A short-term intervention with selenium affects expression of genes implicated in the epithelial-to-mesenchymal transition in the prostate

Oncotarget

Volumn 8, Issue 6, 2017, Pages 10565-10579

  Kok, Dieuwertje E G ^a   Kiemeney, Lambertus A L M ^b   Verhaegh, Gerald W ^b   Schalken, Jack A ^b   van Lin, Emile N J T ^c   Sedelaar, J P Michiel ^b   Witjes, J Alfred ^b   Hulsbergen van de Kaa, Christina A ^b   van't Veer, Pieter ^a   Kampman, Ellen ^a,b   Afman, Lydia A ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Hochschule Bonn Rhein Sieg   (Germany)

Author keywords

EMT; Gene expression; Microarray; Prostatic neoplasms; Selenium

Indexed keywords

EPITHELIAL CELL ADHESION MOLECULE; FIBRONECTIN; PLACEBO; SELENIUM; UVOMORULIN; VIMENTIN; TRANSCRIPTOME;

AGED; ARTICLE; CANCER GROWTH; CELL INVASION; CELL MIGRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; EPITHELIAL MESENCHYMAL TRANSITION; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; INFLAMMATION; MALE; MICROARRAY ANALYSIS; NETHERLANDS; OUTCOME ASSESSMENT; PROSTATE; PROSTATE BIOPSY; RANDOMIZED CONTROLLED TRIAL; SHORT COURSE THERAPY; UPREGULATION; WOUND HEALING; DIETARY SUPPLEMENT; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; TIME FACTOR;

AGED; DIETARY SUPPLEMENTS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MALE; MIDDLE AGED; NETHERLANDS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROSTATE; SELENIUM; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTOME;

EID: 85011949100     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14551     Document Type: Article

References (62)

1. Clark LC, Combs GF, Jr., Turnbull BW, Slate EH, Chalker DK, Chow J, Davis LS, Glover RA, Graham GF, Gross EG, Krongrad A, Lesher JL, Jr., Park HK, Sanders BB, Jr., Smith CL, Taylor JR. Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial. Nutritional Prevention of Cancer Study Group. JAMA. 1996; 276:1957-1963.
2. Duffield-Lillico AJ, Dalkin BL, Reid ME, Turnbull BW, Slate EH, Jacobs ET, Marshall JR, Clark LC. 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. 2003; 91:608-612.
3. Lin DW, Coleman IM, Hawley S, Dumpit R, Gifford D, Kezele P, Hung H, Knudsen BS, Kristal AR, Nelson PS. Influence of surgical manipulation on prostate gene expression: implications for molecular correlates of treatment effects and disease prognosis. J Clin Oncol. 2006; 24:3763-3770.
4. Cai X, Wang C, Yu W, Fan W, Wang S, Shen N, Wu P, Li X, Wang F. Selenium Exposure and Cancer Risk: an Updated Meta-analysis and Meta-regression. Scientific reports. 2016; 6:19213.
5. Allen NE, Appleby PN, Roddam AW, Tjonneland A, Johnsen NF, Overvad K, Boeing H, Weikert S, Kaaks R, Linseisen J, Trichopoulou A, Misirli G, Trichopoulos D, Sacerdote C, Grioni S, Palli D, et al. Plasma selenium concentration and prostate cancer risk: results from the European Prospective Investigation into Cancer and Nutrition (EPIC). Am J Clin Nutr. 2008; 88:1567-1575.
6. Lippman SM, Klein EA, Goodman PJ, Lucia MS, Thompson IM, Ford LG, Parnes HL, Minasian LM, Gaziano JM, Hartline JA, Parsons JK, Bearden JD, Crawford ED, Goodman GE, Claudio J, Winquist E, et al. Effect of Selenium and Vitamin E on Risk of Prostate Cancer and Other Cancers. JAMA. 2009; 301:39-51.
7. Kristal AR, Darke AK, Morris JS, Tangen CM, Goodman PJ, Thompson IM, Meyskens FL, Goodman GE, Minasian LM, Parnes HL, Lippman SM, Klein EA. Baseline Selenium Status and Effects of Selenium and Vitamin E Supplementation on Prostate Cancer Risk. Journal of the National Cancer Institute. doi: 101093/jnci/djt456. 2014.
8. Algotar AM, Stratton MS, Ahmann FR, Ranger-Moore J, Nagle RB, Thompson PA, Slate E, Hsu CH, Dalkin BL, Sindhwani P, Holmes MA, Tuckey JA, Graham DL, Parnes HL, Clark LC, Stratton SP. Phase 3 clinical trial investigating the effect of selenium supplementation in men at high-risk for prostate cancer. Prostate. 2013; 73:328-335.
9. Klein EA, Thompson IM, 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, et al. Vitamin E and the Risk of Prostate Cancer. JAMA. 2011; 306:1549-1556.
10. Fairweather-Tait SJ, Bao Y, Broadley MR, Collings R, Ford D, Hesketh JE, Hurst R. Selenium in human health and disease. Antioxid Redox Signal. 2011; 14:1337-1383.
11. Lu J, Zhang J, Jiang C, Deng Y, Ozten N, Bosland MC. Cancer chemoprevention research with selenium in the post-SELECT era: Promises and challenges. Nutr Cancer. 2016; 68:1-17.
12. Hurst R, Collings R, Harvey LJ, King M, Hooper L, Bouwman J, Gurinovic M, Fairweather-Tait SJ. EURRECA-Estimating Selenium Requirements for Deriving Dietary Reference Values. Critical Reviews in Food Science and Nutrition. 2013; 53:1077-1096.
13. Algotar AM, Stratton MS, Xu MJ, Dalkin BL, Nagle RB, Hsu CH, Ahmann FR, Clark LC, Stratton SP. Dose-Dependent Effects of Selenized Yeast on Total Selenium Levels in Prostatic Tissue of Men With Prostate Cancer. Nutr Cancer. 2011; 63:1-5.
14. Tsavachidou D, McDonnell TJ, Wen S, Wang X, Vakar-Lopez F, Pisters LL, Pettaway CA, Wood CG, Do KA, Thall PF, Stephens C, Efstathiou E, Taylor R, Menter DG, Troncoso P, Lippman SM, et al. Selenium and vitamin E: cell type-and intervention-specific tissue effects in prostate cancer. J Natl Cancer Inst. 2009; 101:306-320.
15. Groger CJ, Grubinger M, Waldhor T, Vierlinger K, Mikulits W. Meta-analysis of gene expression signatures defining the epithelial to mesenchymal transition during cancer progression. PLoS ONE. 2012; 7:e51136.
16. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 2006; 7:131-142.
17. Nieto MA. Epithelial Plasticity: A Common Theme in Embryonic and Cancer Cells. Science. 2013; 342(6159).
18. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelialmesenchymal transitions in development and disease. Cell. 2009; 139:871-890.
19. Gumustekin K, Seven B, Karabulut N, Aktas O, Gursan N, Aslan S, Keles M, Varoglu E, Dane S. Effects of sleep deprivation, nicotine, and selenium on wound healing in rats. The International journal of neuroscience. 2004; 114:1433-1442.
20. Bajpai S, Mishra M, Kumar H, Tripathi K, Singh SK, Pandey HP, Singh RK. Effect of selenium on connexin expression, angiogenesis, and antioxidant status in diabetic wound healing. Biol Trace Elem Res. 2011; 144:327-338.
21. Coutinho P, Qiu C, Frank S, Tamber K, Becker D. Dynamic changes in connexin expression correlate with key events in the wound healing process. Cell Biology International. 2003; 27:525-541.
22. Mori R, Power KT, Wang CM, Martin P, Becker DL. Acute downregulation of connexin43 at wound sites leads to a reduced inflammatory response, enhanced keratinocyte proliferation and wound fibroblast migration. Journal of Cell Science. 2006; 119:5193-5203.
23. Ryszawy D, Sarna M, Rak M, Szpak K, Kedracka-Krok S, Michalik M, Siedlar M, Zuba-Surma E, Burda K, Korohoda W, Madeja Z, Czyz J. Functional links between Snail-1 and Cx43 account for the recruitment of Cx43-positive cells into the invasive front of prostate cancer. Carcinogenesis. 2014.
24. Zhang A, Hitomi M, Bar-Shain N, Dalimov Z, Ellis L, Velpula KK, Fraizer GC, Gourdie RG, Lathia JD. Connexin 43 expression is associated with increased malignancy in prostate cancer cell lines and functions to promote migration. Oncotarget. 2015; 6:11640-11651. doi: 10.18632/oncotarget.3449.
25. Katsuno Y, Lamouille S, Derynck R. TGF-β signaling and epithelial-mesenchymal transition in cancer progression. Current Opinion in Oncology. 2013; 25:76-84 10.1097/CCO.1090b1013e32835b36371.
26. Grande JP. Role of transforming growth factor-beta in tissue injury and repair. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine. 1997; 214:27-40.
27. Algotar AM, Behnejad R, Singh P, Thompson PA, Hsu CH, Stratton SP. Effect of selenium supplementation on proteomic serum biomarkers in elderly men. The Journal of frailty & aging. 2015; 4:107-110.
28. Oettgen P, Finger E, Sun Z, Akbarali Y, Thamrongsak U, Boltax J, Grall F, Dube A, Weiss A, Brown L, Quinn G, Kas K, Endress G, Kunsch C, Libermann TA. PDEF, a Novel Prostate Epithelium-specific Ets Transcription Factor, Interacts with the Androgen Receptor and Activates Prostate-specific Antigen Gene Expression. Journal of Biological Chemistry. 2000; 275:1216-1225.
29. Steffan JJ, Koul HK. Prostate derived ETS factor (PDEF): A putative tumor metastasis suppressor. Cancer Letters. 2011; 310:109-117.
30. Pal M, Koul S, Koul HK. The transcription factor sterile alpha motif (SAM) pointed domain-containing ETS transcription factor (SPDEF) is required for E-cadherin expression in prostate cancer cells. J Biol Chem. 2013; 288:12222-12231.
31. Gu X, Zerbini LF, Otu HH, Bhasin M, Yang Q, Joseph MG, Grall F, Onatunde T, Correa RG, Libermann TA. Reduced PDEF expression increases invasion and expression of mesenchymal genes in prostate cancer cells. Cancer Res. 2007; 67:4219-4226.
32. Johnson TR, Koul S, Kumar B, Khandrika L, Venezia S, Maroni PD, Meacham RB, Koul HK. Loss of PDEF, a prostate-derived Ets factor is associated with aggressive phenotype of prostate cancer: regulation of MMP 9 by PDEF. Mol Cancer. 2010; 9:148.
33. Steffan JJ, Koul S, Meacham RB, Koul HK. The Transcription Factor SPDEF Suppresses Prostate Tumor Metastasis. Journal of Biological Chemistry. 2012; 287:29968-29978.
34. Ghadersohi A, Sharma S, Zhang S, Azrak RG, Wilding GE, Manjili MH, Li F. Prostate-derived Ets transcription factor (PDEF) is a potential prognostic marker in patients with prostate cancer. The Prostate. 2011; 71:1178-1188.
35. Clarke C, Baghdadi H, Howie AF, Mason JI, Walker SW, Beckett GJ. Selenium supplementation attenuates procollagen-1 and interleukin-8 production in fat-loaded human C3A hepatoblastoma cells treated with TGFb1. Biochimica et Biophysica Acta 2010; 1800:611-618.
36. Pei Z, Li H, Guo Y, Jin Y, Lin D. Sodium selenite inhibits the expression of VEGF, TGFbeta(1) and IL-6 induced by LPS in human PC3 cells via TLR4-NF-(K)B signaling blockage. Int Immunopharmacol. 2010; 10:50-56.
37. Zeng H, Briske-Anderson M, Idso JP, Hunt CD. The Selenium Metabolite Methylselenol Inhibits the Migration and Invasion Potential of HT1080 Tumor Cells. The Journal of Nutrition. 2006; 136:1528-1532.
38. Hendrickx W, Decock J, Mulholland F, Bao Y, Fairweather-Tait S. Selenium Biomarkers in Prostate Cancer Cell Lines and Influence of Selenium on Invasive Potential of PC3 Cells. Frontiers in oncology. 2013; 3:239.
39. Tsukamoto T, Hama S, Kogure K, Tsuchiya H. Selenate induces epithelial-mesenchymal transition in a colorectal carcinoma cell line by AKT activation. Experimental cell research. 2013; 319:1913-1921.
40. Zhang J, Wang L, Li G, Anderson LB, Xu Y, Witthuhn B, Lu J. Mouse prostate proteomes are differentially altered by supranutritional intake of four selenium compounds. Nutr Cancer. 2011; 63:778-789.
41. Chiang EC, Shen S, Kengeri SS, Xu H, Combs GF, Morris JS, Bostwick DG, Waters DJ. Defining the Optimal Selenium Dose for Prostate Cancer Risk Reduction: Insights from the U-Shaped Relationship between Selenium Status, DNA Damage, and Apoptosis (a publication of International Hormesis Society). Dose-response. 2009; 8:285-300.
42. Rayman MP. Selenium and human health. The Lancet. 2012; 379:1256-1268.
43. Rayman MP, Infante HG, Sargent M. Food-chain selenium and human health: spotlight on speciation. The British journal of nutrition. 2008; 100:238-253.
44. Hesketh J. Nutrigenomics and selenium: gene expression patterns, physiological targets, and genetics. Annu Rev Nutr. 2008; 28:157-177.
45. Rayman MP. Selenoproteins and human health: insights from epidemiological data. Biochimica et biophysica acta. 2009; 1790:1533-1540.
46. Sinnott JA, Rider JR, Carlsson J, Gerke T, Tyekucheva S, Penney KL, Sesso HD, Loda M, Fall K, Stampfer MJ, Mucci LA, Pawitan Y, Andersson SO, Andren O. Molecular differences in transition zone and peripheral zone prostate tumors. Carcinogenesis. 2015; 36:632-638.
47. Gianduzzo TR, Holmes EG, Tinggi U, Shahin M, Mactaggart P, Nicol D. Prostatic and peripheral blood selenium levels after oral supplementation. J Urol. 2003; 170:870-873.
48. Sabichi AL, Lee JJ, Taylor RJ, Thompson IM, Miles BJ, Tangen CM, Minasian LM, Pisters LL, Caton JR, Basler JW, Lerner SP, Menter DG, Marshall JR, Crawford ED, Lippman SM. Selenium accumulation in prostate tissue during a randomized, controlled short-term trial of l-selenomethionine: a Southwest Oncology Group Study. Clin Cancer Res. 2006; 12:2178-2184.
49. Rayman MP, Thompson AJ, Bekaert B, Catterick J, Galassini R, Hall E, Warren-Perry M, Beckett GJ. Randomized controlled trial of the effect of selenium supplementation on thyroid function in the elderly in the United Kingdom. Am J Clin Nutr. 2008; 87:370-378.
50. Ravn-Haren G, Krath BN, Overvad K, Cold S, Moesgaard S, Larsen EH, Dragsted LO. Effect of long-term selenium yeast intervention on activity and gene expression of antioxidant and xenobiotic metabolising enzymes in healthy elderly volunteers from the Danish Prevention of Cancer by Intervention by Selenium (PRECISE) pilot study. Br J Nutr. 2008; 99:1190-1198.
51. Rayman MP. The use of high-selenium yeast to raise selenium status: how does it measure up? The British journal of nutrition. 2004; 92:557-573.
52. Larsen EH, Hansen M, Paulin H, Moesgaard S, Reid M, Rayman M. Speciation and bioavailability of selenium in yeast-based intervention agents used in cancer chemoprevention studies. Journal of AOAC International. 2004; 87:225-232.
53. Van Dael P, Van Cauwenbergh R, Robberecht H, Deelstra H, Calomme M. Determination of selenium in human serum using electrothermal atomization with longitudinal Zeemaneffect background correction or flow injection hydride generation. At Spectrosc 1995; 16:251-255.
54. Hurst R, Hooper L, Norat T, Lau R, Aune D, Greenwood DC, Vieira R, Collings R, Harvey LJ, Sterne JA, Beynon R, Savovic J, Fairweather-Tait SJ. Selenium and prostate cancer: systematic review and meta-analysis. The American Journal of Clinical Nutrition. 2012; 96:111-122.
55. Geybels MS, Verhage BA, van Schooten FJ, Goldbohm RA, van den Brandt PA. Advanced prostate cancer risk in relation to toenail selenium levels. J Natl Cancer Inst. 2013; 105:1394-1401.
56. Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, Bunney WE, Myers RM, Speed TP, Akil H, Watson SJ, Meng F. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Research. 33:e175.
57. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4:249-264.
58. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004; 3:Article3.
59. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102:15545-15550.
60. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics. 2011; 27:431-432.
61. Merico D, Isserlin R, Stueker O, Emili A, Bader GD. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS ONE. 2010; 5:e13984.
62. Perez-Llamas C, Lopez-Bigas N. Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS ONE. 2011; 6:e19541.