Contrasting Cu, Fe, and Zn isotopic patterns in organs and body fluids of mice and sheep, with emphasis on cellular fractionation

Metallomics

Volumn 5, Issue 11, 2013, Pages 1470-1482

  Balter, Vincent ^a   Lamboux, Aline ^a   Zazzo, Antoine ^b   Télouk, Philippe ^a   Leverrier, Yann ^c   Marvel, Jacqueline ^c   Moloney, Aidan P ^d   Monahan, Frank J ^e   Schmidt, Olaf ^e   Albarède, Francis ^a  

^a UNIVERSITÉ DE LYON   (France)

^b MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^c INSERM   (France)

^d ANIMAL AND GRASSLAND RESEARCH AND INNOVATION CENTRE   (Ireland)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONES; ISOTOPE ABUNDANCE; ISOTOPE FRACTIONATION; ISOTOPIC PATTERN; NATURAL ISOTOPES; REDOX CONDITION; REDOX PROCESS;

AMINO ACIDS; BLOOD; ISOTOPES; MAMMALS;

ZINC;

ASCORBIC ACID; CARBONIC ACID DERIVATIVE; COPPER; CYSTEINE; GLUTATHIONE; HISTIDINE; HYDROXIDE; IRON; ISOTOPE; NITROGEN; OXALIC ACID; PHOSPHATE; SULFUR; ZINC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; BLOOD ANALYSIS; BODY COMPOSITION; BODY FLUID; CELL FRACTIONATION; CHEMICAL BOND; CONFERENCE PAPER; CONTROLLED STUDY; DEGRADATION KINETICS; FECES; FEMALE; ISOTOPE ANALYSIS; KIDNEY; LIQUID; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEEP;

ANIMALS; BODY FLUIDS; COPPER; HUMANS; IRON; ISOTOPES; MICE; SHEEP; ZINC ISOTOPES;

EID: 84886859385     PISSN: 17565901     EISSN: 1756591X     Source Type: Journal    
DOI: 10.1039/c3mt00151b     Document Type: Conference Paper

References (81)

1. T. Walczyk F. von Blanckenburg Natural iron isotope variations in human blood Science 2002 295 2065 2066
2. V. Balter A. Zazzo A. P. Moloney F. Moynier O. Schmidt F. J. Monahan F. Albarede Bodily variability of zinc natural isotope abundances in sheep Rapid Commun. Mass Spectrom. 2010 24 605 612 10.1002/rcm.4425
3. F. Albarede P. Telouk A. Lamboux K. Jaouen V. Balter Isotopic evidence of unaccounted for Fe and Cu erythropoietic pathways Metallomics 2011 3 926 933 10.1039/C1MT00025J
4. L. Van Heghe E. Engstrom I. Rodushkin C. Cloquet F. Vanhaecke Isotopic analysis of the metabolically relevant transition metals Cu, Fe and Zn in human blood from vegetarians and omnivores using multi-collector ICP-mass spectrometry J. Anal. At. Spectrom. 2012 27 1327 1334 10.1039/c2ja30070b
5. P. A. Krayenbuehl T. Walczyk R. Schoenberg F. von Blanckenburg G. Schulthess Hereditary hemochromatosis is reflected in the iron isotope composition of blood Blood 2005 105 3812 3816 10.1182/blood-2004-07-2807
6. M. Aramendia L. Rello M. Resano F. Vanhaecke Isotopic analysis of Cu in serum samples for diagnosis of Wilson's disease: a pilot study J. Anal. At. Spectrom. 2013 28 675 681 10.1039/c3ja30349g
7. A. Büchl C. J. Hawkesworth K. V. Ragnarsdottir D. R. Brown Re-partitioning of Cu and Zn isotopes by modified protein expression Geochem. Trans. 2008 9 10.1186/1467-4866-9-11
8. F. Moynier T. Fujii A. S. Shaw M. Le Borgne Heterogeneous distribution of natural zinc isotopes in mice Metallomics 2013 5 693 699 10.1039/c3mt00008g
9. E. C. Theil K. T. Calvert Effect of copper excess on iron-metabolism in sheep Biochem. J. 1978 170 137 143
10. N. F. Suttle Copper imbalances in ruminants and humans: Unexpected common ground Adv. Nutr. 2012 3 666 674 10.3945/an.112.002220
11. N. E. Soli Chronic copper poisoning in sheep. A review of the literature Nord. Veterinaermed. 1980 32 75 89
12. V. Jubin E. Ventre Y. Leverrier S. Djebali K. Mayol M. Tomkowiak J. Mafille M. Teixeira D. Y. L. Teoh B. Lina T. Walzer C. Arpin J. Marvel T inflammatory memory CD8 T cells participate to antiviral response and generate secondary memory cells with an advantage in XCL1 production Immunol. Res. 2012 52 284 293 10.1007/s12026-012-8340-4
13. C. N. Maréchal P. Télouk F. Albarède Precise analysis of copper and zinc isotopic compositions by plasma-source mass spectrometry Chem. Geol. 1999 156 251 273
14. F. Moynier J. Blichert-Toft P. Telouk J.-M. Luck F. Albarede Comparative stable isotope geochemistry of Ni, Cu, Zn, and Fe in chondrites and iron meteorites Geochim. Cosmochim. Acta 2007 71 4365 4379 10.1016/j.gca.2007.06.049
15. F. Albarède, in Geochemistry of Non-Traditional Stable Isotopes, ed., C. L. Johnson, B. L. Beard, and, F. Albarède, Min. Soc. Amer., 2004, vol. Rev. Min. Geoch. 55, pp. 409-427
16. K. Jaouen V. Balter E. Herrscher A. Lamboux P. Telouk F. Albarede Fe and Cu stable isotopes in archeological human bones and their relationship to sex Am. J. Phys. Anthropol. 2012 148 334 340 10.1002/ajpa.22053
17. F. Albarède and B. L. Beard, in Geochemistry of Non-Traditional Stable Isotopes, ed., C. L. Johnson, B. L. Beard, and, F. Albarède, Min. Soc. Amer., 2004, vol. Rev. Min. Geoch. 55, pp. 113-152
18. T. Ohno A. Shinohara I. Kohge M. Chiba T. Hirata Isotopic analysis of Fe in human red blood cells by multiple collector-ICP-mass spectrometry Anal. Sci. 2004 20 617 621 10.2116/analsci.20.617
19. J. R. Black A. Kavner E. A. Schauble Calculation of equilibrium stable isotope partition function ratios for aqueous zinc complexes and metallic zinc Geochim. Cosmochim. Acta 2011 75 769 783 10.1016/j.gca.2010.11.019
20. T. Fujii F. Moynier M.-L. Pons F. Albarede The origin of Zn isotope fractionation in sulfides Geochim. Cosmochim. Acta 2011 75 7632 7643 10.1016/j.gca.2011.09.036
21. T. Fujii F. Albarede Ab Initio Calculation of the Zn Isotope Effect in Phosphates, Citrates, and Malates and Applications to Plants and Soil PLoS One 2012 7 e30726 10.1371/journal.pone.0030726
22. J. H. Seo S. K. Lee I. Lee Quantum chemical calculations of equilibrium copper(I) isotope fractionations in ore-forming fluids Chem. Geol. 2007 243 225 237 10.1016/j.chemgeo.2007.05.025
23. T. Fujii F. Moynier M. Abe K. Nemoto F. Albarède Copper isotope fractionation between aqueous compounds relevant to low temperature geochemistry and biology Geochim. Cosmochim. Acta. 2013 110 29 44 10.1016/j.gca.2013.02.007
24. +)(6): Implications for iron stable isotope geochemistry Geochim. Cosmochim. Acta 2005 69 825 837 10.1016/j.gca.2004.06.012
25. V. B. Polyakov Equilibrium fractionation of the iron isotopes: Estimation from Mossbauer spectroscopy data Geochim. Cosmochim. Acta 1997 61 4213 4217 10.1016/s0016-7037(97)00204-4
26. V. B. Polyakov S. D. Mineev The use of Mossbauer spectroscopy in stable isotope geochemistry Geochim. Cosmochim. Acta 2000 64 849 865 10.1016/s0016-7037(99)00329-4
27. E. A. Schauble G. R. Rossman H. P. Taylor Jr. Theoretical estimates of equilibrium Fe-isotope fractionations from vibrational spectroscopy Geochim. Cosmochim. Acta 2001 65 2487 2497
28. Y. Furukawa A. S. Torres T. V. O'Halloran Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS EMBO J. 2004 23 2872 2881 10.1038/sj.emboj.7600276
29. L. Banci I. Bertini F. Cantini T. Kozyreva C. Massagni P. Palumaa J. T. Rubino K. Zovo Human superoxide dismutase 1 (hSOD1) maturation through interaction with human copper chaperone for SOD1 (hCCS) Proc. Natl. Acad. Sci. U. S. A. 2012 109 13555 13560 10.1073/pnas.1207493109
30. I. Bento C. Peixoto V. N. Zaitsev P. F. Lindley Ceruloplasmin revisited: structural and functional roles of various metal cation-binding sites Acta Crystallogr., Sect. D: Biol. Crystallogr. 2007 63 240 248 10.1107/ s090744490604947x
31. I. Zaitseva V. Zaitsev G. Card K. Moshkov B. Bax A. Ralph P. Lindley The X-ray structure of human serum ceruloplasmin at 3.1 angstrom: Nature of the copper centres J. Biol. Inorg. Chem. 1996 1 15 23
32. C. J. De Feo S. G. Aller G. S. Siluvai N. J. Blackburn V. M. Unger Three-dimensional structure of the human copper transporter hCTR1 Proc. Natl. Acad. Sci. U. S. A. 2009 106 4237 4242 10.1073/pnas.0810286106
33. A. Otoikhian A. N. Barry M. Mayfield M. Nilges Y. Huang S. Lutsenko N. J. Blackburn Lumenal loop M672-P707 of the Menkes Protein (ATP7A) transfers copper to peptidylglycine monooxygenase J. Am. Chem. Soc. 2012 134 10458 10468 10.1021/ja301221s
34. M. DiDonato H. F. Hsu S. Narindrasorasak L. Que B. Sarkar Copper-induced conformational changes in the N-terminal domain of the Wilson disease copper-transporting ATPase Biochemistry 2000 39 1890 1896 10.1021/bi992222j
35. S. Adhikari R. Joshi C. Gopinathan Bilirubin as an anti precipitant against copper mediated denaturation of bovine serum albumin: formation of copper-bilirubin complex Biochim. Biophys. Acta, Gen. Subj. 1998 1380 109 114 10.1016/S0304-4165(97)00141-4
36. S. F. Asad S. Singh A. Ahmad S. M. Hadi Bilirubin-Cu(II) complex degrades DNA Biochim. Biophys. Acta, Gen. Subj. 1999 1428 201 208 10.1016/s0304-4165(99) 00075-6
37. Y. Song D. Wang H. Qi S. Xiao R. Xue F. Li Metal ion binding of the first external loop of DCT1 in aqueous solution Metallomics 2009 1 392 394 10.1039/b909702n
38. T. Hirano, M. Murakami, T. Fukada, K. Nishida, S. Yamasaki and T. Suzuki, in Adv. Immunol., ed., W. A. Frederick, Academic Press, 2008, vol. 97, pp. 149-176
39. L. A. Lichten R. J. Cousins Annu. Rev. Nutr. 2009 29 153 176
40. R. A. Colvin W. R. Holmes C. P. Fontaine W. Maret Cytosolic zinc buffering and muffling: Their role in intracellular zinc homeostasis Metallomics 2010 2 306 317 10.1039/b926662c
41. T. Fukada S. Yamasaki K. Nishida M. Murakami T. Hirano Zinc homeostasis and signaling in health and diseases J. Biol. Inorg. Chem. 2011 16 1123 1134 10.1007/s00775-011-0797-4
42. W. Maret Y. Li Coordination dynamics of zinc in proteins Chem. Rev. 2009 109 4682 4707 10.1021/cr800556u
43. W. Maret New perspectives of zinc coordination environments in proteins J. Inorg. Biochem. 2012 111 110 116 10.1016/j.jinorgbio.2011.11.018
44. G. Parkin Synthetic analogues relevant to the structure and function of zinc enzymes Chem. Rev. 2004 104 699 767 10.1021/cr0206263
45. V. Kumar K. K. Kannan Enzyme-substrate interactions-structure of human carbonic-anhydrase-i complexed with bicarbonate J. Mol. Biol. 1994 241 226 232 10.1006/jmbi.1994.1491
46. J. Jeong D. J. Eide The SLC39 family of zinc transporters Mol. Aspects Med. 2013 34 612 619 10.1016/j.mam.2012.05.011
47. L. C. Costello C. C. Fenselau R. B. Franklin Evidence for operation of the direct zinc ligand exchange mechanism for trafficking, transport, and reactivity of zinc in mammalian cells J. Inorg. Biochem. 2011 105 589 599 10.1016/j.jinorgbio.2011.02.002
48. R. E. Dempski, in Current Topics in Membranes, ed., M. A. José, and, L. Svetlana, Academic Press, 2012, vol. 69, pp. 221-245
49. S. Haumont Distribution of zinc in bone tissue J. Histochem. Cytochem. 1961 9 141 145 10.1177/9.2.141
50. M. Yamaguchi Role of nutritional zinc in the prevention of osteoporosis Mol. Cell. Biochem. 2010 338 241 254 10.1007/s11010-009-0358-0
51. T. Ohno A. Shinohara M. Chiba T. Hirata Precise Zn isotopic ratio measurements of human red blood cell and hair samples by multiple collector ICP mass spectrometry Anal. Sci. 2005 21 425 428 10.2116/analsci.21.425
52. L. A. Gaither D. Eide Functional expression of the human hZIP2 zinc transporter FASEB J. 2000 14 A228
53. 3--related species Biochim. Biophys. Acta, Proteins Proteomics 2010 1804 410 421 10.1016/j.bbapap.2009.10.021
54. D. Sterling R. A. Reithmeier J. R. Casey Carbonic anhydrase: in the driver's seat for bicarbonate transport J. Pancreas 2001 2 165 70
55. 3-anion exchanger binding site to the amino-terminal region of carbonic anhydrase II Biochemistry 2000 39 13344 13349 10.1021/bi0015111
56. B.-E. Kim T. Nevitt D. J. Thiele Mechanisms for copper acquisition, distribution and regulation Nat. Chem. Biol. 2008 4 176 185 10.1038/nchembio.72
57. S. Lutsenko A. Gupta J. L. Burkhead V. Zuzel Cellular multitasking: The dual role of human Cu-ATPases in cofactor delivery and intracellular copper balance Arch. Biochem. Biophys. 2008 476 22 32 10.1016/j.abb.2008.05.005
58. S. Lutsenko Human copper homeostasis: a network of interconnected pathways Curr. Opin. Chem. Biol. 2010 14 211 217 10.1016/j.cbpa.2010.01.003
59. E. A. Roberts B. Sarkar Liver as a key organ in the supply, storage, and excretion of copper Am. J. Clin. Nutr. 2008 88 851S 854S
60. R. S. Ohgami D. R. Campagna A. McDonald M. D. Fleming The Steap proteins are metalloreductases Blood 2006 108 1388 1394 10.1182/blood-2006-02-003681
61. B. Zhou J. Gitschier hCTR1: A human gene for copper uptake identified by complementation in yeast Proc. Natl. Acad. Sci. U. S. A. 1997 94 7481 7486 10.1073/pnas.94.14.7481
62. L. W. J. Klomp S. J. Lin D. S. Yuan R. D. Klausner V. C. Culotta J. D. Gitlin Identification and functional expression of HAH1, a novel human gene involved in copper homeostasis J. Biol. Chem. 1997 272 9221 9226
63. S. C. Leary D. R. Winge P. A. Cobine "Pulling the plug" on cellular copper: The role of mitochondria in copper export Biochim. Biophys. Acta, Mol. Cell Res. 2009 1793 146 153 10.1016/j.bbamcr.2008.05.002
64. S. La Fontaine J. F. B. Mercer Trafficking of the copper-ATPases, ATP7A and ATP7B: Role in copper homeostasis Arch. Biochem. Biophys. 2007 463 149 167 10.1016/j.abb.2007.04.021
65. K. H. Weiss J. Wurz D. Gotthardt U. Merle W. Stremmel J. Fuellekrug Localization of the Wilson disease protein in murine intestine J. Anat. 2008 213 232 240 10.1111/j.1469-7580.2008.00954.x
66. N. A. Veldhuis V. A. Valova A. P. Gaeth N. Palstra K. M. Hannan B. J. Michell L. E. Kelly I. Jennings B. E. Kemp R. B. Pearson P. J. Robinson J. Camakaris Phosphorylation regulates copper-responsive trafficking of the Menkes copper transporting P-type ATPase Int. J. Biochem. Cell Biol. 2009 41 2403 2412 10.1016/j.biocel.2009.06.008
67. L. Barrow M. S. Tanner Expression of the ceruloplasmin gene in adult and neonatal rat-liver Gut 1988 29 A1436
68. K. C. Weiss M. C. Linder Copper transport in rats involving a new plasma protein Am. J. Physiol. 1985 249 E77 E88
69. P. L. Wirth M. C. Linder Distribution of copper among components of human-serum JNCI, J. Natl. Cancer Inst. 1985 75 277 284
70. S. D. P. Moore K. E. Helmle L. M. Prat D. W. Cox Tissue localization of the copper chaperone ATOX1 and its potential role in disease Mamm. Genome 2002 13 563 568 10.1007/s00335-002-2172-9
71. C. L. Linster E. Van Schaftingen Vitamin C: Biosynthesis, recycling and degradation in mammals FEBS J. 2007 274 1 22 10.1111/j.1742-4658.2006.05607.x
72. L. Robitaille O. A. Mamer W. H. Miller Jr. M. Levine S. Assouline D. Melnychuk C. Rousseau L. J. Hoffer Oxalic acid excretion after intravenous ascorbic acid administration Metab., Clin. Exp. 2009 58 263 269 10.1016/j.metabol.2008.09.023
73. N. C. Andrews Forging a field: the golden age of iron biology Blood 2008 112 219 230 10.1182/blood-2007-12-077388
74. R. E. Fleming B. R. Bacon Orchestration of iron homeostasis N. Engl. J. Med. 2005 352 1741 1744
75. J. Wang K. Pantopoulos Regulation of cellular iron metabolism Biochem. J. 2011 434 365 381 10.1042/BJ20101825
76. J. F. Collins J. R. Prohaska M. D. Knutson Metabolic crossroads of iron and copper Nutr. Rev. 2010 68 133 147 10.1111/j.1753-4887.2010.00271.x
77. H. Shi K. Z. Bencze T. L. Stemmler C. C. Philpott A cytosolic iron chaperone that delivers iron to ferritin Science 2008 320 1207 1210 10.1126/science.1157643
78. F. Chimienti S. Devergnas F. Pattou F. Schuit R. Garcia-Cuenca B. Vandewalle J. Kerr-Conte L. Van Lommel D. Grunwald A. Favier M. Seve In vivo expression and functional characterization of the zinc transporter ZnT8 in glucose-induced insulin secretion J. Cell Sci. 2006 119 4199 4206 10.1242/jcs.03164
79. J. A. Goss N. R. Barshes S. J. Karpen F.-Q. Gao S. Wyllie Liver ischemia and ischemia-reperfusion induces and trafficks the multi-specific metal transporter Atp7b to bile duct canaliculi: Possible preferential transport of iron into bile Biol. Trace Elem. Res. 2008 122 26 41 10.1007/s12011-007-8057-8
80. R. C. DeLisle M. P. Sarras J. Hidalgo G. K. Andrews Metallothionein is a component of exocrine pancreas secretion: Implications for zinc homeostasis Am. J. Physiol.: Cell Physiol. 1996 271 C1103 C1110
81. P. Coyle J. C. Philcox L. C. Carey A. M. Rofe Metallothionein: The multipurpose protein Cell. Mol. Life Sci. 2002 59 627 647 10.1007/s00018-002- 8454-2