Preclinical evidences toward the use of triterpenoid CDDO-Me for solid cancer prevention and treatment

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Wang, Yan Yang ^a   Zhe, Hong ^a   Zhao, Ren ^a  

^a NINGXIA MEDICAL UNIVERSITY   (China)

Author keywords

CDDO Me; Mechanisms; Prevention; Solid cancer; Treatment; Triterpenoid

Indexed keywords

6 [1 (5,6,7,8 TETRAHYDRO 3,5,5,8,8 PENTAMETHYL 2 NAPHTHYL)CYCLOPROPYL]NICOTINIC ACID; BARDOXOLONE METHYL; DEATH RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; JANUS KINASE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; PROTEIN KINASE B1; STAT PROTEIN; UNCLASSIFIED DRUG;

ABSENCE OF SIDE EFFECTS; ANTINEOPLASTIC ACTIVITY; CANCER CHEMOTHERAPY; CANCER PREVENTION; DRUG DOSE INCREASE; DRUG MECHANISM; DRUG TARGETING; HUMAN; IMMUNOCOMPETENT CELL; IN VIVO STUDY; MAXIMUM TOLERATED DOSE; NONHUMAN; PANCREAS CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION; SOLID TUMOR;

ANIMALIA;

ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; NEOPLASMS; OLEANOLIC ACID;

EID: 84896731739     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-30     Document Type: Review

References (61)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000, 100:57-70. 10.1016/S0092-8674(00)81683-9, 10647931.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674. 10.1016/j.cell.2011.02.013, 21376230.
3. Patlolla JM, Rao CV. Triterpenoids for cancer prevention and treatment: current status and future prospects. Curr Pharm Biotechnol 2012, 13:147-155. 10.2174/138920112798868719, 21466427.
4. Petronelli A, Pannitteri G, Testa U. Triterpenoids as new promising anticancer drugs. Anticancer Drugs 2009, 20:880-892. 10.1097/CAD.0b013e328330fd90, 19745720.
5. Liby KT, Sporn MB. Synthetic oleanane triterpenoids: multifunctional drugs with a broad range of applications for prevention and treatment of chronic disease. Pharmacol Rev 2012, 64:972-1003. 10.1124/pr.111.004846, 3462991, 22966038.
6. Yadav VR, Prasad S, Sung B, Kannappan R, Aggarwal BB. Targeting inflammatory pathways by triterpenoids for prevention and treatment of cancer. Toxins (Basel) 2010, 2:2428-2466. 10.3390/toxins2102428, 3153165, 22069560.
7. Liby KT, Yore MM, Sporn MB. Triterpenoids and rexinoids as multifunctional agents for the prevention and treatment of cancer. Nat Rev Cancer 2007, 7:357-369. 10.1038/nrc2129, 17446857.
8. Ovesná Z, Vachálková A, Horváthová K, Tóthová D. Pentacyclic triterpenoic acids: new chemoprotective compounds. Minireview. Neoplasma 2004, 51:327-333.
9. Bishayee A, Ahmed S, Brankov N, Perloff M. Triterpenoids as potential agents for the chemoprevention and therapy of breast cancer. Front Biosci 2011, 16:980-996.
10. Setzer WN, Setzer MC. Plant-derived triterpenoids as potential antineoplastic agents. Mini Rev Med Chem 2003, 3:540-556. 10.2174/1389557033487854, 12871157.
11. Laszczyk MN. Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy. Planta Med 2009, 75:1549-1560. 10.1055/s-0029-1186102, 19742422.
12. Murakami A, Ohigashi H. Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals. Int J Cancer 2007, 121:2357-2363. 10.1002/ijc.23161, 17893865.
13. Kundu JK, Surh YJ. Inflammation: gearing the journey to cancer. Mutat Res 2008, 659:15-30. 10.1016/j.mrrev.2008.03.002, 18485806.
14. Suh N, Wang Y, Honda T, Gribble GW, Dmitrovsky E, Hickey WF, Maue RA, Place AE, Porter DM, Spinella MJ, Williams CR, Wu G, Dannenberg AJ, Flanders KC, Letterio JJ, Mangelsdorf DJ, Nathan CF, Nguyen L, Porter WW, Ren RF, Roberts AB, Roche NS, Subbaramaiah K, Sporn MB. A novel synthetic oleanane triterpenoid, 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid, with potent differentiating, antiproliferative, and anti-inflammatory activity. Cancer Res 1999, 59:336-341.
15. Deeb D, Gao X, Dulchavsky SA, Gautam SC. CDDO-Me inhibits proliferation, induces apoptosis, down-regulates Akt, mTOR, NF-kappaB and NF-kappaB-regulated antiapoptotic and proangiogenic proteins in TRAMP prostate cancer cells. J Exp Ther Oncol 2008, 7:31-39.
16. Liby K, Royce DB, Williams CR, Risingsong R, Yore MM, Honda T, Gribble GW, Dmitrovsky E, Sporn TA, Sporn MB. The synthetic triterpenoids CDDO-methyl ester and CDDO-ethyl amide prevent lung cancer induced by vinyl carbamate in A/J mice. Cancer Res 2007, 67:2414-2419. 10.1158/0008-5472.CAN-06-4534, 17363558.
17. Liby K, Risingsong R, Royce DB, Williams CR, Yore MM, Honda T, Gribble GW, Lamph WW, Vannini N, Sogno I, Albini A, Sporn MB. Prevention and treatment of experimental estrogen receptor-negative mammary carcinogenesis by the synthetic triterpenoid CDDO-methyl Ester and the rexinoid LG100268. Clin Cancer Res 2008, 14:4556-4563. 10.1158/1078-0432.CCR-08-0040, 18628471.
18. Liby KT, Royce DB, Risingsong R, Williams CR, Maitra A, Hruban RH, Sporn MB. Synthetic triterpenoids prolong survival in a transgenic mouse model of pancreatic cancer. Cancer PrevRes (Phila) 2010, 3:1427-1434.
19. Tran K, Risingsong R, Royce D, Williams CR, Sporn MB, Liby K. The synthetic triterpenoid CDDO-methyl ester delays estrogen receptor-negative mammary carcinogenesis in polyoma middle T mice. Cancer Prev Res (Phila) 2012, 5:726-734. 10.1158/1940-6207.CAPR-11-0404, 22401982.
20. Kim EH, Deng C, Sporn MB, Royce DB, Risingsong R, Williams CR, Liby KT. CDDO-methyl ester delays breast cancer development in BRCA1-mutated mice. Cancer Prev Res (Phila) 2012, 5:89-97. 10.1158/1940-6207.CAPR-11-0359, 3252488, 21933912.
21. Deeb D, Gao X, Liu Y, Jiang D, Divine GW, Arbab AS, Dulchavsky SA, Gautam SC. Synthetic triterpenoid CDDO prevents the progression and metastasis of prostate cancer in TRAMP mice by inhibiting survival signaling. Carcinogenesis 2011, 32:757-764. 10.1093/carcin/bgr030, 3086702, 21325633.
22. Gao X, Deeb D, Liu Y, Arbab AS, Divine GW, Dulchavsky SA, Gautam SC. Prevention of prostate cancer with oleanane synthetic triterpenoid CDDO-Me in the TRAMP mouse model of prostate cancer. Cancers (Basel) 2011, 3:3353-3369. 10.3390/cancers3033353, 3180910,3180910, 21961053.
23. Liu Y, Gao X, Deeb D, Arbab AS, Gautam SC. Telomerase reverse transcriptase (TERT) is a therapeutic target of oleanane triterpenoid CDDO-Me in prostate cancer. Molecules 2012, 17:14795-14809. 10.3390/molecules171214795, 3607816, 23519253.
24. Karin M. NF-kappaB as a critical link between inflammation and cancer. Cold Spring Harb Perspect Biol 2009, 1:a000141. 2773649, 20066113.
25. Ben-Neriah Y, Karin M. Inflammation meets cancer, with NF-κB as the match maker. Nat Immunol 2011, 12:715-723. 10.1038/ni.2060, 21772280.
26. Deeb D, Gao X, Dulchavsky SA, Gautam SC. CDDO-me induces apoptosis and inhibits Akt, mTOR and NF-kappaB signaling proteins in prostate cancer cells. Anticancer Res 2007, 27:3035-3044.
27. Engelman JA. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 2009, 9:550-562. 10.1038/nrc2664, 19629070.
28. Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer 2010, 10:342-352. 10.1038/nrc2842, 20414202.
29. McNamara CR, Degterev A. Small-molecule inhibitors of the PI3K signaling network. Future Med Chem 2011, 3:549-565. 10.4155/fmc.11.12, 3132554, 21526896.
30. Deeb D, Gao X, Jiang H, Dulchavsky SA, Gautam SC. Oleanane triterpenoid CDDO-Me inhibits growth and induces apoptosis in prostate cancer cells by independently targeting pro-survival Akt and mTOR. Prostate 2009, 69:851-860. 10.1002/pros.20937, 3865612, 19189297.
31. Deeb D, Gao X, Jiang H, Janic B, Arbab AS, Rojanasakul Y, Dulchavsky SA, Gautam SC. Oleanane triterpenoid CDDO-Me inhibits growth and induces apoptosis in prostate cancer cells through a ROS-dependent mechanism. Biochem Pharmacol 2010, 79:350-360. 10.1016/j.bcp.2009.09.006, 2822351, 19782051.
32. Deeb D, Gao X, Arbab AS, Barton K, Dulchavsky SA, Gautam SC. CDDO-Me: a novel synthetic triterpenoid for the treatment of pancreatic cancer. Cancers (Basel) 2010, 2:1779-1793. 10.3390/cancers2041779, 3143824,3143824, 21799944.
33. Deeb D, Gao X, Liu YB, Gautam SC. Inhibition of cell proliferation and induction of apoptosis by CDDO-Me in pancreatic cancer cells is ROS-dependent. J Exp Ther Oncol 2012, 10:51-64. 3846287, 22946344.
34. Gao X, Deeb D, Hao J, Liu Y, Arbab AS, Dulchavsky SA, Gautam SC. Synthetic triterpenoids inhibit growth, induce apoptosis and suppress pro-survival Akt, mTOR and NF-{kappa}B signaling proteins in colorectal cancer cells. Anticancer Res 2010, 30:785-792. 3816511, 20392997.
35. Gao X, Deeb D, Liu P, Liu Y, Arbab-Ali S, Dulchavsky SA, Gautam SC. Role of reactive oxygen species (ROS) in CDDO-Me-mediated growth inhibition and apoptosis in colorectal cancer cells. J Exp Ther Oncol 2011, 9:119-127. 3750951, 21699019.
36. Gao X, Liu Y, Deeb D, Arbab AS, Guo AM, Dulchavsky SA, Gautam SC. Synthetic oleanane triterpenoid, CDDO-Me, induces apoptosis in ovarian cancer cells by inhibiting prosurvival AKT/NF-κB/mTOR signaling. Anticancer Res 2011, 31:3673-3681. 3711099, 22110186.
37. Gao X, Liu Y, Deeb D, Liu P, Liu A, Arbab AS, Gautam SC. ROS mediate proapoptotic and antisurvival activity of oleanane triterpenoid CDDO-Me in ovarian cancer cells. Anticancer Res 2013, 33:215-221. 3711076, 23267148.
38. Gao X, Deeb D, Jiang H, Liu Y, Dulchavsky SA, Gautam SC. Synthetic triterpenoids inhibit growth and induce apoptosis in human glioblastoma and neuroblastoma cells through inhibition of prosurvival Akt, NF-kappaB and Notch1 signaling. J Neurooncol 2007, 84:147-157. 10.1007/s11060-007-9364-9, 17361329.
39. Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 2009, 9:798-809. 10.1038/nrc2734, 19851315.
40. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine Growth Factor Rev 2010, 21:11-19. 10.1016/j.cytogfr.2009.11.005, 2834864, 20018552.
41. Ahmad R, Raina D, Meyer C, Kufe D. Triterpenoid CDDO-methyl ester inhibits the Janus-activated kinase-1 (JAK1) → signal transducer and activator of transcription-3 (STAT3) pathway by direct inhibition of JAK1 and STAT3. Cancer Res 2008, 68:2920-2926. 10.1158/0008-5472.CAN-07-3036, 3092292, 18413761.
42. Duan Z, Ames RY, Ryan M, Hornicek FJ, Mankin H, Seiden MV. CDDO-Me, a synthetic triterpenoid, inhibits expression of IL-6 and Stat3 phosphorylation in multi-drug resistant ovarian cancer cells. Cancer Chemother Pharmacol 2009, 63:681-689. 10.1007/s00280-008-0785-8, 2875930, 18587580.
43. Ryu K, Susa M, Choy E, Yang C, Hornicek FJ, Mankin HJ, Duan Z. Oleanane triterpenoid CDDO-Me induces apoptosis in multidrug resistant osteosarcoma cells through inhibition of Stat3 pathway. BMC Cancer 2010, 10:187. 10.1186/1471-2407-10-187, 2874784, 20459702.
44. Hengartner MO. The biochemistry of apoptosis. Nature 2000, 407:770-776. 10.1038/35037710, 11048727.
45. Kim KB, Lotan R, Yue P, Sporn MB, Suh N, Gribble GW, Honda T, Wu GS, Hong WK, Sun SY. Identification of a novel synthetic triterpenoid, methyl-2-cyano-3,12-dioxooleana-1,9-dien-28-oate, that potently induces caspase-mediated apoptosis in human lung cancer cells. Mol Cancer Ther 2002, 1:177-184.
46. Konopleva M, Tsao T, Ruvolo P, Stiouf I, Estrov Z, Leysath CE, Zhao S, Harris D, Chang S, Jackson CE, Munsell M, Suh N, Gribble G, Honda T, May WS, Sporn MB, Andreeff M. Novel triterpenoid CDDO-Me is a potent inducer of apoptosis and differentiation in acute myelogenous leukemia. Blood 2002, 99:326-335. 10.1182/blood.V99.1.326, 11756188.
47. Zou W, Liu X, Yue P, Zhou Z, Sporn MB, Lotan R, Khuri FR, Sun SY. c-Jun NH2-terminal kinase-mediated up-regulation of death receptor 5 contributes to induction of apoptosis by the novel synthetic triterpenoid methyl-2-cyano-3,12-dioxooleana-1, 9-dien-28-oate in human lung cancer cells. Cancer Res 2004, 64:7570-7578. 10.1158/0008-5472.CAN-04-1238, 15492284.
48. Zou W, Yue P, Khuri FR, Sun SY. Coupling of endoplasmic reticulum stress to CDDO-Me-induced up-regulation of death receptor 5 via a CHOP-dependent mechanism involving JNK activation. Cancer Res 2008, 68:7484-7492. 10.1158/0008-5472.CAN-08-1318, 2597446, 18794136.
49. Zou W, Chen S, Liu X, Yue P, Sporn MB, Khuri FR, Sun SY. c-FLIP downregulation contributes to apoptosis induction by the novel synthetic triterpenoid methyl-2-cyano-3, 12-dioxooleana-1, 9-dien-28-oate (CDDO-Me) in human lung cancer cells. Cancer Biol Ther 2007, 6:1614-1620. 10.4161/cbt.6.10.4763, 18253090.
50. Greider CW. Chromosome first aid. Cell 1991, 67:645-647. 10.1016/0092-8674(91)90058-7, 1934066.
51. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW. Specific association of human telomerase activity with immortal cells and cancer. Science 1994, 266:2011-2015. 10.1126/science.7605428, 7605428.
52. Shay JW, Bacchetti S. A survey of telomerase activity in human cancer. Eur J Cancer 1997, 33:787-791. 10.1016/S0959-8049(97)00062-2, 9282118.
53. Cech TR. Beginning to understand the end of the chromosome. Cell 2004, 116:273-279. 10.1016/S0092-8674(04)00038-8, 14744437.
54. Deeb D, Gao X, Liu Y, Kim SH, Pindolia KR, Arbab AS, Gautam SC. Inhibition of cell proliferation and induction of apoptosis by oleanane triterpenoid (CDDO-Me) in pancreatic cancer cells is associated with the suppression of hTERT gene expression and its telomerase activity. Biochem Biophys Res Commun 2012, 422:561-567. 10.1016/j.bbrc.2012.05.024, 3576813, 22609405.
55. Deeb D, Gao X, Liu Y, Varma NR, Arbab AS, Gautam SC. Inhibition of telomerase activity by oleanane triterpenoid CDDO-Me in pancreatic cancer cells is ROS-dependent. Molecules 2013, 18:3250-3265. 10.3390/molecules18033250, 3632053, 23486104.
56. Nagaraj S, Youn JI, Weber H, Iclozan C, Lu L, Cotter MJ, Meyer C, Becerra CR, Fishman M, Antonia S, Sporn MB, Liby KT, Rawal B, Lee JH, Gabrilovich DI. Anti-inflammatory triterpenoid blocks immune suppressive function of MDSCs and improves immune response in cancer. Clin Cancer Res 2010, 16:1812-1823. 10.1158/1078-0432.CCR-09-3272, 2840181, 20215551.
57. Ostrand-Rosenberg S. Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 2010, 59:1593-1600. 10.1007/s00262-010-0855-8, 3706261, 20414655.
58. Youn JI, Gabrilovich DI. The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 2010, 40:2969-2975. 10.1002/eji.201040895, 3277452, 21061430.
59. Jutooru I, Chadalapaka G, Abdelrahim M, Basha MR, Samudio I, Konopleva M, Andreeff M, Safe S. Methyl 2-cyano-3,12-dioxooleana-1,9-dien-28-oate decreases specificity protein transcription factors and inhibits pancreatic tumor growth: role of microRNA-27a. Mol Pharmacol 2010, 78:226-236. 10.1124/mol.110.064451, 2917860, 20488920.
60. Ling X, Konopleva M, Zeng Z, Ruvolo V, Stephens LC, Schober W, McQueen T, Dietrich M, Madden TL, Andreeff M. The novel triterpenoid C-28 methyl ester of 2-cyano-3, 12-dioxoolen-1, 9-dien-28-oic acid inhibits metastatic murine breast tumor growth through inactivation of STAT3 signaling. Cancer Res 2007, 67:4210-4218. 10.1158/0008-5472.CAN-06-3629, 17483332.
61. Hong DS, Kurzrock R, Supko JG, He X, Naing A, Wheler J, Lawrence D, Eder JP, Meyer CJ, Ferguson DA, Mier J, Konopleva M, Konoplev S, Andreeff M, Kufe D, Lazarus H, Shapiro GI, Dezube BJ. A phase I first-in-human trial of bardoxolone methyl in patients with advanced solid tumors and lymphomas. Clin Cancer Res 2012, 18:3396-3406. 10.1158/1078-0432.CCR-11-2703, 22634319.