51.
26. Thompson IM, Goodman PJ, Tangen CM, Lucia MS, Miller GJ, Ford LG, Lieber MM, Cespedes RD, Atkins JN, Lippman SM, Carlin SM, Ryan A, et al. The influence of finasteride on the development of prostate cancer. N Engl J Med 2003; 349: 215-24. (Pubitemid 36859473)
27. Gomella LG,. Chemoprevention using dutasteride: the REDUCE trial. Curr Opin Urol 2005; 15: 29-32. (Pubitemid 40105522)
28. Kaestner P, Stolz A, Bastians H,. Determinants for the efficiency of anticancer drugs targeting either Aurora-A or Aurora-B kinases in human colon carcinoma cells. Mol Cancer Ther 2009; 8: 2046-56.
29. Vankayalapati H, Bearss DJ, Saldanha JW, Munoz RM, Rojanala S, Von Hoff DD, Mahadevan D,. Targeting aurora2 kinase in oncogenesis: a structural bioinformatics approach to target validation and rational drug design. Mol Cancer Ther 2003; 2: 283-94.
30. Marumoto T, Zhang D, Saya H,. Aurora-A-a guardian of poles. Nat Rev Cancer 2005; 5: 42-50.
31. Qu Y, Zhang L, Mao M, Zhao F, Huang X, Yang C, Xiong Y, Mu D,. Effects of DNAzymes targeting Aurora kinase A on the growth of human prostate cancer. Cancer Gene Ther 2008; 15: 517-25.
32. Comperat E, Bieche I, Dargere D, Laurendeau I, Vieillefond A, Benoit G, Vidaud M, Camparo P, Capron F, Verret C, Cussenot O, Bedossa P, et al. Gene expression study of Aurora-A reveals implication during bladder carcinogenesis and increasing values in invasive urothelial cancer. Urology 2008; 72: 873-7.
33. Li D, Zhu J, Firozi PF, Abbruzzese JL, Evans DB, Cleary K, Friess H, Sen S,. Overexpression of oncogenic STK15/BTAK/Aurora A kinase in human pancreatic cancer. Clin Cancer Res 2003; 9: 991-7. (Pubitemid 36323702)
34. Lee EC, Frolov A, Li R, Ayala G, Greenberg NM,. Targeting Aurora kinases for the treatment of prostate cancer. Cancer Res 2006; 66: 4996-5002. (Pubitemid 43844918)
35. Matarasso N, Bar-Shira A, Rozovski U, Rosner S, Orr-Urtreger A,. Functional analysis of the Aurora Kinase A Ile31 allelic variant in human prostate. Neoplasia 2007; 9: 707-15. (Pubitemid 47523232)
36. Qu Y, Zhang L, Mu DZ, Huang X, Wei DP, Zhao FY, Liu BL,. Effect of aurora A on carcinogenesis of human prostate cancer. Sichuan Da Xue Xue Bao Yi Xue Ban 2008; 39: 1-5.
37. Buschhorn HM, Klein RR, Chambers SM, Hardy MC, Green S, Bearss D, Nagle RB,. Aurora-A over-expression in high-grade PIN lesions and prostate cancer. Prostate 2005; 64: 341-6. (Pubitemid 41193246)
38. Kumano M, Miyake H, Terakawa T, Furukawa J, Fujisawa M,. Suppressed tumour growth and enhanced chemosensitivity by RNA interference targeting Aurora-A in the PC3 human prostate cancer model. BJU Int 2010; 106: 121-7.
39. Dar AA, Goff LW, Majid S, Berlin J, El-Rifai W,. Aurora kinase inhibitors-rising stars in cancer therapeutics? Mol Cancer Ther 2010; 9: 268-78.
40. Gorgun G, Calabrese E, Hideshima T, Ecsedy J, Perrone G, Mani M, Ikeda H, Bianchi G, Hu Y, Cirstea D, Santo L, Tai YT, et al. A novel aurora-A kinase inhibitor MLN8237 induces cytotoxicity and cell cycle arrest in multiple myeloma. Blood 2010; 115: 5202-13.
41. Blangy A, Lane HA, d'Herin P, Harper M, Kress M, Nigg EA,. Phosphorylation by p34cdc2 regulates spindle association of human Eg5, a kinesin-related motor essential for bipolar spindle formation in vivo. Cell 1995; 83: 1159-69.
42. Peter M, Nakagawa J, Doree M, Labbe JC, Nigg EA,. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 1990; 61: 591-602.
43. Kimura K, Hirano M, Kobayashi R, Hirano T,. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 1998; 282: 487-90. (Pubitemid 28483678)
44. Perez de Castro I, de Carcer G, Montoya G, Malumbres M,. Emerging cancer therapeutic opportunities by inhibiting mitotic kinases. Curr Opin Pharmacol 2008; 8: 375-83.
45. Hirota T, Kunitoku N, Sasayama T, Marumoto T, Zhang D, Nitta M, Hatakeyama K, Saya H,. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 2003; 114: 585-98. (Pubitemid 37159255)
46. Hata T, Furukawa T, Sunamura M, Egawa S, Motoi F, Ohmura N, Marumoto T, Saya H, Horii A,. RNA interference targeting aurora kinase a suppresses tumor growth and enhances the taxane chemosensitivity in human pancreatic cancer cells. Cancer Res 2005; 65: 2899-905. (Pubitemid 40490094)
47. Sasayama T, Marumoto T, Kunitoku N, Zhang D, Tamaki N, Kohmura E, Saya H, Hirota T,. Over-expression of Aurora-A targets cytoplasmic polyadenylation element binding protein and promotes mRNA polyadenylation of Cdk1 and cyclin B1. Genes Cells 2005; 10: 627-38. (Pubitemid 40932344)
48. Israels LG, Israels ED,. Apoptosis. The Oncologist 1999; 4: 332-9. (Pubitemid 29409310)
49. Cao Y,. Angiogenesis: what can it offer for future medicine? Exp Cell Res 2010; 316: 1304-8.