Persistent cyclooxygenase-2 inhibition downregulates NF-κB, resulting in chronic intestinal inflammation in the Min/+ mouse model of colon tumorigenesis

Cancer Research

Volumn 70, Issue 11, 2010, Pages 4433-4442

  Carothers, Adelaide M ^a   Davids, Jennifer S ^a   Damas, Beatrice C ^a   Bertagnolli, Monica M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELECOXIB; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; STRESS ACTIVATED PROTEIN KINASE 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLON CARCINOGENESIS; CONTROLLED STUDY; ENTERITIS; ENZYME INHIBITION; HUMAN; MOUSE; MYOFIBROBLAST; NONHUMAN; PANETH CELL; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD34; CELL TRANSFORMATION, NEOPLASTIC; COLITIS; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; DOWN-REGULATION; ILEUM; INTERLEUKIN-1BETA; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; NF-KAPPA B; PYRAZOLES; SULFONAMIDES; TOLL-LIKE RECEPTORS;

EID: 77953169550     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-09-4289     Document Type: Article

References (51)

1. Rhodes JM, Campbell BJ. Inflammation and colorectal cancer: IBD-associated and sporadic cancer compared. Trends Mol Med 2002;8:10-16
2. Bertagnolli MM. Chemoprevention of colorectal cancer with cyclooxygenase-2 inhibitors: two steps forward, one step back. Lancet Oncol 2007;8:439-443
3. Carothers AM, Moran AE, Cho NL, et al. Changes in the antitumor response in C57BL/6J-Min/+ mice during long-term administration of a selective cyclooxygenase-2 inhibitor. Cancer Res 2006;66:6432-6438
4. Davids JS, Carothers AM, Damas BC, Bertagnolli MM. Chronic cyclooxygenase-2 inhibition promotes myofibroblasts-associated intestinal fibrosis. Cancer Prev Res 2010;3:348-358
5. Karin M. Nuclear factor-κB in cancer development and progression. Nature 2006;441:431-436
6. Greten FR, Arkan MC, Bollrath J, et al. NF-κB is a negative regulator of IL-1β secretion as revealed by genetic and pharmacological inhibition of IKKβ. Cell 2007;130:918-931
7. Eckmann L, Nebelsiek T, Fingerle AA, et al. Opposing functions of IKKβ during acute and chronic intestinal inflammation. Proc Natl Acad Sci U S A 2008;105:15058-15063
8. Fukata M, Abreu MT. Role of Toll-like receptors in gastrointestinal malignancies. Oncogene 2008;27:234-243
9. Min/+ mice. J Infect Dis 2001;184:227-230
10. Rakoff-Nahous S, Medzhitov R. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88. Science 2007; 317:124-127
11. Brown SL, Riehl TE, Walker MR, et al. Myd88-dependent positioning of Ptgs2-expressing stromal cells maintains colonic epithelial proliferation during injury. J Clin Invest 2007;117:258-269
12. Shim J-H, Xiao C, Paschal AE, et al. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 2005:2668-2681
13. Lu T, Tian L, Han Y, Vogelbaum M, Stark GR. Dose-dependent crosstalk between the transforming growth factor-β and interleukin-1 signaling pathways. Proc Natl Acad Sci U S A 2007;104:4365-4370
14. Kajino-Sakamoto R, Inagaki M, Lippert E, et al. Enterocyte-derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis. J Immunol 2008;181:1143-1152
15. Yan M, Rerko RM, Platzer P, et al. 15-Hydroxyprostaglandin dehydrogenase, a Cox-2 oncogene antagonist is a TGFβ-induced suppressor of human gastrointestinal cancers. Proc Natl Acad Sci U S A 2004;101:17468-17473
16. Min/+ mice. Cancer Res 2002;62:403-408
17. Wall EA, Zavzavadjian JR, Chang MS, et al. Suppression of LPS-induced TNF-α production in macrophages by cAMP is mediated by PKA-AKAP95-p105. Sci Signal 2009;2:ra28.
18. Schiller M, Dennler S, Anderegg U, et al. Increased cAMP levels modulate transforming growth factor-β (TGF-β)/SMAD-induced expression of extracellular matrix components and other key fibroblast effector functions. J Biol Chem 2010;285:409-421
19. Buchanan FG, DuBois RN. Connecting Cox-2 and Wnt in cancer. Cancer Cell 2006;9:6-8.
20. Seno H, Miyoshi H, Brown SL, Geske MJ, Colonna M, Stappenbeck TS. Efficient colonic mucosal wound repair requires Trem2 signaling. Proc Natl Acad Sci U S A 2009;106:256-261
21. Tang Q, Chen W, Gonzales MS, Finch J, Inoue H, Bowden GT. Role of cyclic AMP response element in the UVB induction of cyclooxygenase-2 transcription in human keratinocytes. Oncogene 2001;20: 5164-5172
22. Chen AE, Ginty DD, Fan CM. Protein kinase A signaling via CREB controls myogenesis induced by Wnt proteins. Nature 2005;433: 317-322
23. Moran AE, Hunt DH, Javid SH, Redston M, Carothers AM, Bertagnolli MM. Apc deficiency is associated with increased Egfr activity in the intestinal enterocytes and adenomas of C57BL/6J-Min/+ mice. J Biol Chem 2004;279:43261-43272
24. Davis RJ. Signal transduction by the JNK group of MAP kinases. Cell 2000;103:239-252
25. Berger G, Hannahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8:592-603.
26. Carothers AM, Melstrom KA, Mueller JD, Weyant MJ, Bertagnolli MM. Progressive changes in adherens junction structure during intestinal adenoma formation in Apc mutant mice. J Biol Chem 2001; 276:39094-39102
27. National Institutes of Health. Image Processing and Analysis in Java Program (ImageJ). Available from: http://rsbweb.nih.gov/ij/.
28. 2 enhances osteoclastic differentiation of precursor cells through protein kinase A-dependent phosphorylation of TAK-1. J Biol Chem 2005;280:11395-11403
29. Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006;3: 390-407.
30. Masferrer JL, Leahy KM, Koki AT, et al. Antiangiogenic and anti-tumor activities of cyclooxygenase-2 inhibitors. Cancer Res 2000; 60:1306-1311
31. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A 2002;99:15451-15455
32. Crabtree B, Holloway DE, Baker MD, Acharya KR, Subramanian V. Biological and structural features of murine angiogenin-4, an angiogenic protein. Biochemistry 2007;46:2431-2443
33. 2-terminal kinase and p38 MAPK signal pathways in rat renal mesangial cells. J Biol Chem 1998;273:28670-28676
34. Araki Y, Okamura S, Perwez Hussain S, et al. Regulation of cyclooxygenase-2 expression by the Wnt and Ras pathways. Cancer Res 2005;65:728-734
35. Lee HK, Jeong S. β-Catenin stabilizes cyclooxygenase-2 mRNA by interacting with AU-rich elements of 3′-UTR. Nucleic Acid Res 2006; 34:5705-5714
36. Zaric J, Rüegg CJ. Integrin-mediated adhesion and soluble ligand binding stabilize COX-2 protein levels in endothelial cells by inducing expression and preventing degradation. J Biol Chem 2005;280: 1077-1085
37. Yazawa K, Tsuno NH, Kitayama J, et al. Selective inhibition of cylooxygenase-2 inhibits colon cancer cell adhesion to extracellular matrix by expression of β1 integrin. Cancer Sci 2005;96:93-99
38. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 2008;105:20858-20863
39. Wilson CL, Heppner KJ, Labosky PA, Hogan BL, Matrisian LM. Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci U S A 1997;94: 1402-1407
40. Wilson CL, Ouellett AJ, Satchell DP, et al. Regulation of intestinal α-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 1999;286:113-117
41. Kaser A, Blumberg RS. Paneth cells and inflammation dance together in Crohn's disease. Cell Res 2008;18:1160-1162
42. Kobayashi KS, Chamaillard M, Ogura Y, et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005;307:731-734
43. Steinbrecher KA, Harmel-Laws E, Sitcheran R, Baldwin AS. Loss of epithelial RelA results in deregulated intestinal proliferative/apoptotic homeostasis and susceptibility to inflammation. J Immunol 2008; 180:2588-2599
44. Glebov OK, Rodriquez LM, Lynch P, et al. Celecoxib treatment alters the gene expression profile of normal colonic mucosa. Cancer Epidemiol Biomarkers Prev 2006;15:1382-1391
45. Maier TJ, Tausch L,Hoernig M, et al. Celecoxib inhibits 5-lipoxygenase. Biochem Pharmacol 2008;76:862-872
46. Soh JW, Kazi JU, Li H, Thompson WJ, Weinstein IB. Celecoxib-induced growth inhibition in SW480 colon cancer cells is associated with activation of protein kinase G. Mol Carcinog 2008;47: 519-525
47. Sethi G, Tergaonkar V. Potential pharmacological control of the NF-κB pathway. Trends Pharmacol Sci 2009;30:313-321
48. Zaph C, Troy AE, Taylor BC, et al. Epithelial-cell-intrinsic IKK-β expression regulates intestinal immune homeostasis. Nature 2007; 446:552-556
49. Zhou Q, Liao JK. Rho kinase: an important mediator of atherosclerosis and vascular disease. Curr Pharm Des 2009;15:3108-3115
50. Weltz-Schmidt G, Welzenbach K, Brinkmann V, et al. Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site. Nature Med 2001;7:687-692
51. Riganti C, Doublier S, Costamagna C, et al. Activation of nuclear factor-κB pathway by simvastatin and RhoA silencing increases doxorubicin cytotoxicity in human colon cancer HT29 cells. Mol Pharmacol 2008;74:476-484