Iron and copper in mitochondrial diseases

Cell Metabolism

Volumn 17, Issue 3, 2013, Pages 319-328

  Xu, Wenjing ^a   Barrientos, Tomasa ^a   Andrews, Nancy C ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINOLEVULINATE SYNTHASE; ADENOSINE TRIPHOSPHATE; ALPHA SYNUCLEIN; AMYLOID PRECURSOR PROTEIN; CARDIOLIPIN; CERULOPLASMIN; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE; FERRITIN; FERROPORTIN; GLUTAREDOXIN; IRON; MANGANESE SUPEROXIDE DISMUTASE; MENKES PROTEIN; PRION PROTEIN; REACTIVE OXYGEN METABOLITE; TRANSFERRIN RECEPTOR;

CARDIOMYOPATHY; CATALYSIS; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CYTOSOL; DEGENERATIVE DISEASE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA REPAIR; DNA REPLICATION; ELECTRON TRANSPORT; ENDOPLASMIC RETICULUM; FRIEDREICH ATAXIA; GENE OVEREXPRESSION; METAL METABOLISM; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; TELOMERE HOMEOSTASIS;

HEME; HOMEOSTASIS; HUMANS; IRON; IRON-SULFUR PROTEINS; MITOCHONDRIAL DISEASES; MODELS, BIOLOGICAL;

EID: 84875345177     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.02.004     Document Type: Review

References (101)

1. A.C. Adam, C. Bornhövd, H. Prokisch, W. Neupert, and K. Hell The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria EMBO J. 25 2006 174 183
2. R. Allikmets, W.H. Raskind, A. Hutchinson, N.D. Schueck, M. Dean, and D.M. Koeller Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked sideroblastic anemia and ataxia (XLSA/A) Hum. Mol. Genet. 8 1999 743 749
3. N.C. Andrews Forging a field: the golden age of iron biology Blood 112 2008 219 230
4. H. Antonicka, S.C. Leary, G.H. Guercin, J.N. Agar, R. Horvath, N.G. Kennaway, C.O. Harding, M. Jaksch, and E.A. Shoubridge Mutations in COX10 result in a defect in mitochondrial heme A biosynthesis and account for multiple, early-onset clinical phenotypes associated with isolated COX deficiency Hum. Mol. Genet. 12 2003 2693 2702
5. M. Babcock, D. de Silva, R. Oaks, S. Davis-Kaplan, S. Jiralerspong, L. Montermini, M. Pandolfo, and J. Kaplan Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin Science 276 1997 1709 1712
6. L. Banci, I. Bertini, S. Ciofi-Baffoni, T. Hadjiloi, M. Martinelli, and P. Palumaa Mitochondrial copper(I) transfer from Cox17 to Sco1 is coupled to electron transfer Proc. Natl. Acad. Sci. USA 105 2008 6803 6808
7. T.B. Bartnikas, D.R. Campagna, B. Antiochos, H. Mulhern, C. Pondarré, and M.D. Fleming Characterization of mitochondrial ferritin-deficient mice Am. J. Hematol. 85 2010 958 960
8. A. Bayot, R. Santos, J.M. Camadro, and P. Rustin Friedreich's ataxia: the vicious circle hypothesis revisited BMC Med. 9 2011 112
9. S. Bekri, G. Kispal, H. Lange, E. Fitzsimons, J. Tolmie, R. Lill, and D.F. Bishop Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia with disruption of cytosolic iron-sulfur protein maturation Blood 96 2000 3256 3264
10. P. Bénit, A. Slama, F. Cartault, I. Giurgea, D. Chretien, S. Lebon, C. Marsac, A. Munnich, A. Rötig, and P. Rustin Mutant NDUFS3 subunit of mitochondrial complex I causes Leigh syndrome J. Med. Genet. 41 2004 14 17
11. M. Bugiani, V. Tiranti, L. Farina, G. Uziel, and M. Zeviani Novel mutations in COX15 in a long surviving Leigh syndrome patient with cytochrome c oxidase deficiency J. Med. Genet. 42 2005 e28
12. F.A. Bundschuh, A. Hannappel, O. Anderka, and B. Ludwig Surf1, associated with Leigh syndrome in humans, is a heme-binding protein in bacterial oxidase biogenesis J. Biol. Chem. 284 2009 25735 25741
13. Y. Bykhovskaya, K. Casas, E. Mengesha, A. Inbal, and N. Fischel-Ghodsian Missense mutation in pseudouridine synthase 1 (PUS1) causes mitochondrial myopathy and sideroblastic anemia (MLASA) Am. J. Hum. Genet. 74 2004 1303 1308
14. S.E. Calvo, E.J. Tucker, A.G. Compton, D.M. Kirby, G. Crawford, N.P. Burtt, M. Rivas, C. Guiducci, D.L. Bruno, and O.A. Goldberger High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency Nat. Genet. 42 2010 851 858
15. C. Camaschella, A. Campanella, L. De Falco, L. Boschetto, R. Merlini, L. Silvestri, S. Levi, and A. Iolascon The human counterpart of zebrafish shiraz shows sideroblastic-like microcytic anemia and iron overload Blood 110 2007 1353 1358
16. J.M. Cameron, A. Janer, V. Levandovskiy, N. Mackay, T.A. Rouault, W.H. Tong, I. Ogilvie, E.A. Shoubridge, and B.H. Robinson Mutations in iron-sulfur cluster scaffold genes NFU1 and BOLA3 cause a fatal deficiency of multiple respiratory chain and 2-oxoacid dehydrogenase enzymes Am. J. Hum. Genet. 89 2011 486 495
17. W. Chen, P.N. Paradkar, L. Li, E.L. Pierce, N.B. Langer, N. Takahashi-Makise, B.B. Hyde, O.S. Shirihai, D.M. Ward, J. Kaplan, and B.H. Paw Abcb10 physically interacts with mitoferrin-1 (Slc25a37) to enhance its stability and function in the erythroid mitochondria Proc. Natl. Acad. Sci. USA 106 2009 16263 16268
18. P.D. Cotter, M. Baumann, and D.F. Bishop Enzymatic defect in "X-linked" sideroblastic anemia: molecular evidence for erythroid delta-aminolevulinate synthase deficiency Proc. Natl. Acad. Sci. USA 89 1992 4028 4032
19. R. Covian, and B.L. Trumpower Regulatory interactions in the dimeric cytochrome bc(1) complex: the advantages of being a twin Biochim. Biophys. Acta 1777 2008 1079 1091
20. D.R. Crooks, S.Y. Jeong, W.H. Tong, M.C. Ghosh, H. Olivierre, R.G. Haller, and T.A. Rouault Tissue specificity of a human mitochondrial disease: differentiation-enhanced mis-splicing of the Fe-S scaffold gene ISCU renders patient cells more sensitive to oxidative stress in ISCU myopathy J. Biol. Chem. 287 2012 40119 40130
21. S.C. Dodani, S.C. Leary, P.A. Cobine, D.R. Winge, and C.J. Chang A targetable fluorescent sensor reveals that copper-deficient SCO1 and SCO2 patient cells prioritize mitochondrial copper homeostasis J. Am. Chem. Soc. 133 2011 8606 8616
22. J.A. Duce, A. Tsatsanis, M.A. Cater, S.A. James, E. Robb, K. Wikhe, S.L. Leong, K. Perez, T. Johanssen, and M.A. Greenough Iron-export ferroxidase activity of β-amyloid precursor protein is inhibited by zinc in Alzheimer's disease Cell 142 2010 857 867
23. K.H. Ebrahimi, P.L. Hagedoorn, and W.R. Hagen A synthetic peptide with the putative iron binding motif of amyloid precursor protein (APP) does not catalytically oxidize iron PLoS ONE 7 2012 e40287
24. L. Faes, and G. Callewaert Mitochondrial dysfunction in familial amyotrophic lateral sclerosis J. Bioenerg. Biomembr. 43 2011 587 592
25. M.D. Fleming Congenital sideroblastic anemias: iron and heme lost in mitochondrial translation Hematology (Am Soc Hematol Educ Program) 2011 2011 525 531
26. F. Foury, and T. Roganti Deletion of the mitochondrial carrier genes MRS3 and MRS4 suppresses mitochondrial iron accumulation in a yeast frataxin-deficient strain J. Biol. Chem. 277 2002 24475 24483
27. C. Gelling, I.W. Dawes, N. Richhardt, R. Lill, and U. Mühlenhoff Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes Mol. Cell. Biol. 28 2008 1851 1861
28. D.L. Guernsey, H. Jiang, D.R. Campagna, S.C. Evans, M. Ferguson, M.D. Kellogg, M. Lachance, M. Matsuoka, M. Nightingale, and A. Rideout Mutations in mitochondrial carrier family gene SLC25A38 cause nonsyndromic autosomal recessive congenital sideroblastic anemia Nat. Genet. 41 2009 651 653
29. T.B. Haack, B. Rolinski, B. Haberberger, F. Zimmermann, J. Schum, V. Strecker, E. Graf, U. Athing, T. Hoppen, and I. Wittig Homozygous missense mutation in BOLA3 causes multiple mitochondrial dysfunctions syndrome in two siblings J. Inherit. Metab. Dis. 36 2012 55 62
30. M.B. Hartig, A. Iuso, T. Haack, T. Kmiec, E. Jurkiewicz, K. Heim, S. Roeber, V. Tarabin, S. Dusi, and M. Krajewska-Walasek Absence of an orphan mitochondrial protein, c19orf12, causes a distinct clinical subtype of neurodegeneration with brain iron accumulation Am. J. Hum. Genet. 89 2011 543 550
31. N. Hegde, M.W. Rich, and C. Gayomali The cardiomyopathy of iron deficiency Tex. Heart Inst. J. 33 2006 340 344
32. V. Helias, C. Saison, B.A. Ballif, T. Peyrard, J. Takahashi, H. Takahashi, M. Tanaka, J.C. Deybach, H. Puy, and M. Le Gall ABCB6 is dispensable for erythropoiesis and specifies the new blood group system Langereis Nat. Genet. 44 2012 170 173
33. M.W. Hentze, M.U. Muckenthaler, B. Galy, and C. Camaschella Two to tango: regulation of Mammalian iron metabolism Cell 142 2010 24 38
34. J.M. Herrmann, and J. Riemer Mitochondrial disulfide relay: redox-regulated protein import into the intermembrane space J. Biol. Chem. 287 2012 4426 4433
35. R.C. Hider, and X.L. Kong Glutathione: a key component of the cytoplasmic labile iron pool Biometals 24 2011 1179 1187
36. M.L. Huang, E.M. Becker, M. Whitnall, Y. Suryo Rahmanto, P. Ponka, and D.R. Richardson Elucidation of the mechanism of mitochondrial iron loading in Friedreich's ataxia by analysis of a mouse mutant Proc. Natl. Acad. Sci. USA 106 2009 16381 16386
37. M.A. Huynen, C.A. Spronk, T. Gabaldón, and B. Snel Combining data from genomes, Y2H and 3D structure indicates that BolA is a reductase interacting with a glutaredoxin FEBS Lett. 579 2005 591 596
38. Y. Ichikawa, M. Bayeva, M. Ghanefar, V. Potini, L. Sun, R.K. Mutharasan, R. Wu, A. Khechaduri, T. Jairaj Naik, and H. Ardehali Disruption of ATP-binding cassette B8 in mice leads to cardiomyopathy through a decrease in mitochondrial iron export Proc. Natl. Acad. Sci. USA 109 2012 4152 4157
39. S.Y. Jeong, D.R. Crooks, H. Wilson-Ollivierre, M.C. Ghosh, R. Sougrat, J. Lee, S. Cooperman, J.B. Mitchell, C. Beaumont, and T.A. Rouault Iron insufficiency compromises motor neurons and their mitochondrial function in Irp2-null mice PLoS ONE 6 2011 e25404
40. H. Kawamata, and G. Manfredi Different regulation of wild-type and mutant Cu,Zn superoxide dismutase localization in mammalian mitochondria Hum. Mol. Genet. 17 2008 3303 3317
41. H. Kawamata, and G. Manfredi Import, maturation, and function of SOD1 and its copper chaperone CCS in the mitochondrial intermembrane space Antioxid. Redox Signal. 13 2010 1375 1384
42. B.E. Kim, M.L. Turski, Y. Nose, M. Casad, H.A. Rockman, and D.J. Thiele Cardiac copper deficiency activates a systemic signaling mechanism that communicates with the copper acquisition and storage organs Cell Metab. 11 2010 353 363
43. L.M. Klevay Cardiovascular disease from copper deficiency - a history J. Nutr. 130 2S, Suppl 2000 489S 492S
44. P.C. Krishnamurthy, G. Du, Y. Fukuda, D. Sun, J. Sampath, K.E. Mercer, J. Wang, B. Sosa-Pineda, K.G. Murti, and J.D. Schuetz Identification of a mammalian mitochondrial porphyrin transporter Nature 443 2006 586 589
45. J.B. Lamarche, M. Côté, and B. Lemieux The cardiomyopathy of Friedreich's ataxia morphological observations in 3 cases Can. J. Neurol. Sci. 7 1980 389 396
46. S.C. Leary, P.A. Cobine, B.A. Kaufman, G.H. Guercin, A. Mattman, J. Palaty, G. Lockitch, D.R. Winge, P. Rustin, R. Horvath, and E.A. Shoubridge The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis Cell Metab. 5 2007 9 20
47. S.C. Leary, F. Sasarman, T. Nishimura, and E.A. Shoubridge Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1 Hum. Mol. Genet. 18 2009 2230 2240
48. S.C. Leary, D.R. Winge, and P.A. Cobine "Pulling the plug" on cellular copper: the role of mitochondria in copper export Biochim. Biophys. Acta 1793 2009 146 153
49. S. Levi, B. Corsi, M. Bosisio, R. Invernizzi, A. Volz, D. Sanford, P. Arosio, and J. Drysdale A human mitochondrial ferritin encoded by an intronless gene J. Biol. Chem. 276 2001 24437 24440
50. Y. Li, T.T. Huang, E.J. Carlson, S. Melov, P.C. Ursell, J.L. Olson, L.J. Noble, M.P. Yoshimura, C. Berger, and P.H. Chan Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase Nat. Genet. 11 1995 376 381
51. H. Li, D.T. Mapolelo, N.N. Dingra, G. Keller, P.J. Riggs-Gelasco, D.R. Winge, M.K. Johnson, and C.E. Outten Histidine 103 in Fra2 is an iron-sulfur cluster ligand in the [2Fe-2S] Fra2-Grx3 complex and is required for in vivo iron signaling in yeast J. Biol. Chem. 286 2011 867 876
52. R. Lill, K. Diekert, A. Kaut, H. Lange, W. Pelzer, C. Prohl, and G. Kispal The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins Biol. Chem. 380 1999 1157 1166
53. R. Lill, B. Hoffmann, S. Molik, A.J. Pierik, N. Rietzschel, O. Stehling, M.A. Uzarska, H. Webert, C. Wilbrecht, and U. Mühlenhoff The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism Biochim. Biophys. Acta 1823 2012 1491 1508
54. J. Loeffen, J. Smeitink, R. Triepels, R. Smeets, M. Schuelke, R. Sengers, F. Trijbels, B. Hamel, R. Mullaart, and L. van den Heuvel The first nuclear-encoded complex I mutation in a patient with Leigh syndrome Am. J. Hum. Genet. 63 1998 1598 1608
55. A.B. Maxfield, D.N. Heaton, and D.R. Winge Cox17 is functional when tethered to the mitochondrial inner membrane J. Biol. Chem. 279 2004 5072 5080
56. M. Mimaki, X. Wang, M. McKenzie, D.R. Thorburn, and M.T. Ryan Understanding mitochondrial complex I assembly in health and disease Biochim. Biophys. Acta 1817 2012 851 862
57. F. Mochel, M.A. Knight, W.H. Tong, D. Hernandez, K. Ayyad, T. Taivassalo, P.M. Andersen, A. Singleton, T.A. Rouault, K.H. Fischbeck, and R.G. Haller Splice mutation in the iron-sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance Am. J. Hum. Genet. 82 2008 652 660
58. U. Mühlenhoff, J.A. Stadler, N. Richhardt, A. Seubert, T. Eickhorst, R.J. Schweyen, R. Lill, and G. Wiesenberger A specific role of the yeast mitochondrial carriers MRS3/4p in mitochondrial iron acquisition under iron-limiting conditions J. Biol. Chem. 278 2003 40612 40620
59. A. Nandal, J.C. Ruiz, P. Subramanian, S. Ghimire-Rijal, R.A. Sinnamon, T.L. Stemmler, R.K. Bruick, and C.C. Philpott Activation of the HIF prolyl hydroxylase by the iron chaperones PCBP1 and PCBP2 Cell Metab. 14 2011 647 657
60. A. Navarro-Sastre, F. Tort, O. Stehling, M.A. Uzarska, J.A. Arranz, M. Del Toro, M.T. Labayru, J. Landa, A. Font, and J. Garcia-Villoria A fatal mitochondrial disease is associated with defective NFU1 function in the maturation of a subset of mitochondrial Fe-S proteins Am. J. Hum. Genet. 89 2011 656 667
61. T. Nevitt, H. Ohrvik, and D.J. Thiele Charting the travels of copper in eukaryotes from yeast to mammals Biochim. Biophys. Acta 1823 2012 1580 1593
62. G. Nie, A.D. Sheftel, S.F. Kim, and P. Ponka Overexpression of mitochondrial ferritin causes cytosolic iron depletion and changes cellular iron homeostasis Blood 105 2005 2161 2167
63. M. Nikpour, C. Scharenberg, A. Liu, S. Conte, M. Karimi, T. Mortera-Blanco, V. Giai, M. Fernandez-Mercado, E. Papaemmanuil, and K. Högstrand The transporter ABCB7 is a mediator of the phenotype of acquired refractory anemia with ring sideroblasts Leukemia 2012 10.1038/leu.2012.298 in press. Published online October 16, 2012
64. A. Nordin, E. Larsson, L.E. Thornell, and M. Holmberg Tissue-specific splicing of ISCU results in a skeletal muscle phenotype in myopathy with lactic acidosis, while complete loss of ISCU results in early embryonic death in mice Hum. Genet. 129 2011 371 378
65. A. Olsson, L. Lind, L.E. Thornell, and M. Holmberg Myopathy with lactic acidosis is linked to chromosome 12q23.3-24.11 and caused by an intron mutation in the ISCU gene resulting in a splicing defect Hum. Mol. Genet. 17 2008 1666 1672
66. L.C. Papadopoulou, C.M. Sue, M.M. Davidson, K. Tanji, I. Nishino, J.E. Sadlock, S. Krishna, W. Walker, J. Selby, and D.M. Glerum Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene Nat. Genet. 23 1999 333 337
67. P.N. Paradkar, K.B. Zumbrennen, B.H. Paw, D.M. Ward, and J. Kaplan Regulation of mitochondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2 Mol. Cell. Biol. 29 2009 1007 1016
68. V.A. Patil, J.L. Fox, V.M. Gohil, D.R. Winge, and M.L. Greenberg Loss of cardiolipin leads to perturbation of mitochondrial and cellular iron homeostasis J. Biol. Chem. 288 2012 1696 1705
69. R.M. Payne, and G.R. Wagner Cardiomyopathy in Friedreich ataxia: clinical findings and research J. Child Neurol. 27 2012 1179 1186
70. D.H. Petering, K.L. Stemmer, S. Lyman, S. Krezoski, and H.G. Petering Iron deficiency in growing male rats: a cause of development of cardiomyopathy Ann. Nutr. Metab. 34 1990 232 243
71. P. Ponka, A. Wilczynska, and H.M. Schulman Iron utilization in rabbit reticulocytes. A study using succinylacetone as an inhibitor or heme synthesis Biochim. Biophys. Acta 720 1982 96 105
72. H. Puccio, D. Simon, M. Cossée, P. Criqui-Filipe, F. Tiziano, J. Melki, C. Hindelang, R. Matyas, P. Rustin, and M. Koenig Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits Nat. Genet. 27 2001 181 186
73. L.G. Riley, S. Cooper, P. Hickey, J. Rudinger-Thirion, M. McKenzie, A. Compton, S.C. Lim, D. Thorburn, M.T. Ryan, and R. Giegé Mutation of the mitochondrial tyrosyl-tRNA synthetase gene, YARS2, causes myopathy, lactic acidosis, and sideroblastic anemia - MLASA syndrome Am. J. Hum. Genet. 87 2010 52 59
74. A. Rötig, V. Cormier, F. Koll, C.E. Mize, J.M. Saudubray, A. Veerman, H.A. Pearson, and A. Munnich Site-specific deletions of the mitochondrial genome in the Pearson marrow-pancreas syndrome Genomics 10 1991 502 504
75. T.A. Rouault The role of iron regulatory proteins in mammalian iron homeostasis and disease Nat. Chem. Biol. 2 2006 406 414
76. T.A. Rouault Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease Dis. Model Mech. 5 2012 155 164
77. T.A. Rouault, and W.H. Tong Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis Nat. Rev. Mol. Cell Biol. 6 2005 345 351
78. J. Rutter, D.R. Winge, and J.D. Schiffman Succinate dehydrogenase - Assembly, regulation and role in human disease Mitochondrion 10 2010 393 401
79. A.A. Salahudeen, J.W. Thompson, J.C. Ruiz, H.W. Ma, L.N. Kinch, Q. Li, N.V. Grishin, and R.K. Bruick An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis Science 326 2009 722 726
80. M. Schlame, D. Rua, and M.L. Greenberg The biosynthesis and functional role of cardiolipin Prog. Lipid Res. 39 2000 257 288
81. S. Schmucker, A. Martelli, F. Colin, A. Page, M. Wattenhofer- Donzé, L. Reutenauer, and H. Puccio Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex PLoS ONE 6 2011 e16199
82. A. Seyda, R.F. Newbold, T.J. Hudson, A. Verner, N. MacKay, S. Winter, A. Feigenbaum, S. Malaney, D. Gonzalez-Halphen, A.P. Cuthbert, and B.H. Robinson A novel syndrome affecting multiple mitochondrial functions, located by microcell-mediated transfer to chromosome 2p14-2p13 Am. J. Hum. Genet. 68 2001 386 396
83. D.I. Shah, N. Takahashi-Makise, J.D. Cooney, L. Li, I.J. Schultz, E.L. Pierce, A. Narla, A. Seguin, S.M. Hattangadi, and A.E. Medlock Mitochondrial Atpif1 regulates haem synthesis in developing erythroblasts Nature 491 2012 608 612
84. G.C. Shaw, J.J. Cope, L. Li, K. Corson, C. Hersey, G.E. Ackermann, B. Gwynn, A.J. Lambert, R.A. Wingert, and D. Traver Mitoferrin is essential for erythroid iron assimilation Nature 440 2006 96 100
85. H. Shi, K.Z. Bencze, T.L. Stemmler, and C.C. Philpott A cytosolic iron chaperone that delivers iron to ferritin Science 320 2008 1207 1210
86. Y. Shi, M. Ghosh, G. Kovtunovych, D.R. Crooks, and T.A. Rouault Both human ferredoxins 1 and 2 and ferredoxin reductase are important for iron-sulfur cluster biogenesis Biochim. Biophys. Acta 1823 2012 484 492
87. W.H. Tong, G.N. Jameson, B.H. Huynh, and T.A. Rouault Subcellular compartmentalization of human Nfu, an iron-sulfur cluster scaffold protein, and its ability to assemble a [4Fe-4S] cluster Proc. Natl. Acad. Sci. USA 100 2003 9762 9767
88. C.L. Tsai, and D.P. Barondeau Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex Biochemistry 49 2010 9132 9139
89. I. Valnot, S. Osmond, N. Gigarel, B. Mehaye, J. Amiel, V. Cormier-Daire, A. Munnich, J.P. Bonnefont, P. Rustin, and A. Rötig Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy Am. J. Hum. Genet. 67 2000 1104 1109
90. A.A. Vashisht, K.B. Zumbrennen, X. Huang, D.N. Powers, A. Durazo, D. Sun, N. Bhaskaran, A. Persson, M. Uhlen, and O. Sangfelt Control of iron homeostasis by an iron-regulated ubiquitin ligase Science 326 2009 718 721
91. C. Vilain, C. Rens, A. Aeby, D. Balériaux, P. Van Bogaert, G. Remiche, J. Smet, R. Van Coster, M. Abramowicz, and I. Pirson A novel NDUFV1 gene mutation in complex I deficiency in consanguineous siblings with brainstem lesions and Leigh syndrome Clin. Genet. 82 2012 264 270
92. K. Volz The functional duality of iron regulatory protein 1 Curr. Opin. Struct. Biol. 18 2008 106 111
93. Y. Wang, V. Hodgkinson, S. Zhu, G.A. Weisman, and M.J. Petris Advances in the understanding of mammalian copper transporters Adv. Nutr. 2 2011 129 137
94. N. Wiedemann, E. Urzica, B. Guiard, H. Müller, C. Lohaus, H.E. Meyer, M.T. Ryan, C. Meisinger, U. Mühlenhoff, R. Lill, and N. Pfanner Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins EMBO J. 25 2006 184 195
95. D.R. Winge Sealing the mitochondrial respirasome Mol. Cell. Biol. 32 2012 2647 2652
96. R.A. Wingert, J.L. Galloway, B. Barut, H. Foott, P. Fraenkel, J.L. Axe, G.J. Weber, K. Dooley, A.J. Davidson, B. Schmid Tübingen 2000 Screen Consortium Deficiency of glutaredoxin 5 reveals Fe-S clusters are required for vertebrate haem synthesis Nature 436 2005 1035 1039
97. L.J. Wong Mitochondrial syndromes with leukoencephalopathies Semin. Neurol. 32 2012 55 61
98. C.K. Wu, H.A. Dailey, J.P. Rose, A. Burden, V.M. Sellers, and B.C. Wang The 2.0 A structure of human ferrochelatase, the terminal enzyme of heme biosynthesis Nat. Struct. Biol. 8 2001 156 160
99. H. Ye, S.Y. Jeong, M.C. Ghosh, G. Kovtunovych, L. Silvestri, D. Ortillo, N. Uchida, J. Tisdale, C. Camaschella, and T.A. Rouault Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human erythroblasts J. Clin. Invest. 120 2010 1749 1761
100. S. Yoshikawa, K. Muramoto, and K. Shinzawa-Itoh Proton-pumping mechanism of cytochrome C oxidase Annu. Rev. Biophys. 40 2011 205 223
101. B. Zhou, S.K. Westaway, B. Levinson, M.A. Johnson, J. Gitschier, and S.J. Hayflick A novel pantothenate kinase gene (PANK2) is defective in Hallervorden-Spatz syndrome Nat. Genet. 28 2001 345 349