Tumor suppressor function of the plasma glutathione peroxidase Gpx3 in colitis-associated carcinoma

Cancer Research

Volumn 73, Issue 3, 2013, Pages 1245-1255

  Barrett, Caitlyn W ^a,b   Ning, Wei ^a,b   Chen, Xi ^c   Smith, Jesse Joshua ^d   Washington, Mary K ^b   Hill, Kristina E ^a   Coburn, Lori A ^a,f   Peek, Richard M ^a,b,e   Chaturvedi, Rupesh ^a,b   Wilson, Keith T ^a,b,e,f   Burk, Raymond F ^a   Williams, Christopher S ^a,b,d,e,f  

^a Division of Gastroenterology   (United States)

^b Department of Cancer Biology ^*  (United States)

^c Department of Medicine   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e VANDERBILT INGRAM CANCER CENTER   (United States)

^f Veterans Affairs Tennessee Valley Health Care System   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; DNA; GLUTATHIONE PEROXIDASE 3; PROTEIN M2; REACTIVE OXYGEN METABOLITE; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL INFILTRATION; CELL PROLIFERATION; COLITIS; COLON CARCINOMA; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; GENE LOSS; GENE SILENCING; GENETIC ANALYSIS; GENETIC ASSOCIATION; GLUTATHIONE PEROXIDASE 3 GENE; IN VITRO STUDY; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; ONCOGENE; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CACO-2 CELLS; COLITIS; COLONIC NEOPLASMS; DNA DAMAGE; GLUTATHIONE PEROXIDASE; HUMANS; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; TUMOR SUPPRESSOR PROTEINS;

EID: 84873466001     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3150     Document Type: Article

References (49)

1. Dincer Y, Erzin Y, Himmetoglu S, Gunes KN, Bal K, Akcay T. Oxidative DNA damage and antioxidant activity in patients with inflammatory bowel disease. Dig Dis Sci 2007;52:1636-41.
2. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-17.
3. Rachmilewitz D, Stamler JS, Bachwich D, Karmeli F, Ackerman Z, Podolsky DK. Enhanced colonic nitric oxide generation and nitric oxide synthase activity in ulcerative colitis and Crohn's disease. Gut 1995;36:718-23.
4. Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 1990;323: 1228-33.
5. Irons R, Carlson BA, Hatfield DL, Davis CD. Both selenoproteins and low molecular weight selenocompounds reduce colon cancer risk in mice with genetically impaired selenoprotein expression. J Nutr 2006;136:1311-7.
6. Hudson TS, Carlson BA, Hoeneroff MJ, Young HA, Sordillo L, Muller WJ, et al. Selenoproteins reduce susceptibility to DMBA-induced mammary carcinogenesis. Carcinogenesis 2012;33:1225-30.
7. Maiorino M, Aumann KD, Brigelius-Flohe R, Doria D, van den Heuvel J, McCarthy J, et al. Probing the presumed catalytic triad of seleniumcontaining peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol Chem Hoppe Seyler 1995;376:651-60.
8. Brigelius-Flohe R. Tissue-specific functions of individual glutathione peroxidases. Free Radic Biol Med 1999;27:951-65.
9. Olson GE, Whitin JC, Hill KE, Winfrey VP, Motley AK, Austin LM, et al. Extracellular glutathione peroxidase (Gpx3) binds specifically to basement membranes of mouse renal cortex tubule cells. Am J Physiol Renal Physiol 2010;298:F1244-53.
10. Maeda K, Okubo K, Shimomura I, Mizuno K, Matsuzawa Y, Matsubara K. Analysis of an expression profile of genes in the human adipose tissue. Gene 1997;190:227-35.
11. Chu FF, Esworthy RS, Doroshow JH, Doan K, Liu XF. Expression of plasma glutathione peroxidase in human liver in addition to kidney, heart, lung, and breast in humans and rodents. Blood 1992;79: 3233-8.
12. Tham DM, Whitin JC, Kim KK, Zhu SX, Cohen HJ. Expression of extracellular glutathione peroxidase in human and mouse gastrointestinal tract. Am J Physiol 1998;275(6 Pt 1):G1463-71.
13. Avissar N, Ornt DB, Yagil Y, Horowitz S, Watkins RH, Kerl EA, et al. Human kidney proximal tubules are the main source of plasma glutathione peroxidase. Am J Physiol 1994;266(2 Pt 1):C367-75.
14. Burk RF, Olson GE, Winfrey VP, Hill KE, Yin D. Glutathione peroxidase-3 produced by the kidney binds to a population of basement membranes in the gastrointestinal tract and in other tissues. Am J Physiol Gastrointest Liver Physiol 2011;301:G32-8.
15. Chen B, Rao X, House MG, Nephew KP, Cullen KJ, Guo Z. GPx3 promoter hypermethylation is a frequent event in human cancer and is associated with tumorigenesis and chemotherapy response. Cancer Lett 2011;309:37-45.
16. Zhang X, Yang JJ, Kim YS, Kim KY, Ahn WS, Yang S. An 8-gene signature, including methylated and down-regulated glutathione peroxidase 3, of gastric cancer. Int J Oncol 2010;36:405-14.
17. Yu YP, Yu G, Tseng G, Cieply K, Nelson J, Defrances M, et al. Glutathione peroxidase 3, deleted or methylated in prostate cancer, suppresses prostate cancer growth and metastasis. Cancer Res 2007;67:8043-50.
18. Murawaki Y, Tsuchiya H, Kanbe T, Harada K, Yashima K, Nozaka K, et al. Aberrant expression of selenoproteins in the progression of colorectal cancer. Cancer Lett 2008;259:218-30.
19. Esworthy RS, Aranda R, Martin MG, Doroshow JH, Binder SW, Chu FF. Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol 2001;281:G848-55.
20. Chu FF, Esworthy RS, Doroshow JH. Role of Se-dependent glutathione peroxidases in gastrointestinal inflammation and cancer. Free Radic Biol Med 2004;36:1481-95.
21. Krehl S, Loewinger M, Florian S, Kipp AP, Banning A, Wessjohann LA, et al. Glutathione peroxidase-2 and selenium decreased inflammation and tumors in a mouse model of inflammation-associated carcinogenesis whereas sulforaphane effects differed with selenium supply. Carcinogenesis 2012;33:620-8.
22. D'Odorico A, D'Inca R, Mestriner C, Di Leo V, Ferronato A, Sturniolo GC. Influence of disease site and activity on peripheral neutrophil function in inflammatory bowel disease. Dig Dis Sci 2000;45:1594-600.
23. Eaden J. Review article: colorectal carcinoma and inflammatory bowel disease. Aliment Pharmacol Ther 2004;20(Suppl 4):24-30.
24. Mayer R, Wong WD, Rothenberger DA, Goldberg SM, Madoff RD. Colorectal cancer in inflammatory bowel disease: a continuing problem. Dis Colon Rectum 1999;42:343-7.
25. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004;118:285-96.
26. Fukata M, Chen A, Vamadevan AS, Cohen J, Breglio K, Krishnareddy S, et al. Toll-like receptor-4 promotes the development of colitisassociated colorectal tumors. Gastroenterology 2007;133:1869-81.
27. Popivanova BK, Kitamura K, Wu Y, Kondo T, Kagaya T, Kaneko S, et al. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 2008;118:560-70.
28. Barrett CW, Fingleton B, Williams A, Ning W, Fischer MA, Washington MK, et al. MTGR1 is required for tumorigenesis in the murine AOM/DSS colitis-associated carcinoma model. Cancer Res 2011; 71:1302-12.
29. 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: 103-13.
30. Uronis JM, Muhlbauer M, Herfarth HH, Rubinas TC, Jones GS, Jobin C. Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility. PLoS ONE 2009;4:e6026.
31. Dieleman LA, Palmen MJ, Akol H, Bloemena E, Pena AS, Meuwissen SG, et al. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol 1998;114:385-91.
32. Becker C, Fantini MC, Neurath MF. High resolution colonoscopy in live mice. Nat Protoc 2006;1:2900-4.
33. Lawrence RA, Burk RF. Glutathione peroxidase activity in seleniumdeficient rat liver. Biochem Biophys Res Commun 1976;71:952-8.
34. Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158-69.
35. Chaturvedi R, Asim M, Romero-Gallo J, Barry DP, Hoge S, de Sablet T, et al. Spermine oxidase mediates the gastric cancer risk associated with Helicobacter pylori CagA. Gastroenterology 2011;141:1696-708 e1-2.
36. Becker C, Fantini MC, Wirtz S, Nikolaev A, Kiesslich R, Lehr HA, et al. In vivo imaging of colitis and colon cancer development in mice using high resolution chromoendoscopy. Gut 2005;54:950-4.
37. Kipp A, Banning A, van Schothorst EM, Meplan C, Schomburg L, Evelo C, et al. Four selenoproteins, protein biosynthesis, and Wnt signalling are particularly sensitive to limited selenium intake in mouse colon. Mol Nutr Food Res 2009;53:1561-72.
38. Tanaka T, Kohno H, Suzuki R, Yamada Y, Sugie S, Mori H. A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci 2003;94: 965-73.
39. Carlson BA, Yoo MH, Sano Y, Sengupta A, Kim JY, Irons R, et al. Selenoproteins regulate macrophage invasiveness and extracellular matrix-related gene expression. BMC Immunol 2009;10:57.
40. Yasui Y, Tanaka T. Protein expression analysis of inflammation-related colon carcinogenesis. J Carcinog 2009;8:10.
41. Bartsch H, Nair J. Potential role of lipid peroxidation derived DNA damage in human colon carcinogenesis: studies on exocyclic base adducts as stable oxidative stress markers. Cancer Detect Prev 2002;26:308-12.
42. Fridovich I. Fundamental aspects of reactive oxygen species, or what's the matter with oxygen? Ann N Y Acad Sci 1999;893:13-8.
43. Muscoli C, Cuzzocrea S, Riley DP, Zweier JL, Thiemermann C, Wang ZQ, et al. On the selectivity of superoxide dismutase mimetics and its importance in pharmacological studies. Br J Pharmacol 2003;140: 445-60.
44. Dix TA, Hess KM, Medina MA, Sullivan RW, Tilly SL, Webb TL. Mechanism of site-selective DNA nicking by the hydrodioxyl (perhydroxyl) radical. Biochemistry 1996;35:4578-83.
45. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J Biol Chem 1992;267:166-72.
46. Hussain SP, Harris CC. Molecular epidemiology of human cancer: contribution of mutation spectra studies of tumor suppressor genes. Cancer Res 1998;58:4023-37.
47. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007;117:1155-66.
48. Kiremidjian-Schumacher L, Roy M, Wishe HI, Cohen MW, Stotzky G. Regulation of cellular immune responses by selenium. Biol Trace Elem Res 1992;33:23-35.
49. Kiremidjian-Schumacher L, Roy M, Wishe HI, Cohen MW, Stotzky G. Supplementation with selenium and human immune cell functions. II. Effect on cytotoxic lymphocytes and natural killer cells. Biol Trace Elem Res 1994;41:115-27.