An α-acetoxy-tirucallic acid isomer inhibits Akt/mTOR signaling and induces oxidative stress in prostate cancer cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 352, Issue 1, 2015, Pages 33-42

  El Gaafary, Menna ^a   Büchele, Berthold ^a   Syrovets, Tatiana ^a   Agnolet, Sara ^b   Schneider, Bernd ^b   Schmidt, Christoph Q ^a   Simmet, Thomas ^a  

^a UNIVERSITY OF ULM   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 OXO TIR 8,24 DIEN 21 OIC ACID; 3ALPHA ACETYLOXY TIR 8,24 DIEN 21 OIC ACID; ANTINEOPLASTIC AGENT; CASPASE 3; CYCLIN B1; CYCLIN D1; CYCLIN DEPENDENT KINASE 3; CYCLIN DEPENDENT KINASE 4; CYCLIN E; DOCETAXEL; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROTEIN KINASE B; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; RETINOBLASTOMA PROTEIN; S6 KINASE; S6 KINASE 1; TERPENOID; UNCLASSIFIED DRUG; 3-ACETYLOXYTIR-8,24-DIEN-21-OIC ACID; MTOR PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TRITERPENE;

ACIDIC VESICULAR ORGANELLE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BOSWELLIA SERRATA; CANCER INHIBITION; CELL CYCLE ARREST; CELL ORGANELLE; CHICK EMBRYO; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG STRUCTURE; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME MEMBRANE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; BOSWELLIA; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; CHORIOALLANTOIS; CONFORMATION; CYTOLOGY; DRUG EFFECTS; ISOLATION AND PURIFICATION; ISOMERISM; METABOLISM; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BOSWELLIA; CELL LINE, TUMOR; CELL PROLIFERATION; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; HUMANS; ISOMERISM; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; ORGANELLES; OXIDATIVE STRESS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRITERPENES;

EID: 84919722774     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.217323     Document Type: Article

References (43)

1. Abdel-Tawab M, Werz O, and Schubert-Zsilavecz M (2011) Boswellia serrata: an overall assessment of in vitro, preclinical, pharmacokinetic and clinical data. Clin Pharmacokinet 50:349-369.
2. Aggarwal BB, Takada Y, and Oommen OV (2004) From chemoprevention to chemotherapy: common targets and common goals. Expert Opin Investig Drugs 13:1327-1338.
3. Aits S and Jäättelä M (2013) Lysosomal cell death at a glance. J Cell Sci 126:1905-1912.
4. Akihisa T, Tabata K, Banno N, Tokuda H, Nishimura R, Nakamura Y, Kimura Y, Yasukawa K, and Suzuki T (2006) Cancer chemopreventive effects and cytotoxic activities of the triterpene acids from the resin of Boswellia carteri. Biol Pharm Bull 29:1976-1979.
5. Ammon HP (2006) Boswellic acids in chronic inflammatory diseases. Planta Med 72: 1100-1116.
6. Antonarakis ES, Carducci MA, and Eisenberger MA (2010) Novel targeted therapeutics for metastatic castration-resistant prostate cancer. Cancer Lett 291:1-13.
7. Banno N, Akihisa T, Yasukawa K, Tokuda H, Tabata K, Nakamura Y, Nishimura R, Kimura Y, and Suzuki T (2006) Anti-inflammatory activities of the triterpene acids from the resin of Boswellia carteri. J Ethnopharmacol 107:249-253.
8. Bhushan S, Malik F, Kumar A, Isher HK, Kaur IP, Taneja SC, and Singh J (2009) Activation of p53/p21/PUMA alliance and disruption of PI-3/Akt in multimodal targeting of apoptotic signaling cascades in cervical cancer cells by a pentacyclic triterpenediol from Boswellia serrata. Mol Carcinog 48:1093-1108.
9. Boden SE, Schweizer S, Bertsche T, Düfer M, Drews G, and Safayhi H (2001) Stimulation of leukotriene synthesis in intact polymorphonuclear cells by the 5-lipoxygenase inhibitor 3-oxo-tirucallic acid. Mol Pharmacol 60:267-273.
10. Brown RE, Zotalis G, Zhang PL, and Zhao B (2008) Morphoproteomic confirmation of a constitutively activated mTOR pathway in high grade prostatic intraepithelial neoplasia and prostate cancer. Int J Clin Exp Pathol 1:333-342.
11. Büchele B, Zugmaier W, Estrada A, Genze F, Syrovets T, Paetz C, Schneider B, and Simmet T (2006) Characterization of 3a-acetyl-11-keto-α-boswellic acid, a pentacyclic triterpenoid inducing apoptosis in vitro and in vivo. Planta Med 72:1285-1289.
12. Clute P and Pines J (1999) Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1:82-87.
13. Colognato R, Slupsky JR, Jendrach M, Burysek L, Syrovets T, and Simmet T (2003) Differential expression and regulation of protease-activated receptors in human peripheral monocytes and monocyte-derived antigen-presenting cells. Blood 102:2645-2652.
14. -/- mice. Arterioscler Thromb Vasc Biol 28:272-277.
15. Efeyan A and Sabatini DM (2010) mTOR and cancer: many loops in one pathway. Curr Opin Cell Biol 22:169-176.
16. Estrada AC, Syrovets T, Pitterle K, Lunov O, Büchele B, Schimana-Pfeifer J, Schmidt T, Morad SA, and Simmet T (2010) Tirucallic acids are novel pleckstrin homology domain-dependent Akt inhibitors inducing apoptosis in prostate cancer cells. Mol Pharmacol 77:378-387.
17. Fink SL and Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73:1907-1916.
18. Fischer U and Schulze-Osthoff K (2005) New approaches and therapeutics targeting apoptosis in disease. Pharmacol Rev 57:187-215.
19. Freedland SJ (2011) Screening, risk assessment, and the approach to therapy in patients with prostate cancer. Cancer 117:1123-1135.
20. Graff JR, Konicek BW, Lynch RL, Dumstorf CA, Dowless MS, McNulty AM, Parsons SH, Brail LH, Colligan BM, Koop JW, et al. (2009) eIF4E activation is commonly elevated in advanced human prostate cancers and significantly related to reduced patient survival. Cancer Res 69:3866-3873.
21. Green DR and Reed JC (1998) Mitochondria and apoptosis. Science 281:1309-1312.
22. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445-544.
23. Lawen A (2003) Apoptosis-an introduction. BioEssays 25:888-896.
24. Loos C, Syrovets T, Musyanovych A, Mailänder V, Landfester K, and Simmet T (2014) Amino-functionalized nanoparticles as inhibitors of mTOR and inducers of cell cycle arrest in leukemia cells. Biomaterials 35:1944-1953.
25. Lu M, Xia L, Hua H, and Jing Y (2008) Acetyl-keto-β-boswellic acid induces apoptosis through a death receptor 5-mediated pathway in prostate cancer cells. Cancer Res 68:1180-1186.
26. Morad SA, Schmid M, Büchele B, Siehl HU, El Gafaary M, Lunov O, Syrovets T, and Simmet T (2013) A novel semisynthetic inhibitor of the FRB domain of mammalian target of rapamycin blocks proliferation and triggers apoptosis in chemoresistant prostate cancer cells. Mol Pharmacol 83:531-541.
27. Moriyama Y, Takano T, and Ohkuma S (1982) Acridine orange as a fluorescent probe for lysosomal proton pump. J Biochem 92:1333-1336.
28. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, and Riccardi C (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 139:271-279.
29. Park B, Prasad S, Yadav V, Sung B, and Aggarwal BB (2011) Boswellic acid suppresses growth and metastasis of human pancreatic tumors in an orthotopic nude mouse model through modulation of multiple targets. PLoS ONE 6:e26943.
30. Poeckel D and Werz O (2006) Boswellic acids: biological actions and molecular targets. Curr Med Chem 13:3359-3369.
31. Porta C, Paglino C, and Mosca A (2014) Targeting PI3K/Akt/mTOR signaling in cancer. Front Oncol 4:64.
32. Repnik U, Cesen MH, and Turk B (2013) The endolysosomal system in cell death and survival. Cold Spring Harb Perspect Biol 5:a008755.
33. Siegel R, Naishadham D, and Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63:11-30.
34. Syrovets T, Tippler B, Rieks M, and Simmet T (1997) Plasmin is a potent and specific chemoattractant for human peripheral monocytes acting via a cyclic guanosine monophosphate-dependent pathway. Blood 89:4574-4583.
35. Syrovets T, Büchele B, Gedig E, Slupsky JR, and Simmet T (2000) Acetyl-boswellic acids are novel catalytic inhibitors of human topoisomerases I and IIalpha. Mol Pharmacol 58:71-81.
36. Syrovets T, Jendrach M, Rohwedder A, Schüle A, and Simmet T (2001) Plasmininduced expression of cytokines and tissue factor in human monocytes involves AP-1 and IKKbeta-mediated NF-kappaB activation. Blood 97:3941-3950.
37. Syrovets T, Büchele B, Krauss C, Laumonnier Y, and Simmet T (2005a) Acetylboswellic acids inhibit lipopolysaccharide-mediated TNF-α induction in monocytes by direct interaction with IkappaB kinases. J Immunol 174:498-506.
38. Syrovets T, Gschwend JE, Büchele B, Laumonnier Y, Zugmaier W, Genze F, and Simmet T (2005b) Inhibition of IkappaB kinase activity by acetyl-boswellic acids promotes apoptosis in androgen-independent PC-3 prostate cancer cells in vitro and in vivo. J Biol Chem 280:6170-6180.
39. Trachootham D, Alexandre J, and Huang P (2009) Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8: 579-591.
40. Wang H, Syrovets T, Kess D, Büchele B, Hainzl H, Lunov O, Weiss JM, Scharffetter-Kochanek K, and Simmet T (2009) Targeting NF-κB with a natural triterpenoid alleviates skin inflammation in a mouse model of psoriasis. J Immunol 183: 4755-4763.
41. Yadav VR, Prasad S, Sung B, Gelovani JG, Guha S, Krishnan S, and Aggarwal BB (2012) Boswellic acid inhibits growth and metastasis of human colorectal cancer in orthotopic mouse model by downregulating inflammatory, proliferative, invasive and angiogenic biomarkers. Int J Cancer 130:2176-2184.
42. Yvon AM, Wadsworth P, and Jordan MA (1999) Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol Biol Cell 10:947-959.
43. Zoncu R, Efeyan A, and Sabatini DM (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12:21-35.