Syndromic parkinsonism and dementia associated with OPA1 missense mutations

Annals of Neurology

Volumn 78, Issue 1, 2015, Pages 21-38

  Carelli, Valerio ^a   Musumeci, Olimpia ^b   Caporali, Leonardo ^a   Zanna, Claudia ^a   La Morgia, Chiara ^a   Del Dotto, Valentina ^c   Porcelli, Anna Maria ^c   Rugolo, Michela ^c   Valentino, Maria Lucia ^a   Iommarini, Luisa ^c   Maresca, Alessandra ^a   Barboni, Piero ^d   Carbonelli, Michele ^d   Trombetta, Costantino ^b   Valente, Enza Maria ^e   Patergnani, Simone ^f   Giorgi, Carlotta ^f   Pinton, Paolo ^f   Rizzo, Giovanni ^a   Tonon, Caterina ^a   Lodi, Raffaele ^a   Avoni, Patrizia ^a   Liguori, Rocco ^a   Baruzzi, Agostino ^a   Toscano, Antonio ^b   Zeviani, Massimo ^g   more..

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF MESSINA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d Studio Oculistico   (Italy)

^e CASA SOLLIEVO DELLA SOFFERENZA HOSPITAL   (Italy)

^f UNIVERSITY OF FERRARA   (Italy)

^g MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CYTOCHROME C OXIDASE; GUANOSINE TRIPHOSPHATASE; MESSENGER RNA; MITOCHONDRIAL DNA; OPA1 PROTEIN, HUMAN;

AEROBIC METABOLISM; AGED; ARTICLE; AUTOPHAGY; BIOENERGY; CASE REPORT; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; COGNITIVE DEFECT; CONTROLLED STUDY; DEMENTIA; GENE; GENE DELETION; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC SCREENING; HETEROZYGOSITY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; ITALIAN (CITIZEN); MALE; MFN2 GENE; MISSENSE MUTATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MYOPATHY; MITOPHAGY; MUSCLE BIOPSY; NERVE DEGENERATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPA1 GENE; OPTICAL COHERENCE TOMOGRAPHY; PARKINSONISM; PATHOGENESIS; PERCEPTION DEAFNESS; PRIORITY JOURNAL; PROTEIN DOMAIN; RETINA NERVE CELL; SKIN FIBROBLAST; COMPLICATION; FEMALE; GENETIC PREDISPOSITION; GENETICS; ITALY; PEDIGREE;

AGED; DEMENTIA; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GTP PHOSPHOHYDROLASES; HUMANS; ITALY; MALE; MUTATION, MISSENSE; OPHTHALMOPLEGIA, CHRONIC PROGRESSIVE EXTERNAL; PARKINSONIAN DISORDERS; PEDIGREE;

EID: 84933178508     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.24410     Document Type: Article

References (53)

1. Zeviani M, Servidei S, Gellera C, et al., An autosomal dominant disorder with multiple deletions of mitochondrial DNA starting at the D-loop region. Nature 1989; 339: 309-311.
2. Spinazzola A, Zeviani M., Disorders of nuclear-mitochondrial intergenomic communication. Biosci Rep 2007; 27: 39-51.
3. Van Goethem G, Dermaut B, Lofgren A, et al. Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat Genet 2001; 28: 211-212.
4. Longley MJ, Clark S, Yu Wai Man C, et al., Mutant POLG2 disrupts DNA polymerase gamma subunits and causes progressive external ophthalmoplegia. Am J Hum Genet 2006; 78: 1026-1034.
5. Spelbrink JN, Li FY, Tiranti V, et al., Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat Genet 2001; 28: 223-231.
6. Ronchi D, Di Fonzo A, Lin W, et al., Mutations in DNA2 link progressive myopathy to mitochondrial DNA instability. Am J Hum Genet 2013; 92: 293-300.
7. Kaukonen J, Juselius JK, Tiranti V, et al., Role of adenine nucleotide translocator 1 in mtDNA maintenance. Science 2000; 289: 782-785.
8. Nishino I, Spinazzola A, Hirano M., Thymidine phosphorylase gene mutations in MNGIE, a human mitochondrial disorder. Science 1999; 283: 689-692.
9. Tyynismaa H, Sun R, Ahola-Erkkilä S, et al., Thymidine kinase 2 mutations in autosomal recessive progressive external ophthalmoplegia with multiple mitochondrial DNA deletions. Hum Mol Genet 2012; 21: 66-75.
10. Tyynismaa H, Ylikallio E, Patel M, et al., A heterozygous truncating mutation in RRM2B causes autosomal-dominant progressive external ophthalmoplegia with multiple mtDNA deletions. Am J Hum Genet 2009; 85: 290-295.
11. Ronchi D, Garone C, Bordoni A, et al., Next-generation sequencing reveals DGUOK mutations in adult patients with mitochondrial DNA multiple deletions. Brain 2012; 135: 3404-3415.
12. Garone C, Rubio JC, Calvo SE, et al., MPV17 mutations causing adult-onset multisystemic disorder with multiple mitochondrial DNA deletions. Arch Neurol 2012; 69: 1648-1651.
13. Luoma P, Melberg A, Rinne JO, et al., Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study. Lancet 2004; 364: 875-882.
14. Baloh RH, Salavaggione E, Milbrandt J, Pestronk A., Familial parkinsonism and ophthalmoplegia from a mutation in the mitochondrial DNA helicase twinkle. Arch Neurol 2007; 64: 998-1000.
15. Bender A, Krishnan KJ, Morris CM, et al., High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat Genet 2006; 38: 515-517.
16. Hudson G, Amati-Bonneau P, Blakely EL, et al., Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: a novel disorder of mtDNA maintenance. Brain 2008; 131: 329-337.
17. Amati-Bonneau P, Valentino ML, Reynier P, et al., OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 2008; 131: 338-351.
18. Alexander C, Votruba M, Pesch UE, et al., OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 2000; 26: 211-215.
19. Delettre C, Lenaers G, Griffoin JM, et al., Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 2000; 26: 207-210.
20. Ferré M, Amati-Bonneau P, Tourmen Y, et al., eOPA1: an online database for OPA1 mutations. Hum Mutat 2005; 25: 423-428.
21. Yu-Wai-Man P, Griffiths PG, Gorman GS, et al., Multi-system neurological disease is common in patients with OPA1 mutations. Brain 2010; 133: 771-786.
22. Maresca A, la Morgia C, Caporali L, et al., The optic nerve: a »mito-window« on mitochondrial neurodegeneration. Mol Cell Neurosci 2013; 55: 62-76.
23. Elachouri G, Vidoni S, Zanna C, et al., OPA1 links human mitochondrial genome maintenance to mtDNA replication and distribution. Genome Res 2011; 21: 12-20.
24. Rouzier C, Bannwarth S, Chaussenot A, et al., The MFN2 gene is responsible for mitochondrial DNA instability and optic atrophy 'plus' phenotype. Brain 2012; 135: 23-34.
25. Savini G, Carbonelli M, Barboni P., Retinal nerve fiber layer thickness measurement by Fourier-domain optical coherence tomography: a comparison between cirrus-HD OCT and RTVue in healthy eyes. J Glaucoma 2010; 19: 369-372.
26. La Morgia C, Achilli A, Iommarini L, et al., Rare mtDNA variants in Leber hereditary optic neuropathy families with recurrence of myoclonus. Neurology 2008; 70: 762-770.
27. Ratiney H, Sdika M, Coenradie Y, et al., Time-domain semi-parametric estimation based on a metabolite basis set. NMR Biomed 2005; 18: 1-13.
28. Lodi R, Tonon C, Valentino ML, et al., Defective mitochondrial ATP production in skeletal muscle from patients with dominant optic atrophy due to OPA1 mutations. Arch Neurol 2011; 68: 67-73.
29. Valente EM, Abou-Sleiman PM, Caputo V, et al., Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004; 304: 1158-1160.
30. Kitada T, Asakawa S, Hattori N, et al., Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998; 392: 605-608.
31. Zanna C, Ghelli A, Porcelli AM, et al., OPA1 mutations associated with dominant optic atrophy impair oxidative phosphorylation and mitochondrial fusion. Brain 2008; 131: 352-367.
32. Pesch UE, Leo-Kottler B, Mayer S, et al., OPA1 mutations in patients with autosomal dominant optic atrophy and evidence for semi-dominant inheritance. Hum Mol Genet 2001; 10: 1359-1368.
33. Trounce IA, Kim YL, Jun AS, Wallace DC., Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 1996; 264: 484-509.
34. Porcelli AM, Angelin A, Ghelli A, et al., Respiratory complex I dysfunction due to mitochondrial DNA mutations shifts the voltage threshold for opening of the permeability transition pore toward resting levels. J Biol Chem 2009; 284: 2045-2052.
35. Robinson BH, Petrova-Benedict R, Buncic JR, Wallace DC., Nonviability of cells with oxidative defects in galactose medium: a screening test for affected patient fibroblasts. Biochem Med Metab Biol 1992; 48: 122-126.
36. Patergnani S, Marchi S, Rimessi A, et al., PRKCB/protein kinase C, beta and the mitochondrial axis as key regulators of autophagy. Autophagy 2013; 9: 1367-1385.
37. Klionsky DJ, Abdalla FC, Abeliovich H, et al., Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
38. Patergnani S, Pinton P., Mitophagy and mitochondrial balance. Methods Mol Biol 2015; 1241: 181-194.
39. Milone M, Younge BR, Wang J, et al., Mitochondrial disorder with OPA1 mutation lacking optic atrophy. Mitochondrion 2009; 9: 279-281.
40. Suomalainen A, Majander A, Haltia M, et al., Multiple deletions of mitochondrial DNA in several tissues of a patient with severe retarded depression and familial progressive external ophthalmoplegia. J Clin Invest 1992; 90: 61-66.
41. Austin SA, Vriesendorp FJ, Thandroyen FT, et al., Expanding the phenotype of the 8344 transfer RNAlysine mitochondrial DNA mutation. Neurology 1998; 51: 1447-1450.
42. Mancuso M, Ricci G, Choub A, et al., Autosomal dominant psychiatric disorders and mitochondrial DNA multiple deletions: report of a family. J Affect Disord 2008; 106: 173-177.
43. Hannah-Shmouni F, Sirrs S, Mezei MM, et al., Increased prevalence of hypertension in young adults with high heteroplasmy levels of the MELAS m.3243A>G mutation. JIMD Rep 2014; 12: 17-23.
44. Agier V, Oliviero P, Lainé J, et al., Defective mitochondrial fusion, altered respiratory function, and distorted cristae structure in skin fibroblasts with heterozygous OPA1 mutations. Biochim Biophys Acta 2012; 1822: 1570-1580.
45. Ashrafi G, Schwarz TL., The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ 2013; 20: 31-42.
46. Suen DF, Narendra DP, Tanaka A, et al., Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proc Natl Acad Sci U S A 2010; 107: 11835-11840.
47. White KE, Davies VJ, Hogan VE, et al., OPA1 deficiency associated with increased autophagy in retinal ganglion cells in a murine model of dominant optic atrophy. Invest Ophthalmol Vis Sci 2009; 50: 2567-2571.
48. Sarzi E, Angebault C, Seveno M, et al., The human OPA1delTTAG mutation induces premature age-related systemic neurodegeneration in mouse. Brain 2012; 135: 3599-3613.
49. Narendra D, Walker JE, Youle R., Mitochondrial quality control mediated by PINK1 and Parkin: links to parkinsonism. Cold Spring Harb Perspect Biol 2012; 4.
50. Corti O, Brice A., Mitochondrial quality control turns out to be the principal suspect in parkin and PINK1-related autosomal recessive Parkinson's disease. Curr Opin Neurobiol 2013; 23: 100-108.
51. Marongiu R, Ferraris A, Ialongo T, et al., PINK1 heterozygous rare variants: prevalence, significance and phenotypic spectrum. Hum Mutat 2008; 29: 565.
52. Müller-Rischart AK, Pilsl A, Beaudette P, et al., The E3 ligase parkin maintains mitochondrial integrity by increasing linear ubiquitination of NEMO. Mol Cell 2013; 49: 908-921.
53. Lutz AK, Exner N, Fett ME, et al., Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J Biol Chem 2009; 284: 22938-22951.