Transcriptomic responses of cancerous and noncancerous human colon cells to sulforaphane and selenium

Chemical Research in Toxicology

Volumn 27, Issue 3, 2014, Pages 377-386

  Constantinescu, Simona ^a,b   Hecht, Katrin ^a   Sobotzki, Nadine ^a   Erzinger, Melanie M ^a   Bovet, Cédric ^a   Shay, Jerry W ^c   Wollscheid, Bernd ^a   Sturla, Shana J ^a   Marra, Giancarlo ^d   Beerenwinkel, Niko ^a,b  

^a ETH ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 15; SELENIUM; SELENOPROTEIN W; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTOME;

AKR1B10 GENE; AKR1C1 GENE; AKR1C2 GENE; AKR1C3 GENE; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL GROWTH; COLON CANCER; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; TUMOR GROWTH; UNC5B; UPREGULATION;

20-HYDROXYSTEROID DEHYDROGENASES; CELL LINE; COLON; DOWN-REGULATION; EPITHELIAL CELLS; HT29 CELLS; HUMANS; ISOTHIOCYANATES; ISOTOPE LABELING; METABOLIC NETWORKS AND PATHWAYS; PRINCIPAL COMPONENT ANALYSIS; SELENIUM; TRANSCRIPTOME; UP-REGULATION;

EID: 84896369379     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx400427t     Document Type: Article

References (83)

1. Steinmetz, K. A. and Potter, J. D. (1996) Vegetables, fruit, and cancer prevention J. Am. Diet. Assoc. 96, 1027-1039
2. Trock, B., Lanza, E., and Greenwald, P. (1990) Dietary fiber, vegetables, and colon cancer: Critical review and meta-analyses of the epidemiologic evidence J. Natl. Cancer Inst. 82, 650-661
3. Willett, W. C., Stampfer, M. J., Colditz, G. A., Rosner, B. A., and Speizer, F. E. (1990) Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women N. Engl. J. Med. 323, 1664-1672
4. Verhoeven, D. T., Goldbohm, R. A., van Poppel, G., Verhagen, H., and van den Brandt, P. A. (1996) Epidemiological studies on brassica vegetables and cancer risk Cancer Epidemiol., Biomarkers Prev. 5, 733-748
5. Colorectal Cancer Incidence, Mortality and Prevalence Worldwide in 2008, Report from the International Agency for Research on Cancer, Lyon, France.
6. Key, T. J., Schatzkin, A., Willett, W. C., Allen, N. E., Spencer, E. A., and Travis, R. C. (2004) Diet, nutrition and the prevention of cancer Public Health Nutr. 7, 187-200
7. Martínez, M. E. and Giovannucci, E. (1997) Diet and the prevention of cancer Cancer Metastasis Rev. 16, 357-376
8. Gamet-Payrastre, L., Li, P., Lumeau, S., Cassar, G., Dupont, M.-A., Chevolleau, S., Gasc, N., Tulliez, J., and Tercé, F. (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells Cancer Res. 60, 1426-1433
9. Bovet, C., Erzinger, M. M., Hecht, K., Winiker, P., Constantinescu, S., Sobotzki, N., Beerenwinkel, N., Wollscheid, B., Marra, G., and Sturla, S. J. (2013) Unpublished work.
10. Andělová, H., Rudolf, E., and Červinka, M. (2007) In vitro antiproliferative effects of sulforaphane on human colon cancer cell line SW620 Acta Med. 50, 171-176
11. El-Bayoumy, K. and Sinha, R. (2005) Molecular chemoprevention by selenium: A genomic approach Mutat. Res., Fundam. Mol. Mech. Mutagen. 591, 224-236
12. Nano, J. L., Czerucka, D., Menguy, F., and Rampal, P. (1989) Effect of selenium on the growth of three human colon cancer cell lines Biol. Trace Elem. Res. 20, 31-43
13. Corpet, D. E. and Taché, S. (2002) Most effective colon cancer chemopreventive agents in rats: a systematic review of aberrant crypt foci and tumor data, ranked by potency Nutr. Cancer 43, 1-21
14. Gasper, A. V., Traka, M., Bacon, J. R., Smith, J. A., Taylor, M. A., Hawkey, C. J., Barrett, D. A., and Mithen, R. F. (2007) Consuming broccoli does not induce genes associated with xenobiotic metabolism and cell cycle control in human gastric mucosa J. Nutr. 137, 1718-1724
15. Clark, L. C., Combs, G. F., Turnbull, B. W., Slate, E. H., Chalker, D. K., Chow, J., Davis, L. S., Glover, R. A., Graham, G. F., and Gross, E. G. (1996) Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial J. Am. Med. Assoc. 276, 1957-1963
16. Navarro-Alarcon, M. and Cabrera-Vique, C. (2008) Selenium in food and the human body: A review Sci. Total Environ. 400, 115-141
17. (2012) Selenium: Its Molecular Biology and Role in Human Health (Hatfield, D. L., Berry, M. J., and Gladyshev, V. N., Eds.) Springer, New York.
18. (2005) Vitamin and Mineral Requirements in Human Nutrition, World Health Organization, Geneva, Switzerland.
19. Zeng, H. (2009) Selenium as an essential micronutrient: Roles in cell cycle and apoptosis Molecules 14, 1263-1278
20. Gallegos, A., Berggren, M., Gasdaska, J. R., and Powis, G. (1997) Mechanisms of the regulation of thioredoxin reductase activity in cancer cells by the chemopreventive agent selenium Cancer Res. 57, 4965-4970
21. Zhang, J., Švehlíková, V., Bao, Y., Howie, A. F., Beckett, G. J., and Williamson, G. (2003) Synergy between sulforaphane and selenium in the induction of thioredoxin reductase 1 requires both transcriptional and translational modulation Carcinogenesis 24, 497-503
22. Liu, X., Pietsch, K. E., and Sturla, S. J. (2011) Susceptibility of the antioxidant selenoenyzmes thioredoxin reductase and glutathione peroxidase to alkylation-mediated inhibition by anticancer acylfulvenes Chem. Res. Toxicol. 24, 726-736
23. Tanasova, M. and Sturla, S. J. (2012) Chemistry and biology of acylfulvenes: Sesquiterpene-derived antitumor agents Chem. Rev. 112, 3578-3610
24. Hintze, K. J., Wald, K. A., Zeng, H., Jeffery, E. H., and Finley, J. W. (2003) Thioredoxin reductase in human hepatoma cells is transcriptionally regulated by sulforaphane and other electrophiles via an antioxidant response element J. Nutr. 133, 2721-2727
25. Wang, W., Wang, S., Howie, A. F., Beckett, G. J., Mithen, R., and Bao, Y. (2005) Sulforaphane, erucin, and iberin up-regulate thioredoxin reductase 1 expression in human MCF-7 cells J. Agric. Food Chem. 53, 1417-1421
26. Banning, A., Deubel, S., Kluth, D., Zhou, Z., and Brigelius-Flohé, R. (2005) The GI-GPx gene is a target for Nrf2 Mol. Cell. Biol. 25, 4914-4923
27. Boddupalli, S., Mein, J. R., Lakkanna, S., and James, D. R. (2012) Induction of phase 2 antioxidant enzymes by broccoli sulforaphane: Perspectives in maintaining the antioxidant activity of vitamins A, C, and E Front. Genet. 3, 7
28. Cramer, J. M., Teran-Garcia, M., and Jeffery, E. H. (2011) Enhancing sulforaphane absorption and excretion in healthy men through the combined consumption of fresh broccoli sprouts and a glucoraphanin-rich powder Br. J. Nutr. 13, 1-6
29. Gasper, A. V., Al-Janobi, A., Smith, J. A., Bacon, J. R., Fortun, P., Atherton, C., Taylor, M. A., Hawkey, C. J., Barrett, D. A., and Mithen, R. F. (2005) Glutathione S-transferase M1 polymorphism and metabolism of sulforaphane from standard and high-glucosinolate broccoli Am. J. Clin. Nutr. 82, 1283-1291
30. Hecht, S. S. (2000) Inhibition of carcinogenesis by isothiocyanates Drug Metab. Rev. 32, 395-411
31. Brigelius-Flohé, R. and Banning, A. (2006) Part of the series: From dietary antioxidants to regulators in cellular signaling and gene regulation. Sulforaphane and selenium, partners in adaptive response and prevention of cancer Free Radical Res. 40, 775-787
32. Juge, N., Mithen, R. F., and Traka, M. (2007) Molecular basis for chemoprevention by sulforaphane: A comprehensive review Cell. Mol. Life Sci. 64, 1105-1127
33. Thimmulappa, R. K., Mai, K. H., Srisuma, S., Kensler, T. W., Yamamoto, M., and Biswal, S. (2002) Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray Cancer Res. 62, 5196-5203
34. Sharma, R., Sharma, A., Chaudhary, P., Pearce, V., Vatsyayan, R., Singh, S. V., Awasthi, S., and Awasthi, Y. C. (2010) Role of lipid peroxidation in cellular responses to d, l -sulforaphane, a promising cancer chemopreventive agent Biochemistry 49, 3191-3202
35. Hu, C., Eggler, A. L., Mesecar, A. D., and van Breemen, R. B. (2011) Modification of Keap1 cysteine residues by sulforaphane Chem. Res. Toxicol. 24, 515-521
36. Hong, F., Freeman, M. L., and Liebler, D. C. (2005) Identification of sensor cysteines in human Keap1 modified by the cancer chemopreventive agent sulforaphane Chem. Res. Toxicol. 18, 1917-1926
37. Zhang, D. D. and Hannink, M. (2003) Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress Mol. Cell. Biol. 23, 8137-8151
38. Bonnesen, C., Eggleston, I. M., and Hayes, J. D. (2001) Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines Cancer Res. 61, 6120-6130
39. MacLeod, A. K., McMahon, M., Plummer, S. M., Higgins, L. G., Penning, T. M., Igarashi, K., and Hayes, J. D. (2009) Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: Demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds Carcinogenesis 30, 1571-1580
40. Agyeman, A. S., Chaerkady, R., Shaw, P. G., Davidson, N. E., Visvanathan, K., Pandey, A., and Kensler, T. W. (2012) Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles Breast Cancer Res. Treat. 132, 175-187
41. Stewart, M. S., Davis, R. L., Walsh, L. P., and Pence, B. C. (1997) Induction of differentiation and apoptosis by sodium selenite in human colonic carcinoma cells (HT29) Cancer Lett. 117, 35-40
42. Roig, A. I., Eskiocak, U., Hight, S. K., Kim, S. B., Delgado, O., Souza, R. F., Spechler, S. J., Wright, W. E., and Shay, J. W. (2010) Immortalized epithelial cells derived from human colon biopsies express stem cell markers and differentiate in vitro Gastroenterology 138, 1012-1021
43. Cattaneo, E., Laczko, E., Buffoli, F., Zorzi, F., Bianco, M. A., Menigatti, M., Bartosova, Z., Haider, R., Helmchen, B., Sabates-Bellver, J., Tiwar, A., Jiricny, J., and Marra, G. (2011) Preinvasive colorectal lesion transcriptomes correlate with endoscopic morphology (polypoid vs. nonpolypoid) EMBO Mol. Med. 3, 334-347
44. R Core Team (2013) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria.
45. Carvalho, B. S. and Irizarry, R. A. (2010) A framework for oligonucleotide microarray preprocessing Bioinformatics 26, 2363-2367
46. Smyth, G. K. (2005) Limma: Linear models for microarray data, in Bioinformatics and Computational Biology Solutions Using R and Bioconductor, pp 397-420, Springer, New York.
47. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing J. R. Stat. Soc., Ser. B 1, 289-300
48. Väremo, L., Nielsen, J., and Nookaew, I. (2013) Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods Nucleic Acids Res. 41, 4378-4391
49. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., and Eppig, J. T. (2000) Gene ontology: Tool for the unification of biology Nat. Genet. 25, 25-29
50. Efron, B. and Tibshirani, R. (2007) On testing the significance of sets of genes Ann. Appl. Stat. 1, 107-129
51. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., and Lander, E. S. (2005) Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550
52. Durinck, S., Moreau, Y., Kasprzyk, A., Davis, S., De Moor, B., Brazma, A., and Huber, W. (2005) BioMart and Bioconductor: A powerful link between biological databases and microarray data analysis Bioinformatics 21, 3439-3440
53. Warde-Farley, D., Donaldson, S. L., Comes, O., Zuberi, K., Badrawi, R., Chao, P., Franz, M., Grouios, C., Kazi, F., and Lopes, C. T. (2010) The GeneMANIA prediction server: Biological network integration for gene prioritization and predicting gene function Nucleic Acids Res. 38, W214-W220
54. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., and Gross, B. (2007) Integration of biological networks and gene expression data using Cytoscape Nat. Protoc. 2, 2366-2382
55. Li, J., Lee, J.-M., and Johnson, J. A. (2002) Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in IMR-32 cells J. Biol. Chem. 277, 388-394
56. Devling, T. W. P., Lindsay, C. D., McLellan, L. I., McMahon, M., and Hayes, J. D. (2005) Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype Proc. Natl. Acad. Sci. U.S.A. 102, 7280-7285
57. Hawkes, W. C. and Alkan, Z. (2011) Delayed cell cycle progression from SEPW1 depletion is p53- and p21-dependent in MCF-7 breast cancer cells Biochem. Biophys. Res. Commun. 413, 36-40
58. Kipp, A. P., Frombach, J., Deubel, S., and Brigelius-Flohe, R. (2012) Selenoprotein W as biomarker for the efficacy of selenium compounds to act as source for selenoprotein biosynthesis Methods Enzymol. 527, 87-112
59. Reszka, E. (2012) Selenoproteins in bladder cancer Clin. Chim. Acta 413, 847-854
60. Zeng, H. (2002) Selenite and selenomethionine promote HL-60 cell cycle progression J. Nutr. 132, 674-679
61. Zeng, H. and Combs, G. F., Jr. (2008) Selenium as an anticancer nutrient: roles in cell proliferation and tumor cell invasion J. Nutr. Biochem. 19, 1-7
62. Castets, M., Coissieux, M.-M., Delloye-Bourgeois, C., Bernard, L., Delcros, J.-G., Bernet, A., Laudet, V., and Mehlen, P. (2009) Inhibition of endothelial cell apoptosis by netrin-1 during angiogenesis Dev. Cell 16, 614-620
63. He, K., Jang, S.-W., Joshi, J., Yoo, M.-H., and Ye, K. (2011) Akt-phosphorylated PIKE-A inhibits UNC5B-induced apoptosis in cancer cell lines in a p53-dependent manner Mol. Biol. Cell 22, 1943-1954
64. Breit, S. N., Johnen, H., Cook, A. D., Tsai, V. W. W., Mohammad, M. G., Kuffner, T., Zhang, H. P., Marquis, C. P., Jiang, L., and Lockwood, G. (2011) The TGF-β superfamily cytokine, MIC-1/GDF15: A pleotrophic cytokine with roles in inflammation, cancer and metabolism Growth Factors 29, 187-195
65. Tomasini, R., Seux, M., Nowak, J., Bontemps, C., Carrier, A., Dagorn, J.-C., Pébusque, M.-J., Iovanna, J. L., and Dusetti, N. J. (2005) TP53INP1 is a novel p73 target gene that induces cell cycle arrest and cell death by modulating p73 transcriptional activity Oncogene 24, 8093-8104
66. Löhr, K., Möritz, C., Contente, A., and Dobbelstein, M. (2003) p21/CDKN1A mediates negative regulation of transcription by p53 J. Biol. Chem. 278, 32507-32516
67. Han, M.-K., Song, E.-K., Guo, Y., Ou, X., Mantel, C., and Broxmeyer, H. E. (2008) SIRT1 regulates apoptosis and nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization Cell Stem Cell 2, 241-251
68. Daixing, Z., Chengye, Z., Qiang, Z., and Shusheng, L. (2013) Upregulation of sestrin-2 expression via P53 protects against 1-methyl-4-phenylpyridinium (MPP+) neurotoxicity J. Mol. Neurosci. 51, 967-975
69. Conover, C. A., Bale, L. K., Overgaard, M. T., Johnstone, E. W., Laursen, U. H., Füchtbauer, E.-M., Oxvig, C., and van Deursen, J. (2004) Metalloproteinase pregnancy-associated plasma protein A is a critical growth regulatory factor during fetal development Development 131, 1187-1194
70. Christians, J. K., Hoeflich, A., and Keightley, P. D. (2006) PAPPA2, an enzyme that cleaves an insulin-like growth-factor-binding protein, is a candidate gene for a quantitative trait locus affecting body size in mice Genetics 173, 1547-1553
71. McCleland, M. L., Gardner, R. D., Kallio, M. J., Daum, J. R., Gorbsky, G. J., Burke, D. J., and Stukenberg, P. T. (2003) The highly conserved Ndc80 complex is required for kinetochore assembly, chromosome congression, and spindle checkpoint activity Genes Dev. 17, 101-114
72. Kabeche, L. and Compton, D. A. (2013) Cyclin A regulates kinetochore microtubules to promote faithful chromosome segregation Nature 502, 110-113
73. Nabetani, A., Koujin, T., Tsutsumi, C., Haraguchi, T., and Hiraoka, Y. (2001) A conserved protein, Nuf2, is implicated in connecting the centromere to the spindle during chromosome segregation: A link between the kinetochore function and the spindle checkpoint Chromosoma 110, 322-334
74. McGarry, T. J. and Kirschner, M. W. (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis Cell 93, 1043-1053
75. Zhu, W., Chen, Y., and Dutta, A. (2004) Rereplication by depletion of geminin is seen regardless of p53 status and activates a G2/M checkpoint Mol. Cell. Biol. 24, 7140-7150
76. Bravou, V., Nishitani, H., Song, S. Y., Taraviras, S., and Varakis, J. (2005) Expression of the licensing factors, Cdt1 and Geminin, in human colon cancer Int. J. Oncol. 27, 1511
77. Wohlschlegel, J. A., Kutok, J. L., Weng, A. P., and Dutta, A. (2002) Expression of geminin as a marker of cell proliferation in normal tissues and malignancies Am. J. Pathol. 161, 267-273
78. Chorley, B. N., Campbell, M. R., Wang, X., Karaca, M., Sambandan, D., Bangura, F., Xue, P., Pi, J., Kleeberger, S. R., and Bell, D. A. (2012) Identification of novel NRF2-regulated genes by ChIP-Seq: Influence on retinoid X receptor alpha Nucleic Acids Res. 40, 7416-7429
79. Wu, G., Feng, X., and Stein, L. (2010) A human functional protein interaction network and its application to cancer data analysis Genome Biol. 11, 1-23
80. Nagaraj, N. S., Beckers, S., Mensah, J. K., Waigel, S., Vigneswaran, N., and Zacharias, W. (2006) Cigarette smoke condensate induces cytochromes P450 and aldo-keto reductases in oral cancer cells Toxicol. Lett. 165, 182-194
81. Knowles, L. M., Yang, C., Osterman, A., and Smith, J. W. (2008) Inhibition of fatty-acid synthase induces caspase-8-mediated tumor cell apoptosis by up-regulating DDIT4 J. Biol. Chem. 283, 31378-31384
82. Hashimoto, O., Ushiro, Y., Sekiyama, K., Yamaguchi, O., Yoshioka, K., Mutoh, K.-I., and Hasegawa, Y. (2006) Impaired growth of pancreatic exocrine cells in transgenic mice expressing human activin βE subunit Biochem. Biophys. Res. Commun. 341, 416-424
83. Papaiahgari, S., Kleeberger, S. R., Cho, H.-Y., Kalvakolanu, D. V., and Reddy, S. P. (2004) NADPH oxidase and ERK signaling regulates hyperoxia-induced Nrf2-ARE transcriptional response in pulmonary epithelial cells J. Biol. Chem. 279, 42302-42312