Radiation protection of the gastrointestinal tract and growth inhibition of prostate cancer xenografts by a single compound

Molecular Cancer Therapeutics

Volumn 13, Issue 12, 2014, Pages 2968-2977

  Alexeev, Vitali ^a   Lash, Elizabeth ^a   Aguillard, April ^a   Corsini, Laura ^a   Bitterman, Avi ^a   Ward, Keith ^b   Dicker, Adam P ^b   Linnenbach, Alban ^a   Rodeck, Ulrich ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b Reata Pharmaceuticals Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; 2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; AMIFOSTINE; ANTINEOPLASTIC AGENT; ETHYL PYRUVATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LITHIUM CHLORIDE; RTA 408; THIOL; TRITERPENOID; UNCLASSIFIED DRUG; GLYCOGEN SYNTHASE KINASE 3; N-(11-CYANO-2,2,6A,6B,9,9,12A-HEPTMETHYL-10,14-DIOXO-1,3,4,5,6A,6B,7,8,8A,9,10,12A,14,14A,14B-HEXADECAHYDRO-2H-PICEN-4A-YL)-2-2-DIFLUOROPROPIONAMIDE; RADIOPROTECTIVE AGENT; TRITERPENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL LINE; CANCER TISSUE; CELL PROLIFERATION; CELL PROTECTION; CONTROLLED STUDY; DRUG EFFICACY; GASTROINTESTINAL TRACT; GROWTH INHIBITION; HEMATOPOIETIC SYSTEM; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LETHAL DOSE; LNCAP CELL LINE; MALE; MOUSE; NONHUMAN; ORGAN SYSTEMS; PROSTATE CANCER; RADIATION PROTECTION; SIGNAL TRANSDUCTION; SKIN; TUMOR XENOGRAFT; ANIMAL; CELL SURVIVAL; DISEASE MODEL; DRUG EFFECTS; DRUG SCREENING; ENZYME ACTIVATION; METABOLISM; MORTALITY; PATHOLOGY; PROSTATE TUMOR; RADIATION RESPONSE; TUMOR CELL LINE; TUMOR VOLUME; WHOLE BODY RADIATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; GASTROINTESTINAL TRACT; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; MICE; NF-KAPPA B; PROSTATIC NEOPLASMS; RADIATION-PROTECTIVE AGENTS; TRITERPENES; TUMOR BURDEN; WHOLE-BODY IRRADIATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84918494247     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0354     Document Type: Article

References (50)

1. Kountouras J, Zavos C. Recent advances in the management of radiation colitis. World J Gastroenterol 2008;14:7289-301.
2. Souhami L, Bae K, Pilepich M, Sandler H. Impact of the duration of adjuvant hormonal therapy in patients with locally advanced prostate cancer treated with radiotherapy: a secondary analysis of RTOG 85-31. J Clin Oncol 2009;27:2137-43.
3. Simone NL, Menard C, Soule BP, Albert PS, Guion P, Smith S, et al. Intrarectal amifostine during external beam radiation therapy for prostate cancer produces significant improvements in Quality of Life measured by EPIC score. Int J Radiat Oncol Biol Phys 2008;70:90-5.
4. Spitz DRD, Hauer-Jensen M. Ionizing radiation-induced responses: where free radical chemistry meets redox biology and medicine. Antioxid Redox Signal 2014;20:1407-9.
5. Deorukhkar A, Krishnan S. Targeting inflammatory pathways for tumor radiosensitization. Biochem Pharmacol 2010;80:1904-14.
6. Daroczi B, Kari G, Ren Q, Dicker AP, Rodeck U. Nuclear factor kappaB inhibitors alleviate and the proteasome inhibitor PS-341 exacerbates radiation toxicity in zebrafish embryos. Mol Cancer Ther 2009;8:2625-34.
7. Thotala DK, Hallahan DE, Yazlovitskaya EM. Inhibition of glycogen synthase kinase 3 beta attenuates neurocognitive dysfunction resulting from cranial irradiation. Cancer Res 2008;68:5859-68.
8. Thotala DK, Geng L, Dickey AK, Hallahan DE, Yazlovitskaya EM. A new class of molecular targeted radioprotectors: GSK-3beta inhibitors. Int J Radiat Oncol Biol Phys 2010;76:557-65.
9. Jacobs KM, Bhave SR, Ferraro DJ, Jaboin JJ, Hallahan DE, Thotala D. GSK-3beta: A Bifunctional Role in Cell Death Pathways. Int J Cell Biol 2012;2012:930710.
10. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000;406:86-90.
11. Cremer TJ, Shah P, Cormet-Boyaka E, Valvano MA, Butchar JP, Tridandapani S. Akt-mediated proinflammatory response of mononuclear phagocytes infected with Burkholderia cenocepacia occurs by a novel GSK3beta-dependent, IkappaB kinase-independent mechanism. J Immunol 2011;187:635-43.
12. Hall EJ, Giaccia AJ. Cell survival curves. Radiobiology for the radiologist. Philadelphia, PA: Lippincott Williams & Wilkins; 2006. p. 30-46.
13. Epperly M, Jin S, Nie S, Cao S, Zhang X, Franicola D, et al. Ethyl pyruvate, a potentially effective mitigator of damage after total-body irradiation. Radiat Res 2007;168:552-9.
14. Daroczi B, Kari G, McAleer MF, Wolf JC, Rodeck U, Dicker AP. In vivo radioprotection by the fullerene nanoparticle DF-1 as assessed in a zebrafish model. Clin Cancer Res 2006;12:7086-91.
15. Han Y, Englert JA, Yang R, Delude RL, Fink MP. Ethyl pyruvate inhibits nuclear factor-kappaB-dependent signaling by directly targeting p65. J Pharmacol Exp Ther 2005;312:1097-105.
16. Ahmad R, Raina D, Meyer C, Kharbanda S, Kufe D. Triterpenoid CDDO-Me blocks the NF-kappaB pathway by direct inhibition of IKKbeta on Cys-179. J Biol Chem 2006;281:35764-9.
17. Liby K, Hock T, Yore MM, Suh N, Place AE, Risingsong R, et al. The synthetic triterpenoids, CDDO and CDDO-imidazolide, are potent inducers of heme oxygenase-1 and Nrf2/ARE signaling. Cancer Res 2005;65:4789-98.
18. Coghlan MP, Culbert AA, Cross DA, Corcoran SL, Yates JW, Pearce NJ, et al. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem Biol 2000;7:793-803.
19. Zhang F, Phiel CJ, Spece L, Gurvich N, Klein PS. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J Biol Chem 2003;278:33067-77.
20. Saha S, Bhanja P, Liu L, Alfieri AA, Yu D, Kandimalla ER, et al. TLR9 agonist protects mice from radiation-induced gastrointestinal syndrome. PLoS ONE 2012;7:e29357.
21. Chen CD, Sawyers CL. NF-kappa B activates prostate-specific antigen expression and is upregulated in androgen-independent prostate cancer. Mol Cell Biol 2002;22:2862-70.
22. Zhang L, Altuwaijri S, Deng F, Chen L, Lal P, Bhanot UK, et al. NF-kappaB regulates androgen receptor expression and prostate cancer growth. Am J Pathol 2009;175:489-99.
23. McCall P, Bennett L, Ahmad I, Mackenzie LM, Forbes IW, Leung HY, et al. NFkappaB signalling is upregulated in a subset of castrate-resistant prostate cancer patients and correlates with disease progression. Br J Cancer 2012;107:1554-63.
24. Siddiqui IA, Shukla Y, Adhami VM, Sarfaraz S, Asim M, Hafeez BB, et al. Suppression of NFkappaB and its regulated gene products by oral administration of green tea polyphenols in an autochthonous mouse prostate cancer model. Pharm Res 2008;25:2135-42.
25. Andela VB, Gordon AH, Zotalis G, Rosier RN, Goater JJ, Lewis GD, et al. NFkappaB: a pivotal transcription factor in prostate cancer metastasis to bone. Clin Orthop Relat Res 2003:S75-85.
26. Jin R, Sterling JA, Edwards JR, DeGraff DJ, Lee C, Park SI, et al. Activation of NF-kappa B signaling promotes growth of prostate cancer cells in bone. PLoS ONE 2013;8:e60983.
27. Pajonk F, Pajonk K, McBride WH. Inhibition of NF-kappaB, clonogenicity, and radiosensitivity of human cancer cells. J Natl Cancer Inst 1999;91:1956-60.
28. Chendil D, Ranga RS, Meigooni D, Sathishkumar S, Ahmed MM. Curcumin confers radiosensitizing effect in prostate cancer cell line PC-3. Oncogene 2004;23:1599-607.
29. Sun Y, St Clair DK, Fang F, Warren GW, Rangnekar VM, Crooks PA, et al. The radiosensitization effect of parthenolide in prostate cancer cells is mediated by nuclear factor-kappaB inhibition and enhanced by the presence of PTEN. Mol Cancer Ther 2007;6:2477-86.
30. Xu Y, Fang F, St Clair DK, Sompol P, Josson S, St Clair WH. SN52, a novel nuclear factor-kappaB inhibitor, blocks nuclear import of RelB: p52 dimer and sensitizes prostate cancer cells to ionizing radiation. Mol Cancer Ther 2008;7:2367-76.
31. 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;27:3035-44.
32. 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;7:31-9.
33. Gao X, Deeb D, Liu Y, Arbab AS, Divine GW, Dulchavsky SA, et al. Prevention of prostate cancer with oleanane synthetic triterpenoid CDDO-Me in the TRAMP mouse model of prostate cancer. Cancers 2011;3:3353-69.
34. Shishodia S, Sethi G, Konopleva M, Andreeff M, Aggarwal BB. A synthetic triterpenoid, CDDO-Me, inhibits IkappaBalpha kinase and enhances apoptosis induced by TNF and chemotherapeutic agents through down-regulation of expression of nuclear factor kappaB-regulated gene products in human leukemic cells. Clin Cancer Res 2006;12:1828-38.
35. Samudio I, Kurinna S, Ruvolo P, Korchin B, Kantarjian H, Beran M, et al. Inhibition of mitochondrial metabolism by methyl-2-cyano-3,12-diox-ooleana-1,9-diene-28-oate induces apoptotic or autophagic cell death in chronic myeloid leukemia cells. Mol Cancer Ther 2008;7:1130-9.
36. Stadheim TA, Suh N, Ganju N, Sporn MB, Eastman A. The novel triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO) potently enhances apoptosis induced by tumor necrosis factor in human leukemia cells. J Biol Chem 2002;277:16448-55.
37. Pedersen IM, Kitada S, Schimmer A, Kim Y, Zapata JM, Charboneau L, et al. The triterpenoid CDDO induces apoptosis in refractory CLL B cells. Blood 2002;100:2965-72.
38. Qin Y, Deng W, Ekmekcioglu S, Grimm EA. Identification of unique sensitizing targets for anti-inflammatory CDDO-Me in metastatic melanoma by a large-scale synthetic lethal RNAi screening. Pigment Cell Melanoma Res 2013;26:97-112.
39. Konopleva M, Zhang W, Shi YX, McQueen T, Tsao T, Abdelrahim M, et al. Synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces growth arrest in HER2-overexpressing breast cancer cells. Mol Cancer Ther 2006;5:317-28.
40. 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;63:681-9.
41. Gao X, Deeb D, Liu P, Liu Y, Arbab-Ali S, Dulchavsky SA, et al. Role of reactive oxygen species (ROS) in CDDO-Me-mediated growth inhibition and apoptosis in colorectal cancer cells. J Exp Ther Oncol 2011;9:119-27.
42. Zou W, Chen S, Liu X, Yue P, Sporn MB, Khuri FR, et al. 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;6:1614-20.
43. Deeb D, Gao X, Jiang H, Janic B, Arbab AS, Rojanasakul Y, et al. Oleanane triterpenoid CDDO-Me inhibits growth and induces apoptosis in prostate cancer cells through a ROS-dependent mechanism. Biochem Pharmacol 2010;79:350-60.
44. Kim SB, Pandita RK, Eskiocak U, Ly P, Kaisani A, Kumar R, et al. Targeting of Nrf2 induces DNA damage signaling and protects colonic epithelial cells from ionizing radiation. Proc Natl Acad Sci U S A 2012;109:E2949-55.
45. Reisman SA, Lee C-Y, Meyer CJ, Proksch JW, Sonis ST, Ward KW. Topical application of the synthetic triterpenoid RTA 408 protects mice from radiation-induced dermatitis. Radiat Res 2014;181:512-20.
46. Xu Y, Fang F, Miriyala S, Crooks PA, Oberley TD, Chaiswing L, et al. KEAP1 is a redox sensitive target that arbitrates the opposing radiosensitive effects of parthenolide in normal and cancer cells. Cancer Res 2013;73:4406-17.
47. Garcia-Pineres AJ, Castro V, Mora G, Schmidt TJ, Strunck E, Pahl HL, et al. Cysteine 38 in p65/NF-kappaB plays a crucial role in DNA binding inhibition by sesquiterpene lactones. J BiolChem2001;276:39713-20.
48. Kwok BH, Koh B, Ndubuisi MI, Elofsson M, Crews CM. The antiinflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem Biol 2001;8:759-66.
49. Hehner SP, Hofmann TG, Droge W, Schmitz ML. The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-kappa B by targeting the I kappa B kinase complex. J Immunol 1999;163:5617-23.
50. Nagaraj S, Youn JI, Weber H, Iclozan C, Lu L, Cotter MJ, et al. Antiinflammatory triterpenoid blocks immune suppressive function of MDSCs and improves immune response in cancer. Clin Cancer Res 2010;16:1812-23.