A water soluble parthenolide analog suppresses in vivo tumor growth of two tobacco-associated cancers, lung and bladder cancer, by targeting NF-κB and generating reactive oxygen species

International Journal of Cancer

Volumn 128, Issue 10, 2011, Pages 2481-2494

  Shanmugam, Rajasubramaniam ^a   Kusumanchi, Praveen ^a   Appaiah, Hitesh ^a   Cheng, Liang ^a   Crooks, Peter ^b   Neelakantan, Sundar ^b   Peat, Tyler ^a   Klaunig, James ^a   Matthews, William ^c   Nakshatri, Harikrishna ^a,d   Sweeney, Christopher J ^a,e  

^a INDIANA UNIVERSITY   (United States)

^b University of Kentucky   (United States)

^c Leuchemix Inc   (United States)

^d WALTHER CANCER INSTITUTE   (United States)

^e DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

apoptosis; cancer; cell cycle; dimethylaminoparthenolide

Indexed keywords

4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; ANTINEOPLASTIC AGENT; BROXURIDINE; CARCINOGEN; CYCLIN D1; DIMETHYLAMINOPARTHENOLIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NITROSAMINE KETONE; PARTHENOLIDE; PEPTIDES AND PROTEINS; PROTEIN P21; PROTEIN P73; PROTEIN TRAF 2; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLADDER CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CARCINOGENICITY; CELL CYCLE ARREST; CELL PROLIFERATION; CELL TYPE; CELL VIABILITY; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVATION; ENZYME INHIBITION; FLOW CYTOMETRY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG CANCER; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; MALE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; TOBACCO; TRANSITIONAL CELL CARCINOMA; TUMOR VOLUME; UPREGULATION; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; CARCINOGENS; CELL CYCLE; CELL DIVISION; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLOW CYTOMETRY; LUNG NEOPLASMS; MALE; MICE; MICE, NUDE; NF-KAPPA B; NITROSAMINES; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SESQUITERPENES; TOBACCO; URINARY BLADDER NEOPLASMS;

EID: 79953212611     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25587     Document Type: Article

References (47)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ,. Cancer statistics, 2008. CA Cancer J Clin 2008; 58: 71-96. (Pubitemid 351521864)
2. Sedjo RL, Byers T, Barrera E, Jr, Cohen C, Fontham ET, Newman LA, Runowicz CD, Thorson AG, Thun MJ, Ward E, Wender RC, Eyre HJ,. A midpoint assessment of the American Cancer Society challenge goal to decrease cancer incidence by 25% between 1992 and 2015. CA Cancer J Clin 2007; 57: 326-40. (Pubitemid 350234399)
3. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, Tan EH, Hirsh V, Thongprasert S, Campos D, Maoleekoonpiroj S, Smylie M, Martins R, van Kooten M, Dediu M, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 2005; 353: 123-32. (Pubitemid 41058344)
4. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, Lilenbaum R, Johnson DH,. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006; 355: 2542-50. (Pubitemid 44917502)
5. Bork PM, Schmitz ML, Kuhnt M, Escher C, Heinrich M,. Sesquiterpene lactone containing Mexican Indian medicinal plants and pure sesquiterpene lactones as potent inhibitors of transcription factor NF-kappaB. FEBS Lett 1997; 402: 85-90. (Pubitemid 27056030)
6. Wen J, You KR, Lee SY, Song CH, Kim DG,. Oxidative stress-mediated apoptosis. The anticancer effect of the sesquiterpene lactone parthenolide. J Biol Chem 2002; 277: 38954-64. (Pubitemid 35154761)
7. Hehner SP, Heinrich M, Bork PM, Vogt M, Ratter F, Lehmann V, Schulze-Osthoff K, Droge W, Schmitz ML,. Sesquiterpene lactones specifically inhibit activation of NF-kappa B by preventing the degradation of I kappa B-alpha and I kappa B-beta. J Biol Chem 1998; 273: 1288-97. (Pubitemid 28133643)
8. Sweeney C, Li L, Shanmugam R, Bhat-Nakshatri P, Jayaprakasan V, Baldridge LA, Gardner T, Smith M, Nakshatri H, Cheng L,. Nuclear factor-kappaB is constitutively activated in prostate cancer in vitro and is overexpressed in prostatic intraepithelial neoplasia and adenocarcinoma of the prostate. Clin Cancer Res 2004; 10: 5501-7. (Pubitemid 39100488)
9. Mendonca MS, Chin-Sinex H, Gomez-Millan J, Datzman N, Hardacre M, Comerford K, Nakshatri H, Nye M, Benjamin L, Mehta S, Patino F, Sweeney C,. Parthenolide sensitizes cells to X-ray-induced cell killing through inhibition of NF-kappaB and split-dose repair. Radiat Res 2007; 168: 689-97. (Pubitemid 351295105)
10. Gopal YN, Chanchorn E, van Dyke MW,. Parthenolide promotes the ubiquitination of MDM2 and activates p53 cellular functions. Mol Cancer Ther 2009; 8: 552-62.
11. Curry EA, III, Murry DJ, Yoder C, Fife K, Armstrong V, Nakshatri H, O'Connell M, Sweeney CJ,. Phase I dose escalation trial of feverfew with standardized doses of parthenolide in patients with cancer. Invest New Drugs 2004; 22: 299-305. (Pubitemid 39012569)
12. Shanmugam R, Jayaprakasan V, Gokmen-Polar Y, Kelich S, Miller KD, Yip-Schneider M, Cheng L, Bhat-Nakshatri P, Sledge GW, Jr, Nakshatri H, Zheng Q-H, Miller MA, et al. Restoring chemotherapy and hormone therapy sensitivity by parthenolide in a xenograft hormone refractory prostate cancer model. Prostate 2006; 66: 1498-511. (Pubitemid 44465816)
13. Neelakantan S, Nasim S, Guzman ML, Jordan CT, Crooks PA,. Aminoparthenolides as novel anti-leukemic agents: discovery of the NF-kappaB inhibitor, DMAPT (LC-1). Bioorg Med Chem Lett 2009; 19: 4346-9.
14. Guzman ML, Rossi RM, Neelakantan S, Li X, Corbett CA, Hassane DC, Becker MW, Bennett JM, Sullivan E, Lachowicz JL, Vaughan A, Sweeney CJ, et al. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood 2007; 110: 4427-35. (Pubitemid 351377809)
15. Hewamana S, Alghazal S, Lin TT, Clement M, Jenkins C, Guzman ML, Jordan CT, Neelakantan S, Crooks PA, Burnett AK, Pratt G, Fegan C, et al. The NF-kappaB subunit Rel A is associated with in vitro survival and clinical disease progression in chronic lymphocytic leukemia and represents a promising therapeutic target. Blood 2008; 111: 4681-9.
16. Jenkins C, Hewamana S, Gilkes A, Neelakantan S, Crooks P, Mills K, Pepper C, Burnett A,. Nuclear factor-kappaB as a potential therapeutic target for the novel cytotoxic agent LC-1 in acute myeloid leukaemia. Br J Haematol 2008; 143: 661-71.
17. Vegeler RC, Yip-Schneider MT, Ralstin M, Wu H, Crooks PA, Neelakantan S, Nakshatri H, Sweeney CJ, Schmidt CM,. Effect of celecoxib and novel agent LC-1 in a hamster model of lung cancer. J Surg Res 2007; 143: 169-76. (Pubitemid 47562462)
18. Yip-Schneider MT, Wu H, Njoku V, Ralstin M, Holcomb B, Crooks PA, Neelakantan S, Sweeney CJ, Schmidt CM,. Effect of celecoxib and the novel anti-cancer agent, dimethylamino-parthenolide, in a developmental model of pancreatic cancer. Pancreas 2008; 37: e45-53.
19. Yip-Schneider MT, Wu H, Ralstin M, Yiannoutsos C, Crooks PA, Neelakantan S, Noble S, Nakshatri H, Sweeney CJ, Schmidt CM,. Suppression of pancreatic tumor growth by combination chemotherapy with sulindac and LC-1 is associated with cyclin D1 inhibition in vivo. Mol Cancer Ther 2007; 6: 1736-44. (Pubitemid 46954050)
20. Chang GC, Yu CT, Tsai CH, Tsai JR, Chen JC, Wu CC, Wu WJ, Hsu SL,. An epidermal growth factor inhibitor, Gefitinib, induces apoptosis through a p53-dependent upregulation of pro-apoptotic molecules and downregulation of anti-apoptotic molecules in human lung adenocarcinoma A549 cells. Eur J Pharmacol 2008; 600: 37-44.
21. Mack PC, Gandara DR, Bowen C, Edelman MJ, Paglieroni T, Schnier JB, Gelmann EP, Gumerlock PH,. RB status as a determinant of response to UCN-01 in non-small cell lung carcinoma. Clin Cancer Res 1999; 5: 2596-604. (Pubitemid 29437347)
22. Sun SH, Zheng M, Ding K, Wang S, Sun Y,. A small molecule that disrupts Mdm2-p53 binding activates p53, induces apoptosis and sensitizes lung cancer cells to chemotherapy. Cancer Biol Ther 2008; 7: 845-52.
23. Ikediobi ON, Davies H, Bignell G, Edkins S, Stevens C, O'Meara S, Santarius T, Avis T, Barthorpe S, Brackenbury L, Buck G, Butler A, et al. Mutation analysis of 24 known cancer genes in the NCI-60 cell line set. Mol Cancer Therap 2006; 5: 2606-12. (Pubitemid 44848987)
24. Lonardo F, Dragnev KH, Freemantle SJ, Ma Y, Memoli N, Sekula D, Knauth EA, Beebe JS, Dmitrovsky E,. Evidence for the epidermal growth factor receptor as a target for lung cancer prevention. Clin Cancer Res 2002; 8: 54-60. (Pubitemid 34101459)
25. Chang YC, Lin P,. Trans, trans-2,4-decadienal induced cell proliferation via p27 pathway in human bronchial epithelial cells. Toxicol Appl Pharmacol 2008; 228: 76-83.
26. Decesse JT, Medjkane S, Datto MB, Cremisi CE,. RB regulates transcription of the p21/WAF1/CIP1 gene. Oncogene 2001; 20: 962-71. (Pubitemid 32207113)
27. Lehman TA, Modali R, Boukamp P, Stanek J, Bennett WP, Welsh JA, Metcalf RA, Stampfer MR, Fusenig N, Rogan EM, et al. p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 1993; 14: 833-9. (Pubitemid 23169134)
28. Sanchez-Carbayo M, Socci ND, Charytonowicz E, Lu M, Prystowsky M, Childs G, Cordon-Cardo C,. Molecular profiling of bladder cancer using cDNA microarrays: defining histogenesis and biological phenotypes. Cancer Res 2002; 62: 6973-80. (Pubitemid 35424089)
29. Backhus LM, Sievers E, Lin GY, Castanos R, Bart RD, Starnes VA, Bremner RM,. Perioperative cyclooxygenase 2 inhibition to reduce tumor cell adhesion and metastatic potential of circulating tumor cells in non-small cell lung cancer. J Thorac Cardiovasc Surg 2006; 132: 297-303. (Pubitemid 44092828)
30. Pugh TD, King JH, Koen H, Nychka D, Chover J, Wahba G, He YH, Goldfarb S,. Reliable stereological method for estimating the number of microscopic hepatocellular foci from their transections. Cancer Res 1983; 43: 1261-8. (Pubitemid 13160053)
31. Zhang S, Ong C-N, Shen H-M,. Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett 2004; 208: 143-53. (Pubitemid 38624155)
32. Temkin V, Karin M,. From death receptor to reactive oxygen species and c-Jun N-terminal protein kinase: the receptor-interacting protein 1 odyssey. Immunol Rev 2007; 220: 8-21. (Pubitemid 350045563)
33. Nakshatri H, Rice SE, Bhat-Nakshatri P,. Antitumor agent parthenolide reverses resistance of breast cancer cells to tumor necrosis factor-related apoptosis-inducing ligand through sustained activation of c-Jun N-terminal kinase. Oncogene 2004; 23: 7330-44. (Pubitemid 39382136)
34. Anand P, Thomas SG, Kunnumakkara AB, Sundaram C, Harikumar KB, Sung B, Tharakan ST, Misra K, Priyadarsini IK, Rajasekharan KN, Aggarwal BB,. Biological activities of curcumin and its analogues (Congeners) made by man and Mother Nature. Biochem Pharmacol 2008; 76: 1590-611.
35. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M, Baselga J, Norton L,. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001; 344: 783-92. (Pubitemid 32222155)
36. Liu J, Lin A,. Role of JNK activation in apoptosis: a double-edged sword. Cell Res 2005; 15: 36-42. (Pubitemid 41653963)
37. Faruqi RM, Poptic EJ, Faruqi TR, de La Motte C, DiCorleto PE,. Distinct mechanisms for N-acetylcysteine inhibition of cytokine-induced E-selectin and VCAM-1 expression. Am J Physiol 1997; 273: H817-26.
38. Shanmugam R, Kusumanchi K, Cheng L, Crooks P, Neelakantan S, Matthews W, Nakshatri H, Sweeney CJ,. A water soluble parthenolide analogue suppresses in vivo prostate cancer growth by targeting NF-κB and generating reactive oxygen species. Prostate 2010; 70: 1074-86.
39. Kastan MB, Bartek J,. Cell-cycle checkpoints and cancer. Nature 2004; 432: 316-23. (Pubitemid 39551659)
40. Helbig G, Christopherson KW, II, Bhat-Nakshatri P, Kumar S, Kishimoto H, Miller KD, Broxmeyer HE, Nakshatri H,. NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem 2003; 278: 21631-8. (Pubitemid 36792563)
41. Jones PL, Ping D, Boss JM,. Tumor necrosis factor alpha and interleukin-1beta regulate the murine manganese superoxide dismutase gene through a complex intronic enhancer involving C/EBP-beta and NF-kappaB. Mol Cell Biol 1997; 17: 6970-81. (Pubitemid 27505927)
42. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C,. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev 1999; 13: 382-7. (Pubitemid 29108753)
43. Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G,. NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc Natl Acad Sci USA 1999; 96: 9136-41. (Pubitemid 29374720)
44. Baldini N,. Multidrug resistance-a multiplex phenomenon. Nat Med 1997; 3: 378-80.
45. Wang CY, Mayo MW, Baldwin AS, Jr,. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 1996; 274: 784-7. (Pubitemid 26398259)
46. Karashima T, Sweeney P, Kamat A, Huang S, Kim SJ, Bar-Eli M, McConkey DJ, Dinney CP,. Nuclear factor-kappaB mediates angiogenesis and metastasis of human bladder cancer through the regulation of interleukin-8. Clin Cancer Res 2003; 9: 2786-97. (Pubitemid 36842125)
47. Joyce D, Albanese C, Steer J, Fu M, Bouzahzah B, Pestell RG,. NF-kappaB and cell-cycle regulation: the cyclin connection. Cytokine Growth Factor Rev 2001; 12: 73-90. (Pubitemid 32294588)