NF-κB and Nrf2 signaling pathways contribute to wogonin-mediated inhibition of inflammation-associated colorectal carcinogenesis

Cell Death and Disease

Volumn 5, Issue 6, 2014, Pages

  Yao, J ^a   Zhao, L ^a   Zhao, Q ^a   Zhao, Y ^a   Sun, Y ^a   Zhang, Y ^a   Miao, H ^a   You, Q D ^a   Hu, R ^a   Guo, Q L ^a  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

AOM DSS mouse model; Colitis associated cancer; NF B; Nrf2; Wogonin

Indexed keywords

AZOXYMETHANE; DEXTRAN SULFATE; I KAPPA B; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR NRF2; WOGONIN; FLAVANONE DERIVATIVE; IL1B PROTEIN, HUMAN; IL1B PROTEIN, MOUSE; IL6 PROTEIN, HUMAN; NFE2L2 PROTEIN, HUMAN; NFE2L2 PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INCIDENCE; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; COLITIS; COLORECTAL ADENOMA; COLORECTAL CARCINOGENESIS; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; DRUG MECHANISM; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HCT116 CELL LINE; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; THP 1 CELL LINE; ACTIVE TRANSPORT; ANIMAL; CELL NUCLEUS; COLORECTAL NEOPLASMS; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; SECRETION (PROCESS); TUMOR CELL LINE;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; COLORECTAL NEOPLASMS; FLAVANONES; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; MICE; NEOPLASM PROTEINS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84903760264     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.221     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T et al. Cancer statistics, 2008. CA Cancer J Clin 2008; 58: 71-96.
2. Neufert C, Becker C, Neurath MF. An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc 2007; 2: 1998-2004.
3. Suzuki R, Kohno H, Sugie S, Nakagama H, Tanaka T. Strain differences in the susceptibility to azoxymethane and dextran sodium sulfate-induced colon carcinogenesis in mice. Carcinogenesis 2006; 27: 162-169.
4. Yen D, Cheung J, Scheerens H, Poulet F, McClanahan T, McKenzie B et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 2006; 116: 1310-1316.
5. Yadav A, Kumar B, Datta J, Teknos TN, Kumar P. IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway. Mol Cancer Res 2011; 9: 1658-1667.
6. Tu S, Bhagat G, Cui G, Takaishi S, Kurt-Jones EA, Rickman B et al. Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 2008; 14: 408-419.
7. Karin M, Greten FR. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 2005; 5: 749-759.
8. Karin M, Cao Y, Greten FR, Li ZW. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2002; 2: 301-310.
9. Motohashi H, Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 2004; 10: 549-557.
10. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K et al. Oncogeneinduced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011; 475: 106-109.
11. Cullinan SB, Gordan JD, Jin J, Harper JW, Diehl JA. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol 2004; 24: 8477-8486.
12. Zhang DD, Lo SC, Sun Z, Habib GM, Lieberman MW, Hannink M. Ubiquitination of Keap1, a BTB-Kelch substrate adaptor protein for Cul3, targets Keap1 for degradation by a proteasome-independent pathway. J Biol Chem 2005; 280: 30091-30099.
13. Boutten A, Goven D, Artaud-Macari E, Boczkowski J, Bonay M. NRF2 targeting: a promising therapeutic strategy in chronic obstructive pulmonary disease. Trends Mol Med 2011; 17: 363-371.
14. Malhotra D, Thimmulappa R, Vij N, Navas-Acien A, Sussan T, Merali S et al. Heightened endoplasmic reticulum stress in the lungs of patients with chronic obstructive pulmonary disease: the role of Nrf2-regulated proteasomal activity. Am J Respir Crit Care Med 2009; 180: 1196-1207.
15. Chi YS, Lim H, Park H, Kim HP. Effects of wogonin, a plant flavone from Scutellaria radix, on skin inflammation: in vivo regulation of inflammation-associated gene expression. Biochem Pharmacol 2003; 66: 1271-1278.
16. Shen SC, Lee WR, Lin HY, Huang HC, Ko CH, Yang LL et al. In vitro and in vivo inhibitory activities of rutin, wogonin, and quercetin on lipopolysaccharide-induced nitric oxide and prostaglandin E(2) production. Eur J Pharmacol 2002; 446: 187-194.
17. Tang NY, Yang JS, Chang YH, Lu HF, Hsia TC, Lin WC et al. Effects of wogonin on the levels of cytokines and functions of leukocytes associated with NF-kappa B expression in Sprague-Dawley rats. In Vivo 2006; 20: 527-532.
18. Zhang YC, Gan FF, Shelar SB, Ng KY, Chew EH. Antioxidant and Nrf2 inducing activities of luteolin, a flavonoid constituent in Ixeris sonchifolia Hance, provide neuroprotective effects against ischemia-induced cellular injury. Food Chem Toxicol 2013; 59: 272-280.
19. Ehren JL, Maher P. Concurrent regulation of the transcription factors Nrf2 and ATF4 mediates the enhancement of glutathione levels by the flavonoid fisetin. Biochem Pharmacol 2013; 85: 1816-1826.
20. Zhai X, Lin M, Zhang F, Hu Y, Xu X, Li Y et al. Dietary flavonoid genistein induces Nrf2 and phase II detoxification gene expression via ERKs and PKC pathways and protects against oxidative stress in Caco-2 cells. Mol Nutr Food Res 2013; 57: 249-259.
21. Liu L, Li YH, Niu YB, Sun Y, Guo ZJ, Li Q et al. An apple oligogalactan prevents against inflammation and carcinogenesis by targeting LPS/TLR4/NF-kappaB pathway in a mouse model of colitis-associated colon cancer. Carcinogenesis 2010; 31: 1822-1832.
22. Nishitani Y, Zhang L, Yoshida M, Azuma T, Kanazawa K, Hashimoto T et al. Intestinal antiinflammatory activity of lentinan: influence on IL-8 and TNFR1 expression in intestinal epithelial cells. PLoS One 2013; 8: e62441.
23. Shaker A, Swietlicki EA, Wang L, Jiang S, Onal B, Bala S et al. Epimorphin deletion protects mice from inflammation-induced colon carcinogenesis and alters stem cell niche myofibroblast secretion. J Clin Invest 2010; 120: 2081-2093.
24. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009; 15: 103-113.
25. Ahmed S, Pakozdi A, Koch AE. Regulation of interleukin-1beta-induced chemokine production and matrix metalloproteinase 2 activation by epigallocatechin-3-gallate in rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 2006; 54: 2393-2401.
26. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006; 441: 431-436.
27. Surh YJ. NF-kappa B and Nrf2 as potential chemopreventive targets of some antiinflammatory and antioxidative phytonutrients with anti-inflammatory and antioxidative activities. Asia Pac J Clin Nutr 2008; 17(Suppl 1): 269-272.
28. Kundu JK, Surh YJ. Nrf2-Keap1 signaling as a potential target for chemoprevention of inflammation-associated carcinogenesis. Pharm Res 2010; 27: 999-1013.
29. Mantovani A. Cancer: inflaming metastasis. Nature 2009; 457: 36-37.
30. Joyce JA. Therapeutic targeting of the tumor microenvironment. Cancer Cell 2005; 7: 513-520.
31. Weisser SB, Brugger HK, Voglmaier NS, McLarren KW, van Rooijen N, Sly LM. SHIPdeficient, alternatively activated macrophages protect mice during DSS-induced colitis. J Leukoc Biol 2011; 90: 483-492.
32. Song YA, Park YL, Kim KY, Chung CY, Lee GH, Cho DH et al. Black tea extract prevents lipopolysaccharide-induced NF-kappaB signaling and attenuates dextran sulfate sodiuminduced experimental colitis. BMC Complement Altern Med 2011; 11:21.
33. Liu YW, Su YW, Ong WK, Cheng TH, Tsai YC. Oral administration of Lactobacillus plantarum K68 ameliorates DSS-induced ulcerative colitis in BALB/c mice via the anti-inflammatory and immunomodulatory activities. Int Immunopharmacol 2011; 11: 2159-2166.
34. Cai C, Teng L, Vu D, He JQ, Guo Y, Li Q et al. The heme oxygenase 1 inducer (CoPP) protects human cardiac stem cells against apoptosis through activation of the extracellular signal-regulated kinase (ERK)/NRF2 signaling pathway and cytokine release. J Biol Chem 2012; 287: 33720-33732.
35. Wang H, Khor TO, Saw CL, Lin W, Wu T, Huang Y et al. Role of Nrf2 in suppressing LPS-induced inflammation in mouse peritoneal macrophages by polyunsaturated fatty acids docosahexaenoic acid and eicosapentaenoic acid. Mol Pharm 2010; 7: 2185-2193.
36. Reddy NM, Kleeberger SR, Kensler TW, Yamamoto M, Hassoun PM, Reddy SP. Disruption of Nrf2 impairs the resolution of hyperoxia-induced acute lung injury and inflammation in mice. J Immunol 2009; 182: 7264-7271.
37. Shen H, Zhou S, Wang J. The paradoxical role of Nrf2 in tumor biology. Crit Rev Eukaryot Gene Expr 2013; 23: 37-47.
38. Akhdar H, Loyer P, Rauch C, Corlu A, Guillouzo A, Morel F. Involvement of Nrf2 activation in resistance to 5-fluorouracil in human colon cancer HT-29 cells. Eur J Cancer 2009; 45: 2219-2227.
39. Lau A, Villeneuve NF, Sun Z, Wong PK, Zhang DD. Dual roles of Nrf2 in cancer. Pharmacol Res 2008; 58: 262-270.
40. Chen N, Yi X, Abushahin N, Pang S, Zhang D, Kong B et al. Nrf2 expression in endometrial serous carcinomas and its precancers. Int J Clin Exp Pathol 2010; 4: 85-96.
41. Stacy DR, Ely K, Massion PP, Yarbrough WG, Hallahan DE, Sekhar KR et al. Increased expression of nuclear factor E2 p45-related factor 2 (NRF2) in head and neck squamous cell carcinomas. Head Neck 2006; 28: 813-818.
42. Cheng JH, Hung CF, Yang SC, Wang JP, Won SJ, Lin CN. Synthesis and cytotoxic, antiinflammatory, and anti-oxidant activities of 2',5'- dialkoxylchalcones as cancer chemopreventive agents. Bioorg Med Chem 2008; 16: 7270-7276.
43. Wu TY, Khor TO, Saw CL, Loh SC, Chen AI, Lim SS et al. Anti-inflammatory/Anti-oxidative stress activities and differential regulation of Nrf2-mediated genes by non-polar fractions of tea Chrysanthemum zawadskii and licorice Glycyrrhiza uralensis. AAPS J 2011; 13: 1-13.
44. Jin W, Zhu L, Guan Q, Chen G, Wang QF, Yin HX et al. Influence of Nrf2 genotype on pulmonary NF-kappaB activity and inflammatory response after traumatic brain injury. Ann Clin Lab Sci 2008; 38: 221-227.
45. Jin W, Wang H, Ji Y, Hu Q, Yan W, Chen G et al. Increased intestinal inflammatory response and gut barrier dysfunction in Nrf2-deficient mice after traumatic brain injury. Cytokine 2008; 44: 135-140.
46. Grivennikov S, Karin M. Autocrine IL-6 signaling: a key event in tumorigenesis? Cancer Cell 2008; 13: 7-9.
47. Li C, Lu N, Qi Q, Li F, Ling Y, Chen Y et al. Gambogic acid inhibits tumor cell adhesion by suppressing integrin beta1 and membrane lipid rafts-associated integrin signaling pathway. Biochem Pharmacol 2011; 82: 1873-1883.
48. Yao J, Hu R, Sun J, Lin B, Zhao L, Sha Y et al. Oroxylin A prevents inflammation-related tumor through down-regulation of inflammatory gene expression by inhibiting NF-kappaB signaling. Mol Carcinog 2014; 53: 145-158.
49. Zhao Q, Yang Y, Yu J, You QD, Zeng S, Gu HY et al. Posttranscriptional regulation of the telomerase hTERT by gambogic acid in human gastric carcinoma 823 cells. Cancer Lett 2008; 262: 223-231.