Abstract
Stable isotope composition varies due to different reactivity or mobility among the isotopes. Various pioneering studies revealed that isotope fractionation is common for many elements, and it is now widely recognized that the stable isotope compositions of biometals can be used as new tracers for element metabolism. In this review, we summarize the recently published isotope compositions of iron (Fe), copper (Cu), zinc (Zn), and calcium (Ca) in various biological samples, including tissues from plants, animals, and humans. Discussions were carried out with respect to age, sex, organ, and the presence or absence of particular diseases for animals and humans. For Fe and Cu isotopes, changes in oxidation states generate large isotopic fractionation through the metabolism of those elements. Isotope composition of Zn greatly fractionates among tissues even without changes in oxidation state. Isotopic composition of Ca is a powerful tracer for the metabolism of Ca in bones. The review results suggest that the stable isotope compositions of the biometals can be used as effective markers for diagnostics of various kinds of diseases related to metabolic disorders.
Similar content being viewed by others
References
R. R. Holt, J. Y. Uriu-Adams, and C. L. Keen, in “Present Knowledge in Nutrition”, ed. J. W. Erdman Jr., I. A. Macdonald, and S. H. Zeisel, 2012, Chap. 34, ILSI Press, 521–539.
S. L. Volpe, in “Present Knowledge in Nutrition”, ed. J. W. Erdman Jr., I. A. Macdonald, and S. H. Zeisel, 2012, Chap. 30, ILSI Press, 459–474.
H. Haraguchi, J. Anal. At. Spectrom., 2004, 19, 5.
H. Haraguchi, in “Metallomics; Recent Analytical Techniques and Selected Applications’”, ed. Y. Ogura and T. Hirata, 2017, Springer, 3–39.
H. G. Preuss and D. L. Clouatre, in “Present Knowledge in Nutrition”, ed. J. W. Erdman Jr., I. A. Macdonald, and S. H. Zeisel, 2012, Chap. 31, ILSI Press, 475–492.
C. M. Weaver, in “Present Knowledge in Nutrition”, ed, J. W. Erdman Jr., I. A. Macdonald, and S. H. Zeisel, 2012, Chap. 28, ILSI Press, 434–446.
Y. Mawani and C. Orvig, in “Bioinorganic Medicinal Chemistry’”, ed. E. Alessio, 2011, Chap. 11, WILEY-VCH Verlag GmbH & Co. KGaA, 307–350.
V. Mudgal, N. Madaan, A. Mudgal, R. B. Singh, and S. Mishra, Open Nutraceuticals J., 2010, 3, 94.
B. L. Beard, C. M. Johnson, L. Cox, H. Sun, K. H. Nealson, and C. Aguilar, Science, 1999, 285, 1889.
C. M. Johnson, J. L. Skulan, B. L. Beard, H. Sun, K. H. Nealson, and P. S. Braterman, EPSL, 2002, 195, 141.
X. K. Zhu, Y. Guo, R. J. P. Williams, R. K. O'Nions, A. Matthews, N. S. Belshaw, G. W. Canters, E. C. de Waal, U. Weser, B. K. Burgess, and B. Salvato, EPSL, 2002, 200, 47.
J. Bigeleisen and M. G. Mayer, J. Chem. Phys., 1947, 15, 261.
H. C. Urey, J. Chem. Soc., 1947, 562.
M. Tanimizu, Y. Sohrin, and T. Hirata, Anal. Bioanal. Chem., 2013, 405, 2771.
T. Walczyk and F. von Blanckenburg, Science, 2002, 295, 2065.
M. Guelke and F. von Blanckenburg, Environ. Sci. Technol., 2007, 41, 1896.
K. Hotz, H. Augsburgerb, and T. Walczyk, J. Anal. At. Spectrom., 2011, 26, 1347.
K. Jaouen, M-L. Pons, and V. Balter, EPSL, 2013a, 374, 164.
V. Balter, A. Lamboux, A. Zazzo, P. Télouk, Y. Leverrier, J. Marvel, A. P. Moloney, F. J. Monahan, O. Schmidt, and F. Albarède, Metallomics, 2013, 5, 1470.
T. Ohno, A. Shinohara, I. Kohge, M. Chiba, and T. Hirata, Anal. Sci., 2004, 20, 617.
T. Walczyk and F. von Blanckenburg, Int. J. Mass Spectrom., 2005, 242, 117.
P-A. Krayenbuehl, T. Walczyk, R. Schoenberg, F. von Blanckenburg, and G. Schulthess, Blood, 2005, 105, 3812.
A. Stenberg, D. Malinovsky, B. Ohlander, H. Andren, W. Forsling, L. M. Engström, A. Wahlin, E. Engström, I. Rodushkin, and D. C. Baxter, J. Trace. Elem. Med. Biol., 2005, 19, 55.
F. Albarède, P. Télouk, A. Lamboux, K. Jaouen, and V. Balter, Metallomics, 2011, 3, 926.
K. Jaouen, V. Balter, E. Herrscher, A. Lamboux, P. Télouk, and F. Albarède, Am. J. Phys. Anthropol., 2012, 148, 334.
K. Hotz, P.-A. Krayenbuehl, and T. Walczyk, J. Biol. Inorg. Chem., 2012, 17, 301.
L. Van Heghe, E. Engström, I. Rodushkin, C. Cloquet, and F. Vanhaecke, J. Anal. At. Spectrom., 2012, 27, 1327.
K. Hotz and T. Walczyk, J. Biol. Inorg. Chem., 2013, 18, 1.
L. Van Heghe, J. Delanghe, H. Van Vlierberghe, and F. Vanhaecke, Metallomics, 2013, 5, 1503.
K. Jaouen, M. Gibert, A. Lamboux, P. Télouk, F. Fourel, F. Albarède, A. N. Alekseev, E. Crubézy, and V. Balter, Metallomics, 2013b, 5, 1016.
L. Van Heghe, O. Deltombe, J. Delanghe, H. Depypere, and F. Vanhaecke, J. Anal. At. Spectrom., 2014, 29, 478.
K. Jaouen and V. Balter, Am. J. Phys. Anthropol., 2014, 153, 280.
F. von Blanckenburg, M. Oelze, D. G. Schmid, K. van Zuilen, H. P. Gschwind, A. J. Slade, S. Stitah, D. Kaufmann, and P. Swart, Metallomics, 2014, 6, 2052.
Y. Tanaka, K. Takata, T. Kawasaki, A. Shinohara, K. Ishikawa-Takata, and T. Hirata, in “Metallomics; Recent Analytical Techniques and Selected Applications”, ed. Y. Ogura and T. Hirata, 2017a, Chap. 12, Springer, 239–263.
J. C. Cikomola, M. R. Flórez, M. Costas-Rodríguez, Y. Anoshkina, K. Vandepoele, P. B. Katchunga, A. S. Kishabongo, M. M. Speeckaert, F. Vanhaecke, and J. R. Delanghe, Metallomics, 2017, 9, 1142.
Y. Anoshkina, M. Costas-Rodríguez, M. Speeckaert, W. Van Biesen, J. Delanghe, and F. Vanhaecke, Metallomics, 2017, 9, 517.
M. R. Flórez, Y. Anoshkina, M. Costas-Rodríguez, C. Grootaert, J. Van Camp, J. Delanghe, and F. Vanhaecke, J. Anal. At. Spectrom., 2017, 32, 1713.
R. Yip, in “Present Knowledge in Nutrition”, ed. B. A. Bowman and R. M. Russell, 2002, Chap. 30, ILSI Press, 311–328.
L. R. Zacharski, D. L. Ornstein, S. Woloshin, and L. M. Schwartz, Am. Heart J., 2000, 140, 98.
E. A. Liebold and B. Guo, Annu. Rev. Nutr., 1992, 12, 345.
S. Abboud and D. J. Haile, J. Biol. Chem, 2000, 275, 19906.
D. M. Frazer, S. J. Wilkins, E. M. Becker, T. L. Murphy, C. D. Vulpe, A. T. McKie, and G. J. Anderson, Gut., 2003, 52, 340.
I. de Domenico, D. M. Ward, and J. Kaplan, J. Clin. Invest., 2007, 117, 1755.
M. V. Verga Falzacappa, M. Vujic Spasic, R. Kessler, J. Stolte, M. W. Hentze, and M. U. Muckenthaler, Blood, 2007, 109, 353.
A. Pietrangelo, Hepatology, 2007, 46, 1291.
R. E. Fleming, M. C. Migas, X.Y. Zhou, J. Jiang, R. S. Britton, E. M. Brunt, S. Tomatsu, A. Waheed, B. R. Bacon, and W. S. Sly, PNAS, 1999, 96, 3143.
C. Weinstein, F. Moynier, K. Wang, R. Paniello, J. Foriel, J. Catalano, and S. Pichat, Chem. Geol., 2011, 286, 266.
D. Jouvin, D. J. Weiss, T. F. M. Mason, M. N. Bravin, P. Louvat, F. Zhao, F. Ferec, P. Hinsinger, and M. F. Benedetti, Environ. Sci. Technol., 2012, 46, 2652.
J. U. Navarrete, D. M. Borrok, M. Viveros, and J. T. Ellzey, Geochim. Cosmochim. Acta, 2011, 75, 784.
R. S. Ohgami, D. R. Campagna, A. McDonald, and M. D. Fleming, Blood, 2006, 108, 1388.
A. Tennant, A. Rauk, and M. E. Wieser, Metallomics, 2017, 9, 1809.
J. R. Prohaska, in “Present Knowledge in Nutrition”, ed. J. W. Erdman Jr., I. A. Macdonald, and S. H. Zeisel, 2012, Chap. 35, ILSI Press, 540–553.
M. Aramendía, L. Rello, M. Resano, and F. Vanhaecke, J. Anal. At. Spectrom., 2013, 28, 675.
M. Costas-Rodríguez, Y. Anoshkina, S. Lauwens, H. Van Vlierberghe, J. Delanghe, and F. Vanhaecke, Metallomics, 2015, 7, 491.
V. Balter, A. Nogueira da Costa, V. P. Bondanese, K. Jaouen, A. Lamboux, S. Sangrajrang, N. Vincent, F. Fourel, P. Télouk, M. Gigou, C. Lécuyer, P. Srivatanakul, C. Bréchot, F. Albarède, and P. Hainaut, PNAS, 2015, 112, 982.
P. Télouk, A. Puisieux, T. Fujii, V. Balter, V. P. Bondanese, A.-P. Morel, G. Clapisson, A. Lamboux, and F. Albarède, Metallomics, 2015, 7, 299.
V. P. Bondanese, A. Lamboux, M. Simon, J. E. Lafont, E. Albalat, S. Pichat, J.-M. Vanacker, P. Télouk, V. Balter, P. Oger, and F. Albarède, Metallomics, 2016, 8, 1177.
J.-L. Cadiou, S. Pichat, V. P. Bondanese, A. Soulard, T. Fujii, F. Albarède, and P. Oger, Sci. Rep., 2017, 7, 44533.
C. Coulouarn, C. Derambure, G. Lefebvre, R. Daveau, M. Hiron, M. Scotte, A. François, M. Daveau, and J.-P. Salier, J. Hepatol., 2005, 42, 860.
M. R. Flórez, M. Costas-Rodríguez, C. Grootaert, J. Van Camp, and F. Vanhaecke, Anal. Bioanal. Chem., 2018, 410, 2385.
M. Valko, D. Leibfritz, J. Moncol, M. T. Cronin, M. Mazur, and J. Telser, Int. J. Biochem. Cell Biol., 2007, 39, 44.
K. H. Brown, J. A. Rivera, Z. Bhutta, R. S. Gibson, J. C. King, B. Lönnerdal, M. T. Ruel, B. Sandtröm, E. Wasantwisut, and C. Hotz, FoodNutr. Bull., 2004, 25, S99
V. Balter, A. Zazzo, A. P. Moloney, F. Moynier, O. Schmidt, F. J. Monahan, and F. Albarède, Rapid Commun. Mass Spectrom., 2010, 24, 605.
D. J. Weiss, T. F. D. Mason, F. J. Zhao, G. J. D. Kirk, B. J. Coles, and M. S. A. Horstwood, New Phytologist, 2005, 165, 703.
F. Moynier, S. Pichat, M.-L. Pons, D. Fike, V. Balter, and F. Albarède, Chem. Geol., 2009, 267, 125.
F. Moynier, T. Fujii, A. S. Shaw, and M. Le Borgne, Metallomics, 2013, 5, 693.
R. J. Cousins, Physiol. Rev., 1985, 65, 238.
A. A. Rehman, H. Ahsan, and F. H. Khan, J. Cell Physiol., 2013, 228, 1665.
N. Dimakis, M. J. Farooqi, E. S. Garza, and G. Bunker, J. Chem. Phys., 2008, 128, 115104.
T. Ohno, A. Shinohara, M. Chiba, and T. Hirata, Anal. Sci., 2005, 21, 425.
M. Costas-Rodríguez, L. Van Heghe, and F. Vanhaecke, Metallomics, 2014, 6, 139.
A. Büchl, C. J. Hawkesworth, K. V. Ragnarsdottir, and D. R. Brown, Geochem. Trans., 2008, 9, 11.
F. Larner, L. N. Woodley, S. Shousha, A. Moyes, E. Humphreys-Williams, S. Strekopytov, A. N. Halliday, M. Rehkämper, and R. C. Coombes, Metallomics, 2015, 7, 112.
S. Alam and S. L. Kelleher, Nutrients, 2012, 4, 875.
S. C. Manolagas, Endocr. Rev., 2000, 21, 115.
J. Skulan, D. J. DePaolo, and T. Owens, Geochim. Cosmochim. Acta, 1997, 61, 2505.
M. T. Clementz, P. Holden, and P. L. Koch, Int. J. Osteoarchaeol., 2003, 13, 29.
J. Skulan and D. J. DePaolo, PNAS, 1999, 96, 13709.
T. Hirata, M. Tanoshima, A. Suga, Y. Tanaka, Y. Nagata, A. Shinohara, and M. Chiba, Anal. Sci., 2008, 24, 1501.
L. M. Reynard, G. M. Henderson, and R. E. M. Hedges, Geochim. Cosmochim. Acta, 2010, 74, 3735.
J. L. L. Morgan, J. L. Skulan, G. W. Gordon, S. J. Romaniello, S. M. Smith, and A. D. Anbar, PNAS, 2012, 109, 9989.
M. B. Channon, G. W. Gordon, J. L. L. Morgan, J. L. Skulan, S. M. Smith, and A. D. Anbar, Bone, 2015, 77, 69.
J. Skulan, T. Bullen, A. D. Anbar, J. E. Puzas, L. Shackelford, A. LeBlanc, and S. M. Smith, Clin. Chem., 2007, 53, 1155.
A. Heuser and A. Eisenhauer, Bone, 2010, 46, 889.
G. W. Gordon, J. Monge, M. B. Channon, Q. Wu, J. L. Skulan, A. D. Anbar, and R. Fonseca, Leukemia, 2014, 28, 2112.
E. Terpos, G. Morgan, M. A. Dimopoulos, M. T. Drake, S. Lentzsch, N. Raje, O. Sezer, R. García-Sanz, K. Shimizu, I. Turesson, T. Reiman, A. Jurczyszyn, G. Merlini, A. Spencer, X. Leleu, M. Cavo, N. Munshi, S. V. Rajkumar, B. G. Durie, and G. D. Roodman, J. Clin. Oncol., 2013, 31, 2347.
Y. Tanaka, N. Yajima, Y. Higuchi, H. Yamato, and T. Hirata, Metallomics, 2017b, 9, 1745.
N.-C. Chu, G. M. Henderson, N. S. Belshaw, and R. E. M. Hedges, Appl. Geochem., 2006, 21, 1656.
K. Jaouen, P. Szpak, and M. P. Richards, PLoS ONE, 2016a, 11, e0152299.
K. Jaouen, M. Beasley, M. Schoeninger, J.-J. Hublin, and M. P. Richards, Sci. Rep., 2016b, 6, 26281.
T. Fujii and F. Albarède, PLoS ONE, 2012, 7, e30726.
F. Albarède, P. Télouk, V. Balter, V. P. Bondanese, E. Albalat, P. Oger, P. Bonaventura, P. Miossec, and T. Fujii, Metallomics, 2016, 8, 1056.
F. Moynier and T. Fujii, Sci. Rep., 2017, 7, 44255.
Acknowledgments
This work was financially supported by a Grant-in-Aid for Scientific Research to TH (A26247094) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tanaka, YK., Hirata, T. Stable Isotope Composition of Metal Elements in Biological Samples as Tracers for Element Metabolism. ANAL. SCI. 34, 645–655 (2018). https://doi.org/10.2116/analsci.18SBR02
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2116/analsci.18SBR02