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AP180 N-Terminal Homology (ANTH) and Epsin N-Terminal Homology (ENTH) Domains: Physiological Functions and Involvement in Disease

  • Sho Takatori
  • Taisuke Tomita
Chapter
Part of the Advances in Experimental Medicine and Biology book series

Abstract

The AP180 N-terminal homology (ANTH) and Epsin N-terminal homology (ENTH) domains are crucially involved in membrane budding processes. All the ANTH/ENTH-containing proteins share the phosphoinositide-binding activity and can interact with clathrin or its related proteins via multiple binding motifs. Their function also include promotion of clathrin assembly, induction of membrane curvature, and recruitment of various effector proteins, such as those involved in membrane fission. Furthermore, they play a role in the sorting of specific cargo proteins, thereby enabling the cargos to be accurately transported and function at their appropriate locations. As the structural bases underlying these functions are clarified, contrary to their apparent similarity, the mechanisms by which these proteins recognize lipids and proteins have unexpectedly been found to differ from each other. In addition, studies using knockout mice have suggested that their physiological roles may be more complicated than merely supporting membrane budding processes. In this chapter, we review the current knowledge on the biochemical features of ANTH/ENTH domains, their functions predicted from the phenotypes of animals deficient in these domain-containing proteins, and recent findings on the structural basis enabling specific recognition of their ligands. We also discuss the association of these domains with human diseases. Here we focus on CALM, a protein containing an ANTH domain, which is implicated in the pathogenesis of blood cancers and Alzheimer disease, and discuss how alteration of CALM function is involved in these diseases.

Keywords

Endocytosis Clathrin Phosphoinositide ANTH ENTH Alzheimer disease 

Notes

Acknowledgements

This work was supported in part by Grant-in-Aid for Young Scientists (B) from the Japan Society for the Promotion of Science (JSPS) [17 K15446 to S.T.], Grants-in-Aid for Scientific Research (A) from the Japan Society for the Promotion of Science [15H02492 to T.T.], by the Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) from the Japan Agency for Medical Research and Development (AMED) [17dm0207014h0004 to T.T.] and Sunbor Grant from the Suntory Foundation for Life Sciences [to S.T.].

Conflicts of Interest

None declared.

References

  1. Ando K, Tomimura K, Sazdovitch V et al (2016) Level of PICALM, a key component of clathrin-mediated endocytosis, is correlated with levels of phosphotau and autophagy-related proteins and is associated with tau inclusions in AD, PSP and pick disease. Neurobiol Dis 94:32–43.  https://doi.org/10.1016/j.nbd.2016.05.017CrossRefGoogle Scholar
  2. Baig S, Joseph SA, Tayler H et al (2010) Distribution and expression of picalm in Alzheimer disease. J Neuropathol Exp Neurol 69:1071–1077.  https://doi.org/10.1097/NEN.0b013e3181f52e01CrossRefGoogle Scholar
  3. Barriere H, Nemes C, Lechardeur D et al (2006) Molecular basis of oligoubiquitin-dependent internalization of membrane proteins in mammalian cells. Traffic 7:282–297.  https://doi.org/10.1111/j.1600-0854.2006.00384.xCrossRefGoogle Scholar
  4. Biffi A, Anderson CD, Desikan RS et al (2010) Genetic variation and neuroimaging measures in Alzheimer disease. Arch Neurol 67:677.  https://doi.org/10.1001/archneurol.2010.108CrossRefGoogle Scholar
  5. Borner GHH, Antrobus R, Hirst J et al (2012) Multivariate proteomic profiling identifies novel accessory proteins of coated vesicles. J Cell Biol 197:141–160.  https://doi.org/10.1083/jcb.201111049CrossRefGoogle Scholar
  6. Boucrot E, Pick A, Çamdere G et al (2012) Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149:124–136.  https://doi.org/10.1016/j.cell.2012.01.047CrossRefGoogle Scholar
  7. Boucrot E, Ferreira APA, Almeida-Souza L et al (2015) Endophilin marks and controls a clathrin-independent endocytic pathway. Nature 517:460–465.  https://doi.org/10.1038/nature14067CrossRefGoogle Scholar
  8. Boulant S, Kural C, Zeeh J-C et al (2011) Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13:1124–1131.  https://doi.org/10.1038/ncb2307CrossRefGoogle Scholar
  9. Bradley SV, Hyun TS, Oravecz-Wilson KI et al (2007) Degenerative phenotypes caused by the combined deficiency of murine HIP1 and HIP1r are rescued by human HIP1. Hum Mol Genet 16:1279–1292.  https://doi.org/10.1093/hmg/ddm076CrossRefGoogle Scholar
  10. Brett TJ, Legendre-Guillemin V, McPherson PS, Fremont DH (2006) Structural definition of the F-actin-binding THATCH domain from HIP1R. Nat Struct Mol Biol 13:121–130.  https://doi.org/10.1038/nsmb1043CrossRefGoogle Scholar
  11. Burston HE, Maldonado-Báez L, Davey M et al (2009) Regulators of yeast endocytosis identified by systematic quantitative analysis. J Cell Biol 185:1097–1110.  https://doi.org/10.1083/jcb.200811116CrossRefGoogle Scholar
  12. Buss F, Arden SD, Lindsay M et al (2001) Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J 20:3676–3684.  https://doi.org/10.1093/emboj/20.14.3676CrossRefGoogle Scholar
  13. Carrasquillo MM, Belbin O, Hunter TA et al (2010) Replication of CLU, CR1, and PICALM associations with Alzheimer disease. Arch Neurol 67:961–964.  https://doi.org/10.1001/archneurol.2010.147CrossRefGoogle Scholar
  14. Chen H, Fre S, Slepnev VI et al (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394:793–797.  https://doi.org/10.1038/29555CrossRefGoogle Scholar
  15. Chen H, Ko G, Zatti A et al (2009) Embryonic arrest at midgestation and disruption of Notch signaling produced by the absence of both epsin 1 and epsin 2 in mice. Proc Natl Acad Sci U S A 106:13838–13843.  https://doi.org/10.1073/pnas.0907008106CrossRefGoogle Scholar
  16. Cocucci E, Aguet F, Boulant S, Kirchhausen T (2012) The first five seconds in the life of a clathrin-coated pit. Cell 150:495–507.  https://doi.org/10.1016/j.cell.2012.05.047CrossRefGoogle Scholar
  17. Conway AE, Scotland PB, Lavau CP, Wechsler DS (2013) A CALM-derived nuclear export signal is essential for CALM-AF10-mediated leukemogenesis. Blood 121:4758–4768.  https://doi.org/10.1182/blood-2012-06-435792CrossRefGoogle Scholar
  18. Corneveaux JJ, Myers AJ, Allen AN et al (2010) Association of CR1, CLU and PICALM with Alzheimer’s disease in a cohort of clinically characterized and neuropathologically verified individuals. Hum Mol Genet 19:3295–3301.  https://doi.org/10.1093/hmg/ddq221CrossRefGoogle Scholar
  19. De Craene J-O, Ripp R, Lecompte O et al (2012) Evolutionary analysis of the ENTH/ANTH/VHS protein superfamily reveals a coevolution between membrane trafficking and metabolism. BMC Genomics 13:297.  https://doi.org/10.1186/1471-2164-13-297CrossRefGoogle Scholar
  20. Dittman JS, Kaplan JM (2006) Factors regulating the abundance and localization of synaptobrevin in the plasma membrane. Proc Natl Acad Sci 103:11399–11404.  https://doi.org/10.1073/pnas.0600784103CrossRefGoogle Scholar
  21. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902.  https://doi.org/10.1146/annurev.biochem.78.081307.110540CrossRefGoogle Scholar
  22. Dreyling MH, Martinez-Climent JA, Zheng M et al (1996) The t(10;11)(p13;q14) in the U937 cell line results in the fusion of the AF10 gene and CALM, encoding a new member of the AP-3 clathrin assembly protein family. Proc Natl Acad Sci U S A 93:4804–4809Google Scholar
  23. Engqvist-Goldstein AE, Kessels MM, Chopra VS et al (1999) An actin-binding protein of the Sla2/Huntingtin interacting protein 1 family is a novel component of clathrin-coated pits and vesicles. J Cell Biol 147:1503–1518Google Scholar
  24. Engqvist-Goldstein AEY, Zhang CX, Carreno S et al (2004) RNAi-mediated Hip1R silencing results in stable association between the endocytic machinery and the actin assembly machinery. Mol Biol Cell 15:1666–1679.  https://doi.org/10.1091/mbc.E03-09-0639CrossRefGoogle Scholar
  25. Ford MG, Pearse BM, Higgins MK et al (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291:1051–1055.  https://doi.org/10.1126/science.291.5506.1051CrossRefGoogle Scholar
  26. Ford MGJ, Mills IG, Peter BJ et al (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419:361–366.  https://doi.org/10.1038/nature01020CrossRefGoogle Scholar
  27. Furney SJ, Simmons A, Breen G et al (2011) Genome-wide association with MRI atrophy measures as a quantitative trait locus for Alzheimer’s disease. Mol Psychiatry 16:1130–1138.  https://doi.org/10.1038/mp.2010.123CrossRefGoogle Scholar
  28. Furuta N, Fujita N, Noda T et al (2010) Combinational soluble N-Ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical Autophagosomes with lysosomes. Mol Biol Cell 21:1001–1010.  https://doi.org/10.1091/mbc.E09-08-0693CrossRefGoogle Scholar
  29. Gleisner M, Kroppen B, Fricke C et al (2016) Epsin N-terminal homology domain (ENTH) activity as a function of membrane tension. J Biol Chem 291:19953–19961.  https://doi.org/10.1074/jbc.M116.731612CrossRefGoogle Scholar
  30. Hao W, Tan Z, Prasad K et al (1997) Regulation of AP-3 function by inositides. Identification of phosphatidylinositol 3,4,5-trisphosphate as a potent ligand. J Biol Chem 272:6393–6398Google Scholar
  31. Hao W, Luo Z, Zheng L et al (1999) AP180 and AP-2 interact directly in a complex that cooperatively assembles clathrin. J Biol Chem 274:22785–22794Google Scholar
  32. Harold D, Abraham R, Hollingworth P et al (2009) Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer’s disease. Nat Genet 41:1088–1093.  https://doi.org/10.1038/ng.440CrossRefGoogle Scholar
  33. Hawryluk MJ, Keyel PA, Mishra SK et al (2006) Epsin 1 is a polyubiquitin-selective clathrin-associated sorting protein. Traffic 7:262–281.  https://doi.org/10.1111/j.1600-0854.2006.00383.xCrossRefGoogle Scholar
  34. Hayashi I, Takatori S, Urano Y et al (2012) Neutralization of the γ-secretase activity by monoclonal antibody against extracellular domain of nicastrin. Oncogene 31:787–798.  https://doi.org/10.1038/onc.2011.265CrossRefGoogle Scholar
  35. Henne WM, Boucrot E, Meinecke M et al (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328:1281–1284.  https://doi.org/10.1126/science.1188462CrossRefGoogle Scholar
  36. Hirst J, Motley A, Harasaki K et al (2003) EpsinR: an ENTH domain-containing protein that interacts with AP-1. Mol Biol Cell 14:625–641.  https://doi.org/10.1091/mbc.E02-09-0552CrossRefGoogle Scholar
  37. Hirst J, Miller SE, Taylor MJ et al (2004) EpsinR is an adaptor for the SNARE protein Vti1b. Mol Biol Cell 15:5593–5602.  https://doi.org/10.1091/mbc.E04-06-0468CrossRefGoogle Scholar
  38. Hom RA, Vora M, Regner M et al (2007) pH-dependent binding of the Epsin ENTH domain and the AP180 ANTH domain to PI(4,5)P2-containing bilayers. J Mol Biol 373:412–423.  https://doi.org/10.1016/j.jmb.2007.08.016CrossRefGoogle Scholar
  39. Huang KM, D’Hondt K, Riezman H, Lemmon SK (1999) Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J 18:3897–3908.  https://doi.org/10.1093/emboj/18.14.3897CrossRefGoogle Scholar
  40. Hyman J, Chen H, Di Fiore PP et al (2000) Epsin 1 undergoes nucleocytosolic shuttling and its eps15 interactor NH(2)-terminal homology (ENTH) domain, structurally similar to Armadillo and HEAT repeats, interacts with the transcription factor promyelocytic leukemia Zn(2)+ finger protein (PLZF). J Cell Biol 149:537–546Google Scholar
  41. Hyun TS, Rao DS, Saint-Dic D et al (2004) HIP1 and HIP1r stabilize receptor tyrosine kinases and bind 3-Phosphoinositides via Epsin N-terminal homology domains. J Biol Chem 279:14294–14306.  https://doi.org/10.1074/jbc.M312645200CrossRefGoogle Scholar
  42. Ishikawa Y, Maeda M, Pasham M et al (2015) Role of the clathrin adaptor PICALM in normal hematopoiesis and polycythemia vera pathophysiology. Haematologica 100:439–451.  https://doi.org/10.3324/haematol.2014.119537CrossRefGoogle Scholar
  43. Itakura E, Kishi-Itakura C, Mizushima N (2012) The hairpin-type tail-anchored SNARE Syntaxin 17 targets to Autophagosomes for fusion with endosomes/lysosomes. Cell 151:1256–1269.  https://doi.org/10.1016/j.cell.2012.11.001CrossRefGoogle Scholar
  44. Itoh T, De Camilli P (2006) BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim Biophys Acta 1761:897–912.  https://doi.org/10.1016/j.bbalip.2006.06.015CrossRefGoogle Scholar
  45. Itoh T, Koshiba S, Kigawa T et al (2001) Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291:1047–1051.  https://doi.org/10.1126/science.291.5506.1047CrossRefGoogle Scholar
  46. Jackson LP, Kelly BT, McCoy AJ et al (2010) A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141:1220–1229.  https://doi.org/10.1016/j.cell.2010.05.006CrossRefGoogle Scholar
  47. Jones EL, Mok K, Hanney M et al (2013) Evidence that PICALM affects age at onset of Alzheimer’s dementia in Down syndrome. Neurobiol Aging 34:2441.e1–2441.e5.  https://doi.org/10.1016/j.neurobiolaging.2013.03.018CrossRefGoogle Scholar
  48. Jonsson T, Atwal JK, Steinberg S et al (2012) A mutation in APP protects against Alzheimer’s disease and age-related cognitive decline. Nature 488:96–99.  https://doi.org/10.1038/nature11283CrossRefGoogle Scholar
  49. Kaksonen M, Roux A (2018) Mechanisms of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 19:313.  https://doi.org/10.1038/nrm.2017.132CrossRefGoogle Scholar
  50. Kalthoff C, Alves J, Urbanke C et al (2002) Unusual structural organization of the endocytic proteins AP180 and epsin 1. J Biol Chem 277:8209–8216.  https://doi.org/10.1074/jbc.M111587200CrossRefGoogle Scholar
  51. Kanatsu K, Morohashi Y, Suzuki M et al (2014) Decreased CALM expression reduces Aβ42 to total Aβ ratio through clathrin-mediated endocytosis of γ-secretase. Nat Commun 5:3386.  https://doi.org/10.1038/ncomms4386CrossRefGoogle Scholar
  52. Kanatsu K, Hori Y, Takatori S et al (2016) Partial loss of CALM function reduces Aβ42 production and amyloid deposition in vivo. Hum Mol Genet 25:3988–3997.  https://doi.org/10.1093/hmg/ddw239CrossRefGoogle Scholar
  53. Kauwe JSK, Cruchaga C, Karch CM et al (2011) Fine mapping of genetic variants in BIN1, CLU, CR1 and PICALM for association with cerebrospinal fluid biomarkers for Alzheimer’s disease. PLoS One 6:e15918.  https://doi.org/10.1371/journal.pone.0015918CrossRefGoogle Scholar
  54. Kay BK, Yamabhai M, Wendland B, Emr SD (1999) Identification of a novel domain shared by putative components of the endocytic and cytoskeletal machinery. Protein Sci 8:435–438.  https://doi.org/10.1110/ps.8.2.435CrossRefGoogle Scholar
  55. Kovall RA, Gebelein B, Sprinzak D, Kopan R (2017) The canonical notch signaling pathway: structural and biochemical insights into shape, sugar, and force. Dev Cell 41:228–241.  https://doi.org/10.1016/j.devcel.2017.04.001CrossRefGoogle Scholar
  56. Lambert J-C, Heath S, Even G et al (2009) Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer’s disease. Nat Genet 41:1094–1099.  https://doi.org/10.1038/ng.439CrossRefGoogle Scholar
  57. Lambert J-C, Zelenika D, Hiltunen M et al (2011) Evidence of the association of BIN1 and PICALM with the AD risk in contrasting European populations. Neurobiol Aging 32:756.e11–7756.15.  https://doi.org/10.1016/j.neurobiolaging.2010.11.022CrossRefGoogle Scholar
  58. Loerke D, Mettlen M, Yarar D et al (2009) Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7:e1000057.  https://doi.org/10.1371/journal.pbio.1000057CrossRefGoogle Scholar
  59. Ma L, Umasankar PK, Wrobel AG et al (2016) Transient Fcho1/2⋅Eps15/R⋅AP-2 nanoclusters prime the AP-2 clathrin adaptor for cargo binding. Dev Cell 37(5):428–443.  https://doi.org/10.1016/j.devcel.2016.05.003CrossRefGoogle Scholar
  60. Meinecke M, Boucrot E, Camdere G et al (2013) Cooperative recruitment of dynamin and BIN/amphiphysin/Rvs (BAR) domain-containing proteins leads to GTP-dependent membrane scission. J Biol Chem 288:6651–6661.  https://doi.org/10.1074/jbc.M112.444869CrossRefGoogle Scholar
  61. Meloty-Kapella L, Shergill B, Kuon J et al (2012) Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins, and actin. Dev Cell 22:1299–1312.  https://doi.org/10.1016/j.devcel.2012.04.005CrossRefGoogle Scholar
  62. Melville SA, Buros J, Parrado AR et al (2012) Multiple loci influencing hippocampal degeneration identified by genome scan. Ann Neurol 72:65–75.  https://doi.org/10.1002/ana.23644CrossRefGoogle Scholar
  63. Messa M, Fernández-Busnadiego R, Sun EW et al (2014) Epsin deficiency impairs endocytosis by stalling the actin-dependent invagination of endocytic clathrin-coated pits. elife 3:e03311.  https://doi.org/10.7554/eLife.03311CrossRefGoogle Scholar
  64. Metzler M, Li B, Gan L et al (2003) Disruption of the endocytic protein HIP1 results in neurological deficits and decreased AMPA receptor trafficking. EMBO J 22:3254–3266.  https://doi.org/10.1093/emboj/cdg334CrossRefGoogle Scholar
  65. Meyerholz A, Hinrichsen L, Esk P et al (2005) Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic 6(12):1225–1234.  https://doi.org/10.1111/j.1600-0854.2005.00355.xCrossRefGoogle Scholar
  66. Miller SE, Collins BM, McCoy AJ et al (2007) A SNARE-adaptor interaction is a new mode of cargo recognition in clathrin-coated vesicles. Nature 450:570–574.  https://doi.org/10.1038/nature06353CrossRefGoogle Scholar
  67. Miller SE, Sahlender DA, Graham SC et al (2011) The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147:1118–1131.  https://doi.org/10.1016/j.cell.2011.10.038CrossRefGoogle Scholar
  68. Miller SE, Mathiasen S, Bright NA et al (2015) CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev Cell 33:163–175.  https://doi.org/10.1016/j.devcel.2015.03.002CrossRefGoogle Scholar
  69. Mills IG, Praefcke GJK, Vallis Y et al (2003) EpsinR: an AP1/clathrin interacting protein involved in vesicle trafficking. J Cell Biol 160:213–222.  https://doi.org/10.1083/jcb.200208023CrossRefGoogle Scholar
  70. Moreau K, Fleming A, Imarisio S et al (2014) PICALM modulates autophagy activity and tau accumulation. Nat Commun 5:4998.  https://doi.org/10.1038/ncomms5998CrossRefGoogle Scholar
  71. Morgan JR, Prasad K, Jin S et al (2003) Eps15 homology domain-NPF motif interactions regulate clathrin coat assembly during synaptic vesicle recycling. J Biol Chem 278:33583–33592.  https://doi.org/10.1074/jbc.M304346200CrossRefGoogle Scholar
  72. Naj AC, Jun G, Beecham GW et al (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer’s disease. Nat Genet 43:436–441.  https://doi.org/10.1038/ng.801CrossRefGoogle Scholar
  73. Naj AC, Jun G, Reitz C et al (2014) Effects of multiple genetic loci on age at onset in late-onset Alzheimer disease. JAMA Neurol 71:1394.  https://doi.org/10.1001/jamaneurol.2014.1491CrossRefGoogle Scholar
  74. Nonet ML, Holgado AM, Brewer F et al (1999) UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell 10:2343–2360Google Scholar
  75. Norris FA, Ungewickell E, Majerus PW (1995) Inositol hexakisphosphate binds to clathrin assembly protein 3 (AP-3/AP180) and inhibits clathrin cage assembly in vitro. J Biol Chem 270:214–217Google Scholar
  76. Okada Y, Feng Q, Lin Y et al (2005) hDOT1L links histone methylation to leukemogenesis. Cell 121:167–178.  https://doi.org/10.1016/j.cell.2005.02.020CrossRefGoogle Scholar
  77. Okada Y, Jiang Q, Lemieux M et al (2006) Leukaemic transformation by CALM–AF10 involves upregulation of Hoxa5 by hDOT1L. Nat Cell Biol 8:1017–1024.  https://doi.org/10.1038/ncb1464CrossRefGoogle Scholar
  78. Oravecz-Wilson KI, Kiel MJ, Li L et al (2004) Huntingtin interacting protein 1 mutations lead to abnormal hematopoiesis, spinal defects and cataracts. Hum Mol Genet 13:851–867.  https://doi.org/10.1093/hmg/ddh102CrossRefGoogle Scholar
  79. Overstreet E, Chen X, Wendland B, Fischer JA (2003) Either part of a Drosophila epsin protein, divided after the ENTH domain, functions in endocytosis of delta in the developing eye. Curr Biol 13:854–860Google Scholar
  80. Overstreet E, Fitch E, Fischer JA (2004) Fat facets and liquid facets promote delta endocytosis and delta signaling in the signaling cells. Development 131:5355–5366.  https://doi.org/10.1242/dev.01434CrossRefGoogle Scholar
  81. Parikh I, Fardo DW, Estus S (2014) Genetics of PICALM expression and Alzheimer’s disease. PLoS One 9:e91242.  https://doi.org/10.1371/journal.pone.0091242CrossRefGoogle Scholar
  82. Pimm J, McQuillin A, Thirumalai S et al (2005) The epsin 4 gene on chromosome 5q, which encodes the clathrin-associated protein Enthoprotin, is involved in the genetic susceptibility to schizophrenia. Am J Hum Genet 76:902–907.  https://doi.org/10.1086/430095CrossRefGoogle Scholar
  83. Ponomareva NV, Andreeva TV, Protasova MS et al (2017) Quantitative EEG during normal aging: association with the Alzheimer’s disease genetic risk variant in PICALM gene. Neurobiol Aging 51:177.e1–177.e8.  https://doi.org/10.1016/j.neurobiolaging.2016.12.010CrossRefGoogle Scholar
  84. Posor Y, Eichhorn-Gruenig M, Puchkov D et al (2013) Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499:233–237.  https://doi.org/10.1038/nature12360CrossRefGoogle Scholar
  85. Prasad K, Lippoldt RE (1988) Molecular characterization of the AP180 coated vesicle assembly protein. Biochemistry 27:6098–6104Google Scholar
  86. Puri C, Renna M, Bento CF et al (2013) Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154:1285–1299.  https://doi.org/10.1016/j.cell.2013.08.044CrossRefGoogle Scholar
  87. Rao DS, Chang JC, Kumar PD et al (2001) Huntingtin interacting protein 1 is a clathrin coat binding protein required for differentiation of late spermatogenic progenitors. Mol Cell Biol 21:7796–7806.  https://doi.org/10.1128/MCB.21.22.7796-7806.2001CrossRefGoogle Scholar
  88. Robinson MS (2015) Forty years of clathrin-coated vesicles. Traffic 16:1210–1238.  https://doi.org/10.1111/tra.12335CrossRefGoogle Scholar
  89. Rosenthal JA, Chen H, Slepnev VI et al (1999) The epsins define a family of proteins that interact with components of the clathrin coat and contain a new protein module. J Biol Chem 274:33959–33965.  https://doi.org/10.1074/jbc.274.48.33959CrossRefGoogle Scholar
  90. Sato Y, Yoshikawa A, Mimura H et al (2009) Structural basis for speci c recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J 28:1–8.  https://doi.org/10.1038/emboj.2009.160CrossRefGoogle Scholar
  91. Schjeide B-MM, Schnack C, Lambert J-C et al (2011) The role of clusterin, complement receptor 1, and phosphatidylinositol binding clathrin assembly protein in Alzheimer disease risk and cerebrospinal fluid biomarker levels. Arch Gen Psychiatry 68:207.  https://doi.org/10.1001/archgenpsychiatry.2010.196CrossRefGoogle Scholar
  92. Seshadri S, Fitzpatrick AL, Ikram MA et al (2010) Genome-wide analysis of genetic loci associated with Alzheimer disease. JAMA 303:1832–1840.  https://doi.org/10.1001/jama.2010.574CrossRefGoogle Scholar
  93. Sevigny J, Chiao P, Bussière T et al (2016) The antibody aducanumab reduces Aβ plaques in Alzheimer’s disease. Nature 537:50–56.  https://doi.org/10.1038/nature19323CrossRefGoogle Scholar
  94. Sims JJ, Cohen RE (2009) Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of Rap80. Mol Cell 33:775–783.  https://doi.org/10.1016/j.molcel.2009.02.011CrossRefGoogle Scholar
  95. Skruzny M, Desfosses A, Skruzny M et al (2015) An organized co-assembly of clathrin adaptors is essential for endocytosis article an organized co-assembly of clathrin adaptors is essential for endocytosis. Dev Cell 33:150–162.  https://doi.org/10.1016/j.devcel.2015.02.023CrossRefGoogle Scholar
  96. Stachowiak JC, Schmid EM, Ryan CJ et al (2012) Membrane bending by protein–protein crowding. Nat Cell Biol 14:944–949.  https://doi.org/10.1038/ncb2561CrossRefGoogle Scholar
  97. Stahelin RV, Long F, Peter BJ et al (2003) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J Biol Chem 278:28993–28999.  https://doi.org/10.1074/jbc.M302865200CrossRefGoogle Scholar
  98. Stephenson NL, Avis JM (2012) Direct observation of proteolytic cleavage at the S2 site upon forced unfolding of the notch negative regulatory region. Proc Natl Acad Sci U S A 109:E2757–E2765.  https://doi.org/10.1073/pnas.1205788109CrossRefGoogle Scholar
  99. Suzuki M, Tanaka H, Tanimura A et al (2012) The clathrin assembly protein PICALM is required for erythroid maturation and transferrin internalization in mice. PLoS One 7:e31854.  https://doi.org/10.1371/journal.pone.0031854CrossRefGoogle Scholar
  100. Suzuki M, Yamagata K, Shino M et al (2014) Nuclear export signal within CALM is necessary for CALM-AF10-induced leukemia. Cancer Sci 105:315–323.  https://doi.org/10.1111/cas.12347CrossRefGoogle Scholar
  101. Sweet RA, Seltman H, Emanuel JE et al (2012) Effect of Alzheimer’s disease risk genes on trajectories of cognitive function in the cardiovascular health study. Am J Psychiatry 169:954–962.  https://doi.org/10.1176/appi.ajp.2012.11121815CrossRefGoogle Scholar
  102. Sweitzer SM, Hinshaw JE (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell 93:1021–1029.  https://doi.org/10.1016/S0092-8674(00)81207-6CrossRefGoogle Scholar
  103. Takasugi N, Tomita T, Hayashi I et al (2003) The role of presenilin cofactors in the γ-secretase complex. Nature 422:438–441.  https://doi.org/10.1038/nature01506CrossRefGoogle Scholar
  104. Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediatedendocytosis. Nat Cell Biol 1:33–39.  https://doi.org/10.1038/9004CrossRefGoogle Scholar
  105. Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9:e1000604.  https://doi.org/10.1371/journal.pbio.1000604CrossRefGoogle Scholar
  106. Thambisetty M, An Y, Tanaka T (2013) Alzheimer’s disease risk genes and the age-at-onset phenotype. Neurobiol Aging 34:2696.e1–2692696.e5. doi:  https://doi.org/10.1016/j.neurobiolaging.2013.05.028CrossRefGoogle Scholar
  107. Thomas RS, Henson A, Gerrish A et al (2016) Decreasing the expression of PICALM reduces endocytosis and the activity of β-secretase: implications for Alzheimer’s disease. BMC Neurosci 17:50.  https://doi.org/10.1186/s12868-016-0288-1CrossRefGoogle Scholar
  108. Tian X, Hansen D, Schedl T, Skeath JB (2004) Epsin potentiates Notch pathway activity in Drosophila and C. elegans. Development 131:5807–5815.  https://doi.org/10.1242/dev.01459CrossRefGoogle Scholar
  109. Traub LM (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 10:583–596.  https://doi.org/10.1038/nrm2751CrossRefGoogle Scholar
  110. Vardarajan BN, Ghani M, Kahn A et al (2015) Rare coding mutations identified by sequencing of Alzheimer disease genome-wide association studies loci. Ann Neurol 78:487–498.  https://doi.org/10.1002/ana.24466CrossRefGoogle Scholar
  111. Waelter S, Scherzinger E, Hasenbank R et al (2001) The huntingtin interacting protein HIP1 is a clathrin and alpha-adaptin-binding protein involved in receptor-mediated endocytosis. Hum Mol Genet 10:1807–1817Google Scholar
  112. Wang W, Struhl G (2004) Drosophila epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131:5367–5380.  https://doi.org/10.1242/dev.01413CrossRefGoogle Scholar
  113. Wanker EE, Rovira C, Scherzinger E et al (1997) HIP-1: a huntingtin interacting protein isolated by the yeast two-hybrid system. Hum Mol Genet 6:487–495Google Scholar
  114. Wasiak S, Legendre-Guillemin V, Puertollano R et al (2002) Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics. J Cell Biol 158:855–862.  https://doi.org/10.1083/jcb.200205078CrossRefGoogle Scholar
  115. Wood LA, Royle SJ (2015) Zero tolerance: amphipathic helices in endocytosis. Dev Cell 33:119–120.  https://doi.org/10.1016/j.devcel.2015.04.007CrossRefGoogle Scholar
  116. Xiao Q, Gil S, Yan P et al (2012) Role of phosphatidylinositol clathrin assembly lymphoid-myeloid leukemia (PICALM) in intracellular amyloid precursor protein (APP) processing and amyloid plaque pathogenesis. J Biol Chem 287:21279–21289.  https://doi.org/10.1074/jbc.M111.338376CrossRefGoogle Scholar
  117. Xu W, Wang H-F, Tan L et al (2016) The impact of PICALM genetic variations on reserve capacity of posterior cingulate in AD continuum. Sci Rep 6:24480.  https://doi.org/10.1038/srep24480CrossRefGoogle Scholar
  118. Ye W, Ali N, Bembenek ME et al (1995) Inhibition of clathrin assembly by high affinity binding of specific inositol polyphosphates to the synapse-specific clathrin assembly protein AP-3. J Biol Chem 270:1564–1568Google Scholar
  119. Zhao Z, Sagare AP, Ma Q et al (2015) Central role for PICALM in amyloid-β blood-brain barrier transcytosis and clearance. Nat Neurosci 18:978–987.  https://doi.org/10.1038/nn.4025CrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Laboratory of Neuropathology and Neuroscience, Graduate School of Pharmaceutical SciencesThe University of TokyoTokyoJapan

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