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Review ArticleInvited Review
Open Access

Mitochondrial iron-sulfur cluster biogenesis from molecular understanding to clinical disease

Majid Alfadhel, Marwan Nashabat, Qais Abu Ali and Khalid Hundallah
Neurosciences Journal January 2017, 22 (1) 4-13; DOI: https://doi.org/10.17712/nsj.2017.1.20160542
Majid Alfadhel
From the Department of Pediatrics, King Abdulaziz Medical City, Ministry of National Guard-Health Affairs, Riyadh, Kingdom of Saudi Arabia
MD, FCCMG
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Marwan Nashabat
From the Department of Pediatrics, King Abdulaziz Medical City, Ministry of National Guard-Health Affairs, Riyadh, Kingdom of Saudi Arabia
MBBS, MScCR
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Qais Abu Ali
From the Department of Pediatrics, King Abdulaziz Medical City, Ministry of National Guard-Health Affairs, Riyadh, Kingdom of Saudi Arabia
MD, FACMG
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Khalid Hundallah
From the Department of Pediatrics, King Abdulaziz Medical City, Ministry of National Guard-Health Affairs, Riyadh, Kingdom of Saudi Arabia
MD
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References

  1. ↵
    1. Beinert H,
    2. Holm RH,
    3. Munck E
    (1997) Iron-sulfur clusters:nature’s modular, multipurpose structures. Science 277, 653–659.
    1. Beinert H,
    2. Lee W
    (1961) Evidence for a new type of iron containing electron carrier in mitochondria. Biochem Biophys Res Commun 5, 40–45.
  2. ↵
    1. Beinert H,
    2. Sands RH
    (1960) Studies on succinic and DPNH dehydrogenase preparations by paramagnetic resonance (EPR) spectroscopy. Biochemical and Biophysical Research Communications 3, 47–52.
  3. ↵
    1. Rouault TA,
    2. Tong WH
    (2008) Iron-sulfur cluster biogenesis and human disease. Trends Genet 24, 398–407.
  4. ↵
    1. Campuzano V,
    2. Montermini L,
    3. Molto MD,
    4. Pianese L,
    5. Cossee M,
    6. Cavalcanti F,
    7. et al.
    (1996) Friedreich’s ataxia:autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271, 1423–1427.
  5. ↵
    1. Santos R,
    2. Lefevre S,
    3. Sliwa D,
    4. Seguin A,
    5. Camadro JM,
    6. Lesuisse E
    (2010) Friedreich ataxia:molecular mechanisms, redox considerations, and therapeutic opportunities. Antioxid Redox Signal 13, 651–690.
  6. ↵
    1. Pandolfo M,
    2. Pastore A
    (2009) The pathogenesis of Friedreich ataxia and the structure and function of frataxin. J Neurol 256, 9–17.
  7. ↵
    1. Huynen MA,
    2. Snel B,
    3. Bork P,
    4. Gibson TJ
    (2001) The phylogenetic distribution of frataxin indicates a role in iron-sulfur cluster protein assembly. Hum Mol Genet 10, 2463–2468.
  8. ↵
    1. Lill R,
    2. Hoffmann B,
    3. Molik S,
    4. Pierik AJ,
    5. Rietzschel N,
    6. Stehling O,
    7. et al.
    (2012) The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim Biophys Acta 1823, 1491–1508.
  9. ↵
    1. Roche B,
    2. Aussel L,
    3. Ezraty B,
    4. Mandin P,
    5. Py B,
    6. Barras F
    (2013) Reprint of:Iron/sulfur proteins biogenesis in prokaryotes:formation, regulation and diversity. Biochim Biophys Acta 1827, 923–937.
  10. ↵
    1. Zheng L,
    2. White RH,
    3. Cash VL,
    4. Jack RF,
    5. Dean DR
    (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci U S A 90, 2754–2758.
  11. ↵
    1. Tong WH,
    2. Rouault T
    (2000) Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J 19, 5692–5700.
  12. ↵
    1. Shi Y,
    2. Ghosh MC,
    3. Tong WH,
    4. Rouault TA
    (2009) Human ISD11 is essential for both iron-sulfur cluster assembly and maintenance of normal cellular iron homeostasis. Hum Mol Genet 18, 3014–3025.
  13. ↵
    1. Sheftel AD,
    2. Stehling O,
    3. Pierik AJ,
    4. Elsasser HP,
    5. Muhlenhoff U,
    6. Webert H,
    7. et al.
    (2010) 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, 11775–11780.
  14. ↵
    1. Shi Y,
    2. Ghosh M,
    3. Kovtunovych G,
    4. Crooks DR,
    5. Rouault TA
    (2012) Both human ferredoxins 1 and 2 and ferredoxin reductase are important for iron-sulfur cluster biogenesis. Biochim Biophys Acta 1823, 484–492.
  15. ↵
    1. Cozar-Castellano I,
    2. del Valle Machargo M,
    3. Trujillo E,
    4. Arteaga MF,
    5. Gonzalez T,
    6. Martin-Vasallo P,
    7. et al.
    (2004) hIscA:a protein implicated in the biogenesis of iron-sulfur clusters. Biochim Biophys Acta 1700, 179–188.
  16. ↵
    1. Sheftel AD,
    2. Wilbrecht C,
    3. Stehling O,
    4. Niggemeyer B,
    5. Elsasser HP,
    6. Muhlenhoff U,
    7. et al.,
    8. The human mitochondrial ISCA1, ISCA2 and IBA57 proteins are required for [4Fe-4S] protein maturation
    (2012) Mol Biol Cell 23, 1157–1166.
  17. ↵
    1. Shan Y,
    2. Napoli E,
    3. Cortopassi G
    (2007) Mitochondrial frataxin interacts with ISD11 of the NFS1/ISCU complex and multiple mitochondrial chaperones. Hum Mol Genet 16, 929–941.
  18. ↵
    1. Dores-Silva PR,
    2. Minari K,
    3. Ramos CH,
    4. Barbosa LR,
    5. Borges JC
    (2013) Structural and stability studies of the human mtHsp70-escort protein 1:an essential mortalin co-chaperone. Int J Biol Macromol 56, 140–148.
  19. ↵
    1. Uhrigshardt H,
    2. Singh A,
    3. Kovtunovych G,
    4. Ghosh M,
    5. Rouault TA
    (2010) Characterization of the human HSC20, an unusual DnaJ type III protein, involved in iron-sulfur cluster biogenesis. Hum Mol Genet 19, 3816–3834.
  20. ↵
    1. Ye H,
    2. Jeong SY,
    3. Ghosh MC,
    4. Kovtunovych G,
    5. Silvestri L,
    6. Ortillo D,
    7. et al.
    (2010) Glutaredoxin 5 deficiency causes sideroblastic anemia by specifically impairing heme biosynthesis and depleting cytosolic iron in human erythroblasts. J Clin Invest 120, 1749–1761.
  21. ↵
    1. Tong WH,
    2. Jameson GN,
    3. Huynh BH,
    4. 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 U S A 100, 9762–9767.
  22. ↵
    1. Zhou YB,
    2. Cao JB,
    3. Wan BB,
    4. Wang XR,
    5. Ding GH,
    6. Zhu H,
    7. et al.
    (2008) hBolA, novel non-classical secreted proteins, belonging to different BolA family with functional divergence. Mol Cell Biochem 317, 61–68.
  23. ↵
    1. Cameron JM,
    2. Janer A,
    3. Levandovskiy V,
    4. Mackay N,
    5. Rouault TA,
    6. Tong WH,
    7. et al.
    (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, 486–495.
  24. ↵
    1. Mayr JA,
    2. Zimmermann FA,
    3. Fauth C,
    4. Bergheim C,
    5. Meierhofer D,
    6. Radmayr D,
    7. et al.
    (2011) Lipoic acid synthetase deficiency causes neonatal-onset epilepsy, defective mitochondrial energy metabolism, and glycine elevation. Am J Hum Genet 89, 792–797.
  25. ↵
    1. Sheftel AD,
    2. Stehling O,
    3. Pierik AJ,
    4. Netz DJ,
    5. Kerscher S,
    6. Elsasser HP,
    7. et al.
    (2009) Human ind1, an iron-sulfur cluster assembly factor for respiratory complex I. Mol Cell Biol 29, 6059–6073.
  26. ↵
    1. Kispal G,
    2. Csere P,
    3. Guiard B,
    4. Lill R
    (1997) The ABC transporter Atm1p is required for mitochondrial iron homeostasis. FEBS Lett 418, 346–350.
  27. ↵
    1. Mesecke N,
    2. Terziyska N,
    3. Kozany C,
    4. Baumann F,
    5. Neupert W,
    6. Hell K,
    7. et al.
    (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121, 1059–1069.
  28. ↵
    1. Lill R,
    2. Diekert K,
    3. Kaut A,
    4. Lange H,
    5. Pelzer W,
    6. Prohl C,
    7. et al.
    (1999) The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins. Biol Chem 380, 1157–1166.
    1. Kispal G,
    2. Csere P,
    3. Prohl C,
    4. Lill R
    (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J 18, 3981–3989.
  29. ↵
    1. Netz DJ,
    2. Mascarenhas J,
    3. Stehling O,
    4. Pierik AJ,
    5. Lill R
    (2014) Maturation of cytosolic and nuclear iron-sulfur proteins. Trends Cell Biol 24, 303–312.
  30. ↵
    1. Lill R
    (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831–838.
  31. ↵
    1. Zheng L,
    2. White RH,
    3. Cash VL,
    4. Dean DR
    (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33, 4714–4720.
  32. ↵
    1. Kaiser JT,
    2. Clausen T,
    3. Bourenkow GP,
    4. Bartunik HD,
    5. Steinbacher S,
    6. Huber R
    (2000) Crystal structure of a NifS-like protein from Thermotoga maritima:implications for iron sulphur cluster assembly. J Mol Biol 297, 451–464.
  33. ↵
    1. Chen W,
    2. Paradkar PN,
    3. Li L,
    4. Pierce EL,
    5. Langer NB,
    6. Takahashi-Makise N,
    7. et al.
    (2009) Abcb10 physically interacts with mitoferrin-1 (Slc25a37) to enhance its stability and function in the erythroid mitochondria. Proc Natl Acad Sci U S A 106, 16263–16268.
  34. ↵
    1. Gerber J,
    2. Muhlenhoff U,
    3. Lill R
    (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep 4, 906–911.
  35. ↵
    1. Tsai CL,
    2. Barondeau DP
    (2010) Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry 49, 9132–9139.
  36. ↵
    1. Muhlenhoff U,
    2. Gerber J,
    3. Richhardt N,
    4. Lill R
    (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO J 22, 4815–4825.
  37. ↵
    1. Lange H,
    2. Kaut A,
    3. Kispal G,
    4. Lill R
    (2000) A mitochondrial ferredoxin is essential for biogenesis of cellular iron-sulfur proteins. Proc Natl Acad Sci U S A 97, 1050–1055.
  38. ↵
    1. Bonomi F,
    2. Iametti S,
    3. Morleo A,
    4. Ta D,
    5. Vickery LE
    (2008) Studies on the mechanism of catalysis of iron-sulfur cluster transfer from IscU[2F.e2S] by HscA/HscB chaperones. Biochemistry 47, 12795–12801.
  39. ↵
    1. Herrero E,
    2. de la Torre-Ruiz MA
    (2007) Monothiol glutaredoxins:a common domain for multiple functions. Cell Mol Life Sci 64, 1518–1530.
  40. ↵
    1. Bandyopadhyay S,
    2. Gama F,
    3. Molina-Navarro MM,
    4. Gualberto JM,
    5. Claxton R,
    6. Naik SG,
    7. et al.
    (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27, 1122–1133.
  41. ↵
    1. Maio N,
    2. Rouault TA
    (2015) Iron-sulfur cluster biogenesis in mammalian cells:New insights into the molecular mechanisms of cluster delivery. Biochim Biophys Acta 1853, 1493–1512.
  42. ↵
    1. Payne RM,
    2. Wagner GR
    (2012) Cardiomyopathy in Friedreich ataxia:clinical findings and research. J Child Neurol 27, 1179–1186.
    1. Regner SR,
    2. Wilcox NS,
    3. Friedman LS,
    4. Seyer LA,
    5. Schadt KA,
    6. Brigatti KW,
    7. et al.
    (2012) Friedreich ataxia clinical outcome measures:natural history evaluation in 410 participants. J Child Neurol 27, 1152–1158.
    1. Delatycki MB,
    2. Corben LA
    (2012) Clinical features of Friedreich ataxia. J Child Neurol 27, 1133–1137.
    1. Lynch DR,
    2. Farmer JM,
    3. Balcer LJ,
    4. Wilson RB
    (2002) Friedreich ataxia:effects of genetic understanding on clinical evaluation and therapy. Arch Neurol 59, 743–747.
    1. Alikasifoglu M,
    2. Topaloglu H,
    3. Tuncbilek E,
    4. Ceviz N,
    5. Anar B,
    6. Demir E,
    7. et al.
    (1999) Clinical and genetic correlate in childhood onset Friedreich ataxia. Neuropediatrics 30, 72–76.
  43. ↵
    1. De Michele G,
    2. Di Maio L,
    3. Filla A,
    4. Majello M,
    5. Cocozza S,
    6. Cavalcanti F,
    7. et al.
    (1996) Childhood onset of Friedreich ataxia:a clinical and genetic study of 36 cases. Neuropediatrics 27, 3–7.
  44. ↵
    1. Thorburn DR,
    2. Chow CW,
    3. Kirby DM
    (2004) Respiratory chain enzyme analysis in muscle and liver. Mitochondrion 4, 363–375.
  45. ↵
    1. Lim SC,
    2. Friemel M,
    3. Marum JE,
    4. Tucker EJ,
    5. Bruno DL,
    6. Riley LG,
    7. et al.
    (2013) Mutations in LYRM4, encoding iron-sulfur cluster biogenesis factor ISD11, cause deficiency of multiple respiratory chain complexes. Hum Mol Genet 22, 4460–4473.
  46. ↵
    1. Farhan SM,
    2. Wang J,
    3. Robinson JF,
    4. Lahiry P,
    5. Siu VM,
    6. Prasad C,
    7. et al.
    (2014) Exome sequencing identifies NFS1 deficiency in a novel Fe-S cluster disease, infantile mitochondrial complex II/III deficiency. Mol Genet Genomic Med 2, 73–80.
  47. ↵
    1. Pagon RA,
    2. Adam MP,
    3. Ardinger HH,
    4. Wallace SE,
    5. Amemiya A,
    6. Bean LJH,
    7. et al.
    1. Mochel F,
    2. Haller RG
    (1993) Myopathy with Deficiency of ISCU. in Gene Reviews(R), eds Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, et al. (University of Washington, Seattle (WA)).
    1. Sanaker PS,
    2. Toompuu M,
    3. Hogan VE,
    4. He L,
    5. Tzoulis C,
    6. Chrzanowska-Lightowlers ZM,
    7. et al.
    (2010) Differences in RNA processing underlie the tissue specific phenotype of ISCU myopathy. Biochim Biophys Acta 1802, 539–244.
    1. Kollberg G,
    2. Tulinius M,
    3. Melberg A,
    4. Darin N,
    5. Andersen O,
    6. Holmgren D,
    7. et al.
    (2009) Clinical manifestation and a new ISCU mutation in iron-sulphur cluster deficiency myopathy. Brain 132, 2170–2179.
  48. ↵
    1. Olsson A,
    2. Lind L,
    3. Thornell LE,
    4. Holmberg M
    (2008) 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, 1666–1672.
  49. ↵
    1. Spiegel R,
    2. Saada A,
    3. Halvardson J,
    4. Soiferman D,
    5. Shaag A,
    6. Edvardson S,
    7. et al.
    (2014) Deleterious mutation in FDX1L gene is associated with a novel mitochondrial muscle myopathy. Eur J Hum Genet 22, 902–906.
  50. ↵
    1. Fassone E,
    2. Rahman S
    (2012) Complex I deficiency:clinical features, biochemistry and molecular genetics. J Med Genet 49, 578–590.
  51. ↵
    1. Wydro MM,
    2. Sharma P,
    3. Foster JM,
    4. Bych K,
    5. Meyer EH,
    6. Balk J
    (2013) The evolutionarily conserved iron-sulfur protein INDH is required for complex I assembly and mitochondrial translation in Arabidopsis [corrected]. Plant Cell 25, 4014–4027.
  52. ↵
    1. Kevelam SH,
    2. Rodenburg RJ,
    3. Wolf NI,
    4. Ferreira P,
    5. Lunsing RJ,
    6. Nijtmans LG,
    7. et al.
    (2013) NUBPL mutations in patients with complex I deficiency and a distinct MRI pattern. Neurology 80, 1577–1583.
    1. Tenisch EV,
    2. Lebre AS,
    3. Grevent D,
    4. de Lonlay P,
    5. Rio M,
    6. Zilbovicius M,
    7. et al.
    (2012) Massive and exclusive pontocerebellar damage in mitochondrial disease and NUBPL mutations. Neurology 79, 391.
    1. Tucker EJ,
    2. Mimaki M,
    3. Compton AG,
    4. McKenzie M,
    5. Ryan MT,
    6. Thorburn DR
    (2012) Next-generation sequencing in molecular diagnosis:NUBPL mutations highlight the challenges of variant detection and interpretation. Hum Mutat 33, 411–418.
  53. ↵
    1. Calvo SE,
    2. Tucker EJ,
    3. Compton AG,
    4. Kirby DM,
    5. Crawford G,
    6. Burtt NP,
    7. et al.
    (2010) High-throughput, pooled sequencing identifies mutations in NUBPL and FOXRED1 in human complex I deficiency. Nat Genet 42, 851–858.
  54. ↵
    1. Dolatshad H,
    2. Pellagatti A,
    3. Liberante FG,
    4. Llorian M,
    5. Repapi E,
    6. Steeples V,
    7. et al.
    (2016) Cryptic splicing events in the iron transporter ABCB7 and other key target genes in SF3B1-mutant myelodysplastic syndromes. Leukemia 30, 2322–2331.
    1. Protasova MS,
    2. Grigorenko AP,
    3. Tyazhelova TV,
    4. Andreeva TV,
    5. Reshetov DA,
    6. Gusev FE,
    7. et al.
    (2016) Whole-genome sequencing identifies a novel ABCB7 gene mutation for X-linked congenital cerebellar ataxia in a large family of Mongolian ancestry. Eur J Hum Genet 24, 550–555.
  55. ↵
    1. D’Hooghe M,
    2. Selleslag D,
    3. Mortier G,
    4. Van Coster R,
    5. Vermeersch P,
    6. Billiet J,
    7. et al.
    (2012) X-linked sideroblastic anemia and ataxia:a new family with identification of a fourth ABCB7 gene mutation. Eur J Paediatr Neurol 16, 730–735.
  56. ↵
    1. Pagon RA,
    2. Adam MP,
    3. Ardinger HH,
    4. Wallace SE,
    5. Amemiya A,
    6. Bean LJH,
    7. et al.
    1. Bekri S,
    2. D’Hooghe M,
    3. Vermeersch P
    (1993) X-Linked Sideroblastic Anemia and Ataxia. in GeneReviews(R), eds Pagon RA, Adam MP, Ardinger HH, Wallace SE, Amemiya A, Bean LJH, et al. (University of Washington, Seattle (WA)).
  57. ↵
    1. Shebib SM,
    2. Reed MH,
    3. Shuckett EP,
    4. Cross HG,
    5. Perry JB,
    6. Chudley AE
    (1991) Newly recognized syndrome of cerebral, ocular, dental, auricular, skeletal anomalies:CODAS syndrome--a case report. Am J Med Genet 40, 88–93.
  58. ↵
    1. Royer-Bertrand B,
    2. Castillo-Taucher S,
    3. Moreno-Salinas R,
    4. Cho TJ,
    5. Chae JH,
    6. Choi M,
    7. et al.
    (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.
  59. ↵
    1. Schmitz-Abe K,
    2. Ciesielski SJ,
    3. Schmidt PJ,
    4. Campagna DR,
    5. Rahimov F,
    6. Schilke BA,
    7. et al.
    (2015) Congenital sideroblastic anemia due to mutations in the mitochondrial HSP70 homologue HSPA9. Blood 126, 2734–2738.
  60. ↵
    1. Ahting U,
    2. Mayr JA,
    3. Vanlander AV,
    4. Hardy SA,
    5. Santra S,
    6. Makowski C,
    7. et al.
    (2015) Clinical, biochemical, and genetic spectrum of seven patients with NFU1 deficiency. Front Genet 6, 123.
    1. Ferrer-Cortes X,
    2. Font A,
    3. Bujan N,
    4. Navarro-Sastre A,
    5. Matalonga L,
    6. Arranz JA,
    7. et al.
    (2013) Protein expression profiles in patients carrying NFU1 mutations. Contribution to the pathophysiology of the disease. J Inherit Metab Dis 36, 841–847.
  61. ↵
    1. Navarro-Sastre A,
    2. Tort F,
    3. Stehling O,
    4. Uzarska MA,
    5. Arranz JA,
    6. Del Toro M,
    7. et al.
    (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, 656–667.
  62. ↵
    1. Haack TB,
    2. Rolinski B,
    3. Haberberger B,
    4. Zimmermann F,
    5. Schum J,
    6. Strecker V,
    7. et al.
    (2013) Homozygous missense mutation in BOLA3 causes multiple mitochondrial dysfunctions syndrome in two siblings. J Inherit Metab Dis 36, 55–62.
  63. ↵
    1. Baker PR 2nd.,
    2. Friederich MW,
    3. Swanson MA,
    4. Shaikh T,
    5. Bhattacharya K,
    6. Scharer GH,
    7. et al.
    (2014) Variant non ketotic hyperglycinemia is caused by mutations in LIAS, BOLA3 and the novel gene GLRX5. Brain 137, 366–379.
  64. ↵
    1. Debray FG,
    2. Stumpfig C,
    3. Vanlander AV,
    4. Dideberg V,
    5. Josse C,
    6. Caberg JH,
    7. et al.
    (2015) Mutation of the iron-sulfur cluster assembly gene IBA57 causes fatal infantile leukodystrophy. J Inherit Metab Dis 38, 1147–1153.
    1. Lossos A,
    2. Stumpfig C,
    3. Stevanin G,
    4. Gaussen M,
    5. Zimmerman BE,
    6. Mundwiller E,
    7. et al.
    (2015) Fe/S protein assembly gene IBA57 mutation causes hereditary spastic paraplegia. Neurology 84, 659–667.
  65. ↵
    1. Ajit Bolar N,
    2. Vanlander AV,
    3. Wilbrecht C,
    4. Van der Aa N,
    5. Smet J,
    6. De Paepe B,
    7. et al.
    (2013) Mutation of the iron-sulfur cluster assembly gene IBA57 causes severe myopathy and encephalopathy. Hum Mol Genet 22, 2590–2602.
  66. ↵
    1. Al-Hassnan ZN,
    2. Al-Dosary M,
    3. Alfadhel M,
    4. Faqeih EA,
    5. Alsagob M,
    6. Kenana R,
    7. et al.
    (2015) ISCA2 mutation causes infantile neurodegenerative mitochondrial disorder. J Med Genet 52, 186–194.
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Neurosciences Journal: 22 (1)
Neurosciences Journal
Vol. 22, Issue 1
1 Jan 2017
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Mitochondrial iron-sulfur cluster biogenesis from molecular understanding to clinical disease
Majid Alfadhel, Marwan Nashabat, Qais Abu Ali, Khalid Hundallah
Neurosciences Journal Jan 2017, 22 (1) 4-13; DOI: 10.17712/nsj.2017.1.20160542

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Mitochondrial iron-sulfur cluster biogenesis from molecular understanding to clinical disease
Majid Alfadhel, Marwan Nashabat, Qais Abu Ali, Khalid Hundallah
Neurosciences Journal Jan 2017, 22 (1) 4-13; DOI: 10.17712/nsj.2017.1.20160542
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