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Selenoneine: a Unique Reactive Selenium Species From the Blood of Tuna With Implications for Human Diseases

  • Rama Alhasan
  • Muhammad Jawad Nasim
  • Claus Jacob
  • Caroline GaucherEmail author
Redox Modulators (C Jacob, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Redox Modulators

Abstract

Purpose of Review

The trace element selenium is found in many dietary components, from grains to Brazil nuts. In humans, this chalcogen is essential for many physiological processes. A couple of years ago, selenoneine, a rather unusual seleno-histidine derivative, has been isolated from tuna.

Recent Findings

Whilst there is a limited number of other naturally occurring small selenium compounds, large quantities of selenoneine can be generated in genetically engineered microorganisms and via chemical synthesis. Due to a rare selenol/selenone tautomerism, this compound exhibits unique redox properties and promising biological activities, which range of traditional antioxidant action to the interaction and subsequent protection of metal ions.

Summary

Selenoneine may indeed provide a promising lead for a new generation of selenium supplements and chemopreventive agents.

Keywords

Antioxidants Cardiovascular diseases Reactive selenium species Selenol/selenone tautomerism Selenoneine Tuna 

Notes

Acknowledgements

The authors express special thanks to Ken Rory, Ashfiq Al-Fakhim, Rosa Ponte, Vulgar Prol, Trafique Basel and many other colleagues of the “Academiacs International” (www.academiacs.eu) and “Pharmasophy” networks for the helpful discussions and inspiration.

Funding Information

Support was provided by the INTERREG VA GR programme (BIOVAL, Grant No. 4-09-21), the NutRedOx (Cost project CA16112), the “Landesforschungsförderungsprogramm” of the State of Saarland (Grant No. WT/2–LFFP 16/01) and the respective Universities: University of Saarland, Université de Lorraine, CITHEFOR, Nancy, France and Alex Ekwueme Federal University.

Compliance with Ethical Standards

Conflict of Interest

There are no real or potential conflicts to declare.

Human and Animal Rights and Informed

All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Kurokawa S, Berry MJ. Selenium. Role of the essential metalloid in health. Met Ions Life Sci. 2013;13:499–534.  https://doi.org/10.1007/978-94-007-7500-8_16.CrossRefGoogle Scholar
  2. 2.
    Reich HJ, Hondal RJ. Why nature chose selenium. ACS Chem Biol. 2016;11(4):821–41.  https://doi.org/10.1021/acschembio.6b00031.CrossRefGoogle Scholar
  3. 3.
    Himeno S, Imura N. New aspects of physiological and pharmacological roles of selenium. J Health Sci. 2000;46(6):393–8.  https://doi.org/10.1248/jhs.46.393.CrossRefGoogle Scholar
  4. 4.
    Tinggi U. Selenium: its role as antioxidant in human health. Environ Health Prev Med. 2008;13(2):102–8.  https://doi.org/10.1007/s12199-007-0019-4.CrossRefGoogle Scholar
  5. 5.
    Rayman MP. The importance of selenium to human health. Lancet. 2000;356(9225):233–41.  https://doi.org/10.1016/s0140-6736(00)02490-9.CrossRefGoogle Scholar
  6. 6.
    Schrauzer GN. Nutritional selenium supplements: product types, quality, and safety. J Am Coll Nutr. 2001;20(1):1–4.  https://doi.org/10.1080/07315724.2001.10719007.CrossRefGoogle Scholar
  7. 7.
    Reilly C. Selenium in food and health. New York: Springer; 2006.Google Scholar
  8. 8.
    Fairweather-Tait SJ, Bao Y, Broadley MR, Collings R, Ford D, Hesketh JE, et al. Selenium in human health and disease. Antioxid Redox Signal. 2011;14(7):1337–83.  https://doi.org/10.1089/ars.2010.3275.
  9. 9.
    Rayman MP. The argument for increasing selenium intake. Proc Nutr Soc. 2002;61(2):203–15.  https://doi.org/10.1079/pns2002153.CrossRefGoogle Scholar
  10. 10.
    Papp LV, Holmgren A, Khanna KK. Selenium and selenoproteins in health and disease. Antioxid Redox Signal. 2010;12(7):793–5.  https://doi.org/10.1089/ars.2009.2973.CrossRefGoogle Scholar
  11. 11.
    Winkel LH, Johnson CA, Lenz M, Grundl T, Leupin OX, Amini M, et al. Environmental selenium research: from microscopic processes to global understanding. Environ Sci Technol. 2012;46(2):571–9.  https://doi.org/10.1021/es203434d.CrossRefGoogle Scholar
  12. 12.
    Jukes TH. Selenium, an “essential poison”. J Appl Biochem. 1983;5(4–5):233–4.Google Scholar
  13. 13.
    Fordyce F. Selenium deficiency and toxicity in: Selinus O, editors. the environment. Essentials of medical geology. Elsevier; 2005.Google Scholar
  14. 14.
    Hira CK, Partal K, Dhillon K. Dietary selenium intake by men and women in high and low selenium areas of Punjab. Public Health Nutr. 2004;7(1):39–43.  https://doi.org/10.1079/PHN2003513.CrossRefGoogle Scholar
  15. 15.
    Reilly C. Selenium in food and health. London: Academic and Professional; 1997.Google Scholar
  16. 16.
    Haug A, Graham RD, Christophersen OA, Lyons GH. How to use the world’s scarce selenium resources efficiently to increase the selenium concentration in food. Microb Ecol Health Dis. 2007;19(4):209–28.  https://doi.org/10.1080/08910600701698986.CrossRefGoogle Scholar
  17. 17.
    Stewart MS, Spallholz JH, Neldner K, Pence B. Selenium compounds have disparate abilities to impose oxidative stress and induce apoptosis. Free Radic Biol Med. 1999;26(1–2):42–8.  https://doi.org/10.1016/S0891-5849(98)00147-6.CrossRefGoogle Scholar
  18. 18.
    Ghadi FE, Ghara AR, Bhattacharyya S, Dhawan DK. Selenium as a chemopreventive agent in experimentally induced colon carcinogenesis. World J Gastrointest Oncol. 2009;1(1):74–81.  https://doi.org/10.4251/wjgo.v1.i1.74.CrossRefGoogle Scholar
  19. 19.
    Jacob C, Giles GI, Giles NM, Sies H. Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed Eng. 2003;42(39):4742–58.  https://doi.org/10.1002/anie.200300573.CrossRefGoogle Scholar
  20. 20.
    Sharpless KB, Lauer RF, Teranishi AY. Electrophilic and nucleophilic organoselenium reagents. New routes to .alpha.,.beta.-unsaturated carbonyl compounds. J. Am. Chem Soc. 1973;95(18):6137–9.  https://doi.org/10.1021/ja00799a062.CrossRefGoogle Scholar
  21. 21.
    Belcastro M, Marino T, Russo N, Toscano M. Interaction of cysteine with Cu2+ and group IIb (Zn2+, Cd2+, Hg2+) metal cations: a theoretical study. J Mass Spectrom. 2005;40(3):300–6.  https://doi.org/10.1002/jms.755.CrossRefGoogle Scholar
  22. 22.
    Aaseth J, Gerhardsson L, Skaug MA, Alexander J. General chemistry of metal toxicity and basis for metal complexation. In: Aaseth J, Crisponi G, Andersen O, editors. Chelation therapy in the treatment of metal intoxication. Boston: Academic Press; 2016.Google Scholar
  23. 23.
    Plateau P, Saveanu C, Lestini R, Dauplais M, Decourty L, Jacquier A, et al. Exposure to selenomethionine causes selenocysteine misincorporation and protein aggregation in Saccharomyces cerevisiae. Sci Rep. 2017;7:44761.  https://doi.org/10.1038/srep44761.
  24. 24.
    Lazard M, Dauplais M, Blanquet S, Plateau P. Recent advances in the mechanism of selenoamino acids toxicity in eukaryotic cells. Biomol Concepts. 2017;24;8(2):93–104.  https://doi.org/10.1515/bmc-2017-0007.Google Scholar
  25. 25.
    Avery CJ, Hoffmann RP. Selenium, selenoproteins, and immunity. Nutrients. 2018;10(9).  https://doi.org/10.3390/nu10091203.
  26. 26.
    Zoidis E, Seremelis I, Kontopoulos N, Danezis GP. Selenium-dependent antioxidant enzymes: actions and properties of selenoproteins. Antioxidants (Basel). 2018;7(5):66.  https://doi.org/10.3390/antiox7050066.CrossRefGoogle Scholar
  27. 27.
    Hatfield DL, Gladyshev VN. How selenium has altered our understanding of the genetic code. Mol Cel Biol. 2002;22(11):3565–76.  https://doi.org/10.1128/mcb.22.11.3565-3576.2002.CrossRefGoogle Scholar
  28. 28.
    Ma Q. Role of Nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol. 2013;53:401–26.  https://doi.org/10.1146/annurev-pharmtox-011112-140320.CrossRefGoogle Scholar
  29. 29.
    Mills GC. Hemoglobin catabolism: I. Glutathione peroxidase, an erythrocyte enzyme which protects hemoglobin from oxidative breakdown. J Biol Chem. 1957;229(1):189–97.Google Scholar
  30. 30.
    Bhabak KP, Mugesh G. Synthetic mimics of selenoproteins. In: Liu J, Luo G, Mu Y, editors. Selenoproteins and mimics. Berlin: Springer; 2011.CrossRefGoogle Scholar
  31. 31.
    Gladyshev V, Hatfield DL. Selenocysteine-containing proteins in mammals. J Biomed Sci. 1999;6(3):151–60.CrossRefGoogle Scholar
  32. 32.
    Fairweather-Tait S, Berry R, Hurst R. Selenium bioavailability: current knowledge and future research requirements. Am J Clin Nutr. 2010;91(5):1484S–91S.  https://doi.org/10.3945/ajcn.2010.28674J.CrossRefGoogle Scholar
  33. 33.
    Shiobara Y, Ogra Y, Suzuki KT. Exchange of endogenous selenium for dietary selenium as 82Se-enriched selenite in brain, liver, kidneys and testes. Life Sci. 2000;67(25):3041–9.  https://doi.org/10.1016/S0024-3205(00)00894-8.CrossRefGoogle Scholar
  34. 34.
    Ganther HE. Reduction of the selenotrisulfide derivative of glutathione to a persulfide analog by gluthathione reductase. Biochemistry. 1971;10(22):4089–98.  https://doi.org/10.1021/bi00798a013.CrossRefGoogle Scholar
  35. 35.
    Högberg J, Alexander JAN. Selenium. In: Nordberg GF, Fowler BA, Nordberg M, Friberg LT, editors. Handbook on the toxicology of metals. Third ed. Burlington: Academic Press; 2007.Google Scholar
  36. 36.
    Ali W, Álvarez-Pérez M, Domínguez-Álvarez E, Handzlik J, Marc MA, Salardón-Jiménez N. The anticancer and chemopreventive activity of selenocyanate-containing compounds. CPR. 2018;481:468–81.  https://doi.org/10.1007/s40495-018-0160-3.Google Scholar
  37. 37.
    Álvarez-Pérez M, Ali W, Marć MA, Handzlik J, Domínguez-Álvarez E. Selenides and diselenides: a review of their anticancer and chemopreventive activity. Molecules (Basel, Switzerland). 2018;23(3):628.  https://doi.org/10.3390/molecules23030628.
  38. 38.
    Yin J, Wang B, Zhu X, Qu X, Huang Y, Lv S, et al. The small glutathione peroxidase mimic 5P may represent a new strategy for the treatment of liver cancer. Molecules (Basel, Switzerland). 2017;22(9):1495.  https://doi.org/10.3390/molecules22091495.CrossRefGoogle Scholar
  39. 39.
    Müller A, Cadenas E, Graf P, Sies H. A novel biologically active seleno-organic compound—1: glutathione peroxidase-like activity in vitro and antioxidant capacity of PZ 51 (Ebselen). Biochem Pharmacol. 1984;33(20):3235–9.  https://doi.org/10.1016/0006-2952(84)90083-2.CrossRefGoogle Scholar
  40. 40.
    Wendel A, Fausel M, Safayhi H, Tiegs G, Otter R. A novel biologically active seleno-organic compound—II: activity of PZ 51 in relation to glutathione peroxidase. Biochem Pharmacol. 1984;33(20):3241–5.  https://doi.org/10.1016/0006-2952(84)90084-4.CrossRefGoogle Scholar
  41. 41.
    Kade IJ, Balogun BD, Rocha JBT. In vitro glutathione peroxidase mimicry of ebselen is linked to its oxidation of critical thiols on key cerebral suphydryl proteins—a novel component of its GPx-mimic antioxidant mechanism emerging from its thiol-modulated toxicology and pharmacology. Chem Biol Interact. 2013;206(1):27–36.  https://doi.org/10.1016/j.cbi.2013.07.014.CrossRefGoogle Scholar
  42. 42.
    Azad G, Tomar R. Ebselen, a promising antioxidant drug: mechanisms of action and targets of biological pathways. Mol Biol Rep. 2014;41(8):4865–79.  https://doi.org/10.1007/s11033-014-3417-x.CrossRefGoogle Scholar
  43. 43.
    •• Yamashita Y, Yamashita M. Identification of a novel selenium-containing compound, selenoneine, as the predominant chemical form of organic selenium in the blood of bluefin tuna. J Biol Chem. 2010;285(24):18134–8.  https://doi.org/10.1074/jbc.C110.106377. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  44. 44.
    •• Yamashita Y, Yabu T, Yamashita M. Discovery of the strong antioxidant selenoneine in tuna and selenium redox metabolism. World J Biol Chem. 2010;1(5):144–50.  https://doi.org/10.4331/wjbc.v1.i5.144.
  45. 45.
    • Hagmar L, Persson-Moschos M, Akesson B, Schutz A. Plasma levels of selenium, selenoprotein P and glutathione peroxidase and their correlations to fish intake and serum levels of thyrotropin and thyroid hormones: a study on Latvian fish consumers. Eur J Clin Nutr. 1998;52(11):796–800.  https://doi.org/10.1007/0-306-47466-2_74. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  46. 46.
    Jacob C. A scent of therapy: pharmacological implications of natural products containing redox-active sulfur atoms. Nat Prod Rep. 2006;23(6):851–63.  https://doi.org/10.1039/b609523m.CrossRefGoogle Scholar
  47. 47.
    • Song H, Leninger M, Lee N, Liu P. Regioselectivity of the oxidative C-S bond formation in ergothioneine and ovothiol biosyntheses. Org Lett. 2013;15(18):4854–7.  https://doi.org/10.1021/ol402275t. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  48. 48.
    Paul BD, Snyder SH. The unusual amino acid L-ergothioneine is a physiologic cytoprotectant. Cell Death Differ. 2010;17(7):1134–40.  https://doi.org/10.1038/cdd.2009.163.CrossRefGoogle Scholar
  49. 49.
    Avendaño C, Menéndez JC. Chapter 13—cancer chemoprevention. In: Avendaño C, Menéndez JC, editors. Medicinal chemistry of anticancer drugs. Amsterdam: Elsevier; 2008. p. 417–29.CrossRefGoogle Scholar
  50. 50.
    Xiao L, Zhao L, Li T, Hartle DK, Aruoma OI, Taylor EW. Activity of the dietary antioxidant ergothioneine in a virus gene-based assay for inhibitors of HIV transcription. BioFactors. 2006;27(1–4):157–65.  https://doi.org/10.1002/biof.5520270114.CrossRefGoogle Scholar
  51. 51.
    Health NIo. Dietary Supplement Fact Sheet: Selenium. 2009. http://ods.od.nih.gov/factsheets/selenium.asp.
  52. 52.
    •• T. Seko K. Ishihara, Y. Yamashita, M. Yamashita. Antioxidative effects of selenium containing imidazole compound, selenoneine, on human leukemic K562 cells. 2018:13–15. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative. Google Scholar
  53. 53.
    Khan MAK, Wang F. Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environ Toxicol Chem. 2009;28(8):1567–77.  https://doi.org/10.1897/08-375.1.CrossRefGoogle Scholar
  54. 54.
    Carocci A, Rovito N, Sinicropi MS, Genchi G. Mercury toxicity and neurodegenerative effects. Rev Environ Contam Toxicol. 2014;229:1–18.  https://doi.org/10.1007/978-3-319-03777-6_1.Google Scholar
  55. 55.
    Stadtman TC. Selenium-dependent enzymes. Annu Rev Biochem. 1980;49:93–110.  https://doi.org/10.1146/annurev.bi.49.070180.000521.CrossRefGoogle Scholar
  56. 56.
    •• Yamashita M, Yamashita Y, Ando T, Wakamiya J, Akiba S. Identification and determination of selenoneine, 2-selenyl-N α, N α, N α-trimethyl-L-histidine, as the major organic selenium in blood cells in a fish-eating population on remote Japanese Islands. Biol Trace Elem Res. 2013;156(1–3):36–44.  https://doi.org/10.1007/s12011-013-9846-x. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  57. 57.
    •• Yamashita M, Yamashita Y, Suzuki T, Kani Y, Mizusawa N, Imamura S, et al. Selenoneine, a novel selenium-containing compound, mediates detoxification mechanisms against methylmercury accumulation and toxicity in zebrafish embryo. Mar Biotechnol (NY). 2013;15(5):559–70.  https://doi.org/10.1007/s10126-013-9508-1. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  58. 58.
    •• Masuda J, Umemura C, Yokozawa M, Yamauchi K, Seko T, Yamashita M, et al. Dietary supplementation of selenoneine-containing tuna dark muscle extract effectively reduces pathology of experimental colorectal cancers in mice. Nutrients. 2018;10(10):1380.  https://doi.org/10.3390/nu10101380. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  59. 59.
    Masuda J, Takayama E, Strober W, Satoh A, Morimoto Y, Honjo Y, et al. Tumor growth limited to subcutaneous site vs tumor growth in pulmonary site exhibit differential effects on systemic immunities. Oncol Rep. 2017;38(1):449–55.  https://doi.org/10.3892/or.2017.5646.CrossRefGoogle Scholar
  60. 60.
    Masuda J, Shigehiro T, Matsumoto T, Satoh A, Mizutani A, Umemura C, et al. Cytokine expression and macrophage localization in xenograft and allograft tumor models stimulated with lipopolysaccharide. Int J Mol Sci. 2018;19(4).  https://doi.org/10.3390/ijms19041261.
  61. 61.
    Ostrand-Rosenberg S, Sinha P, Beury DW, Clements VK. Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol. 2012;22(4):275–81.  https://doi.org/10.1016/j.semcancer.2012.01.011.CrossRefGoogle Scholar
  62. 62.
    Corzo CA, Cotter MJ, Cheng P, Cheng F, Kusmartsev S, Sotomayor E, et al. Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol. 2009;182(9):5693–701.  https://doi.org/10.4049/jimmunol.0900092.
  63. 63.
    Pariagh SMTasker KH Fry F, Holme AA Collins C, Okarter N et al. Asymmetric organotellurides as potent antioxidants and building blocks of protein conjugates 2005.Google Scholar
  64. 64.
    •• Yamashita Y, Amlund H, Suzuki T, Hara T, Hossain MA, Yabu T, et al. Selenoneine, total selenium, and total mercury content in the muscle of fishes. Fish Sci. 2011;77(4):679–86.  https://doi.org/10.1007/s12562-011-0360-9. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  65. 65.
    Suzuki T, Hongo T, Ohba T, Kobayashi K, Imai H, Ishida H, et al. The relation of dietary selenium to erythrocyte and plasma selenium concentrations in Japanese college women. Nutr Res. 1989;9(8):839–48.  https://doi.org/10.1016/S0271-5317(89)80029-6.
  66. 66.
    Rayman MP, Infante HG, Sargent M. Food-chain selenium and human health: spotlight on speciation. Br J Nutr. 2008;100(2):238–53.  https://doi.org/10.1017/S0007114508922522.Google Scholar
  67. 67.
    Alfthan G, Aro A, Arvilommi H, Huttunen JK. Selenium metabolism and platelet glutathione peroxidase activity in healthy Finnish men: effects of selenium yeast, selenite, and selenate. Am J Clin Nutr. 1991;53(1):120–5.  https://doi.org/10.1093/ajcn/53.1.120.CrossRefGoogle Scholar
  68. 68.
    Fox TE, Atherton C, Dainty JR, Lewis DJ, Langford NJ, Baxter MJ, et al. Absorption of selenium from wheat, garlic, and cod intrinsically labeled with Se-77 and Se-82 stable isotopes. Int J Vitam Nutr Res. 2005;75(3):179–86.  https://doi.org/10.1024/0300-9831.75.3.179.CrossRefGoogle Scholar
  69. 69.
    •• Pluskal T, Ueno M, Yanagida M. Genetic and metabolomic dissection of the ergothioneine and selenoneine biosynthetic pathway in the fission yeast, S. pombe, and construction of an overproduction system. PloS one. 2014:9(5):e97774-e.  https://doi.org/10.1371/journal.pone.0097774. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative.
  70. 70.
    •• Turrini NG, Kroepfl N, Jensen KB, Reiter TC, Francesconi KA, Schwerdtle T, et al. Biosynthesis and isolation of selenoneine from genetically modified fission yeast. Metallomics. 2018;10(10):1532–8.  https://doi.org/10.1039/c8mt00200b. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative
  71. 71.
    •• Li Wei LY, Xiong Xiaohui, Li Fangshi, Wei Ping (李壹, 刘媛媛, 熊晓辉, 李方实, 韦萍), inventor Nanjing Tech University (南京工业大学), assignee. Chemical synthesis method of novel natural antioxidant selenoneine China 2014. The following references were highlighted due to their important contribution to the discovery of selenoneine and the prime scientific investigations that have added up to the current knowledge surrounding this selenium derivative. Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Rama Alhasan
    • 1
  • Muhammad Jawad Nasim
    • 1
  • Claus Jacob
    • 1
  • Caroline Gaucher
    • 2
    Email author
  1. 1.Division of Bioorganic Chemistry, School of PharmacySaarland UniversitySaarbrueckenGermany
  2. 2.Université de Lorraine, CITHEFORNancyFrance

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