Mitochondrial iron-sulfur protein biogenesis and human disease

Biochimie

Volumn 100, Issue 1, 2014, Pages 61-77

  Stehling, Oliver ^a   Wilbrecht, Claudia ^a   Lill, Roland ^a,b,c  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c Offensive for the Development of Scientific and Economic Excellence of the State of Hesse LOEWE   (Germany)

Author keywords

Genome integrity; Iron regulation; Iron sulfur cluster; Mitochondrial ISC system

Indexed keywords

BACTERIAL PROTEIN; FERREDOXIN II; IRON; IRON SULFUR PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

BIOGENESIS; CELL FUNCTION; CELL MATURATION; CELL METABOLISM; CEREBELLAR ATAXIA; DISEASES; ERYTHROPOIETIC PROTOPORPHYRIA; GENE MUTATION; GENETIC CODE; HEREDITARY MUSCLE DISEASE; HUMAN; LACTIC ACIDOSIS; MITOCHONDRIAL ENCEPHALOMYOPATHY; MITOCHONDRION; MULTIPLE MITOCHONDRIAL DYSFUNCTION SYNDROME; MYOPATHY; OXIDATIVE PHOSPHORYLATION; PROTEIN FOLDING; PROTEIN SYNTHESIS; REFRACTORY ANEMIA WITH RINGED SIDEROBLASTS; REVIEW; SIDEROBLASTIC ANEMIA; SYNDROME; X LINKED SIDEROBLASTIC ANEMIA;

GENOME INTEGRITY; IRON REGULATION; IRON-SULFUR CLUSTER; MITOCHONDRIAL ISC SYSTEM;

ANIMALS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; IRON; IRON-SULFUR PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MOLECULAR CHAPERONES; MUTATION; PROTEIN BIOSYNTHESIS;

EID: 84897000909     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2014.01.010     Document Type: Review

References (177)

1. K. Volz, The functional duality of iron regulatory protein 1, Curr. Opin. Struct. Biol. 18 (2008) 106-111.
2. J.L. Giel, A.D. Nesbit, E.L. Mettert, A.S. Fleischhacker, B.T. Wanta, P.J. Kiley, Regulation of ironesulphur cluster homeostasis through transcriptional control of the Isc pathway by [2Fee2S]-IscR in Escherichia coli, Mol. Microbiol. 87 (2012) 478-492.
3. P.J. Kiley, H. Beinert, Oxygen sensing by the global regulator, FNR: the role of the ironesulfur cluster, FEMS Microbiol. Rev. 22 (1998) 341-352. (Pubitemid 29074341)
4. B. Zhang, J.C. Crack, S. Subramanian, J. Green, A.J. Thomson, N.E. Le Brun, M.K. Johnson, Reversible cycling between cysteine persulfide-ligated [2Fe-2S] and cysteine-ligated [4Fe-4S] clusters in the FNR regulatory protein, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 15734-15739.
5. D.J. Netz, C.M. Stith, M. Stumpfig, G. Kopf, D. Vogel, H.M. Genau, J.L. Stodola, R. Lill, P.M. Burgers, A.J. Pierik, Eukaryotic DNA polymerases require an irone sulfur cluster for the formation of active complexes, Nat. Chem. Biol. 8 (2012) 125-132.
6. J. Rudolf, V. Makrantoni, W.J. Ingledew, M.J. Stark, M.F. White, The DNA repair helicases XPD and FancJ have essential ironesulfur domains, Mol. Cell. 23 (2006) 801-808. (Pubitemid 44344515)
7. Y. Hu, M.W. Ribbe, Nitrogenase assembly, Biochim. Biophys. Acta 1827 (2013) 1112-1122.
8. J.W. Peters, J.B. Broderick, Emerging paradigms for complex ironesulfur cofactor assembly and insertion, Annu. Rev. Biochem. 81 (2012) 429-450.
9. M. Müller, W. Martin, The genome of Rickettsia prowazekii and some thoughts on the origin of mitochondria and hydrogenosomes, BioEssays 21 (1999) 377-381. (Pubitemid 29223309)
10. R. Lill, Function and biogenesis ironesulphur proteins, Nature 460 (2009) 831-838.
11. R. Lill, B. Hoffmann, S. Molik, A.J. Pierik, N. Rietzschel, O. Stehling, M.A. Uzarska, H. Webert, C. Wilbrecht, U. Mühlenhoff, The role of mitochondria in cellular ironesulfur protein biogenesis and iron metabolism, Biochim. Biophys. Acta 1823 (2012) 1491-1508.
12. R. Lill, U. Mühlenhoff, Maturation of ironesulfur proteins in eukaryotes: mechanisms, connected processes, and diseases, Annu. Rev. Biochem. 77 (2008) 669-700.
13. O. Stehling, R. Lill, The role of mitochondria in cellular ironesulfur protein biogenesis: mechanisms, connected processes, and diseases, Cold Spring Harbor Perspect. Biol. 5 (2013) a011312.
14. G. Kispal, P. Csere, C. Prohl, R. Lill, The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins, EMBO J. 18 (1999) 3981-3989. (Pubitemid 29335851)
15. R. Miao, H. Kim, U.M. Koppolu, E.A. Ellis, R.A. Scott, P.A. Lindahl, Biophysical characterization of the iron in mitochondria from Atm1p-depleted Saccharomyces cerevisiae, Biochemistry 48 (2009) 9556-9568.
16. H. Lange, T. Lisowsky, J. Gerber, U. Muhlenhoff, G. Kispal, R. Lill, An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins, EMBO Rep. 2 (2001) 715-720. (Pubitemid 32798715)
17. K. Sipos, H. Lange, Z. Fekete, P. Ullmann, R. Lill, G. Kispal, Maturation of cytosolic ironesulfur proteins requires glutathione, J. Biol. Chem. 277 (2002) 26944-26949. (Pubitemid 34951704)
18. A.K. Sharma, L.J. Pallesen, R.J. Spang, W.E. Walden, Cytosolic ironesulfur cluster assembly (CIA) system: factors, mechanism, and relevance to cellular iron regulation, J. Biol. Chem. 285 (2010) 26745-26751.
19. D.J. Netz, J. Mascarenhas, O. Stehling, A.J. Pierik, R. Lill, Maturation of cytosolic and nuclear ironesulfur proteins, Trends Cell. Biol., in press.
20. S.A. Garland, K. Hoff, L.E. Vickery, V.C. Culotta, Saccharomyces cerevisiae ISU1 and ISU2: members of a well-conserved gene family for irone sulfur cluster assembly, J. Mol. Biol. 294 (1999) 897-907. (Pubitemid 30000383)
21. U. Mühlenhoff, J. Gerber, N. Richhardt, R. Lill, Components involved in assembly and dislocation of irone sulfur clusters on the scaffold protein Isu1p, EMBO J. 22 (2003) 4815-4825. (Pubitemid 37162917)
22. L. Zheng, R.H. White, V.L. Cash, D.R. Dean, Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product, Biochemistry 33 (1994) 4714-4720. (Pubitemid 24145122)
23. J.T. Kaiser, T. Clausen, G.P. Bourenkow, H.D. Bartunik, S. Steinbacher, R. Huber, Crystal structure of a NifS-like protein from Thermotoga maritima: implications for iron sulphur cluster assembly, J. Mol. Biol. 297 (2000) 451-464.
24. A.C. Adam, C. Bornhovd, H. Prokisch, W. Neupert, K. Hell, The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria, EMBO J. 25 (2006) 174-183. (Pubitemid 43077306)
25. N. Wiedemann, E. Urzica, B. Guiard, H. Muller, C. Lohaus, H.E. Meyer, M.T. Ryan, C. Meisinger, U. Muhlenhoff, R. Lill, N. Pfanner, Essential role of Isd11 in mitochondrial ironesulfur cluster synthesis on Isu scaffold proteins, EMBO J. 25 (2006) 184-195. (Pubitemid 43077307)
26. H. Angerer, The superfamily of mitochondrial complex1-LYR motif-containing (LYRM) proteins, Biochem. Soc. Trans. 41 (2013) 1335-1341.
27. K. Terali, R.L. Beavil, R.W. Pickersgill, M. van der Giezen, The effect of the adaptor protein Isd11 on the quaternary structure of the eukaryotic cysteine desulphurase Nfs1, Biochem. Biophys. Res. Commun. 440 (2013) 235-240.
28. H. Lange, A. Kaut, G. Kispal, R. Lill, A mitochondrial ferredoxin is essential for biogenesis of cellular ironesulfur proteins, Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 1050-1055. (Pubitemid 30080810)
29. J. Li, S. Saxena, D. Pain, A. Dancis, Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis, J. Biol. Chem. 276 (2001) 1503-1509. (Pubitemid 32096584)
30. A.D. Sheftel, O. Stehling, A.J. Pierik, H.P. Elsasser, U. Muhlenhoff, H. Webert, A. Hobler, F. Hannemann, R. Bernhardt, R. Lill, Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis, Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 11775-11780.
31. Y. Shi, M. Ghosh, G. Kovtunovych, D.R. Crooks, T.A. Rouault, Both human ferredoxins 1 and 2 and ferredoxin reductase are important for ironesulfur cluster biogenesis, Biochim. Biophys. Acta 1823 (2012) 484-492.
32. H. Lange, G. Kispal, R. Lill, Mechanism of iron transport to the site of heme synthesis inside yeast mitochondria, J. Biol. Chem. 274 (1999) 18989-18996.
33. F. Foury, T. Roganti, Deletion of the mitochondrial carrier genes MRS3 and MRS4 suppresses mitochondrial iron accumulation in a yeast frataxindeficient strain, J. Biol. Chem. 277 (2002) 24475-24483. (Pubitemid 34951972)
34. U. Mühlenhoff, J.A. Stadler, N. Richhardt, A. Seubert, T. Eickhorst, R.J. Schweyen, R. Lill, G. Wiesenberger, A speci fic role of the yeast mitochondrial carriers MRS3/4p in mitochondrial iron acquisition under iron-limiting conditions, J. Biol. Chem. 278 (2003) 40612-40620. (Pubitemid 37280874)
35. G.C. Shaw, J.J. Cope, L. Li, K. Corson, C. Hersey, G.E. Ackermann, B. Gwynn, A.J. Lambert, R.A. Wingert, D. Traver, N.S. Trede, B.A. Barut, Y. Zhou, E. Minet, A. Donovan, A. Brownlie, R. Balzan, M.J. Weiss, L.L. Peters, J. Kaplan, L.I. Zon, B.H. Paw, Mitoferrin is essential for erythroid iron assimilation, Nature 440 (2006) 96-100. (Pubitemid 43336274)
36. P.N. Paradkar, K.B. Zumbrennen, B.H. Paw, D.M. Ward, J. Kaplan, Regulation of mitochondrial iron import through differential turnover of mitoferrin 1 and mitoferrin 2, Mol. Cell. Biol. 29 (2009) 1007-1016.
37. E.M. Froschauer, N. Rietzschel, M.R. Hassler, M. Binder, R.J. Schweyen, R. Lill, U. Muhlenhoff, G. Wiesenberger, The mitochondrial carrier Rim2 co-imports pyrimidine nucleotides and iron, Biochem. J. 455 (2013) 57-65.
38. J. Gerber, U. Mühlenhoff, R. Lill, An interaction between frataxin and Isu1/ Nfs1 that is crucial for Fe/S cluster synthesis on Isu1, EMBO Rep. 4 (2003) 906-911. (Pubitemid 37304409)
39. S. Schmucker, A. Martelli, F. Colin, A. Page, M. Wattenhofer-Donze, L. Reutenauer, H. Puccio, Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 ironesulfur assembly complex, PLoS One 6 (2011) e16199.
40. C.L. Tsai, D.P. Barondeau, Human frataxin is an allosteric switch that activates the Fe eS cluster biosynthetic complex, Biochemistry 49 (2010) 9132-9139.
41. F. Colin, A. Martelli, M. Clemancey, J.M. Latour, S. Gambarelli, L. Zeppieri, C. Birck, A. Page, H. Puccio, S. Ollagnier de Choudens, Mammalian frataxin controls sulfur production and iron entry during de novo Fe4S4 cluster assembly, J. Am. Chem. Soc. 135 (2013) 733-740.
42. R. Dutkiewicz, J. Marszalek, B. Schilke, E.A. Craig, R. Lill, U. Mühlenhoff, The Hsp70 chaperone Ssq1p is dispensable for ironesulfur cluster formation on the scaffold protein Isu1p, J. Biol. Chem. 281 (2006) 7801-7808. (Pubitemid 43847394)
43. B. Schilke, B. Williams, H. Knieszner, S. Pukszta, P. D'Silva, E.A. Craig, J. Marszalek, Evolution of mitochondrial chaperones utilized in FeeS cluster biogenesis, Curr. Biol. 16 (2006) 1660-1665. (Pubitemid 44233273)
44. H.H. Kampinga, E.A. Craig, The HSP70 chaperone machinery: J proteins as drivers of functional specificity, Nat. Rev. Mol. Cell. Biol. 11 (2010) 579-592.
45. S. Pukszta, B. Schilke, R. Dutkiewicz, J. Kominek, K. Moczulska, B. Stepien, K.G. Reitenga, J.M. Bujnicki, B. Williams, E.A. Craig, J. Marszalek, Co-evolution-driven switch of J-protein specificity towards an Hsp70 partner, EMBO Rep. 11 (2010) 360-365.
46. K.G. Hoff, J.R. Cupp-Vickery, L.E. Vickery, Contributions of the LPPVK motif of the ironesulfur template protein IscU to interactions with the Hsc66-Hsc20 chaperone system, J. Biol. Chem. 278 (2003) 37582-37589. (Pubitemid 37175281)
47. R. Dutkiewicz, B. Schilke, S. Cheng, H. Knieszner, E.A. Craig, J. Marszalek, Sequence-specific interaction between mitochondrial FeeS scaffold protein Isu and Hsp70 Ssq1 is essential for their in vivo function, J. Biol. Chem. 279 (2004) 29167-29174. (Pubitemid 38915790)
48. R. Dutkiewicz, B. Schilke, H. Knieszner, W. Walter, E.A. Craig, J. Marszalek, Ssq1, a mitochondrial Hsp70 involved in ironesulfur (Fe/S) center biogenesis. Similarities to and differences from its bacterial counterpart, J. Biol. Chem. 278 (2003) 29719-29727. (Pubitemid 36962358)
49. L.E. Vickery, J.R. Cupp-Vickery, Molecular chaperones HscA/Ssq1 and HscB/Jac1 and their roles in irone sulfur protein maturation, Crit. Rev. Biochem. Mol. Biol. 42 (2007) 95-111. (Pubitemid 46598188)
50. K. Chandramouli, M.K. Johnson, HscA and HscB stimulate [2Fe-2S] cluster transfer from IscU to apoferredoxin in an ATP-dependent reaction, Biochemistry 45 (2006) 11087-11095.
51. P. Shakamuri, B. Zhang, M.K. Johnson, Monothiol glutaredoxins function in storing and transporting [Fe2-2S] clusters assembled on IscU scaffold proteins, J. Am. Chem. Soc. 134 (2012) 15213-15216.
52. S. Bandyopadhyay, F. Gama, M.M. Molina-Navarro, J.M. Gualberto, R. Claxton, S.G. Naik, B.H. Huynh, E. Herrero, J.P. Jacquot, M.K. Johnson, N. Rouhier, Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters, EMBO J. 27 (2008) 1122-1133. (Pubitemid 351508159)
53. C. Johansson, A.K. Roos, S.J. Montano, R. Sengupta, P. Filippakopoulos, K. Guo, F. von Delft, A. Holmgren, U. Oppermann, K.L. Kavanagh, The crystal structure of human GLRX5: ironesulfur cluster co-ordination, tetrameric assembly and monomer activity, Biochem. J. 433 (2011) 303-311.
54. A. Picciocchi, C. Saguez, A. Boussac, C. Cassier-Chauvat, F. Chauvat, CGFS-type monothiol glutaredoxins from the cyanobacterium Synechocystis PCC6803 and other evolutionary distant model organisms possess a glutathioneligated [2Fe-2S] cluster, Biochemistry 46 (2007) 15018-15026. (Pubitemid 350308893)
55. M.A. Uzarska, R. Dutkiewicz, S.A. Freibert, R. Lill, U. Muhlenhoff, The mitochondrial Hsp70 chaperone Ssq1 facilitates Fe/S cluster transfer from Isu1 to Grx5 by complex formation, Mol. Biol. Cell. 24 (2013) 1830-1841.
56. M.T. Rodriguez-Manzaneque, J. Ros, E. Cabiscol, A. Sorribas, E. Herrero, Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae, Mol. Cell. Biol. 19 (1999) 8180-8190. (Pubitemid 30414012)
57. M.T. Rodriguez-Manzaneque, J. Tamarit, G. Belli, J. Ros, E. Herrero, Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes, Mol. Biol. Cell. 13 (2002) 1109-1121. (Pubitemid 34309609)
58. C. Gelling, I.W. Dawes, N. Richhardt, R. Lill, U. Muhlenhoff, Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes, Mol. Cell. Biol. 28 (2008) 1851-1861.
59. U. Mühlenhoff, N. Richter, O. Pines, A.J. Pierik, R. Lill, Specialized function of yeast Isa1 and Isa2 proteins in the maturation of mitochondrial [4Fe-4S] proteins, J. Biol. Chem. 286 (2011) 41205-41216.
60. A.D. Sheftel, C. Wilbrecht, O. Stehling, B. Niggemeyer, H.P. Elsasser, U. Muhlenhoff, R. Lill, The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe-4S] protein maturation, Mol. Biol. Cell. 23 (2012) 1157-1166.
61. K.D. Kim, W.H. Chung, H.J. Kim, K.C. Lee, J.H. Roe, Monothiol glutaredoxin Grx5 interacts with FeeS scaffold proteins Isa1 and Isa2 and supports FeeS assembly and DNA integrity in mitochondria of fission yeast, Biochem. Biophys. Res. Commun. 392 (2010) 467-472.
62. J. Lu, J.P. Bitoun, G. Tan, W. Wang, W. Min, H. Ding, Iron-binding activity of human ironesulfur cluster assembly protein hIscA1, Biochem. J. 428 (2010) 125-131.
63. G. Wu, S.S. Mansy, C. Hemann, R. Hille, K.K. Surerus, J.A. Cowan, Ironesulfur cluster biosynthesis: characterization of Schizosaccharomyces pombe Isa1, J. Biol. Inorg. Chem. 7 (2002) 526-532. (Pubitemid 36067304)
64. V. Gupta, M. Sendra, S.G. Naik, H.K. Chahal, B.H. Huynh, F.W. Outten, M. Fontecave, S. Ollagnier de Choudens, Native Escherichia coli SufA, coexpressed with SufBCDSE, purifi es as a [2Fe-2S] protein and acts as an Fe-S transporter to Fee S target enzymes, J. Am. Chem. Soc. 131 (2009) 6149-6153.
65. B. Py, F. Barras, Building FeeS proteins: bacterial strategies, Nat. Rev. Microbiol. 8 (2010) 436-446.
66. S. Ollagnier-de-Choudens, T. Mattioli, Y. Takahashi, M. Fontecave, Ironesulfur cluster assembly: characterization of IscA and evidence for a specific and functional complex with ferredoxin, J. Biol. Chem. 276 (2001) 22604-22607.
67. W.H. Tong, G.N. Jameson, B.H. Huynh, T.A. Rouault, Subcellular compartmentalization of human Nfu, an ironesulfur cluster scaffold protein, and its ability to assemble a [4Fe-4S] cluster, Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9762-9767. (Pubitemid 37087015)
68. J.M. Cameron, A. Janer, V. Levandovskiy, N. Mackay, T.A. Rouault, W.H. Tong, I. Ogilvie, E.A. Shoubridge, B.H. Robinson, Mutations in ironesulfur 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.
69. A. Navarro-Sastre, F. Tort, O. Stehling, M.A. Uzarska, J.A. Arranz, M. Del Toro, M.T. Labayru, J. Landa, A. Font, J. Garcia-Villoria, B. Merinero, M. Ugarte, L.G. Gutierrez-Solana, J. Campistol, A. Garcia-Cazorla, J. Vaquerizo, E. Riudor, P. Briones, O. Elpeleg, A. Ribes, R. Lill, 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.
70. 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, Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial ironesulfur cluster synthesis, J. Biol. Chem. 283 (2008) 10276-10286.
71. H. Li, C.E. Outten, Monothiol CGFS glutaredoxins and BolA-like proteins: [2Fe-2S] binding partners in iron homeostasis, Biochemistry 51 (2012) 4377-4389.
72. K. Bych, S. Kerscher, D.J. Netz, A.J. Pierik, K. Zwicker, M.A. Huynen, R. Lill, U. Brandt, J. Balk, The ironesulphur protein Ind1 is required for effective complex I assembly, EMBO J. 27 (2008) 1736-1746.
73. A.D. Sheftel, O. Stehling, A.J. Pierik, D.J. Netz, S. Kerscher, H.P. Elsasser, I. Wittig, J. Balk, U. Brandt, R. Lill, Human ind1, an ironesulfur cluster assembly factor for respiratory complex I, Mol. Cell. Biol. 29 (2009) 6059-6073.
74. M.M. Wydro, P. Sharma, J.M. Foster, K. Bych, E.H. Meyer, J. Balk, The evolutionarily conserved ironesulfur protein INDH1 is required for complex I assembly and mitochondrial translation in Arabidopsis, Plant Cell 25 (2013) 4014-4027.
75. M. Cossee, H. Puccio, A. Gansmuller, H. Koutnikova, A. Dierich, M. LeMeur, K. Fischbeck, P. Dolle, M. Koenig, Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation, Hum. Mol. Genet. 9 (2000) 1219-1226. (Pubitemid 30248608)
76. C. Pondarre, B.B. Antiochos, D.R. Campagna, S.L. Clarke, E.L. Greer, K.M. Deck, A. McDonald, A.P. Han, A. Medlock, J.L. Kutok, S.A. Anderson, R.S. Eisenstein, M.D. Fleming, The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic ironesulfur cluster biogenesis, Hum. Mol. Genet. 15 (2006) 953-964. (Pubitemid 43338236)
77. A. Nordin, E. Larsson, L.E. Thornell, 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.
78. C. Camaschella, A. Campanella, L. De Falco, L. Boschetto, R. Merlini, L. Silvestri, S. Levi, A. Iolascon, The human counterpart of zebra fish shiraz shows sideroblastic-like microcytic anemia and iron overload, Blood 110 (2007) 1353-1358. (Pubitemid 47281436)
79. 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, R.G. Haller, Splice mutation in the ironesulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance, Am. J. Hum. Genet. 82 (2008) 652-660.
80. A. Olsson, L. Lind, L.E. Thornell, 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. (Pubitemid 351737170)
81. V. Campuzano, L. Montermini, M.D. Molto, L. Pianese, M. Cossee, F. Cavalcanti, E. Monros, F. Rodius, F. Duclos, A. Monticelli, F. Zara, J. Canizares, H. Koutnikova, S.I. Bidichandani, C. Gellera, A. Brice, P. Trouillas, G. De Michele, A. Filla, R. De Frutos, F. Palau, P.I. Patel, S. Di Donato, J.L. Mandel, S. Cocozza, M. Koenig, M. Pandolfo, Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion, Science 271 (1996) 1423-1427. (Pubitemid 26089479)
82. S. Bekri, G. Kispal, H. Lange, E. Fitzsimons, J. Tolmie, R. Lill, D.F. Bishop, Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia with disruption of cytosolic ironesulfur protein maturation, Blood 96 (2000) 3256-3264.
83. R. Allikmets, W.H. Raskind, A. Hutchinson, N.D. Schueck, M. Dean, 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. (Pubitemid 29189041)
84. S.E. Calvo, E.J. Tucker, A.G. Compton, D.M. Kirby, G. Crawford, N.P. Burtt, M. Rivas, C. Guiducci, D.L. Bruno, O.A. Goldberger, M.C. Redman, E. Wiltshire, C.J. Wilson, D. Altshuler, S.B. Gabriel, M.J. Daly, D.R. Thorburn, V.K. Mootha, High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency, Nat. Genet. 42 (2010) 851-858.
85. A.D. Sheftel, R. Lill, The power plant of the cell is also a smithy: the emerging role of mitochondria in cellular iron homeostasis, Ann. Med. 41 (2009) 82-99.
86. H. Puccio, D. Simon, M. Cossee, P. Criqui-Filipe, F. Tiziano, J. Melki, C. Hindelang, R. Matyas, P. Rustin, M. Koenig, Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and FeeS enzyme deficiency followed by intramitochondrial iron deposits, Nat. Genet. 27 (2001) 181-186. (Pubitemid 32157445)
87. P. Cavadini, G. Biasiotto, M. Poli, S. Levi, R. Verardi, I. Zanella, M. Derosas, R. Ingrassia, M. Corrado, P. Arosio, RNA silencing of the mitochondrial ABCB7 transporter in HeLa cells causes an iron-deficient phenotype with mitochondrial iron overload, Blood 109 (2007) 3552-3559. (Pubitemid 46572549)
88. C.P. Anderson, M. Shen, R.S. Eisenstein, E.A. Leibold, Mammalian iron metabolism and its control by iron regulatory proteins, Biochim. Biophys. Acta 1823 (2012) 1468-1483.
89. A. Sheftel, O. Stehling, R. Lill, Ironesulfur proteins in health and disease, Trends Endocrinol. Metab. 21 (2010) 302-314.
90. M.H. Parkinson, S. Boesch, W. Nachbauer, C. Mariotti, P. Giunti, Clinical features of Friedreich's ataxia: classical and atypical phenotypes, J. Neurochem. 126 (Suppl. 1) (2013) 103-117.
91. A. Martelli, M. Napierala, H. Puccio, Understanding the genetic and molecular pathogenesis of Friedreich's ataxia through animal and cellular models, Dis. Model. Mech. 5 (2012) 165-176.
92. J.H. Willis, G. Isaya, O. Gakh, R.A. Capaldi, M.F. Marusich, Lateral-flow immunoassay for the frataxin protein in Friedreich's ataxia patients and carriers, Mol. Genet. Metab. 94 (2008) 491-497.
93. A. Rötig, P. de Lonlay, D. Chretien, F. Foury, M. Koenig, D. Sidi, A. Munnich, P. Rustin, Aconitase and mitochondrial ironesulphur protein deficiency in Friedreich ataxia, Nat. Genet. 17 (1997) 215-217.
94. L. Lobmayr, D.G. Brooks, R.B. Wilson, Increased IRP1 activity in Friedreich ataxia, Gene 354 (2005) 157-161. (Pubitemid 41116696)
95. J.L. Bradley, J.C. Blake, S. Chamberlain, P.K. Thomas, J.M. Cooper, A.H. Schapira, Clinical, biochemical and molecular genetic correlations in Friedreich's ataxia, Hum. Mol. Genet. 9 (2000) 275-282. (Pubitemid 30052751)
96. K. Li, E.K. Besse, D. Ha, G. Kovtunovych, T.A. Rouault, Iron-dependent regulation of frataxin expression: implications for treatment of Friedreich ataxia, Hum. Mol. Genet. 17 (2008) 2265-2273.
97. G. Uziel, E. Bottacchi, G. Moschen, P. Giovanardi-Rossi, G. Cardace, S. Di Donato, Pyruvate-dehydrogenase complex in ataxic patients: enzyme deficiency in ataxic encephalopathy plus lactic acidosis and normal activity in Friedreich ataxia, Ital. J. Neurol. Sci. 3 (1982) 317-321. (Pubitemid 13155135)
98. B. Bertagnolio, G. Uziel, E. Bottacchi, G. Crenna, A. D' Angelo, S. Di Donato, Friedreich's ataxia II. Biochemical studies in cultured cells, Ital. J. Neurol. Sci. 1 (1980) 239-243. (Pubitemid 11220143)
99. S.B. Melancon, M. Potier, L. Dallaire, P. Rollin, G. Fontaine, B. Grenier, Pyruvate dehydrogenase, lipoamide dehydrogenase and citrate synthase activity in fibroblasts from patients with Friedreich's and Charlevoix-Saguenay ataxia, Can. J. Neurol. Sci. 6 (1979) 241-242. (Pubitemid 9187737)
100. J.P. Blass, R.A. Kark, N.K. Menon, Low activities of the pyruvate and oxoglutarate dehydrogenase complexes in five patients with Friedreich's ataxia, N. Engl. J. Med. 295 (1976) 62-67.
101. D. Simon, H. Seznec, A. Gansmuller, N. Carelle, P. Weber, D. Metzger, P. Rustin, M. Koenig, H. Puccio, Friedreich ataxia mouse models with progressive cerebellar and sensory ataxia reveal autophagic neurodegeneration in dorsal root ganglia, J. Neurosci. 24 (2004) 1987-1995. (Pubitemid 38292812)
102. S. Jiralerspong, Y. Liu, L. Montermini, S. Stifani, M. Pandolfo, Frataxin shows developmentally regulated tissue-speci fic expression in the mouse embryo, Neurobiol. Dis. 4 (1997) 103-113. (Pubitemid 27426390)
103. O. Stehling, H.P. Elsässer, B. Brückel, U. Mühlenhoff, R. Lill, Iron-sulfur protein maturation in human cells: evidence for a function of frataxin, Hum. Mol. Genet. 13 (2004) 3007-3015. (Pubitemid 39585233)
104. A. Martelli, M. Wattenhofer-Donzé, S. Schmucker, S. Bouvet, L. Reutenauer, H. Puccio, Frataxin is essential for extramitochondrial Fe-S cluster proteins in mammalian tissues, Hum. Mol. Genet. 16 (2007) 2651-2658. (Pubitemid 350018507)
105. K. Gari, A.M. Leon Ortiz, V. Borel, H. Flynn, J.M. Skehel, S.J. Boulton, MMS19 links cytoplasmic ironesulfur cluster assembly to DNA metabolism, Science 337 (2012) 243-245.
106. O. Stehling, A.A. Vashisht, J. Mascarenhas, Z.O. Jonsson, T. Sharma, D.J. Netz, A.J. Pierik, J.A. Wohlschlegel, R. Lill, MMS19 assembles ironesulfur proteins required for DNA metabolism and genomic integrity, Science 337 (2012) 195-199.
107. R. Thierbach, G. Drewes, M. Fusser, A. Voigt, D. Kuhlow, U. Blume, T.J. Schulz, C. Reiche, H. Glatt, B. Epe, P. Steinberg, M. Ristow, The Friedreich's ataxia protein frataxin modulates DNA base excision repair in prokaryotes and mammals, Biochem. J. 432 (2010) 165-172.
108. A. Martelli, L.S. Friedman, L. Reutenauer, N. Messaddeq, S.L. Perlman, D.R. Lynch, K. Fedosov, J.B. Schulz, M. Pandolfo, H. Puccio, Clinical data and characterization of the liver conditional mouse model exclude neoplasia as a non-neurological manifestation associated with Friedreich's ataxia, Dis. Model. Mech. 5 (2012) 860-869.
109. A.C. Haugen, N.A. Di Prospero, J.S. Parker, R.D. Fannin, J. Chou, J.N. Meyer, C. Halweg, J.B. Collins, A. Durr, K. Fischbeck, B. Van Houten, Altered gene expression and DNA damage in peripheral blood cells from Friedreich's ataxia patients: cellular model of pathology, PLoS Genet. 6 (2010) e1000812.
110. G. Sanchez-Casis, M. Cote, A. Barbeau, Pathology of the heart in Friedreich's ataxia: review of the literature and report of one case, Can. J. Neurol. Sci. 3 (1976) 349-354. (Pubitemid 8067190)
111. M.B. Delatycki, J. Camakaris, H. Brooks, T. Evans-Whipp, D.R. Thorburn, R. Williamson, S.M. Forrest, Direct evidence that mitochondrial iron accumulation occurs in Friedreich ataxia, Ann. Neurol. 45 (1999) 673-675. (Pubitemid 29217600)
112. H. Seznec, D. Simon, C. Bouton, L. Reutenauer, A. Hertzog, P. Golik, V. Procaccio, M. Patel, J.C. Drapier, M. Koenig, H. Puccio, Friedreich ataxia: the oxidative stress paradox, Hum. Mol. Genet. 14 (2005) 463-474. (Pubitemid 40277462)
113. J.S. Armstrong, O. Khdour, S.M. Hecht, Does oxidative stress contribute to the pathology of Friedreich's ataxia? A radical question, FASEB J. 24 (2010) 2152-2163.
114. L.E. Larsson, H. Linderholm, R. Mueller, T. Ringqvist, R. Soernaes, Hereditary metabolic myopathy with paroxysmal myoglobinuria due to abnormal glycolysis, J. Neurol. Neurosurg. Psychiatr. 27 (1964) 361-380.
115. H. Linderholm, R. Muller, T. Ringqvist, R. Sornas, Hereditary abnormal muscle metabolism with hyperkinetic circulation during exercise, Acta Med. Scand. 185 (1969) 153-166.
116. U. Drugge, M. Holmberg, G. Holmgren, B.G. Almay, H. Linderholm, Hereditary myopathy with lactic acidosis, succinate dehydrogenase and aconitase deficiency in northern Sweden: a genealogical study, J. Med. Genet. 32 (1995) 344-347.
117. R.E. Hall, K.G. Henriksson, S.F. Lewis, R.G. Haller, N.G. Kennaway, Mitochondrial myopathy with succinate dehydrogenase and aconitase deficiency. Abnormalities of several ironesulfur proteins, J. Clin. Investig. 92 (1993) 2660-2666. (Pubitemid 24006530)
118. G. Kollberg, M. Tulinius, A. Melberg, N. Darin, O. Andersen, D. Holmgren, A. Oldfors, E. Holme, Clinical manifestation and a new ISCU mutation in ironesulphur cluster deficiency myopathy, Brain 132 (2009) 2170-2179.
119. R.G. Haller, K.G. Henriksson, L. Jorfeldt, E. Hultman, R. Wibom, K. Sahlin, N.H. Areskog, M. Gunder, K. Ayyad, C.G. Blomqvist, et al., Deficiency of skeletal muscle succinate dehydrogenase and aconitase. Pathophysiology of exercise in a novel human muscle oxidative defect, J. Clin. Investig. 88 (1991) 1197-1206.
120. P.S. Sanaker, M. Toompuu, V.E. Hogan, L. He, C. Tzoulis, Z.M. Chrzanowska-Lightowlers, R.W. Taylor, L.A. Bindoff, Differences in RNA processing underlie the tissue specific phenotype of ISCU myopathy, Biochim. Biophys. Acta 1802 (2010) 539-544.
121. D.R. Crooks, S.Y. Jeong, W.H. Tong, M.C. Ghosh, H. Olivierre, R.G. Haller, 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.
122. A. Nordin, E. Larsson, M. Holmberg, The defective splicing caused by the ISCU intron mutation in patients with myopathy with lactic acidosis is repressed by PTBP1 but can be derepressed by IGF2BP1, Hum. Mutat. 33 (2012) 467-470.
123. G. Kollberg, A. Melberg, E. Holme, A. Oldfors, Transient restoration of succinate dehydrogenase activity after rhabdomyolysis in ironesulphur cluster deficiency myopathy, Neuromuscul. Disord. 21 (2011) 115-120.
124. W.H. Tong, T.A. Rouault, Functions of mitochondrial ISCU and cytosolic ISCU in mammalian ironesulfur cluster biogenesis and iron homeostasis, Cell. Metab. 3 (2006) 199-210.
125. D.R. Crooks, M.C. Ghosh, R.G. Haller, W.H. Tong, T.A. Rouault, Post-translational stability of the heme biosynthetic enzyme ferrochelatase is dependent on iron availability and intact ironesulfur cluster assembly machinery, Blood 115 (2010) 860-869.
126. H. Linderholm, B. Essen-Gustavsson, L.E. Thornell, Low succinate dehydrogenase (SDH) activity in a patient with a hereditary myopathy with paroxysmal myoglobinuria, J. Intern. Med. 228 (1990) 43-52. (Pubitemid 20221939)
127. D.R. Crooks, T.G. Natarajan, S.Y. Jeong, C. Chen, S.Y. Park, H. Huang, M.C. Ghosh, W.H. Tong, R.G. Haller, C. Wu, T.A. Rouault, Elevated FGF21 secretion, PGC-1alpha and ketogenic enzyme expression are hallmarks of ironesulfur cluster depletion in human skeletal muscle, Hum. Mol. Genet. 23 (2013) 24-39.
128. R. Spiegel, A. Saada, J. Halvardson, D. Soiferman, A. Shaag, S. Edvardson, Y. Horovitz, M. Khayat, S.A. Shalev, L. Feuk, O. Elpeleg, Deleterious mutation in FDX1L gene is associated with a novel mitochondrial muscle myopathy, Eur. J. Hum. Genet., in press.
129. D.R. Thorburn, Practical problems in detecting abnormal mitochondrial function and genomes, Hum. Reprod. 15 (Suppl. 2) (2000) 57-67.
130. S.C. Lim, M. Friemel, J.E. Marum, E.J. Tucker, D.L. Bruno, L.G. Riley, J. Christodoulou, E.P. Kirk, A. Boneh, C. Degennaro, M. Springer, V.K. Mootha, T.A. Rouault, S. Leimkuhler, D.R. Thorburn, A.G. Compton, Mutations in LYRM4, encoding ironesulfur cluster biogenesis factor ISD11, cause deficiency of multiple respiratory chain complexes, Hum. Mol. Genet. 22 (2013) 4460-4473.
131. A. Rosenbohm, S.D. Sussmuth, J. Kassubek, H.P. Muller, C. Pontes, A. Abicht, S. Bulst, A.C. Ludolph, E. Pinkhardt, Novel ETFDH mutation and imaging findings in an adult with glutaric aciduria type II, Muscle Nerve, in press.
132. J. Vonck, E. Schafer, Supramolecular organization of protein complexes in the mitochondrial inner membrane, Biochim. Biophys. Acta 1793 (2009) 117-124.
133. A. Jablensky, D. Angelicheva, G.J. Donohoe, M. Cruickshank, D.N. Azmanov, D.W. Morris, A. McRae, C.S. Weickert, K.W. Carter, D. Chandler, B. Alexandrov, A. Usheva, B. Morar, P.L. Verbrugghe, A. Filipovska, O. Rackham, A.R. Bishop, K.O. Rasmussen, M. Dragovic, M. Cooper, M. Phillips, J. Badcock, E. Bramon-Bosch, O.P. Almeida, L. Flicker, M. Gill, A. Corvin, S. MacGregor, L. Kalaydjieva, Promoter polymorphisms in two overlapping 6p25 genes implicate mitochondrial proteins in cognitive deficit in schizophrenia, Mol. Psychiatry 17 (2012) 1328-1339.
134. R.E. Anglin, S.L. Garside, M.A. Tarnopolsky, M.F. Mazurek, P.I. Rosebush, The psychiatric manifestations of mitochondrial disorders: a case and review of the literature, J. Clin. Psychiatry 73 (2012) 506-512.
135. H.B. Clay, S. Sillivan, C. Konradi, Mitochondrial dysfunction and pathology in bipolar disorder and schizophrenia, Int. J. Dev. Neurosci. 29 (2011) 311-324.
136. T. Alcindor, K.R. Bridges, Sideroblastic anaemias, Br. J. Haematol. 116 (2002) 733-743. (Pubitemid 34226991)
137. A.D. Sheftel, D.R. Richardson, J. Prchal, P. Ponka, Mitochondrial iron metabolism and sideroblastic anemia, Acta Haematol. 122 (2009) 120-133.
138. P.R. Baker, 2nd, M.W. Friederich, M.A. Swanson, T. Shaikh, K. Bhattacharya, G.H. Scharer, J. Aicher, G. Creadon-Swindell, E. Geiger, K.N. Maclean, W.T. Lee, C. Deshpande, M.L. Freckmann, L.Y. Shih, M. Wasserstein, M.B. Rasmussen, A.M. Lund, P. Procopis, J.M. Cameron, B.H. Robinson, G.K. Brown, R.M. Brown, A.G. Compton, C.L. Dieckmann, R. Collard, C.R. Coughlin, 2nd, E. Spector, M.F. Wempe, J.L. Van Hove, Variant nonketotic hyperglycinemia is caused by mutations in LIAS, BOLA3 and the novel gene GLRX5, Brain, in press.
139. J. Boultwood, A. Pellagatti, M. Nikpour, B. Pushkaran, C. Fidler, H. Cattan, T.J. Littlewood, L. Malcovati, M.G. Della Porta, M. Jadersten, S. Killick, A. Giagounidis, D. Bowen, E. Hellstrom-Lindberg, M. Cazzola, J.S. Wainscoat, The role of the iron transporter ABCB7 in refractory anemia with ring sideroblasts, PLoS One 3 (2008) e1970.
140. K. Paulsson, C. Haferlach, C. Fonatsch, A. Hagemeijer, M.K. Andersen, M.L. Slovak, B. Johansson, The idic(X)(q13) in myeloid malignancies: breakpoint clustering in segmental duplications and association with TET2 mutations, Hum. Mol. Genet. 19 (2010) 1507-1514.
141. H. Ye, S.Y. Jeong, M.C. Ghosh, G. Kovtunovych, L. Silvestri, D. Ortillo, N. Uchida, J. Tisdale, C. Camaschella, T.A. Rouault, Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human erythroblasts, J. Clin. Investig. 120 (2010) 1749-1761.
142. 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, B.H. Paw, G.C. Shaw, P. Kingsley, J. Palis, H. Schubert, O. Chen, J. Kaplan, L.I. Zon, Deficiency of glutaredoxin 5 reveals FeeS clusters are required for vertebrate haem synthesis, Nature 436 (2005) 1035-1039. (Pubitemid 41191688)
143. M.A. Chiong, P. Procopis, K. Carpenter, B. Wilcken, Late-onset nonketotic hyperglycinemia with leukodystrophy and an unusual clinical course, Pediatr. Neurol. 37 (2007) 283-286. (Pubitemid 47446151)
144. S.H. Wei, W.C. Weng, N.C. Lee, W.L. Hwu, W.T. Lee, Unusual spinal cord lesions in late-onset non-ketotic hyperglycinemia, J. Child. Neurol. 26 (2011) 900-903.
145. D.A. Applegarth, J.R. Toone, Glycine encephalopathy (nonketotic hyperglycinemia): comments and speculations, Am. J. Med. Genet. A 140 (2006) 186-188. (Pubitemid 43054026)
146. M. D'Hooghe, D. Selleslag, G. Mortier, R. Van Coster, P. Vermeersch, J. Billiet, S. Bekri, X-linked sideroblastic anemia and ataxia: a new family with identification of a fourth ABCB7 gene mutation, Eur. J. Paediatr. Neurol. 16 (2012) 730-735.
147. A. Maguire, K. Hellier, S. Hammans, A. May, X-linked cerebellar ataxia and sideroblastic anaemia associated with a missense mutation in the ABC7 gene predicting V411L, Br. J. Haematol. 115 (2001) 910-917. (Pubitemid 34042908)
148. S. Savary, R. Allikmets, F. Denizot, M.F. Luciani, M.G. Mattei, M. Dean, G. Chimini, Isolation and chromosomal mapping of a novel ATP-binding cassette transporter conserved in mouse and human, Genomics 41 (1997) 275-278. (Pubitemid 27175359)
149. Y. Shimada, S. Okuno, A. Kawai, H. Shinomiya, A. Saito, M. Suzuki, Y. Omori, N. Nishino, N. Kanemoto, T. Fujiwara, M. Horie, E. Takahashi, Cloning and chromosomal mapping of a novel ABC transporter gene (hABC7), a candidate for X-linked sideroblastic anemia with spinocerebellar ataxia, J. Hum. Genet. 43 (1998) 115-122. (Pubitemid 128508966)
150. R.A. Pagon, T.D. Bird, X-linked sideroblastic anemia and ataxia, in: R.A. Pagon, M.P. Adam, T.D. Bird, C.R. Dolan, C.T. Fong, K. Stephens (Eds.), GeneReviews, 1993. Seattle (WA).
151. R.A. Pagon, T.D. Bird, J.C. Detter, I. Pierce, Hereditary sideroblastic anaemia and ataxia: an X linked recessive disorder, J. Med. Genet. 22 (1985) 267-273. (Pubitemid 15240345)
152. X. Liu, X. Yu, D.J. Zack, H. Zhu, J. Qian, TiGER: a database for tissue-specific gene expression and regulation, BMC Bioinformatics (2008) 271.
153. C. Pondarre, D.R. Campagna, B. Antiochos, L. Sikorski, H. Mulhern, M.D. Fleming, Abcb7, the gene responsible for X-linked sideroblastic anemia with ataxia, is essential for hematopoiesis, Blood 109 (2007) 3567-3569. (Pubitemid 46572551)
154. S.L. Clarke, A. Vasanthakumar, S.A. Anderson, C. Pondarre, C.M. Koh, K.M. Deck, J.S. Pitula, C.J. Epstein, M.D. Fleming, R.S. Eisenstein, Iron-responsive degradation of iron-regulatory protein 1 does not require the Fe-S cluster, EMBO J. 25 (2006) 544-553. (Pubitemid 43237661)
155. M. Nikpour, A. Pellagatti, A. Liu, M. Karimi, L. Malcovati, V. Gogvadze, A.M. Forsblom, J.S. Wainscoat, M. Cazzola, B. Zhivotovsky, A. Grandien, J. Boultwood, E. Hellstrom-Lindberg, Gene expression profiling of erythroblasts from refractory anaemia with ring sideroblasts (RARS) and effects of G-CSF, Br. J. Haematol. 149 (2010) 844-854.
156. M. Nikpour, C. Scharenberg, A. Liu, S. Conte, M. Karimi, T. Mortera-Blanco, V. Giai, M. Fernandez-Mercado, E. Papaemmanuil, K. Hogstrand, M. Jansson, I. Vedin, J. Stephen Wainscoat, P. Campbell, M. Cazzola, J. Boultwood, A. Grandien, E. Hellstrom-Lindberg, The transporter ABCB7 is a mediator of the phenotype of acquired refractory anemia with ring sideroblasts, Leukemia 27 (2013) 889-896.
157. V. Visconte, H.J. Rogers, J. Singh, J. Barnard, M. Bupathi, F. Traina, J. McMahon, H. Makishima, H. Szpurka, A. Jankowska, A. Jerez, M.A. Sekeres, Y. Saunthararajah, A.S. Advani, E. Copelan, H. Koseki, K. Isono, R.A. Padgett, S. Osman, K. Koide, C. O'Keefe, J.P. Maciejewski, R.V. Tiu, SF3B1 haploinsufficiency leads to formation of ring sideroblasts in myelodysplastic syndromes, Blood 120 (2012) 3173-3186.
158. J. Dierlamm, L. Michaux, A. Criel, I. Wlodarska, W. Zeller, A. Louwagie, J.L. Michaux, C. Mecucci, H. Van den Berghe, Isodicentric (X)(q13) in haematological malignancies: presentation of five new cases, application of fluorescence in situ hybridization (FISH) and review of the literature, Br. J. Haematol. 91 (1995) 885-891.
159. P.D. Cotter, H.F. Willard, J.L. Gorski, D.F. Bishop, Assignment of human erythroid delta-aminolevulinate synthase (ALAS2) to a distal subregion of band Xp11.21 by PCR analysis of somatic cell hybrids containing X; autosome translocations, Genomics 13 (1992) 211-212.
160. G.W. Dewald, M. Brecher, L.B. Travis, P.J. Stupca, Twenty-six patients with hematologic disorders and X chromosome abnormalities. Frequent idic(X)(q13) chromosomes and Xq13 anomalies associated with pathologic ringed sideroblasts, Cancer Genet. Cytogenet. 42 (1989) 173-185. (Pubitemid 19262594)
161. K. Sato, Y. Torimoto, T. Hosoki, K. Ikuta, H. Takahashi, M. Yamamoto, S. Ito, N. Okamura, K. Ichiki, H. Tanaka, M. Shindo, K. Hirai, Y. Mizukami, T. Otake, M. Fujiya, K. Sasaki, Y. Kohgo, Loss of ABCB7 gene: pathogenesis of mitochondrial iron accumulation in erythroblasts in refractory anemia with ringed sideroblast with isodicentric (X)(q13), Int. J. Hematol. 93 (2011) 311-318.
162. N. Ajit Bolar, A.V. Vanlander, C. Wilbrecht, N. Van der Aa, J. Smet, B. De Paepe, G. Vandeweyer, F. Kooy, F. Eyskens, E. De Latter, G. Delanghe, P. Govaert, J.G. Leroy, B. Loeys, R. Lill, L. Van Laer, R. Van Coster, Mutation of the irone sulfur cluster assembly gene IBA57 causes severe myopathy and encephalopathy, Hum. Mol. Genet. 22 (2013) 2590-2602.
163. J.A. Mayr, F.A. Zimmermann, C. Fauth, C. Bergheim, D. Meierhofer, D. Radmayr, J. Zschocke, J. Koch, W. Sperl, Lipoic acid synthetase deficiency causes neonatal-onset epilepsy, defective mitochondrial energy metabolism, and glycine elevation, Am. J. Hum. Genet. 89 (2011) 792-797.
164. R. Nilsson, I.J. Schultz, E.L. Pierce, K.A. Soltis, A. Naranuntarat, D.M. Ward, J.M. Baughman, P.N. Paradkar, P.D. Kingsley, V.C. Culotta, J. Kaplan, J. Palis, B.H. Paw, V.K. Mootha, Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis, Cell. Metab. 10 (2009) 119-130.
165. A. Seyda, R.F. Newbold, T.J. Hudson, A. Verner, N. MacKay, S. Winter, A. Feigenbaum, S. Malaney, D. Gonzalez-Halphen, A.P. Cuthbert, 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. (Pubitemid 32147808)
166. X. Ferrer-Cortes, A. Font, N. Bujan, A. Navarro-Sastre, L. Matalonga, J.A. Arranz, E. Riudor, M. Del Toro, A. Garcia-Cazorla, J. Campistol, P. Briones, A. Ribes, F. Tort, Protein expression profiles in patients carrying NFU1 mutations. Contribution to the pathophysiology of the disease, J. Inherit. Metab. Dis. 36 (2013) 841-847.
167. T.B. Haack, B. Rolinski, B. Haberberger, F. Zimmermann, J. Schum, V. Strecker, E. Graf, U. Athing, T. Hoppen, I. Wittig, W. Sperl, P. Freisinger, J.A. Mayr, T.M. Strom, T. Meitinger, H. Prokisch, Homozygous missense mutation in BOLA3 causes multiple mitochondrial dysfunctions syndrome in two siblings, J. Inherit. Metab. Dis. 36 (2013) 55-62.
168. A.H. Schapira, Mitochondrial diseases, Lancet 379 (2012) 1825-1834.
169. S.H. Kevelam, R.J. Rodenburg, N.I. Wolf, P. Ferreira, R.J. Lunsing, L.G. Nijtmans, A. Mitchell, H.A. Arroyo, D. Rating, A. Vanderver, C.G. van Berkel, T.E. Abbink, P. Heutink, M.S. van der Knaap, NUBPL mutations in patients with complex I deficiency and a distinct MRI pattern, Neurology 80 (2013) 1577-1583.
170. E.V. Tenisch, A.S. Lebre, D. Grevent, P. de Lonlay, M. Rio, M. Zilbovicius, B. Funalot, I. Desguerre, F. Brunelle, A. Rotig, A. Munnich, N. Boddaert, Massive and exclusive pontocerebellar damage in mitochondrial disease and NUBPL mutations, Neurology 79 (2012) 391.
171. E.J. Tucker, M. Mimaki, A.G. Compton, M. McKenzie, M.T. Ryan, D.R. Thorburn, Next-generation sequencing in molecular diagnosis: NUBPL mutations highlight the challenges of variant detection and interpretation, Hum. Mutat. 33 (2012) 411-418.
172. N.I. Wolf, A. Seitz, I. Harting, J.A. Smeitink, F. Trijbels, L.P. van den Heuvel, H. Schlemmer, F. Ebinger, W. Evert, D. Rating, New pattern of brain MRI lesions in isolated complex I deficiency, Neuropediatrics 34 (2003) 156-159. (Pubitemid 36994407)
173. M.M. Wydro, J. Balk, Insights into the pathogenic character of a common NUBPL branch-site mutation associated with mitochondrial disease and complex I deficiency using a yeast model, Dis. Models Mech. 6 (2013) 1279-1284.
174. R.O. Vogel, C.E. Dieteren, L.P. van den Heuvel, P.H. Willems, J.A. Smeitink, W.J. Koopman, L.G. Nijtmans, Identification of mitochondrial complex I assembly intermediates by tracing tagged NDUFS3 demonstrates the entry point of mitochondrial subunits, J. Biol. Chem. 282 (2007) 7582-7590. (Pubitemid 47093656)
175. M. Lecha, H. Puy, J.C. Deybach, Erythropoietic protoporphyria, Orphanet J. Rare Dis. 4 (2009) 19.
176. Y. Wang, N.B. Langer, G.C. Shaw, G. Yang, L. Li, J. Kaplan, B.H. Paw, J.R. Bloomer, Abnormal mitoferrin-1 expression in patients with erythropoietic protoporphyria, Exp. Hematol. 39 (2011) 784-794.
177. R. Lill, Z. Fekete, K. Sipos, C. Rotte, Is there an answer? Why are mitochondria essential for life? IUBMB Life 57 (2005) 701-703. (Pubitemid 41564308)