Dietary Selenium Deficiency Exacerbates DSS-Induced Epithelial Injury and AOM/DSS-Induced Tumorigenesis

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Barrett, Caitlyn W ^a   Singh, Kshipra ^a,c   Motley, Amy K ^a   Lintel, Mary K ^a   Matafonova, Elena ^a   Bradley, Amber M ^a   Ning, Wei ^a   Poindexter, Shenika V ^a   Parang, Bobak ^a   Reddy, Vishruth K ^a   Chaturvedi, Rupesh ^a,c   Fingleton, Barbara M ^a   Washington, Mary K ^a   Wilson, Keith T ^a,b,c   Davies, Sean S ^a   Hill, Kristina E ^a   Burk, Raymond F ^a   Williams, Christopher S ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

AZOXYMETHANE; DEXTRAN SULFATE; EPIDERMAL GROWTH FACTOR; SELENIUM; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CANCER SIZE; CARCINOGENESIS; COLITIS; COLON INJURY; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DNA DAMAGE; EPIDERMAL GROWTH FACTOR GENE; EPITHELIUM DYSPLASIA; FECES ANALYSIS; GENE EXPRESSION; MORBIDITY; MOUSE; NONHUMAN; SELENIUM DEFICIENCY; TRANSFORMING GROWTH FACTOR BETA GENE; WEIGHT REDUCTION;

ANIMALS; AZOXYMETHANE; CARCINOGENESIS; COLITIS; COLONIC NEOPLASMS; DEOXYGUANOSINE; DEXTRAN SULFATE; DIET; DNA DAMAGE; EPIDERMAL GROWTH FACTOR; GENE EXPRESSION REGULATION; INFLAMMATION; MICE; MICE, INBRED C57BL; SELENIUM; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; WEIGHT LOSS;

MUS;

EID: 84879835232     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067845     Document Type: Article

References (79)

1. Rayman MP, (2000) The importance of selenium to human health. Lancet 356: 233-241 doi:--10.1016/S0140-6736(00)02490-9.
2. Kuroki F, Matsumoto T, Iida M, (2003) Selenium is depleted in Crohn's disease on enteral nutrition. Dig Dis 21: 266-270 doi:10.1159/000073346.
3. Hoffenberg EJ, Deutsch J, Smith S, Sokol RJ, (1997) Circulating antioxidant concentrations in children with inflammatory bowel disease. Am J Clin Nutr 65: 1482-1488.
4. Rannem T, Ladefoged K, Hylander E, Hegnhøj J, Jarnum S, (1992) Selenium status in patients with Crohn's disease. Am J Clin Nutr 56: 933-937.
5. Reimund JM, Hirth C, Koehl C, Baumann R, Duclos B, (2000) Antioxidant and immune status in active Crohn's disease. A possible relationship. Clin Nutr 19: 43-48 doi:10.1054/clnu.1999.0073.
6. Andoh A, Hirashima M, Maeda H, Hata K, Inatomi O, et al. (2005) Serum selenoprotein-P levels in patients with inflammatory bowel disease. Nutrition (Burbank, Los Angeles County, Calif) 21: 574-579 doi:10.1016/j.nut.2004.08.025.
7. Loftus EV, (2004) Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology 126: 1504-1517.
8. Kirsner JB, (1979) The local and systemic complications of inflammatory bowel disease. JAMA 242: 1177-1183.
9. Kirsner JB, (1991) Inflammatory bowel disease. Part II: Clinical and therapeutic aspects. Dis Mon 37: 669-746.
10. Kirsner JB, (1991) Inflammatory bowel disease. Part I: Nature and pathogenesis. Dis Mon 37: 605-666.
11. Vatn MH, (2009) Natural history and complications of IBD. Curr Gastroenterol Rep 11: 481-487.
12. Ringstad J, Kildebo S, Thomassen Y, (1993) Serum selenium, copper, and zinc concentrations in Crohn's disease and ulcerative colitis. Scand J Gastroenterol 28: 605-608 doi:10.3109/00365529309096096.
13. Han PD, Burke A, Baldassano RN, Rombeau JL, Lichtenstein GR (1999) Nutrition and inflammatory bowel disease. Gastroenterol Clin North Am 28: 423-43.
14. Sturniolo GC, Mestriner C, Lecis PE, D'Odorico A, Venturi C, et al. (1998) Altered plasma and mucosal concentrations of trace elements and antioxidants in active ulcerative colitis. Scand J Gastroenterol 33: 644-649.
15. Ojuawo A, Keith L, (2002) The serum concentrations of zinc, copper and selenium in children with inflammatory bowel disease. Cent Afr J Med 48: 116-119.
16. Mannick EE, Bonomolo JC, Horswell R, Lentz JJ, Serrano M-S, et al. (2004) Gene expression in mononuclear cells from patients with inflammatory bowel disease. Clin Immunol 112: 247-257 doi:10.1016/j.clim.2004.03.014.
17. Denson LA, Long MD, McGovern DPB, Kugathasan S, Wu GD, et al. (2013) Challenges in IBD Research: Update on Progress and Prioritization of the CCFA's Research Agenda. Inflamm Bowel Dis: -. doi:10.1097/MIB.0b013e31828134b3.
18. Kipp A, Banning A, van Schothorst EM, Mã Plan C, Schomburg L, et al. (2009) Four selenoproteins, protein biosynthesis, and Wnt signalling are particularly sensitive to limited selenium intake in mouse colon. Mol Nutr Food Res 53: 1561-1572 doi:10.1002/mnfr.200900105.
19. Yin F, Sancheti H, Cadenas E, (2012) Mitochondrial thiols in the regulation of cell death pathways. Antioxid Redox Signal 17: 1714-1727 doi:10.1089/ars.2012.4639.
20. Schrauzer GN, (1977) Trace elements, nutrition and cancer: perspectives of prevention. Adv Exp Med Biol 91: 323-344.
21. Combs GF, Gray WP, (1998) Chemopreventive agents: selenium. Pharmacol Ther 79: 179-192.
22. Jaworska K, Gupta S, Durda K, Muszyńska M, Sukiennicki G, et al. (2013) A low selenium level is associated with lung and laryngeal cancers. PLoS ONE 8: e59051 doi:10.1371/journal.pone.0059051.
23. Clark LC, Cantor KP, Allaway WH, (1991) Selenium in forage crops and cancer mortality in U.S. counties. Arch Environ Health 46: 37-42 doi:10.1080/00039896.1991.9937427.
24. Steinbrenner H, Speckmann B, Sies H (2013) Toward Understanding Success and Failures in the Use of Selenium for Cancer Prevention. Antioxid Redox Signal. doi:10.1089/ars.2013.5246.
25. Irons RR, Carlson BAB, Hatfield DLD, Davis CDC, (2006) Both selenoproteins and low molecular weight selenocompounds reduce colon cancer risk in mice with genetically impaired selenoprotein expression. J Nutr 136: 1311-1317.
26. Al-Taie OH, Uceyler N, Eubner U, Jakob F, Mörk H, et al. (2004) Expression profiling and genetic alterations of the selenoproteins GI-GPx and SePP in colorectal carcinogenesis. Nutr Cancer 48: 6-14 doi:_10.1207/s15327914nc4801_2.
27. Florian S, Wingler K, Schmehl K, Jacobasch G, Kreuzer OJ, et al. (2001) Cellular and subcellular localization of gastrointestinal glutathione peroxidase in normal and malignant human intestinal tissue. Free Radic Res 35: 655-663.
28. Mörk H, al-Taie OH, Bähr K, Zierer A, Beck C, et al. (2000) Inverse mRNA expression of the selenocysteine-containing proteins GI-GPx and SeP in colorectal adenomas compared with adjacent normal mucosa. Nutr Cancer 37: 108-116.
29. Lin Y-M, Furukawa Y, Tsunoda T, Yue C-T, Yang K-C, et al. (2002) Molecular diagnosis of colorectal tumors by expression profiles of 50 genes expressed differentially in adenomas and carcinomas. Oncogene 21: 4120-4128 doi:10.1038/sj.onc.1205518.
30. Chu F-F, Esworthy RS, Chu PG, Longmate JA, Huycke MM, et al. (2004) Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res 64: 962-968.
31. Krehl S, Loewinger M, Florian S, Kipp AP, Banning A, et al. (2012) 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 33: 620-628 doi:10.1093/carcin/bgr288.
32. Murawaki Y, Tsuchiya H, Kanbe T, Harada K, Yashima K, et al. (2008) Aberrant expression of selenoproteins in the progression of colorectal cancer. Cancer Lett 259: 218-230 doi:10.1016/j.canlet.2007.10.019.
33. Barrett CW, Ning W, Chen X, Smith JJ, Washington MK, et al. (2013) Tumor suppressor function of the plasma glutathione peroxidase gpx3 in colitis-associated carcinoma. Cancer Research 73: 1245-1255 doi:--10.1158/0008-5472.CAN-12-3150.
34. Dincer Y, Erzin Y, Himmetoglu S, Gunes KN, Bal K, et al. (2007) Oxidative DNA damage and antioxidant activity in patients with inflammatory bowel disease. Dig Dis Sci 52: 1636-1641 doi:---10.1007/s10620-006-9386-8.
35. Ekbom A, Helmick C, Zack M, Adami HO, (1990) Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 323: 1228-1233.
36. Hill KE, Zhou J, McMahan WJ, Motley AK, Burk RF, (2004) Neurological dysfunction occurs in mice with targeted deletion of the selenoprotein P gene. J Nutr 134: 157-161.
37. Greten FR, Eckmann L, Greten TF, Park JM, Li Z-W, et al. (2004) IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118: 285-296 doi:10.1016/j.cell.2004.07.013.
38. Barrett CW, Fingleton B, Williams A, Ning W, Fischer MA, et al. (2011) MTGR1 Is Required for Tumorigenesis in the Murine AOM/DSS Colitis-Associated Carcinoma Model. Cancer Res 71: 1302-1312 doi:--10.1158/0008-5472.CAN-10-3317.
39. Becker C, Fantini MC, Wirtz S, Nikolaev A, Kiesslich R, et al. (2005) In vivo imaging of colitis and colon cancer development in mice using high resolution chromoendoscopy. Gut 54: 950-954 doi:10.1136/gut.2004.061283.
40. Washington MK, Powell AE, Sullivan R, Sundberg J (2013) Pathology of Rodent Models of Intestinal Cancer: Progress Report and Recommendations. Gastroenterology.
41. Boivin GPG, Washington KK, Yang KK, Ward JMJ, Pretlow TPT, et al. (2003) Pathology of mouse models of intestinal cancer: consensus report and recommendations. Gastroenterology 124: 762-777 doi:10.1053/gast.2003.50094.
42. Koh TS, Benson TH, (1983) Critical re-appraisal of fluorometric method for determination of selenium in biological materials. J Assoc Off Anal Chem 66: 918-926.
43. Sheehan TM, Gao M, (1990) Simplified fluorometric assay of total selenium in plasma and urine. Clin Chem 36: 2124-2126.
44. Lawrence RA, Burk RF, (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71: 952-958.
45. Paglia DE, Valentine WN, (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70: 158-169.
46. Milne GL, Sanchez SC, Musiek ES, Morrow JD, (2007) Quantification of F2-isoprostanes as a biomarker of oxidative stress. Nat Protoc 2: 221-226 doi:10.1038/nprot.2006.375.
47. Koller FL, Dozier EA, Nam KT, Swee M, Birkland TP, et al. (2012) Lack of MMP10 exacerbates experimental colitis and promotes development of inflammation-associated colonic dysplasia. Lab Invest 92: 1749-1759 doi:10.1038/labinvest.2012.141.
48. Gentschew L, Bishop KS, Han DY, Morgan AR, Fraser AG, et al. (2012) Selenium, Selenoprotein Genes and Crohn's Disease in a Case-Control Population from Auckland, New Zealand. Nutrients 2012, Vol 4, Pages 1247-1259 4: 1247-1259 doi:10.3390/nu4091247.
49. Circu ML, Aw TY, (2012) Intestinal redox biology and oxidative stress. Semin Cell Dev Biol 23: 729-737 doi:10.1016/j.semcdb.2012.03.014.
50. Burk RF, Hill KE, Nakayama A, Mostert V, Levander XA, et al. (2008) Selenium deficiency activates mouse liver Nrf2-ARE but vitamin E deficiency does not. Free Radic Biol Med 44: 1617-1623 doi:10.1016/j.freeradbiomed.2008.01.016.
51. Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, et al. (2003) PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13: 2129-2141 doi:10.1101/gr.772403.
52. Beckett GJ, Arthur JR, (2005) Selenium and endocrine systems. J Endocrinol 184: 455-465 doi:10.1677/joe.1.05971.
53. Seril DN, Liao J, Yang G-Y, Yang CS, (2003) Oxidative stress and ulcerative colitis-associated carcinogenesis: studies in humans and animal models. Carcinogenesis 24: 353-362.
54. Kadiiska MB, Gladen BC, Baird DD, Germolec D, Graham LB, et al. (2005) Biomarkers of oxidative stress study II: are oxidation products of lipids, proteins, and DNA markers of CCl4 poisoning? Free Radic Biol Med 38: 698-710 doi:10.1016/j.freeradbiomed.2004.09.017.
55. Bera S, De Rosa V, Rachidi W, Diamond AM, (2013) Does a role for selenium in DNA damage repair explain apparent controversies in its use in chemoprevention? Mutagenesis 28: 127-134 doi:10.1093/mutage/ges064.
56. Ferguson LR, Karunasinghe N, Zhu S, Wang AH, (2012) Selenium and its' role in the maintenance of genomic stability. Mutat Res 733: 100-110 doi:10.1016/j.mrfmmm.2011.12.011.
57. Pegg AE, (1984) 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.
58. Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, et al. (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98: 694-702.
59. Okayasu I, Ohkusa T, Kajiura K, Kanno J, Sakamoto S, (1996) Promotion of colorectal neoplasia in experimental murine ulcerative colitis. Gut 39: 87-92.
60. Kipp AP, Müller MF, Göken EM, Deubel S, Brigelius-Flohé R, (2012) The selenoproteins GPx2, TrxR2 and TrxR3 are regulated by Wnt signalling in the intestinal epithelium. Biochim Biophys Acta 1820: 1588-1596 doi:10.1016/j.bbagen.2012.05.016.
61. Hong MY, Turner ND, Carroll RJ, Chapkin RS, Lupton JR, (2005) Differential response to DNA damage may explain different cancer susceptibility between small and large intestine. Exp Biol Med (Maywood) 230: 464-471.
62. Huang Z, Rose AH, Hoffmann PR, (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16: 705-743 doi:10.1089/ars.2011.4145.
63. Stranges S, Marshall JR, Natarajan R, Donahue RP, Trevisan M, et al. (2007) Effects of long-term selenium supplementation on the incidence of type 2 diabetes: a randomized trial. Ann Intern Med 147: 217-223.
64. Chang SH, Reynolds JM, Pappu BP, Chen G, Martinez GJ, et al. (2011) Interleukin-17C promotes Th17 cell responses and autoimmune disease via interleukin-17 receptor E. Immunity. 35: 611-621 doi:10.1016/j.immuni.2011.09.010.
65. Neurath MF, (2007) IL-23: a master regulator in Crohn disease. Nat Med 13: 26-28 doi:-10.1038/nm0107-26.
66. Damiani CR, Benetton CAF, Stoffel C, Bardini KC, Cardoso VH, et al. (2007) Oxidative stress and metabolism in animal model of colitis induced by dextran sulfate sodium. J Gastroenterol Hepatol 22: 1846-1851 doi:-10.1111/j.1440-1746.2007.04890.x.
67. Trivedi PP, Jena GB, (2013) Ulcerative colitis-induced hepatic damage in mice: studies on inflammation, fibrosis, oxidative DNA damage and GST-P expression. Chem Biol Interact 201: 19-30 doi:10.1016/j.cbi.2012.12.004.
68. Stucchi AF, Shofer S, Leeman S, Materne O, Beer E, et al. (2000) NK-1 antagonist reduces colonic inflammation and oxidative stress in dextran sulfate-induced colitis in rats. Am J Physiol Gastrointest Liver Physiol 279: G1298-G1306.
69. Carrier J, Aghdassi E, Cullen J, Allard JP, (2002) Iron supplementation increases disease activity and vitamin E ameliorates the effect in rats with dextran sulfate sodium-induced colitis. J Nutr 132: 3146-3150.
70. Ying Y, Liu XM, Marble A, Lawson KA, Zhao GQ, (2000) Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol 14: 1053-1063.
71. Frierson HF, El-Naggar AK, Welsh JB, Sapinoso LM, Su AI, et al. (2002) Large scale molecular analysis identifies genes with altered expression in salivary adenoid cystic carcinoma. Am J Pathol 161: 1315-1323 doi:--10.1016/S0002-9440(10)64408-2.
72. Langenskiöld M, Holmdahl L, Falk P, Angenete E, Ivarsson M-L, (2008) Increased TGF-beta 1 protein expression in patients with advanced colorectal cancer. J Surg Oncol 97: 409-415 doi:10.1002/jso.20961.
73. Saltzman BS, Yamamoto JF, Decker R, Yokochi L, Theriault AG, et al. (2008) Association of genetic variation in the transforming growth factor beta-1 gene with serum levels and risk of colorectal neoplasia. Cancer Research 68: 1236-1244 doi:--10.1158/0008-5472.CAN-07-2144.
74. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, et al. (2004) ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6: 1-6.
75. Skrzypczak M, Goryca K, Rubel T, Paziewska A, Mikula M, et al. (2010) Modeling oncogenic signaling in colon tumors by multidirectional analyses of microarray data directed for maximization of analytical reliability. PLoS ONE 5: -. doi:10.1371/journal.pone.0013091.
76. Modjtahedi H, Dean C, (1994) The receptor for EGF and its ligands- expression, prognostic value and target for therapy in cancer (review). Int J Oncol 4: 277-296.
77. Pasquale EB, (2010) Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nature Reviews Cancer 10: 165-180 doi:10.1038/nrc2806.
78. Cho M, Kim J-H, Hue J-J, Kang BS, Park H, et al. (2010) Effect of Dietary Selenium on the Colon Carcinogenesis in Male ICR Mice. Journal of Food Hygiene Safety 25: 269-277.
79. Hill KE, Zhou J, McMahan WJ, Motley AK, Atkins JF, et al. (2003) Deletion of selenoprotein P alters distribution of selenium in the mouse. J Biol Chem 278: 13640-13646 doi:10.1074/jbc.M300755200.