Clinical features, molecular heterogeneity, and prognostic implications in YARS2-related mitochondrial myopathy

JAMA Neurology

Volumn 74, Issue 6, 2017, Pages 686-694

  Sommerville, Ewen W ^a   Ng, Yi Shiau ^a   Alston, Charlotte L ^a   Dallabona, Cristina ^b   Gilberti, Micol ^b   He, Langping ^a   Knowles, Charlotte ^a   Chin, Sophie L ^a   Schaefer, Andrew M ^a   Falkous, Gavin ^a   Murdoch, David ^c   Longman, Cheryl ^c   De Visser, Marianne ^d   Bindoff, Laurence A ^e,f   Rawles, John M ^g   Dean, John C S ^h   Petty, Richard K ^c   Farrugia, Maria E ^c   Haack, Tobias B ^i,j   Prokisch, Holger ^i,j   McFarland, Robert ^a   Turnbull, Douglass M ^a   Donnini, Claudia ^b   Taylor, Robert W ^a   Gorman, Gráinne S ^a   more..

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF PARMA   (Italy)

^c QUEEN ELIZABETH UNIVERSITY HOSPITAL   (United Kingdom)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF BERGEN   (Norway)

^f HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^g UNIVERSITY OF ABERDEEN   (United Kingdom)

^h UNIVERSITY OF ABERDEEN   (United Kingdom)

ⁱ INSTITUTE OF EPIDEMIOLOGY   (Germany)

^j TECHNICAL UNIVERSITY OF MUNICH   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

LACTIC ACID; MITOCHONDRIAL DNA; TYROSINE TRANSFER RNA LIGASE;

ADOLESCENT; ADULT; ARTICLE; CASE STUDY; CENTRAL NERVOUS SYSTEM DISEASE; CHILD; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOCHROME C OXIDASE DEFICIENCY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; FIBROBLAST; GENE; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; HUMAN; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; IMMUNOBLOTTING; INFANT; LACTATE BLOOD LEVEL; MALE; MITOCHONDRIAL MYOPATHY; MUSCLE BIOPSY; MUTANT; MYOBLAST; NEWBORN; OBSERVATIONAL STUDY; PRIORITY JOURNAL; PROGNOSIS; RESPIRATORY FAILURE; SIDEROBLASTIC ANEMIA; YARS2 GENE; ACIDOSIS, LACTIC; AGED; ANEMIA, SIDEROBLASTIC; CARDIOMYOPATHIES; COMPLICATION; ENGLAND; ETHNOLOGY; GENETICS; MIDDLE AGED; MUSCLE WEAKNESS; MUTATION; RESPIRATORY INSUFFICIENCY; SCOTLAND;

ACIDOSIS, LACTIC; ADULT; AGED; ANEMIA, SIDEROBLASTIC; CARDIOMYOPATHIES; ENGLAND; FEMALE; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIAL MYOPATHIES; MUSCLE WEAKNESS; MUTATION; PROGNOSIS; RESPIRATORY INSUFFICIENCY; SCOTLAND; TYROSINE-TRNA LIGASE;

EID: 85020752481     PISSN: 21686149     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamaneurol.2016.4357     Document Type: Article

References (51)

1. Skladal D, Halliday J, Thorburn DR. Minimum birth prevalence of mitochondrial respiratory chain disorders in children. Brain. 2003;126(Pt 8):1905-1912.
2. Gorman GS, Schaefer AM, Ng Y, et al. Prevalence of nuclear and mitochondrial DNA mutations related to adult mitochondrial disease. Ann Neurol. 2015;77(5):753-759.
3. Scheper GC, van der Klok T, van Andel RJ, et al. Mitochondrial aspartyl-tRNA synthetase deficiency causes leukoencephalopathy with brain stem and spinal cord involvement and lactate elevation. Nat Genet. 2007;39(4):534-539.
4. Riley LG, Cooper S, Hickey P, et al. Mutation of the mitochondrial tyrosyl-tRNA synthetase gene, YARS2, causes myopathy, lactic acidosis, and sideroblastic anemia - MLASA syndrome. Am J Hum Genet. 2010;87(1):52-59.
5. Steenweg ME, Ghezzi D, Haack T, et al. Leukoencephalopathy with thalamus and brainstem involvement and high lactate "LTBL" caused by EARS2 mutations. Brain. 2012;135(Pt 5):1387-1394.
6. McMillan HJ, Schwartzentruber J, Smith A, et al. Compound heterozygous mutations in glycyl-tRNA synthetase are a proposed cause of systemic mitochondrial disease. BMC Med Genet. 2014;15:36.
7. Sofou K, Kollberg G, Holmström M, et al. Whole exome sequencing reveals mutations in NARS2 and PARS2, encoding the mitochondrial asparaginyl-tRNA synthetase and prolyl-tRNA synthetase, in patients with Alpers syndrome. Mol Genet Genomic Med. 2015;3(1):59-68.
8. Vanlander AV, Menten B, Smet J, et al. Two siblings with homozygous pathogenic splice-site variant in mitochondrial asparaginyl-tRNA synthetase (NARS2). Hum Mutat. 2015;36(2):222-231.
9. Götz A, Tyynismaa H, Euro L, et al. Exome sequencing identifies mitochondrial alanyl-tRNA synthetase mutations in infantile mitochondrial cardiomyopathy. Am J Hum Genet. 2011;88(5):635-642.
10. Diodato D, Melchionda L, Haack TB, et al. VARS2 and TARS2 mutations in patients with mitochondrial encephalomyopathies. Hum Mutat. 2014;35(8):983-989.
11. Pierce SB, Gersak K, Michaelson-Cohen R, et al. Mutations in LARS2, encoding mitochondrial leucyl-tRNA synthetase, lead to premature ovarian failure and hearing loss in Perrault syndrome. Am J Hum Genet. 2013;92(4):614-620.
12. Schwartzentruber J, Buhas D, Majewski J, et al; FORGE Canada Consortium. Mutation in the nuclear-encoded mitochondrial isoleucyl-tRNA synthetase IARS2 in patients with cataracts, growth hormone deficiency with short stature, partial sensorineural deafness, and peripheral neuropathy or with Leigh syndrome. Hum Mutat. 2014;35(11):1285-1289.
13. Bayat V, Thiffault I, Jaiswal M, et al. Mutations in the mitochondrial methionyl-tRNA synthetase cause a neurodegenerative phenotype in flies and a recessive ataxia (ARSAL) in humans. PLoS Biol. 2012;10(3):e1001288.
14. Hallmann K, Zsurka G, Moskau-Hartmann S, et al. A homozygous splice-site mutation in CARS2 is associated with progressive myoclonic epilepsy. Neurology. 2014;83(23):2183-2187.
15. Elo JM, Yadavalli SS, Euro L, et al. Mitochondrial phenylalanyl-tRNA synthetase mutations underlie fatal infantile Alpers encephalopathy. Hum Mol Genet. 2012;21(20):4521-4529.
16. Pierce SB, Chisholm KM, Lynch ED, et al. Mutations in mitochondrial histidyl tRNA synthetase HARS2 cause ovarian dysgenesis and sensorineural hearing loss of Perrault syndrome. Proc Natl Acad Sci USA. 2011;108(16):6543-6548.
17. Edvardson S, Shaag A, Kolesnikova O, et al. Deleterious mutation in the mitochondrial arginyl-transfer RNA synthetase gene is associated with pontocerebellar hypoplasia. Am J Hum Genet. 2007;81(4):857-862.
18. Belostotsky R, Ben-Shalom E, Rinat C, et al. Mutations in the mitochondrial seryl-tRNA synthetase cause hyperuricemia, pulmonary hypertension, renal failure in infancy and alkalosis, HUPRA syndrome. Am J Hum Genet. 2011;88(2):193-200.
19. Ardissone A, Lamantea E, Quartararo J, et al. A novel homozygous YARS2 mutation in two Italian siblings and a review of literature. JIMD Rep. 2015;20:95-101.
20. Nakajima J, Eminoglu TF, Vatansever G, et al. A novel homozygous YARS2 mutation causes severe myopathy, lactic acidosis, and sideroblastic anemia 2. J Hum Genet. 2014;59(4):229-232.
21. Riley LG, Menezes MJ, Rudinger-Thirion J, et al. Phenotypic variability and identification of novel YARS2 mutations in YARS2 mitochondrial myopathy, lactic acidosis and sideroblastic anaemia. Orphanet J Rare Dis. 2013;8:193.
22. Sasarman F, Nishimura T, Thiffault I, Shoubridge EA. A novel mutation in YARS2 causes myopathy with lactic acidosis and sideroblastic anemia. Hum Mutat. 2012;33(8):1201-1206.
23. Shahni R, Wedatilake Y, Cleary MA, Lindley KJ, Sibson KR, Rahman S. A distinct mitochondrial myopathy, lactic acidosis and sideroblastic anemia (MLASA) phenotype associates with YARS2 mutations. Am J Med Genet A. 2013;161A(9):2334-2338.
24. Bykhovskaya Y, Casas K, Mengesha E, Inbal A, Fischel-Ghodsian N. Missense mutation in pseudouridine synthase 1 (PUS1) causes mitochondrial myopathy and sideroblastic anemia (MLASA). Am J Hum Genet. 2004;74(6):1303-1308.
25. Riley LG, Rudinger-Thirion J, Schmitz-Abe K, et al. LARS2 variants associated with hydrops, lactic acidosis, sideroblastic anemia, and multisystem failure [published online November 5, 2015]. JIMD Rep.
26. Burrage LC, Tang S, Wang J, et al. Mitochondrial myopathy, lactic acidosis, and sideroblastic anemia (MLASA) plus associated with a novel de novo mutation (m.8969G>A) in the mitochondrial encoded ATP6 gene. Mol Genet Metab. 2014;113(3):207-212.
27. Pearson HA, Lobel JS, Kocoshis SA, et al. A new syndrome of refractory sideroblastic anemia with vacuolization of marrow precursors and exocrine pancreatic dysfunction. J Pediatr. 1979;95(6):976-984.
28. McShane MA, Hammans SR, Sweeney M, et al. Pearson syndrome and mitochondrial encephalomyopathy in a patient with a deletion of mtDNA. Am J Hum Genet. 1991;48(1):39-42.
29. Rawles JM, Weller RO. Familial association of metabolic myopathy, lactic acidosis and sideroblastic anemia. Am J Med. 1974;56(6):891-897.
30. World Medical Association. World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-2194.
31. Taylor RW, Schaefer AM, Barron MJ, McFarland R, Turnbull DM. The diagnosis of mitochondrial muscle disease. Neuromuscul Disord. 2004;14(4):237-245.
32. Kirby DM, Thorburn DR, Turnbull DM, Taylor RW. Biochemical assays of respiratory chain complex activity. Methods Cell Biol. 2007;80:93-119.
33. Kloss-Brandstätter A, Pacher D, Schönherr S, et al. HaploGrep: a fast and reliable algorithm for automatic classification of mitochondrial DNA haplogroups. Hum Mutat. 2011;32(1):25-32.
34. Taylor RW, Pyle A, Griffin H, et al. Use of whole-exome sequencing to determine the genetic basis of multiple mitochondrial respiratory chain complex deficiencies. JAMA. 2014;312(1):68-77.
35. Haack TB, Hogarth P, Kruer MC, et al. Exome sequencing reveals de novo WDR45 mutations causing a phenotypically distinct, X-linked dominant form of NBIA. Am J Hum Genet. 2012;91(6):1144-1149.
36. Untergasser A, Cutcutache I, Koressaar T, et al. Primer3 - new capabilities and interfaces. Nucleic Acids Res. 2012;40(15):e115.
37. Raney BJ, Dreszer TR, Barber GP, et al. Track data hubs enable visualization of user-defined genome-wide annotations on the UCSC Genome Browser. Bioinformatics. 2014;30(7):1003-1005.
38. Inbal A, Avissar N, Shaklai M, et al. Myopathy, lactic acidosis, and sideroblastic anemia: a new syndrome. Am J Med Genet. 1995;55(3):372-378.
39. Fernandez-Vizarra E, Berardinelli A, Valente L, Tiranti V, Zeviani M. Nonsense mutation in pseudouridylate synthase 1 (PUS1) in two brothers affected by myopathy, lactic acidosis and sideroblastic anaemia (MLASA). J Med Genet. 2007;44(3):173-180.
40. Zeharia A, Fischel-Ghodsian N, Casas K, et al. Mitochondrial myopathy, sideroblastic anemia, and lactic acidosis: an autosomal recessive syndrome in Persian Jews caused by a mutation in the PUS1 gene. J Child Neurol. 2005;20(5):449-452.
41. Metodiev MD, Assouline Z, Landrieu P, et al. Unusual clinical expression and long survival of a pseudouridylate synthase (PUS1) mutation into adulthood. Eur J Hum Genet. 2015;23(6):880-882.
42. Cao M, Donà M, Valentino ML, et al. Clinical and molecular study in a long-surviving patient with MLASA syndrome due to novel PUS1 mutations. Neurogenetics. 2016;17(1):65-70.
43. Casas KA, Fischel-Ghodsian N. Mitochondrial myopathy and sideroblastic anemia. Am J Med Genet A. 2004;125A(2):201-204.
44. Larsson NG, Holme E, Kristiansson B, Oldfors A, Tulinius M. Progressive increase of the mutated mitochondrial DNA fraction in Kearns-Sayre syndrome. Pediatr Res. 1990;28(2):131-136.
45. Blakely EL, Alston CL, Lecky B, et al. Distal weakness with respiratory insufficiency caused by them.8344A > G"MERRF" mutation. Neuromuscul Disord. 2014;24(6):533-536.
46. Alston CL, Schaefer AM, Raman P, et al. Late-onset respiratory failure due to TK2 mutations causing multiple mtDNA deletions. Neurology. 2013;81(23):2051-2053.
47. Amornvit J, Pasutharnchat N, Pachinburavan M, Jongpiputvanich S, Joyjinda Y. Fulminant respiratory muscle paralysis, an expanding clinical spectrum of mitochondrial A3243G tRNALeu mutation. J Med Assoc Thai. 2014;97(4):467-472.
48. Pfeffer G, Povitz M, Gibson GJ, Chinnery PF. Diagnosis of muscle diseases presenting with early respiratory failure. J Neurol. 2015;262(5):1101-1114.
49. Bates MG, Bourke JP, Giordano C, d'Amati G, Turnbull DM, Taylor RW. Cardiac involvement in mitochondrial DNA disease: clinical spectrum, diagnosis, and management. Eur Heart J. 2012;33(24):3023-3033.
50. Castro MG, Huerta C, Reguero JR, et al. Mitochondrial DNA haplogroups in Spanish patients with hypertrophic cardiomyopathy. Int J Cardiol. 2006;112(2):202-206.
51. Hagen CM, Aidt FH, Hedley PL, et al. Mitochondrial haplogroups modify the risk of developing hypertrophic cardiomyopathy in a Danish population. PLoS One. 2013;8(8):e71904.