The spectrum of pyruvate oxidation defects in the diagnosis of mitochondrial disorders

Journal of Inherited Metabolic Disease

Volumn 38, Issue 3, 2015, Pages 391-403

  Sperl, Wolfgang ^a   Fleuren, Leanne ^a,b   Freisinger, Peter ^c   Haack, Tobias B ^d,e   Ribes, Antonia ^f   Feichtinger, René G ^a   Rodenburg, Richard J ^b   Zimmermann, Franz A ^a   Koch, Johannes ^a   Rivera, Isabel ^g,h   Prokisch, Holger ^d,e   Smeitink, Jan A ^b   Mayr, Johannes A ^a  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Kreisklinikum Reutlingen ^*  (Germany)

^d INSTITUTE OF EPIDEMIOLOGY   (Germany)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^g RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^h UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

COCARBOXYLASE; IRON SULFUR PROTEIN; PYRUVATE DEHYDROGENASE COMPLEX; THIOCTIC ACID;

CLASSIFICATION; ENERGY METABOLISM; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; OXIDATION REDUCTION REACTION; PYRUVATE DEHYDROGENASE COMPLEX DEFICIENCY DISEASE;

ENERGY METABOLISM; FEMALE; HUMANS; IRON-SULFUR PROTEINS; MALE; OXIDATION-REDUCTION; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATE DEHYDROGENASE COMPLEX DEFICIENCY DISEASE; THIAMINE PYROPHOSPHATE; THIOCTIC ACID;

EID: 84939966297     PISSN: 01418955     EISSN: 15732665     Source Type: Journal    
DOI: 10.1007/s10545-014-9787-3     Document Type: Article

References (87)

1. Ah Mew N, Loewenstein JB, Kadom N et al (2011) MRI features of 4 female patients with pyruvate dehydrogenase E1 alpha deficiency. Pediatr Neurol 45:57–59
2. Ajit Bolar N, Vanlander AV, Wilbrecht C et al (2013) Mutation of the iron-sulfur cluster assembly gene IBA57 causes severe myopathy and encephalopathy. Hum Mol Genet 22:2590–2602
3. Alfadhel M, Almuntashri M, Jadah RH et al (2013) Biotin-responsive basal ganglia disease should be renamed biotin-thiamine-responsive basal ganglia disease: a retrospective review of the clinical, radiological and molecular findings of 18 new cases. Orphanet J Rare Dis 8:83
4. Aral B, Benelli C, Ait-Ghezala G et al (1997) Mutations in PDX1, the human lipoyl-containing component X of the pyruvate dehydrogenase-complex gene on chromosome 11p1, in congenital lactic acidosis. Am J Hum Genet 61:1318–1326
5. Baker PR 2nd, Friederich MW, Swanson MA et al (2014) Variant non ketotic hyperglycinemia is caused by mutations in LIAS, BOLA3 and the novel gene GLRX5. Brain 137:366–379
6. Blass JP, Avigan J, Uhlendorf BW (1970) A defect in pyruvate decarboxylase in a child with an intermittent movement disorder. J Clin Invest 49:423–432
7. Bonne G, Benelli C, De Meirleir L et al (1993) E1 pyruvate dehydrogenase deficiency in a child with motor neuropathy. Pediatr Res 33:284–288
8. Bookelman H, Trijbels JM, Sengers RC, Janssen AJ, Veerkamp JH, Stadhouders AM (1978) Pyruvate oxidation in rat and human skeletal muscle mitochondria. Biochem Med 20:395–403
9. Brassier A, Ottolenghi C, Boutron A et al (2013) Dihydrolipoamide dehydrogenase deficiency: a still overlooked cause of recurrent acute liver failure and Reye-like syndrome. Mol Genet Metab 109:28–32
10. Bricker DK, Taylor EB, Schell JC et al (2012) A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 337:96–100
11. Brivet M, Garcia-Cazorla A, Lyonnet S et al (2003) Impaired mitochondrial pyruvate importation in a patient and a fetus at risk. Mol Genet Metab 78:186–192
12. Brown G (2014) Defects of thiamine transport and metabolism. J Inherit Metab Dis 37:577–585
13. Brown RM, Head RA, Boubriak II, Leonard JV, Thomas NH, Brown GK (2004) Mutations in the gene for the E1beta subunit: a novel cause of pyruvate dehydrogenase deficiency. Hum Genet 115:123–127
14. Cameron JM, Janer A, Levandovskiy V 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
15. Cameron JM, Maj M, Levandovskiy V et al (2009) Pyruvate dehydrogenase phosphatase 1 (PDP1) null mutation produces a lethal infantile phenotype. Hum Genet 125:319–326
16. Carrozzo R, Torraco A, Fiermonte G, et al (2014) Riboflavin responsive mitochondrial myopathy is a new phenotype of dihydrolipoamide dehydrogenase deficiency. The chaperon-like effect of vitamin B2. Mitochondrion
17. Danhauser K, Sauer SW, Haack TB et al (2012) DHTKD1 mutations cause 2-aminoadipic and 2-oxoadipic aciduria. Am J Hum Genet 91:1082–1087
18. DeBrosse SD, Okajima K, Zhang S et al (2012) Spectrum of neurological and survival outcomes in pyruvate dehydrogenase complex (PDC) deficiency: lack of correlation with genotype. Mol Genet Metab 107:394–402
19. Debs R, Depienne C, Rastetter A et al (2010) Biotin-responsive basal ganglia disease in ethnic Europeans with novel SLC19A3 mutations. Arch Neurol 67:126–130
20. Di Rocco M, Lamba LD, Minniti G, Caruso U, Naito E (2000) Outcome of thiamine treatment in a child with Leigh disease due to thiamine-responsive pyruvate dehydrogenase deficiency. Eur J Paediatr Neurol 4:115–117
21. Djouadi F, Bastin J (2011) Species differences in the effects of bezafibrate as a potential treatment of mitochondrial disorders. Cell Metab 14:715–716, author reply 717
22. El-Gharbawy AH, Boney A, Young SP, Kishnani PS (2011) Follow-up of a child with pyruvate dehydrogenase deficiency on a less restrictive ketogenic diet. Mol Genet Metab 102:214–215
23. Endo H, Hasegawa K, Narisawa K, Tada K, Kagawa Y, Ohta S (1989) Defective gene in lactic acidosis: abnormal pyruvate dehydrogenase E1 alpha-subunit caused by a frame shift. Am J Hum Genet 44:358–364
24. Ferriero R, Brunetti-Pierri N (2013) Phenylbutyrate increases activity of pyruvate dehydrogenase complex. Oncotarget 4:804–805
25. Ferriero R, Manco G, Lamantea E et al (2013) Phenylbutyrate therapy for pyruvate dehydrogenase complex deficiency and lactic acidosis. Sci Transl Med 5:175ra131
26. Fraser J, Vanderver A, Yang S et al (2014) Thiamine pyrophosphokinase deficiency causes a Leigh disease like phenotype in a sibling pair: identification through whole exome sequencing and management strategies. Mol Genet Metab Rep 1:66–70
27. Geoffroy V, Fouque F, Benelli C et al (1996) Defect in the X-lipoyl-containing component of the pyruvate dehydrogenase complex in a patient with neonatal lactic acidemia. Pediatrics 97:267–272
28. Gerards M, Kamps R, van Oevelen J et al (2013) Exome sequencing reveals a novel Moroccan founder mutation in SLC19A3 as a new cause of early-childhood fatal Leigh syndrome. Brain 136:882–890
29. Giribaldi G, Doria-Lamba L, Biancheri R et al (2012) Intermittent-relapsing pyruvate dehydrogenase complex deficiency: a case with clinical, biochemical, and neuroradiological reversibility. Dev Med Child Neurol 54:472–476
30. Haack TB, Klee D, Strom TM et al (2014) Infantile Leigh-like syndrome caused by SLC19A3 mutations is a treatable disease. Brain 137:e295
31. Haack TB, Rolinski B, Haberberger B et al (2013) Homozygous missense mutation in BOLA3 causes multiple mitochondrial dysfunctions syndrome in two siblings. J Inherit Metab Dis 36:55–62
32. Han Z, Berendzen K, Zhong L et al (2008) A combined therapeutic approach for pyruvate dehydrogenase deficiency using self-complementary adeno-associated virus serotype-specific vectors and dichloroacetate. Mol Genet Metab 93:381–387
33. Haviv R, Zeharia A, Belaiche C, Haimi Cohen Y, Saada A (2014) Elevated plasma citrulline: look for dihydrolipoamide dehydrogenase deficiency. Eur J Pediatr 173:243–245
34. Head RA, Brown RM, Zolkipli Z et al (2005) Clinical and genetic spectrum of pyruvate dehydrogenase deficiency: dihydrolipoamide acetyltransferase (E2) deficiency. Ann Neurol 58:234–241
35. Herzig S, Raemy E, Montessuit S et al (2012) Identification and functional expression of the mitochondrial pyruvate carrier. Science 337:93–96
36. Imbard A, Boutron A, Vequaud C et al (2011) Molecular characterization of 82 patients with pyruvate dehydrogenase complex deficiency. Structural implications of novel amino acid substitutions in E1 protein. Mol Genet Metab 104:507–516
37. Ivanov IS, Azmanov DN, Ivanova MB et al (2014) Founder p.Arg 446* mutation in the PDHX gene explains over half of cases with congenital lactic acidosis in Roma children. Mol Genet Metab 113:76–83
38. Kennerson ML, Yiu EM, Chuang DT et al (2013) A new locus for X-linked dominant Charcot-Marie-Tooth disease (CMTX6) is caused by mutations in the pyruvate dehydrogenase kinase isoenzyme 3 (PDK3) gene. Hum Mol Genet 22:1404–1416
39. Kevelam SH, Bugiani M, Salomons GS et al (2013) Exome sequencing reveals mutated SLC19A3 in patients with an early-infantile, lethal encephalopathy. Brain 136:1534–1543
40. Kollberg G, Tulinius M, Melberg A et al (2009) Clinical manifestation and a new ISCU mutation in iron-sulphur cluster deficiency myopathy. Brain 132:2170–2179
41. Lawson JE, Park SH, Mattison AR, Yan J, Reed LJ (1997) Cloning, expression, and properties of the regulatory subunit of bovine pyruvate dehydrogenase phosphatase. J Biol Chem 272:31625–31629
42. Lissens W, De Meirleir L, Seneca S et al (2000) Mutations in the X-linked pyruvate dehydrogenase (E1) alpha subunit gene (PDHA1) in patients with a pyruvate dehydrogenase complex deficiency. Hum Mutat 15:209–219
43. Liu TC, Kim H, Arizmendi C, Kitano A, Patel MS (1993) Identification of two missense mutations in a dihydrolipoamide dehydrogenase-deficient patient. Proc Natl Acad Sci U S A 90:5186–5190
44. Magner M, Vinsova K, Tesarova M et al (2011) Two patients with clinically distinct manifestation of pyruvate dehydrogenase deficiency due to mutations in PDHA1 gene. Prague Med Rep 112:18–28
45. Maj MC, MacKay N, Levandovskiy V et al (2005) Pyruvate dehydrogenase phosphatase deficiency: identification of the first mutation in two brothers and restoration of activity by protein complementation. J Clin Endocrinol Metab 90:4101–4107
46. Mayr JA, Feichtinger RG, Tort F, Ribes A, Sperl W (2014) Lipoic acid biosynthesis defects. J Inherit Metab Dis 37:553–563
47. Mayr JA, Freisinger P, Schlachter K et al (2011a) Thiamine pyrophosphokinase deficiency in encephalopathic children with defects in the pyruvate oxidation pathway. Am J Hum Genet 89:806–812
48. Mayr JA, Koch J, Fauth C et al (2012) A 1.1 million base pair X-chromosomal deletion covering the PDHA1 and CDKL5 genes in a female patient with West syndrome and pyruvate oxidation deficiency. Neuropediatrics 43:130–134
49. Mayr JA, Zimmermann FA, Fauth C et al (2011b) Lipoic acid synthetase deficiency causes neonatal-onset epilepsy, defective mitochondrial energy metabolism, and glycine elevation. Am J Hum Genet 89:792–797
50. McWilliam CA, Ridout CK, Brown RM, McWilliam RC, Tolmie J, Brown GK (2010) Pyruvate dehydrogenase E2 deficiency: a potentially treatable cause of episodic dystonia. Eur J Paediatr Neurol 14:349–353
51. Mochel F, Knight MA, Tong WH et al (2008) Splice mutation in the iron-sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance. Am J Hum Genet 82:652–660
52. Naito E, Ito M, Yokota I et al (2002) Thiamine-responsive pyruvate dehydrogenase deficiency in two patients caused by a point mutation (F205L and L216F) within the thiamine pyrophosphate binding region. Biochim Biophys Acta 1588:79–84
53. Navarro-Sastre A, Tort F, Stehling O 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
54. Nizon M, Boutron A, Boddaert N et al (2014) Leukoencephalopathy with cysts and hyperglycinemia may result from NFU1 deficiency. Mitochondrion 15:59–64
55. Okajima K, Korotchkina LG, Prasad C et al (2008) Mutations of the E1beta subunit gene (PDHB) in four families with pyruvate dehydrogenase deficiency. Mol Genet Metab 93:371–380
56. Olsson A, Lind L, Thornell LE, 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
57. Ortigoza-Escobar JD, Serrano M, Molero M et al (2014) Thiamine transporter-2 deficiency: outcome and treatment monitoring. Orphanet J Rare Dis 9:92
58. Pastoris O, Savasta S, Foppa P, Catapano M, Dossena M (1996) Pyruvate dehydrogenase deficiency in a child responsive to thiamine treatment. Acta Paediatr 85:625–628
59. Patel KP, O'Brien TW, Subramony SH, Shuster J, Stacpoole PW (2012) The spectrum of pyruvate dehydrogenase complex deficiency: clinical, biochemical and genetic features in 371 patients. Mol Genet Metab 105:34–43
60. Paul VD, Lill R (2014) SnapShot: Eukaryotic Fe-S Protein Biogenesis. Cell Metab 20(384–384):e381
61. Pfeffer G, Horvath R, Klopstock T et al (2013) New treatments for mitochondrial disease-no time to drop our standards. Nat Rev Neurol 9:474–481
62. Prasad C, Rupar T, Prasad AN (2011) Pyruvate dehydrogenase deficiency and epilepsy. Brain Dev 33:856–865
63. Quinonez SC, Leber SM, Martin DM, Thoene JG, Bedoyan JK (2013) Leigh syndrome in a girl with a novel DLD mutation causing E3 deficiency. Pediatr Neurol 48:67–72
64. Quinonez SC, Thoene JG (1993) Dihydrolipoamide dehydrogenase deficiency. In Pagon RA, Adam MP, Ardinger HH et al (eds.) GeneReviews. University of Washington, Seattle
65. Quintana E, Mayr JA, Garcia Silva MT et al (2009) PDH E1beta deficiency with novel mutations in two patients with Leigh syndrome. J Inherit Metab Dis 32(Suppl 1):S339–S343
66. Quintana E, Pineda M, Font A et al (2010) Dihydrolipoamide dehydrogenase (DLD) deficiency in a Spanish patient with myopathic presentation due to a new mutation in the interface domain. J Inherit Metab Dis 33(Suppl 3):S315–S319
67. Rustin P, Chretien D, Bourgeron T et al (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin Chim Acta 228:35–51
68. Sanaker PS, Toompuu M, Hogan VE et al (2010) Differences in RNA processing underlie the tissue specific phenotype of ISCU myopathy. Biochim Biophys Acta 1802:539–544
69. Seyda A, Newbold RF, Hudson TJ et al (2001) A novel syndrome affecting multiple mitochondrial functions, located by microcell-mediated transfer to chromosome 2p14-2p13. Am J Hum Genet 68:386–396
70. Shaag A, Saada A, Berger I et al (1999) Molecular basis of lipoamide dehydrogenase deficiency in Ashkenazi Jews. Am J Med Genet 82:177–182
71. Sheftel AD, Wilbrecht C, Stehling O et al (2012) The human mitochondrial ISCA1, ISCA2, and IBA57 proteins are required for [4Fe-4S] protein maturation. Mol Biol Cell 23:1157–1166
72. Silva MJ, Pinheiro A, Eusebio F, Gaspar A, Tavares de Almeida I, Rivera I (2009) Pyruvate dehydrogenase deficiency: identification of a novel mutation in the PDHA1 gene which responds to amino acid supplementation. Eur J Pediatr 168:17–22
73. Singhi P, De Meirleir L, Lissens W, Singhi S, Saini AG (2013) Pyruvate dehydrogenase-e1alpha deficiency presenting as recurrent demyelination: an unusual presentation and a novel mutation. JIMD Rep 10:107–111
74. Soreze Y, Boutron A, Habarou F et al (2013) Mutations in human lipoyltransferase gene LIPT1 cause a Leigh disease with secondary deficiency for pyruvate and alpha-ketoglutarate dehydrogenase. Orphanet J Rare Dis 8:192
75. Sperl W, Ruitenbeek W, Sengers RC et al (1992) Combined deficiencies of the pyruvate dehydrogenase complex and enzymes of the respiratory chain in mitochondrial myopathies. Eur J Pediatr 151:192–195
76. Sperl W, Trijbels JM, Ruitenbeek W et al (1993) Measurement of totally activated pyruvate dehydrogenase complex activity in human muscle: evaluation of a useful assay. Enzyme Protein 47:37–46
77. Spiegel R, Shaag A, Edvardson S et al (2009) SLC25A19 mutation as a cause of neuropathy and bilateral striatal necrosis. Ann Neurol 66:419–424
78. Stacpoole PW, Kerr DS, Barnes C et al (2006) Controlled clinical trial of dichloroacetate for treatment of congenital lactic acidosis in children. Pediatrics 117:1519–1531
79. Stehling O, Wilbrecht C, Lill R (2014) Mitochondrial iron-sulfur protein biogenesis and human disease. Biochimie 100:61–77
80. Steller J, Gargus JJ, Gibbs LH, Hasso AN, Kimonis VE (2014) Mild phenotype in a male with pyruvate dehydrogenase complex deficiency associated with novel hemizygous in-frame duplication of the E1alpha subunit gene (PDHA1). Neuropediatrics 45:56–60
81. Strassburg HM, Koch J, Mayr J, Sperl W, Boltshauser E (2006) Acute flaccid paralysis as initial symptom in 4 patients with novel E1alpha mutations of the pyruvate dehydrogenase complex. Neuropediatrics 37:137–141
82. Tamaru S, Kikuchi A, Takagi K et al (2012) A case of pyruvate dehydrogenase E1alpha subunit deficiency with antenatal brain dysgenesis demonstrated by prenatal sonography and magnetic resonance imaging. J Clin Ultrasound 40:234–238
83. Tort F, Ferrer-Cortes X, Thio M et al (2014) Mutations in the lipoyltransferase LIPT1 gene cause a fatal disease associated with a specific lipoylation defect of the 2-ketoacid dehydrogenase complexes. Hum Mol Genet 23:1907–1915
84. Wexler ID, Hemalatha SG, McConnell J et al (1997) Outcome of pyruvate dehydrogenase deficiency treated with ketogenic diets. Studies in patients with identical mutations. Neurology 49:1655–1661
85. Wibom R, Hagenfeldt L, von Dobeln U (2002) Measurement of ATP production and respiratory chain enzyme activities in mitochondria isolated from small muscle biopsy samples. Anal Biochem 311:139–151
86. Yoshida I, Sweetman L, Kulovich S, Nyhan WL, Robinson BH (1990) Effect of lipoic acid in a patient with defective activity of pyruvate dehydrogenase, 2-oxoglutarate dehydrogenase, and branched-chain keto acid dehydrogenase. Pediatr Res 27:75–79
87. Zeng WQ, Al-Yamani E, Acierno JS Jr et al (2005) Biotin-responsive basal ganglia disease maps to 2q36.3 and is due to mutations in SLC19A3. Am J Hum Genet 77:16–26