Selenoproteins and oxidative stress-induced inflammatory tumorigenesis in the gut

Cellular and Molecular Life Sciences

Volumn 74, Issue 4, 2017, Pages 607-616

  Barrett, Caitlyn W ^d   Short, Sarah P ^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 MEDICAL CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Antioxidant; Enteroids; Glutathione peroxidase; Inflammation; Interferon ; Selenoprotein P; Stem cells

Indexed keywords

EPIDERMAL GROWTH FACTOR; GAMMA INTERFERON; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE PEROXIDASE 3; INTERLEUKIN 13; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SELENIUM; SELENOPROTEIN; TRANSFORMING GROWTH FACTOR BETA; SELENOPROTEIN P; SEPP1 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ANTIOXIDANT ACTIVITY; CANCER RISK; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; COLITIS; COLORECTAL CANCER; DIET SUPPLEMENTATION; GENE MUTATION; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN MOTIF; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SELENIUM DEFICIENCY; VITAMIN SUPPLEMENTATION; ANIMAL; COLON; COLONIC NEOPLASMS; COMPLICATION; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ANIMALS; CARCINOGENESIS; COLITIS; COLON; COLONIC NEOPLASMS; GLUTATHIONE PEROXIDASE; HUMANS; INFLAMMATORY BOWEL DISEASES; OXIDATIVE STRESS; SELENIUM; SELENOPROTEIN P; SELENOPROTEINS;

EID: 84983380062     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-016-2339-2     Document Type: Review

References (94)

1. Kaplan GG (2015) The global burden of IBD: from 2015 to 2025. Nat Rev Gastroenterol Hepatol 12:720–727
2. Podolsky DK (1991) Inflammatory bowel disease (1). N Engl J Med 325:928–937
3. Abraham C, Cho JH (2009) Inflammatory bowel disease. N Engl J Med 361:2066–2078
4. Roessner A, Kuester D, Malfertheiner P, Schneider-Stock R (2008) Oxidative stress in ulcerative colitis-associated carcinogenesis. Pathol Res Pract 204:511–524
5. Itzkowitz SH, Yio X (2004) Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 287:G7–17
6. Emsley J (2011) Nature’s building blocks: an A–Z guide to the elements. Oxford University Press, Oxford
7. Stadtman TC (2000) Selenium biochemistry. Mammalian selenoenzymes. Ann N Y Acad Sci 899:399–402
8. Stadtman TC (1996) Selenocysteine. Annu Rev Biochem 65:83–100
9. Labunskyy VM, Yoo MH, Hatfield DL, Gladyshev VN (2009) Sep15, a thioredoxin-like selenoprotein, is involved in the unfolded protein response and differentially regulated by adaptive and acute ER stresses. Biochemistry 48:8458–8465
10. Ye Y, Shibata Y, Yun C, Ron D, Rapoport TA (2004) A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature 429:841–847
11. Kaya A, Lee BC, Gladyshev VN (2015) Regulation of protein function by reversible methionine oxidation and the role of selenoprotein MsrB1. Antioxid Redox Signal 23:814–822
12. Burk RF, Hill KE (1993) Regulation of selenoproteins. Annu Rev Nutr 13:65–81
13. Hoffmann PR, Berry MJ (2005) Selenoprotein synthesis: a unique translational mechanism used by a diverse family of proteins. Thyroid 15:769–775
14. Turanov AA, Xu XM, Carlson BA, Yoo MH, Gladyshev VN, Hatfield DL (2011) Biosynthesis of selenocysteine, the 21st amino acid in the genetic code, and a novel pathway for cysteine biosynthesis. Adv Nutr 2:122–128
15. Schriever SC, Barnes KM, Evenson JK, Raines AM, Sunde RA (2009) Selenium requirements are higher for glutathione peroxidase-1 mRNA than gpx1 activity in rat testis. Exp Biol Med (Maywood) 234:513–521
16. Barnes KM, Evenson JK, Raines AM, Sunde RA (2009) Transcript analysis of the selenoproteome indicates that dietary selenium requirements of rats based on selenium-regulated selenoprotein mRNA levels are uniformly less than those based on glutathione peroxidase activity. J Nutr 139:199–206
17. Hatfield D, Lee BJ, Hampton L, Diamond AM (1991) Selenium induces changes in the selenocysteine tRNA[Ser]Sec population in mammalian cells. Nucleic Acids Res 19:939–943
18. Hatfield DL, Carlson BA, Xu XM, Mix H, Gladyshev VN (2006) Selenocysteine incorporation machinery and the role of selenoproteins in development and health. Prog Nucleic Acid Res Mol Biol 81:97–142
19. Schoenmakers E, Carlson B, Agostini M, Moran C, Rajanayagam O, Bochukova E, Tobe R, Peat R, Gevers E, Muntoni F, Guicheney P, Schoenmakers N, Farooqi S, Lyons G, Hatfield D, Chatterjee K (2016) Mutation in human selenocysteine transfer RNA selectively disrupts selenoprotein synthesis. J Clin Invest 126:992–996
20. Chen J (2012) An original discovery: selenium deficiency and Keshan disease (an endemic heart disease). Asia Pacific J Clin Nutr 21:320–326
21. Yao Y, Pei F, Kang P (2011) Selenium, iodine, and the relation with Kashin–Beck disease. Nutrition 27:1095–1100
22. Cheng YY, Qian PC (1990) The effect of selenium-fortified table salt in the prevention of Keshan disease on a population of 1.05 million. Biomed Environ Sci BES 3:422–428
23. Yang C, Niu C, Bodo M, Gabriel E, Notbohm H, Wolf E, Muller PK (1993) Fulvic acid supplementation and selenium deficiency disturb the structural integrity of mouse skeletal tissue. An animal model to study the molecular defects of Kashin–Beck disease. Biochem J 289(Pt 3):829–835
24. Moreno-Reyes R, Mathieu F, Boelaert M, Begaux F, Suetens C, Rivera MT, Neve J, Perlmutter N, Vanderpas J (2003) Selenium and iodine supplementation of rural Tibetan children affected by Kashin–Beck osteoarthropathy. Am J Clin Nutr 78:137–144
25. Schoenmakers E, Agostini M, Mitchell C, Schoenmakers N, Papp L, Rajanayagam O, Padidela R, Ceron-Gutierrez L, Doffinger R, Prevosto C, Luan J, Montano S, Lu J, Castanet M, Clemons N, Groeneveld M, Castets P, Karbaschi M, Aitken S, Dixon A, Williams J, Campi I, Blount M, Burton H, Muntoni F, O’Donovan D, Dean A, Warren A, Brierley C, Baguley D, Guicheney P, Fitzgerald R, Coles A, Gaston H, Todd P, Holmgren A, Khanna KK, Cooke M, Semple R, Halsall D, Wareham N, Schwabe J, Grasso L, Beck-Peccoz P, Ogunko A, Dattani M, Gurnell M, Chatterjee K (2010) Mutations in the selenocysteine insertion sequence-binding protein 2 gene lead to a multisystem selenoprotein deficiency disorder in humans. J Clin Invest 120:4220–4235
26. Ashrafi MR, Shams S, Nouri M, Mohseni M, Shabanian R, Yekaninejad MS, Chegini N, Khodadad A, Safaralizadeh R (2007) A probable causative factor for an old problem: selenium and glutathione peroxidase appear to play important roles in epilepsy pathogenesis. Epilepsia 48:1750–1755
27. Zhang S, Rocourt C, Cheng WH (2010) Selenoproteins and the aging brain. Mech Ageing Dev 131:253–260
28. Baum MK, Shor-Posner G, Lai S, Zhang G, Lai H, Fletcher MA, Sauberlich H, Page JB (1997) High risk of HIV-related mortality is associated with selenium deficiency. J Acquir Immune Defic Syndr Hum Retrovirol Off Publ Int Retrovirol Assoc 15:370–374
29. Daoud AH, Griffin AC (1980) Effect of retinoic acid, butylated hydroxytoluene, selenium and sorbic acid on azo-dye hepatocarcinogenesis. Cancer Lett 9:299–304
30. van Rensburg SJ, Hall JM, Gathercole PS (1986) Inhibition of esophageal carcinogenesis in corn-fed rats by riboflavin, nicotinic acid, selenium, molybdenum, zinc, and magnesium. Nutr Cancer 8:163–170
31. Woutersen RA, Appel MJ, Van Garderen-Hoetmer A (1999) Modulation of pancreatic carcinogenesis by antioxidants. Food Chem Toxicol 37:981–984
32. Wang L, Bonorden MJ, Li GX, Lee HJ, Hu H, Zhang Y, Liao JD, Cleary MP, Lu J (2009) Methyl-selenium compounds inhibit prostate carcinogenesis in the transgenic adenocarcinoma of mouse prostate model with survival benefit. Cancer Prev Res (Phila) 2:484–495
33. Baines AT, Holubec H, Basye JL, Thorne P, Bhattacharyya AK, Spallholz J, Shriver B, Cui H, Roe D, Clark LC, Earnest DL, Nelson MA (2000) The effects of dietary selenomethionine on polyamines and azoxymethane-induced aberrant crypts. Cancer Lett 160:193–198
34. Ip C, Thompson HJ, Ganther HE (2000) Selenium modulation of cell proliferation and cell cycle biomarkers in normal and premalignant cells of the rat mammary gland. Cancer Epidemiol Biomark Prev 9:49–54
35. Clark LC, Dalkin B, Krongrad A, Combs GF Jr, Turnbull BW, Slate EH, Witherington R, Herlong JH, Janosko E, Carpenter D, Borosso C, Falk S, Rounder J (1998) Decreased incidence of prostate cancer with selenium supplementation: results of a double-blind cancer prevention trial. Br J Urol 81:730–734
36. Duffield-Lillico AJ, Dalkin BL, Reid ME, Turnbull BW, Slate EH, Jacobs ET, Marshall JR, Clark LC (2003) Selenium supplementation, baseline plasma selenium status and incidence of prostate cancer: an analysis of the complete treatment period of the Nutritional Prevention of Cancer Trial. BJU Int 91:608–612
37. Jacobs ET, Jiang R, Alberts DS, Greenberg ER, Gunter EW, Karagas MR, Lanza E, Ratnasinghe L, Reid ME, Schatzkin A, Smith-Warner SA, Wallace K, Martinez ME (2004) Selenium and colorectal adenoma: results of a pooled analysis. J Natl Cancer Inst 96:1669–1675
38. Klein EA, Thompson IM Jr, Tangen CM, Crowley JJ, Lucia MS, Goodman PJ, Minasian LM, Ford LG, Parnes HL, Gaziano JM, Karp DD, Lieber MM, Walther PJ, Klotz L, Parsons JK, Chin JL, Darke AK, Lippman SM, Goodman GE, Meyskens FL Jr, Baker LH (2011) Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 306:1549–1556
39. Wallace K, Byers T, Morris JS, Cole BF, Greenberg ER, Baron JA, Gudino A, Spate V, Karagas MR (2003) Prediagnostic serum selenium concentration and the risk of recurrent colorectal adenoma: a nested case-control study. Cancer Epidemiol Biomark Prev 12:464–467
40. Papaioannou D, Cooper KL, Carroll C, Hind D, Squires H, Tappenden P, Logan RF (2011) Antioxidants in the chemoprevention of colorectal cancer and colorectal adenomas in the general population: a systematic review and meta-analysis. Colorectal Dis 13:1085–1099
41. Geerling BJ, Badart-Smook A, Stockbrugger RW, Brummer RJ (1998) Comprehensive nutritional status in patients with long-standing Crohn disease currently in remission. Am J Clin Nutr 67:919–926
42. Hinks LJ, Inwards KD, Lloyd B, Clayton B (1988) Reduced concentrations of selenium in mild Crohn’s disease. J Clin Pathol 41:198–201
43. Kuroki F, Matsumoto T, Iida M (2003) Selenium is depleted in Crohn’s disease on enteral nutrition. Dig Dis 21:266–270
44. Loeschke K, Konig A, Trebert Haeberlin S, Lux F (1987) Low blood selenium concentration in Crohn disease. Ann Intern Med 106:908
45. Penny WJ, Mayberry JF, Aggett PJ, Gilbert JO, Newcombe RG, Rhodes J (1983) Relationship between trace elements, sugar consumption, and taste in Crohn’s disease. Gut 24:288–292
46. Rannem T, Ladefoged K, Hylander E, Hegnhoj J, Jarnum S (1992) Selenium status in patients with Crohn’s disease. Am J Clin Nutr 56:933–937
47. 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
48. Barrett CW, Singh K, Motley AK, Lintel MK, Matafonova E, Bradley AM, Ning W, Poindexter SV, Parang B, Reddy VK, Chaturvedi R, Fingleton BM, Washington MK, Wilson KT, Davies SS, Hill KE, Burk RF, Williams CS (2013) Dietary selenium deficiency exacerbates DSS-induced epithelial injury and AOM/DSS-induced tumorigenesis. PLoS One 8:e67845
49. Moustafa ME, Carlson BA, El-Saadani MA, Kryukov GV, Sun QA, Harney JW, Hill KE, Combs GF, Feigenbaum L, Mansur DB, Burk RF, Berry MJ, Diamond AM, Lee BJ, Gladyshev VN, Hatfield DL (2001) Selective inhibition of selenocysteine tRNA maturation and selenoprotein synthesis in transgenic mice expressing isopentenyladenosine-deficient selenocysteine tRNA. Mol Cell Biol 21:3840–3852
50. Irons R, Carlson BA, Hatfield DL, Davis CD (2006) Both selenoproteins and low molecular weight selenocompounds reduce colon cancer risk in mice with genetically impaired selenoprotein expression. J Nutr 136:1311–1317
51. Diwadkar-Navsariwala V, Prins GS, Swanson SM, Birch LA, Ray VH, Hedayat S, Lantvit DL, Diamond AM (2006) Selenoprotein deficiency accelerates prostate carcinogenesis in a transgenic model. Proc Natl Acad Sci USA 103:8179–8184
52. Moustafa ME, Carlson BA, Anver MR, Bobe G, Zhong N, Ward JM, Perella CM, Hoffmann VJ, Rogers K, Combs GF Jr, Schweizer U, Merlino G, Gladyshev VN, Hatfield DL (2013) Selenium and selenoprotein deficiencies induce widespread pyogranuloma formation in mice, while high levels of dietary selenium decrease liver tumor size driven by TGFalpha. PLoS One 8:e57389
53. Bosl MR, Takaku K, Oshima M, Nishimura S, Taketo MM (1997) Early embryonic lethality caused by targeted disruption of the mouse selenocysteine tRNA gene (Trsp). Proc Natl Acad Sci USA 94:5531–5534
54. Kumaraswamy E, Carlson BA, Morgan F, Miyoshi K, Robinson GW, Su D, Wang S, Southon E, Tessarollo L, Lee BJ, Gladyshev VN, Hennighausen L, Hatfield DL (2003) Selective removal of the selenocysteine tRNA [Ser]Sec gene (Trsp) in mouse mammary epithelium. Mol Cell Biol 23:1477–1488
55. Shrimali RK, Weaver JA, Miller GF, Starost MF, Carlson BA, Novoselov SV, Kumaraswamy E, Gladyshev VN, Hatfield DL (2007) Selenoprotein expression is essential in endothelial cell development and cardiac muscle function. Neuromuscul Disord 17:135–142
56. Carlson BA, Xu XM, Gladyshev VN, Hatfield DL (2005) Selective rescue of selenoprotein expression in mice lacking a highly specialized methyl group in selenocysteine tRNA. J Biol Chem 280:5542–5548
57. Sengupta A, Lichti UF, Carlson BA, Ryscavage AO, Gladyshev VN, Yuspa SH, Hatfield DL (2010) Selenoproteins are essential for proper keratinocyte function and skin development. PLoS One 5:e12249
58. 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
59. Suzuki T, Kelly VP, Motohashi H, Nakajima O, Takahashi S, Nishimura S, Yamamoto M (2008) Deletion of the selenocysteine tRNA gene in macrophages and liver results in compensatory gene induction of cytoprotective enzymes by Nrf2. J Biol Chem 283:2021–2030
60. Kaushal N, Kudva AK, Patterson AD, Chiaro C, Kennett MJ, Desai D, Amin S, Carlson BA, Cantorna MT, Prabhu KS (2014) Crucial role of macrophage selenoproteins in experimental colitis. J Immunol 193:3683–3692
61. Tham DM, Whitin JC, Cohen HJ (2002) Increased expression of extracellular glutathione peroxidase in mice with dextran sodium sulfate-induced experimental colitis. Pediatr Res 51:641–646
62. Hiller F, Besselt K, Deubel S, Brigelius-Flohe R, Kipp AP (2015) GPx2 induction is mediated through STAT transcription factors during acute colitis. Inflamm Bowel Dis 21:2078–2089
63. 2? Eur J Gastroenterol Hepatol 20:555–560
64. Yant LJ, Ran Q, Rao L, Van Remmen H, Shibatani T, Belter JG, Motta L, Richardson A, Prolla TA (2003) The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic Biol Med 34:496–502
65. Esworthy RS, Aranda R, Martin MG, Doroshow JH, Binder SW, Chu FF (2001) Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol 281:G848–G855
66. Esworthy RS, Kim BW, Chow J, Shen B, Doroshow JH, Chu FF (2014) Nox1 causes ileocolitis in mice deficient in glutathione peroxidase-1 and -2. Free Radic Biol Med 68:315–325
67. Esworthy RS, Kim BW, Wang Y, Gao Q, Doroshow JH, Leto TL, Chu FF (2013) The Gdac1 locus modifies spontaneous and Salmonella-induced colitis in mice deficient in either Gpx2 or Gpx1 gene. Free Radic Biol Med 65:1273–1283
68. Barrett CW, Ning W, Chen X, Smith JJ, Washington MK, Hill KE, Coburn LA, Peek RM, Chaturvedi R, Wilson KT, Burk RF, Williams CS (2013) Tumor suppressor function of the plasma glutathione peroxidase gpx3 in colitis-associated carcinoma. Cancer Res 73:1245–1255
69. Krehl S, Loewinger M, Florian S, Kipp AP, Banning A, Wessjohann LA, Brauer MN, Iori R, Esworthy RS, Chu FF, Brigelius-Flohe R (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
70. Hill KE, Zhou J, Austin LM, Motley AK, Ham AJ, Olson GE, Atkins JF, Gesteland RF, Burk RF (2007) The selenium-rich C-terminal domain of mouse selenoprotein P is necessary for the supply of selenium to brain and testis but not for the maintenance of whole body selenium. J Biol Chem 282:10972–10980
71. Olson GE, Winfrey VP, Nagdas SK, Hill KE, Burk RF (2007) Apolipoprotein E receptor-2 (ApoER2) mediates selenium uptake from selenoprotein P by the mouse testis. J Biol Chem 282:12290–12297
72. Burk RF, Hill KE, Olson GE, Weeber EJ, Motley AK, Winfrey VP, Austin LM (2007) Deletion of apolipoprotein E receptor-2 in mice lowers brain selenium and causes severe neurological dysfunction and death when a low-selenium diet is fed. J Neurosci 27:6207–6211
73. Hill KE, Wu S, Motley AK, Stevenson TD, Winfrey VP, Capecchi MR, Atkins JF, Burk RF (2012) Production of selenoprotein P (Sepp1) by hepatocytes is central to selenium homeostasis. J Biol Chem 287:40414–40424
74. Saito Y, Hayashi T, Tanaka A, Watanabe Y, Suzuki M, Saito E, Takahashi K (1999) Selenoprotein P in human plasma as an extracellular phospholipid hydroperoxide glutathione peroxidase. Isolation and enzymatic characterization of human selenoprotein p. J Biol Chem 274:2866–2871
75. Kurokawa S, Eriksson S, Rose KL, Wu S, Motley AK, Hill S, Winfrey VP, McDonald WH, Capecchi MR, Atkins JF, Arner ES, Hill KE, Burk RF (2014) Sepp1(UF) forms are N-terminal selenoprotein P truncations that have peroxidase activity when coupled with thioredoxin reductase-1. Free Radic Biol Med 69:67–76
76. Al-Taie OH, Uceyler N, Eubner U, Jakob F, Mork H, Scheurlen M, Brigelius-Flohe R, Schottker K, Abel J, Thalheimer A, Katzenberger T, Illert B, Melcher R, Kohrle J (2004) Expression profiling and genetic alterations of the selenoproteins GI-GPx and SePP in colorectal carcinogenesis. Nutr Cancer 48:6–14
77. Calvo A, Xiao N, Kang J, Best CJ, Leiva I, Emmert-Buck MR, Jorcyk C, Green JE (2002) Alterations in gene expression profiles during prostate cancer progression: functional correlations to tumorigenicity and down-regulation of selenoprotein-P in mouse and human tumors. Cancer Res 62:5325–5335
78. Steinbrecher A, Meplan C, Hesketh J, Schomburg L, Endermann T, Jansen E, Akesson B, Rohrmann S, Linseisen J (2010) Effects of selenium status and polymorphisms in selenoprotein genes on prostate cancer risk in a prospective study of European men. Cancer Epidemiol Biomark Prev 19:2958–2968
79. Peters U, Chatterjee N, Hayes RB, Schoen RE, Wang Y, Chanock SJ, Foster CB (2008) Variation in the selenoenzyme genes and risk of advanced distal colorectal adenoma. Cancer Epidemiol Biomark Prev 17:1144–1154
80. Al-Taie OH, Seufert J, Mork H, Treis H, Mentrup B, Thalheimer A, Starostik P, Abel J, Scheurlen M, Kohrle J, Jakob F (2002) A complex DNA-repeat structure within the Selenoprotein P promoter contains a functionally relevant polymorphism and is genetically unstable under conditions of mismatch repair deficiency. Eur J Hum Genet 10:499–504
81. Smith JJ, Deane NG, Wu F, Merchant NB, Zhang B, Jiang A, Lu P, Johnson JC, Schmidt C, Bailey CE, Eschrich S, Kis C, Levy S, Washington MK, Heslin MJ, Coffey RJ, Yeatman TJ, Shyr Y, Beauchamp RD (2010) Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 138:958–968
82. Barrett CW, Reddy VK, Short SP, Motley AK, Lintel MK, Bradley AM, Freeman T, Vallance J, Ning W, Parang B, Poindexter SV, Fingleton B, Chen X, Washington MK, Wilson KT, Shroyer NF, Hill KE, Burk RF, Williams CS (2015) Selenoprotein P influences colitis-induced tumorigenesis by mediating stemness and oxidative damage. J Clin Invest 125:2646–2660
83. Solinas G, Schiarea S, Liguori M, Fabbri M, Pesce S, Zammataro L, Pasqualini F, Nebuloni M, Chiabrando C, Mantovani A, Allavena P (2010) Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J Immunol 185:642–652
84. Dreher I, Jakobs TC, Kohrle J (1997) Cloning and characterization of the human selenoprotein P promoter. Response of selenoprotein P expression to cytokines in liver cells. J Biol Chem 272:29364–29371
85. Mostert V, Dreher I, Kohrle J, Abel J (1999) Transforming growth factor-beta1 inhibits expression of selenoprotein P in cultured human liver cells. FEBS Lett 460:23–26
86. Sato T, Clevers H (2013) Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340:1190–1194
87. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469:415–418
88. Durand A, Donahue B, Peignon G, Letourneur F, Cagnard N, Slomianny C, Perret C, Shroyer NF, Romagnolo B (2012) Functional intestinal stem cells after Paneth cell ablation induced by the loss of transcription factor Math1 (Atoh1). Proc Natl Acad Sci USA 109:8965–8970
89. Farin HF, Van Es JH, Clevers H (2012) Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology 143(1518–1529):e1517
90. Clevers H (2004) Wnt breakers in colon cancer. Cancer Cell 5:5–6
91. Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, Ford LG, Parnes HL, Minasian LM, Gaziano JM, Hartline JA, Parsons JK, Bearden JD 3rd, Crawford ED, Goodman GE, Claudio J, Winquist E, Cook ED, Karp DD, Walther P, Lieber MM, Kristal AR, Darke AK, Arnold KB, Ganz PA, Santella RM, Albanes D, Taylor PR, Probstfield JL, Jagpal TJ, Crowley JJ, Meyskens FL Jr, Baker LH, Coltman CA Jr (2009) Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 301:39–51
92. 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
93. Andoh A, Hirashima M, Maeda H, Hata K, Inatomi O, Tsujikawa T, Sasaki M, Takahashi K, Fujiyama Y (2005) Serum selenoprotein-P levels in patients with inflammatory bowel disease. Nutrition 21:574–579
94. Cooper ML, Adami HO, Gronberg H, Wiklund F, Green FR, Rayman MP (2008) Interaction between single nucleotide polymorphisms in selenoprotein P and mitochondrial superoxide dismutase determines prostate cancer risk. Cancer Res 68:10171–10177