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Erschienen in: Orphanet Journal of Rare Diseases 1/2013

Open Access 01.12.2013 | Research

Phenotypic variability in ARCA2 and identification of a core ataxic phenotype with slow progression

verfasst von: Cyril Mignot, Emmanuelle Apartis, Alexandra Durr, Charles Marques Lourenço, Perrine Charles, David Devos, Caroline Moreau, Pascale de Lonlay, Nathalie Drouot, Lydie Burglen, Nadine Kempf, Elsa Nourisson, Sandra Chantot-Bastaraud, Anne-Sophie Lebre, Marlène Rio, Yves Chaix, Eric Bieth, Emmanuel Roze, Isabelle Bonnet, Sandrine Canaple, Coralie Rastel, Alexis Brice, Agnès Rötig, Isabelle Desguerre, Christine Tranchant, Michel Koenig, Mathieu Anheim

Erschienen in: Orphanet Journal of Rare Diseases | Ausgabe 1/2013

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Abstract

Autosomal recessive cerebellar ataxia 2 (ARCA2) is a recently identified recessive ataxia due to ubiquinone deficiency and biallelic mutations in the ADCK3 gene. The phenotype of the twenty-one patients reported worldwide varies greatly. Thus, it is difficult to decide which ataxic patients are good candidates for ADCK3 screening without evidence of ubiquinone deficiency. We report here the clinical and molecular data of 10 newly diagnosed patients from seven families and update the disease history of four additional patients reported in previous articles to delineate the clinical spectrum of ARCA2 phenotype and to provide a guide to the molecular diagnosis. First signs occurred before adulthood in all 14 patients. Cerebellar atrophy appeared in all instances. The progressivity and severity of ataxia varied greatly, but no patients had the typical inexorable ataxic course that characterizes other childhood-onset recessive ataxias. The ataxia was frequently associated with other neurological signs. Importantly, stroke-like episodes contributed to significant deterioration of the neurological status in two patients. Ubidecarenone therapy markedly improved the movement disorders, including ataxia, in two other patients. The 7 novel ADCK3 mutations found in the 10 new patients were two missense and five truncating mutations. There was no apparent correlation between the genotype and the phenotype. Our series reveals that the clinical spectrum of ARCA2 encompasses a range of ataxic phenotypes. On one end, it may manifest as a pure ataxia with very slow progressivity and, on the other end, as a severe infantile encephalopathy with cerebellar atrophy. The phenotype of most patients, however, lies in between. It is characterized by a very slowly progressive or apparently stable ataxia associated with other signs of central nervous system involvement. We suggest undergoing the molecular analysis of ADCK3 in patients with this phenotype and in those with cerebellar atrophy and a stroke-like episode. The diagnosis of patients with a severe ARCA2 phenotype may also be performed on the basis of biological data, i.e. low ubiquinone level or functional evidence of ubiquinone deficiency. This diagnosis is crucial since the neurological status of some patients may be improved by ubiquinone therapy.
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Literatur
1.
Zurück zum Zitat Anheim M, Tranchant C, Koenig M: The autosomal recessive cerebellar ataxias. N Engl J Med. 2012, 366: 636-646. 10.1056/NEJMra1006610.PubMedCrossRef Anheim M, Tranchant C, Koenig M: The autosomal recessive cerebellar ataxias. N Engl J Med. 2012, 366: 636-646. 10.1056/NEJMra1006610.PubMedCrossRef
2.
Zurück zum Zitat Gerards M, van den Bosch B, Calis C, Schoonderwoerd K, Van Engelen K, Tijssen M, et al: Nonsense mutations in CABC1/ADCK3 cause progressive cerebellar ataxia and atrophy. Mitochondrion. 2010, 10: 510-515. 10.1016/j.mito.2010.05.008.PubMedCrossRef Gerards M, van den Bosch B, Calis C, Schoonderwoerd K, Van Engelen K, Tijssen M, et al: Nonsense mutations in CABC1/ADCK3 cause progressive cerebellar ataxia and atrophy. Mitochondrion. 2010, 10: 510-515. 10.1016/j.mito.2010.05.008.PubMedCrossRef
3.
Zurück zum Zitat Horvath R, Czermin B, Gulati S, Demuth S, Houge G, Pyle A, et al: Adult-onset cerebellar ataxia due to mutations in CABC1/ADCK3. J Neurol Neurosurg Psychiatry. 2011, 83: 174-178.PubMedCrossRef Horvath R, Czermin B, Gulati S, Demuth S, Houge G, Pyle A, et al: Adult-onset cerebellar ataxia due to mutations in CABC1/ADCK3. J Neurol Neurosurg Psychiatry. 2011, 83: 174-178.PubMedCrossRef
4.
Zurück zum Zitat Lagier-Tourenne C, Tazir M, Lopez LC, Quinzii CM, Assoum M, Drouot N, et al: ADCK3, an ancestral kinase, is mutated in a form of recessive ataxia associated with coenzyme Q10 deficiency. Am J Hum Genet. 2008, 82: 661-672. 10.1016/j.ajhg.2007.12.024.PubMedCentralPubMedCrossRef Lagier-Tourenne C, Tazir M, Lopez LC, Quinzii CM, Assoum M, Drouot N, et al: ADCK3, an ancestral kinase, is mutated in a form of recessive ataxia associated with coenzyme Q10 deficiency. Am J Hum Genet. 2008, 82: 661-672. 10.1016/j.ajhg.2007.12.024.PubMedCentralPubMedCrossRef
5.
Zurück zum Zitat Mollet J, Delahodde A, Serre V, Chretien D, Schlemmer D, Lombes A, et al: CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures. Am J Hum Genet. 2008, 82: 623-630. 10.1016/j.ajhg.2007.12.022.PubMedCentralPubMedCrossRef Mollet J, Delahodde A, Serre V, Chretien D, Schlemmer D, Lombes A, et al: CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures. Am J Hum Genet. 2008, 82: 623-630. 10.1016/j.ajhg.2007.12.022.PubMedCentralPubMedCrossRef
6.
Zurück zum Zitat Terracciano A, Renaldo F, Zanni G, D’Amico A, Pastore A, Barresi S, et al: The use of muscle biopsy in the diagnosis of undefined ataxia with cerebellar atrophy in children. Eur J Paediatr Neurol. 2012, 16: 248-256. 10.1016/j.ejpn.2011.07.016.PubMedCrossRef Terracciano A, Renaldo F, Zanni G, D’Amico A, Pastore A, Barresi S, et al: The use of muscle biopsy in the diagnosis of undefined ataxia with cerebellar atrophy in children. Eur J Paediatr Neurol. 2012, 16: 248-256. 10.1016/j.ejpn.2011.07.016.PubMedCrossRef
7.
Zurück zum Zitat Auré K, Benoist JF, Ogier DeBaulny H, Romero NB, Rigal O, Lombes A: Progression despite replacement of a myopathic form of coenzyme Q10 defect. Neurology. 2004, 63: 727-729. 10.1212/01.WNL.0000134607.76780.B2.PubMedCrossRef Auré K, Benoist JF, Ogier DeBaulny H, Romero NB, Rigal O, Lombes A: Progression despite replacement of a myopathic form of coenzyme Q10 defect. Neurology. 2004, 63: 727-729. 10.1212/01.WNL.0000134607.76780.B2.PubMedCrossRef
8.
Zurück zum Zitat Anheim M, Fleury M, Monga B, Laugel V, Chaigne D, Rodier G, et al: Epidemiological, clinical, paraclinical and molecular study of a cohort of 102 patients affected with autosomal recessive progressive cerebellar ataxia from Alsace, Eastern France: implications for clinical management. Neurogenetics. 2010, 11: 1-12. 10.1007/s10048-009-0196-y.PubMedCrossRef Anheim M, Fleury M, Monga B, Laugel V, Chaigne D, Rodier G, et al: Epidemiological, clinical, paraclinical and molecular study of a cohort of 102 patients affected with autosomal recessive progressive cerebellar ataxia from Alsace, Eastern France: implications for clinical management. Neurogenetics. 2010, 11: 1-12. 10.1007/s10048-009-0196-y.PubMedCrossRef
9.
Zurück zum Zitat Anheim M, Monga B, Fleury M, Charles P, Barbot C, Salih M, et al: Ataxia with oculomotor apraxia type 2: clinical, biological and genotype/phenotype correlation study of a cohort of 90 patients. Brain. 2009, 132: 2688-2698. 10.1093/brain/awp211.PubMedCrossRef Anheim M, Monga B, Fleury M, Charles P, Barbot C, Salih M, et al: Ataxia with oculomotor apraxia type 2: clinical, biological and genotype/phenotype correlation study of a cohort of 90 patients. Brain. 2009, 132: 2688-2698. 10.1093/brain/awp211.PubMedCrossRef
10.
Zurück zum Zitat Schmitz-Hubsch T, Du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al: Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006, 66: 1717-1720. 10.1212/01.wnl.0000219042.60538.92.PubMedCrossRef Schmitz-Hubsch T, Du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, et al: Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology. 2006, 66: 1717-1720. 10.1212/01.wnl.0000219042.60538.92.PubMedCrossRef
11.
Zurück zum Zitat Marelli C, Figoni J, Charles P, Anheim M, Tchikviladze M, Vincitorio CM, et al: Annual change in Friedreich’s ataxia evaluated by the Scale for the Assessment and Rating of Ataxia (SARA) is independent of disease severity. Mov Disord. 2011, 27: 135-138.PubMedCrossRef Marelli C, Figoni J, Charles P, Anheim M, Tchikviladze M, Vincitorio CM, et al: Annual change in Friedreich’s ataxia evaluated by the Scale for the Assessment and Rating of Ataxia (SARA) is independent of disease severity. Mov Disord. 2011, 27: 135-138.PubMedCrossRef
12.
Zurück zum Zitat Anheim M, Fleury MC, Franques J, Moreira MC, Delaunoy JP, Stoppa-Lyonnet D, et al: Clinical and molecular findings of ataxia with oculomotor apraxia type 2 in 4 families. Arch Neurol. 2008, 65: 958-962. 10.1001/archneur.65.7.958.PubMed Anheim M, Fleury MC, Franques J, Moreira MC, Delaunoy JP, Stoppa-Lyonnet D, et al: Clinical and molecular findings of ataxia with oculomotor apraxia type 2 in 4 families. Arch Neurol. 2008, 65: 958-962. 10.1001/archneur.65.7.958.PubMed
13.
Zurück zum Zitat Tezenas DuMontcel S, Charles P, Goizet C, Marelli C, Ribai P, Vincitorio C, et al: Factors influencing disease progression in autosomal dominant cerebellar ataxia and spastic paraplegia. Arch Neurol. 2012, 69: 500-508. 10.1001/archneurol.2011.2713.CrossRef Tezenas DuMontcel S, Charles P, Goizet C, Marelli C, Ribai P, Vincitorio C, et al: Factors influencing disease progression in autosomal dominant cerebellar ataxia and spastic paraplegia. Arch Neurol. 2012, 69: 500-508. 10.1001/archneurol.2011.2713.CrossRef
14.
Zurück zum Zitat Diomedi-Camassei F, Di Giandomenico S, Santorelli FM, Caridi G, Piemonte F, Montini G, et al: COQ2 nephropathy: a newly described inherited mitochondriopathy with primary renal involvement. J Am Soc Nephrol. 2007, 18: 2773-2780. 10.1681/ASN.2006080833.PubMedCrossRef Diomedi-Camassei F, Di Giandomenico S, Santorelli FM, Caridi G, Piemonte F, Montini G, et al: COQ2 nephropathy: a newly described inherited mitochondriopathy with primary renal involvement. J Am Soc Nephrol. 2007, 18: 2773-2780. 10.1681/ASN.2006080833.PubMedCrossRef
15.
Zurück zum Zitat Tzoulis C, Bindoff LA: Acute mitochondrial encephalopathy reflects neuronal energy failure irrespective of which genome the genetic defect affects. Brain. 2012, 135: 3627-3634. 10.1093/brain/aws223.PubMedCrossRef Tzoulis C, Bindoff LA: Acute mitochondrial encephalopathy reflects neuronal energy failure irrespective of which genome the genetic defect affects. Brain. 2012, 135: 3627-3634. 10.1093/brain/aws223.PubMedCrossRef
16.
Zurück zum Zitat De Siqueira LF: Progressive myoclonic epilepsies: review of clinical, molecular and therapeutic aspects. J Neurol. 2010, 257: 1612-1619. 10.1007/s00415-010-5641-1.PubMedCrossRef De Siqueira LF: Progressive myoclonic epilepsies: review of clinical, molecular and therapeutic aspects. J Neurol. 2010, 257: 1612-1619. 10.1007/s00415-010-5641-1.PubMedCrossRef
17.
Zurück zum Zitat Kälviäinen R, Khyuppenen J, Koskenkorva P, Eriksson K, Vanninen R, Mervaala E: Clinical picture of EPM1-Unverricht-Lundborg disease. Epilepsia. 2008, 49: 549-556. 10.1111/j.1528-1167.2008.01546.x.PubMedCrossRef Kälviäinen R, Khyuppenen J, Koskenkorva P, Eriksson K, Vanninen R, Mervaala E: Clinical picture of EPM1-Unverricht-Lundborg disease. Epilepsia. 2008, 49: 549-556. 10.1111/j.1528-1167.2008.01546.x.PubMedCrossRef
18.
Zurück zum Zitat Hoischen A, Gilissen C, Arts P, Wieskamp N, van der Vliet W, Vermeer S, et al: Massively parallel sequencing of ataxia genes after array-based enrichment. Hum Mutat. 2010, 31: 494-499. 10.1002/humu.21221.PubMedCrossRef Hoischen A, Gilissen C, Arts P, Wieskamp N, van der Vliet W, Vermeer S, et al: Massively parallel sequencing of ataxia genes after array-based enrichment. Hum Mutat. 2010, 31: 494-499. 10.1002/humu.21221.PubMedCrossRef
19.
Zurück zum Zitat Ku CS, Cooper DN, Polychronakos C, Naidoo N, Wu M, Soong R: Exome sequencing: dual role as a discovery and diagnostic tool. Ann Neurol. 2012, 71: 5-14. 10.1002/ana.22647.PubMedCrossRef Ku CS, Cooper DN, Polychronakos C, Naidoo N, Wu M, Soong R: Exome sequencing: dual role as a discovery and diagnostic tool. Ann Neurol. 2012, 71: 5-14. 10.1002/ana.22647.PubMedCrossRef
20.
Metadaten
Titel
Phenotypic variability in ARCA2 and identification of a core ataxic phenotype with slow progression
verfasst von
Cyril Mignot
Emmanuelle Apartis
Alexandra Durr
Charles Marques Lourenço
Perrine Charles
David Devos
Caroline Moreau
Pascale de Lonlay
Nathalie Drouot
Lydie Burglen
Nadine Kempf
Elsa Nourisson
Sandra Chantot-Bastaraud
Anne-Sophie Lebre
Marlène Rio
Yves Chaix
Eric Bieth
Emmanuel Roze
Isabelle Bonnet
Sandrine Canaple
Coralie Rastel
Alexis Brice
Agnès Rötig
Isabelle Desguerre
Christine Tranchant
Michel Koenig
Mathieu Anheim
Publikationsdatum
01.12.2013
Verlag
BioMed Central
Erschienen in
Orphanet Journal of Rare Diseases / Ausgabe 1/2013
Elektronische ISSN: 1750-1172
DOI
https://doi.org/10.1186/1750-1172-8-173

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Reviewer Acknowledgement

Reviewer acknowledgement 2013