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The Iron Metallome in Eukaryotic Organisms

  • Adrienne C. Dlouhy
  • Caryn E. Outten
Chapter
First Online:
Part of the Metal Ions in Life Sciences book series (MILS, volume 12)

Abstract

This chapter is focused on the iron metallome in eukaryotes at the cellular and subcellular level, including properties, utilization in metalloproteins, trafficking, storage, and regulation of these processes. Studies in the model eukaryote Saccharomyces cerevisiae and mammalian cells will be highlighted. The discussion of iron properties will center on the speciation and localization of intracellular iron as well as the cellular and molecular mechanisms for coping with both low iron bioavailability and iron toxicity. The section on iron metalloproteins will emphasize heme, iron-sulfur cluster, and non-heme iron centers, particularly their cellular roles and mechanisms of assembly. The section on iron uptake, trafficking, and storage will compare methods used by yeast and mammalian cells to import iron, how this iron is brought into various organelles, and types of iron storage proteins. Regulation of these processes will be compared between yeast and mammalian cells at the transcriptional, post-transcriptional, and post-translational levels.

Keywords

eukaryote heme iron metallome iron-sulfur cluster iron trafficking metal homeostasis 

Abbreviations

ABC

ATP-binding cassette

ALA

δ-aminolevulinic acid

ALAD

aminolevulinate dehydratase

ALAS

ALA synthase

ARE

AU-rich elements

ATP

adenosine 5’-triphosphate

BDH2

3-hydroxybutyrate dehydrogenase, type 2

BMP

bone morphogenic protein

C/EBPα

CCAAT enhancer-binding protein α

CIA

cytosolic Fe-S protein assembly

CoA

coenzyme A

Cp

ceruloplasmin

CPgenIII

coproporphyrinogen III

CPOX

coproporphyrinogen oxidase

DHBA

dihydroxybenzoic acid

DMTI

divalent metal transporter 1 (= SCL11A1)

dNDP

deoxynucleoside diphosphate

dNTP

deoxynucleoside triphosphate

EPR

electron paramagnetic resonance

ER

endoplasmic reticulum

EXAFS

extended X-ray absorption fine structure

FECH

ferrochelatase

FeRE

iron-responsive element

FIH1

factor inhibiting HIF

FPN

ferroportin

Grx

glutaredoxin

GSH

glutathione

GST

glutathione S-transferase

HCP1

heme carrier protein 1

HIF

hypoxia-inducible factor

HMB

hydroxymethylbilane

HO-1

heme oxygenase-1

HRG

heme responsive gene

IMS

intermembrane space

IRE

iron regulatory element

IRP

iron regulatory protein

ISC

iron-sulfur cluster

LIP

labile iron pool

Mfrn

mitoferrin

NADH

nicotinamide adenine dinucleotide reduced

NDP

nucleoside 5’-diphosphate

NRAMP

natural resistance-associated macrophage protein

NTP

nucleoside 5’-triphosphate

PBGD

porphobilinogen deaminase

PCBP

poly (rC) binding protein

PHD

prolyl hydroxylase

PIXE

particle-induced X-ray emission

PPgenIX

protoporphyrinogen IX

PPIX

protoporphyrin IX

PPOX

protoporphyrinogen oxidase

RBC

red blood cells

RNR

ribonucleotide reductase

ROS

reactive oxygen species

RNS

reactive nitrogen species

SCF

SKP1-CUL1-F-box

SOD

superoxide dismutase

STEAP

six-transmembrane epithelial antigen of the prostate

TCA

tricarboxylic acid

Tf

transferrin

TfR

Tf receptor

TTP

tristetraprolin

TZF

tandem zinc finger

UPgenIII

uroporphyrinogen III

URO3S

uroporphyrinogen III synthase

UROD

uroporphyrinogen decarboxylase

UTR

untranslated region

VHL

von Hippel-Lindau

XANES

X-ray absorption near edge structure

XAS

X-ray absorption spectroscopy

XRFM

X-ray fluorescence microscopy

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Notes

Acknowledgments

This work was funded by the National Institutes of Health Grants ES013780 and GM086619 and the South Carolina Research Foundation. The authors would like to thank Dr. L. Celeste for helpful discussions.

References

  1. 1.
    D. J. Eide, S. Clark, T. M. Nair, M. Gehl, M. Gribskov, M. L. Guerinot, J. F. Harper, Genome Biol. 2005, 6, R77.PubMedGoogle Scholar
  2. 2.
    S. Epsztejn, H. Glickstein, V. Picard, I. N. Slotki, W. Breuer, C. Beaumont, Z. I. Cabantchik, Blood 1999, 94, 3593–3603.PubMedGoogle Scholar
  3. 3.
    F. Petrat, U. Rauen, H. de Groot, Hepatology 1999, 29, 1171–1179.PubMedGoogle Scholar
  4. 4.
    D. Ceccarelli, D. Gallesi, F. Giovannini, M. Ferrali, A. Masini, Biochem. Biophys. Res. Commun. 1995, 209, 53–59.PubMedGoogle Scholar
  5. 5.
    X. Gao, M. Qian, J. L. Campian, J. Marshall, Z. Zhou, A. M. Roberts, Y. J. Kang, S. D. Prabhu, X. F. Sun, J. W. Eaton, Free Radic. Biol. Med. 2010, 49, 401–407.Google Scholar
  6. 6.
    J. Petrak, D. Myslivcova, P. Man, R. Cmejla, J. Cmejlova, D. Vyoral, Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, G1059–1066.Google Scholar
  7. 7.
    R. Miao, G. P. Holmes-Hampton, P. A. Lindahl, Biochemistry 2011, 50, 2660–2671.PubMedGoogle Scholar
  8. 8.
    P. A. Lindahl, G. P. Holmes-Hampton, Curr. Opin. Chem. Biol. 2011, 15, 342–346.PubMedGoogle Scholar
  9. 9.
    A. L. Cockrell, G. P. Holmes-Hampton, S. P. McCormick, M. Chakrabarti, P. A. Lindahl, Biochemistry 2011, 50, 10275–10283.PubMedGoogle Scholar
  10. 10.
    G. P. Holmes-Hampton, R. Miao, J. Garber Morales, Y. Guo, E. Munck, P. A. Lindahl, Biochemistry 2010, 49, 4227–4234.PubMedGoogle Scholar
  11. 11.
    R. Miao, H. Kim, U. M. Koppolu, E. A. Ellis, R. A. Scott, P. A. Lindahl, Biochemistry 2009, 48, 9556–9568.PubMedGoogle Scholar
  12. 12.
    R. Ortega, G. Deves, A. Carmona, J. R. Soc. Interface 2009, 6 Suppl 5, S649–658.Google Scholar
  13. 13.
    C. J. Fahrni, Curr. Opin. Chem. Biol. 2007, 11, 121–127.PubMedGoogle Scholar
  14. 14.
    T. C. Iancu, Y. Deugnier, J. W. Halliday, L. W. Powell, P. Brissot, J. Hepatol. 1997, 27, 628–638.PubMedGoogle Scholar
  15. 15.
    C. D. Kaplan, J. Kaplan, Chem. Rev. 2009, 109, 4536–4552.PubMedGoogle Scholar
  16. 16.
    M. W. Hentze, M. U. Muckenthaler, N. C. Andrews, Cell 2004, 117, 285–297.PubMedGoogle Scholar
  17. 17.
    G. Bao, M. Clifton, T. M. Hoette, K. Mori, S. X. Deng, A. Qiu, M. Viltard, D. Williams, N. Paragas, T. Leete, R. Kulkarni, X. Li, B. Lee, A. Kalandadze, A. J. Ratner, J. C. Pizarro, K. M. Schmidt-Ott, D. W. Landry, K. N. Raymond, R. K. Strong, J. Barasch, Nat. Chem. Biol. 2010, 6, 602–609.PubMedGoogle Scholar
  18. 18.
    L. R. Devireddy, D. O. Hart, D. H. Goetz, M. R. Green, Cell 2010, 141, 1006–1017.PubMedGoogle Scholar
  19. 19.
    C. Correnti, R. K. Strong, J. Biol. Chem. 2012, 287, 13524–13531.Google Scholar
  20. 20.
    F. Petrat, H. de Groot, U. Rauen, Biochem. J. 2001, 356, 61–69.PubMedGoogle Scholar
  21. 21.
    M. W. Hentze, M. U. Muckenthaler, B. Galy, C. Camaschella, Cell 2010, 142, 24–38.PubMedGoogle Scholar
  22. 22.
    R. C. Hider, X. L. Kong, Biometals 2011, 24, 1179–1187.PubMedGoogle Scholar
  23. 23.
    U. Muhlenhoff, S. Molik, J. R. Godoy, M. A. Uzarska, N. Richter, A. Seubert, Y. Zhang, J. Stubbe, F. Pierrel, E. Herrero, C. H. Lillig, R. Lill, Cell Metab. 2010, 12, 373–385.PubMedGoogle Scholar
  24. 24.
    F. Petrat, D. Weisheit, M. Lensen, H. de Groot, R. Sustmann, U. Rauen, Biochem. J. 2002, 362, 137–147.PubMedGoogle Scholar
  25. 25.
    U. Rauen, A. Springer, D. Weisheit, F. Petrat, H. G. Korth, H. de Groot, R. Sustmann, Chembiochem 2007, 8, 341–352.PubMedGoogle Scholar
  26. 26.
    B. Sturm, U. Bistrich, M. Schranzhofer, J. P. Sarsero, U. Rauen, B. Scheiber-Mojdehkar, H. de Groot, P. Ioannou, F. Petrat, J. Biol. Chem. 2005, 280, 6701–6708.Google Scholar
  27. 27.
    J. P. Kehrer, Toxicology 2000, 149, 43–50.PubMedGoogle Scholar
  28. 28.
    I. I. Rovira, T. Finkel, B. S. Masters, M. B. Dickman, J. Lee, S. W. Ragsdale, C. C. Lee, in Redox Biochemistry, Eds R. Banerjee, D. F. Becker, M. B. Dickman, V. N. Gladyshev, S. W. Ragsdale, John Wiley & Sons, Inc., Hoboken, NJ, USA, 2007.Google Scholar
  29. 29.
    K. Jomova, M. Valko, Toxicology 2011, 283, 65–87.PubMedGoogle Scholar
  30. 30.
    H. Lin, L. Li, X. Jia, D. M. Ward, J. Kaplan, J. Biol. Chem. 2011, 286, 3851–3862.Google Scholar
  31. 31.
    R. M. Lebovitz, H. Zhang, H. Vogel, J. Cartwright, Jr., L. Dionne, N. Lu, S. Huang, M. M. Matzuk, Proc. Natl. Acad. Sci. USA 1996, 93, 9782–9787.Google Scholar
  32. 32.
    Y. Li, T. T. Huang, E. J. Carlson, S. Melov, P. C. Ursell, J. L. Olson, L. J. Noble, M. P. Yoshimura, C. Berger, P. H. Chan, D. C. Wallace, C. J. Epstein, Nat. Genet. 1995, 11, 376–381.PubMedGoogle Scholar
  33. 33.
    A. Naranuntarat, L. T. Jensen, S. Pazicni, J. E. Penner-Hahn, V. C. Culotta, J. Biol. Chem. 2009, 284, 22633–22640.Google Scholar
  34. 34.
    M. Yang, P. A. Cobine, S. Molik, A. Naranuntarat, R. Lill, D. R. Winge, V. C. Culotta, EMBO J. 2006, 25, 1775–1783.PubMedGoogle Scholar
  35. 35.
    H. A. Jouihan, P. A. Cobine, R. C. Cooksey, E. A. Hoagland, S. Boudina, E. D. Abel, D. R. Winge, D. A. McClain, Mol. Med. 2008, 14, 98–108.PubMedGoogle Scholar
  36. 36.
    L. Yin, N. Wu, J. C. Curtin, M. Qatanani, N. R. Szwergold, R. A. Reid, G. M. Waitt, D. J. Parks, K. H. Pearce, G. B. Wisely, M. A. Lazar, Science 2007, 318, 1786–1789.PubMedGoogle Scholar
  37. 37.
    M. K. Johnson, Curr. Opin. Chem. Biol. 1998, 2, 173–181.PubMedGoogle Scholar
  38. 38.
    K. M. Lancaster, M. Roemelt, P. Ettenhuber, Y. Hu, M. W. Ribbe, F. Neese, U. Bergmann, S. DeBeer, Science 2011, 334, 974–977.PubMedGoogle Scholar
  39. 39.
    T. Spatzal, M. Aksoyoglu, L. Zhang, S. L. Andrade, E. Schleicher, S. Weber, D. C. Rees, O. Einsle, Science 2011, 334, 940.PubMedGoogle Scholar
  40. 40.
    A. Sheftel, O. Stehling, R. Lill, Trends Endocrinol. Metab. 2010, 21, 302–314.Google Scholar
  41. 41.
    I. Hamza, ACS Chem. Biol. 2006, 1, 627–629.Google Scholar
  42. 42.
    R. S. Ajioka, J. D. Phillips, J. P. Kushner, Biochim. Biophys. Acta 2006, 1763, 723–736.Google Scholar
  43. 43.
    P. M. Shoolingin-Jordan, A. Al-Dbass, L. A. McNeill, M. Sarwar, D. Butler, Biochem. Soc. Trans. 2003, 31, 731–735.PubMedGoogle Scholar
  44. 44.
    P. C. Krishnamurthy, G. Du, Y. Fukuda, D. Sun, J. Sampath, K. E. Mercer, J. Wang, B. Sosa-Pineda, K. G. Murti, J. D. Schuetz, Nature 2006, 443, 586–589.PubMedGoogle Scholar
  45. 45.
    I. J. Schultz, C. Chen, B. H. Paw, I. Hamza, J. Biol. Chem. 2010, 285, 26753–26759.Google Scholar
  46. 46.
    H. A. Dailey, Biochem. Soc. Trans. 2002, 30, 590–595.PubMedGoogle Scholar
  47. 47.
    S. Park, O. Gakh, H. A. O’Neill, A. Mangravita, H. Nichol, G. C. Ferreira, G. Isaya, J. Biol. Chem. 2003, 278, 31340–31351.Google Scholar
  48. 48.
    T. A. Rouault, Dis. Model. Mech. 2012, 5, 155–164.PubMedGoogle Scholar
  49. 49.
    S. Severance, I. Hamza, Chem. Rev. 2009, 109, 4596–4616.PubMedGoogle Scholar
  50. 50.
    N. Spielewoy, H. Schulz, J. M. Grienenberger, L. Thony-Meyer, G. Bonnard, J. Biol. Chem. 2001, 276, 5491–5497.Google Scholar
  51. 51.
    J. W. Harvey, E. Beutler, Blood 1982, 60, 1227–1230.PubMedGoogle Scholar
  52. 52.
    Y. Nakai, N. Umeda, T. Suzuki, M. Nakai, H. Hayashi, K. Watanabe, H. Kagamiyama, J. Biol. Chem. 2004, 279, 12363–12368.Google Scholar
  53. 53.
    R. Lill, U. Muhlenhoff, Annu. Rev. Biochem. 2008, 77, 669–700.PubMedGoogle Scholar
  54. 54.
    P. Subramanian, A. V. Rodrigues, S. Ghimire-Rijal, T. L. Stemmler, Curr. Opin. Chem. Biol. 2011, 15, 312–318.PubMedGoogle Scholar
  55. 55.
    J. Bridwell-Rabb, C. Iannuzzi, A. Pastore, D. P. Barondeau, Biochemistry 2012, 51, 2506–2514.PubMedGoogle Scholar
  56. 56.
    Y. Ichikawa, M. Bayeva, M. Ghanefar, V. Potini, L. Sun, R. K. Mutharasan, R. Wu, A. Khechaduri, T. Jairaj Naik, H. Ardehali, Proc. Natl. Acad. Sci. USA 2012, 109, 4152–4157.Google Scholar
  57. 57.
    T. Bedekovics, H. Li, G. B. Gajdos, G. Isaya, J. Biol. Chem. 2011, 286, 40878–40888.Google Scholar
  58. 58.
    L. Banci, I. Bertini, S. Ciofi-Baffoni, F. Boscaro, A. Chatzi, M. Mikolajczyk, K. Tokatlidis, J. Winkelmann, Chem. Biol. 2011, 18, 794–804.PubMedGoogle Scholar
  59. 59.
    A. K. Sharma, L. J. Pallesen, R. J. Spang, W. E. Walden, J. Biol. Chem. 2010, 285, 26745–26751.Google Scholar
  60. 60.
    H. Li, D. T. Mapolelo, N. N. Dingra, G. Keller, P. J. Riggs-Gelasco, D. R. Winge, M. K. Johnson, C. E. Outten, J. Biol. Chem. 2011, 286, 867–876.Google Scholar
  61. 61.
    J. A. Cotruvo, J. Stubbe, Annu. Rev. Biochem. 2011, 80, 733–767.PubMedGoogle Scholar
  62. 62.
    Y. Zhang, L. Liu, X. Wu, X. An, J. Stubbe, M. Huang, J. Biol. Chem. 2011, 286, 41499–41509.Google Scholar
  63. 63.
    M. R. Bleackley, R. T. Macgillivray, Biometals 2011, 24, 785–809.PubMedGoogle Scholar
  64. 64.
    A. Kumanovics, O. S. Chen, L. Li, D. Bagley, E. M. Adkins, H. Lin, N. N. Dingra, C. E. Outten, G. Keller, D. Winge, D. M. Ward, J. Kaplan, J. Biol. Chem. 2008, 283, 10276–10286.Google Scholar
  65. 65.
    H. Li, D. T. Mapolelo, N. N. Dingra, S. G. Naik, N. S. Lees, B. M. Hoffman, P. J. Riggs-Gelasco, B. H. Huynh, M. K. Johnson, C. E. Outten, Biochemistry 2009, 48, 9569–9581.PubMedGoogle Scholar
  66. 66.
    M. Shayeghi, G. O. Latunde-Dada, J. S. Oakhill, A. H. Laftah, K. Takeuchi, N. Halliday, Y. Khan, A. Warley, F. E. McCann, R. C. Hider, D. M. Frazer, G. J. Anderson, C. D. Vulpe, R. J. Simpson, A. T. McKie, Cell 2005, 122, 789–801.PubMedGoogle Scholar
  67. 67.
    G. J. Anderson, C. D. Vulpe, Cell. Mol. Life Sci. 2009, 66, 3241–3261.Google Scholar
  68. 68.
    A. Rajagopal, A. U. Rao, J. Amigo, M. Tian, S. K. Upadhyay, C. Hall, S. Uhm, M. K. Mathew, M. D. Fleming, B. H. Paw, M. Krause, I. Hamza, Nature 2008, 453, 1127–1131.PubMedGoogle Scholar
  69. 69.
    A. Nandal, J. C. Ruiz, P. Subramanian, S. Ghimire-Rijal, R. A. Sinnamon, T. L. Stemmler, R. K. Bruick, C. C. Philpott, Cell Metab. 2011, 14, 647–657.PubMedGoogle Scholar
  70. 70.
    P. Haunhorst, C. Berndt, S. Eitner, J. R. Godoy, C. H. Lillig, Biochem. Biophys. Res. Commun. 2010, 394, 372–376.PubMedGoogle Scholar
  71. 71.
    H. Li, D. T. Mapolelo, S. Randeniya, M. K. Johnson, C. E. Outten, Biochemistry 2012, 51, 1687–1696.PubMedGoogle Scholar
  72. 72.
    E. C. Theil, Curr. Opin. Chem. Biol. 2011, 15, 304–311.PubMedGoogle Scholar
  73. 73.
    J. Wang, K. Pantopoulos, Biochem. J. 2011, 434, 365–381.PubMedGoogle Scholar
  74. 74.
    F. Bou-Abdallah, P. Santambrogio, S. Levi, P. Arosio, N. D. Chasteen, J. Mol. Biol. 2005, 347, 543–554.Google Scholar
  75. 75.
    P. Santambrogio, B. G. Erba, A. Campanella, A. Cozzi, V. Causarano, L. Cremonesi, A. Galli, M. G. Della Porta, R. Invernizzi, S. Levi, Haematologica 2011, 96, 1424–1432.PubMedGoogle Scholar
  76. 76.
    D. R. Richardson, D. J. Lane, E. M. Becker, M. L. Huang, M. Whitnall, Y. Suryo Rahmanto, A. D. Sheftel, P. Ponka, Proc. Natl. Acad. Sci. USA 2010, 107, 10775–10782.Google Scholar
  77. 77.
    M. L. Huang, D. J. Lane, D. R. Richardson, Antioxid. Redox Signal. 2011, 15, 3003–3019.Google Scholar
  78. 78.
    L. Li, O. S. Chen, D. McVey Ward, J. Kaplan, J. Biol. Chem. 2001, 276, 29515–29519.Google Scholar
  79. 79.
    C. C. Philpott, O. Protchenko, Eukaryot. Cell 2008, 7, 20–27.Google Scholar
  80. 80.
    A. Singh, N. Kaur, D. J. Kosman, J. Biol. Chem. 2007, 282, 28619–28626.Google Scholar
  81. 81.
    T. Kurz, J. W. Eaton, U. T. Brunk, Int. J. Biochem. Cell Biol. 2011, 43, 1686–1697.Google Scholar
  82. 82.
    P. D. Toman, G. Chisholm, H. McMullin, L. M. Giere, D. R. Olsen, R. J. Kovach, S. D. Leigh, B. E. Fong, R. Chang, G. A. Daniels, R. A. Berg, R. A. Hitzeman, J. Biol. Chem. 2000, 275, 23303–23309.Google Scholar
  83. 83.
    I. De Domenico, M. B. Vaughn, P. N. Paradkar, E. Lo, D. M. Ward, J. Kaplan, Cell Metab. 2011, 13, 57–67.PubMedGoogle Scholar
  84. 84.
    F. Missirlis, S. Kosmidis, T. Brody, M. Mavrakis, S. Holmberg, W. F. Odenwald, E. M. Skoulakis, T. A. Rouault, Genetics 2007, 177, 89–100.PubMedGoogle Scholar
  85. 85.
    A. A. Alkhateeb, J. R. Connor, Biochim. Biophys. Acta 2010, 1800, 793–797.Google Scholar
  86. 86.
    S. A. Gurgueira, R. Meneghini, J. Biol. Chem. 1996, 271, 13616–13620.Google Scholar
  87. 87.
    J. Kaplan, D. McVey Ward, R. J. Crisp, C. C. Philpott, Biochim. Biophys. Acta 2006, 1763, 646–651.Google Scholar
  88. 88.
    P. L. Blaiseau, E. Lesuisse, J. M. Camadro, J. Biol. Chem. 2001, 276, 34221–34226.Google Scholar
  89. 89.
    J. C. Rutherford, A. J. Bird, Eukaryot. Cell 2004, 3, 1–13.Google Scholar
  90. 90.
    J. C. Rutherford, S. Jaron, D. R. Winge, J. Biol. Chem. 2003, 278, 27636–27643.Google Scholar
  91. 91.
    M. Courel, S. Lallet, J. M. Camadro, P. L. Blaiseau, Mol. Cell. Biol. 2005, 25, 6760–6771.PubMedGoogle Scholar
  92. 92.
    L. Li, X. Jia, D. M. Ward, J. Kaplan, J. Biol. Chem. 2011, 286, 38488–38497.Google Scholar
  93. 93.
    L. Li, D. Bagley, D. M. Ward, J. Kaplan, Mol. Cell. Biol. 2008, 28, 1326–1337.PubMedGoogle Scholar
  94. 94.
    D. R. Winge, K. B. Nielson, W. R. Gray, D. H. Hamer, J. Biol. Chem. 1985, 260, 14464–14470.Google Scholar
  95. 95.
    X. Q. Ding, E. Bill, A. X. Trautwein, H. J. Hartmann, U. Weser, Eur. J. Biochem. 1994, 223, 841–845.PubMedGoogle Scholar
  96. 96.
    M. Mastrogiannaki, P. Matak, B. Keith, M. C. Simon, S. Vaulont, C. Peyssonnaux, J. Clin. Invest. 2009, 119, 1159–1166.Google Scholar
  97. 97.
    Y. M. Shah, T. Matsubara, S. Ito, S. H. Yim, F. J. Gonzalez, Cell Metab. 2009, 9, 152–164.PubMedGoogle Scholar
  98. 98.
    C. C. Philpott, S. Leidgens, A. G. Frey, Biochim. Biophys. Acta 2012, 1823, 1509–1520.Google Scholar
  99. 99.
    S. Puig, S. V. Vergara, D. J. Thiele, Cell Metab. 2008, 7, 555–564.PubMedGoogle Scholar
  100. 100.
    S. Puig, E. Askeland, D. J. Thiele, Cell 2005, 120, 99–110.PubMedGoogle Scholar
  101. 101.
    C. D. Kaplan, J. Kaplan, Cell Metab. 2005, 2, 4–6.PubMedGoogle Scholar
  102. 102.
    R. Yao, Z. Zhang, X. An, B. Bucci, D. L. Perlstein, J. Stubbe, M. Huang, Proc. Natl. Acad. Sci. USA 2003, 100, 6628–6633.Google Scholar
  103. 103.
    N. Sanvisens, M. C. Bano, M. Huang, S. Puig, Mol. Cell 2011, 44, 759–769.Google Scholar
  104. 104.
    S. Recalcati, G. Minotti, G. Cairo, Antioxid. Redox Signal. 2010, 13, 1593–1616.Google Scholar
  105. 105.
    T. A. Rouault, Nat. Chem. Biol. 2006, 2, 406–414.PubMedGoogle Scholar
  106. 106.
    K. Pantopoulos, Ann. N. Y. Acad. Sci. 2004, 1012, 1–13.PubMedGoogle Scholar
  107. 107.
    J. C. Rutherford, L. Ojeda, J. Balk, U. Muhlenhoff, R. Lill, D. R. Winge, J. Biol. Chem. 2005, 280, 10135–10140.Google Scholar
  108. 108.
    N. Pujol-Carrion, G. Bellí, E. Herrero, A. Nogues, M. A. de la Torre-Ruiz, J. Cell Sci. 2006, 119, 4554–4564.Google Scholar
  109. 109.
    L. Li, G. Murdock, D. Bagley, X. Jia, D. M. Ward, J. Kaplan, J. Biol. Chem. 2010, 285, 10232–10242.Google Scholar
  110. 110.
    H. Li, C. E. Outten, Biochemistry 2012, 51, 4377–4389.Google Scholar
  111. 111.
    J. Kaplan, D. M. Ward, I. De Domenico, Int. J. Hematol. 2011, 93, 14–20.PubMedGoogle Scholar
  112. 112.
    K. Gkouvatsos, G. Papanikolaou, K. Pantopoulos, Biochim. Biophys. Acta 2012, 1820, 188–202.Google Scholar
  113. 113.
    M. Sanchez, B. Galy, M. U. Muckenthaler, M. W. Hentze, Nat. Struct. Mol. Biol. 2007, 14, 420–426.PubMedGoogle Scholar
  114. 114.
    A. A. Salahudeen, J. W. Thompson, J. C. Ruiz, H. W. Ma, L. N. Kinch, Q. Li, N. V. Grishin, R. K. Bruick, Science 2009, 326, 722–726.PubMedGoogle Scholar
  115. 115.
    A. A. Vashisht, K. B. Zumbrennen, X. Huang, D. N. Powers, A. Durazo, D. Sun, N. Bhaskaran, A. Persson, M. Uhlen, O. Sangfelt, C. Spruck, E. A. Leibold, J. A. Wohlschlegel, Science 2009, 326, 718–721.PubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Chemistry and BiochemistryUniversity of South CarolinaColumbiaUSA

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