Parthenolide induces apoptosis in colitis-associated colon cancer, inhibiting NF-κB signaling

Oncology Letters

Volumn 9, Issue 5, 2015, Pages 2135-2142

  Kim, Se Lim ^a,b   Liu, Yu Chuan ^a,b   Seo, Seung Young ^a,b   Kim, Seong Hun ^a,b   Kim, In Hee ^a,b   Lee, Seung Ok ^a,b   Lee, Soo Teik ^a,b   Kim, Dae Ghon ^a,b   Kim, Sang Wook ^a,b  

^a Chonbuk National University Medical School and Hospital   (South Korea)

^b Chonbuk National University Medical School   (South Korea)

Author keywords

Apoptosis; Colitis associated colon cancer; Nuclear factor B; Parthenolide

Indexed keywords

AZOXYMETHANE; CASPASE 3; DEXTRAN SULFATE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PARTHENOLIDE; PROTEIN BCL 2; PROTEIN BCL XL; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TRANSCRIPTION FACTOR RELA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; COLON CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; FEMALE; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; ULCERATIVE COLITIS; WESTERN BLOTTING;

EID: 84925423145     PISSN: 17921074     EISSN: 17921082     Source Type: Journal    
DOI: 10.3892/ol.2015.3017     Document Type: Article

References (51)

1. Podolsky DK: Inflammatory bowel disease. N Engl J Med 347: 417-429, 2002.
2. Eaden JA, Abrams KR and Mayberry JF: The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48: 526-535, 2001.
3. Papadakis KA and Targan SR: Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med 51: 289-298, 2000.
4. Rogler G and Andus T: Cytokines in inflammatory bowel disease. World J Surg 22: 382-389, 1998.
5. Neurath MF, Fuss I, Schürmann G, et al: Cytokine gene transcription by NF-kappa B family members in patients with inflammatory bowel disease. Ann NY Acad Sci 859: 149-159, 1998.
6. Blackwell TS and Christman JW: The role of nuclear factor-kappa B in cytokine gene regulation. Am J Respir Cell Mol Biol 17: 3-9, 1997.
7. Baeuerle PA and Henkel T: Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12: 141-179, 1994.
8. Baldwin AS Jr: The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 14: 649-683, 1996.
9. Knight DW: Feverfew: chemistry and biological activity. Nat Prod Rep 12: 271-276, 1995.
10. Murphy JJ, Heptinstall S and Mitchell JR : Randomised double-blind placebo-controlled trial of feverfew in migraine prevention. Lancet 2: 189-192, 1988.
11. Hehner SP, Heinrich M, Bork PM, et al : 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 273: 1288-1297, 1998.
12. Lyss G, Knorre A, Schmidt TJ, Pahl HL and Merfort I: The anti-inflammatory sesquiterpene lactone helenalin inhibits the transcription factor NF-kappaB by directly targeting p65. J Biol Chem 273: 33508-33516, 1998.
13. Zhang S, Ong CN and Shen HM: Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett 208: 143-153, 2004.
14. Wen J, You KR, Lee SY, Song CH and Kim DG: Oxidative stress-mediated apoptosis. The anticancer effect of the sesquiterpene lactone parthenolide. J Biol Chem 277: 38954-38964, 2002.
15. Sweeney CJ, Mehrotra S, Sadaria MR, et al: The sesquiterpene lactone parthenolide in combination with docetaxel reduces metastasis and improves survival in a xenograft model of breast cancer. Mol Cancer Ther 4: 1004-1012, 2005.
16. Saadane A, Masters S, DiDonato J, Li J and Berger M: Parthenolide inhibits IkappaB kinase, NF-kappaB activation, and inflammatory response in cystic fibrosis cells and mice. Am J Respir Cell Mol Biol 36: 728-736, 2007.
17. Miyata N, Gon Y, Nunomura S, et al: Inhibitory effects of parthenolide on antigen-induced microtubule formation and degranulation in mast cells. Int Immunopharmacol 8: 874-880, 2008.
18. Hehner SP, Hofmann TG, Dröge W and Schmitz ML: The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-kappa B by targeting the I kappaB kinase complex. J Immunol 163: 5617-5623, 1999.
19. Kwok BH, Koh B, Ndubuisi MI, et al: The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem Biol 8: 759-766, 2001.
20. Kim SL, Trang KT, Kim SH, et al: Parthenolide suppresses tumor growth in a xenograft model of colorectal cancer cells by inducing mitochondrial dysfunction and apoptosis. Int J Oncol 41: 1547-1553, 2012.
21. Wang Y, Zhang HX, Sun YP, et al: Rig-I-/- mice develop colitis associated with downregulation of G alpha i2. Cell Res 17: 858-868, 2007.
22. Arthur JC, Perez-Chanona E, Mühlbauer M, et al: Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338: 120-123, 2012.
23. Pegg AE: Methylation of the O6 position of guanine in DNA is the most likely initiating event in carcinogenesis by methylating agents. Cancer Invest 2: 223-231, 1984.
24. Popivanova BK, Kitamura K, Wu Y, et al: Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 118: 560-570, 2008.
25. Tanaka T, Suzuki R, Kohno H, et al: Colonic adenocarcinomas rapidly induced by the combined treatment with 2-amino-1-methyl-6-phenylimidazo [4,5-b]pyridine and dextran sodium sulfate in male ICR mice possess beta-catenin gene mutations and increases immunoreactivity for beta-catenin, cyclooxygenase-2 and inducible nitric oxide synthase. Carcinogenesis 26: 229-238, 2005.
26. Kohno H, Suzuki R, Sugie S and Tanaka T: Beta-Catenin mutations in a mouse model of inflammation-related colon carcinogenesis induced by 1,2-dimethylhydrazine and dextran sodium sulfate. Cancer Sci 96: 69-76, 2005.
27. Hayden MS and Ghosh S: Shared principles in NF-kappaB signaling. Cell 132: 344-362, 2008.
28. Kim SL, Trang KT, Kim SH, et al: Parthenolide suppresses tumor growth in a xenograft model of colorectal cancer cells by inducing mitochondrial dysfunction and apoptosis. Int J Oncol 41: 1547-1553, 2012.
29. Okayasu I, Ohkusa T, Kajiura K, et al: Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut 39: 87-92, 1996.
30. Greten FR, Eckmann L, Greten TF, et al: IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118: 285-296, 2004.
31. Grivennikov S, Karin E, Terzic J, et al: IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15: 103-113, 2009.
32. Sobota R, Szwed M, Kasza A, et al: Parthenolide inhibits activation of signal transducers and activators of transcription (STATs) induced by cytokines of the IL-6 family. Biochem Biophys Res Commun 267: 329-333, 2000.
33. Song JM, Qian X, Upadhyayya P, et al: Dimethylaminoparthenolide, a water soluble parthenolide, suppresses lung tumorigenesis through down-regulating the STAT3 signaling pathway. Curr Cancer Drug Targets 14: 59-69, 2014.
34. Luo JL, Kamata H and Karin M: IKK/NF-kappaB signaling: balancing life and death - a new approach to cancer therapy. J Clin Invest 115: 2625-2632, 2005.
35. Hayden MS and Ghosh S: Signaling to NF-kappaB. Genes Dev 18: 2195-2224, 2004.
36. Karin M Ben-Neriah Y,and Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 18: 621-663, 2000.
37. Coussens LM and Werb Z: Inflammation and cancer. Nature 420: 860-867, 2002.
38. Lawrence T, Willoughby DA and Gilroy DW: Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat Rev Immunol 2: 787-795, 2002.
39. Vakkila J and Lotze MT: Inflammation and necrosis promote tumour growth. Nat Rev Immunol 4: 641-648, 2004.
40. Schottenfeld D, and Beebe-Dimmer J: Chronic inflammation: a common and important factor in the pathogenesis of neoplasia. CA Cancer J Clin 56: 69-83, 2006.
41. Schottenfeld D and Beebe-Dimmer JL: Advances in cancer epidemiology: understanding causal mechanisms and the evidence for implementing interventions. Annu Rev Public Health 26: 37-60, 2005.
42. Neurath MF, Pettersson S, Meyer zum Büschenfelde KH and Strober W: Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappaB abrogates established experimental colitis in mice. Nat Med 2: 998-1004, 1996.
43. Rogler G, Brand K, Vogl D, Page S, Hofmeister R, et al: Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology 115: 357-369, 1998.
44. Ardite E, Panés J, Miranda M, et al: Effects of steroid treatment on activation of nuclear factor kappaB in patients with inflammatory bowel disease. Br J Pharmacol 124: 431-433, 1998.
45. Kang BY, Chung SW and Kim TS: Inhibition of interleukin-12 production in lipopolysaccharide-activated mouse macrophages by parthenolide, a predominant sesquiterpene lactone in Tanacetum parthenium: involvement of nuclear factor-kappaB. Immunol Lett 77: 159-163, 2001.
46. Zhao ZJ, Xiang JY, Liu L, Huang XL and Gan HT: Parthenolide, an inhibitor of the nuclear factor-κB pathway, ameliorates dextran sulfate sodium-induced colitis in mice. Int Immunopharmacol 12: 169-174, 2012.
47. Wang CY, Mayo MW and Baldwin AS Jr: TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB. Science 274: 784-787, 1996.
48. Van Antwerp DJ, Martin SJ, Kafri T, Green DR and Verma IM: Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274: 787-789, 1996.
49. Beg AA and Baltimore D: An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274: 782-784, 1996.
50. Wang YW, Wang SJ, Zhou YN, Pan SH and Sun B: Escin augments the efficacy of gemcitabine through down-regulation of nuclear factor-κB and nuclear factor-κB-regulated gene products in pancreatic cancer both in vitro and in vivo. J Cancer Res Clin Oncol 138: 785-797, 2012.
51. Sun JG, Chen CY, Luo KW, et al: 3,5-Dimethyl-H-furo[3,2-g] chromen-7-one as a potential anticancer drug by inducing p53-dependent apoptosis in human hepatoma HepG2 cells. Chemotherapy 57: 162-172, 2011.