#125250
OPTIC ATROPHY WITH OR WITHOUT DEAFNESS, OPHTHALMOPLEGIA, MYOPATHY, ATAXIA, AND NEUROPATHY

Alternative titles; symbols
DOMINANT OPTIC ATROPHY PLUS SYNDROME; DOA+

Phenotype Gene Relationships
Location Phenotype Phenotype
MIM number
Gene/Locus Gene/Locus
MIM number
3q29 Optic atrophy with or without deafness, ophthalmoplegia, myopathy, ataxia, and neuropathy 125250 OPA1 605290


TEXT
A number sign (#) is used with this entry because this syndromic form of optic atrophy can be caused by heterozygous mutation in the OPA1 gene (605290).

See also optic atrophy-1 (OPA1; 165500), which is an allelic disorder without extraocular neurologic complications.

Description
Syndromic optic atrophy, also known as DOA+ syndrome, is a neurologic disorder characterized most commonly by an insidious onset of visual loss and sensorineural hearing loss in childhood with variable presentation of other clinical manifestations including progressive external ophthalmoplegia (PEO), muscle cramps, hyperreflexia, and ataxia. There appears to be a wide range of intermediate phenotypes (Yu-Wai-Man et al., 2010).

Clinical Features
Konigsmark et al. (1974, 1974) described an association of congenital deafness with late-onset, progressive optic atrophy which resulted in only mildly reduced visual acuity. Six persons in 4 generations were affected. No male-to-male transmission was noted. However, males and females were equally severely affected and a daughter of an affected male was not affected. Gernet (1964) reported the same disorder in mother and daughter.

In 23 members of 5 generations of a family, Treft et al. (1984) described a syndrome of early-onset optic atrophy and deafness. Some patients developed ophthalmoplegia, ptosis, ataxia, and nonspecific myopathy in middle age. The optic atrophy was progressive and associated with an abnormal electroretinogram without retinal pigment changes. The hearing loss was also progressive and sensorineural in type, usually becoming evident in the first or second decade of life. Many of the features suggested the Kearns-Sayre syndrome (530000), but the involvement of the son of the propositus, the only instance of male-to-male transmission, appeared to rule out a mitochondrial causation.

Shimizu et al. (2003) reported a Japanese patient with optic atrophy and moderate hearing loss in both ears.

Amati-Bonneau et al. (2005) found fragmentation of the mitochondrial network and defects in oxidative phosphorylation in skin fibroblasts from 5 patients with optic atrophy and deafness.

Hudson et al. (2008) reported 7 affected members from a family with optic atrophy, ataxia, and external ophthalmoplegia and variable presentation of hearing loss, myopathy, and neuropathy.

Ferraris et al. (2008) reported a 42-year-old man with PEO, loss of central vision, sensorineural deafness, and mild ataxia. Other features included macrocytic anemia and hypogonadism. Muscle biopsy showed mild variation in fiber size, atrophic fibers, and multiple mitochondrial DNA deletions. Although no ragged-red fibers were identified, several fibers were devoid of cytochrome-c oxidase activity.

Other Features
Verny et al. (2008) reported a patient with genetically-confirmed OPA1 who presented with a phenotype suggestive of multiple sclerosis (MS; 126200). He developed bilateral loss of visual acuity at age 43, followed by pain in the lower left limb and trigeminal neuralgia. Neurologic examination showed brisk tendon reflexes, spastic gait, and clonus in the left lower limb. MRI scan showed high intensity lesions in the cerebrum and spinal cord. Mitochondrial studies demonstrated severely impaired respiration and decreased ATP synthesis, which the authors postulated may have led to central demyelination in this patient.

Yu-Wai-Man et al. (2010) reported the results of a large multicenter study of 104 patients from 45 families with OPA1 mutations, including 60 new cases. Extraocular neurologic complications were common, and affected up to 20% of all mutation carriers. The most prominent manifestation after optic neuropathy (85.6%) was bilateral sensorineural deafness (62.5%) beginning in late childhood and early adulthood, followed by a combination of ataxia (29.8%), myopathy (35.6%), peripheral neuropathy (29.8%), and progressive external ophthalmoplegia (46.2%). These additional features became manifest from the third decade of life onwards. Spastic paraparesis was reported in 2 families, and a multiple sclerosis-like disorder was reported in 2 families, including the previously reported patient of Verny et al. (2008).

Molecular Genetics
In a Japanese patient with optic atrophy and moderate hearing loss, Shimizu et al. (2003) identified a heterozygous mutation in the OPA1 gene (R445H; 605290.0011).

Payne et al. (2004) identified the R445H mutation in the large Utah family with dominantly inherited optic atrophy, sensorineural hearing loss, ptosis, and ophthalmoplegia, originally described by Treft et al. (1984), and in an unrelated Belgian family with a similar phenotype, originally reported by Meire et al. (1985).

Li et al. (2005) identified the R445H mutation in another family with optic atrophy and hearing loss and noted that affected members of this family did not have extraocular motility abnormalities or ptosis, thus illustrating the intra- and interfamilial phenotype variability associated with this mutation.

Amati-Bonneau et al. (2005) identified the R445H mutation in 5 patients from 4 unrelated families with optic atrophy and deafness, thus confirming that this mutation is specifically associated with hearing loss. One of the patients had previously been reported by Amati-Bonneau et al. (2003). In the Spanish mother and daughter previously reported by Amati-Bonneau et al. (2005), Amati-Bonneau et al. (2008) noted that the mother also had myopathy, neuropathy, and progressive external ophthalmoplegia.

In a patient with sporadic occurrence of progressive external ophthalmoplegia (PEO), hearing loss, mild myopathy, and ataxia, Ferraris et al. (2008) identified a heterozygous mutation in the OPA1 gene (605290.0013).

Stewart et al. (2008) identified mutations in the OPA1 gene (605290.0011 and 605290.0014) in 3 (14.2%) of 21 probands with mitochondrial DNA deletions. The probands had optic atrophy, variable deafness, and myopathy. The findings confirmed the report by Ferraris et al. (2008) that OPA1 mutation may cause multiple mtDNA deletions and myopathy.

Hudson et al. (2008) identified a heterozygous mutation (605290.0015) in 7 affected members of a family with optic atrophy, ataxia, and external ophthalmoplegia and variable presentation of hearing loss, myopathy, and neuropathy. Yu-Wai-Man et al. (2010) identified the same heterozygous mutation in 3 affected members of an Austrian family with optic atrophy, ataxia, and external ophthalmoplegia with variable presentation of deafness and neuropathy and in French proband with optic atrophy, deafness, ataxia, myopathy, and neuropathy.

Amati-Bonneau et al. (2008) identified a heterozygous mutation (605290.0016) in an Italian father and daughter with optic atrophy and deafness. The father also had ataxia, myopathy, neuropathy, and PEO.

Genotype/Phenotype Correlations
Among 104 patients from 45 families with 33 different OPA1 mutations, Yu-Wai-Man et al. (2010) found that multisystem neurologic disease was associated with all types of mutations; however, there was an increased risk with missense mutations (odds ratio (OR) of 3.06; p = 0.0027) and with mutations located within the GTPase region (OR of 2.29; p = 0.0271). Skeletal muscle biopsies from those with extraocular neurologic features showed higher levels of cytochrome c oxidase-deficient fibers and mitochondrial DNA deletions compared to those with pure optic neuropathy, suggesting a causal role for these secondary mitochondrial DNA defects in disease pathophysiology.

REFERENCES
1. Amati-Bonneau, P., Guichet, A., Olichon, A., Chevrollier, A., Viala, F., Miot, S., Ayuso, C., Odent, S., Arrouet, C., Verny, C., Calmels, M.-N., Simard, G., Belenguer, P., Wang, J., Puel, J.-L., Hamel, C., Malthiery, Y., Bonneau, D., Lenaers, G., Reynier, P. OPA1 R445H mutation in optic atrophy associated with sensorineural deafness. Ann. Neurol. 58: 958-963, 2005. [PubMed: 16240368, related citations] [Full Text: John Wiley & Sons, Inc., Pubget]

2. Amati-Bonneau, P., Odent, S., Derrien, C., Pasquier, L., Malthiery, Y., Reynier, P., Bonneau, D. The association of autosomal dominant optic atrophy and moderate deafness may be due to the R445H mutation in the OPA1 gene. Am. J. Ophthal. 136: 1170-1171, 2003. [PubMed: 14644237, related citations] [Full Text: Elsevier Science, Pubget]

3. Amati-Bonneau, P., Valentino, M. L., Reynier, P., Gallardo, M. E., Bornstein, B., Boissiere, A., Campos, Y., Rivera, H., de la Aleja, J. G., Carroccia, R., Iommarini, L., Labauge, P., and 22 others. OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain 131: 338-351, 2008. [PubMed: 18158317, related citations] [Full Text: HighWire Press, Pubget]

4. Ferraris, S., Clark, S., Garelli, E., Davidzon, G., Moore, S. A., Kardon, R. H., Bienstock, R. J., Longley, M. J., Mancuso, M., Rios, P. G., Hirano, M., Copeland, W. C., DiMauro, S. Progressive external ophthalmoplegia and vision and hearing loss in a patient with mutations in POLG2 and OPA1. Arch. Neurol. 65: 125-131, 2008. [PubMed: 18195150, related citations] [Full Text: HighWire Press, Pubget]

5. Gernet, H. Hereditaere Opticusatrophie in Kombination mit Taubheit. Dtsch. Ophthal. Ges. 65: 545-547, 1964.

6. Hudson, G., Amati-Bonneau, P., Blakely, E. L., Stewart, J. D., He, L., Schaefer, A. M., Griffiths, P. G., Ahlqvist, K., Suomalainen, A., Reynier, P., McFarland, R., Turnbull, D. M., Chinnery, P. F., Taylor, R. W. Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness, and multiple mitochondrial deletions: a novel disorder of mtDNA maintenance. Brain 131: 329-337, 2008. [PubMed: 18065439, related citations] [Full Text: HighWire Press, Pubget]

7. Konigsmark, B. W., Knox, D. L., Hussels, I. E., Moses, H. Dominant congenital deafness and progressive optic nerve atrophy. Arch. Ophthal. 91: 99-103, 1974. [PubMed: 4544000, related citations] [Full Text: HighWire Press, Pubget]

8. Konigsmark, B. W., Knox, D. L., Hussels, I. E., Moses, H. Dominant congenital deafness and progressive optic atrophy: report of a family through four generations. Acta Genet. Med. Gemellol. 23: 377-379, 1974.

9. Li, C., Kosmorsky, G., Zhang, K., Katz, B. J., Ge, J., Traboulsi, E. I. Optic atrophy and sensorineural hearing loss in a family caused by an R445H OPA1 mutation. Am. J. Med. Genet. 138A: 208-211, 2005. [PubMed: 16158427, related citations] [Full Text: John Wiley & Sons, Inc., Pubget]

10. Meire, F., De Laey, J. J., de Bie, S., van Staey, M., Matton, M. T. Dominant optic nerve atrophy with progressive hearing loss and chronic progressive external ophthalmoplegia (CPEO). Ophthalmic Paediat. Genet. 5: 91-97, 1985. [PubMed: 4058877, related citations] [Full Text: Pubget]

11. Payne, M., Yang, Z., Katz, B. J., Warner, J. E. A., Weight, C. J., Zhao, Y., Pearson, E. D., Treft, R. L., Hillman, T., Kennedy, R. J., Meire, F. M., Zhang, K. Dominant optic atrophy, sensorineural hearing loss, ptosis, and ophthalmoplegia: a syndrome caused by a missense mutation in OPA1. Am. J. Ophthal. 138: 749-755, 2004. [PubMed: 15531309, related citations] [Full Text: Elsevier Science, Pubget]

12. Shimizu, S., Mori, N., Kishi, M., Sugata, H., Tsuda, A., Kubota, N. A novel mutation in the OPA1 gene in a Japanese patient with optic atrophy. Am. J. Ophthal. 135: 256-257, 2003. [PubMed: 12566046, related citations] [Full Text: Elsevier Science, Pubget]

13. Stewart, J. D., Hudson, G., Yu-Wai-Man, P., Blakeley, E. L., He, L., Horvath, R., Maddison, P., Wright, A., Griffiths, P. G., Turnbull, D. M., Taylor, R. W., Chinnery, P. F. OPA1 in multiple mitochondrial DNA deletion disorders. Neurology 71: 1829-1831, 2008. [PubMed: 19029523, related citations] [Full Text: HighWire Press, Pubget]

14. Treft, R. L., Sanborn, G. E., Carey, J., Swartz, M., Crisp, D., Wester, D. C., Creel, D. Dominant optic atrophy, deafness, ptosis, ophthalmoplegia, dystaxia, and myopathy: a new syndrome. Ophthalmology 91: 908-915, 1984. [PubMed: 6493699, related citations] [Full Text: Pubget]

15. Verny, C., Loiseau, D., Scherer, C., Lejeune, P., Chevrollier, A., Gueguen, N., Guillet, V., Dubas, F., Reynier, P., Amati-Bonneau, P., Bonneau, D. Multiple sclerosis-like disorder in OPA1-related autosomal dominant optic atrophy. Neurology 70: 1152-1153, 2008. [PubMed: 18287570, related citations] [Full Text: HighWire Press, Pubget]

16. Yu-Wai-Man, P., Griffiths, P. G., Gorman, G. S., Lourenco, C. M., Wright, A. F., Auer-Grumbach, M., Toscano, A., Musumeci, O., Valentino, M. L., Caporali, L., Lamperti, C., Tallaksen, C. M., and 24 others. Multi-system neurological disease is common in patients with OPA1 mutations. Brain 133: 771-786, 2010. [PubMed: 20157015, related citations] [Full Text: HighWire Press, Pubget]

Contributors: Cassandra L. Kniffin - updated : 5/19/2011
Cassandra L. Kniffin - updated : 3/16/2009
Cassandra L. Kniffin - updated : 1/7/2009
Cassandra L. Kniffin - updated : 3/9/2006
Creation Date: Victor A. McKusick : 6/4/1986
Edit History: wwang : 06/20/2011
wwang : 6/20/2011
ckniffin : 5/19/2011
terry : 10/13/2010
wwang : 3/25/2009
ckniffin : 3/16/2009
wwang : 1/9/2009
ckniffin : 1/7/2009
carol : 3/10/2006
ckniffin : 3/9/2006
mimadm : 6/25/1994
supermim : 3/16/1992
supermim : 3/20/1990
ddp : 10/26/1989
marie : 3/25/1988
reenie : 10/17/1986