A novel mutation in BCS1L associated with deafness, tubulopathy, growth retardation and microcephaly

European Journal of Pediatrics

Volumn 175, Issue 4, 2016, Pages 517-525

  Jackson, C B ^a,f   Bauer, M F ^b   Schaller, A ^a   Kotzaeridou, U ^c   Ferrarini, A ^d   Hahn, D ^a   Chehade, H ^e   Barbey, F ^e   Tran, C ^e   Gallati, S ^a   Haeberli, A ^a   Eggimann, S ^a   Bonafe L ^e   Nuoffer, J M ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b KLINIKUM LUDWIGSHAFEN   (Germany)

^c Division of Pediatric Nephrology   (Germany)

^d Ospedale Regionale di Bellinzona e Valli   (Switzerland)

^e LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^f UNIVERSITY OF HELSINKI   (Finland)

Author keywords

BCS1L; Deafness; Fanconi syndrome; Glycosuria; Growth retardation; Hypoglycaemia; Isolated complex III deficiency and assembly; Lactic acidosis; Microcephaly; Mitochondrial disorder; Rieske iron sulphur protein

Indexed keywords

ETIRACETAM; GROWTH HORMONE; OXCARBAZEPINE; PHOSPHATE; BCS1L PROTEIN, HUMAN; UBIQUINOL CYTOCHROME C REDUCTASE;

ADULT; ANTICONVULSANT THERAPY; ARTICLE; BIOCHEMICAL ANALYSIS; CASE REPORT; CHILD; CLINICAL FEATURE; CONVULSION; DELAYED PUBERTY; ELECTROENCEPHALOGRAPHY; FANCONI RENOTUBULAR SYNDROME; FEMALE; GENE; GENETIC ASSOCIATION; GROWTH RETARDATION; HEARING AID; HEARING IMPAIRMENT; HUMAN; HUMAN TISSUE; HYPOPHOSPHATEMIC RICKETS; MALE; MICROCEPHALY; MISSENSE MUTATION; MUSCLE BIOPSY; PERCEPTION DEAFNESS; PRIORITY JOURNAL; SCHOOL CHILD; SUBSTITUTION THERAPY; UBIQUINOL CYTOCHROME C REDUCTASE SYNTHESIS LIKE GENE; YOUNG ADULT; ADOLESCENT; AMINOACIDURIA; CHOLESTASIS; DEFICIENCY; DIFFERENTIAL DIAGNOSIS; FANCONI SYNDROME; GENETICS; GROWTH DISORDER; HEMOSIDEROSIS; HOMOZYGOTE; INBORN ERROR OF METABOLISM; INTELLECTUAL IMPAIRMENT; INTRAUTERINE GROWTH RETARDATION; LACTIC ACIDOSIS; MITOCHONDRIAL DISEASES; NEWBORN; POLYACRYLAMIDE GEL ELECTROPHORESIS; WESTERN BLOTTING;

ACIDOSIS, LACTIC; ADOLESCENT; ADULT; BLOTTING, WESTERN; CHOLESTASIS; DEAFNESS; DIAGNOSIS, DIFFERENTIAL; ELECTRON TRANSPORT COMPLEX III; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FANCONI SYNDROME; FEMALE; FETAL GROWTH RETARDATION; GROWTH DISORDERS; HEMOSIDEROSIS; HOMOZYGOTE; HUMANS; INFANT, NEWBORN; INTELLECTUAL DISABILITY; MALE; METABOLISM, INBORN ERRORS; MICROCEPHALY; MITOCHONDRIAL DISEASES; MUTATION, MISSENSE; RENAL AMINOACIDURIAS;

EID: 84946944648     PISSN: 03406199     EISSN: 14321076     Source Type: Journal    
DOI: 10.1007/s00431-015-2661-y     Document Type: Article

References (29)

1. Al-Owain M, Colak D, Albakheet A, Al-Younes B, Al-Humaidi Z, Al-Sayed M, Al-Hindi H, Al-Sugair A, Al-Muhaideb A, Rahbeeni Z, Al-Sehli A, Al-Fadhli F, Ozand PT, Taylor RW, Kaya N (2013) Clinical and biochemical features associated with BCS1L mutation. J Inherit Metab Dis 36:813–820. doi:10.1007/s10545-012-9536-4
2. Bénit P, Lebon S, Rustin P (2009) Respiratory-chain diseases related to complex III deficiency. Biochim Biophys Acta 1793:181–185. doi:10.1016/j.bbamcr.2008.06.004
3. Blázquez A, Gil-Borlado MC, Morán M, Verdú A, Cazorla-Calleja MR, Martín MA, Arenas J, Ugalde C (2009) Infantile mitochondrial encephalomyopathy with unusual phenotype caused by a novel BCS1L mutation in an isolated complex III-deficient patient. Neuromuscul Disord 19:143–146. doi:10.1016/j.nmd.2008.11.016
4. Conte L, Zara V (2011) The Rieske iron-sulfur protein: import and assembly into the cytochrome bc(1) complex of yeast mitochondria. Bioinorg Chem Appl 2011:363941–363949. doi:10.1155/2011/363941
5. Davey GP, Canevari L, Clark JB (1997) Threshold effects in synaptosomal and nonsynaptic mitochondria from hippocampal CA1 and paramedian neocortex brain regions. J Neurochem 69:2564–2570
6. de Lonlay P, Valnot I, Barrientos A, Gorbatyuk M, Tzagoloff A, Taanman JW, Benayoun E, Chrétien D, Kadhom N, Lombès A, de Baulny HO, Niaudet P, Munnich A, Rustin P, Rotig A (2001) A mutant mitochondrial respiratory chain assembly protein causes complex III deficiency in patients with tubulopathy, encephalopathy and liver failure. Nat Genet 29:57–60. doi:10.1038/ng706
7. Fellman V, Rapola J, Pihko H, Varilo T, Raivio KO (1998) Iron-overload disease in infants involving fetal growth retardation, lactic acidosis, liver haemosiderosis, and aminoaciduria. Lancet 351:490–493. doi:10.1016/S0140-6736(97)09272-6
8. Fernandez-Vizarra E, Bugiani M, Goffrini P, Carrara F, Farina L, Procopio E, Donati A, Uziel G, Ferrero I, Zeviani M (2007) Impaired complex III assembly associated with BCS1L gene mutations in isolated mitochondrial encephalopathy. Hum Mol Genet 16:1241–1252. doi:10.1093/hmg/ddm072
9. Fernandez-Vizarra E, Zeviani M (2015) Nuclear gene mutations as the cause of mitochondrial complex III deficiency. Front Genet. doi:10.3389/fgene.2015.00134
10. Fölsch H, Guiard B, Neupert W, Stuart RA (1996) Internal targeting signal of the BCS1 protein: a novel mechanism of import into mitochondria. EMBO J 15:479–487
11. Ghezzi D, Arzuffi P, Zordan M, Da Re C, Lamperti C, Benna C, D’Adamo P, Diodato D, Costa R, Mariotti C, Uziel G, Smiderle C, Zeviani M (2011) Mutations in TTC19 cause mitochondrial complex III deficiency and neurological impairment in humans and flies. Nat Genet 43:259–263. doi:10.1038/ng.761
12. Ghezzi D, Zeviani M (2012) Assembly factors of human mitochondrial respiratory chain complexes: physiology and pathophysiology. Adv Exp Med Biol 748:65–106. doi:10.1007/978-1-4614-3573-0_4
13. Hinson JT, Fantin VR, Schönberger J, Breivik N, Siem G, McDonough B, Sharma P, Keogh I, Godinho R, Santos F, Esparza A, Nicolau Y, Selvaag E, Cohen BH, Hoppel CL, Tranebjaerg L, Eavey RD, Seidman JG, Seidman CE (2007) Missense mutations in the BCS1L gene as a cause of the Björnstad syndrome. N Engl J Med 356:809–819. doi:10.1056/NEJMoa055262
14. Hinson JT, Fantin VR, Schönberger J, Breivik N, Siem G, McDonough B, Sharma P, Keogh I, Godinho R, Santos F, Esparza A, Nicolau Y, Selvaag E, Cohen BH, Hoppel CL, Tranebjaerg L, Eavey RD, Seidman JG, Seidman CE (2007) Missense mutations in the BCS1L gene as a cause of the Björnstad syndrome. N Engl J Med 356:809–819. doi:10.1056/NEJMoa055262
15. Invernizzi F, Tigano M, Dallabona C, Donnini C, Ferrero I, Cremonte M, Ghezzi D, Lamperti C, Zeviani M (2013) A homozygous mutation in LYRM7/MZM1L associated with early onset encephalopathy, lactic acidosis, and severe reduction of mitochondrial complex III activity. Hum Mutat 34:1619–1622. doi:10.1002/humu.22441
16. Jackson CB, Nuoffer JM, Hahn D, Prokisch H, Haberberger B, Gautschi M, Haberli A, Gallati S, Schaller A (2014) Mutations in SDHD lead to autosomal recessive encephalomyopathy and isolated mitochondrial complex II deficiency. J Med Genet 51:170–175. doi:10.1136/jmedgenet-2013-101932
17. Kleinle S, Wiesmann U, Superti-Furga A, Krähenbühl S, Boltshauser E, Reichen J, Liechti-Gallati S (1997) Detection and characterization of mitochondrial DNA rearrangements in Pearson and Kearns-Sayre syndromes by long PCR. Hum Genet 100:643–650
18. Kotarsky H, Karikoski R, Mörgelin M, Marjavaara S, Bergman P, Zhang D-L, Smet J, van Coster R, Fellman V (2010) Characterization of complex III deficiency and liver dysfunction in GRACILE syndrome caused by a BCS1L mutation. Mitochondrion 10:497–509. doi:10.1016/j.mito.2010.05.009
19. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
20. Marín-Buera L, García-Bartolomé A, Morán M, López-Bernardo E, Cadenas S, Hidalgo B, Sánchez R, Seneca S, Arenas J, Martín MA, Ugalde C (2014) Differential proteomic profiling unveils new molecular mechanisms associated with mitochondrial complex III deficiency. J Proteome 113C:38–56. doi:10.1016/j.jprot.2014.09.007
21. McFarland R, Turnbull DM (2009) Batteries not included: diagnosis and management of mitochondrial disease. J Intern Med 265:210–228. doi:10.1111/j.1365-2796.2008.02066.x
22. Moran (2010) Cellular pathophysiological consequences of BCS1L mutations in mitochondrial complex III enzyme deficiency. 1–12. doi:10.1002/humu.21294
23. Nobrega FG, Nobrega MP, Tzagoloff A (1992) BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. EMBO J 11:3821–3829
24. Shepherd D, Garland PB (1969) The kinetic properties of citrate synthase from rat liver mitochondria. Biochem J 114:597–610
25. Suomalainen A (2011) Therapy for mitochondrial disorders: little proof, high research activity, some promise. Semin Fetal Neonatal Med 16:236–240. doi:10.1016/j.siny.2011.05.003
26. Tucker EJ, Wanschers BFJ, Szklarczyk R, Mountford HS, Wijeyeratne XW, van den Brand MAM, Leenders AM, Rodenburg RJ, Reljić B, Compton AG, Frazier AE, Bruno DL, Christodoulou J, Endo H, Ryan MT, Nijtmans LG, Huynen MA, Thorburn DR (2013) Mutations in the UQCC1-interacting protein, UQCC2, cause human complex III deficiency associated with perturbed cytochrome b protein expression. PLoS Genet 9:e1004034. doi:10.1371/journal.pgen.1004034
27. Visapää I, Fellman V, Vesa J, Dasvarma A, Hutton JL, Kumar V, Payne GS, Makarow M, van Coster R, Taylor RW, Turnbull DM, Suomalainen A, Peltonen L (2002) GRACILE syndrome, a lethal metabolic disorder with iron overload, is caused by a point mutation in BCS1L. Am J Hum Genet 71:863–876. doi:10.1086/342773
28. Wagener N, Ackermann M, Funes S, Neupert W (2011) A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol Cell 44:191–202. doi:10.1016/j.molcel.2011.07.036
29. Wanschers BFJ, Szklarczyk R, van den Brand MAM, Jonckheere A, Suijskens J, Smeets R, Rodenburg RJ, Stephan K, Helland IB, Elkamil A, Rootwelt T, Ott M, van den Heuvel L, Nijtmans LG, Huynen MA (2014) A mutation in the human CBP4 ortholog UQCC3 impairs complex III assembly, activity and cytochrome b stability. Hum Mol Genet. doi:10.1093/hmg/ddu357