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Current Nutraceuticals

Editor-in-Chief

ISSN (Print): 2665-9786
ISSN (Online): 2665-9794

Research Article

Selenite-induced Expression of a Caenorhabditis elegans Pro-aging Factor and Ortholog of Human Selenium-binding Protein 1

Author(s): Karl Köhnlein, Nadine Urban, Holger Steinbrenner, David Guerrero-Gómez, Antonio Miranda-Vizuete, Christoph Kaether and Lars-Oliver Klotz*

Volume 1, Issue 1, 2020

Page: [73 - 79] Pages: 7

DOI: 10.2174/2665978601666200212105825

Abstract

Background: The essential trace element and micronutrient selenium exerts most of its biological actions through incorporation into selenoproteins as selenocysteine. Two further types of Se-containing proteins exist, including those that have selenomethionine incorporated instead of methionine, and the group of selenium-binding proteins. We previously described an ortholog of selenium-binding protein 1 (SELENBP1) in the nematode Caenorhabditis elegans, Y37A1B.5, and demonstrated that it confers resistance to toxic selenite concentrations while impairing general stress resistance and life expectancy of C. elegans.

Objective: We tested for the effect of selenite on Y37A1B.5 expression, and we analyzed whether Y37A1B.5 also shows a lifespan-modulating effect when the nematodes are deficient in the selenoenzyme thioredoxin reductase-1 (TRXR-1).

Methods: C. elegans expressing a translational reporter construct encoding GFP-tagged Y37A1B.5 under the control of the Y37A1B.5 promoter were exposed to selenite, followed by fluorescence microscopic analysis of GFP levels. Lifespan analyses and RNA interference experiments were performed in trxr-1-deficient worms.

Results: We here demonstrate that selenite at toxic concentrations stimulates the expression of the translational Y37A1B.5 reporter. The lifespan-extending effect of Y37A1B.5 deficiency was preserved upon the deletion of the only selenoprotein in C. elegans, TRXR-1.

Conclusion: These data suggest that (1) Y37A1B.5 may serve as a selenite-responsive buffer against high environmental selenium concentrations and that (2) lifespan extension elicited by Y37A1B.5 knockdown does not require functional TRXR-1.

Keywords: Selenium-binding protein, selenite, stress signaling, Caenorhabditis elegans, lifespan, thioredoxin reductase.

Graphical Abstract

[1]
Brigelius-Flohé, R.; Flohé, L. Selenium and redox signaling. Arch. Biochem. Biophys., 2017, 617, 48-59.
[http://dx.doi.org/10.1016/j.abb.2016.08.003] [PMID: 27495740]
[2]
Fairweather-Tait, S.J.; Bao, Y.; Broadley, M.R.; Collings, R.; Ford, D.; Hesketh, J.E.; Hurst, R. Selenium in human health and disease. Antioxid. Redox Signal., 2011, 14(7), 1337-1383.
[http://dx.doi.org/10.1089/ars.2010.3275] [PMID: 20812787]
[3]
Steinbrenner, H.; Speckmann, B.; Klotz, L.O. Selenoproteins: Antioxidant selenoenzymes and beyond. Arch. Biochem. Biophys., 2016, 595, 113-119.
[http://dx.doi.org/10.1016/j.abb.2015.06.024] [PMID: 27095226]
[4]
Steinbrenner, H.; Brigelius-Flohé, R. Das essenzielle Spurenelement Selen: Selenbedarf in gesundheit und krankheit (the essential trace element selenium: Requirements for selenium intake in health and disease). Aktuel. Ernahrungsmed., 2015, 40, 368-378.
[http://dx.doi.org/10.1055/s-0035-1552774]
[5]
Kryukov, G.V.; Castellano, S.; Novoselov, S.V.; Lobanov, A.V.; Zehtab, O.; Guigó, R.; Gladyshev, V.N. Characterization of mammalian selenoproteomes. Science, 2003, 300(5624), 1439-1443.
[http://dx.doi.org/10.1126/science.1083516] [PMID: 12775843]
[6]
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., 2007, 9(7), 775-806.
[http://dx.doi.org/10.1089/ars.2007.1528] [PMID: 17508906]
[7]
Bansal, M.P.; Oborn, C.J.; Danielson, K.G.; Medina, D. Evidence for two selenium-binding proteins distinct from glutathione peroxidase in mouse liver. Carcinogenesis, 1989, 10(3), 541-546.
[http://dx.doi.org/10.1093/carcin/10.3.541] [PMID: 2924398]
[8]
Steinbrenner, H.; Micoogullari, M.; Hoang, N.A.; Bergheim, I.; Klotz, L.O.; Sies, H. Selenium-binding protein 1 (SELENBP1) is a marker of mature adipocytes. Redox Biol., 2019, 20, 489-495.
[http://dx.doi.org/10.1016/j.redox.2018.11.004] [PMID: 30469030]
[9]
Li, T.; Yang, W.; Li, M.; Byun, D.S.; Tong, C.; Nasser, S.; Zhuang, M.; Arango, D.; Mariadason, J.M.; Augenlicht, L.H. Expression of selenium-binding protein 1 characterizes intestinal cell maturation and predicts survival for patients with colorectal cancer. Mol. Nutr. Food Res., 2008, 52(11), 1289-1299.
[http://dx.doi.org/10.1002/mnfr.200700331] [PMID: 18435490]
[10]
Elhodaky, M.; Diamond, A.M. Selenium-Binding Protein 1 in Human Health and Disease. Int. J. Mol. Sci., 2018, 19(11) E3437
[http://dx.doi.org/10.3390/ijms19113437] [PMID: 30400135]
[11]
Wang, Y.; Fang, W.; Huang, Y.; Hu, F.; Ying, Q.; Yang, W.; Xiong, B. Reduction of selenium-binding protein 1 sensitizes cancer cells to selenite via elevating extracellular glutathione: a novel mechanism of cancer-specific cytotoxicity of selenite. Free Radic. Biol. Med., 2015, 79, 186-196.
[http://dx.doi.org/10.1016/j.freeradbiomed.2014.11.015] [PMID: 25445402]
[12]
Pol, A.; Renkema, G.H.; Tangerman, A.; Winkel, E.G.; Engelke, U.F.; de Brouwer, A.P.M.; Lloyd, K.C.; Araiza, R.S.; van den Heuvel, L.; Omran, H.; Olbrich, H.; Oude Elberink, M.; Gilissen, C.; Rodenburg, R.J.; Sass, J.O.; Schwab, K.O.; Schäfer, H.; Venselaar, H.; Sequeira, J.S.; Op den Camp, H.J.M.; Wevers, R.A. Mutations in SELENBP1, encoding a novel human methanethiol oxidase, cause extraoral halitosis. Nat. Genet., 2018, 50(1), 120-129.
[http://dx.doi.org/10.1038/s41588-017-0006-7] [PMID: 29255262]
[13]
Köhnlein, K.; Urban, N.; Guerrero-Gómez, D.; Steinbrenner, H.; Urbánek, P.; Priebs, J.; Koch, P.; Kaether, C.; Miranda-Vizuete, A.; Klotz, L.O. A Caenorhabditis elegans ortholog of human selenium-binding protein 1 is a pro-aging factor protecting against selenite toxicity. Redox Biol., 2020, 28 101323
[http://dx.doi.org/10.1016/j.redox.2019.101323] [PMID: 31557719]
[14]
Taskov, K.; Chapple, C.; Kryukov, G.V.; Castellano, S.; Lobanov, A.V.; Korotkov, K.V.; Guigó, R.; Gladyshev, V.N. Nematode selenoproteome: the use of the selenocysteine insertion system to decode one codon in an animal genome? Nucleic Acids Res., 2005, 33(7), 2227-2238.
[http://dx.doi.org/10.1093/nar/gki507] [PMID: 15843685]
[15]
Stenvall, J.; Fierro-González, J.C.; Swoboda, P.; Saamarthy, K.; Cheng, Q.; Cacho-Valadez, B.; Arnér, E.S.; Persson, O.P.; Miranda-Vizuete, A.; Tuck, S. Selenoprotein TRXR-1 and GSR-1 are essential for removal of old cuticle during molting in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA, 2011, 108(3), 1064-1069.
[http://dx.doi.org/10.1073/pnas.1006328108] [PMID: 21199936]
[16]
Fraser, A.G.; Kamath, R.S.; Zipperlen, P.; Martinez-Campos, M.; Sohrmann, M.; Ahringer, J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature, 2000, 408(6810), 325-330.
[http://dx.doi.org/10.1038/35042517] [PMID: 11099033]
[17]
Rohn, I.; Marschall, T.A.; Kroepfl, N.; Jensen, K.B.; Aschner, M.; Tuck, S.; Kuehnelt, D.; Schwerdtle, T.; Bornhorst, J. Selenium species-dependent toxicity, bioavailability and metabolic transformations in Caenorhabditis elegans. Metallomics, 2018, 10(6), 818-827.
[http://dx.doi.org/10.1039/C8MT00066B] [PMID: 29770420]
[18]
Boehler, C.J.; Raines, A.M.; Sunde, R.A. Deletion of thioredoxin reductase and effects of selenite and selenate toxicity in Caenorhabditis elegans. PLoS One, 2013, 8(8) e71525
[http://dx.doi.org/10.1371/journal.pone.0071525] [PMID: 23936512]
[19]
Li, W.; Bandyopadhyay, J.; Hwaang, H.S.; Park, B.J.; Cho, J.H.; Lee, J.I.; Ahnn, J.; Lee, S.K. Two thioredoxin reductases, trxr-1 and trxr-2, have differential physiological roles in Caenorhabditis elegans. Mol. Cells, 2012, 34(2), 209-218.
[http://dx.doi.org/10.1007/s10059-012-0155-6] [PMID: 22836943]

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