Mammalian mitochondrial iron–sulfur cluster biogenesis and transfer and related human diseases

Adam AC, Bornhovd C, Prokisch H, Neupert W, Hell K (2006) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J 25(1): 174−183

Ajit Bolar N, Vanlander AV, Wilbrecht C, Van der Aa N, Smet J, De Paepe B, Vandeweyer G, Kooy F, Eyskens F, De Latter E, Delanghe G, Govaert P, Leroy JG, Loeys B, Lill R, Van Laer L, Van Coster R (2013) Mutation of the iron–sulfur cluster assembly gene IBA57 causes severe myopathy and encephalopathy. Hum Mol Genet 22(13): 2590−2602

Al-Hassnan ZN, Al-Dosary M, Alfadhel M, Faqeih EA, Alsagob M, Kenana R, Almass R, Al-Harazi OS, Al-Hindi H, Malibari OI, Almutari FB, Tulbah S, Alhadeq F, Al-Sheddi T, Alamro R, AlAsmari A, Almuntashri M, Alshaalan H, Al-Mohanna FA, Colak D, Kaya N (2015) ISCA2 mutation causes infantile neurodegenerative mitochondrial disorder. J Med Genet 52(3): 186−194

Allikmets R, Raskind WH, Hutchinson A, Schueck ND, Dean M, Koeller DM (1999) Mutation of a putative mitochondrial iron transporter gene (ABC7) in X-linked sideroblastic anemia and ataxia (XLSA/A). Hum Mol Genet 8(5): 743−749

Andrew AJ, Dutkiewicz R, Knieszner H, Craig EA, Marszalek J (2006) Characterization of the interaction between the J-protein Jac1p and the scaffold for Fe–S cluster biogenesis, Isu1p. J Biol Chem 281(21): 14580−14587

Banci L, Brancaccio D, Ciofi-Baffoni S, Del Conte R, Gadepalli R, Mikolajczyk M, Neri S, Piccioli M, Winkelmann J (2014) [2Fe–2S] cluster transfer in iron–sulfur protein biogenesis. Proc Natl Acad Sci USA 111(17): 6203−6208

Beilschmidt LK, Ollagnier de Choudens S, Fournier M, Sanakis I, Hograindleur MA, Clemancey M, Blondin G, Schmucker S, Eisenmann A, Weiss A, Koebel P, Messaddeq N, Puccio H, Martelli A (2017) ISCA1 is essential for mitochondrial Fe4S4 biogenesis in vivo. Nat Commun 8: 15124. https://doi.org/10.1038/ncomms15124

Bekri S, Kispal G, Lange H, Fitzsimons E, Tolmie J, Lill R, Bishop DF (2000) Human ABC7 transporter: gene structure and mutation causing X-linked sideroblastic anemia with ataxia with disruption of cytosolic iron–sulfur protein maturation. Blood 96(9): 3256−3264

Braymer JJ, Lill R (2017) Iron–sulfur cluster biogenesis and trafficking in mitochondria. J Biol Chem 292(31): 12754−12763

Bridwell-Rabb J, Fox NG, Tsai CL, Winn AM, Barondeau DP (2014) Human frataxin activates Fe–S cluster biosynthesis by facilitating sulfur transfer chemistry. Biochemistry 53(30): 4904−4913

Cai K, Frederick RO, Dashti H, Markley JL (2018a) Architectural features of human mitochondrial cysteine desulfurase complexes from crosslinking mass spectrometry and small-angle X-ray scattering. Structure 26(8): 1127−1136

Cai K, Frederick RO, Markley JL (2020) ISCU interacts with NFU1, and ISCU[4Fe–4S] transfers its Fe–S cluster to NFU1 leading to the production of holo-NFU1. J Struct Biol 210(2): 107491. https://doi.org/10.1016/j.jsb.2020.107491

Cai K, Frederick RO, Tonelli M, Markley JL (2018b) ISCU(M108I) and ISCU(D39V) Differ from wild-type ISCU in their failure to form cysteine desulfurase complexes containing both frataxin and ferredoxin. Biochemistry 57(9): 1491−1500

Calvo SE, Tucker EJ, Compton AG, Kirby DM, Crawford G, Burtt NP, Rivas M, Guiducci C, Bruno DL, Goldberger OA, Redman MC, Wiltshire E, Wilson CJ, Altshuler D, Gabriel SB, Daly MJ, Thorburn DR, Mootha VK (2010) High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency. Nat Genet 42(10): 851−858

Camaschella C, Campanella A, De Falco L, Boschetto L, Merlini R, Silvestri L, Levi S, Iolascon A (2007) The human counterpart of zebrafish shiraz shows sideroblastic-like microcytic anemia and iron overload. Blood 110(4): 1353−1358

Cameron JM, Janer A, Levandovskiy V, Mackay N, Rouault TA, Tong WH, Ogilvie I, Shoubridge EA, Robinson BH (2011) 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(4): 486−495

Campuzano V, Montermini L, Molto MD, Pianese L, Cossee M, Cavalcanti F, Monros E, Rodius F, Duclos F, Monticelli A, Zara F, Canizares J, Koutnikova H, Bidichandani SI, Gellera C, Brice A, Trouillas P, De Michele G, Filla A, De Frutos R, Palau F, Patel PI, Di Donato S, Mandel JL, Cocozza S, Koenig M, Pandolfo M (1996) Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271(5254): 1423−1427

Chan SY, Zhang YY, Hemann C, Mahoney CE, Zweier JL, Loscalzo J (2009) MicroRNA-210 controls mitochondrial metabolism during hypoxia by repressing the iron–sulfur cluster assembly proteins ISCU1/2. Cell Metab 10(4): 273−284

Crispin A, Schmidt P, Campagna D, Cao C, Lichtenstein D, Sendamarai A, Guo CS, Chen CY, Hildick-Smith GJ, Huston NC, Boudreaux J, Bottomley SS, Heeney MM, Paw BH, Fleming MD, Ducamp S (2017) Hscb, a mitochondrial iron-sulfur cluster assembly co-chaperone, is a novel candidate gene for congenital sideroblastic anemia. Blood 130(Suppl_1): 79. https://doi.org/10.1182/blood.V130.Suppl_1.79.79

Colin F, Martelli A, Clémancey M, Latour JM, Gambarelli S, Zeppieri L, Birck C, Page A, Puccio H, Ollagnier de Choudens S (2013) Mammalian frataxin controls sulfur production and iron entry during de novo Fe4S4 cluster assembly. J Am Chem Soc 135(2): 733−740

Cory SA, Van Vranken JG, Brignole EJ, Patra S, Winge DR, Drennan CL, Rutter J, Barondeau DP (2017) Structure of human Fe–S assembly subcomplex reveals unexpected cysteine desulfurase architecture and acyl-ACP-ISD11 interactions. Proc Natl Acad Sci USA 114(27): E5325−E5334

Cossee M, Puccio H, Gansmuller A, Koutnikova H, Dierich A, LeMeur M, Fischbeck K, Dolle P, Koenig M (2000) Inactivation of the Friedreich ataxia mouse gene leads to early embryonic lethality without iron accumulation. Hum Mol Genet 9(8): 1219−1226

Cozar-Castellano I, del Valle Machargo M, Trujillo E, Arteaga MF, Gonzalez T, Martin-Vasallo P, Avila J (2004) hIscA: a protein implicated in the biogenesis of iron–sulfur clusters. Biochim Biophys Acta 1700(2): 179−188

Crack JC, Le Brun NE (2018) Redox-sensing iron–sulfur cluster regulators. Antioxid Redox Signal 29(18): 1809−1829

Ding H, Clark RJ, Ding B (2004) IscA mediates iron delivery for assembly of iron–sulfur clusters in IscU under the limited accessible free iron conditions. J Biol Chem 279(36): 37499−37504

Farhan SM, Wang J, Robinson JF, Lahiry P, Siu VM, Prasad C, Kronick JB, Ramsay DA, Rupar CA, Hegele RA (2014) Exome sequencing identifies NFS1 deficiency in a novel Fe–S cluster disease, infantile mitochondrial complex II/III deficiency. Mol Genet Genomic Med 2(1): 73−80

Feng D, Witkowski A, Smith S (2009) Down-regulation of mitochondrial acyl carrier protein in mammalian cells compromises protein lipoylation and respiratory complex I and results in cell death. J Biol Chem 284(17): 11436−11445

Fox NG, Yu X, Feng X, Bailey HJ, Martelli A, Nabhan JF, Strain-Damerell C, Bulawa C, Yue WW, Han S (2019) Structure of the human frataxin-bound iron–sulfur cluster assembly complex provides insight into its activation mechanism. Nat Commun 10(1): 2210. https://doi.org/10.1038/s41467-019-09989-y

Fuss JO, Tsai CL, Ishida JP, Tainer JA (2015) Emerging critical roles of Fe–S clusters in DNA replication and repair. Biochim Biophys Acta 1853(6): 1253−1271

Gellera C, Castellotti B, Mariotti C, Mineri R, Seveso V, Didonato S, Taroni F (2007) Frataxin gene point mutations in Italian Friedreich ataxia patients. Neurogenetics 8(4): 289−299

Gurgel-Giannetti J, Lynch DS, Paiva ARB, Lucato LT, Yamamoto G, Thomsen C, Basu S, Freua F, Giannetti AV, de Assis BDR, Ribeiro MDO, Barcelos I, Sayao Souza K, Monti F, Melo US, Amorim S, Silva LGL, Macedo-Souza LI, Vianna-Morgante AM, Hirano M, Van der Knaap MS, Lill R, Vainzof M, Oldfors A, Houlden H, Kok F (2018) A novel complex neurological phenotype due to a homozygous mutation in FDX2. Brain 141(8): 2289−2298

Haack TB, Rolinski B, Haberberger B, Zimmermann F, Schum J, Strecker V, Graf E, Athing U, Hoppen T, Wittig I, Sperl W, Freisinger P, Mayr JA, Strom TM, Meitinger T, Prokisch H (2013) Homozygous missense mutation in BOLA3 causes multiple mitochondrial dysfunctions syndrome in two siblings. J Inherit Metab Dis 36(1): 55−62

Jeong SY, Crooks DR, Wilson-Ollivierre H, Ghosh MC, Sougrat R, Lee J, Cooperman S, Mitchell JB, Beaumont C, Rouault TA (2011) Iron insufficiency compromises motor neurons and their mitochondrial function in Irp2-null mice. PLoS One 6(10): e25404. https://doi.org/10.1371/journal.pone.0025404

Kaul SC, Wadhwa R, Matsuda Y, Hensler PJ, Pereira-Smith OM, Komatsu Y, Mitsui Y (1995) Mouse and human chromosomal assignments of mortalin, a novel member of the murine hsp70 family of proteins. FEBS Lett 361(2-3): 269−272

Kevelam SH, Rodenburg RJ, Wolf NI, Ferreira P, Lunsing RJ, Nijtmans LG, Mitchell A, Arroyo HA, Rating D, Vanderver A, van Berkel CG, Abbink TE, Heutink P, van der Knaap MS (2013) NUBPL mutations in patients with complex I deficiency and a distinct MRI pattern. Neurology 80(17): 1577−1583

Koeppen AH (2011) Friedreich's ataxia: pathology, pathogenesis, and molecular genetics. J Neurol Sci 303(1-2): 1−12

Kollberg G, Tulinius M, Melberg A, Darin N, Andersen O, Holmgren D, Oldfors A, Holme E (2009) Clinical manifestation and a new ISCU mutation in iron–sulphur cluster deficiency myopathy. Brain 132(Pt 8): 2170−2179

Land T, Rouault TA (1998) Targeting of a human iron–sulfur cluster assembly enzyme, nifs, to different subcellular compartments is regulated through alternative AUG utilization. Mol Cell 2(6): 807−815

Li H, Liu Y, Shang L, Cai J, Wu J, Zhang W, Pu X, Dong W, Qiao T, Li K (2019) Iron regulatory protein 2 modulates the switch from aerobic glycolysis to oxidative phosphorylation in mouse embryonic fibroblasts. Proc Natl Acad Sci USA 116(20): 9871−9876

Li H, Zhao H, Hao S, Shang L, Wu J, Song C, Meyron-Holtz EG, Qiao T, Li K (2018) Iron regulatory protein deficiency compromises mitochondrial function in murine embryonic fibroblasts. Sci Rep 8(1): 5118. https://doi.org/10.1038/s41598-018-23175-y

Li J, Cowan JA (2015) Glutathione-coordinated [2Fe–2S] cluster: a viable physiological substrate for mitochondrial ABCB7 transport. Chem Commun (Camb) 51(12): 2253−2255

Li K (2019) Iron pathophysiology in Friedreich's ataxia. Adv Exp Med Biol 1173: 125−143

Li K, Besse EK, Ha D, Kovtunovych G, Rouault TA (2008) Iron-dependent regulation of frataxin expression: implications for treatment of Friedreich ataxia. Hum Mol Genet 17(15): 2265−2273

Li K, Tong WH, Hughes RM, Rouault TA (2006) Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron–sulfur cluster assembly. J Biol Chem 281(18): 12344−12351

Lill R, Fekete Z, Sipos K, Rotte C (2005) Is there an answer? Why are mitochondria essential for life? IUBMB Life 57(10): 701−703

Lim SC, Friemel M, Marum JE, Tucker EJ, Bruno DL, Riley LG, Christodoulou J, Kirk EP, Boneh A, DeGennaro CM, Springer M, Mootha VK, Rouault TA, Leimkuhler S, Thorburn DR, Compton AG (2013) Mutations in LYRM4, encoding iron–sulfur cluster biogenesis factor ISD11, cause deficiency of multiple respiratory chain complexes. Hum Mol Genet 22(22): 4460−4473

Lin CW, McCabe JW, Russell DH, Barondeau DP (2020) Molecular mechanism of ISC iron–sulfur cluster biogenesis revealed by high-resolution native mass spectrometry. J Am Chem Soc 142(13): 6018−6029

Lin D, Shi YF, Miller WL (1990) Cloning and sequence of the human adrenodoxin reductase gene. Proc Natl Acad Sci USA 87(21): 8516−8520

Liu G, Guo S, Anderson GJ, Camaschella C, Han B, Nie G (2014) Heterozygous missense mutations in the GLRX5 gene cause sideroblastic anemia in a Chinese patient. Blood 124(17): 2750−2751

Lorain S, Lecluse Y, Scamps C, Mattei MG, Lipinski M (2001) Identification of human and mouse HIRA-interacting protein-5(HIRIP5), two mammalian representatives in a family of phylogenetically conserved proteins with a role in the biogenesis of Fe/S proteins. Biochim Biophys Acta 1517(3): 376−383

Lossos A, Stumpfig C, Stevanin G, Gaussen M, Zimmerman BE, Mundwiller E, Asulin M, Chamma L, Sheffer R, Misk A, Dotan S, Gomori JM, Ponger P, Brice A, Lerer I, Meiner V, Lill R (2015) Fe/S protein assembly gene IBA57 mutation causes hereditary spastic paraplegia. Neurology 84(7): 659−667

Maio N, Jain A, Rouault TA (2020) Mammalian iron–sulfur cluster biogenesis: Recent insights into the roles of frataxin, acyl carrier protein and ATPase-mediated transfer to recipient proteins. Curr Opin Chem Biol 55: 34−44

Maio N, Singh A, Uhrigshardt H, Saxena N, Tong WH, Rouault TA (2014) Cochaperone binding to LYR motifs confers specificity of iron sulfur cluster delivery. Cell Metab 19(3): 445−457

Mayank AK, Pandey V, Vashisht AA, Barshop WD, Rayatpisheh S, Sharma T, Haque T, Powers DN, Wohlschlegel JA (2019) An oxygen-dependent interaction between FBXL5 and the CIA-targeting complex regulates iron homeostasis. Mol Cell 75(2): 382−393

Meyron-Holtz EG, Ghosh MC, Iwai K, LaVaute T, Brazzolotto X, Berger UV, Land W, Ollivierre-Wilson H, Grinberg A, Love P, Rouault TA (2004) Genetic ablations of iron regulatory proteins 1 and 2 reveal why iron regulatory protein 2 dominates iron homeostasis. EMBO J 23(2): 386−395

Mochel F, Knight MA, Tong WH, Hernandez D, Ayyad K, Taivassalo T, Andersen PM, Singleton A, Rouault TA, Fischbeck KH, Haller RG (2008) Splice mutation in the iron–sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance. Am J Hum Genet 82(3): 652−660

Navarro-Sastre A, Tort F, Stehling O, Uzarska MA, Arranz JA, Del Toro M, Labayru MT, Landa J, Font A, Garcia-Villoria J, Merinero B, Ugarte M, Gutierrez-Solana LG, Campistol J, Garcia-Cazorla A, Vaquerizo J, Riudor E, Briones P, Elpeleg O, Ribes A, Lill R (2011) 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(5): 656−667

Nilsson R, Schultz IJ, Pierce EL, Soltis KA, Naranuntarat A, Ward DM, Baughman JM, Paradkar PN, Kingsley PD, Culotta VC, Kaplan J, Palis J, Paw BH, Mootha VK (2009) Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis. Cell Metab 10(2): 119−130

Okamura T, John ME, Zuber MX, Simpson ER, Waterman MR (1985) Molecular cloning and amino acid sequence of the precursor form of bovine adrenodoxin: evidence for a previously unidentified COOH-terminal peptide. Proc Natl Acad Sci USA 82(17): 5705−5709

Patra S, Barondeau DP (2019) Mechanism of activation of the human cysteine desulfurase complex by frataxin. Proc Natl Acad Sci USA 116(39): 19421−19430

Paul A, Drecourt A, Petit F, Deguine DD, Vasnier C, Oufadem M, Masson C, Bonnet C, Masmoudi S, Mosnier I, Mahieu L, Bouccara D, Kaplan J, Challe G, Domange C, Mochel F, Sterkers O, Gerber S, Nitschke P, Bole-Feysot C, Jonard L, Gherbi S, Mercati O, Ben Aissa I, Lyonnet S, Rotig A, Delahodde A, Marlin S (2017) FDXR Mutations Cause Sensorial Neuropathies and Expand the Spectrum of Mitochondrial Fe–S-Synthesis Diseases. Am J Hum Genet 101(4): 630−637

Rouault TA, Maio N (2020) How oxidation of a unique iron–sulfur cluster in FBXL5 regulates IRP2 levels and promotes regulation of iron metabolism proteins. Mol Cell 78(1): 1−3

Rouault TA, Tong WH (2008) Iron–sulfur cluster biogenesis and human disease. Trends Genet 24(8): 398−407

Royer-Bertrand B, Castillo-Taucher S, Moreno-Salinas R, Cho TJ, Chae JH, Choi M, Kim OH, Dikoglu E, Campos-Xavier B, Girardi E, Superti-Furga G, Bonafe L, Rivolta C, Unger S, Superti-Furga A (2015) Mutations in the heat-shock protein A9(HSPA9) gene cause the EVEN-PLUS syndrome of congenital malformations and skeletal dysplasia. Sci Rep 5: 17154. https://doi.org/10.1038/srep17154

Ruiz JC, Bruick RK (2014) F-box and leucine-rich repeat protein 5(FBXL5): sensing intracellular iron and oxygen. J Inorg Biochem 133: 73−77

Salahudeen AA, Thompson JW, Ruiz JC, Ma HW, Kinch LN, Li Q, Grishin NV, Bruick RK (2009) An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326(5953): 722−726

Savary S, Allikmets R, Denizot F, Luciani MF, Mattei MG, Dean M, Chimini G (1997) Isolation and chromosomal mapping of a novel ATP-binding cassette transporter conserved in mouse and human. Genomics 41(2): 275−278

Saveliev A, Everett C, Sharpe T, Webster Z, Festenstein R (2003) DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 422(6934): 909−913

Schmitz-Abe K, Ciesielski SJ, Schmidt PJ, Campagna DR, Rahimov F, Schilke BA, Cuijpers M, Rieneck K, Lausen B, Linenberger ML, Sendamarai AK, Guo C, Hofmann I, Newburger PE, Matthews D, Shimamura A, Snijders PJ, Towne MC, Niemeyer CM, Watson HG, Dziegiel MH, Heeney MM, May A, Bottomley SS, Swinkels DW, Markianos K, Craig EA, Fleming MD (2015) Congenital sideroblastic anemia due to mutations in the mitochondrial HSP70 homologue HSPA9. Blood 126(25): 2734−2738

Schmucker S, Argentini M, Carelle-Calmels N, Martelli A, Puccio H (2008) The in vivo mitochondrial two-step maturation of human frataxin. Hum Mol Genet 17(22): 3521−3531

Seyda A, Newbold RF, Hudson TJ, Verner A, MacKay N, Winter S, Feigenbaum A, Malaney S, Gonzalez-Halphen D, Cuthbert AP, Robinson BH (2001) A novel syndrome affecting multiple mitochondrial functions, located by microcell-mediated transfer to chromosome 2p14-2p13. Am J Hum Genet 68(2): 386−396

Sheftel AD, Stehling O, Pierik AJ, Elsasser HP, Muhlenhoff U, Webert H, Hobler A, Hannemann F, Bernhardt R, Lill R (2010) Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis. Proc Natl Acad Sci USA 107(26): 11775−11780

Sheftel AD, Stehling O, Pierik AJ, Netz DJ, Kerscher S, Elsasser HP, Wittig I, Balk J, Brandt U, Lill R (2009) Human ind1, an iron–sulfur cluster assembly factor for respiratory complex I. Mol Cell Biol 29(22): 6059−6073

Sheftel AD, Wilbrecht C, Stehling O, Niggemeyer B, Elsasser HP, Muhlenhoff U, Lill R (2012) The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe–4S] protein maturation. Mol Biol Cell 23(7): 1157−1166

Shi Y, Ghosh M, Kovtunovych G, Crooks DR, Rouault TA (2012) Both human ferredoxins 1 and 2 and ferredoxin reductase are important for iron–sulfur cluster biogenesis. Biochim Biophys Acta 1823(2): 484−492

Shi Y, Ghosh MC, Tong WH, Rouault TA (2009) Human ISD11 is essential for both iron–sulfur cluster assembly and maintenance of normal cellular iron homeostasis. Hum Mol Genet 18(16): 3014−3025

Shukla A, Hebbar M, Srivastava A, Kadavigere R, Upadhyai P, Kanthi A, Brandau O, Bielas S, Girisha KM (2017) Homozygous p.(Glu87Lys) variant in ISCA1 is associated with a multiple mitochondrial dysfunctions syndrome. J Hum Genet 62(7): 723−727

Silberg JJ, Tapley TL, Hoff KG, Vickery LE (2004) Regulation of the HscA ATPase reaction cycle by the co-chaperone HscB and the iron–sulfur cluster assembly protein IscU. J Biol Chem 279(52): 53924−53931

Solish SB, Picado-Leonard J, Morel Y, Kuhn RW, Mohandas TK, Hanukoglu I, Miller WL (1988) Human adrenodoxin reductase: two mRNAs encoded by a single gene on chromosome 17cen----q25 are expressed in steroidogenic tissues. Proc Natl Acad Sci USA 85(19): 7104−7108

Spiegel R, Saada A, Halvardson J, Soiferman D, Shaag A, Edvardson S, Horovitz Y, Khayat M, Shalev SA, Feuk L, Elpeleg O (2014) Deleterious mutation in FDX1L gene is associated with a novel mitochondrial muscle myopathy. Eur J Hum Genet 22(7): 902−906

Stehling O, Lill R (2013) The role of mitochondria in cellular iron–sulfur protein biogenesis: mechanisms, connected processes, and diseases. Cold Spring Harb Perspect Biol 5(8): a011312. https://doi.org/10.1101/cshperspect.a011312

Sun G, Gargus JJ, Ta DT, Vickery LE (2003) Identification of a novel candidate gene in the iron–sulfur pathway implicated in ataxia-susceptibility: human gene encoding HscB, a J-type co-chaperone. J Hum Genet 48(8): 415−419

Tong WH, Jameson GN, Huynh BH, Rouault TA (2003) 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(17): 9762−9767

Tong WH, Rouault T (2000) Distinct iron–sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J 19(21): 5692−5700

Tong WH, Rouault TA (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron–sulfur cluster biogenesis and iron homeostasis. Cell Metab 3(3): 199−210

Tong WH, Rouault TA (2007) Metabolic regulation of citrate and iron by aconitases: role of iron–sulfur cluster biogenesis. Biometals 20(3-4): 549−564

Tsaousis AD (2019) On the origin of iron/sulfur cluster biosynthesis in eukaryotes. Front Microbiol 10: 2478. https://doi.org/10.3389/fmicb.2019.02478

Tsou AY, Paulsen EK, Lagedrost SJ, Perlman SL, Mathews KD, Wilmot GR, Ravina B, Koeppen AH, Lynch DR (2011) Mortality in Friedreich ataxia. J Neurol Sci 307(1-2): 46−49

Uhrigshardt H, Singh A, Kovtunovych G, Ghosh M, Rouault TA (2010) Characterization of the human HSC20, an unusual DnaJ type III protein, involved in iron–sulfur cluster biogenesis. Hum Mol Genet 19(19): 3816−3834

Van Vranken JG, Jeong MY, Wei P, Chen YC, Gygi SP, Winge DR, Rutter J (2016) The mitochondrial acyl carrier protein (ACP) coordinates mitochondrial fatty acid synthesis with iron sulfur cluster biogenesis. Elife 5: e17828. https://doi.org/10.7554/eLife.17828

Vashisht AA, Zumbrennen KB, Huang X, Powers DN, Durazo A, Sun D, Bhaskaran N, Persson A, Uhlen M, Sangfelt O, Spruck C, Leibold EA, Wohlschlegel JA (2009) Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 326(5953): 718−721

Vogtle FN, Brandl B, Larson A, Pendziwiat M, Friederich MW, White SM, Basinger A, Kucukkose C, Muhle H, Jahn JA, Keminer O, Helbig KL, Delto CF, Myketin L, Mossmann D, Burger N, Miyake N, Burnett A, van Baalen A, Lovell MA, Matsumoto N, Walsh M, Yu HC, Shinde DN, Stephani U, Van Hove JLK, Muller FJ, Helbig I (2018) Mutations in PMPCB encoding the catalytic subunit of the mitochondrial presequence protease cause neurodegeneration in early childhood. Am J Hum Genet 102(4): 557−573

Wang H, Shi H, Rajan M, Canarie ER, Hong S, Simoneschi D, Pagano M, Bush MF, Stoll S, Leibold EA, Zheng N (2020) FBXL5 regulates IRP2 stability in iron homeostasis via an oxygen-responsive [2Fe2S] cluster. Mol Cell 78(1): 31−41

Wellcome Trust Case Control C (2007) Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature 447(7145): 661−678

Wiedemann N, Urzica E, Guiard B, Muller H, Lohaus C, Meyer HE, Ryan MT, Meisinger C, Muhlenhoff U, Lill R, Pfanner N (2006) Essential role of Isd11 in mitochondrial iron–sulfur cluster synthesis on Isu scaffold proteins. EMBO J 25(1): 184−195

Wingert RA, Galloway JL, Barut B, Foott H, Fraenkel P, Axe JL, Weber GJ, Dooley K, Davidson AJ, Schmid B, Paw BH, Shaw GC, Kingsley P, Palis J, Schubert H, Chen O, Kaplan J, Zon LI, Tubingen Screen C (2005) Deficiency of glutaredoxin 5 reveals Fe–S clusters are required for vertebrate haem synthesis. Nature 436(7053): 1035−1039

Xia H, Cao Y, Dai X, Marelja Z, Zhou D, Mo R, Al-Mahdawi S, Pook MA, Leimkuhler S, Rouault TA, Li K (2012) Novel frataxin isoforms may contribute to the pathological mechanism of Friedreich ataxia. PLoS One 7(10): e47847. https://doi.org/10.1371/journal.pone.0047847

Yoon H, Knight SA, Pandey A, Pain J, Turkarslan S, Pain D, Dancis A (2015) Turning Saccharomyces cerevisiae into a Frataxin-independent organism. PLoS Genet 11(5): e1005135. https://doi.org/10.1371/journal.pgen.1005135

Zhou YB, Cao JB, Wan BB, Wang XR, Ding GH, Zhu H, Yang HM, Wang KS, Zhang X, Han ZG (2008) hBolA, novel non-classical secreted proteins, belonging to different BolA family with functional divergence. Mol Cell Biochem 317(1-2): 61−68