Recessive germline SDHA and SDHB mutations causing leukodystrophy and isolated mitochondrial complex II deficiency

Journal of Medical Genetics

Volumn 49, Issue 9, 2012, Pages 569-577

  Alston, Charlotte L ^a   Davison, James E ^b,c   Meloni, Francesca ^d   van der Westhuizen, Francois H ^a,e   He, Langping ^a   Hornig Do, Hue Tran ^a   Peet, Andrew C ^b,c   Gissen, Paul ^f,g   Goffrini, Paola ^d   Ferrero, Ileana ^d   Wassmer, Evangeline ^b   McFarland, Robert ^a   Taylor, Robert W ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b BIRMINGHAM CHILDREN S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF PARMA   (Italy)

^e NORTH WEST UNIVERSITY   (South Africa)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DIURETIC AGENT; INOTROPIC AGENT; SDHA ENYZME; SDHB ENZYME; SUCCINATE DEHYDROGENASE; UNCLASSIFIED DRUG;

ARTICLE; CASE REPORT; COMPLEX II DEFICIENCY; CONGESTIVE CARDIOMYOPATHY; CONSANGUINEOUS MARRIAGE; CORPUS CALLOSUM; DEVELOPMENTAL DISORDER; DYSPNEA; ECHOCARDIOGRAPHY; FEMALE; GENE MUTATION; GRAY MATTER; HEART CATHETER; HUMAN; HUMAN TISSUE; LEUKODYSTROPHY; MALE; MUSCLE BIOPSY; MUSCLE HYPOTONIA; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; STEADY STATE; THORAX RADIOGRAPHY;

AMINO ACID SEQUENCE; BASE SEQUENCE; BLOTTING, WESTERN; BRAIN; CHILD, PRESCHOOL; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX II; FEMALE; GENES, RECESSIVE; GENETIC COMPLEMENTATION TEST; GERM-LINE MUTATION; HUMANS; INFANT; INFANT, NEWBORN; LEUKOENCEPHALOPATHIES; MAGNETIC RESONANCE IMAGING; MALE; METABOLISM, INBORN ERRORS; MITOCHONDRIAL DISEASES; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MUTATION; SACCHAROMYCES CEREVISIAE; SUCCINATE DEHYDROGENASE;

EID: 84870281311     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmedgenet-2012-101146     Document Type: Article

References (49)

1. Skladal D, Halliday J, Thorburn DR. Minimum birth prevalence of mitochondrial respiratory chain disorders in children. Brain 2003;126:1905-12.
2. McFarland R, Taylor RW, Turnbull DM. A neurological perspective on mitochondrial disease. Lancet Neurol 2010;9:829-40.
3. Rustin P, Rötig A. Inborn errors of complex II-unusual human mitochondrial diseases. Biochim Biophys Acta 2002;1553:117-22.
4. Parfait B, Chretien D, Rötig A, Marsac C, Munnich A, Rustin P. Compound heterozygous mutations in the flavoprotein gene of the respiratory chain complex II in a patient with Leigh syndrome. Hum Genet 2000;106:236-43.
5. Brière JJ, Favier J, El Ghouzzi V, Djouadi F, Bénit P, Gimenez AP, Rustin P. Succinate dehydrogenase deficiency in human. Cell Mol Life Sci 2005;62:2317-24.
6. Bourgeron T, Rustin P, Chretien D, Birch-Machin M, Bourgeois M, Viegas-Péquignot E, Munnich A, Rötig A. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat Genet 1995;11:144-9.
7. Horvath R, Abicht A, Holinski-Feder E, Laner A, Gempel K, Prokisch H, Lochmüller H, Klopstock T, Jaksch M. Leigh syndrome caused by mutations in the flavoprotein (Fp) subunit of succinate dehydrogenase (SDHA). J Neurol Neurosurg Psychiatry 2006;77:74-6.
8. Pagnamenta AT, Hargreaves IP, Duncan AJ, Taanman JW, Heales SJ, Land JM, Bitner-Glindzicz M, Leonard JV, Rahman S. Phenotypic variability of mitochondrial disease caused by a nuclear mutation in complex II. Mol Genet Metab 2006;89:214-21.
9. Van Coster R, Seneca S, Smet J, Van Hecke R, Gerlo E, Devreese B, Van Beeumen J, Leroy JG, De Meirleir L, Lissens W. Homozygous Gly555Glu mutation in the nuclear-encoded 70 kDa flavoprotein gene causes instability of the respiratory chain complex II. Am J Med Genet A 2003;120:13-18.
10. Levitas A, Muhammad E, Harel G, Saada A, Caspi VC, Manor E, Beck JC, Sheffield V, Parvari R. Familial neonatal isolated cardiomyopathy caused by a mutation in the flavoprotein subunit of succinate dehydrogenase. Eur J Hum Genet 2010;18:1160-5.
11. Ghezzi D, Goffrini P, Uziel G, Horvath R, Klopstock T, Lochmüller H, D'Adamo P, Gasparini P, Strom TM, Prokisch H, Invernizzi F, Ferrero I, Zeviani M. SDHAF1, encoding a LYR complex-II specific assembly factor, is mutated in SDH-defective infantile leukoencephalopathy. Nat Genet 2009;41:654-6.
12. Birch-Machin MA, Taylor RW, Cochran B, Ackrell BA, Turnbull DM. Late-onset optic atrophy, ataxia, and myopathy associated with a mutation of a complex II gene. Ann Neurol 2000;48:330-5.
13. Burnichon N, Brière JJ, Libé R, Vescovo L, Rivière J, Tissier F, Jouanno E, Jeunemaitre X, Bénit P, Tzagoloff A, Rustin P, Bertherat J, Favier J, Gimenez-Roqueplo AP. SDHA is a tumor suppressor gene causing paraganglioma. Hum Mol Genet 2010;19:3011-20.
14. Astuti D, Latif F, Dallol A, Dahia PL, Douglas F, George E, Sköldberg F, Husebye ES, Eng C, Maher ER. Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet 2001;69:49-54.
15. Niemann S, Müller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 2000;26:268-70.
16. Baysal BE, Ferrell RE, Willett-Brozick JE, Lawrence EC, Myssiorek D, Bosch A, van der Mey A, Taschner PE, Rubinstein WS, Myers EN, Richard CW III, Cornelisse CJ, Devilee P, Devlin B. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000;287:848-51.
17. Gimm O, Armanios M, Dziema H, Neumann HP, Eng C. Somatic and occult germ-line mutations in SDHD, a mitochondrial complex II gene, in nonfamilial pheochromocytoma. Cancer Res 2000;60:6822-5.
18. Bayley JP, Kunst HP, Cascon A, Sampietro ML, Gaal J, Korpershoek E, Hinojar-Gutierrez A, Timmers HJ, Hoefsloot LH, Hermsen MA, Suárez C, Hussain AK, Vriends AH, Hes FJ, Jansen JC, Tops CM, Corssmit EP, de Knijff P, Lenders JW, Cremers CW, Devilee P, Dinjens WN, de Krijger RR, Robledo M. SDHAF2 mutations in familial and sporadic paraganglioma and phaeochromocytoma. Lancet Oncol 2010;11:366-72.
19. Bardella C, Pollard PJ, Tomlinson I. SDH mutations in cancer. Biochim Biophys Acta 2011;1807:1432-43.
20. Goffrini P, Ercolino T, Panizza E, Giachè V, Cavone L, Chiarugi A, Dima V, Ferrero I, Mannelli M. Functional study in a yeast model of a novel succinate dehydrogenase subunit B gene germline missense mutation (C191Y) diagnosed in a patient affected by a glomus tumor. Hum Mol Genet 2009;18:1860-8.
21. Wishart DS, Knox C, Guo AC, Eisner R, Young N, Gautam B, Hau DD, Psychogios N, Dong E, Bouatra S, Mandal R, Sinelnikov I, Xia J, Jia L, Cruz JA, Lim E, Sobsey CA, Shrivastava S, Huang P, Liu P, Fang L, Peng J, Fradette R, Cheng D, Tzur D, Clements M, Lewis A, De Souza A, Zuniga A, Dawe M, Xiong Y, Clive D, Greiner R, Nazyrova A, Shaykhutdinov R, Li L, Vogel HJ, Forsythe I. HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res 2009;37:D603-10.
22. Davison JE, Davies NP, Wilson M, Sun Y, Chakrapani A, McKiernan PJ, Walter JH, Gissen P, Peet AC. MR spectroscopy-based brain metabolite profiling in propionic acidaemia: metabolic changes in the basal ganglia during acute decompensation and effect of liver transplantation. Orphanet J Rare Dis 2011;6:19.
23. Kirby DM, Thorburn DR, Turnbull DM, Taylor RW. Biochemical assays of respiratory chain complex activity. Methods Cell Biol 2007;80:93-119.
24. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Gordon L, Hendrix M, Hourlier T, Johnson N, Kähäri AK, Keefe D, Keenan S, Kinsella R, Komorowska M, Koscielny G, Kulesha E, Larsson P, Longden I, McLaren W, Muffato M, Overduin B, Pignatelli M, Pritchard B, Riat HS, Ritchie GR, Ruffier M, Schuster M, Sobral D, Tang YA, Taylor K, Trevanion S, Vandrovcova J, White S, Wilson M, Wilder SP, Aken BL, Birney E, Cunningham F, Dunham I, Durbin R, Fernández-Suarez XM, Harrow J, Herrero J, Hubbard TJ, Parker A, Proctor G, Spudich G, Vogel J, Yates A, Zadissa A, Searle SM. Ensembl 2012. Nucleic Acids Res 2012;40:D84-90.
25. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. A method and server for predicting damaging missense mutations. Nat Methods 2010;7:248-9.
26. Kumar P, Henikoff S, Ng PC. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 2009;4:1073-81.
27. Mathe E, Olivier M, Kato S, Ishioka C, Hainaut P, Tavtigian SV. Computational approaches for predicting the biological effect of p53 missense mutations: a comparison of three sequence analysis based methods. Nucleic Acids Res 2006;34:1317-25.
28. Kelley LA, Sternberg MJ. Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 2009;4:363-71.
29. Bickerton GR, Higueruelo AP, Blundell TL. Comprehensive, atomic-level characterization of structurally characterized protein-protein interactions: the PICCOLO database. BMC Bioinformatics 2011;12:313.
30. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, Clustal W, Clustal X. Version 2.0. Bioinformatics 2007;23:2947-8.
31. Tatusova TA, Madden TL. BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett 1999;174:247-50.
32. Hornig-Do HT, Günther G, Bust M, Lehnartz P, Bosio A, Wiesner RJ. Isolation of functional pure mitochondria by superparamagnetic microbeads. Anal Biochem 2009;389:1-5.
33. Zerbetto E, Vergani L, Dabbeni-Sala F. Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis 1997;18:2059-64.
34. Gietz RD, Schiestl RH. Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2007;2:35-7.
35. Sambrook J, Russel DW. Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2001.
36. Baruffini E, Ferrero I, Foury F. In vivo analysis of mtDNA replication defects in yeast. Methods 2010;51:426-36.
37. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989; 77:51-9.
38. Bonneaud N, Ozier-Kalogeropoulos O, Li GY, Labouesse M, Minvielle-Sebastia L, Lacroute F. A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast 1991;7:609-15.
39. Spiegel R, Pines O, Ta-Shma A, Burak E, Shaag A, Halvardson J, Edvardson S, Mahajna M, Zenvirt S, Saada A, Shalev S, Feuk L, Elpeleg O. Infantile cerebellar-retinal degeneration associated with a mutation in mitochondrial aconitase, ACO2. Am J Hum Genet 2012;90:518-23.
40. van der Knaap MS, van der Voorn P, Barkhof F, Van Coster R, Krägeloh-Mann I, Feigenbaum A, Blaser S, Vles JS, Rieckmann P, Pouwels PJ. A new leukoencephalopathy with brainstem and spinal cord involvement and high lactate. Ann Neurol 2003;53:252-8.
41. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT. Loss of the SdhB, but Not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol Cell Biol 2008;28:718-31.
42. Korpershoek E, Favier J, Gaal J, Burnichon N, van Gessel B, Oudijk L, Badoual C, Gadessaud N, Venisse A, Bayley JP, van Dooren MF, de Herder WW, Tissier F, Plouin PF, van Nederveen FH, Dinjens WN, Gimenez-Roqueplo AP, de Krijger RR. SDHA immunohistochemistry detects germline SDHA gene mutations in apparently sporadic paragangliomas and pheochromocytomas. J Clin Endocrinol Metab 2011;96:E1472-6.
43. Janeway KA, Kim SY, Lodish M, Nosé V, Rustin P, Gaal J, Dahia PL, Liegl B, Ball ER, Raygada M, Lai AH, Kelly L, Hornick JL, O'Sullivan M, de Krijger RR, Dinjens WN, Demetri GD, Antonescu CR, Fletcher JA, Helman L, Stratakis CA. NIH Pediatric and Wild-Type GIST Clinic. Defects in succinate dehydrogenase in gastrointestinal stromal tumors lacking KIT and PDGFRA mutations. Proc Natl Acad Sci USA 2011;108:314-18.
44. Ricketts C, Woodward ER, Killick P, Morris MR, Astuti D, Latif F, Maher ER. Germline SDHB mutations and familial renal cell carcinoma. J Natl Cancer Inst 2008;100:1260-2.
45. Schimke RN, Collins DL, Stolle CA. Paraganglioma, neuroblastoma, and a SDHB mutation: resolution of a 30-year-old mystery. Am J Med Genet A 2010;152:1531-5.
46. Haigis MC, Deng CX, Finley LW, Kim HS, Gius D. SIRT3 is a Mitochondrial tumor suppressor: a scientific tale that connects aberrant cellular ROS, the warburg effect, and carcinogenesis. Cancer Res 2012;72:2468-72.
47. Koivunen P, Hirsilä M, Remes AM, Hassinen IE, Kivirikko KI, Myllyharju J. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem 2007;282:4524-32.
48. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, Pan Y, Simon MC, Thompson CB, Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005;7:77-85.
49. Bugiani M, Lamantea E, Invernizzi F, Moroni I, Bizzi A, Zeviani M, Uziel G. Effects of riboflavin in children with complex II deficiency. Brain Dev 2006;28:576-81.