#600737
INCLUSION BODY MYOPATHY 2, AUTOSOMAL RECESSIVE; IBM2

Alternative titles; symbols
INCLUSION BODY MYOPATHY, AUTOSOMAL RECESSIVE
INCLUSION BODY MYOPATHY, QUADRICEPS-SPARING; QSM

Phenotype Gene Relationships
Location Phenotype Phenotype
MIM number
Gene/Locus Gene/Locus
MIM number
9p13.3 Inclusion body myopathy, autosomal recessive 600737 GNE 603824


TEXT
A number sign (#) is used with this entry because autosomal recessive inclusion body myopathy (IBM2) is caused by homozygous or compound heterozygous mutation in the GNE gene (603824).

Nonaka myopathy (NM; 605820) is an allelic disorder with a similar phenotype.

Clinical Features
Argov and Yarom (1984) described the disorder in Jews of Persian origin. The onset of this disorder usually occurred after the age of 20 years but before the middle of the fourth decade of life. Proximal and distal muscle weakness and wasting of the upper and lower limbs were progressive and resulted in severe incapacitation within 10 to 20 years. Despite this, there typically was sparing of the quadriceps muscles even in advanced stages of the disease, a feature unique to this form of inclusion body myopathy. It was not clear to the authors whether this disorder was primarily neurogenic or myopathic.

Massa et al. (1991) reported 2 unrelated patients, each from a family of Iranian-Kurdish-Jewish origin. The picture was that of adult-onset, slowly progressive limb-girdle muscle weakness with a remarkable sparing of quadriceps muscles.

Zlotogora (1995) reported that this condition had been identified in 19 subjects of Iranian Jewish extraction and 3 others, possibly of that origin. They cited the reports of Adam et al. (1981), Argov and Yarom (1984), and Sadeh et al. (1993). Muscular weakness usually appeared in the third decade as gait difficulties. Progression was gradual, and most patients became severely incapacitated a decade after onset. Ocular, pharyngeal, and cardiac muscles were not involved. The muscles of the shoulder girdle were severely affected in advanced cases, with relative sparing of the deltoid, biceps, and triceps. In the lower limbs, foot dorsiflexion was usually very weak at an early stage of the disease. When leg muscle weakness becomes widespread, the most characteristic finding becomes evident, namely sparing of the quadriceps. The quadriceps muscles stayed strong even in advanced stages of the disorder, and thus the patients were able to stand and walk until late in the course of the disease. Creatine kinase levels were normal or moderately elevated, and nerve conduction velocity was normal.

Pathogenesis
Argov and Yarom (1984) found that muscle biopsies from affected patients showed a rimmed vacuole myopathy and that the degenerating muscle fibers contained abnormal accumulations of beta-amyloid protein (104760) and other pathologic markers found in brain specimens from neurodegenerative disorders such as Alzheimer disease (see 104300). However, there was no central nervous system disease in these patients.

Massa et al. (1991) reported that muscle biopsies of affected patients showed abundant lined vacuoles and characteristic cytoplasmic inclusions of 15- to 18-nm filaments. Many vacuolated muscle fibers showed immunoreactivity to neural cell adhesion molecule (NCAM1; 116930), a fetal muscle antigen. In muscle biopsies, Zlotogora (1995) found many muscle fibers containing clefts or round vacuoles rimmed by granular material that stained basophilic on hematoxylin and eosin.

Ricci et al. (2006) found that NCAM1 was hyposialylated in IBM2 muscle, as suggested by its decreased molecular weight on Western blot analysis. NCAM1 was identified as a discrete band of 130 kD in IBM2 muscle compared to a broad band of 150 to 200 kD in other myopathies. NCAM1 was almost undetectable in normal control muscles, since it is usually detectable in regenerating fibers. Ricci et al. (2006) suggested that this specific abnormality could be used for diagnosis.

In muscle biopsies from 5 patients with IBM2, Krause et al. (2007) found that the GNE protein was expressed at normal levels and showed normal localization, suggesting that the disorder results from impaired GNE function.

By gene expression profiling of muscle specimens from 10 IBM2 patients with the Persian Jewish founder mutation M712T (603824.0005) compared to controls, Eisenberg et al. (2008) found that a large proportion (56 of 300, 18.6%) of differentially expressed mRNAs of known function in IBM2 encoded proteins implicated in various mitochondrial processes. Morphologic analysis of mitochondria using video-rate confocal microscopy showed a high degree of mitochondrial branching in patient cells, which may represent compensatory mechanisms. The results indicated that dysregulation of mitochondrial pathways, such as apoptosis, may be involved in the pathophysiology of IBM2. Eisenberg et al. (2008) suggested that these subtle changes may partially explain the slow evolution of this disorder.

Diagnosis
Ricci et al. (2006) found that NCAM1 (116930) was hyposialylated in IBM2 muscle, as suggested by its increased electrophoretic mobility on Western blot analysis. NCAM1 was identified as a discrete band of 130 kD in IBM2 muscle compared to a broad band of 150 to 200 kD in other myopathies. In a follow-up report, Broccolini et al. (2010) demonstrated that Western blot analysis of muscle NCAM1 could be used for diagnosis of IBM2 in patients with unusual phenotypes. Three patients among 84 patients with proximal or distal muscle weakness were found to have a 130-kD NCAM1 band, and subsequently, all 3 patients were found to have homozygous or compound heterozygous mutations in the GNE gene. These 3 patients had features not typical for IBM2, including lack of rimmed vacuoles on biopsy, severe early onset, and mild very late onset with distal muscle weakness, respectively. The hyposialylated NCAM1 was expressed by abnormal nonregenerating muscle fibers.

Mapping
Mitrani-Rosenbaum et al. (1996) performed linkage analyses in 9 Persian Jewish families selected for study because at least 1 member was previously diagnosed with hereditary IBM. Clinical studies provided evidence for autosomal recessive inheritance. A genomewide analysis demonstrated linkage to 9p1-q1 (D9S166); maximum lod score of 5.32 at theta = 0.0. Ikeuchi et al. (1997) found linkage to 9p1-q1 in Japanese families with autosomal recessive distal myopathy (Nonaka myopathy; 605820), suggesting that that disorder and hereditary inclusion body myopathy are allelic. Christodoulou et al. (1998) performed linkage analysis in 10 families, 6 of Iranian-Jewish origin and 4 from other ethnic groups, with autosomal recessive quadriceps-sparing inclusion body myopathy. They confirmed linkage to chromosome 9p1, with a maximum lod score of 11.33 at a recombination fraction of 0.001 between the disease and locus D9S1859.

Eisenberg et al. (1999, 2001) localized the gene in Middle Eastern Jews to 9p13-p12 within a genomic interval of about 700 kb. Haplotype analysis of the chromosomal region in 104 affected people from 47 Middle Eastern families indicated 1 unique ancestral founder chromosome. By contrast, single non-Jewish families from India, U.S., and the Bahamas, with quadriceps-sparing myopathy and linkage to the same 9p13-p12 region, showed 3 distinct haplotypes.

Molecular Genetics
Sivakumar et al. (1995) analyzed the sequence of exons 16 and 17 of amyloid precursor protein in 8 individuals with familial inclusion body myopathy, including 5 patients from Caucasian families segregating IBM in autosomal dominant fashion and 3 individuals who had apparent autosomal recessive inheritance, 1 of whom was of Iranian-Jewish ancestry. No mutations were demonstrated in these exons.

After excluding other potential candidate genes that mapped to the region, Eisenberg et al. (2001) identified mutations in the GNE gene (603824) in affected members of the QSM families: all patients of Middle Eastern descent shared a single homozygous missense mutation (603824.0005), whereas affected individuals of families of other ethnic origins were compound heterozygotes for distinct mutations.

In 2 second cousins from an Italian family with IBM2, Broccolini et al. (2002) identified compound heterozygosity in the GNE gene: a novel mutation (met171 to val; 603824.0016) and M712T (603824.0005). The authors noted that it was the first report of the M712T mutation in patients of non-Middle Eastern descent. In an American patient with IBM2, Vasconcelos et al. (2002) identified compound heterozygosity in the GNE gene, expanding the genetic heterogeneity of the disorder.

Population Genetics
This disorder, affecting mainly leg muscles but with an unusual distribution that spares the quadriceps, was first described in Jews of Persian descent (Argov and Yarom, 1984). It was later found in Jews originating from other Middle Eastern countries, as well as in non-Jews.

Argov et al. (2003) identified homozygosity for the GNE M712T mutation (603824.0005) in 129 Middle Eastern patients with IBM2 from 55 families. Eleven patients had atypical features: 5 had involvement of the quadriceps muscle, 2 patients did not have distal weakness, 3 patients had facial weakness, and 1 patient had perivascular inflammation. There were 5 unaffected individuals with the homozygous mutation from 5 different IBM2 families, including 2 who were 50 and 68 years old. The families included Middle Eastern Jews, Karaites, and Arab Muslims of Palestinian and Bedouin origin. Argov et al. (2003) offered a detailed historical perspective of the different cultures, and concluded that this founder mutation is approximately 1,300 years old and is not limited to those of Jewish descent.

Animal Model
Malicdan et al. (2007) generated Gne-deficient mice expressing the human D176V-GNE mutation as a mouse model of DMRV-HIBM. Complete knockout of the Gne gene was embryonic lethal. Mice with the D176V mutation showed marked hyposialylation in serum, muscle, and other organs. Reduction in motor performance in these mice could only be seen from 30 weeks of age. By 32 weeks, myofibers developed beta-amyloid deposition, which preceded rimmed vacuole formation at 42 weeks. The findings also suggested that hyposialylation plays an important role in the pathomechanism of DMRV-HIBM. Malicdan et al. (2009) found that D176V-mutant mice treated orally with sialic acid showed increased survival, increased motor performance, and decreased number of rimmed vacuoles in skeletal muscle compared to untreated mice with the disorder. Prophylactic treatment prevented development of the myopathic phenotype. The findings indicated that hyposialylation is a key factor in the pathomechanism of DMRV-HIBM.

REFERENCES
1. Adam, A., Josefsberg, Z., Pertzelan, A., Zadik, Z., Chemke, J. M., Laron, Z. Occurrence of four types of growth hormone-related dwarfism in Israeli communities. Europ. J. Pediat. 137: 35-39, 1981. [PubMed: 7274298, related citations] [Full Text: Pubget]

2. Argov, A., Yarom, R. 'Rimmed vacuole myopathy' sparing the quadriceps: a unique disorder in Iranian Jews. J. Neurol. Sci. 64: 33-43, 1984. [PubMed: 6737002, related citations] [Full Text: Elsevier Science, Pubget]

3. Argov, Z., Eisenberg, I., Grabov-Nardini, G., Sadeh, M., Wirguin, I., Soffer, D., Mitrani-Rosenbaum, S. Hereditary inclusion body myopathy: the Middle Eastern genetic cluster. Neurology 60: 1519-1523, 2003. [PubMed: 12743242, related citations] [Full Text: HighWire Press, Pubget]

4. Broccolini, A., Gidaro, T., Tasca, G., Morosetti, R., Rodolico, C., Ricci, E., Mirabella, M. Analysis of NCAM helps identify unusual phenotypes of hereditary inclusion-body myopathy. Neurology 75: 265-272, 2010. [PubMed: 20644153, related citations] [Full Text: HighWire Press, Pubget]

5. Broccolini, A., Pescatori, M., D'Amico, A., Sabino, A., Silvestri, G., Ricci, E., Servidei, S., Tonali, P. A., Mirabella, M. An Italian family with autosomal recessive inclusion-body myopathy and mutations in the GNE gene. Neurology 59: 1808-1809, 2002. [PubMed: 12473780, related citations] [Full Text: HighWire Press, Pubget]

6. Christodoulou, K., Papadopoulou, E., Tsingis, M., Askanas, V., Engel, W. K., McFerrin, J., Dalakas, M., Rowland, L. P., Mirabella, M., Middleton, L. T. Narrowing of the gene locus for autosomal-recessive quadriceps sparing inclusion-body myopathy (ARQS-IBM) to chromosome 9p1. Acta Myol. 2: 7-9, 1998.

7. Eisenberg, I., Avidan, N., Potikha, T., Hochner, H., Chen, M., Olender, T., Barash, M., Shemesh, M., Sadeh, M., Grabov-Nardini, G., Shmilevich, I., Friedmann, A., Karpati, G., Bradley, W. G., Baumbach, L., Lancet, D., Ben Asher, E., Beckmann, J. S., Argov, Z., Mitrani-Rosenbaum, S. The UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nature Genet. 29: 83-87, 2001. [PubMed: 11528398, related citations] [Full Text: Nature Publishing Group, Pubget]

8. Eisenberg, I., Hochner, H., Shemesh, M., Levi, T., Potikha, T., Sadeh, M., Argov, Z., Jackson, C. L., Mitrani-Rosenbaum, S. Physical and transcriptional map of the hereditary inclusion body myopathy locus on chromosome 9p12-p13. Europ. J. Hum. Genet. 9: 501-509, 2001. [PubMed: 11464241, related citations] [Full Text: Nature Publishing Group, Pubget]

9. Eisenberg, I., Novershtern, N., Itzhaki, Z., Becker-Cohen, M., Sadeh, M., Willems, P. H. G. M., Friedman, N., Koopman, W. J. H., Mitrani-Rosenbaum, S. Mitochondrial processes are impaired in hereditary inclusion body myopathy. Hum. Molec. Genet. 17: 3663-3674, 2008. [PubMed: 18723858, related citations] [Full Text: HighWire Press, Pubget]

10. Eisenberg, I., Thiel, C., Levi, T., Tiram, E., Argov, Z., Sadeh, M., Jackson, C. L., Thierfelder, L., Mitrani-Rosenbaum, S. Fine structure mapping of the hereditary inclusion body myopathy locus. Genomics 55: 43-48, 1999. [PubMed: 9888997, related citations] [Full Text: Elsevier Science, Pubget]

11. Ikeuchi, T., Asaka, T., Saito, M., Tanaka, H., Higuchi, S., Tanaka, K., Saida, K., Uyama, E., Mizusawa, H., Fukuhara, N., Nonaka, I., Takamori, M., Tsuji, S. Gene locus for autosomal recessive distal myopathy with rimmed vacuoles maps to chromosome 9. Ann. Neurol. 41: 432-437, 1997. [PubMed: 9124799, related citations] [Full Text: Pubget]

12. Krause, S., Aleo, A., Hinderlich, S., Merlini, L., Tournev, I., Walter, M. C., Argov, Z., Mitrani-Rosenbaum, S., Lochmuller, H. GNE protein expression and subcellular distribution are unaltered in HIBM. Neurology 69: 655-659, 2007. [PubMed: 17698786, related citations] [Full Text: HighWire Press, Pubget]

13. Malicdan, M. C. V., Noguchi, S., Hayashi, Y. K., Nonaka, I., Nishino, I. Prophylactic treatment with sialic acid metabolites precludes the development of the myopathic phenotype in the DMRV-hIBM mouse model. Nature Med. 15: 690-695, 2009. [PubMed: 19448634, related citations] [Full Text: Nature Publishing Group, Pubget]

14. Malicdan, M. C. V., Noguchi, S., Nonaka, I., Hayashi, Y. K., Nishino, I. A Gne knockout mouse expressing human GNE D176V mutation develops features similar to distal myopathy with rimmed vacuoles or hereditary inclusion body myopathy. Hum. Molec. Genet. 16: 2669-2682, 2007. [PubMed: 17704511, related citations] [Full Text: HighWire Press, Pubget]

15. Massa, R., Weller, B., Karpati, G., Shoubridge, E., Carpenter, S. Familial inclusion body myositis among Kurdish-Iranian Jews. Arch. Neurol. 48: 519-522, 1991. [PubMed: 1850594, related citations] [Full Text: HighWire Press, Pubget]

16. Mitrani-Rosenbaum, S., Argov, Z., Blumenfeld, A., Seidman, C. E., Seidman, J. G. Hereditary inclusion body myopathy maps to chromosome 9p1-q1. Hum. Molec. Genet. 5: 159-163, 1996. [PubMed: 8789455, related citations] [Full Text: HighWire Press, Pubget]

17. Ricci, E., Broccolini, A., Gidaro, T., Morosetti, R., Gliubizzi, C., Frusciante, R., Di Lella, G. M., Tonali, P. A., Mirabella, M. NCAM is hyposialylated in hereditary inclusion body myopathy due to GNE mutations. Neurology 66: 755-758, 2006. [PubMed: 16534119, related citations] [Full Text: HighWire Press, Pubget]

18. Sadeh, M., Gadoth, N., Hadar, H., Ben-David, E. Vacuolar myopathy sparing the quadriceps. Brain 116: 217-232, 1993. [PubMed: 8453459, related citations] [Full Text: HighWire Press, Pubget]

19. Sivakumar, K., Cervenakova, L., Dalakas, M. C., Leon-Monzon, M., Isaacson, S. H., Nagle, J. W., Vasconcelos, O., Goldfarb, I. G. Exons 16 and 17 of the amyloid precursor protein gene in familial inclusion body myopathy. Ann. Neurol. 38: 267-269, 1995. [PubMed: 7654077, related citations] [Full Text: Pubget]

20. Vasconcelos, O. M., Raju, R., Dalakas, M. C. GNE mutations in an American family with quadriceps-sparing IBM and lack of mutations in s-IBM. Neurology 59: 1776-1779, 2002. [PubMed: 12473769, related citations] [Full Text: HighWire Press, Pubget]

21. Zlotogora, J. Hereditary disorders among Iranian Jews. Am. J. Med. Genet. 58: 32-37, 1995. [PubMed: 7573153, related citations] [Full Text: Pubget]

Contributors: Cassandra L. Kniffin - updated : 6/21/2011
Cassandra L. Kniffin - updated : 8/24/2010
Cassandra L. Kniffin - updated : 9/2/2009
Cassandra L. Kniffin - updated : 7/29/2009
Cassandra L. Kniffin - updated : 11/30/2007
Cassandra L. Kniffin - updated : 9/21/2007
Cassandra L. Kniffin - updated : 8/19/2003
Cassandra L. Kniffin - reorganized : 1/24/2003
Cassandra L. Kniffin - updated : 1/17/2003
Victor A. McKusick - updated : 8/23/2001
Ada Hamosh - updated : 6/23/1999
Victor A. McKusick - updated : 6/3/1999
Victor A. McKusick - edited : 6/11/1997
Creation Date: Victor A. McKusick : 8/22/1995
Edit History: wwang : 07/06/2011
ckniffin : 6/21/2011
wwang : 9/16/2010
ckniffin : 8/24/2010
wwang : 9/9/2009
ckniffin : 9/2/2009
wwang : 8/10/2009
ckniffin : 7/29/2009
wwang : 12/7/2007
ckniffin : 11/30/2007
wwang : 10/2/2007
ckniffin : 9/21/2007
ckniffin : 6/30/2005
tkritzer : 2/25/2005
cwells : 8/19/2003
ckniffin : 8/18/2003
carol : 1/24/2003
carol : 1/24/2003
ckniffin : 1/21/2003
ckniffin : 1/17/2003
terry : 6/26/2002
alopez : 8/27/2001
alopez : 8/27/2001
terry : 8/23/2001
mgross : 4/5/2001
kayiaros : 7/13/1999
alopez : 6/23/1999
terry : 6/3/1999
dkim : 12/10/1998
alopez : 9/16/1998
joanna : 6/11/1997
mimadm : 11/3/1995
terry : 10/31/1995
mark : 8/22/1995