Selenium metabolism in cancer cells: The combined application of XAS and XFM techniques to the problem of selenium speciation in biological systems

Nutrients

Volumn 5, Issue 5, 2013, Pages 1734-1756

  Weekley, Claire M ^a   Aitken, Jade B ^b   Finney, Lydia ^c   Vogt, Stefan ^c   Witting, Paul K ^d   Harris, Hugh H ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cancer; SDS PAGE; Selenium; Selenoproteins; XAS; XFM

Indexed keywords

COPPER; SELENITE; SELENIUM; SELENOCYSTEINE; SELENOMETHIONINE;

BULK DENSITY; CANCER CELL; CELL COMPARTMENTALIZATION; CELL LYSATE; CELL SEPARATION; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); HUMAN; METABOLISM; METABOLITE; QUALITATIVE ANALYSIS; REVIEW; STRUCTURE ANALYSIS; X RAY ABSORPTION SPECTROSCOPY; X RAY FLUORESCENCE;

EID: 84878190676     PISSN: 20726643     EISSN: None     Source Type: Journal    
DOI: 10.3390/nu5051734     Document Type: Review

References (86)

1. 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.; Gross, E.G. et al. Effects of selenium supplementation for cancer prevention in patients with carcinoma of the skin. A randomized controlled trial. JAMA 1996, 276, 1957-1963.
2. Rayman, M.P. Selenium and human health. Lancet 2012, 379, 1256-1268.
3. Ganther, H.E. Selenotrisulfides Formation by the reaction of thiols with selenious acid. Biochemistry 1968, 7, 2898-2905.
4. Reeves, M.A.; Hoffmann, P.R. The human selenoproteome: Recent insights into functions and regulation. Cell. Mol. Life Sci. 2009, 66, 2457-2478.
5. Ganther, H.E. Reduction of the selenotrisulfide derivative of glutathione to a persulfide analog by glutathione reductase. Biochemistry 1971, 10, 4089-4098.
6. Hsieh, H.S.; Ganther, H.E. Acid-volatile selenium formation catalyzed by glutathione reductase. Biochemistry 1975, 14, 1632-1636.
7. Kumar, S.; Björnstedt, M.; Holmgren, A. Selenite is a substrate for calf thymus thioredoxin reductase and thioredoxin and elicits a large non-stoichiometric oxidation of NADPH in the presence of oxygen. Eur. J. Biochem. 1992, 207, 435-439.
8. Wallenberg, M.; Olm, E.; Hebert, C.; Björnstedt, M.; Fernandes, A.P. Selenium compounds are substrates for glutaredoxins: A novel pathway for selenium metabolism and a potential mechanism for selenium-mediated cytotoxicity. Biochem. J. 2010, 429, 85-93.
9. Braga, P.; Montes-Bayón, M.; Alvarez, J.; López, J.M.; Sanz-Medel, A. Characterization, biological interactions and in-vivo detection of selenotrisulfide derivatives of glutathion, cysteine and homocysteine by HPLC-ICP-MS. J. Anal. At. Spectrom. 2004, 19, 1128-1133.
10. Hatfield, D.L.; Yoo, M.-H.; Carlson, B.A.; Gladyshev, V.N. Selenoproteins that function in cancer prevention and promotion. Biochim. Biophys. Acta Gen. Subj. 2009, 1790, 1541-1545.
11. Gabel-Jensen, C.; Gammelgaard, B.; Bendahl, L.; Stürup, S.; Jøns, O. Separation and identification of selenotrisulfides in epithelial cell homogenates by LC-ICP-MS and LC-ESI-MS after incubation with selenite. Anal. Bioanal. Chem. 2006, 384, 697-702.
12. Irons, R.; Carlson, B.A.; Hatfield, D.L.; Davis, C.D. Both selenoproteins and low molecular weight selenocompounds reduce colon cancer risk in mice with genetically impaired selenoprotein expression. J. Nutr. 2006, 136, 1311-1317.
13. Lunøe, K.; Gabel-Jensen, C.; Stürup, S.; Andresen, L.; Skov, S.; Gammelgaard, B. Investigation of the selenium metabolism in cancer cell lines. Metallomics 2011, 3, 162-168.
14. Duffield-Lillico, A.J.; Reid, M.E.; Turnbull, B.W.; Combs, G.F., Jr.; Slate, E.H.; Fischbach, L.A.; Marshall, J.R.; Clark, L.C. Baseline characteristics and the effect of selenium supplementation on cancer incidence in a randomized clinical trial: A summary report of the Nutritional Prevention of Cancer Trial. Cancer Epidemiol. Biomark. Prev. 2002, 11, 630-639.
15. Duffield-Lillico, A.J.; Dalkin, B.L.; Reid, M.E.; Turnbull, B.W.; Slate, E.H.; Jacobs, E.T.; Marshall, J.R.; Clark, L.C. Selenium supplementation, baseline plasma selenium status and incidence of prostate cancer: An analysis of the complete treatment period of the Nutritional Prevention of Cancer Trial. BJU Int. 2003, 91, 608-612.
16. Esaki, N.; Nakamura, T.; Tanaka, H.; Soda, K. Selenocysteine lyase, a novel enzyme that specifically acts on selenocysteine. Mammalian distribution and purification and properties of pig liver enzyme. J. Biol. Chem. 1982, 257, 4386-4391.
17. Lippman, S.M.; Goodman, P.J.; Klein, E.A.; Parnes, H.L.; Thompson, I.M.; Kristal, A.R.; Santella, R.M.; Probstfield, J.L.; Moinpour, C.M.; Albanes, D. et al. Designing the Selenium and Vitamin E Cancer Prevention Trial (SELECT). J. Natl. Cancer Inst. 2005, 97, 94-102.
18. Butler, J.A.; Beilstein, M.A.; Whanger, P.D. Influence of dietary methionine on the metabolism of selenomethionine in rats. J. Nutr. 1989, 119, 1001-1009.
19. Lippman, S.M.; Klein, E.A.; Goodman, P.J.; Lucia, M.S.; Thompson, I.M.; Ford, L.G.; Parnes, H.L.; Minasian L.M.; Gaziano, J.M.; Hartline, J.A. et al. Effect of selenium and vitamin e on risk of prostate cancer and other cancers: The Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA 2009, 301, 39-51.
20. Okuno, T.; Kubota, T.; Kuroda, T.; Ueno, H.; Nakamuro, K. Contribution of enzymic alpha, gamma-elimination reaction in detoxification pathway of selenomethionine in mouse liver. Toxicol. Appl. Pharmacol. 2001, 176, 18-23.
21. Klein, E.A. Selenium and Vitamin E: Interesting Biology and Dashed Hope. J. Natl. Cancer Inst. 2009, 101, 283-285.
22. Suzuki, K.T.; Kurasaki, K.; Suzuki, N. Selenocysteine beta-lyase and methylselenol demethylase in the metabolism of Se-methylated selenocompounds into selenide. Biochim. Biophys. Acta Gen. Subj. 2007, 1770, 1053-1061.
23. Rayman, M.P.; Combs, G.F., Jr.; Waters, D.J. Selenium and vitamin E supplementation for cancer prevention. JAMA 2009, 301, 1876.
24. Hatfield, D.L.; Gladyshev, V.N. The outcome of Selenium and Vitamin E Cancer Prevention Trial (SELECT) reveals the need for better understanding of selenium biology. Mol. Interv. 2009, 9, 18-21.
25. Goossens, M.E.; Buntinx, F.; Zeegers, M.P. Re: Selenium and Vitamin E: Interesting biology and dashed hope. J. Natl. Cancer Inst. 2009, 101, 1363-1364.
26. Ganther, H.E.; Lawrence, J.R. Chemical transformations of selenium in living organisms. Improved forms of selenium for cancer prevention. Tetrahedron 1997, 53, 12299-12310.
27. Bird, S.M.; Uden, P.C.; Tyson, J.F.; Block, E.; Denoyer, E. Speciation of selenoamino acids and organoselenium compounds in selenium-enriched yeast using high-performance liquid chromatography-inductively coupled plasma mass spectrometry. J. Anal. At. Spectrom. 1997, 12, 785-788.
28. Uden, P.C.; Boakye, H.T.; Kahakachchi, C.L.; Hafezi, R.; Nolibos, P.; Block, E.; Johnson, S.; Tyson, J.F. Element selective characterization of stability and reactivity of selenium species in selenized yeast. J. Anal. At. Spectrom. 2004, 19, 65-73.
29. Larsen, E.H.; Hansen, M.; Paulin, H.; Moesgaard, S.; Reid, M.; Rayman, M. Speciation and bioavailability of selenium in yeast-based intervention agents used in cancer chemoprevention studies. J. AOAC Int. 2004, 87, 225-232.
30. Rayman, M.P.; Infante, H.G.; Sargent, M. Food-chain selenium and human health: Spotlight on speciation. Br. J. Nutr. 2008, 100, 238-253.
31. Tsuji, Y.; Suzuki, N.; Suzuki, K.T.; Ogra, Y. Selenium metabolism in rats with long-term ingestion of Se-methylselenocysteine using enriched stable isotopes. J. Toxicol. Sci. 2009, 34, 191-200.
32. Ogra, Y.; Anan, Y. Selenometabolomics: Identification of selenometabolites and specification of their biological significance by complementary use of elemental and molecular mass spectrometry. J. Anal. At. Spectrom. 2009, 24, 1477-1488.
33. Gammelgaard, B.; Jackson, M.I.; Gabel-Jensen, C. Surveying selenium speciation from soil to cell-Forms and transformations. Anal. Bioanal. Chem. 2011, 399, 1743-1763.
34. Rayman, M.P. Selenium in cancer prevention: A review of the evidence and mechanism of action. Proc. Nutr. Soc. 2005, 64, 527-542.
35. McConnell, K.P.; Portman, O.W. Excretion of dimethyl selenide by the rat. J. Biol. Chem. 1952, 195, 277-282.
36. Sinha, R.; Unni, E.; Ganther, H.E.; Medina, D. Methylseleninic acid, a potent growth inhibitor of synchronized mouse mammary epithelial tumor cells in vitro. Biochem. Pharmacol. 2001, 61, 311-317.
37. Byard, J.L. Trimethyl selenide. A urinary metabolite of selenite. Arch. Biochem. Biophys. 1969, 130, 556-560.
38. Infante, H.G.; Joel, S.P.; Warburton, E.; Hopley, C.; Hearn, R.; Jüliger, S. Investigation of the selenium species distribution in a human B-cell lymphoma line by HPLC-and GC-ICP-MS in combination with HPLC-ESIMS/MS and GC-TOFMS after incubation with methylseleninic acid. J. Anal. At. Spectrom. 2007, 22, 888-896.
39. Ogra, Y.; Ishiwata, K.; Takayama, H.; Aimi, N.; Suzuki, K.T. Identification of a novel selenium metabolite, Se-methyl-N-acetylselenohexosamine, in rat urine by high-performance liquid chromatography-Inductively coupled plasma mass spectrometry and-Electrospray ionization tandem mass spectrometry. J. Chromatogr. B 2002, 767, 301-312.
40. Francesconi, K.A.; Pannier, F. Selenium metabolites in urine: A critical overview of past work and current status. Clin. Chem. 2004, 50, 2240-2253.
41. Ohta, Y.; Suzuki, K.T. Methylation and demethylation of intermediates selenide and methylselenol in the metabolism of selenium. Toxicol. Appl. Pharmacol. 2008, 226, 169-177.
42. Jacob, C.; Giles, G.; Giles, N.; Sies, H. Sulfur and selenium: The role of oxidation state in protein structure and function. Angew. Chem. Int. Ed. 2003, 42, 4742-4758.
43. Poatajko, A.; Jakubowski, N.; Szpunar, J. State of the art report of selenium speciation in biological samples. J. Anal. At. Spectrom. 2006, 21, 639.
44. Suzuki, K.T.; Ohta, Y.; Suzuki, N. Availability and metabolism of 77Se-methylseleninic acid compared simultaneously with those of three related selenocompounds. Toxicol. Appl. Pharmacol. 2006, 217, 51-62.
45. Gammelgaard, B.; Gabel-Jensen, C.; Stürup, S.; Hansen, H.R. Complementary use of molecular and element-specific mass spectrometry for identification of selenium compounds related to human selenium metabolism. Anal. Bioanal. Chem. 2008, 390, 1691-1706.
46. Ip, C.; Thompson, H.; Zhu, Z.; Ganther, H.E. In vitro and in vivo studies of methylseleninic acid: Evidence that a monomethylated selenium metabolite is critical for cancer chemoprevention. Cancer Res. 2000, 60, 2882-2886.
47. B'Hymer, C.; Caruso, J.A. Selenium speciation analysis using inductively coupled plasma-mass spectrometry. J. Chromatogr. A 2006, 1114, 1-20.
48. Aitken, J.B.; Levina, A.; Lay, P.A. Studies on the biotransformations and biodistributions of metal-containing drugs using X-ray absorption spectroscopy. Curr. Top. Med. Chem. 2011, 11, 553-571.
49. George, G.N.; Hedman, B.; Hodgson, K.O. An edge with XAS. Nat. Struct. Biol. 1998, 5, 645-647.
50. Nakazawa, E.; Ikemoto, T.; Hokura, A.; Terada, Y.; Kunito, T.; Yamamoto, T.; Yamada, T.K.; Rosas, F.C.W.; Fillmann, G.; Tanabe, S.; Nakai, I. Silver speciation in liver of marine mammals by synchrotron X-ray absorption fine structure and X-ray fluorescence spectroscopies. J. Environ. Monit. 2011, 13, 1678.
51. Korbas, M.; O'Donoghue, J.L.; Watson, G.E.; Pickering, I.J.; Singh, S.P.; Myers, G.J.; Clarkson, T.W.; George, G.N. The chemical nature of mercury in human brain following poisoning or environmental exposure. ACS Chem. Neurosci. 2010, 1, 810-818.
52. Esaki, N.; Nakamura, T.; Tanaka, H.; Suzuki, T.; Morino, Y.; Soda, K. Enzymatic synthesis of selenocysteine in rat liver. Biochemistry 1981, 20, 4492-4496.
53. Ortega, R.; Carmona, A.; Llorens, I.; Solari, P.L. X-ray absorption spectroscopy of biological samples. A tutorial. J. Anal. At. Spectrom. 2012, 27, 2054.
54. Pickering, I.J.; George, G.N.; van Fleet-Stalder, V.; Chasteen, T.G.; Prince, R.C. X-ray absorption spectroscopy of selenium-containing amino acids. J. Biol. Inorg. Chem. 1999, 4, 791-794.
55. George, G.N.; Pickering, I.J.; Pushie, M.J.; Nienaber, K.; Hackett, M.J.; Ascone, I.; Hedman, B.; Hodgson, K.O.; Aitken, J.B.; Levina, A. et al. X-ray-induced photo-chemistry and X-ray absorption spectroscopy of biological samples. J. Synchrotron Radiat. 2012, 19, 875-886.
56. Wang, H.C.; Riahi, M.; Pothen, J.; Bayse, C.A.; Riggs-Gelasco, P.; Brumaghim, J.L. Interactions of Cu(I) with selenium-containing amino acids determined by NMR, XAS, and DFT studies. Inorg. Chem. 2011, 50, 10893-10900.
57. Yu-Feng, L.; Xiaoyan, W.; Liming, W.; Bai, L.; Yuxi, G.; Chunying, C. Direct quantitative speciation of selenium in selenium-enriched yeast and yeast-based products by X-ray absorption spectroscopy confirmed by HPLC-ICP-MS. J. Anal. At. Spectrom. 2010, 25, 426-430.
58. Aitken, J.B.; Lay, P.A.; Duong, T.T.; Aran, R.; Witting, P.K.; Harris, H.H.; Lai, B.; Vogt, S.; Giles, G.I. Synchrotron radiation induced X-ray emission studies of the antioxidant mechanism of the organoselenium drug ebselen. J. Biol. Inorg. Chem. 2012, 1-10.
59. Kehr, S.; Malinouski, M.; Finney, L.A.; Vogt, S.; Labunskyy, V.M.; Kasaikina, M.V.; Carlson, B.A.; Zhou, Y.; Hatfield, D.L.; Gladyshev, V.N. X-ray fluorescence microscopy reveals the role of selenium in spermatogenesis. J. Mol. Biol. 2009, 389, 808-818.
60. Malinouski, M.; Kehr, S.; Finney, L.A.; Vogt, S.; Carlson, B.A.; Seravalli, J.; Jin, R.; Handy, D.E.; Park, T.J.; Loscalzo, J. et al. High-resolution imaging of selenium in kidneys: A localized selenium pool associated with glutathione peroxidase 3. Antioxid. Redox Signal. 2012, 16, 185-192.
61. Suzuki, K.T.; Doi, C.; Suzuki, N. Metabolism of Se-76-methylselenocysteine compared with that of Se-77-selenomethionine and Se-82-selenite. Toxicol. Appl. Pharmacol. 2006, 217, 185-195.
62. Chen, T.; Wong, Y.-S. Selenocystine induces reactive oxygen species-mediated apoptosis in human cancer cells. Biomed. Pharmacother. 2009, 63, 105-113.
63. Weekley, C.M.; Aitken, J.B.; Vogt, S.; Finney, L.A.; Paterson, D.J.; de Jonge, M.D.; Howard, D.L.; Musgrave, I.F.; Harris, H.H. Uptake, distribution, and speciation of selenoamino acids by human cancer cells: X-ray absorption and fluorescence methods. Biochemistry 2011, 50, 1641-1650.
64. Weekley, C.M.; Aitken, J.B.; Vogt, S.; Finney, L.A.; Paterson, D.J.; de Jonge, M.D.; Howard, D.L.; Witting, P.K.; Musgrave, I.F.; Harris, H.H. Metabolism of selenite in human lung cancer cells: X-ray absorption and fluorescence studies. J. Am. Chem. Soc. 2011, 133, 18272-18279.
65. Gabel-Jensen, C.; Bak, S.A.; Lauritsen, F.R.; Hansen, H.R.; Badolo, L.; Gammelgaard, B. In situ identification of dimethyl diselenide in hepatocytes treated with methylseleninic acid by membrane inlet mass spectrometry. J. Anal. At. Spectrom. 2009, 24, 949-952.
66. Hackett, M.J.; McQuillan, J.A.; El-Assaad, F.; Aitken, J.B.; Levina, A.; Cohen, D.D.; Siegele, R.; Carter, E.A.; Grau, G.E.; Hunt, N.H.; Lay, P.A. Chemical alterations to murine brain tissue induced by formalin fixation: implications for biospectroscopic imaging and mapping studies of disease pathogenesis. Analyst 2011, 136, 2941-2952.
67. Shen, C.L.; Song, W.; Pence, B.C. Interactions of selenium compounds with other antioxidants in DNA damage and apoptosis in human normal keratinocytes. Cancer Epidemiol. Biomark. Prev. 2001, 10, 385-390.
68. Kezhou, W.; Stowe, H.D.; House, A.M.; Chou, K.; Thiel, T. Comparison of cupric and sulfate ion effects on chronic selenosis in rats. J. Anim. Sci. 1987, 64, 1467-1475.
69. Fahrni, C. Biological applications of X-ray fluorescence microscopy: Exploring the subcellular topography and speciation of transition metals. Curr. Opin. Chem. Biol. 2007, 11, 121-127.
70. Misra, S.; Peak, D.; Niyogi, S. Application of XANES spectroscopy in understanding the metabolism of selenium in isolated rainbow trout hepatocytes: Insights into selenium toxicity. Metallomics 2010, 2, 710-717.
71. Misra, S.; Peak, D.; Chen, N.; Hamilton, C.; Niyogi, S. Tissue-specific accumulation and speciation of selenium in rainbow trout (Oncorhynchus mykiss) exposed to elevated dietary selenomethionine. Comp. Biochem. Phys. C 2012, 155, 560-565.
72. Shanu, A.; Groebler, L.; Kim, H.B.; Wood, S.; Weekley, C.M.; Aitken, J.B.; Harris, H.H.; Witting, P.K. Selenium inhibits renal oxidation and inflammation but not acute kidney injury in an animal model of rhabdomyolysis. Antioxid. Redox Signal. 2013, 18, 756-769.
73. Harris, H.H.; Levina, A.; Dillon, C.T.; Mulyani, I.; Lai, B.; Cai, Z.; Lay, P.A. Time-dependent uptake, distribution and biotransformation of chromium (VI) in individual and bulk human lung cells: application of synchrotron radiation techniques. J. Biol. Inorg. Chem. 2005, 10, 105-118.
74. Weekley, C.M.; Aitken, J.B.; Musgrave, I.F.; Harris, H.H. Methylselenocysteine treatment leads to diselenide formation in human cancer cells: Evidence from X-ray absorption spectroscopy studies. Biochemistry 2012, 51, 736-738.
75. Weekley, C.M. School of Chemistry and Physics, The University of Adelaide, Adelaide, Australia. Unpublished work, 2013.
76. Spallholz, J.E.; Shriver, B.J.; Reid, T.W. Dimethyldiselenide and methylseleninic acid generate superoxide in an in vitro chemiluminescence assay in the presence of glutathione: Implications for the anticarcinogenic activity of L-selenomethionine and L-Se-methylselenocysteine. Nutr. Cancer 2001, 40, 34-41.
77. Huber, R.E.; Criddle, R.S. Comparison of the chemical properties of selenocysteine and selenocystine with their sulfur analogs. Arch. Biochem. Biophys. 1967, 122, 164-173.
78. Gabel-Jensen, C.; Gammelgaard, B. Selenium metabolism in hepatocytes incubated with selenite, selenate, selenomethionine, Se-methylselenocysteine and methylseleninc acid and analysed by LC-ICP-MS. J. Anal. At. Spectrom. 2010, 25, 414-418.
79. Shen, H.M.; Yang, C.F.; Ding, W.X.; Liu, J.; Ong, C.N. Superoxide radical-initiated apoptotic signalling pathway in selenite-treated HepG(2) cells: Mitochondria serve as the main target. Free Radic. Biol. Med. 2001, 30, 9-21.
80. Xiang, N.; Zhao, R.; Zhong, W. Sodium selenite induces apoptosis by generation of superoxide via the mitochondrial-dependent pathway in human prostate cancer cells. Cancer Chemother. Pharmacol. 2009, 63, 351-362.
81. Finney, L.A.; Chishti, Y.; Khare, T.; Giometti, C.; Levina, A.; Lay, P.A.; Vogt, S. Imaging metals in proteins by combining electrophoresis with rapid X-ray fluorescence mapping. ACS Chem. Biol. 2010, 5, 577-587.
82. Raimunda, D.; Khare, T.; Giometti, C.; Vogt, S.; Argüello, J.M.; Finney, L.A. Identifying metalloproteins through X-ray fluorescence mapping and mass spectrometry. Metallomics 2012, 4, 921-927.
83. Vogt, S. MAPS: A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets. J. Phys. IV 2003, 104, 635-638.
84. Martínez, J.; Lisa, S.; Sánchez, R.; Kowalczyk, W.; Zurita, E.; Teixidó, M.; Giralt, E.; Andreu, D.; Avila, J.; Gasset, M. Selenomethionine incorporation into amyloid sequences regulates fibrillogenesis and toxicity. PLoS One 2011, 6, e27999.
85. Pickering, I.J.; Prince, R.C.; Salt, D.E.; George, G.N. Quantitative, chemically specific imaging of selenium transformation in plants. Proc. Natl. Acad. Sci. USA 2000, 97, 10717-10722.
86. Pickering, I.J.; Sneeden, E.Y.; Prince, R.C.; Block, E.; Harris, H.H.; Hirsch, G.; George, G.N. Localizing the chemical forms of sulfur in vivo using X-ray fluorescence spectroscopic imaging: application to onion (Allium cepa) tissues. Biochemistry 2009, 48, 6846-6853.