Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy

Nature Genetics

Volumn 39, Issue 9, 2007, Pages 1134-1139

  Nicot, Anne Sophie ^a,b,c,d,e   Toussaint, Anne ^a,b,c,d,e   Tosch, Valérie ^a,b,c,d,e   Kretz, Christine ^a,b,c,d,e   Wallgren Pettersson, Carina ^f   Iwarsson, Erik ^g   Kingston, Helen ^h   Garnier, Jean Marie ^a,b,c,d,e   Biancalana, Valérie ^d   Oldfors, Anders ⁱ   Mandel, Jean Louis ^a,b,c,d,e   Laporte, Jocelyn ^a,b,c,d,e  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e Centre de Recherche Interdisciplinaire en Biologie   (France)

^f UNIVERSITY OF HELSINKI   (Finland)

^g KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^h MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

ⁱ SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHYSIN; AMPHIPHYSIN 2; BIN1 PROTEIN; DYNAMIN II; PROTEIN SH3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOSOMAL RECESSIVE DISORDER; AUTOSOMAL RECESSIVE INHERITANCE; CARBOXY TERMINAL SEQUENCE; CENTRONUCLEAR MYOPATHY; CONTROLLED STUDY; FAMILY; GENE INTERACTION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC IDENTIFICATION; GENETIC TRANSFECTION; HOMOZYGOSITY; HUMAN; MISSENSE MUTATION; MUSCLE FIBER MEMBRANE; MUSCLE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; TRANSVERSE TUBULAR SYSTEM;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; DYNAMIN II; FEMALE; GENES, RECESSIVE; GREEN FLUORESCENT PROTEINS; HAPLOTYPES; HUMANS; MALE; MICE; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; MUSCULAR DISEASES; MUTATION; NERVE TISSUE PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION;

EID: 34548341774     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng2086     Document Type: Article

References (30)

1. Laporte, J. et al. A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat. Genet. 13, 175-182 (1996).
2. Bitoun, M. et al. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 37, 1207-1209 (2005).
3. Jeannet, P.Y. et al. Clinical and histologic findings in autosomal centronuclear myopathy. Neurology 62, 1484-1490 (2004).
4. Pierson, C.R., Tomczak, K., Agrawal, P., Moghadaszadeh, B. & Beggs, A.H. X-linked myotubular and centronuclear myopathies. J. Neuropathol. Exp. Neurol. 64, 555-564 (2005).
5. Wallgren-Pettersson, C. et al. The myotubular myopathies: differential diagnosis of the X linked recessive, autosomal dominant, and autosomal recessive forms and present state of DNA studies. J. Med. Genet. 32, 673-679 (1995).
6. Dang, H., Li, Z., Skolnik, E.Y. & Fares, H. Disease-related myotubularins function in endocytic traffic in Caenorhabditis elegans. Mol. Biol. Cell 15, 189-196 (2004).
7. Laporte, J., Bedez, F., Bolino, A. & Mandel, J.-L. Myotubularins, a large disease-associated family of cooperating catalytically active and inactive phosphoinositides phosphatases. Hum. Mol. Genet. 12, R285-R292 (2003).
8. Praefcke, G.J. & McMahon, H.T. The dynamin superfamily: universal membrane tubulation and fission molecules? Nat. Rev. Mol. Cell Biol. 5, 133-147 (2004).
9. Tosch, V. et al. A novel PtdIns3P and PtdIns(3,5)P2 phosphatase with an inactivating variant in centronuclear myopathy. Hum. Mol. Genet. 15, 3098-3106 (2006).
10. Kojima, C. et al. Regulation of Bin1 SH3 domain binding by phosphoinositides. EMBO J. 23, 4413-4422 (2004).
11. Lee, E. et al. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193-1196 (2002).
12. Mandel, J.-L., Laporte, J., Buj-Bello, A., Sewry, C. & Wallgren-Pettersson, C. Developmental disorders: X-linked myotubular myopathy. in Structural and Molecular Basis of Skeletal Muscle Diseases (ed. Karpati, G.) 124-129 (ISN Neuropath Press, Basel, Switzerland, 2002).
13. Razzaq, A. et al. Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev. 15, 2967-2979 (2001).
14. Butler, M.H. et al. Amphiphysin II (SH3P9; BIN1), a member of the amphiphysin/Rvs family, is concentrated in the cortical cytomatrix of axon initial segments and nodes of ranvier in brain and around T tubules in skeletal muscle. J. Cell Biol. 137, 1355-1367 (1997).
15. Ramjaun, A.R., Micheva, K.D., Bouchelet, I. & McPherson, P.S. Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J. Biol. Chem. 272, 16700-16706 (1997).
16. Wechsler-Reya, R., Sakamuro, D., Zhang, J., Duhadaway, J. & Prendergast, G.C. Structural analysis of the human BIN1 gene. Evidence for tissue-specific transcriptional regulation and alternate RNA splicing. J. Biol. Chem. 272, 31453-31458 (1997).
17. Itoh, T. & De Camilli, P. BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912 (2006).
18. Peter, B.J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499 (2004).
19. Ren, G., Vajjhala, P., Lee, J.S., Winsor, B. & Munn, A.L. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 70, 37-120 (2006).
20. Sakamuro, D., Elliott, K.J., Wechsler-Reya, R. & Prendergast, G.C. BIN1 is a novel MYC-interacting protein with features of a tumor suppressor. Nat. Genet. 14, 69-77 (1996).
21. Owen, D.J. et al. Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. EMBO J. 17, 5273-5285 (1998).
22. Ge, K. et al. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc. Natl. Acad. Sci. USA 96, 9689-9694 (1999).
23. Ge, K. et al. Losses of the tumor suppressor BIN1 in breast carcinoma are frequent and reflect deficits in programmed cell death capacity. Int. J. Cancer 85, 376-383 (2000).
24. Korshunov, A., Sycheva, R. & Golanov, A. Recurrent cytogenetic aberrations in central neurocytomas and their biological relevance. Acta Neuropathol. (Berl) (2006).
25. Muller, A.J. et al. Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation. Mol. Cell. Biol. 23, 4295-4306 (2003).
26. Wechsler-Reya, R.J., Elliott, K.J. & Prendergast, G.C. A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol. Cell. Biol. 18, 566-575 (1998).
27. Engel, A.G. & Franzini-Armstrong, C. Myology, Basic and Clinical (McGraw-Hill New York, 2004).
28. Buj-Bello, A. et al. The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice. Proc. Natl. Acad. Sci. USA 99, 15060-15065 (2002).
29. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 (1997).
30. Green, S., Issemann, I. & Sheer, E. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering. Nucleic Acids Res. 16, 369 (1988).