Antioxidant properties of mesalamine in colitis inhibit phosphoinositide 3-kinase signaling in progenitor cells

Inflammatory Bowel Diseases

Volumn 19, Issue 10, 2013, Pages 2051-2060

  Managlia, Elizabeth ^a   Katzman, Rebecca B ^a   Brown, Jeffrey B ^a   Barrett, Terrence A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Chronic ulcerative colitis; Intestinal epithelial cells; Mesalamine; PPAR ; ROS

Indexed keywords

BETA CATENIN; CATALASE; HYDROGEN PEROXIDE; MESALAZINE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE CRYPT; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STEM CELL; ULCERATIVE COLITIS;

ADOLESCENT; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; BETA CATENIN; BLOTTING, WESTERN; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CHRONIC DISEASE; COLITIS, ULCERATIVE; COLONIC NEOPLASMS; FLOW CYTOMETRY; HUMANS; HYDROGEN PEROXIDE; INTESTINAL MUCOSA; LASER CAPTURE MICRODISSECTION; MESALAMINE; MICE; MICE, INBRED C57BL; OXIDANTS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PPAR GAMMA; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELLS;

EID: 84884538411     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0b013e318297d741     Document Type: Article

References (60)

1. Bernstein CN, Blanchard JF, Kliewer E, et al. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer. 2001;91: 854-862.
2. Ekbom A, Helmick C, Zack M, et al. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med. 1990;323:1228-1233.
3. Karlen P, Lofberg R, Brostrom O, et al. Increased risk of cancer in ulcerative colitis: a population-based cohort study. Am J Gastroenterol. 1999;94:1047-1052.
4. Tang J, Sharif O, Pai C, et al. Mesalamine protects against colorectal cancer in inflammatory bowel disease. Dig Dis Sci. 2010;55:1696-1703.
5. Stolfi C, Fina D, Caruso R, et al. Cyclooxygenase-2-dependent and -independent inhibition of proliferation of colon cancer cells by 5-aminosalicylic acid. Biochem Pharmacol. 2008;75:668-676.
6. Kennedy M, Wilson L, Szabo C, et al. 5-aminosalicylic acid inhibits iNOS transcription in human intestinal epithelial cells. Int J Mol Med. 1999;4: 437-443.
7. Subramanian S, Rhodes JM, Hart CA, et al. Characterization of epithelial IL-8 response to inflammatory bowel disease mucosal E. coli and its inhibition by mesalamine. Inflamm Bowel Dis. 2008;14:162-175.
8. Kaiser GC, Yan F, Polk DB. Mesalamine blocks tumor necrosis factor growth inhibition and nuclear factor kappaB activation in mouse colonocytes. Gastroenterology. 1999;116:602-609.
9. Stenson WF, Lobos E. Sulfasalazine inhibits the synthesis of chemotactic lipids by neutrophils. J Clin Invest. 1982;69:494-497.
10. Bantel H, Berg C, Vieth M, et al. Mesalazine inhibits activation of transcription factor NF-kappaB in inflamed mucosa of patients with ulcerative colitis. Am J Gastroenterol. 2000;95:3452-3457.
11. Egan LJ, Mays DC, Huntoon CJ, et al. Inhibition of interleukin-1- stimulated NF-kappaB RelA/p65 phosphorylation by mesalamine is accompanied by decreased transcriptional activity. J Biol Chem. 1999;274:26448-26453.
12. Kim YH, Kim MH, Kim BJ, et al. Inhibition of cell proliferation and invasion in a human colon cancer cell line by 5-aminosalicylic acid. Dig Liver Dis. 2009;41:328-337.
13. Nielsen OH, Munck LK. Drug insight: aminosalicylates for the treatment of IBD. Nat Clin Pract Gastroenterol Hepatol. 2007;4:160-170.
14. Rubin DT, LoSavio A, Yadron N, et al. Aminosalicylate therapy in the prevention of dysplasia and colorectal cancer in ulcerative colitis. Clin Gastroenterol Hepatol. 2006;4:1346-1350.
15. Velayos FS, Terdiman JP, Walsh JM. Effect of 5-aminosalicylate use on colorectal cancer and dysplasia risk: a systematic review and metaanalysis of observational studies. Am J Gastroenterol. 2005;100:1345-1353.
16. Ahnfelt-Ronne I, Nielsen OH, Christensen A, et al. Clinical evidence supporting the radical scavenger mechanism of 5-aminosalicylic acid. Gastroenterology. 1990;98:1162-1169.
17. Gionchetti P, Guarnieri C, Campieri M, et al. Scavenger effect of sulphasalazine (SASP), 5-aminosalicylic acid (5-ASA), and olsalazine (OAZ). Gut. 1990;31:730-731.
18. Luciani MG, Campregher C, Fortune JM, et al. 5-ASA affects cell cycle progression in colorectal cells by reversibly activating a replication checkpoint. Gastroenterology. 2007;132:221-235.
19. Brown WA, Farmer KC, Skinner SA, et al. 5-aminosalicyclic acid and olsalazine inhibit tumor growth in a rodent model of colorectal cancer. Dig Dis Sci. 2000;45:1578-1584.
20. Bus PJ, Nagtegaal ID, Verspaget HW, et al. Mesalazine-induced apoptosis of colorectal cancer: on the verge of a new chemopreventive era? Aliment Pharmacol Ther. 1999;13:1397-1402.
21. Parenti S, Ferrarini F, Zini R, et al. Mesalazine inhibits the beta-catenin signalling pathway acting through the up-regulation of mu-protocadherin gene in colo-rectal cancer cells. Aliment Pharmacol Ther. 2010;31:108-119.
22. Rousseaux C, Lefebvre B, Dubuquoy L, et al. Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator- activated receptor-gamma. J Exp Med. 2005;201:1205-1215.
23. Sarraf P, Mueller E, Jones D, et al. Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med. 1998;4:1046-1052.
24. Gupta RA, Sarraf P, Mueller E, et al. Peroxisome proliferator-activated receptor gamma-mediated differentiation: a mutation in colon cancer cells reveals divergent and cell type-specific mechanisms. J Biol Chem. 2003;278:22669-22677.
25. Gupta RA, Brockman JA, Sarraf P, et al. Target genes of peroxisome proliferator-activated receptor gamma in colorectal cancer cells. J Biol Chem. 2001;276:29681-29687.
26. Patel L, Pass I, Coxon P, et al. Tumor suppressor and anti-inflammatory actions of PPARgamma agonists are mediated via upregulation of PTEN. Curr Biol. 2001;11:764-768.
27. Yki-Jarvinen H. Thiazolidinediones. N Engl J Med. 2004;351:1106-1118.
28. Lewis JD, Lichtenstein GR, Deren JJ, et al. Rosiglitazone for active ulcerative colitis: a randomized placebo-controlled trial. Gastroenterology. 2008;134:688-695.
29. Liang HL, Ouyang Q. A clinical trial of combined use of rosiglitazone and 5- aminosalicylate for ulcerative colitis. World J Gastroenterol. 2008;14:114-119.
30. Burgermeister E, Seger R. MAPK kinases as nucleo-cytoplasmic shuttles for PPARgamma. Cell Cycle. 2007;6:1539-1548.
31. Sarraf P, Mueller E, Smith WM, et al. Loss-of-function mutations in PPAR gamma associated with human colon cancer. Mol Cell. 1999;3:799-804.
32. Fujisawa T, Nakajima A, Fujisawa N, et al. Peroxisome proliferator-activated receptor gamma (PPARgamma) suppresses colonic epithelial cell turnover and colon carcinogenesis through inhibition of the beta-catenin/T cell factor (TCF) pathway. J Pharmacol Sci. 2008;106:627-638.
33. Liu J, Wang H, Zuo Y, et al. Functional interaction between peroxisome proliferator-activated receptor gamma and beta-catenin. Mol Cell Biol. 2006;26:5827-5837.
34. Taketo MM. Wnt signaling and gastrointestinal tumorigenesis in mouse models. Oncogene. 2006;25:7522-7530.
35. Hurlstone A, Clevers H. T-cell factors: turn-ons and turn-offs. EMBO J. 2002;21:2303-2311.
36. He TC, Sparks AB, Rago C, et al. Identification of c-MYC as a target of the APC pathway. Science. 1998;281:1509-1512.
37. Barker N, van Es JH, Kuipers J, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 2007;449:1003-1007.
38. Crawford HC, Fingleton BM, Rudolph-Owen LA, et al. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene. 1999;18:2883-2891.
39. Brown JB, Lee G, Managlia E, et al. Mesalamine inhibits epithelial betacatenin activation in chronic ulcerative colitis. Gastroenterology. 2010; 138:595-605.
40. Stambolic V, Suzuki A, de la Pompa JL, et al. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell. 1998;95:29-39.
41. Vazquez F, Grossman SR, Takahashi Y, et al. Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J Biol Chem. 2001;276:48627-48630.
42. Lee S-R, Yang K-S, Kwon J, et al. Reversible inactivation of the tumor suppressor PTEN by H2O2. J Biol Chem. 2002;277:20336-20342.
43. Schwab M, Reynders V, Loitsch S, et al. PPARgamma is involved in mesalazine-mediated induction of apoptosis and inhibition of cell growth in colon cancer cells. Carcinogenesis. 2008;29:1407-1414.
44. Sutherland LR, Martin F, Greer S, et al. 5-Aminosalicylic acid enema in the treatment of distal ulcerative colitis, proctosigmoiditis, and proctitis. Gastroenterology. 1987;92:1894-1898.
45. Truelove SC, Richards WC. Biopsy studies in ulcerative colitis. Br Med J. 1956;1:1315-1318.
46. van de Wetering M, Sancho E, Verweij C, et al. The b-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell. 2002;111:241-250.
47. Girnun GD, Domann FE, Moore SA, et al. Identification of a functional peroxisome proliferator-activated receptor response element in the rat catalase promoter. Mol Endocrinol. 2002;16:2793-2801.
48. Sheng H, Shao J, Townsend CM Jr, et al. Phosphatidylinositol 3-kinase mediates proliferative signals in intestinal epithelial cells. Gut. 2003;52: 1472-1478.
49. Lee G, Goretsky T, Managlia E, et al. Phosphoinositide 3-kinase signaling mediates beta-catenin activation in intestinal epithelial stem and progenitor cells in colitis. Gastroenterology. 2010;139:869-881, 881.e1-e9.
50. Dahan S, Roda G, Pinn D, et al. Epithelial: lamina propria lymphocyte interactions promote epithelial cell differentiation. Gastroenterology. 2008;134:192-203.
51. Humphries A, Graham TA, McDonald SA. Stem cells and inflammation in the intestine. Recent Results Cancer Res. 2011;185:51-63.
52. Tsatmali M, Walcott EC, Crossin KL. Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors. Brain Res. 2005;1040:137-150.
53. Smith J, Ladi E, Mayer-Pröschel M, et al. Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc Natl Acad Sci. 2000;97:10032-10037.
54. Pearson DC, Jourd'heuil D, Meddings JB. The anti-oxidant properties of 5-aminosalicylic acid. Free Radic Biol Med. 1996;21:367-373.
55. Dubuquoy L, Rousseaux C, Thuru X, et al. PPARg as a new therapeutic target in inflammatory bowel diseases. Gut. 2006;55:1341-1349.
56. Burns KA, Vanden Heuvel JP. Modulation of PPAR activity via phosphorylation. Biochim Biophys Acta. 2007;1771:952-960.
57. Sandborn WJ, Hanauer SB. Systematic review: the pharmacokinetic profiles of oral mesalazine formulations and mesalazine pro-drugs used in the management of ulcerative colitis. Aliment Pharmacol Ther. 2003;17:29-42.
58. Barker N, Ridgway RA, van Es JH, et al. Crypt stem cells as the cells-oforigin of intestinal cancer. Nature. 2009;457:608-611.
59. Diehn M, Cho RW, Lobo NA, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009;458:780-783.
60. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105-111.