#254130
MIYOSHI MUSCULAR DYSTROPHY 1; MMD1

Alternative titles; symbols
MIYOSHI MYOPATHY
MUSCULAR DYSTROPHY, DISTAL, LATE-ONSET, AUTOSOMAL RECESSIVE

Phenotype Gene Relationships
Location Phenotype Phenotype
MIM number
Gene/Locus Gene/Locus
MIM number
2p13.2 Miyoshi muscular dystrophy 1 254130 DYSF 603009


TEXT
A number sign (#) is used with this entry because Miyoshi muscular dystrophy-1 (MMD1) is caused by homozygous mutation in the gene encoding dysferlin (DYSF; 603009) on chromosome 2p13.

A form of limb-girdle muscular dystrophy (LGMD2B; 253601) is also caused by mutation in the dysferlin gene.

See also Welander myopathy (604454), an autosomal dominant form of late-onset distal myopathy.

Miyoshi muscular dystrophy is a genetically heterogeneous disorder: MMD2 (613318) has been mapped to chromosome 10p, and MMD3 (613319) is caused by mutation in the ANO5 gene (608662) on chromosome 11p14.

Clinical Features
Miyoshi et al. (1967) reported 4 patients from 2 Japanese families with distal myopathy inherited in an autosomal recessive pattern. Sasaki et al. (1969) and Ideta et al. (1973) each reported 4 affected patients. Kuhn and Schroder (1981) reported 2 affected Caucasian brothers born of consanguineous parents. They had early-adult onset in the distal leg muscles and elevated creatine kinase.

Miyoshi et al. (1986) described in detail 17 cases from 8 families including an autopsy case. Consanguinity was found in 7 of the 8 families and in 2 families there was pseudodominance, i.e., affected father and children. Eighty percent of the cases had onset between 16 and 20 years with long survival. Serum CK activity was markedly elevated in all except 1 patient, aged 56 years; CK was mildly elevated in preclinical stages. The pattern of muscle involvement was distinctive; the muscles of the lower legs and forearms were involved, whereas the small muscles of the feet and hands were relatively spared. Skilled movements of the fingers were not disturbed, but grip strength was decreased early in the disease. No lesions were detected in the brain, spinal cord, or peripheral nerves. Miyoshi et al. (1986) noted that the disorder could be distinguished from Welander myopathy, which shows atrophy of small muscles of the hands and extensor muscles of the legs with inability to stand on the heels but ability to stand on tip-toes, whereas in Miyoshi myopathy, impaired toe-standing was an early symptom and heel-standing was normal.

Isaacs et al. (1988) described 5 patients with autosomal recessive distal myopathy of late onset; 3 of the patients belonged to a single sibship. One of the cases resembled the Nonaka form (605820). The authors concluded that autosomal recessive distal myopathy can occur in different ethnic groups.

Yamanouchi et al. (1994) examined 19 muscle biopsies from 14 patients with autosomal recessive distal muscular dystrophy. The histologic features were similar to those of Duchenne muscular dystrophy (DMD; 310200) with active muscle fiber necrosis and regeneration, as well as disorganization of the intermyofibrillar network. In half of the patients, small angular fibers and scattered rimmed vacuoles were found. However, dystrophin (300377) and utrophin (128240) were expressed normally, even in severely affected gastrocnemius muscles.

In a large, inbred, aboriginal Canadian kindred with 9 muscular dystrophy patients, Weiler et al. (1996) found that the ancestry of all but 2 of the carrier parents could be traced to a founder couple 7 generations earlier. Seven patients presented with proximal myopathy consistent with limb-girdle muscular dystrophy, whereas 2 patients manifested predominantly distal wasting and weakness consistent with Miyoshi myopathy. Age at onset of symptoms, degree of creatine kinase elevation, and muscle histology were similar in both phenotypes. Segregation of LGMD/MD was consistent with autosomal recessive inheritance.

Rowin et al. (1999) described 2 patients with a clinical diagnosis of Miyoshi myopathy who demonstrated marked inflammatory changes on muscle biopsy of clinically less affected muscles. The findings illustrated the importance of recognizing the marked variability in histopathology of Miyoshi myopathy, which may include an inflammatory infiltrate on muscle biopsy, mimicking the histopathologic picture of an inflammatory myopathy. One patient was a 25-year-old Pakistani man, born of consanguineous parents, with a 1.5-year history of progressive atrophy of both calves associated with 'limping.' He denied involvement of the upper extremities. The second patient was a 29-year-old woman who had had progressive difficulty in walking, particularly in high-heeled shoes, beginning at the age of 18 and progressing to include difficulty walking up stairs and stumbling over her feet.

Ro et al. (2004) reported 4 Chinese patients from 2 unrelated families living in Taiwan with MM confirmed by molecular identification of mutations in the dysferlin gene. Three sibs in 1 family experienced difficulty in toe walking beginning at ages 17 to 18 years. In the following 2 to 5 years, all had difficulty in climbing stairs and rising from a squatting position accompanied by moderate to severe weakness in the gastrocnemius and soleus muscles and mild weakness in the hamstring and quadriceps muscles. The tibialis anterior muscle was relatively spared. Two patients had muscle wasting and weakness in the lower legs. Reflexes were decreased or absent in the ankles. CK was elevated and muscle biopsies showed dystrophic patterns with decreased or absent dysferlin staining. MRI showed a mild to moderate increase of signal intensity in the affected muscles of the lower legs, reflecting fatty infiltration. The 1 patient from the other family had a similar clinical course and MRI findings.

Illa et al. (2007) reported 2 sibs with Miyoshi myopathy due to a homozygous mutation in the DYSF gene (G519R; 603009.0015). Age at onset was 18 and 15 years, respectively, of distal weakness of the lower limbs with progression to proximal muscle involvement and later upper limb involvement. Both were wheelchair-bound in their thirties. The patients' father, who was heterozygous for the G519R mutation, developed calf myalgias and mild progressive difficulties in walking at age 65 years. He had moderately increased serum creatine kinase and decreased dysferlin immunostaining on muscle biopsy, although DYSF mRNA levels were normal. The findings indicated that heterozygous DYSF mutation carriers may develop late-onset milder manifestations of the disorder.

Spuler et al. (2008) reported 2 sibs with Miyoshi myopathy caused by mutation in the DYSF gene (G299W; 603009.0018). Skeletal muscle biopsy of 1 showed amyloid fibrils on skeletal muscle biopsy. Amyloid was located in the sarcolemma of muscle cells as well as in blood vessel walls and interstitium. Spuler et al. (2008) postulated that the mutation destabilized the protein structure of dysferlin and increased the propensity to form amyloid fibrils.

Diagnosis
Cacciottolo et al. (2011) found that all of 55 patients with an undetermined LGMD clinical phenotype and 10 patients with a Miyoshi myopathy phenotype who had less than 20% dysferlin on skeletal muscle biopsy determined by Western blot analysis had pathogenic mutations in the DYSF gene. Exhaustive mutation analysis was performed, including genomic DNA sequencing, mRNA analysis, array CGH, and PCR. Sixty-five different mutations were identified throughout the gene and there were no mutation hotspots. Cacciottolo et al. (2011) noted the difficulty of sequencing the DYSF gene because of its larger size, and concluded that protein analysis showing a dysferlin reduction to 20% of normal values in skeletal muscle or in peripheral blood monocytes can be used to identify LGMD2B/MMD1 caused by DYSF mutations with 100% accuracy.

Mapping
Bejaoui et al. (1995) identified a putative Miyoshi myopathy disease locus on chromosome 2p14-p12 (lod score of 15.3 at marker D2S291) by a study of 12 families with MM. Five of the families were consanguineous.

Weiler et al. (1996) linked a Canadian family in which some members had features of limb-girdle muscular dystrophy and others had features of distal myopathy to 2p (lod score greater than 3.0). The putative region included the LGMD2B locus on 2p. Analysis of microsatellite markers surrounding the disease locus disputed the original hypothesis that the affected patients would be homozygous by descent. Rather, 2 different core haplotypes, encompassing a 4-cM region spanned by D2S291-D2S145-D2S286, segregated with the disease, indicating 2 mutant alleles of independent origin. There was no association between phenotype and haplotype. Weiler et al. (1996) concluded that LGMD and MM in this population were caused by the same mutation at the LGMD2B locus and that additional factors, both genetic and nongenetic, contributed to the clinical phenotype.

By examining critical recombination events in 2 consanguineous families of Tunisian origin with MM, Bejaoui et al. (1998) refined the MM locus to a 360-kb segment. They mapped the cytoskeletal protein beta-adducin gene (102681) within the MM candidate region, but failed to find a consistent pattern of mutation of this gene in MM patients.

Although Welander distal myopathy also links to 2p13, von Tell et al. (2003) used extended linkage analysis to exclude the dysferlin gene as the cause of that disease.

Molecular Genetics
In 9 families with either Miyoshi myopathy or LGMD2B, Liu et al. (1998) identified 9 mutations in the dysferlin gene (see, e.g., 603009.0001), indicating that they are allelic disorders.

Nomenclature
In a review of limb-girdle muscular dystrophies, Bushby (1999) referred to LGMD2B and Miyoshi myopathy as dysferlinopathies.

REFERENCES
1. Bejaoui, K., Hirabayashi, K., Hentati, F., Haines, J. L., Ben Hamida, C., Belal, S., Miller, R. G., McKenna-Yasek, D., Weissenbach, J., Rowland, L. P., Griggs, R. C., Munsat, T. L., Ben Hamida, M., Arahata, K., Brown, R. H., Jr. Linkage of Miyoshi myopathy (distal autosomal recessive muscular dystrophy) locus to chromosome 2p12-14. Neurology 45: 768-772, 1995. [PubMed: 7723968, related citations] [Full Text: Pubget]

2. Bejaoui, K., Liu, J., McKenna-Yasek, D., Le Paslier, D., Bossie, K., Gilligan, D. M., Brown, R. H. Genetic fine mapping of the Miyoshi myopathy locus and exclusion of eight candidate genes. Neurogenetics 1: 189-196, 1998. [PubMed: 10737122, related citations] [Full Text: Springer, Pubget]

3. Bushby, K. M. D. The limb-girdle muscular dystrophies--multiple genes, multiple mechanisms. Hum. Molec. Genet. 8: 1875-1882, 1999. [PubMed: 10469840, related citations] [Full Text: HighWire Press, Pubget]

4. Cacciottolo, M., Numitone, G., Aurino, S., Caserta, I. R., Fanin, M., Politano, L., Minetti, C., Ricci, E., Piluso, G., Angelini, C., Nigro, V. Muscular dystrophy with marked dysferlin deficiency is consistently caused by primary dysferlin gene mutations. Europ. J. Hum. Genet. 19: 974-980, 2011. [PubMed: 21522182, related citations] [Full Text: Nature Publishing Group, Pubget]

5. Ideta, T., Shikai, T., Uchino, M., Okajima, T., Akatsuka, M. Distal myopathy--report of 4 cases in two families. Clin. Neurol. 13: 579-586, 1973.

6. Illa, I., De Luna, N., Dominguez-Perles, R., Rojas-Garcia, R., Paradas, C., Palmer, J., Marquez, C., Gallano, P., Gallardo, E. Symptomatic dysferlin gene mutation carriers: characterization of two cases. Neurology 68: 1284-1289, 2007. [PubMed: 17287450, related citations] [Full Text: HighWire Press, Pubget]

7. Isaacs, H., Badenhorst, M. E., Whistler, T. Autosomal recessive distal myopathy. J. Clin. Path. 41: 188-194, 1988. [PubMed: 3350979, related citations] [Full Text: HighWire Press, Pubget]

8. Kuhn, E., Schroder, J. M. A new type of distal myopathy in two brothers. J. Neurol. 226: 181-185, 1981. [PubMed: 6172565, related citations] [Full Text: Pubget]

9. Liu, J., Aoki, M., Illa, I., Wu, C., Fardeau, M., Angelini, C., Serrano, C., Urtizberea, J. A., Hentati, F., Ben Hamida, M., Bohlega, S., Culper, E. J., Amato, A. A., Bossie, K., Oeltjen, J., Bejaoui, K., McKenna-Yasek, D., Hosler, B. A., Schurr, E., Arahata, K., de Jong, P. J., Brown, R. H., Jr. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nature Genet. 20: 31-36, 1998. [PubMed: 9731526, related citations] [Full Text: Nature Publishing Group, Pubget]

10. Miyoshi, K., Kawai, H., Iwasa, M., Kusaka, K., Nishino, H. Autosomal recessive distal muscular dystrophy as a new type of progressive muscular dystrophy: seventeen cases in eight families including an autopsied case. Brain 109: 31-54, 1986. [PubMed: 3942856, related citations] [Full Text: HighWire Press, Pubget]

11. Miyoshi, K., Saijo, K., Kuryu, T., Tada, Y., Otsuka, Y., Oshima, Y., Nakano, N., Kawai, H., Miyake, M., Okazawa, T., Kohama, T., Kunishige, A. Four cases of distal myopathy in two families. Jpn. J. Hum. Genet. 12: 113, 1967.

12. Ro, L.-S., Lee-Chen, G.-J., Lin, T.-C., Wu, Y.-R., Chen, C.-M., Lin, C.-Y., Chen, S.-T. Phenotypic features and genetic findings in 2 Chinese families with Miyoshi distal myopathy. Arch. Neurol. 61: 1594-1599, 2004. [PubMed: 15477515, related citations] [Full Text: HighWire Press, Pubget]

13. Rowin, J., Meriggioli, M. N., Cochran, E. J., Sanders, D. B. Prominent inflammatory changes on muscle biopsy in patients with Miyoshi myopathy. Neuromusc. Disord. 9: 417-420, 1999. [PubMed: 10545047, related citations] [Full Text: Pubget]

14. Sasaki, K., Mori, H., Takahashi, K., Nakamura, H. Distal myopathy--report of four cases. Clin. Neurol. 9: 627-637, 1969.

15. Spuler, S., Carl, M., Zabojszcza, J., Straub, V., Bushby, K., Moore, S. A., Bahring, S., Wenzel, K., Vinkemeier, U., Rocken, C. Dysferlin-deficient muscular dystrophy features amyloidosis. Ann. Neurol. 63: 323-328, 2008. [PubMed: 18306167, related citations] [Full Text: John Wiley & Sons, Inc., Pubget]

16. von Tell, D., Bruder, C. E. G., Anderson, L. V. B., Anvret, M., Ahlberg, G. Refined mapping of the Welander distal myopathy region on chromosome 2p13 positions the new candidate region telomeric of the DYSF locus. Neurogenetics 4: 173-177, 2003. [PubMed: 12836053, related citations] [Full Text: Springer, Pubget]

17. Weiler, T., Greenberg, C. R., Nylen, E., Halliday, W., Morgan, K., Eggertson, D., Wrogemann, K. Limb-girdle muscular dystrophy and Miyoshi myopathy in an aboriginal Canadian kindred map to LGMD2B and segregate with the same haplotype. Am. J. Hum. Genet. 59: 872-878, 1996. [PubMed: 8808603, related citations] [Full Text: Pubget]

18. Yamanouchi, Y., Ozawa, E., Nonaka, I. Autosomal recessive distal muscular dystrophy: normal expression of dystrophin, utrophin and dystrophin-associated proteins in muscle fibers. J. Neurol. Sci. 126: 70-76, 1994. [PubMed: 7836950, related citations] [Full Text: Pubget]

Contributors: Cassandra L. Kniffin - updated : 9/22/2011
Cassandra L. Kniffin - updated : 3/24/2009
Cassandra L. Kniffin - updated : 12/5/2007
Marla J. F. O'Neill - updated : 8/2/2007
Cassandra L. Kniffin - reorganized : 12/15/2004
Cassandra L. Kniffin - updated : 12/10/2004
Victor A. McKusick - updated : 1/10/2000
Victor A. McKusick - updated : 10/12/1999
Victor A. McKusick - updated : 8/27/1998
Victor A. McKusick - updated : 5/6/1998
Orest Hurko - updated : 7/25/1995
Creation Date: Victor A. McKusick : 6/4/1986
Edit History: carol : 09/29/2011
ckniffin : 9/22/2011
carol : 3/25/2010
carol : 3/25/2010
ckniffin : 3/24/2010
wwang : 3/31/2009
ckniffin : 3/24/2009
wwang : 12/11/2007
ckniffin : 12/5/2007
wwang : 8/15/2007
terry : 8/2/2007
tkritzer : 12/15/2004
ckniffin : 12/10/2004
ckniffin : 8/12/2003
carol : 3/20/2002
mgross : 4/5/2001
mgross : 4/5/2001
mgross : 1/24/2000
mcapotos : 1/20/2000
terry : 1/10/2000
carol : 10/12/1999
carol : 10/11/1999
alopez : 9/2/1998
alopez : 8/31/1998
terry : 8/27/1998
carol : 5/13/1998
terry : 5/6/1998
alopez : 7/3/1997
joanna : 11/14/1996
jamie : 11/1/1996
mark : 10/25/1996
terry : 10/16/1996
mimman : 2/8/1996
carol : 1/20/1995
pfoster : 7/25/1994
davew : 6/6/1994
supermim : 3/17/1992
carol : 2/28/1992