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

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References

  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).
    Article CAS Google Scholar
  2. Bitoun, M. et al. Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat. Genet. 37, 1207–1209 (2005).
    Article CAS Google Scholar
  3. Jeannet, P.Y. et al. Clinical and histologic findings in autosomal centronuclear myopathy. Neurology 62, 1484–1490 (2004).
    Article Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  10. Kojima, C. et al. Regulation of Bin1 SH3 domain binding by phosphoinositides. EMBO J. 23, 4413–4422 (2004).
    Article CAS Google Scholar
  11. Lee, E. et al. Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297, 1193–1196 (2002).
    Article CAS Google Scholar
  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).
    Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  18. Peter, B.J. et al. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499 (2004).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  27. Engel, A.G. & Franzini-Armstrong, C. Myology, Basic and Clinical (McGraw-Hill New York, 2004).
    Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS Google Scholar

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Acknowledgements

We thank the affected individuals and their families for participation in this study. We also thank J. Wahlström for providing samples from one of the families, P. De Camilli (Yale University) for providing the BIN1-iso8 and BIN1-BAR* cDNA constructs, P. McPherson (McGill University) for providing the BIN1 SH3 domain cDNA construct, M. Argentini for peptide mass fingerprinting, G. Duval for generation of antibodies, S. Vicaire for DNA sequencing, C. Thibault for DNA microarray analysis and H. Rohde, N. Dondaine and E. Klein for experimental help. This work was supported by the Institut National de la Santé et de la Recherche Médicale, the Centre National de la Recherche Scientifique, the Collège de France, the Agence Nationale de la Recherche and the Association Française Contre les Myopathies (AFM). A.-S.N. is the recipient of an ATER from Collège de France, and A.T. is the recipient of a fellowship from AFM.

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Author notes

  1. Anne-Sophie Nicot and Anne Toussaint: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Molecular Pathology, Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Illkirch, F-67400, France
    Anne-Sophie Nicot, Anne Toussaint, Valérie Tosch, Christine Kretz, Jean-Marie Garnier, Jean-Louis Mandel & Jocelyn Laporte
  2. Institut National de la Santé et de la Recherche Médicale (INSERM), U596, Illkirch, F-67400, France
    Anne-Sophie Nicot, Anne Toussaint, Valérie Tosch, Christine Kretz, Jean-Marie Garnier, Jean-Louis Mandel & Jocelyn Laporte
  3. the Centre National de la Recherche Scientifique (CNRS), UMR7104, Illkirch, F-67400, France
    Anne-Sophie Nicot, Anne Toussaint, Valérie Tosch, Christine Kretz, Jean-Marie Garnier, Jean-Louis Mandel & Jocelyn Laporte
  4. Université Louis Pasteur, Strasbourg, F-67000, France
    Anne-Sophie Nicot, Anne Toussaint, Valérie Tosch, Christine Kretz, Jean-Marie Garnier, Jean-Louis Mandel & Jocelyn Laporte
  5. Collège de France, Chaire de Génétique Humaine, Illkirch, F-67400, France
    Anne-Sophie Nicot, Anne Toussaint, Valérie Tosch, Christine Kretz, Jean-Marie Garnier, Jean-Louis Mandel & Jocelyn Laporte
  6. Department of Medical Genetics, University of Helsinki, and The Folkhälsan Institute of Genetics, Biomedicum, Helsinki, FIN-00014, Finland
    Carina Wallgren-Pettersson
  7. Department of Molecular Medicine and Surgery, Clinical Genetics Unit, Karolinska University Hospital, Stockholm, S-171 76, Sweden
    Erik Iwarsson
  8. Academic Unit of Medical Genetics and Regional Genetic Service, Central Manchester and Manchester Children's University Hospitals, Manchester, M13 OJH, UK
    Helen Kingston
  9. Laboratoire de Diagnostic Génétique, CHRU–Faculté de Médecine et Laboratoire de Génétique Médicale EA3949, Université Louis Pasteur, Strasbourg, F-67085, France
    Valérie Biancalana & Jean-Louis Mandel
  10. Department of Pathology, Sahlgrenska University Hospital, Göteborg, SE-413 45, Sweden
    Anders Oldfors

Authors

  1. Anne-Sophie Nicot
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  2. Anne Toussaint
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  3. Valérie Tosch
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  4. Christine Kretz
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  5. Helen Kingston
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  6. Jean-Marie Garnier
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  7. Valérie Biancalana
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  8. Anders Oldfors
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  9. Jean-Louis Mandel
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  10. Jocelyn Laporte
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Contributions

Experiments were performed by A.-S.N., A.T., V.T., C.K., J.-M.G., V.B., A.O. and J.L. A.-S.N., A.T. and J.L. analyzed the data. C.W.-P., E.I. and H.K. contributed clinical samples and patient data. The study was designed and coordinated by J.-L.M. and J.L., and the paper was written by J.L.

Corresponding author

Correspondence toJocelyn Laporte.

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The authors declare no competing financial interests.

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Nicot, AS., Toussaint, A., Tosch, V. et al. Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy.Nat Genet 39, 1134–1139 (2007). https://doi.org/10.1038/ng2086

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