Selenium-regulated hierarchy of human selenoproteome in cancerous and immortalized cells lines

Biochimica et Biophysica Acta - General Subjects

Volumn 1862, Issue 11, 2018, Pages 2493-2505

  Touat Hamici, Zahia ^a   Bulteau, Anne Laure ^b   Bianga, Juliusz ^c   Jean Jacques, Hélène ^d   Szpunar, Joanna ^c   Lobinski, Ryszard ^c   Chavatte, Laurent ^e  

^a CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE PAU ET DES PAYS DE L'ADOUR   (France)

^d INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^e CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

Author keywords

Glutathione peroxidase; IEF LA ICP MS; SECIS; Selenoprotein hierarchy; Thioredoxin reductase; UGA recoding

Indexed keywords

GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE PEROXIDASE 2; GLUTATHIONE PEROXIDASE 3; GLUTATHIONE PEROXIDASE 6; MESSENGER RNA; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; SELENIUM; SELENOF PROTEIN; SELENOM PROTEIN; SELENOPROTEIN; SELENOPROTEIN P; SELENOPROTEIN W; SELENOS PROTEIN; SEPHS2 PROTEIN; THIOREDOXIN REDUCTASE; THIOREDOXIN REDUCTASE 1; THIOREDOXIN REDUCTASE 2; THIOREDOXIN REDUCTASE 3; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL LINE; CONTROLLED STUDY; GENE EXPRESSION; HACAT CELL LINE; HEK293 CELL LINE; HEP-G2 CELL LINE; HUMAN; HUMAN CELL; IMMORTALIZED CELL LINE; LNCAP CELL LINE; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSLATION REGULATION;

EID: 85045755435     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2018.04.012     Document Type: Article

References (55)

1. Sonet, J., Bulteau, A.-L., Chavatte, L., Selenium and selenoproteins in human health and diseases. Michalke, B., (eds.) Metallomics: Analytical Techniques and Speciation Methods, 2016, Wiley-VCH Verlag GmbH & Co. KGaA, 364–381.
2. Hatfield, D.L., Tsuji, P.A., Carlson, B.A., Gladyshev, V.N., Selenium and selenocysteine: roles in cancer, health, and development. Trends Biochem. Sci. 39 (2014), 112–120.
3. Kurokawa, S., Berry, M.J., Selenium. Role of the essential metalloid in health. Met. Ions Life Sci. 13 (2013), 499–534.
4. Rayman, M.P., Selenium and human health. Lancet 379 (2012), 1256–1268.
5. Papp, L.V., Holmgren, A., Khanna, K.K., Selenium and selenoproteins in health and disease. Antioxid. Redox Signal. 12 (2010), 793–795.
6. Hatfield, D.L., Carlson, B.A., Xu, X.M., Mix, H., Gladyshev, V.N., Selenocysteine incorporation machinery and the role of selenoproteins in development and health. Prog. Nucleic Acid Res. Mol. Biol. 81 (2006), 97–142.
7. Latrèche, L., Chavatte, L., Selenium incorporation into selenoproteins, implications in human health. Metal Ions in Biology and Medicine, X, 2008, 731–737.
8. Whanger, P.D., Selenium and its relationship to cancer: an update. Br. J. Nutr. 91 (2004), 11–28.
9. Meplan, C., Hesketh, J., Selenium and cancer: a story that should not be forgotten-insights from genomics. Cancer Treat. Res. 159 (2014), 145–166.
10. Mariotti, M., Ridge, P.G., Zhang, Y., Lobanov, A.V., Pringle, T.H., Guigo, R., Hatfield, D.L., Gladyshev, V.N., Composition and evolution of the vertebrate and mammalian selenoproteomes. PLoS One, 7, 2012, e33066.
11. Lobanov, A.V., Hatfield, D.L., Gladyshev, V.N., Eukaryotic selenoproteins and selenoproteomes. Biochim. Biophys. Acta 1790 (2009), 1424–1428.
12. Kryukov, G.V., Castellano, S., Novoselov, S.V., Lobanov, A.V., Zehtab, O., Guigo, R., Gladyshev, V.N., Characterization of mammalian selenoproteomes. Science 300 (2003), 1439–1443.
13. Gladyshev, V.N., Arner, E.S., Berry, M.J., Brigelius-Flohe, R., Bruford, E.A., Burk, R.F., Carlson, B.A., Castellano, S., Chavatte, L., Conrad, M., Copeland, P.R., Diamond, A.M., Driscoll, D.M., Ferreiro, A., Flohe, L., Green, F.R., Guigo, R., Handy, D.E., Hatfield, D.L., Hesketh, J., Hoffmann, P.R., Holmgren, A., Hondal, R.J., Howard, M.T., Huang, K., Kim, H.-Y., Kim, I.Y., Kohrle, J., Krol, A., Kryukov, G.V., Lee, B.J., Lee, B.C., Lei, X.G., Liu, Q., Lescure, A., Lobanov, A.V., Loscalzo, J., Maiorino, M., Mariotti, M., Sandeep Prabhu, K., Rayman, M.P., Rozovsky, S., Salinas, G., Schmidt, E.E., Schomburg, L., Schweizer, U., Simonovic, M., Sunde, R.A., Tsuji, P.A., Tweedie, S., Ursini, F., Whanger, P.D., Zhang, Y., Selenoprotein gene nomenclature. J. Biol. Chem. 291 (2016), 24036–24040.
14. Labunskyy, V.M., Hatfield, D.L., Gladyshev, V.N., Selenoproteins: molecular pathways and physiological roles. Physiol. Rev. 94 (2014), 739–777.
15. Shchedrina, V.A., Zhang, Y., Labunskyy, V.M., Hatfield, D.L., Gladyshev, V.N., Structure-function relations, physiological roles, and evolution of mammalian ER-resident selenoproteins. Antioxid. Redox Signal. 12 (2009), 839–849.
16. Papp, L.V., Lu, J., Holmgren, A., Khanna, K.K., From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid. Redox Signal. 9 (2007), 775–806.
17. Carlson, B.A., Lee, B.J., Tsuji, P.A., Tobe, R., Park, J.M., Schweizer, U., Gladyshev, V.N., Hatfield, D.L., Selenocysteine tRNA [Ser]Sec: from nonsense suppressor tRNA to the quintessential constituent in selenoprotein biosynthesis. S., U., Hatfield, D.L., Tsuji, P.A., Gladyshev, V.N., (eds.) Selenium: Its Molecular Biology and Role in Human Health, 4th Edition, 2016, Springer Science + Business Media, LLC, New York, NY, 3–12.
18. Squires, J.E., Berry, M.J., Eukaryotic selenoprotein synthesis: mechanistic insight incorporating new factors and new functions for old factors. IUBMB Life 60 (2008), 232–235.
19. Allmang, C., Krol, A., Selenoprotein synthesis: UGA does not end the story. Biochimie 88 (2006), 1561–1571.
20. Driscoll, D.M., Copeland, P.R., Mechanism and regulation of selenoprotein synthesis. Annu. Rev. Nutr. 23 (2003), 17–40.
21. Bulteau, A.L., Chavatte, L., Update on selenoprotein biosynthesis. Antioxid. Redox Signal. 23 (2015), 775–794.
22. Tujebajeva, R.M., Copeland, P.R., Xu, X.M., Carlson, B.A., Harney, J.W., Driscoll, D.M., Hatfield, D.L., Berry, M.J., Decoding apparatus for eukaryotic selenocysteine insertion. EMBO Rep. 1 (2000), 158–163.
23. Fagegaltier, D., Hubert, N., Yamada, K., Mizutani, T., Carbon, P., Krol, A., Characterization of mSelB, a novel mammalian elongation factor for selenoprotein translation. EMBO J. 19 (2000), 4796–4805.
24. Copeland, P.R., Fletcher, J.E., Carlson, B.A., Hatfield, D.L., Driscoll, D.M., A novel RNA binding protein, SBP2, is required for the translation of mammalian selenoprotein mRNAs. EMBO J. 19 (2000), 306–314.
25. Howard, M.T., Carlson, B.A., Anderson, C.B., Hatfield, D.L., Translational redefinition of UGA codons is regulated by selenium availability. J. Biol. Chem. 288 (2013), 19401–19413.
26. Turanov, A.A., Everley, R.A., Hybsier, S., Renko, K., Schomburg, L., Gygi, S.P., Hatfield, D.L., Gladyshev, V.N., Regulation of selenocysteine content of human selenoprotein P by dietary selenium and insertion of cysteine in place of selenocysteine. PLoS One, 10, 2015, e0140353.
27. Turanov, A.A., Xu, X.-M., Carlson, B.A., Yoo, M.-H., Gladyshev, V.N., Hatfield, D.L., Biosynthesis of selenocysteine, the 21st amino acid in the genetic code, and a novel pathway for cysteine biosynthesis. Adv. Nutr. 2 (2011), 122–128.
28. Xu, X.M., Turanov, A.A., Carlson, B.A., Yoo, M.H., Everley, R.A., Nandakumar, R., Sorokina, I., Gygi, S.P., Gladyshev, V.N., Hatfield, D.L., Targeted insertion of cysteine by decoding UGA codons with mammalian selenocysteine machinery. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 21430–21434.
29. Weiss Sachdev, S., Sunde, R.A., Selenium regulation of transcript abundance and translational efficiency of glutathione peroxidase-1 and -4 in rat liver. Biochem. J. 357 (2001), 851–858.
30. Bermano, G., Arthur, J.R., Hesketh, J.E., Selective control of cytosolic glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase mRNA stability by selenium supply. FEBS Lett. 387 (1996), 157–160.
31. Bermano, G., Arthur, J.R., Hesketh, J.E., Role of the 3′ untranslated region in the regulation of cytosolic glutathione peroxidase and phospholipid-hydroperoxide glutathione peroxidase gene expression by selenium supply. Biochem. J. 320:Pt 3 (1996), 891–895.
32. Bermano, G., Nicol, F., Dyer, J.A., Sunde, R.A., Beckett, G.J., Arthur, J.R., Hesketh, J.E., Tissue-specific regulation of selenoenzyme gene expression during selenium deficiency in rats. Biochem. J. 311:Pt 2 (1995), 425–430.
33. Touat-Hamici, Z., Legrain, Y., Bulteau, A.L., Chavatte, L., Selective up-regulation of human selenoproteins in response to oxidative stress. J. Biol. Chem. 289 (2014), 14750–14761.
34. Papp, L.V., Lu, J., Striebel, F., Kennedy, D., Holmgren, A., Khanna, K.K., The redox state of SECIS binding protein 2 controls its localization and selenocysteine incorporation function. Mol. Cell. Biol. 26 (2006), 4895–4910.
35. Legrain, Y., Touat-Hamici, Z., Chavatte, L., Interplay between selenium levels, selenoprotein expression, and replicative senescence in WI-38 human fibroblasts. J. Biol. Chem. 289 (2014), 6299–6310.
36. Hammad, G., Legrain, Y., Touat-Hamici, Z., Duhieu, S., Cornu, D., Bulteau, A.L., Chavatte, L., Interplay between selenium levels and replicative senescence in WI-38 human fibroblasts: a proteomic approach. Antioxid. (Basel), 7, 2018.
37. Touat-Hamici, Z., Legrain, Y., Sonet, J., Bulteau, A.-L., Chavatte, L., Alteration of selenoprotein expression during stress and in aging. S., U., Hatfield, D.L., Tsuji, P.A., Gladyshev, V.N., (eds.) Selenium: Its Molecular Biology and Role in Human Health, 4th Edition, 2016, Springer Science + Business Media, LLC, New York, NY, 539–551.
38. Carlson, B.A., Xu, X.M., Gladyshev, V.N., Hatfield, D.L., Selective rescue of selenoprotein expression in mice lacking a highly specialized methyl group in selenocysteine tRNA. J. Biol. Chem. 280 (2005), 5542–5548.
39. Hatfield, D.L., Gladyshev, V.N., How selenium has altered our understanding of the genetic code. Mol. Cell. Biol. 22 (2002), 3565–3576.
40. Chittum, H.S., Hill, K.E., Carlson, B.A., Lee, B.J., Burk, R.F., Hatfield, D.L., Replenishment of selenium deficient rats with selenium results in redistribution of the selenocysteine tRNA population in a tissue specific manner. Biochim. Biophys. Acta 1359 (1997), 25–34.
41. Hatfield, D., Lee, B.J., Hampton, L., Diamond, A.M., Selenium induces changes in the selenocysteine tRNA[Ser]Sec population in mammalian cells. Nucleic Acids Res. 19 (1991), 939–943.
42. Latreche, L., Duhieu, S., Touat-Hamici, Z., Jean-Jean, O., Chavatte, L., The differential expression of glutathione peroxidase 1 and 4 depends on the nature of the SECIS element. RNA Biol. 9 (2012), 681–690.
43. Sonet, J., Mounicou, S., Chavatte, L., Detection of selenoproteins by laser ablation inductively coupled plasma mass spectrometry (LA-ICP MS) in immobilized pH gradient (IPG) strips. Methods Mol. Biol. 1661 (2018), 205–217.
44. Bianga, J., Touat-Hamici, Z., Bierla, K., Mounicou, S., Szpunar, J., Chavatte, L., Lobinski, R., Speciation analysis for trace levels of selenoproteins in cultured human cells. J. Proteome 108 (2014), 316–324.
45. Shaw, G., Morse, S., Ararat, M., Graham, F.L., Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 16 (2002), 869–871.
46. Boukamp, P., Petrussevska, R.T., Breitkreutz, D., Hornung, J., Markham, A., Fusenig, N.E., Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106 (1988), 761–771.
47. Horoszewicz, J.S., Leong, S.S., Kawinski, E., Karr, J.P., Rosenthal, H., Chu, T.M., Mirand, E.A., Murphy, G.P., LNCaP model of human prostatic carcinoma. Cancer Res. 43 (1983), 1809–1818.
48. Latreche, L., Jean-Jean, O., Driscoll, D.M., Chavatte, L., Novel structural determinants in human SECIS elements modulate the translational recoding of UGA as selenocysteine. Nucleic Acids Res. 37 (2009), 5868–5880.
49. Sonet, J., Mounicou, S., Chavatte, L., Nonradioactive isotopic labeling and tracing of selenoproteins in cultured cell lines. Methods Mol. Biol. 1661 (2018), 193–203.
50. Bianga, J., Ballihaut, G., Pecheyran, C., Touat, Z., Preud'homme, H., Mounicou, S., Chavatte, L., Lobinski, R., Szpunar, J., Detection of selenoproteins in human cell extracts by laser ablation-ICP MS after separation by polyacrylamide gel electrophoresis and blotting. J. Anal. Atom Spectrom. 27 (2012), 25–32.
51. Sunde, R.A., Raines, A.M., Selenium regulation of the selenoprotein and nonselenoprotein transcriptomes in rodents. Adv. Nutr. 2 (2011), 138–150.
52. Sunde, R.A., mRNA transcripts as molecular biomarkers in medicine and nutrition. J. Nutr. Biochem. 21 (2010), 665–670.
53. Sunde, R.A., Raines, A.M., Barnes, K.M., Evenson, J.K., Selenium status highly regulates selenoprotein mRNA levels for only a subset of the selenoproteins in the selenoproteome. Biosci. Rep. 29 (2009), 329–338.
54. Bierla, K., Szpunar, J., Lobinski, R., Biological selenium species and selenium speciation in biological samples. S., U., Hatfield, D.L., Tsuji, P.A., Gladyshev, V.N., (eds.) Selenium: Its Molecular Biology and Role in Human Health, 4th Edition, 2016, Springer Science + Business Media, LLC, New York, NY, 413–424.
55. Sonet, J., Bierla, K., Bulteau, A.L., Lobinski, R., Chavatte, L., Comparison of analytical methods using enzymatic activity, immunoaffinity and selenium-specific mass spectrometric detection for the quantitation of glutathione peroxidase 1. Anal. Chim. Acta 1011 (2018), 11–19.