The synthetic triterpenoids, CDDO and CDDO-imidazolide, are potent inducers of heme oxygenase-1 and Nrf2/ARE signaling

Cancer Research

Volumn 65, Issue 11, 2005, Pages 4789-4798

  Liby, Karen ^a   Hock, Thomas ^c   Yore, Mark M ^a   Suh, Nanjoo ^a   Place, Andrew E ^a   Risingsong, Renee ^a   Williams, Charlotte R ^a   Royce, Darlene B ^a   Honda, Tadashi ^b   Honda, Yukiko ^b   Gribble, Gordon W ^b   Hill Kapturczak, Nathalie ^c   Agarwal, Anupam ^c   Sporn, Michael B ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH COLLEGE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [2 CYANO 3,12 DIOXOOLEANA 1,19(11) DIEN 28 OYL]IMIDAZOLE; 2 CYANO 3,12 DIOXOOLEANA 1,9 DIEN 28 OIC ACID; CYCLIC AMP; HEME OXYGENASE 1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; TRITERPENOID; UNCLASSIFIED DRUG;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CANCER PREVENTION; CHEMOPROPHYLAXIS; CHEMOTHERAPY; CONTROLLED STUDY; CRYOPROTECTION; DETOXIFICATION; E BOX ELEMENT; GENE CONTROL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALS; ANTIOXIDANTS; CELL LINE, TUMOR; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA-BINDING PROTEINS; ENZYME INDUCTION; GENE EXPRESSION REGULATION, LEUKEMIC; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HUMANS; IMIDAZOLES; MEMBRANE PROTEINS; MICE; NF-E2-RELATED FACTOR 2; OLEANOLIC ACID; OXIDATIVE STRESS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSFECTION; U937 CELLS;

EID: 21144431523     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-4539     Document Type: Article

References (62)

1. Huang MT, Ho CT Wang ZY, et al. Inhibition of skin tumorigenesis by rosemary and its constituents carnosol and ursolic acid. Cancer Res 1994;54: 701-8.
2. Nishino H, Nishino A, Takayasu J, et al. Inhibition of the tumor-promoting action of 12-O-tetradecanoylphorbol-13-acetate by some oleanane-type trlterpenoid compounds. Cancer Res 1988;48: 5210-5.
3. Hirota M, Mori T, Yoshida M, Iriye R. Suppression of tumor promoter-induced inflammation of mouse ear by ursolic acid and 4,4-dimethylcholestane derivatives. Agricultural and Biol Chem 1990;54:1073-5.
4. Singh GB, Singh S, Bani S, Gupta BD, Banerjee SK. Antiinflammatory activity of oleanolic acid in rats and mice. J Pharm Pharmacol 1992;44:456-8.
5. Honda T, Rounds BV, Gribble GW, Suh N, Wang Y, Sporn MB. Design and synthesis of 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid, a novel and highly active Inhibitor of nitric oxide production in mouse macrophages. Bioorg Med Chem Lett 1998;6:2711-4.
6. Honda T, Gribble GW, Suh N, et al. Novel synthetic oleanane and ursane triterpenoids with various enone functionalities In ring A as inhibitors of nitric oxide production in mouse macrophages. J Med Chem 2000;43:1866-77.
7. Honda T, Rounds BV, Bore L, et al. Synthetic oleanane and ursane triterpenoids with modified rings A and C: a series of highly active inhibitors of nitric oxide production in mouse macrophages. J Med Chem 2000;43:4233-46.
8. Honda T, Honda Y, Favaloro FG Jr, et al. A novel dicyanotriterpenoid. 2-cyano-3,12-dioxooleana-1,9(11)-dien-28-onitrile, active at picomolar concentrations for inhibition of nitric oxide production. Bioorg Med Chem Lett 2002;12:1027-30.
9. Suh N, Wang Y, Honda T, et al. 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;59:336-41.
10. Ito Y, Pandey P, Place A, et al. The novel triterpenoid 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid Induces apoptosis of human myelold leukemia cells by a cospase-8-dependent mechanism. Cell Growth Differ 2000;11:261-7.
11. Suh WS, Kim YS, Schimmer AD, et al. Synthetic triterpenoids activate a pathway for apoptosis In AML cells Involving downregulation of FLIP and sensitization to TRAIL, Leukemia 2003;17:2122-9.
12. Chauhan D, Li G, Podar K, et al. The bortezomib/proteasome inhibitor PS-341 and triterpenold CDDO-Im Induce synergistic anti-multiple myeloma (MM) activity and overcome bortezomib resistance, Blood 2004;103:3158-66.
13. Place AE, Suh N, Williams CR, et al. The novel synthetic triterpenold, CDDO-imidazolide, inhibits inflammatory response and tumor growth in vivo. Clin Cancer Res 2003;9:2798-806.
14. Wang Y, Porter WW, Suh N, et al. A synthetic triterpenoid, 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO), is a ligand for the peroxisome prollferator-activated receptor γ. Mol Endocrinol 2000;14: 1550-6.
15. Lapillonne H, Konopleva M, Taao T, et al. Activation of peroxisome proliferacor-activated receptor γ by a novel synthetic triterpenoid 2-cyano-3, 12-dioxooleana-1,9-dten-28-olc acid Induces growth arrest and apoptosis in breast cancer cells. Cancer Res 2003;63:5926-39.
16. Cruse I, Moines MD. Evidence suggesting that the two forms of heme oxygenase are products of different genes, J Biol Chem 1988;263:3348-53.
17. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 1986;261:411-9.
18. McCoubrey WK Jr, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 1997;247:725-32.
19. Hayaishi S, Omata Y, Sakamoto H, et al Characterization of rat heme oxygenase-3 gene. Implication of processed pseudogenes derived from heme oxygenase-2 gene. Gene 2004;336:241-50.
20. Ryter SW, Otterbein LE, Morse D, Choi AM. Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 2002;234-5:249-63.
21. Morse D, Choi AM. Heme oxygenase-1: the "emerging molecule" has arrived. Am J Respir Cell Mol Biol 2002; 27:8-16.
22. Takahashi T, Morita K, Akagi R, Sassa S. Heme oxygenase-1: a novel therapeutic target In oxidative tissue injuries. Curr Med Chem 2004:11: 1545-61.
23. Alcaraz MJ, Fernandez P, Guillen MI, Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr Pharm Des 2003;9:2541-51.
24. Gong E Stewart D, Hu B, et al. Activation of the mouse heme oxygenase-1 gene by 15-deoxy-δ(12,14)-prostaglandin J(2) is mediated by the stress response elements and transcription factor Nrf2, Antioxid Redox Signal 2002;4:249-57.
25. Alam J, Cal J, Smith A. Isolation and characterization of the mouse heme oxygenase-1 gene. Distal 5′ sequences are required for induction by heme or heavy metals. J Biol Chem 1994;269:1001-9.
26. Martin D. Rojo AI, Salinas M, et al. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-klnase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemlcal carnosol. J Biol Chem 2004;279:8919-29.
27. Hill-Kapturczak N. Voakes C, Garcia J, Visner G, Nick HS, Agarwal A. A cis-Acting region regulates oxidized lipld-mediated Induction of the human heme oxygenase-1 gene In endothelial cells. Arterloscler Thromb Vase Biol 2003;23:1416-22.
28. Hill-Kapturczak N, Sikorski E, Voakes C, Garcia J, Nick HS, Agarwal A. An internal enhancer regulates heme- and cadmium-mediated induction of human heme oxygenase-1. Am J Physiol Renal Physiol 2003; 285:F515-23.
29. Alvarez-Maqueda M, El Bekay R, Alba G. et al. 15-deoxy-δ 12,14-prostaglandin J2 induces heme oxygenase-1 gene expression in a reactive oxygen species-dependent manner in human lymphocytes. J Biol Chem 2004;279:21929-37.
30. Kronke G, Bochkov VN, Huber J, et al. Oxidized phospholipids induce expression of human heme oxygenase-1 involving activation of cAMP-responsive element-binding protein. J Biol Chem 2003;278:51006-14.
31. Sikorski EM, Hock T, Hill-Kapturczak N, Agarwal A. The story so for: Molecular regulation of the heme oxygenase-1 gene In renal injury. Am J Physiol Renal Physiol 2004;286:F425-41.
32. Balogun E, Hoque M, Gong P, et al. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J 2003;371:887-95.
33. Dhakshinamoorthy S, Jaiswal AK. Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H:quinone oxidoreductase1 gene. Oncogene 2001;20:3906-17.
34. Itoh K, Wakabayashl N, Katoh Y, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the aminoterminal Neh2 domain. Genes Dev 1999;13:76-86.
35. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999;274:2607 1-8.
36. Alam J, Cook JL. Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway. Curr Pharm Des 2003;9: 2499-511.
37. Zhang Y, Gordon GB. A strategy for cancer prevention: stimulation of the Nrf2-ARE signaling pathway. Mol Cancer Ther 2004;3:885-93.
38. Motohashi H, Yamamoto M. Nrfi-Keap1 defines a physiologically Important stress response mechanism. Trends Mol Med 2004;10:549-57.
39. Leung L, Kwong M, Hou S, Lee C, Chan JY. Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J Biol Chem 2003;278:48021-9.
40. Suh N, Honda T, Finlay HJ, et al. Novel triterpenoids suppress inducible nitric oxide synthase (iNOS) and inducible cyclooxygenase (COX-2) in mouse macrophages. Cancer Res 1998;58:717-23.
41. Balla G, Jacob HS, Balla J, et al. Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem 1992;267:18148-53.
42. Agarwal A, Balla J, Alam J, Croatt AJ, Nath KA. Induction of heme oxygenase in toxic renal injury: a protective role in cisplatin nephrotoxicity In the rat. Kidney Int 1995;48:1298-307.
43. Shiojima I, Yefremashvili M, Luo Z, et al. Akt signaling mediates postnatal heart growth in response to Insulin and nutritional status. J Biol Chem 2002;277: 37670-7.
44. Kataoka K, Handa H, Nishizawa M. Induction of cellular ontioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds. J Biol Chem 2001;276: 34074-81.
45. Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C. A dominant-negative inhibitor of CREB reveals that it Is a general mediator of stimulus-dependent transcription of c-fos. Mol Cell Biol 1998;18: 967-77.
46. Qyang Y, Luo X, Lu T, et al. Cell-type-dependent activity of the ubiquitous transcription factor USF in cellular proliferation and transcriptional activation. Mol Cell Biol 1999;19:1508-17.
47. Hock TD, Nick HS, Agarwal A. Upstream stimulatory factors, USF1 and USF2, bind to the human haem oxygenase-1 proximal promoter in vivo and regulate its transcription. Biochem J 2004;383: 209-18.
48. Chen XL. Kunsch C. Induction of cytoproteotive genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr Pharm Des 2004; 10:879-91.
49. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 2002;62:5196-203.
50. Kwak MK Wakabayashl N, Itoh K, Motohashi H, Yamamoto M, Kensler TW. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J Biol Chem 2003;278: 8135-45.
51. Li J, Lee JM, Johnson JA. Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in 1MR-32 cells. J Biol Chem 2002;277:388-94.
52. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992;5:227-31.
53. Prestera T, Talalay P, Alam J, Ahn YI, Lee PJ, Choi AMK. Parallel induction of heme oxygenase-1 and chemoprotective phase-2 enzymes by electrophiles and antioxidants: regulation by upstream antioxidant-responsive elements (ARE). Mol Med 1995;I:827-37.
54. Hill-Kapturczak N, Thamilselvan V, Liu F, Nick HS, Agarwal A. Mechanism of heme oxygenase-1 gene induction by curcumin in human renal proximal tubule cells. Am J Physiol Renal Physiol 2001;281: F851-9.
55. Haridas V, Hanausek M, Nishimura G, et al. Triterpenoid electrophiles (avicIns) activate the innate stress response by redox. regulation of a gene battery. J Clin Invest 2004;113:65-73.
56. Zhuang H, Kim YS. Koehler RC, Dore S, Potential mechanism by which resveratrol, a red wine constituent protects neurons. Ann N Y Acad Sci 2003;993: 276-86.
57. Ma Y, Koza-Taylor PH, DiMattia DA, et al. Microarray analysis uncovers retinoid targets in human bronchial epithelial cells. Oncogene 2003;22:4924-32.
58. Grosser N, Abate A, Oberle S, et al. Heme oxygenase-1 induction may explain the antioxidant profile of aspirin. Biochem Biophys Res Commun 2003;308:956-60.
59. Suttner DM, Dennery PA. Reversal of HO-1 related cytoprotection with increased expression Is due to reactive iron. FASEB J 1999;13:1800-9.
60. Ikeda T, Sporn M, Honda T, Gribble GW, Kufe D. The novel triterpenold CDDO and its derivatives induce apoptosis by disruption of intracellular redox balance. Cancer Res 2003;63:5951-8.
61. Dinkova-Kostova AT, Liby KT, Stephenson KK, et al. Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress. Proc Natl Acad Sci U S A 2005;102:4584-9.
62. Ikeda T, Nakata Y, Kimura F, et al, Induction of redox imbalance and apoptosis in multiple myeloma cells by the novel triterpenoid 2-cyano-3,12-dloxoolean-1,9-dlen-28-oic acid. Mol Cancer Ther 2004; 3:39-45.