Skip to main content Accessibility help
×
Home

Expression profiling indicating low selenium-sensitive microRNA levels linked to cell cycle and cell stress response pathways in the CaCo-2 cell line

  • Mark J. McCann (a1), Kunjana Rotjanapun (a2), John E. Hesketh (a3) and Nicole C. Roy (a1) (a4)

Abstract

Se is an essential micronutrient for human health, and fluctuations in Se levels and the potential cellular dysfunction associated with it may increase the risk for disease. Although Se has been shown to influence several biological pathways important in health, little is known about the effect of Se on the expression of microRNA (miRNA) molecules regulating these pathways. To explore the potential role of Se-sensitive miRNA in regulating pathways linked with colon cancer, we profiled the expression of 800 miRNA in the CaCo-2 human adenocarcinoma cell line in response to a low-Se (72 h at <40 nm) environment using nCounter direct quantification. These data were then examined using a range of in silico databases to identify experimentally validated miRNA–mRNA interactions and the biological pathways involved. We identified ten Se-sensitive miRNA (hsa-miR-93-5p, hsa-miR-106a-5p, hsa-miR-205-5p, hsa-miR-200c-3p, hsa-miR-99b-5p, hsa-miR-302d-3p, hsa-miR-373-3p, hsa-miR-483-3p, hsa-miR-512-5p and hsa-miR-4454), which regulate 3588 mRNA in key pathways such as the cell cycle, the cellular response to stress, and the canonical Wnt/β-catenin, p53 and ERK/MAPK signalling pathways. Our data show that the effects of low Se on biological pathways may, in part, be due to these ten Se-sensitive miRNA. Dysregulation of the cell cycle and of the stress response pathways due to low Se may influence key genes involved in carcinogenesis.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Expression profiling indicating low selenium-sensitive microRNA levels linked to cell cycle and cell stress response pathways in the CaCo-2 cell line
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Expression profiling indicating low selenium-sensitive microRNA levels linked to cell cycle and cell stress response pathways in the CaCo-2 cell line
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Expression profiling indicating low selenium-sensitive microRNA levels linked to cell cycle and cell stress response pathways in the CaCo-2 cell line
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

* Corresponding author: M. J. McCann, email mark.mccann@agresearch.co.nz

References

Hide All
1. Rayman, MP (2012) Selenium and human health. Lancet 379, 12561268.
2. Roman, M, Jitaru, P & Barbante, C (2014) Selenium biochemistry and its role for human health. Metallomics 6, 2554.
3. Lobanov, AV, Hatfield, DL & Gladyshev, VN (2009) Eukaryotic selenoproteins and selenoproteomes. Biochim Biophys Acta 1790, 14241428.
4. Hesketh, J & Méplan, C (2011) Transcriptomics and functional genetic polymorphisms as biomarkers of micronutrient function: focus on selenium as an exemplar. Proc Nutr Soc 70, 365373.
5. Méplan, C & Hesketh, J (2012) The influence of selenium and selenoprotein gene variants on colorectal cancer risk. Mutagenesis 27, 177186.
6. Méplan, C & Hesketh, J (2014) Selenium and cancer: a story that should not be forgotten – insights from genomics. Cancer Treat Res 159, 145166.
7. Méplan, C (2015) Selenium and chronic diseases: a nutritional genomics perspective. Nutrients 7, 36213651.
8. Barrett, CW, Reddy, VK, Short, SP, et al. (2015) Selenoprotein P influences colitis-induced tumorigenesis by mediating stemness and oxidative damage. J Clin Invest 125, 26462660.
9. Hazane-Puch, F, Arnaud, J, Trocmé, C, et al. (2016) Sodium selenite decreased HDAC activity, cell proliferation and induced apoptosis in three human glioblastoma cells. Anticancer Agents Med Chem 16, 490500.
10. Liu, W, Yao, H, Zhao, W, et al. (2016) Selenoprotein W was correlated with the protective effect of selenium on chicken myocardial cells from oxidative damage. Biol Trace Elem Res 171, 419426.
11. Li, Z, Meng, J, Xu, TJ, et al. (2013) Sodium selenite induces apoptosis in colon cancer cells via Bax-dependent mitochondrial pathway. Eur Rev Med Pharmacol Sci 17, 21662171.
12. Hawkes, WC, Printsev, I & Alkan, Z (2012) Selenoprotein W depletion induces a p53- and p21-dependent delay in cell cycle progression in RWPE-1 prostate epithelial cells. J Cell Biochem 113, 6169.
13. Wu, M, Wu, RT, Wang, TT, et al. (2011) Role for p53 in selenium-induced senescence. J Agric Food Chem 59, 1188211887.
14. Wu, M, Kang, MM, Schoene, NW, et al. (2010) Selenium compounds activate early barriers of tumorigenesis. J Biol Chem 285, 1205512062.
15. Wu, RT, Cao, L, Chen, BP, et al. (2014) Selenoprotein H suppresses cellular senescence through genome maintenance and redox regulation. J Biol Chem 289, 3437834388.
16. Hawkes, WC & 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, 3640.
17. Tsuji, PA, Naranjo-Suarez, S, Carlson, BA, et al. (2011) Deficiency in the 15 kDa selenoprotein inhibits human colon cancer cell growth. Nutrients 3, 805817.
18. Pagmantidis, V, Bermano, G, Villette, S, et al. (2005) Effects of Se-depletion on glutathione peroxidase and selenoprotein W gene expression in the colon. FEBS Lett 579, 792796.
19. Lipinski, B (2017) Sodium selenite as an anti-cancer agent. Anticancer Agents Med Chem 17, 658661.
20. Vinceti, M, Dennert, G, Crespi, CM, et al. (2014) Selenium for preventing cancer. The Cochrane Database of Systematic Reviews, issue 3, CD005195.
21. Bartel, DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215233.
22. Friedman, RC, Farh, KK, Burge, CB, et al. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19, 92105.
23. Voorhoeve, PM (2010) MicroRNAs: oncogenes, tumor suppressors or master regulators of cancer heterogeneity? Biochim Biophys Acta 1805, 7286.
24. Zhang, B, Pan, X, Cobb, GP, et al. (2007) MicroRNAs as oncogenes and tumor suppressors. Dev Biol 302, 112.
25. Hata, A & Lieberman, J (2015) Dysregulation of microRNA biogenesis and gene silencing in cancer. Sci Signal 8, re3.
26. Shah, MS, Kim, E, Davidson, LA, et al. (2016) Comparative effects of diet and carcinogen on microRNA expression in the stem cell niche of the mouse colonic crypt. Biochim Biophys Acta 1862, 121134.
27. Ramalingam, S, Subramaniam, D & Anant, S (2015) Manipulating miRNA expression: a novel approach for colon cancer prevention and chemotherapy. Curr Pharmacol Rep 1, 141153.
28. Ross, SA & Davis, CD (2014) The emerging role of microRNAs and nutrition in modulating health and disease. Annu Rev Nutr 34, 305336.
29. Karius, T, Schnekenburger, M, Dicato, M, et al. (2012) MicroRNAs in cancer management and their modulation by dietary agents. Biochem Pharmacol 83, 15911601.
30. Shah, MS, Davidson, LA & Chapkin, RS (2012) Mechanistic insights into the role of microRNAs in cancer: influence of nutrient crosstalk. Front Genet 3, 305.
31. Shah, MS, Schwartz, SL, Zhao, C, et al. (2011) Integrated microRNA and mRNA expression profiling in a rat colon carcinogenesis model: effect of a chemo-protective diet. Physiol Genomics 43, 640654.
32. Maciel-Dominguez, A, Swan, D, Ford, D, et al. (2013) Selenium alters miRNA profile in an intestinal cell line: evidence that miR-185 regulates expression of GPX2 and SEPSH2. Mol Nutr Food Res 57, 21952205.
33. Ferlay, J, Soerjomataram, I, Dikshit, R, et al. (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136, E359E386.
34. Schneikert, J & Behrens, J (2007) The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut 56, 417425.
35. MacDonald, BT, Tamai, K & He, X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17, 926.
36. Kim, EK & Choi, EJ (2010) Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 1802, 396405.
37. Tachibana, M, Kawamata, H, Fujimori, T, et al. (2004) Dysfunction of p53 pathway in human colorectal cancer: analysis of p53 gene mutation and the expression of the p53-associated factors p14ARF, p33ING1, p21WAF1 and MDM2. Int J Oncol 25, 913920.
38. Colussi, D, Brandi, G, Bazzoli, F, et al. (2013) Molecular pathways involved in colorectal cancer: implications for disease behavior and prevention. Int J Mol Sci 14, 1636516385.
39. Jiricny, J & Marra, G (2003) DNA repair defects in colon cancer. Curr Opin Genet Dev 13, 6169.
40. Schetter, AJ & Harris, CC (2011) Alterations of microRNAs contribute to colon carcinogenesis. Semin Oncol 38, 734742.
41. Hutchison, J, Cohen, Z, Onyeagucha, BC, et al. (2013) How microRNAs influence both hereditary and inflammatory-mediated colon cancers. Cancer Genet 206, 309316.
42. Bera, S, De Rosa, V, Rachidi, W, et al. (2013) Does a role for selenium in DNA damage repair explain apparent controversies in its use in chemoprevention? Mutagenesis 28, 127134.
43. Lewis, BP, Shih, IH, Jones-Rhoades, MW, et al. (2003) Prediction of mammalian microRNA targets. Cell 115, 787798.
44. Barrett, CW, Reddy, VK, Short, SP, et al. (2015) Selenoprotein P influences colitis-induced tumorigenesis by mediating stemness and oxidative damage. J Clin Invest 125, 26462660.
45. Tsuji, PA, Carlson, BA, Yoo, MH, et al. (2015) The 15kDa selenoprotein and thioredoxin reductase 1 promote colon cancer by different pathways. PLOS ONE 10, e0124487.
46. Brigelius-Flohé, R & Kipp, AP (2013) Selenium in the redox regulation of the Nrf2 and the Wnt pathway. Methods Enzymol 527, 6586.
47. Kipp, AP, Müller, MF, Göken, EM, et al. (2012) The selenoproteins GPx2, TrxR2 and TrxR3 are regulated by Wnt signalling in the intestinal epithelium. Biochim Biophys Acta 1820, 15881596.
48. Xing, Y, Liu, Z, Yang, G, et al. (2015) MicroRNA expression profiles in rats with selenium deficiency and the possible role of the Wnt/β-catenin signaling pathway in cardiac dysfunction. Int J Mol Med 35, 143152.
49. Luan, Y, Zhao, J, Yao, H, et al. (2016) Selenium deficiency influences the mRNA expression of selenoproteins and cytokines in chicken erythrocytes. Biol Trace Elem Res 171, 427436.
50. Schomburg, L & Schweizer, U (2009) Hierarchical regulation of selenoprotein expression and sex-specific effects of selenium. Biochim Biophys Acta 1790, 14531462.
51. Berry, MJ (2005) Insights into the hierarchy of selenium incorporation. Nat Genet 37, 11621163.
52. Bermano, G, Arthur, JR & Hesketh, JE (1996) Selective control of cytosolic glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase mRNA stability by selenium supply. FEBS Lett 387, 157160.
53. McCann, MJ, Rowland, IR & Roy, NC (2014) The anti-proliferative effects of enterolactone in prostate cancer cells: evidence for the role of DNA licencing genes, miR-106b cluster expression, and PTEN dosage. Nutrients 6, 48394855.
54. Geiss, GK, Bumgarner, RE, Birditt, B, et al. (2008) Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat Biotechnol 26, 317325.
55. Vlachos, IS, Paraskevopoulou, MD, Karagkouni, D, et al. (2015) DIANA-TarBase v7.0: indexing more than half a million experimentally supported miRNA:mRNA interactions. Nucleic Acids Res 43, D153D159.
56. Gene Ontology Consortium (2017) Gene Ontology Consortium database. http://geneontology.org (accessed April 2017).
57. Ashburner, M, Ball, CA, Blake, JA, et al. (2000) Gene ontology: tool for the unification of biology. Nat Genet 25, 2529.
58. Gene Ontology Consortium (2013) Gene Ontology annotations and resources. Nucleic Acids Res 41, D530D535.
59. Mi, H, Poudel, S, Muruganujan, A, et al. (2016) PANTHER version 10: expanded protein families and functions, and analysis tools. Nucleic Acids Res 44, D336D342.
60. Reactome (2017) Reactome Pathway Database. http://www.reactome.org (accessed April 2017).
61. Croft, D, O’Kelly, G, Wu, G, et al. (2011) Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res 39, D691D697.
62. Kipp, A, Banning, A, van Schothorst, EM, 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, 15611572.
63. Wu, Y, Zhang, H, Dong, Y, et al. (2005) Endoplasmic reticulum stress signal mediators are targets of selenium action. Cancer Res 65, 90739079.
64. de Rosa, V, Erkekoğlu, P, Forestier, A, et al. (2012) Low doses of selenium specifically stimulate the repair of oxidative DNA damage in LNCaP prostate cancer cells. Free Radic Res 46, 105116.
65. Touat-Hamici, Z, Legrain, Y, Bulteau, AL, et al. (2014) Selective up-regulation of human selenoproteins in response to oxidative stress. J Biol Chem 289, 1475014761.
66. Kudva, AK, Shay, AE & Prabhu, KS (2015) Selenium and inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 309, G71G77.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed