Celastrol Suppresses Tumor Cell Growth through Targeting an AR-ERG-NF-κB Pathway in TMPRSS2/ERG Fusion Gene Expressing Prostate Cancer

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Shao, Longjiang ^a   Zhou, Zhansong ^b   Cai, Yi ^a   Castro, Patricia ^a   Dakhov, Olga ^a   Shi, Ping ^b   Bai, Yaoxia ^b   Ji, Huixiang ^b   Shen, Wenhao ^b   Wang, Jianghua ^a  

^a SOUTHWEST HOSPITAL   (China)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELASTROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR ERG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER INHIBITION; CONCENTRATION RESPONSE; DRUG EFFICACY; FUSION GENE; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; T/E GENE; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, NUDE; ONCOGENE PROTEINS, FUSION; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR RELA; TRITERPENES;

EID: 84874610297     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058391     Document Type: Article

References (50)

1. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, et al. (2005) Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310: 644-648.
2. Soller MJ, Isaksson M, Elfving P, Soller W, Lundgren R, et al. (2006) Confirmation of the high frequency of the TMPRSS2/ERG fusion gene in prostate cancer. Genes Chromosomes Cancer 45: 717-719.
3. Wang J, Cai Y, Ren C, Ittmann M, (2006) Expression of Variant TMPRSS2/ERG Fusion Messenger RNAs Is Associated with Aggressive Prostate Cancer. Cancer Res 66: 8347-8351.
4. Tomlins SA, Laxman B, Varambally S, Cao X, Yu J, et al. (2008) Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia 10: 177-188.
5. Sun C, Dobi A, Mohamed A, Li H, Thangapazham RL, et al. (2008) TMPRSS2-ERG fusion, a common genomic alteration in prostate cancer activates C-MYC and abrogates prostate epithelial differentiation. Oncogene 27: 5348-5353.
6. Wang J, Cai Y, Yu W, Ren C, Spencer DM, et al. (2008) Pleiotropic biological activities of alternatively spliced TMPRSS2/ERG fusion gene transcripts. Cancer Res 68: 8516-8524.
7. Wang J, Cai Y, Shao LJ, Siddiqui J, Palanisamy N, et al. (2010) Activation of NF-kB by TMPRSS2/ERG fusion isoforms through Toll-like receptor-4. Cancer Res.
8. Hishikawa K, Nakaki T, (2001) [NF-kappa B as a therapeutic drug target]. Nippon Yakurigaku Zasshi 118: 197-202.
9. Rajasekhar VK, Studer L, Gerald W, Socci ND, Scher HI, (2011) Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-kappaB signalling. Nat Commun 2: 162.
10. Zhang L, Altuwaijri S, Deng F, Chen L, Lal P, et al. (2009) NF-kappaB regulates androgen receptor expression and prostate cancer growth. Am J Pathol 175: 489-499.
11. Seo SI, Song SY, Kang MR, Kim MS, Oh JE, et al. (2009) Immunohistochemical analysis of NF-kappaB signaling proteins IKKepsilon, p50/p105, p52/p100 and RelA in prostate cancers. APMIS 117: 623-628.
12. Jin RJ, Lho Y, Connelly L, Wang Y, Yu X, et al. (2008) The nuclear factor-kappaB pathway controls the progression of prostate cancer to androgen-independent growth. Cancer Res 68: 6762-6769.
13. Tamaki K, Otaka M, Shibuya T, Sakamoto N, Yamamoto S, et al. (2012) Traditional Herbal Medicine, Rikkunshito, Induces HSP60 and Enhances Cytoprotection of Small Intestinal Mucosal Cells as a Nontoxic Chaperone Inducer. Evid Based Complement Alternat Med 2012: 278958.
14. Guo H, Liu JX, Xu L, Madebo T, Baak JP, (2011) Traditional Chinese medicine herbal treatment may have a relevant impact on the prognosis of patients with stage IV adenocarcinoma of the lung treated with platinum-based chemotherapy or combined targeted therapy and chemotherapy. Integr Cancer Ther 10: 127-137.
15. Kannaiyan R, Shanmugam MK, Sethi G, (2011) Molecular targets of celastrol derived from Thunder of God Vine: potential role in the treatment of inflammatory disorders and cancer. Cancer Lett 303: 9-20.
16. Salminen A, Lehtonen M, Paimela T, Kaarniranta K, (2010) Celastrol: Molecular targets of Thunder God Vine. Biochem Biophys Res Commun 394: 439-442.
17. Morita T, (2010) Celastrol: a new therapeutic potential of traditional Chinese medicine. Am J Hypertens 23: 821.
18. Lee JH, Koo TH, Yoon H, Jung HS, Jin HZ, et al. (2006) Inhibition of NF-kappa B activation through targeting I kappa B kinase by celastrol, a quinone methide triterpenoid. Biochem Pharmacol 72: 1311-1321.
19. Zhu H, Liu XW, Cai TY, Cao J, Tu CX, et al. (2010) Celastrol acts as a potent antimetastatic agent targeting beta1 integrin and inhibiting cell-extracellular matrix adhesion, in part via the p38 mitogen-activated protein kinase pathway. J Pharmacol Exp Ther 334: 489-499.
20. Zhang T, Hamza A, Cao X, Wang B, Yu S, et al. (2008) A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Mol Cancer Ther 7: 162-170.
21. Huang Y, Zhou Y, Fan Y, Zhou D, (2008) Celastrol inhibits the growth of human glioma xenografts in nude mice through suppressing VEGFR expression. Cancer Lett 264: 101-106.
22. Yang H, Chen D, Cui QC, Yuan X, Dou QP, (2006) Celastrol, a triterpene extracted from the Chinese "Thunder of God Vine," is a potent proteasome inhibitor and suppresses human prostate cancer growth in nude mice. Cancer Res 66: 4758-4765.
23. Dai Y, DeSano JT, Meng Y, Ji Q, Ljungman M, et al. (2009) Celastrol potentiates radiotherapy by impairment of DNA damage processing in human prostate cancer. Int J Radiat Oncol Biol Phys 74: 1217-1225.
24. Zhu H, Liu XW, Ding WJ, Xu DQ, Zhao YC, et al. (2010) Up-regulation of death receptor 4 and 5 by celastrol enhances the anti-cancer activity of TRAIL/Apo-2L. Cancer Lett 297: 155-164.
25. Kim Y, Kang H, Jang SW, Ko J, (2011) Celastrol Inhibits Breast Cancer Cell Invasion via Suppression of NF-kB-mediated Matrix Metalloproteinase-9 Expression. Cell Physiol Biochem 28: 175-184.
26. Kannaiyan R, Manu KA, Chen L, Li F, Rajendran P, et al. (2011) Celastrol inhibits tumor cell proliferation and promotes apoptosis through the activation of c-Jun N-terminal kinase and suppression of PI3 K/Akt signaling pathways. Apoptosis.
27. Paimela T, Hyttinen JM, Viiri J, Ryhanen T, Karjalainen RO, et al. (2011) Celastrol regulates innate immunity response via NF-kappaB and Hsp70 in human retinal pigment epithelial cells. Pharmacol Res.
28. Cai Y, Wang J, Li R, Ayala G, Ittmann M, et al. (2009) GGAP2/PIKE-a directly activates both the Akt and nuclear factor-kappaB pathways and promotes prostate cancer progression. Cancer Res 69: 819-827.
29. Wang J, Stockton DW, Ittmann M, (2004) The fibroblast growth factor receptor-4 Arg388 allele is associated with prostate cancer initiation and progression. Clin Cancer Res 10: 6169-6178.
30. Shirley RB, Kaddour-Djebbar I, Patel DM, Lakshmikanthan V, Lewis RW, et al. (2005) Combination of proteasomal inhibitors lactacystin and MG132 induced synergistic apoptosis in prostate cancer cells. Neoplasia 7: 1104-1111.
31. Loberg RD, Day LL, Harwood J, Ying C, St John LN, et al. (2006) CCL2 is a potent regulator of prostate cancer cell migration and proliferation. Neoplasia 8: 578-586.
32. Lu Y, Cai Z, Galson DL, Xiao G, Liu Y, et al. (2006) Monocyte chemotactic protein-1 (MCP-1) acts as a paracrine and autocrine factor for prostate cancer growth and invasion. Prostate 66: 1311-1318.
33. Roca H, Varsos Z, Pienta KJ, (2008) CCL2 protects prostate cancer PC3 cells from autophagic death via phosphatidylinositol 3-kinase/AKT-dependent survivin up-regulation. J Biol Chem 283: 25057-25073.
34. Roebuck KA, Carpenter LR, Lakshminarayanan V, Page SM, Moy JN, et al. (1999) Stimulus-specific regulation of chemokine expression involves differential activation of the redox-responsive transcription factors AP-1 and NF-kappaB. J Leukoc Biol 65: 291-298.
35. Dai Y, Desano J, Tang W, Meng X, Meng Y, et al. (2010) Natural proteasome inhibitor celastrol suppresses androgen-independent prostate cancer progression by modulating apoptotic proteins and NF-kappaB. PLoS One 5: e14153.
36. Kannaiyan R, Manu KA, Chen L, Li F, Rajendran P, et al. (2011) Celastrol inhibits tumor cell proliferation and promotes apoptosis through the activation of c-Jun N-terminal kinase and suppression of PI3 K/Akt signaling pathways. Apoptosis 16: 1028-1041.
37. Tomlins SA, Rhodes DR, Yu J, Varambally S, Mehra R, et al. (2008) The role of SPINK1 in ETS rearrangement-negative prostate cancers. Cancer Cell 13: 519-528.
38. Goldstein AS, Zong Y, Witte ON, (2011) A two-step toward personalized therapies for prostate cancer. Sci Transl Med 3: 72ps77.
39. Pang X, Yi Z, Zhang J, Lu B, Sung B, et al. (2010) Celastrol suppresses angiogenesis-mediated tumor growth through inhibition of AKT/mammalian target of rapamycin pathway. Cancer Res 70: 1951-1959.
40. Vermeulen L, De Wilde G, Notebaert S, Vanden Berghe W, Haegeman G, (2002) Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit. Biochem Pharmacol 64: 963-970.
41. Viatour P, Merville MP, Bours V, Chariot A, (2005) Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30: 43-52.
42. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W, (1999) IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 274: 30353-30356.
43. Jiang X, Takahashi N, Matsui N, Tetsuka T, Okamoto T, (2003) The NF-kappa B activation in lymphotoxin beta receptor signaling depends on the phosphorylation of p65 at serine 536. J Biol Chem 278: 919-926.
44. Buss H, Dorrie A, Schmitz ML, Hoffmann E, Resch K, et al. (2004) Constitutive and interleukin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein kinases including I{kappa}B kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J Biol Chem 279: 55633-55643.
45. Sasaki CY, Barberi TJ, Ghosh P, Longo DL, (2005) Phosphorylation of RelA/p65 on serine 536 defines an I{kappa}B{alpha}-independent NF-{kappa}B pathway. J Biol Chem 280: 34538-34547.
46. Jeong SJ, Pise-Masison CA, Radonovich MF, Park HU, Brady JN, (2005) A novel NF-kappaB pathway involving IKKbeta and p65/RelA Ser-536 phosphorylation results in p53 Inhibition in the absence of NF-kappaB transcriptional activity. J Biol Chem 280: 10326-10332.
47. Perkins ND, (2007) Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat Rev Mol Cell Biol 8: 49-62.
48. Guo Z, Yang X, Sun F, Jiang R, Linn DE, et al. (2009) A novel androgen receptor splice variant is up-regulated during prostate cancer progression and promotes androgen depletion-resistant growth. Cancer Res 69: 2305-2313.
49. Wang W, Liu K, Dong H, Liu W, (2008) High-performance liquid chromatography spectrometric analysis of tripterin in rat plasma. J Chromatogr B Analyt Technol Biomed Life Sci 863: 163-166.
50. Huang Y, Zhou D, Hang T, Wu Z, Liu J, et al. (2012) Preparation, characterization, and assessment of the antiglioma effects of liposomal celastrol. Anticancer Drugs 23: 515-524.