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Amphiphysin 2 (BIN1) in physiology and diseases

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Abstract

Amphiphysin 2, also named bridging integrator-1 (BIN1) or SH3P9, has been recently implicated in rare and common diseases affecting different tissues and physiological functions. BIN1 downregulation is linked to cancer progression and also correlates with ventricular cardiomyopathy and arrhythmia preceding heart failure. Increased BIN1 expression is linked to increased susceptibility for late-onset Alzheimer’s disease. In addition, altered splicing may account for the muscle component of myotonic dystrophies, while recessive germinal mutations cause centronuclear myopathy. Despite undoubtedly underlining the relevance of BIN1 in human diseases, the molecular and cellular bases leading to such different diseases are unclear at present. BIN1 is a key regulator of endocytosis and membrane recycling, cytoskeleton regulation, DNA repair, cell cycle progression, and apoptosis. In light of the recent findings on the molecular, cellular, and physiological roles of BIN1, we discuss potential pathological mechanisms and highlight common disease pathways and also tissue-specific regulation. Next challenges will be to validate BIN1 both as a prognostic marker for the related diseases and as a potential therapeutic target.

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References

  1. Mao NC, Steingrimsson E, DuHadaway J, Wasserman W, Ruiz JC, Copeland NG, Jenkins NA, Prendergast GC (1999) The murine Bin1 gene functions early in myogenesis and defines a new region of synteny between mouse chromosome 18 and human chromosome 2. Genomics 56:51–58

    Article  PubMed  CAS  Google Scholar 

  2. Leprince C, Romero F, Cussac D, Vayssiere B, Berger R, Tavitian A, Camonis J (1997) A new member of the amphiphysin family connecting endocytosis and signal transduction pathways. FASEB J 11:A928–A928

    Google Scholar 

  3. Owen DJ, Wigge P, Vallis Y, Moore JDA, Evans PR, McMahon HT (1998) Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation. EMBO J 17:5273–5285

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  4. Bauerfeind R, Takei K, De Camilli P (1997) Amphiphysin I is associated with coated endocytic intermediates and undergoes stimulation-dependent dephosphorylation in nerve terminals. J Biol Chem 272:30984–30992

    Article  PubMed  CAS  Google Scholar 

  5. Munn AL, Stevenson BJ, Geli MI, Riezman H (1995) End5, End6, and End7—mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol Biol Cell 6:1721–1742

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  6. Bauer F, Urdaci M, Aigle M, Crouzet M (1993) Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol Cell Biol 13:5070–5084

    PubMed Central  PubMed  CAS  Google Scholar 

  7. Sakamuro D, Elliott KJ, WechslerReya R, Prendergast GC (1996) BIN1 is a novel MYC-interacting protein with features of a tumour suppressor. Nat Genet 14:69–77

    Article  PubMed  CAS  Google Scholar 

  8. Butler MH, David C, Ochoa GC, Freyberg Z, Daniell L, Grabs D, Cremona O, De Camilli P (1997) 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  9. Cassimere EK, Pyndiah S, Sakamuro D (2009) The c-MYC-interacting proapoptotic tumor suppressor BIN1 is a transcriptional target for E2F1 in response to DNA damage. Cell Death Differ 16:1641–1653

    Article  PubMed  CAS  Google Scholar 

  10. Pyndiah S, Tanida S, Ahmed KM, Cassimere EK, Choe C, Sakamuro D (2011) c-MYC Suppresses BIN1 to Release Poly (ADP-Ribose) Polymerase 1: A Mechanism by Which Cancer Cells Acquire Cisplatin Resistance. Sci Signal 4. doi:10.1126/scisignal.2001556

  11. Tsutsui K, Maeda Y, Tsutsui K, Seki S, Tokunaga A (1997) cDNA cloning of a novel amphiphysin isoform and tissue-specific expression of its multiple splice variants. Biochem Biophys Res Commun 236:178–183

    Article  PubMed  CAS  Google Scholar 

  12. Ellis JD, Barrios-Rodiles M, Colak R, Irimia M, Kim T, Calarco JA, Wang XC, Pan Q, O’Hanlon D, Kim PM et al (2012) Tissue-specific alternative splicing remodels protein-protein interaction networks. Mol Cell 46:884–892

    Article  PubMed  CAS  Google Scholar 

  13. WechslerReya R, Sakamuro D, Zhang J, Duhadaway J, Prendergast GC (1997) Structural analysis of the human BIN1 gene. Evidence for tissue-specific transcriptional regulation and alternate RNA splicing. J Biol Chem 272:31453–31458

    Article  CAS  Google Scholar 

  14. Toussaint A, Cowling BS, Hnia K, Mohr M, Oldfors A, Schwab Y, Yis U, Maisonobe T, Stojkovic T, Wallgren-Pettersson C et al (2011) Defects in amphiphysin 2 (BIN1) and triads in several forms of centronuclear myopathies. Acta Neuropathol 121:253–266

    Article  PubMed  Google Scholar 

  15. Fugier C, Klein AF, Hammer C, Vassilopoulos S, Ivarsson Y, Toussaint A, Tosch V, Vignaud A, Ferry A, Messaddeq N et al (2011) Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat Med 17:720–725

    Article  PubMed  CAS  Google Scholar 

  16. Ge K, DuHadaway J, Du W, Herlyn M, Rodeck U, Prendergast GC (1999) 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 U S A 96:9689–9694

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  17. Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137:191–196

    Article  PubMed  CAS  Google Scholar 

  18. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495–499

    Article  PubMed  CAS  Google Scholar 

  19. Ramjaun AR, McPherson PS (1998) Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J Neurochem 70:2369–2376

    Article  PubMed  CAS  Google Scholar 

  20. Slepnev VI, Ochoa GC, Butler MH, Grabs D, De Camilli P (1998) Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science 281:821–824

    Article  PubMed  CAS  Google Scholar 

  21. Di Paolo G, Sankaranarayanan S, Wenk MR, Daniell L, Perucco E, Caldarone BJ, Flavell R, Picciotto MR, Ryan TA, Cremona O et al (2002) Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron 33:789–804

    Article  PubMed  Google Scholar 

  22. Nicot AS, Toussaint A, Tosch V, Kretz C, Wallgren-Pettersson C, Iwarsson E, Kingston H, Garnier JM, Biancalana V, Oldfors A et al (2007) Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat Genet 39:1134–1139

    Article  PubMed  CAS  Google Scholar 

  23. Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA, Ochoa GC, Farsad K, Wenk MR, De Camilli P (2002) Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297:1193–1196

    Article  PubMed  CAS  Google Scholar 

  24. Kojima C, Hashimoto A, Yabuta I, Hirose M, Hashimoto S, Kanaho Y, Sumimoto H, Ikegami T, Sabe H (2004) Regulation of Bin1 SH3 domain binding by phosphoinositides. Embo J 23:4413–4422

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  25. Ramjaun AR, Micheva KD, Bouchelet I, McPherson PS (1997) Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J Biol Chem 272:16700–16706

    Article  PubMed  CAS  Google Scholar 

  26. Wechsler-Reya RJ, Elliott KJ, Prendergast GC (1998) A role for the putative tumor suppressor Bin1 in muscle cell differentiation. Mol Cell Biol 18:566–575

    PubMed Central  PubMed  CAS  Google Scholar 

  27. Yu HT, Chen JK, Feng SB, Dalgarno DC, Brauer AW, Schreiber SL (1994) Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76:933–945

    Article  PubMed  CAS  Google Scholar 

  28. Royer B, Hnia K, Gavriilidis C, Tronchere H, Tosch V, Laporte J (2013) The myotubularin-amphiphysin 2 complex in membrane tubulation and centronuclear myopathies. EMBO Rep 14:907–915

    Article  PubMed  CAS  Google Scholar 

  29. Marks B, McMahon HT (1998) Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr Bio 8:740–749

    Article  CAS  Google Scholar 

  30. Hojlund K, Bowen BP, Hwang H, Flynn CR, Madireddy L, Geetha T, Langlais P, Meyer C, Mandarino LJ, Yi Z (2009) In vivo phosphoproteome of human skeletal muscle revealed by phosphopeptide enrichment and HPLC-ESI-MS/MS. J Proteome Res 8:4954–4965

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  31. David C, McPherson PS, Mundigl O, de Camilli P (1996) A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc Natl Acad Sci USA 93:331–335

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  32. Shupliakov O, Low P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, Brodin L (1997) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259–263

    Article  PubMed  CAS  Google Scholar 

  33. Wigge P, Kohler K, Vallis Y, Doyle CA, Owen D, Hunt SP, McMahon HT (1997) Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol Biol Cell 8:2003–2015

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  34. McMahon HT, Wigge P, Smith C (1997) Clathrin interacts specifically with amphiphysin and is displaced by dynamin. FEBS letters 413:319–322

    Article  PubMed  CAS  Google Scholar 

  35. McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, Grabs D, Sossin WS, Bauerfeind R, Nemoto Y, De Camilli P (1996) A presynaptic inositol-5-phosphatase. Nature 379:353–357

    Article  PubMed  CAS  Google Scholar 

  36. Micheva KD, Ramjaun AR, Kay BK, McPherson PS (1997) SH3 domain dependent interactions of endophilin with amphiphysin (vol 414, pg 308, 1997). FEBS letters 419:150

    CAS  Google Scholar 

  37. Ringstad N, Nemoto Y, DeCamilli P (1997) The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. P Natl Acad Sci USA 94:8569–8574

    Article  CAS  Google Scholar 

  38. Taylor MJ, Perrais D, Merrifield CJ (2011) A High Precision Survey of the Molecular Dynamics of Mammalian Clathrin-Mediated Endocytosis. Plos Biol 9. doi:10.1371/journal.pbio.1000604

  39. Pant S, Sharma M, Patel K, Caplan S, Carr CM, Grant BD (2009) AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 11:1399–1410

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  40. Muller AJ, Baker JF, DuHadaway JB, Ge K, Farmer G, Donover PS, Meade R, Reid C, Grzanna R, Roach AH et al (2003) 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  41. Posey AD, Jr., Swanson KE, Alvarez MG, Krishnan S, Earley JU, Band H, Pytel P, McNally EM, Demonbreun AR (2014) EHD1 mediates vesicle trafficking required for normal muscle growth and transverse tubule development. Dev Biol. doi:10.1016/j.ydbio.2014.01.004

  42. Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1:33–39

    Article  PubMed  CAS  Google Scholar 

  43. Farsad K, Ringstad N, Takei K, Floyd SR, Rose K, De Camilli P (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155:193–200

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  44. Razzaq A, Robinson IM, McMahon HT, Skepper JN, Su Y, Zelhof AC, Jackson AP, Gay NJ, O’Kane CJ (2001) 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  45. Spiegelhalter C, Tosch V, Hentsch D, Koch M, Kessler P, Schwab Y, Laporte J (2010) From dynamic live cell imaging to 3D ultrastructure: novel integrated methods for high pressure freezing and correlative light-electron microscopy. PLoS One 5. doi:10.1371/journal.pone.0009014

  46. Meunier B, Quaranta M, Daviet L, Hatzoglou A, Leprince C (2009) The membrane-tubulating potential of amphiphysin 2/BIN1 is dependent on the microtubule-binding cytoplasmic linker protein 170 (CLIP-170). Eur J Cell Biol 88:91–102

    Article  PubMed  CAS  Google Scholar 

  47. Bohm J, Vasli N, Maurer M, Cowling B, Shelton GD, Kress W, Toussaint A, Prokic I, Schara U, Anderson TJ et al (2013) Altered splicing of the bin1 muscle-specific exon in humans and dogs with highly progressive centronuclear myopathy. PLoS Genet 9. doi:10.1371/journal.pgen.1003430

  48. Yamada H, Padilla-Parra S, Park SJ, Itoh T, Chaineau M, Monaldi I, Cremona O, Benfenati F, De Camilli P, Coppey-Moisan M et al (2009) Dynamic interaction of amphiphysin with N-WASP regulates actin assembly. J Biol Chem 284:34244–34256

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  49. Yamada H, Ohashi E, Abe T, Kusumi N, Li SA, Yoshida Y, Watanabe M, Tomizawa K, Kashiwakura Y, Kumon H et al (2007) Amphiphysin 1 Is Important for actin polymerization during phagocytosis. Mol Biol Cell 18:4669–4680

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  50. Colwill K, Field D, Moore L, Friesen J, Andrews B (1999) In vivo analysis of the domains of yeast Rvs167p suggests Rvs167p function is mediated through multiple protein interactions. Genetics 152:881–893

    PubMed Central  PubMed  CAS  Google Scholar 

  51. Chapuis J, Hansmannel F, Gistelinck M, Mounier A, Van Cauwenberghe C, Kolen KV, Geller F, Sottejeau Y, Harold D, Dourlen P et al (2013) Increased expression of BIN1 mediates Alzheimer genetic risk by modulating tau pathology. Mol Psychiatry 18:1225–1234

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  52. WechslerReya R, Elliott K, Herlyn M, Prendergast GC (1997) The putative tumor suppressor BIN1 is a short-lived nuclear phosphoprotein, the localization of which is altered in malignant cells. Cancer Res 57:3258–3263

    CAS  Google Scholar 

  53. Elliott K, Ge K, Du W, Prendergast GC (2000) The c-Myc-interacting adaptor protein Bin1 activates a caspase-independent cell death program. Oncogene 19:4669–4684

    Article  PubMed  CAS  Google Scholar 

  54. DuHadaway JB, Sakamuro D, Ewert DL, Prendergast GC (2001) Bin1 mediates apoptosis by c-Myc in transformed primary cells. Cancer Res 61:3151–3156

    PubMed  CAS  Google Scholar 

  55. Elliott K, Sakamuro D, Basu A, Du W, Wunner W, Staller P, Gaubatz S, Zhang H, Prochownik E, Eilers M et al (1999) Bin1 functionally interacts with Myc and inhibits cell proliferation via multiple mechanisms. Oncogene 18:3564–3573

    Article  PubMed  CAS  Google Scholar 

  56. Kadlec L, Pendergast AM (1997) The amphiphysin-like protein 1 (ALP1) interacts functionally with the cABL tyrosine kinase and may play a role in cytoskeletal regulation. P Natl Acad Sci USA 94:12390–12395

    Article  CAS  Google Scholar 

  57. Kinney EL, Tanida S, Rodrigue AA, Johnson JK, Tompkins VS, Sakamuro D (2008) Adenovirus E1A oncoprotein liberates c-Myc activity to promote cell proliferation through abating Bin1 expression via an Rb/E2F1-dependent mechanism. J Cell Physiol 216:621–631

    Article  PubMed  CAS  Google Scholar 

  58. Meyer-Ficca ML, Meyer RG, Jacobson EL, Jacobson MK (2005) Poly (ADP-ribose) polymerases: managing genome stability. Int J Biochem Cell Biol 37:920–926

    Article  PubMed  CAS  Google Scholar 

  59. Ramalingam A, Farmer GE, Stamato TD, Prendergast GC (2007) Bin1 interacts with and restrains the DNA end-binding protein complex Ku. Cell Cycle 6:1914–1918

    Article  PubMed  CAS  Google Scholar 

  60. Grelle G, Kostka S, Otto A, Kersten B, Genser KF, Muller EC, Walter S, Boddrich A, Stelzl U, Hanig C et al (2006) Identification of VCP/p97, carboxyl terminus of Hsp70-interacting protein (CHIP), and amphiphysin II interaction partners using membrane-based human proteome arrays. Mol Cell Proteomics 5:234–244

    Article  PubMed  CAS  Google Scholar 

  61. Routhier EL, Donover PS, Prendergast GC (2003) hob1+, the fission yeast homolog of Bin1, is dispensable for endocytosis or actin organization, but required for the response to starvation or genotoxic stress. Oncogene 22:637–648

    Article  PubMed  CAS  Google Scholar 

  62. Chang MY, Boulden J, Katz JB, Wang L, Meyer TJ, Soler AP, Muller AJ, Prendergast GC (2007) Bin1 ablation increases susceptibility to cancer during aging, particularly lung cancer. Cancer Res 67:7605–7612

    Article  PubMed  CAS  Google Scholar 

  63. Zhong XL, Hoelz DJ, Kumar HR, Sandoval JA, Rescorla FJ, Hickey RJ, Malkas LH (2009) Bin1 is linked to metastatic potential and chemosensitivity in neuroblastoma. Pediatr Blood Cancer 53:332–337

    Article  PubMed  Google Scholar 

  64. Pan K, Liang XT, Zhang HK, Zhao JJ, Wang DD, Li JJ, Lian QZ, Chang AE, Li Q, Xia JC (2012) Characterization of bridging integrator 1 (bin1) as a potential tumor suppressor and prognostic marker in hepatocellular carcinoma. Mol Med 18:507–518

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  65. Ghaneie A, Zemba-Palko V, Itoh H, Itoh K, Sakamuro D, Nakamura S, Soler AP, Prendergast GC (2007) Bin1 attenuation in breast cancer is correlated to nodal metastasis and reduced survival. Cancer Biol Ther 6:192–194

    Article  PubMed  Google Scholar 

  66. Ge K, Duhadaway J, Sakamuro D, Wechsler-Reya R, Reynolds C, Prendergast GC (2000) 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

    Article  PubMed  CAS  Google Scholar 

  67. Ge K, Minhas F, Duhadaway J, Mao NC, Wilson D, Buccafusca R, Sakamuro D, Nelson P, Malkowicz SB, Tomaszewski J et al (2000) Loss of heterozygosity and tumor suppressor activity of Bin1 in prostate carcinoma. Int J Cancer 86:155–161

    Article  PubMed  CAS  Google Scholar 

  68. Kennah E, Ringrose A, Zhou LL, Esmailzadeh S, Qian H, Su MW, Zhou YW, Jiang XY (2009) Identification of tyrosine kinase, HCK, and tumor suppressor, BIN1, as potential mediators of AHI-1 oncogene in primary and transformed CTCL cells. Blood 113:4646–4655

    Article  PubMed  CAS  Google Scholar 

  69. Hogarty MD, Liu X, Thompson PM, White PS, Sulman EP, Maris JM, Brodeur GM (2000) BIN1 inhibits colony formation and induces apoptosis in neuroblastoma cell lines with MYCN amplification. Med Pediatr Oncol 35:559–562

    Article  PubMed  CAS  Google Scholar 

  70. Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, Hammond D (1985) Association of multiple copies of the N-Myc oncogene with rapid progression of neuroblastomas. New Engl J Med 313:1111–1116

    Article  PubMed  CAS  Google Scholar 

  71. Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM (1984) Amplification of N-Myc in untreated human neuroblastomas correlates with advanced disease stage. Science 224:1121–1124

    Article  PubMed  CAS  Google Scholar 

  72. Tajiri T, Liu XY, Thompson PM, Tanaka S, Suita S, Zhao HQ, Maris JM, Prendergast GC, Hogarty MD (2003) Expression of a MYCN-interacting isoform of the tumor suppressor BIN1 is reduced in neuroblastomas with unfavorable biological features. Clin Cancer Res 9:3345–3355

    PubMed  CAS  Google Scholar 

  73. Brabec V, Kasparkova J (2005) Modifications of DNA by platinum complexes. Relation to resistance of tumors to platinum antitumor drugs. Drug Resist Updat 8:131–146

    Article  PubMed  CAS  Google Scholar 

  74. Tanida S, Mizoshita T, Ozeki K, Tsukamoto H, Kamiya T, Kataoka H, Sakamuro D, Joh T (2012) Mechanisms of Cisplatin-Induced Apoptosis and of Cisplatin Sensitivity: Potential of BIN1 to Act as a Potent Predictor of Cisplatin Sensitivity in Gastric Cancer Treatment. Int J Surg Oncol 2012: 862879. doi:10.1155/2012/862879

  75. Prendergast G, MAJ C, Ramalingam A, Chang MY (2009) Bar the door: cancer suppression by amphiphysin-like genes. Biochemica et Biophysica Acta 1795:25–36

    CAS  Google Scholar 

  76. Claeys KG, Maisonobe T, Bohm J, Laporte J, Hezode M, Romero NB, Brochier G, Bitoun M, Carlier RY, Stojkovic T (2010) Phenotype of a patient with recessive centronuclear myopathy and a novel BIN1 mutation. Neurology 74:519–521

    Article  PubMed  CAS  Google Scholar 

  77. Romero NB, Bitoun M (2011) Centronuclear myopathies. Semin Pediatr Neurol 18:250–256

    Article  PubMed  Google Scholar 

  78. Bohm J, Yis U, Ortac R, Cakmakci H, Kurul SH, Dirik E, Laporte J (2010) Case report of intrafamilial variability in autosomal recessive centronuclear myopathy associated to a novel BIN1 stop mutation. Orphanet J Rare Dis 5: 35. doi:10.1186/1750-1172-5-35

  79. Bitoun M, Maugenre S, Jeannet PY, Lacene E, Ferrer X, Laforet P, Martin JJ, Laporte J, Lochmuller H, Beggs AH et al (2005) Mutations in dynamin 2 cause dominant centronuclear myopathy. Nat Genet 37:1207–1209

    Article  PubMed  CAS  Google Scholar 

  80. Tjondrokoesoemo A, Park KH, Ferrante C, Komazaki S, Lesniak S, Brotto M, Ko JK, Zhou J, Weisleder N, Ma J (2011) Disrupted membrane structure and intracellular Ca (2) (+) signaling in adult skeletal muscle with acute knockdown of Bin1. PLoS One 6: e25740. doi:10.1371/journal.pone.0025740

  81. Fernando P, Sandoz JS, Ding W, de Repentigny Y, Brunette S, Kelly JF, Kothary R, Megeney LA (2009) Bin1 SRC homology 3 domain acts as a scaffold for myofiber sarcomere assembly. J Biol Chem 284:27674–27686

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  82. Hong TT, Cogswell R, James CA, Kang G, Pullinger CR, Malloy MJ, Kane JP, Wojciak J, Calkins H, Scheinman MM et al (2012) Plasma BIN1 correlates with heart failure and predicts arrhythmia in patients with arrhythmogenic right ventricular cardiomyopathy. Heart Rhythm 9:961–967

    Article  PubMed Central  PubMed  Google Scholar 

  83. Asimaki A (2012) BIN1: a new biomarker to track ARVC? Heart rhythm 9:968–969

    Article  PubMed  Google Scholar 

  84. Hong TT, Smyth JW, Chu KY, Vogan JM, Fong TS, Jensen BC, Fang K, Halushka MK, Russell SD, Colecraft H et al (2012) BIN1 is reduced and Cav1.2 trafficking is impaired in human failing cardiomyocytes. Heart Rhythm 9:812–820

    Article  PubMed Central  PubMed  Google Scholar 

  85. Hong TT, Smyth JW, Gao D, Chu KY, Vogan JM, Fong TS, Jensen BC, Colecraft HM, Shaw RM (2010) BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLoS Biol 8. doi:10.1371/journal.pbio.1000312

  86. Seshadri S, Fitzpatrick AL, Ikram MA, DeStefano AL, Gudnason V, Boada M, Bis JC, Smith AV, Carassquillo MM, Lambert JC et al (2010) Genome-wide analysis of genetic loci associated with Alzheimer disease. Jama 303:1832–1840

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  87. Masoodi TA, Al Shammari SA, Al-Muammar MN, Alhamdan AA, Talluri VR (2013) Exploration of deleterious single nucleotide polymorphisms in late-onset Alzheimer disease susceptibility genes. Gene 512:429–437

    Article  PubMed  CAS  Google Scholar 

  88. Hu XL, Pickering E, Liu YC, Hall S, Fournier H, Katz E, Dechairo B, John S, Van Eerdewegh P, Soares H et al. (2011) Meta-analysis for genome-wide association study identifies multiple variants at the BIN1 locus associated with late-onset Alzheimer's disease. PLoS One 6. doi:10.1371/journal.pone.0016616

  89. Wijsman EM, Pankratz ND, Choi Y, Rothstein JH, Faber KM, Cheng R, Lee JH, Bird TD, Bennett DA, Diaz-Arrastia R et al (2011) Genome-wide association of familial late-onset Alzheimer’s disease replicates BIN1 and CLU and nominates CUGBP2 in interaction with APOE. Plos Genet 7. doi:10.1371/journal.pgen.1001308

  90. Carrasquillo MM, Belbin O, Hunter TA, Ma L, Bisceglio GD, Zou FG, Crook JE, Pankratz VS, Sando SB, Aasly JO et al (2011) Replication of BIN1 association with Alzheimer’s disease and evaluation of genetic interactions. J Alzheimers Dis 24:751–758

    PubMed Central  PubMed  CAS  Google Scholar 

  91. Lambert JC, Zelenika D, Hiltunen M, Chouraki V, Combarros O, Bullido MJ, Tognoni G, Fievet N, Boland A, Arosio B et al (2011) Evidence of the association of BIN1 and PICALM with the AD risk in contrasting European populations. Neurobiol Aging 32. doi:10.1016/j.neurobiolaging.2010.11.022

  92. Lee JH, Cheng R, Barral S, Reitz C, Medrano M, Lantigua R, Jimenez-Velazquez IZ, Rogaeva E, George-Hyslop PHS, Mayeux R (2011) Identification of novel loci for Alzheimer disease and replication of CLU, PICALM, and BIN1 in Caribbean Hispanic individuals. Arch Neurol-Chicago 68:320–328

    PubMed Central  PubMed  Google Scholar 

  93. Lambert JC, Ibrahim-Verbaas CA, Harold D, Naj AC, Sims R, Bellenguez C, Jun G, Destefano AL, Bis JC, Beecham GW et al (2013) Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer’s disease. Nat Genet 45:1452–1458

    Article  CAS  Google Scholar 

  94. Schaeffer EL, Figueiro M, Gattaz WF (2011) Insights into Alzheimer disease pathogenesis from studies in transgenic animal models. Clinics 66:45–54

    Article  PubMed Central  PubMed  Google Scholar 

  95. Tan MS, Yu JT, Tan L (2013) Bridging integrator 1 (BIN1): form, function, and Alzheimer’s disease. Trends Mol Med 10:594–603

    Article  CAS  Google Scholar 

  96. Raj T, Shulman JM, Keenan BT, Chibnik LB, Evans DA, Bennett DA, Stranger BE, De Jager PL (2012) Alzheimer disease susceptibility loci: evidence for a protein network under natural selection. Am J Hum Genet 90:720–726

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  97. Morel E, Chamoun Z, Lasiecka ZM, Chan RB, Williamson RL, Vetanovetz C, Dall’Armi C, Simoes S, Du Jour KSP, McCabe BD et al (2013) Phosphatidylinositol-3-phosphate regulates sorting and processing of amyloid precursor protein through the endosomal system. Nat Commun 4:2250

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  98. Hnia K, Vaccari I, Bolino A, Laporte J (2012) Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology. Trends Mol Med 18:317–327

    Article  PubMed  CAS  Google Scholar 

  99. Ramjaun AR, Philie J, de Heuvel E, McPherson PS (1999) The N terminus of amphiphysin II mediates dimerization and plasma membrane targeting. J Biol Chem 274:19785–19791

    Article  PubMed  CAS  Google Scholar 

  100. Huser S, Suri G, Crottet P, Spiess M (2013) Interaction of amphiphysins with AP-1 clathrin adaptors at the membrane. Biochem J 450:73–83

    Article  PubMed  CAS  Google Scholar 

  101. Grabs D, Slepnev VI, Zhou SY, David C, Lynch M, Cantley LC, DeCamilli P (1997) The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J Biol Chem 272:13419–13425

    Article  PubMed  CAS  Google Scholar 

  102. Dong J, Misselwitz R, Welfle H, Westermann P (2000) Expression and purification of dynamin II domains and initial studies on structure and function. Protein Expr Purif 20:314–323

    Article  PubMed  CAS  Google Scholar 

  103. Kajiho H, Saito K, Tsujita K, Kontani K, Araki Y, Kurosu H, Katada T (2003) RIN3: a novel Rab5 GEF interacting with amphiphysin II involved in the early endocytic pathway. J Cell Sci 116:4159–4168

    Article  PubMed  CAS  Google Scholar 

  104. Leprince C, Le Scolan E, Meunier B, Fraisier V, Brandon N, De Gunzburg J, Camonis J (2003) Sorting nexin 4 and amphiphysin 2, a new partnership between endocytosis and intracellular trafficking. J Cell Sci 116:1937–1948

    Article  PubMed  CAS  Google Scholar 

  105. Lee C, Kim SR, Chung JK, Frohman MA, Kilimann MW, Rhee SG (2000) Inhibition of phospholipase D by amphiphysins. J Biol Chem 275:18751–18758

    Article  PubMed  CAS  Google Scholar 

  106. Cousin MA, Tan TC, Robinson PJ (2001) Protein phosphorylation is required for endocytosis in nerve terminals: potential role for the dephosphins dynamin I and synaptojanin, but not AP180 or amphiphysin. J Neurochem 76:105–116

    Article  PubMed  CAS  Google Scholar 

  107. Wixler V, Laplantine E, Geerts D, Sonnenberg A, Petersohn D, Eckes B, Paulsson M, Aumailley M (1999) Identification of novel interaction partners for the conserved membrane proximal region of alpha-integrin cytoplasmic domains. FEBS Lett 445:351–355

    Article  PubMed  CAS  Google Scholar 

  108. Messina S, Onofri F, Bongiorno-Borbone L, Giovedi S, Valtorta F, Girault JA, Benfenati F (2003) Specific interactions of neuronal focal adhesion kinase isoforms with Src kinases and amphiphysin. J Neurochem 84:253–265

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We apologize to colleagues whose work was not cited because of space limitations. A.P. is supported by Association Francaise contre les Myopathies, B.S.C. by a fellowship from Fondation Recherche Médicale and J.L. by the Institut National de la Santé et de la Recherche Médicale and by a translational research stipend with Assistance Publique–Hôpitaux de Paris.

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The authors declare that they have no conflict of interests.

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Authors and Affiliations

  1. IGBMC (Institut de Génétique et de Biologie Moléculaire et Cellulaire), Illkirch, France

    Ivana Prokic, Belinda S. Cowling & Jocelyn Laporte

  2. Inserm, U964, Illkirch, France

    Ivana Prokic, Belinda S. Cowling & Jocelyn Laporte

  3. CNRS, UMR7104, Illkirch, France

    Ivana Prokic, Belinda S. Cowling & Jocelyn Laporte

  4. Université de Strasbourg, Illkirch, France

    Ivana Prokic, Belinda S. Cowling & Jocelyn Laporte

  5. Collège de France, chaire de génétique humaine, Illkirch, France

    Ivana Prokic, Belinda S. Cowling & Jocelyn Laporte

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  1. Ivana Prokic
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  2. Belinda S. Cowling
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  3. Jocelyn Laporte
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Correspondence to Jocelyn Laporte.

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Prokic, I., Cowling, B.S. & Laporte, J. Amphiphysin 2 (BIN1) in physiology and diseases. J Mol Med 92, 453–463 (2014). https://doi.org/10.1007/s00109-014-1138-1

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  • DOI: https://doi.org/10.1007/s00109-014-1138-1

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