Tumor necrosis factor-α sensitizes breast cancer cells to natural products with proteasome-inhibitory activity leading to apoptosis

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Lu, Li ^a,b   Shi, Wenli ^a   Deshmukh, Rahul R ^b   Long, Jie ^a   Cheng, Xiaoli ^a   Ji, Weidong ^a   Zeng, Guohua ^a   Chen, Xianliang ^a   Zhang, Yajie ^a   Dou, Q Ping ^b  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 9; CELASTROL; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEASOME; TUMOR NECROSIS FACTOR ALPHA; WITHAFERIN A; X LINKED INHIBITOR OF APOPTOSIS; BIOLOGICAL PRODUCT; INHIBITOR OF APOPTOSIS PROTEIN; TRANSCRIPTION FACTOR RELA; TRIPTERINE; TRITERPENE; TUMOR NECROSIS FACTOR; WITHANOLIDE; XIAP PROTEIN, HUMAN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CONTROLLED STUDY; DRUG POTENTIATION; DRUG SENSITIZATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UPREGULATION; BREAST TUMOR; CELL PROLIFERATION; DOSE RESPONSE; DRUG EFFECTS; ENZYME ACTIVATION; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

APOPTOSIS; BIOLOGICAL PRODUCTS; BLOTTING, WESTERN; BREAST NEOPLASMS; CASPASE 3; CASPASE 9; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MICROSCOPY, FLUORESCENCE; PROTEASOME ENDOPEPTIDASE COMPLEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTOR RELA; TRITERPENES; TUMOR NECROSIS FACTOR-ALPHA; WITHANOLIDES; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84912573923     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113783     Document Type: Article

References (44)

1. Aggarwal BB, Sethi G, Baladandayuthapani V, Krishnan S, Shishodia S (2007) Targeting cell signaling pathways for drug discovery: an old lock needs a new key. J Cell Biochem 102: 580-592.
2. Shohat B, Gitter S, Abraham A, Lavie D (1967) Antitumor activity of withaferin A (NSC-101088). Cancer Chemother Rep 51: 271-276.
3. Mohan R, Hammers HJ, Bargagna-Mohan P, Zhan XH, Herbstritt CJ, et al. (2004) Withaferin A is a potent inhibitor of angiogenesis. Angiogenesis 7: 115-122.
4. Stan SD, Hahm ER, Warin R, Singh SV (2008) Withaferin A causes FOXO3a- and Bim-dependent apoptosis and inhibits growth of human breast cancer cells in vivo. Cancer Res 68: 7661-7669.
5. Malik F, Kumar A, Bhushan S, Khan S, Bhatia A, et al. (2007) Reactive oxygen species generation and mitochondrial dysfunction in the apoptotic cell death of human myeloid leukemia HL-60 cells by a dietary compound withaferin A with concomitant protection by N-acetyl cysteine. Apoptosis 12: 2115-2133.
6. Yang H, Shi G, Dou QP (2007) The tumor proteasome is a primary target for the natural anticancer compound Withaferin A isolated from "Indian winter cherry". Mol Pharmacol 71: 426-437.
7. Srinivasan S, Ranga RS, Burikhanov R, Han SS, Chendil D (2007) Par-4-dependent apoptosis by the dietary compound withaferin A in prostate cancer cells. Cancer Res 67: 246-253.
8. Devi PU, Kamath R, Rao BS (2000) Radiosensitization of a mouse melanoma by withaferin A: in vivo studies. Indian J Exp Biol 38: 432-437.
9. Bargagna-Mohan P, Hamza A, Kim YE, Khuan AHY, Mor-Vaknin N, et al. (2007) The tumor inhibitor and antiangiogenic agent withaferin A targets the intermediate filament protein vimentin. Chem Biol 14: 623-634.
10. Li H, Zhang YY, Huang XY, Sun YN, Jia YF, et al. (2005) Beneficial effect of tripterine on systemic lupus erythematosus induced by active chromatin in BALB/c mice. Eur J Pharmacol 512: 231-237.
11. Tao X, Cush JJ, Garret M, Lipsky PE (2001) A phase I study of ethyl acetate extract of the chinese antirheumatic herb Tripterygium wilfordii hook F in rheumatoid arthritis. J Rheumatol 28: 2160-2167.
12. Allison AC, Cacabelos R, Lombardi VR, Alvarez XA, Vigo C (2001) Celastrol, a potent antioxidant and anti-inflammatory drug, as a possible treatment for Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 25: 1341-1357.
13. Kiaei M, Kipiani K, Petri S, Chen J, Calingasan NY, et al. (2005) Celastrol blocks neuronal cell death and extends life in transgenic mouse model of amyotrophic lateral sclerosis. Neurodegener Dis 2: 246-254.
14. 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.
15. Sethi G, Ahn KS, Pandey MK, Aggarwal BB (2007) Celastrol, a novel triterpene, potentiates TNF-induced apoptosis and suppresses invasion of tumor cells by inhibiting NF-kappaB-regulated gene products and TAK1-mediated NF-kappaB activation. Blood 109: 2727-2735.
16. 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.
17. Nagase M, Oto J, Sugiyama S, Yube K, Takaishi Y, et al. (2003) Apoptosis induction in HL-60 cells and inhibition of topoisomerase II by triterpene celastrol. Biosci Biotechnol Biochem 67: 1883-1887.
18. Trott A, West JD, Klaic L, Westerheide SD, Silverman RB, et al. (2008) Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Mol Biol Cell 19: 1104-1112.
19. 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.
20. Wang X, Lin Y (2008) Tumor necrosis factor and cancer, buddies or foes? Acta Pharmacol Sin 29: 1275-1288.
21. Balkwill F (2009) Tumour necrosis factor and cancer. Nat Rev Cancer 9: 361-371.
22. Wang P, Qiu W, Dudgeon C, Liu H, Huang C, et al. (2009) PUMA is directly activated by NF-kappaB and contributes to TNF-alpha-induced apoptosis. Cell Death Differ 16: 1192-1202.
23. Mantovani A (2010) Molecular pathways linking inflammation and cancer. Curr Mol Med 10: 369-373.
24. Geisler F, Algul H, Paxian S, Schmid RM (2007) Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology 132: 2489-2503.
25. Ben-Neriah Y, Karin M (2011) Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat Immunol 12: 715-723.
26. LaCasse EC, Baird S, Korneluk RG, MacKenzie AE (1998) The inhibitors of apoptosis (IAPs) and their emerging role in cancer. Oncogene 17: 3247-3259.
27. Deveraux QL, Reed JC (1999) IAP family proteins-suppressors of apoptosis. Genes Dev 13: 239-252.
28. Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, et al. (2001) Structural basis for the inhibition of caspase-3 by XIAP. Cell 104: 791-800.
29. Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, et al. (2003) Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell 11: 519-527.
30. Gyrd-Hansen M, Meier P (2010) IAPs: from caspase inhibitors to modulators of NF-kappaB, inflammation and cancer. Nat Rev Cancer 10: 561-574.
31. Lu L, Kanwar J, Schmitt S, Cui QC, Zhang C, et al. (2011) Inhibition of tumor cellular proteasome activity by triptolide extracted from the Chinese medicinal plant 'thunder god vine'. Anticancer Res 31: 1-10.
32. Hussain AR, Ahmed M, Al-Jomah NA, Khan AS, Manogaran P, et al. (2008) Curcumin suppresses constitutive activation of nuclear factor-kappa B and requires functional Bax to induce apoptosis in Burkitt's lymphoma cell lines. Mol Cancer Ther 7: 3318-3329.
33. Lu L, Qin A, Huang H, Zhou P, Zhang C, et al. (2011) Shikonin extracted from medicinal Chinese herbs exerts anti-inflammatory effect via proteasome inhibition. European Journal of Pharmacology 658: 242-247.
34. Michalaki V, Syrigos K, Charles P, Waxman J (2004) Serum levels of IL-6 and TNF-alpha correlate with clinicopathological features and patient survival in patients with prostate cancer. Br J Cancer 90: 2312-2316.
35. Balkwill F (2006) TNF-alpha in promotion and progression of cancer. Cancer Metastasis Rev 25: 409-416.
36. Miles DW, Happerfield LC, Naylor MS, Bobrow LG, Rubens RD, et al. (1994) Expression of tumour necrosis factor (TNF alpha) and its receptors in benign and malignant breast tissue. Int J Cancer 56: 777-782.
37. Mandal C, Dutta A, Mallick A, Chandra S, Misra L, et al. (2008) Withaferin A induces apoptosis by activating p38 mitogen-activated protein kinase signaling cascade in leukemic cells of lymphoid and myeloid origin through mitochondrial death cascade. Apoptosis 13: 1450-1464.
38. Sung B, Park B, Yadav VR, Aggarwal BB (2010) Celastrol, a triterpene, enhances TRAIL-induced apoptosis through the down-regulation of cell survival proteins and up-regulation of death receptors. J Biol Chem 285: 11498-11507.
39. Wang CY, Mayo MW, Baldwin AJ (1996) TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274: 784-787.
40. Beg AA, Baltimore D (1996) An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274: 782-784.
41. Gupta SC, Sundaram C, Reuter S, Aggarwal BB (2010) Inhibiting NF-kappaB activation by small molecules as a therapeutic strategy. Biochim Biophys Acta 1799: 775-787.
42. Stehlik C, de Martin R, Kumabashiri I, Schmid JA, Binder BR, et al. (1998) Nuclear factor (NF)- kappaB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis. J Exp Med 188: 211-216.
43. Gupta SV, Hertlein E, Lu Y, Sass EJ, Lapalombella R, et al. (2013) The proteasome inhibitor carfilzomib functions independently of p53 to induce cytotoxicity and an atypical NF-kappaB response in chronic lymphocytic leukemia cells. Clin Cancer Res 19: 2406-2419.
44. Kanarek N, Ben-Neriah Y (2012) Regulation of NF-kappaB by ubiquitination and degradation of the IkappaBs. Immunol Rev 246: 77-94.