CoChat
Sign Up
Cited by 44Cellular transport and secretionAutophagy in Disease and TherapyReceptor Mechanisms and Signaling

Endocytic Adaptor Proteins in Health and Disease: Lessons from Model Organisms and Human Mutations

Open access
Azarnia Tehran, Domenico, López-Hernández, Tania, Maritzen, Tanja·2019·Cells
DOI 10.3390/cells8111345PMC PMC6912373
Open this paper in CoChat — free accountOpen PDF

Abstract

Cells need to exchange material and information with their environment. This is largely achieved via cell-surface receptors which mediate processes ranging from nutrient uptake to signaling responses. Consequently, their surface levels have to be dynamically controlled. Endocytosis constitutes a powerful mechanism to regulate the surface proteome and to recycle vesicular transmembrane proteins that strand at the plasma membrane after exocytosis. For efficient internalization, the cargo proteins need to be linked to the endocytic machinery via adaptor proteins such as the heterotetrameric endocytic adaptor complex AP-2 and a variety of mostly monomeric endocytic adaptors. In line with the importance of endocytosis for nutrient uptake, cell signaling and neurotransmission, animal models and human mutations have revealed that defects in these adaptors are associated with several diseases ranging from metabolic disorders to encephalopathies. This review will discuss the physiological functions of the so far known adaptor proteins and will provide a comprehensive overview of their links to human diseases.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/cells8111345

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Clathrin-mediated endocytic protein AP2 modulates cell migration and invasion of pancreatic, ovarian, and melanoma cancer through CXCR2.

    “Clathrin-mediated endocytic protein AP2 modulates the cell migration and invasion of pancreatic, ovarian, and melanoma cancer through CXCR2 [111].”

    From Insights of Endocytosis Signaling in Health and Disease (2023) · cites this paper as [111]

    Section 2.1.3 says AP-2 could modulate tumor-cell migration and invasion, but describes a possible mechanism involving αTAT1 and microtubule acetylation, not CXCR2. The References section lists a study of AP2 and CXCR2-mediated cell migration; our copy does not connect that mechanism to invasion or to pancreatic, ovarian, and melanoma cancers. Page numbers are unavailable in our copy. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 370

  1. [1]Garcia C.K. Wilund K. Arca M. Zuliani G. Fellin R. Maioli M. Calandra S. Bertolini S. Cossu F. Grishin N. Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein Science 2001 292 1394 1398 10.1126/science.1060458 11326085 · DOI · Paper page
  2. [2]Tessneer K.L. Pasula S. Cai X. Dong Y. Liu X. Yu L. Hahn S. McManus J. Chen Y. Chang B. Endocytic adaptor protein epsin is elevated in prostate cancer and required for cancer progression ISRN Oncol. 2013 2013 420597 10.1155/2013/420597 23691361 PMC3649151 · DOI
  3. [3]Helbig I. Lopez-Hernandez T. Shor O. Galer P. Ganesan S. Pendziwiat M. Rademacher A. Ellis C.A. Humpfer N. Schwarz N. A Recurrent Missense Variant in AP2M1 Impairs Clathrin-Mediated Endocytosis and Causes Developmental and Epileptic Encephalopathy Am. J. Hum. Genet. 2019 104 1060 1072 10.1016/j.ajhg.2019.04.001 31104773 PMC6556875 · DOI
  4. [4]Kaksonen M. Roux A. Mechanisms of clathrin-mediated endocytosis Nat. Rev. Mol. Cell Biol. 2018 19 313 326 10.1038/nrm.2017.132 29410531 · DOI · Paper page
  5. [5]Letourneur F. Klausner R.D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains Cell 1992 69 1143 1157 10.1016/0092-8674(92)90636-Q 1535555 · DOI · Paper page
  6. [6]Pond L. Kuhn L.A. Teyton L. Schutze M.P. Tainer J.A. Jackson M.R. Peterson P.A. A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway J. Biol. Chem. 1995 270 19989 19997 10.1074/jbc.270.34.19989 7650016 · DOI
  7. [7]Kelly B.T. McCoy A.J. Spate K. Miller S.E. Evans P.R. Honing S. Owen D.J. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex Nature 2008 456 976 979 10.1038/nature07422 19140243 PMC4340503 · DOI
  8. [8]Traub L.M. Bonifacino J.S. Cargo recognition in clathrin-mediated endocytosis Cold Spring Harb. Perspect. Biol. 2013 5 a016790 10.1101/cshperspect.a016790 24186068 PMC3809577 · DOI
  9. [9]Ohno H. Fournier M.C. Poy G. Bonifacino J.S. Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains J. Biol. Chem. 1996 271 29009 29015 10.1074/jbc.271.46.29009 8910552 · DOI
  10. [10]Ohno H. Stewart J. Fournier M.C. Bosshart H. Rhee I. Miyatake S. Saito T. Gallusser A. Kirchhausen T. Bonifacino J.S. Interaction of tyrosine-based sorting signals with clathrin-associated proteins Science 1995 269 1872 1875 10.1126/science.7569928 7569928 · DOI
  11. [11]Jung N. Wienisch M. Gu M. Rand J.B. Muller S.L. Krause G. Jorgensen E.M. Klingauf J. Haucke V. Molecular basis of synaptic vesicle cargo recognition by the endocytic sorting adaptor stonin 2 J. Cell Biol. 2007 179 1497 1510 10.1083/jcb.200708107 18166656 PMC2373488 · DOI
  12. [12]Jung S. Maritzen T. Wichmann C. Jing Z. Neef A. Revelo N.H. Al-Moyed H. Meese S. Wojcik S.M. Panou I. Disruption of adaptor protein 2mu (AP-2mu) in cochlear hair cells impairs vesicle reloading of synaptic release sites and hearing EMBO J. 2015 34 2686 2702 10.15252/embj.201591885 26446278 PMC4641533 · DOI
  13. [13]Kelly B.T. Graham S.C. Liska N. Dannhauser P.N. Honing S. Ungewickell E.J. Owen D.J. Clathrin adaptors. AP2 controls clathrin polymerization with a membrane-activated switch Science 2014 345 459 463 10.1126/science.1254836 25061211 PMC4333214 · DOI
  14. [14]Idrissi F.Z. Blasco A. Espinal A. Geli M.I. Ultrastructural dynamics of proteins involved in endocytic budding Proc. Natl. Acad. Sci. USA 2012 109 E2587 E2594 10.1073/pnas.1202789109 22949647 PMC3465411 · DOI
  15. [15]Kukulski W. Schorb M. Kaksonen M. Briggs J.A. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography Cell 2012 150 508 520 10.1016/j.cell.2012.05.046 22863005 · DOI
  16. [16]Collins A. Warrington A. Taylor K.A. Svitkina T. Structural organization of the actin cytoskeleton at sites of clathrin-mediated endocytosis Curr. Biol. 2011 21 1167 1175 10.1016/j.cub.2011.05.048 21723126 PMC3143238 · DOI
  17. [17]Almeida-Souza L. Frank R.A.W. Garcia-Nafria J. Colussi A. Gunawardana N. Johnson C.M. Yu M. Howard G. Andrews B. Vallis Y. A Flat BAR Protein Promotes Actin Polymerization at the Base of Clathrin-Coated Pits Cell 2018 174 325 337.e14 10.1016/j.cell.2018.05.020 29887380 PMC6057269 · DOI
  18. [18]Antonny B. Burd C. De Camilli P. Chen E. Daumke O. Faelber K. Ford M. Frolov V.A. Frost A. Hinshaw J.E. Membrane fission by dynamin: What we know and what we need to know EMBO J. 2016 35 2270 2284 10.15252/embj.201694613 27670760 PMC5090216 · DOI
  19. [19]Bashkirov P.V. Akimov S.A. Evseev A.I. Schmid S.L. Zimmerberg J. Frolov V.A. GTPase cycle of dynamin is coupled to membrane squeeze and release, leading to spontaneous fission Cell 2008 135 1276 1286 10.1016/j.cell.2008.11.028 19084269 PMC2768395 · DOI
  20. [20]Ungewickell E. The 70-kd mammalian heat shock proteins are structurally and functionally related to the uncoating protein that releases clathrin triskelia from coated vesicles EMBO J. 1985 4 3385 3391 10.1002/j.1460-2075.1985.tb04094.x 2868889 PMC554674 · DOI
  21. [21]Newmyer S.L. Christensen A. Sever S. Auxilin-dynamin interactions link the uncoating ATPase chaperone machinery with vesicle formation Dev. Cell 2003 4 929 940 10.1016/S1534-5807(03)00157-6 12791276 · DOI
  22. [22]Sousa R. Lafer E.M. The role of molecular chaperones in clathrin mediated vesicular trafficking Front. Mol. Biosci. 2015 2 26 10.3389/fmolb.2015.00026 26042225 PMC4436892 · DOI
  23. [23]Kirchhausen T. Owen D. Harrison S.C. Molecular structure, function, and dynamics of clathrin-mediated membrane traffic Cold Spring Harb. Perspect. Biol. 2014 6 a016725 10.1101/cshperspect.a016725 24789820 PMC3996469 · DOI
  24. [24]McMahon H.T. Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis Nat. Rev. Mol. Cell Biol. 2011 12 517 533 10.1038/nrm3151 21779028 · DOI · Paper page
  25. [25]Maritzen T. Podufall J. Haucke V. Stonins--specialized adaptors for synaptic vesicle recycling and beyond? Traffic 2010 11 8 15 10.1111/j.1600-0854.2009.00971.x 19732400 · DOI
  26. [26]Reider A. Barker S.L. Mishra S.K. Im Y.J. Maldonado-Baez L. Hurley J.H. Traub L.M. Wendland B. Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation EMBO J. 2009 28 3103 3116 10.1038/emboj.2009.248 19713939 PMC2771086 · DOI
  27. [27]Maritzen T. Koo S.J. Haucke V. Turning CALM into excitement: AP180 and CALM in endocytosis and disease Biol. Cell 2012 104 588 602 10.1111/boc.201200008 22639918 · DOI
  28. [28]Gottfried I. Ehrlich M. Ashery U. The Sla2p/HIP1/HIP1R family: Similar structure, similar function in endocytosis? BioChem. Soc. Trans. 2010 38 187 191 10.1042/BST0380187 20074057 · DOI
  29. [29]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 2006 1761 897 912 10.1016/j.bbalip.2006.06.015 16938488 · DOI · Paper page
  30. [30]Traub L.M. A nanobody-based molecular toolkit provides new mechanistic insight into clathrin-coat initiation Elife 2019 8 10.7554/eLife.41768 PMC6524969 31038455 · DOI
  31. [31]Mishra S.K. Jha A. Steinhauser A.L. Kokoza V.A. Washabaugh C.H. Raikhel A.S. Foster W.A. Traub L.M. Internalization of LDL-receptor superfamily yolk-protein receptors during mosquito oogenesis involves transcriptional regulation of PTB-domain adaptors J. Cell Sci. 2008 121 1264 1274 10.1242/jcs.025833 18388314 · DOI
  32. [32]Maurer M.E. Cooper J.A. Endocytosis of megalin by visceral endoderm cells requires the Dab2 adaptor protein J. Cell Sci. 2005 118 5345 5355 10.1242/jcs.02650 16263760 · DOI
  33. [33]Gulino A. Di Marcotullio L. Screpanti I. The multiple functions of Numb Exp. Cell Res. 2010 316 900 906 10.1016/j.yexcr.2009.11.017 19944684 · DOI
  34. [34]Puca L. Brou C. Alpha-arrestins - new players in Notch and GPCR signaling pathways in mammals J. Cell Sci. 2014 127 1359 1367 10.1242/jcs.142539 24687185 · DOI
  35. [35]Pryor P.R. Jackson L. Gray S.R. Edeling M.A. Thompson A. Sanderson C.M. Evans P.R. Owen D.J. Luzio J.P. Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the ArfGAP Hrb Cell 2008 134 817 827 10.1016/j.cell.2008.07.023 18775314 PMC2648964 · DOI
  36. [36]Tosoni D. Puri C. Confalonieri S. Salcini A.E. De Camilli P. Tacchetti C. Di Fiore P.P. TTP specifically regulates the internalization of the transferrin receptor Cell 2005 123 875 888 10.1016/j.cell.2005.10.021 16325581 · DOI
  37. [37]Mudduluru G. Ilm K. Dahlman M. Stein U. MACC1, a Novel Player in Solid Cancer Carcinogenesis Mechanisms of Molecular Carcinogenesis Springer Cham, Switzerland 2017 Volume 1 11 38
  38. [38]Kononenko N.L. Classen G.A. Kuijpers M. Puchkov D. Maritzen T. Tempes A. Malik A.R. Skalecka A. Bera S. Jaworski J. Retrograde transport of TrkB-containing autophagosomes via the adaptor AP-2 mediates neuronal complexity and prevents neurodegeneration Nat. Commun. 2017 8 14819 10.1038/ncomms14819 28387218 PMC5385568 · DOI
  39. [39]Mitsunari T. Nakatsu F. Shioda N. Love P.E. Grinberg A. Bonifacino J.S. Ohno H. Clathrin adaptor AP-2 is essential for early embryonal development Mol. Cell Biol. 2005 25 9318 9323 10.1128/MCB.25.21.9318-9323.2005 16227583 PMC1265839 · DOI
  40. [40]Li W. Puertollano R. Bonifacino J.S. Overbeek P.A. Everett E.T. Disruption of the murine Ap2beta1 gene causes nonsyndromic cleft palate Cleft Palate Craniofac. J. 2010 47 566 573 10.1597/09-145 20500056 PMC3691559 · DOI
  41. [41]Gorvin C.M. Rogers A. Stewart M. Paudyal A. Hough T.A. Teboul L. Wells S. Brown S.D. Cox R.D. Thakker R.V. N-ethyl-N-nitrosourea-Induced Adaptor Protein 2 Sigma Subunit 1 (Ap2s1) Mutations Establish Ap2s1 Loss-of-Function Mice JBMR Plus 2017 1 3 15 10.1002/jbm4.10001 29479578 PMC5824975 · DOI
  42. [42]Li K. Li J. Zheng J. Qin S. Reactive Astrocytes in Neurodegenerative Diseases Aging Dis. 2019 10 664 675 10.14336/AD.2018.0720 31165009 PMC6538217 · DOI · Paper page
  43. [43]Nesbit M.A. Hannan F.M. Howles S.A. Reed A.A. Cranston T. Thakker C.E. Gregory L. Rimmer A.J. Rust N. Graham U. Mutations in AP2S1 cause familial hypocalciuric hypercalcemia type 3 Nat. Genet. 2013 45 93 97 10.1038/ng.2492 23222959 PMC3605788 · DOI
  44. [44]Lee J.Y. Shoback D.M. Familial hypocalciuric hypercalcemia and related disorders Best Pract. Res. Clin. Endocrinol. Metab. 2018 32 609 619 10.1016/j.beem.2018.05.004 30449544 PMC6767927 · DOI
  45. [45]Hannan F.M. Howles S.A. Rogers A. Cranston T. Gorvin C.M. Babinsky V.N. Reed A.A. Thakker C.E. Bockenhauer D. Brown R.S. Adaptor protein-2 sigma subunit mutations causing familial hypocalciuric hypercalcaemia type 3 (FHH3) demonstrate genotype-phenotype correlations, codon bias and dominant-negative effects Hum. Mol. Genet. 2015 24 5079 5092 10.1093/hmg/ddv226 26082470 PMC4550820 · DOI
  46. [46]Gorvin C.M. Metpally R. Stokes V.J. Hannan F.M. Krishnamurthy S.B. Overton J.D. Reid J.G. Breitwieser G.E. Thakker R.V. Large-scale exome datasets reveal a new class of adaptor-related protein complex 2 sigma subunit (AP2sigma) mutations, located at the interface with the AP2 alpha subunit, that impair calcium-sensing receptor signalling Hum. Mol. Genet. 2018 27 901 911 10.1093/hmg/ddy010 29325022 PMC5982735 · DOI
  47. [47]Raj T. Li Y.I. Wong G. Humphrey J. Wang M. Ramdhani S. Wang Y.C. Ng B. Gupta I. Haroutunian V. Integrative transcriptome analyses of the aging brain implicate altered splicing in Alzheimer’s disease susceptibility Nat. Genet. 2018 50 1584 1592 10.1038/s41588-018-0238-1 30297968 PMC6354244 · DOI · Paper page
  48. [48]Buser D.P. Ritz M.F. Moes S. Tostado C. Frank S. Spiess M. Mariani L. Jeno P. Boulay J.L. Hutter G. Quantitative proteomics reveals reduction of endocytic machinery components in gliomas EBioMedicine 2019 46 32 41 10.1016/j.ebiom.2019.07.039 31331834 PMC6711119 · DOI
  49. [49]Montagnac G. Meas-Yedid V. Irondelle M. Castro-Castro A. Franco M. Shida T. Nachury M.V. Benmerah A. Olivo-Marin J.C. Chavrier P. alphaTAT1 catalyses microtubule acetylation at clathrin-coated pits Nature 2013 502 567 570 10.1038/nature12571 24097348 PMC3970258 · DOI
  50. [50]Neveu G. Ziv-Av A. Barouch-Bentov R. Berkerman E. Mulholland J. Einav S. AP-2-associated protein kinase 1 and cyclin G-associated kinase regulate hepatitis C virus entry and are potential drug targets J. Virol. 2015 89 4387 4404 10.1128/JVI.02705-14 25653444 PMC4442395 · DOI
  51. [51]Stoneham C.A. Singh R. Jia X. Xiong Y. Guatelli J. Endocytic activity of HIV-1 Vpu: Phosphoserine-dependent interactions with clathrin adaptors Traffic 2017 18 545 561 10.1111/tra.12495 28504462 PMC5600163 · DOI
  52. [52]Rollason R. Korolchuk V. Hamilton C. Schu P. Banting G. Clathrin-mediated endocytosis of a lipid-raft-associated protein is mediated through a dual tyrosine motif J. Cell Sci. 2007 120 3850 3858 10.1242/jcs.003343 17940069 · DOI
  53. [53]Meyer K. Kirchner M. Uyar B. Cheng J.Y. Russo G. Hernandez-Miranda L.R. Szymborska A. Zauber H. Rudolph I.M. Willnow T.E. Mutations in Disordered Regions Can Cause Disease by Creating Dileucine Motifs Cell 2018 175 239 253.e217 10.1016/j.cell.2018.08.019 30197081 · DOI · Paper page
  54. [54]Andrews J. Smith M. Merakovsky J. Coulson M. Hannan F. Kelly L.E. The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides Genetics 1996 143 1699 1711 8844157 PMC1207432
  55. [55]Grigliatti T.A. Hall L. Rosenbluth R. Suzuki D.T. Temperature-sensitive mutations in Drosophila melanogaster. XIV. A selection of immobile adults Mol. Gen. Genet. 1973 120 107 114 10.1007/BF00267238 4631264 · DOI
  56. [56]Fergestad T. Broadie K. Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis J. Neurosci. 2001 21 1218 1227 10.1523/JNEUROSCI.21-04-01218.2001 11160392 PMC6762239 · DOI
  57. [57]Fergestad T. Davis W.S. Broadie K. The stoned proteins regulate synaptic vesicle recycling in the presynaptic terminal J. Neurosci. 1999 19 5847 5860 10.1523/JNEUROSCI.19-14-05847.1999 10407025 PMC6783101 · DOI
  58. [58]Fernandez-Chacon R. Konigstorfer A. Gerber S.H. Garcia J. Matos M.F. Stevens C.F. Brose N. Rizo J. Rosenmund C. Sudhof T.C. Synaptotagmin I functions as a calcium regulator of release probability Nature 2001 410 41 49 10.1038/35065004 11242035 · DOI · Paper page
  59. [59]Grass I. Thiel S. Honing S. Haucke V. Recognition of a basic AP-2 binding motif within the C2B domain of synaptotagmin is dependent on multimerization J. Biol. Chem. 2004 279 54872 54880 10.1074/jbc.M409995200 15491995 · DOI
  60. [60]Haucke V. Wenk M.R. Chapman E.R. Farsad K. De Camilli P. Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation Embo J. 2000 19 6011 6019 10.1093/emboj/19.22.6011 11080148 PMC305843 · DOI
  61. [61]Feany M.B. Buckley K.M. The synaptic vesicle protein synaptotagmin promotes formation of filopodia in fibroblasts Nature 1993 364 537 540 10.1038/364537a0 8166886 · DOI
  62. [62]Jarousse N. Kelly R.B. The AP2 binding site of synaptotagmin 1 is not an internalization signal but a regulator of endocytosis J. Cell Biol. 2001 154 857 866 10.1083/jcb.200103040 11502761 PMC2196445 · DOI
  63. [63]Diril M.K. Wienisch M. Jung N. Klingauf J. Haucke V. Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling Dev. Cell 2006 10 233 244 10.1016/j.devcel.2005.12.011 16459302 · DOI
  64. [64]Martina J.A. Bonangelino C.J. Aguilar R.C. Bonifacino J.S. Stonin 2: An adaptor-like protein that interacts with components of the endocytic machinery J. Cell Biol. 2001 153 1111 1120 10.1083/jcb.153.5.1111 11381094 PMC2174325 · DOI
  65. [65]Phillips A.M. Smith M. Ramaswami M. Kelly L.E. The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin J. Neurosci. 2000 20 8254 8261 10.1523/JNEUROSCI.20-22-08254.2000 11069931 PMC6773190 · DOI
  66. [66]Walther K. Krauss M. Diril M.K. Lemke S. Ricotta D. Honing S. Kaiser S. Haucke V. Human stoned B interacts with AP-2 and synaptotagmin and facilitates clathrin-coated vesicle uncoating EMBO Rep. 2001 2 634 640 10.1093/embo-reports/kve134 11454741 PMC1083948 · DOI
  67. [67]Kononenko N.L. Diril M.K. Puchkov D. Kintscher M. Koo S.J. Pfuhl G. Winter Y. Wienisch M. Klingauf J. Breustedt J. Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2 Proc. Natl. Acad. Sci. USA 2013 110 E526 E535 10.1073/pnas.1218432110 23345427 PMC3568307 · DOI
  68. [68]Bartholome O. Van den Ackerveken P. Sanchez Gil J. de la Brassinne Bonardeaux O. Leprince P. Franzen R. Rogister B. Puzzling Out Synaptic Vesicle 2 Family Members Functions Front. Mol. Neurosci. 2017 10 148 10.3389/fnmol.2017.00148 28588450 PMC5438990 · DOI · Paper page
  69. [69]Lazzell D.R. Belizaire R. Thakur P. Sherry D.M. Janz R. SV2B regulates synaptotagmin 1 by direct interaction J. Biol. Chem. 2004 279 52124 52131 10.1074/jbc.M407502200 15466855 · DOI
  70. [70]Schivell A.E. Batchelor R.H. Bajjalieh S.M. Isoform-specific, calcium-regulated interaction of the synaptic vesicle proteins SV2 and synaptotagmin J. Biol. Chem. 1996 271 27770 27775 10.1074/jbc.271.44.27770 8910372 · DOI
  71. [71]Schivell A.E. Mochida S. Kensel-Hammes P. Custer K.L. Bajjalieh S.M. SV2A and SV2C contain a unique synaptotagmin-binding site Mol. Cell. Neurosci. 2005 29 56 64 10.1016/j.mcn.2004.12.011 15866046 · DOI
  72. [72]Yao J. Nowack A. Kensel-Hammes P. Gardner R.G. Bajjalieh S.M. Cotrafficking of SV2 and synaptotagmin at the synapse J. Neurosci. 2010 30 5569 5578 10.1523/JNEUROSCI.4781-09.2010 20410110 PMC2866018 · DOI · Paper page
  73. [73]Kaempf N. Kochlamazashvili G. Puchkov D. Maritzen T. Bajjalieh S.M. Kononenko N.L. Haucke V. Overlapping functions of stonin 2 and SV2 in sorting of the calcium sensor synaptotagmin 1 to synaptic vesicles Proc. Natl. Acad. Sci. USA 2015 112 7297 7302 10.1073/pnas.1501627112 26015569 PMC4466747 · DOI · Paper page
  74. [74]Gordon S.L. Leube R.E. Cousin M.A. Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis J. Neurosci. 2011 31 14032 14036 10.1523/JNEUROSCI.3162-11.2011 21957264 PMC3188371 · DOI
  75. [75]Rajappa R. Gauthier-Kemper A. Boning D. Huve J. Klingauf J. Synaptophysin 1 Clears Synaptobrevin 2 from the Presynaptic Active Zone to Prevent Short-Term Depression Cell Rep. 2016 14 1369 1381 10.1016/j.celrep.2016.01.031 26854222 · DOI
  76. [76]Awasthi A. Ramachandran B. Ahmed S. Benito E. Shinoda Y. Nitzan N. Heukamp A. Rannio S. Martens H. Barth J. Synaptotagmin-3 drives AMPA receptor endocytosis, depression of synapse strength, and forgetting Science 2019 363 10.1126/science.aav1483 30545844 · DOI
  77. [77]Feutlinske F. Browarski M. Ku M.C. Trnka P. Waiczies S. Niendorf T. Stallcup W.B. Glass R. Krause E. Maritzen T. Stonin1 mediates endocytosis of the proteoglycan NG2 and regulates focal adhesion dynamics and cell motility Nat. Commun. 2015 6 8535 10.1038/ncomms9535 26437238 PMC4600748 · DOI
  78. [78]Breedveld G.J. Fabbrini G. Oostra B.A. Berardelli A. Bonifati V. Tourette disorder spectrum maps to chromosome 14q31.1 in an Italian kindred Neurogenetics 2010 11 417 423 10.1007/s10048-010-0244-7 20437249 PMC2956568 · DOI
  79. [79]Luan Z. Zhang Y. Lu T. Ruan Y. Zhang H. Yan J. Li L. Sun W. Wang L. Yue W. Positive association of the human STON2 gene with schizophrenia Neuroreport 2011 22 288 293 10.1097/WNR.0b013e328345ac22 21407139 · DOI
  80. [80]Shimada A. Yamaguchi A. Kohda D. Structural basis for the recognition of two consecutive mutually interacting DPF motifs by the SGIP1 mu homology domain Sci. Rep. 2016 6 19565 10.1038/srep19565 26822536 PMC4731787 · DOI
  81. [81]Mulkearns E.E. Cooper J.A. FCH domain only-2 organizes clathrin-coated structures and interacts with Disabled-2 for low-density lipoprotein receptor endocytosis Mol. Biol. Cell 2012 23 1330 1342 10.1091/mbc.e11-09-0812 22323290 PMC3315808 · DOI
  82. [82]Katoh M. Katoh M. Identification and characterization of human FCHO2 and mouse Fcho2 genes in silico Int. J. Mol. Med. 2004 14 327 331 15254787
  83. [83]Henne W.M. Kent H.M. Ford M.G. Hegde B.G. Daumke O. Butler P.J. Mittal R. Langen R. Evans P.R. McMahon H.T. Structure and analysis of FCHo2 F-BAR domain: A dimerizing and membrane recruitment module that effects membrane curvature Structure 2007 15 839 852 10.1016/j.str.2007.05.002 17540576 · DOI
  84. [84]Uezu A. Horiuchi A. Kanda K. Kikuchi N. Umeda K. Tsujita K. Suetsugu S. Araki N. Yamamoto H. Takenawa T. SGIP1alpha is an endocytic protein that directly interacts with phospholipids and Eps15 J. Biol. Chem. 2007 282 26481 26489 10.1074/jbc.M703815200 17626015 · DOI
  85. [85]Henne W.M. Boucrot E. Meinecke M. Evergren E. Vallis Y. Mittal R. McMahon H.T. FCHo proteins are nucleators of clathrin-mediated endocytosis Science 2010 328 1281 1284 10.1126/science.1188462 20448150 PMC2883440 · DOI · Paper page
  86. [86]Uezu A. Umeda K. Tsujita K. Suetsugu S. Takenawa T. Nakanishi H. Characterization of the EFC/F-BAR domain protein, FCHO2 Genes Cells 2011 16 868 878 10.1111/j.1365-2443.2011.01536.x 21762413 · DOI
  87. [87]Umasankar P.K. Sanker S. Thieman J.R. Chakraborty S. Wendland B. Tsang M. Traub L.M. Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning Nat. Cell Biol. 2012 14 488 501 10.1038/ncb2473 22484487 PMC3354769 · DOI · Paper page
  88. [89]Hollopeter G. Lange J.J. Zhang Y. Vu T.N. Gu M. Ailion M. Lambie E.J. Slaughter B.D. Unruh J.R. Florens L. The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex Elife 2014 3 10.7554/eLife.03648 PMC4215536 25303366 · DOI
  89. [90]Ma L. Umasankar P.K. Wrobel A.G. Lymar A. McCoy A.J. Holkar S.S. Jha A. Pradhan-Sundd T. Watkins S.C. Owen D.J. Transient Fcho1/2Eps15/RAP-2 Nanoclusters Prime the AP-2 Clathrin Adaptor for Cargo Binding Dev. Cell 2016 37 428 443 10.1016/j.devcel.2016.05.003 27237791 PMC4921775 · DOI · Paper page
  90. [91]Umasankar P.K. Ma L. Thieman J.R. Jha A. Doray B. Watkins S.C. Traub L.M. A clathrin coat assembly role for the muniscin protein central linker revealed by TALEN-mediated gene editing Elife 2014 3 10.7554/eLife.04137 PMC4215538 25303365 · DOI
  91. [92]Lee S.E. Jeong S. Lee U. Chang S. SGIP1alpha functions as a selective endocytic adaptor for the internalization of synaptotagmin 1 at synapses Mol. Brain 2019 12 41 10.1186/s13041-019-0464-1 31053155 PMC6499997 · DOI
  92. [93]Hajkova A. Techlovska S. Dvorakova M. Chambers J.N. Kumpost J. Hubalkova P. Prezeau L. Blahos J. SGIP1 alters internalization and modulates signaling of activated cannabinoid receptor 1 in a biased manner Neuropharmacology 2016 107 201 214 10.1016/j.neuropharm.2016.03.008 26970018 · DOI
  93. [94]Calzoni E. Platt C.D. Keles S. Kuehn H.S. Beaussant-Cohen S. Zhang Y. Pazmandi J. Lanzi G. Pala F. Tahiat A. F-BAR domain only protein 1 (FCHO1) deficiency is a novel cause of combined immune deficiency in human subjects J. Allergy Clin. Immunol. 2019 143 2317 2321.e2312 10.1016/j.jaci.2019.02.014 30822429 PMC6701838 · DOI
  94. [95]Trevaskis J. Walder K. Foletta V. Kerr-Bayles L. McMillan J. Cooper A. Lee S. Bolton K. Prior M. Fahey R. Src homology 3-domain growth factor receptor-bound 2-like (endophilin) interacting protein 1, a novel neuronal protein that regulates energy balance Endocrinology 2005 146 3757 3764 10.1210/en.2005-0282 15919751 · DOI
  95. [96]Cummings N. Shields K.A. Curran J.E. Bozaoglu K. Trevaskis J. Gluschenko K. Cai G. Comuzzie A.G. Dyer T.D. Walder K.R. Genetic variation in SH3-domain GRB2-like (endophilin)-interacting protein 1 has a major impact on fat mass Int. J. Obes. (Lond.) 2012 36 201 206 10.1038/ijo.2011.67 21407171 · DOI
  96. [97]Yako Y.Y. Echouffo-Tcheugui J.B. Balti E.V. Matsha T.E. Sobngwi E. Erasmus R.T. Kengne A.P. Genetic association studies of obesity in Africa: A systematic review Obes. Rev. 2015 16 259 272 10.1111/obr.12260 25641693 · DOI
  97. [98]Chwedorowicz R. Raszewski G. Kapka-Skrzypczak L. Sawicki K. Studzinski T. Event-related potentials (ERP) and SGIP1 gene polymorphisms in alcoholics: Relation to family history of alcoholism and drug usage Ann. Agric. Environ. Med. 2016 23 618 624 10.5604/12321966.1226856 28030933 · DOI
  98. [99]Derringer J. Krueger R.F. Manz N. Porjesz B. Almasy L. Bookman E. Edenberg H.J. Kramer J.R. Tischfield J.A. Bierut L.J. Nonreplication of an association of SGIP1 SNPs with alcohol dependence and resting theta EEG power Psychiatr. Genet. 2011 21 265 266 10.1097/YPG.0b013e32834371fd 21317682 PMC3139721 · DOI
  99. [100]Hodgkinson C.A. Enoch M.A. Srivastava V. Cummins-Oman J.S. Ferrier C. Iarikova P. Sankararaman S. Yamini G. Yuan Q. Zhou Z. Genome-wide association identifies candidate genes that influence the human electroencephalogram Proc. Natl. Acad. Sci. USA 2010 107 8695 8700 10.1073/pnas.0908134107 20421487 PMC2889314 · DOI
  100. [101]van Setten J. Verweij N. Mbarek H. Niemeijer M.N. Trompet S. Arking D.E. Brody J.A. Gandin I. Grarup N. Hall L.M. Genome-wide association meta-analysis of 30,000 samples identifies seven novel loci for quantitative ECG traits Eur. J. Hum. Genet. 2019 27 952 962 10.1038/s41431-018-0295-z 30679814 PMC6777533 · DOI
  101. [102]Ahle S. Ungewickell E. Purification and properties of a new clathrin assembly protein EMBO J. 1986 5 3143 3149 10.1002/j.1460-2075.1986.tb04621.x 3816757 PMC1167304 · DOI
  102. [103]Kohtz D.S. Puszkin S. A neuronal protein (NP185) associated with clathrin-coated vesicles. Characterization of NP185 with monoclonal antibodies J. Biol. Chem. 1988 263 7418 7425 2452823
  103. [104]Dreyling M.H. Martinez-Climent J.A. Zheng M. Mao J. Rowley J.D. Bohlander S.K. 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. USA 1996 93 4804 4809 10.1073/pnas.93.10.4804 8643484 PMC39360 · DOI · Paper page
  104. [105]Koo S.J. Kochlamazashvili G. Rost B. Puchkov D. Gimber N. Lehmann M. Tadeus G. Schmoranzer J. Rosenmund C. Haucke V. Vesicular Synaptobrevin/VAMP2 Levels Guarded by AP180 Control Efficient Neurotransmission Neuron 2015 88 330 344 10.1016/j.neuron.2015.08.034 26412491 · DOI
  105. [106]Tebar F. Bohlander S.K. Sorkin A. Clathrin assembly lymphoid myeloid leukemia (CALM) protein: Localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic Mol. Biol. Cell 1999 10 2687 2702 10.1091/mbc.10.8.2687 10436022 PMC25500 · DOI · Paper page
  106. [107]Yao P.J. Petralia R.S. Bushlin I. Wang Y. Furukawa K. Synaptic distribution of the endocytic accessory proteins AP180 and CALM J. Comp. Neurol. 2005 481 58 69 10.1002/cne.20362 15558718 · DOI · Paper page
  107. [108]Ford M.G. Pearse B.M. Higgins M.K. Vallis Y. Owen D.J. Gibson A. Hopkins C.R. Evans P.R. McMahon H.T. Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes Science 2001 291 1051 1055 10.1126/science.291.5506.1051 11161218 · DOI
  108. [109]Ye W. Lafer E.M. Bacterially expressed F1-20/AP-3 assembles clathrin into cages with a narrow size distribution: Implications for the regulation of quantal size during neurotransmission J. Neurosci. Res. 1995 41 15 26 10.1002/jnr.490410104 7674375 PMC4455046 · DOI
  109. [111]Meyerholz A. Hinrichsen L. Groos S. Esk P.C. Brandes G. Ungewickell E.J. Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation Traffic 2005 6 1225 1234 10.1111/j.1600-0854.2005.00355.x 16262731 · DOI
  110. [112]Sahlender D.A. Kozik P. Miller S.E. Peden A.A. Robinson M.S. Uncoupling the functions of CALM in VAMP sorting and clathrin-coated pit formation PLoS ONE 2013 8 e64514 10.1371/journal.pone.0064514 23741335 PMC3669311 · DOI
  111. [113]Ishikawa Y. Maeda M. Pasham M. Aguet F. Tacheva-Grigorova S.K. Masuda T. Yi H. Lee S.U. Xu J. Teruya-Feldstein J. Role of the clathrin adaptor PICALM in normal hematopoiesis and polycythemia vera pathophysiology Haematologica 2015 100 439 451 10.3324/haematol.2014.119537 25552701 PMC4380716 · DOI
  112. [114]Burston H.E. Maldonado-Baez L. Davey M. Montpetit B. Schluter C. Wendland B. Conibear E. Regulators of yeast endocytosis identified by systematic quantitative analysis J. Cell Biol. 2009 185 1097 1110 10.1083/jcb.200811116 19506040 PMC2711619 · DOI
  113. [115]Wen Y. Stavrou I. Bersuker K. Brady R.J. De Lozanne A. O’Halloran T.J. AP180-mediated trafficking of Vamp7B limits homotypic fusion of Dictyostelium contractile vacuoles Mol. Biol. Cell 2009 20 4278 4288 10.1091/mbc.e09-03-0243 19692567 PMC2762145 · DOI
  114. [116]Dittman J.S. Kaplan J.M. Factors regulating the abundance and localization of synaptobrevin in the plasma membrane Proc. Natl. Acad. Sci. USA 2006 103 11399 11404 10.1073/pnas.0600784103 16844789 PMC1544097 · DOI
  115. [117]Nonet M.L. Holgado A.M. Brewer F. Serpe C.J. Norbeck B.A. Holleran J. Wei L. Hartwieg E. Jorgensen E.M. Alfonso A. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles Mol. Biol. Cell 1999 10 2343 2360 10.1091/mbc.10.7.2343 10397769 PMC25452 · DOI
  116. [118]Burbea M. Dreier L. Dittman J.S. Grunwald M.E. Kaplan J.M. Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans Neuron 2002 35 107 120 10.1016/S0896-6273(02)00749-3 12123612 · DOI
  117. [119]Bao H. Daniels R.W. MacLeod G.T. Charlton M.P. Atwood H.L. Zhang B. AP180 maintains the distribution of synaptic and vesicle proteins in the nerve terminal and indirectly regulates the efficacy of Ca2+-triggered exocytosis J. Neurophysiol. 2005 94 1888 1903 10.1152/jn.00080.2005 15888532 · DOI
  118. [120]Zhang B. Koh Y.H. Beckstead R.B. Budnik V. Ganetzky B. Bellen H.J. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis Neuron 1998 21 1465 1475 10.1016/S0896-6273(00)80664-9 9883738 · DOI · Paper page
  119. [121]Koo S.J. Markovic S. Puchkov D. Mahrenholz C.C. Beceren-Braun F. Maritzen T. Dernedde J. Volkmer R. Oschkinat H. Haucke V. SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses Proc. Natl. Acad. Sci. USA 2011 108 13540 13545 10.1073/pnas.1107067108 21808019 PMC3158172 · DOI
  120. [122]Miller S.E. Sahlender D.A. Graham S.C. Honing S. Robinson M.S. Peden A.A. Owen D.J. The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM Cell 2011 147 1118 1131 10.1016/j.cell.2011.10.038 22118466 PMC3267021 · DOI · Paper page
  121. [123]Moreau K. Fleming A. Imarisio S. Lopez Ramirez A. Mercer J.L. Jimenez-Sanchez M. Bento C.F. Puri C. Zavodszky E. Siddiqi F. PICALM modulates autophagy activity and tau accumulation Nat. Commun. 2014 5 4998 10.1038/ncomms5998 25241929 PMC4199285 · DOI · Paper page
  122. [124]Suzuki M. Tanaka H. Tanimura A. Tanabe K. Oe N. Rai S. Kon S. Fukumoto M. Takei K. Abe T. The Clathrin Assembly Protein PICALM Is Required for Erythroid Maturation and Transferrin Internalization in Mice PLoS ONE 2012 7 e31854 10.1371/journal.pone.0031854 22363754 PMC3283694 · DOI
  123. [125]Goes F.S. Hamshere M.L. Seifuddin F. Pirooznia M. Belmonte-Mahon P. Breuer R. Schulze T. Nothen M. Cichon S. Rietschel M. Genome-wide association of mood-incongruent psychotic bipolar disorder Trans. Psychiatry 2012 2 e180 10.1038/tp.2012.106 PMC3565814 23092984 · DOI
  124. [129]Merthan L. Haller A. Thal D.R. von Einem B. von Arnim C.A.F. The role of PTB domain containing adaptor proteins on PICALM-mediated APP endocytosis and localization BioChem. J. 2019 476 2093 2109 10.1042/BCJ20180840 31300465 · DOI
  125. [130]Xiao Q. Gil S.C. Yan P. Wang Y. Han S. Gonzales E. Perez R. Cirrito J.R. Lee J.M. Role of phosphatidylinositol clathrin assembly lymphoid-myeloid leukemia (PICALM) in intracellular amyloid precursor protein (APP) processing and amyloid plaque pathogenesis J. Biol. Chem. 2012 287 21279 21289 10.1074/jbc.M111.338376 22539346 PMC3375549 · DOI · Paper page
  126. [131]Kanatsu K. Morohashi Y. Suzuki M. Kuroda H. Watanabe T. Tomita T. Iwatsubo T. Decreased CALM expression reduces Abeta42 to total Abeta ratio through clathrin-mediated endocytosis of gamma-secretase Nat. Commun. 2014 5 3386 10.1038/ncomms4386 24577224 · DOI
  127. [132]Park S.K. Ratia K. Ba M. Valencik M. Liebman S.W. Inhibition of Abeta42 oligomerization in yeast by a PICALM ortholog and certain FDA approved drugs Microb. Cell 2016 3 53 64 10.15698/mic2016.02.476 28357335 PMC5349104 · DOI
  128. [134]Kalchman M.A. Koide H.B. McCutcheon K. Graham R.K. Nichol K. Nishiyama K. Kazemi-Esfarjani P. Lynn F.C. Wellington C. Metzler M. HIP1, a human homologue of S. cerevisiae Sla2p, interacts with membrane-associated huntingtin in the brain Nat. Genet. 1997 16 44 53 10.1038/ng0597-44 9140394 · DOI
  129. [135]Chopra V.S. Metzler M. Rasper D.M. Engqvist-Goldstein A.E. Singaraja R. Gan L. Fichter K.M. McCutcheon K. Drubin D. Nicholson D.W. HIP12 is a non-proapoptotic member of a gene family including HIP1, an interacting protein with huntingtin Mamm Genome 2000 11 1006 1015 10.1007/s003350010195 11063258 · DOI
  130. [136]Seki N. Muramatsu M. Sugano S. Suzuki Y. Nakagawara A. Ohhira M. Hayashi A. Hori T. Saito T. Cloning, expression analysis, and chromosomal localization of HIP1R, an isolog of huntingtin interacting protein (HIP1) J. Hum. Genet. 1998 43 268 271 10.1007/s100380050087 9852681 · DOI
  131. [137]Legendre-Guillemin V. Metzler M. Charbonneau M. Gan L. Chopra V. Philie J. Hayden M.R. McPherson P.S. HIP1 and HIP12 display differential binding to F-actin, AP2, and clathrin. Identification of a novel interaction with clathrin light chain J. Biol. Chem. 2002 277 19897 19904 10.1074/jbc.M112310200 11889126 · DOI
  132. [138]Metzler M. Li B. Gan L. Georgiou J. Gutekunst C.A. Wang Y. Torre E. Devon R.S. Oh R. Legendre-Guillemin V. Disruption of the endocytic protein HIP1 results in neurological deficits and decreased AMPA receptor trafficking EMBO J. 2003 22 3254 3266 10.1093/emboj/cdg334 12839988 PMC165658 · DOI
  133. [139]Hyun T.S. Li L. Oravecz-Wilson K.I. Bradley S.V. Provot M.M. Munaco A.J. Mizukami I.F. Sun H. Ross T.S. Hip1-related mutant mice grow and develop normally but have accelerated spinal abnormalities and dwarfism in the absence of HIP1 Mol. Cell Biol. 2004 24 4329 4340 10.1128/MCB.24.10.4329-4340.2004 15121852 PMC400480 · DOI
  134. [140]Engqvist-Goldstein A.E. Kessels M.M. Chopra V.S. Hayden M.R. Drubin D.G. 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. 1999 147 1503 1518 10.1083/jcb.147.7.1503 10613908 PMC2174256 · DOI
  135. [141]Metzler M. Legendre-Guillemin V. Gan L. Chopra V. Kwok A. McPherson P.S. Hayden M.R. HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2 J. Biol. Chem. 2001 276 39271 39276 10.1074/jbc.C100401200 11517213 · DOI
  136. [142]Waelter S. Scherzinger E. Hasenbank R. Nordhoff E. Lurz R. Goehler H. Gauss C. Sathasivam K. Bates G.P. Lehrach H. The huntingtin interacting protein HIP1 is a clathrin and alpha-adaptin-binding protein involved in receptor-mediated endocytosis Hum. Mol. Genet. 2001 10 1807 1817 10.1093/hmg/10.17.1807 11532990 · DOI
  137. [143]Metzler M. Gan L. Wong T.P. Liu L. Helm J. Liu L. Georgiou J. Wang Y. Bissada N. Cheng K. NMDA receptor function and NMDA receptor-dependent phosphorylation of huntingtin is altered by the endocytic protein HIP1 J. Neurosci. 2007 27 2298 2308 10.1523/JNEUROSCI.5175-06.2007 17329427 PMC6673493 · DOI
  138. [144]Mishra S.K. Agostinelli N.R. Brett T.J. Mizukami I. Ross T.S. Traub L.M. Clathrin- and AP-2-binding sites in HIP1 uncover a general assembly role for endocytic accessory proteins J. Biol. Chem. 2001 276 46230 46236 10.1074/jbc.M108177200 11577110 · DOI
  139. [145]Legendre-Guillemin V. Metzler M. Lemaire J.F. Philie J. Gan L. Hayden M.R. McPherson P.S. Huntingtin interacting protein 1 (HIP1) regulates clathrin assembly through direct binding to the regulatory region of the clathrin light chain J. Biol. Chem. 2005 280 6101 6108 10.1074/jbc.M408430200 15533941 · DOI
  140. [146]Senetar M.A. Foster S.J. McCann R.O. Intrasteric inhibition mediates the interaction of the I/LWEQ module proteins Talin1, Talin2, Hip1, and Hip12 with actin Biochemistry 2004 43 15418 15428 10.1021/bi0487239 15581353 · DOI
  141. [147]Le Clainche C. Pauly B.S. Zhang C.X. Engqvist-Goldstein A.E. Cunningham K. Drubin D.G. A Hip1R-cortactin complex negatively regulates actin assembly associated with endocytosis EMBO J. 2007 26 1199 1210 10.1038/sj.emboj.7601576 17318189 PMC1817625 · DOI
  142. [148]Engqvist-Goldstein A.E. Zhang C.X. Carreno S. Barroso C. Heuser J.E. Drubin D.G. RNAi-mediated Hip1R silencing results in stable association between the endocytic machinery and the actin assembly machinery Mol. Biol. Cell 2004 15 1666 1679 10.1091/mbc.e03-09-0639 14742709 PMC379265 · DOI
  143. [149]Bradley S.V. Hyun T.S. Oravecz-Wilson K.I. Li L. Waldorff E.I. Ermilov A.N. Goldstein S.A. Zhang C.X. Drubin D.G. Varela K. Degenerative phenotypes caused by the combined deficiency of murine HIP1 and HIP1r are rescued by human HIP1 Hum. Mol. Genet. 2007 16 1279 1292 10.1093/hmg/ddm076 17452370 · DOI
  144. [150]Parker J.A. Metzler M. Georgiou J. Mage M. Roder J.C. Rose A.M. Hayden M.R. Neri C. Huntingtin-interacting protein 1 influences worm and mouse presynaptic function and protects Caenorhabditis elegans neurons against mutant polyglutamine toxicity J. Neurosci. 2007 27 11056 11064 10.1523/JNEUROSCI.1941-07.2007 17928447 PMC6672856 · DOI
  145. [151]Rao D.S. Chang J.C. Kumar P.D. Mizukami I. Smithson G.M. Bradley S.V. Parlow A.F. Ross T.S. Huntingtin interacting protein 1 Is a clathrin coat binding protein required for differentiation of late spermatogenic progenitors Mol. Cell Biol. 2001 21 7796 7806 10.1128/MCB.21.22.7796-7806.2001 11604514 PMC99949 · DOI
  146. [152]Khatchadourian K. Smith C.E. Metzler M. Gregory M. Hayden M.R. Cyr D.G. Hermo L. Structural abnormalities in spermatids together with reduced sperm counts and motility underlie the reproductive defect in HIP1-/- mice Mol. Reprod Dev. 2007 74 341 359 10.1002/mrd.20564 16967501 · DOI
  147. [153]Oravecz-Wilson K.I. Kiel M.J. Li L. Rao D.S. Saint-Dic D. Kumar P.D. Provot M.M. Hankenson K.D. Reddy V.N. Lieberman A.P. Huntingtin Interacting Protein 1 mutations lead to abnormal hematopoiesis, spinal defects and cataracts Hum. Mol. Genet. 2004 13 851 867 10.1093/hmg/ddh102 14998932 · DOI
  148. [154]Liu Z. Demitrack E.S. Keeley T.M. Eaton K.A. El-Zaatari M. Merchant J.L. Samuelson L.C. IFNgamma contributes to the development of gastric epithelial cell metaplasia in Huntingtin interacting protein 1 related (Hip1r)-deficient mice Lab. Investig. 2012 92 1045 1057 10.1038/labinvest.2012.73 22525425 PMC3387317 · DOI
  149. [155]Wijayatunge R. Holmstrom S.R. Foley S.B. Mgbemena V.E. Bhargava V. Perez G.L. McCrum K. Ross T.S. Deficiency of the Endocytic Protein Hip1 Leads to Decreased Gdpd3 Expression, Low Phosphocholine, and Kypholordosis Mol. Cell Biol. 2018 38 10.1128/MCB.00385-18 PMC6234285 30224518 · DOI
  150. [156]Laragione T. Brenner M. Lahiri A. Gao E. Harris C. Gulko P.S. Huntingtin-interacting protein 1 (HIP1) regulates arthritis severity and synovial fibroblast invasiveness by altering PDGFR and Rac1 signalling Ann. Rheum Dis. 2018 77 1627 1635 10.1136/annrheumdis-2018-213498 30049830 · DOI
  151. [157]Bradley S.V. Oravecz-Wilson K.I. Bougeard G. Mizukami I. Li L. Munaco A.J. Sreekumar A. Corradetti M.N. Chinnaiyan A.M. Sanda M.G. Serum antibodies to huntingtin interacting protein-1: A new blood test for prostate cancer Cancer Res. 2005 65 4126 4133 10.1158/0008-5472.CAN-04-4658 15899803 · DOI
  152. [158]Bradley S.V. Smith M.R. Hyun T.S. Lucas P.C. Li L. Antonuk D. Joshi I. Jin F. Ross T.S. Aberrant Huntingtin interacting protein 1 in lymphoid malignancies Cancer Res. 2007 67 8923 8931 10.1158/0008-5472.CAN-07-2153 17875735 · DOI
  153. [159]Hyun T.S. Ross T.S. HIP1: Trafficking roles and regulation of tumorigenesis Trends Mol. Med. 2004 10 194 199 10.1016/j.molmed.2004.02.003 15059611 · DOI
  154. [160]Rao D.S. Hyun T.S. Kumar P.D. Mizukami I.F. Rubin M.A. Lucas P.C. Sanda M.G. Ross T.S. Huntingtin-interacting protein 1 is overexpressed in prostate and colon cancer and is critical for cellular survival J. Clin. Investig. 2002 110 351 360 10.1172/JCI0215529 12163454 PMC151092 · DOI
  155. [161]Bradley S.V. Holland E.C. Liu G.Y. Thomas D. Hyun T.S. Ross T.S. Huntingtin interacting protein 1 is a novel brain tumor marker that associates with epidermal growth factor receptor Cancer Res. 2007 67 3609 3615 10.1158/0008-5472.CAN-06-4803 17440072 · DOI
  156. [162]Choi S.A. Kim S.J. Chung K.C. Huntingtin-interacting protein 1-mediated neuronal cell death occurs through intrinsic apoptotic pathways and mitochondrial alterations FEBS Lett. 2006 580 5275 5282 10.1016/j.febslet.2006.08.076 16979168 · DOI
  157. [163]Mills I.G. Gaughan L. Robson C. Ross T. McCracken S. Kelly J. Neal D.E. Huntingtin interacting protein 1 modulates the transcriptional activity of nuclear hormone receptors J. Cell Biol. 2005 170 191 200 10.1083/jcb.200503106 16027218 PMC2171420 · DOI
  158. [164]Hong M. Kim R.N. Song J.Y. Choi S.J. Oh E. Lira M.E. Mao M. Takeuchi K. Han J. Kim J. HIP1-ALK, a novel fusion protein identified in lung adenocarcinoma J. Thorac. Oncol. 2014 9 419 422 10.1097/JTO.0000000000000061 24518094 · DOI
  159. [165]Ou S.H. Klempner S.J. Greenbowe J.R. Azada M. Schrock A.B. Ali S.M. Ross J.S. Stephens P.J. Miller V.A. Identification of a novel HIP1-ALK fusion variant in Non-Small-Cell Lung Cancer (NSCLC) and discovery of ALK I1171 (I1171N/S) mutations in two ALK-rearranged NSCLC patients with resistance to Alectinib J. Thorac. Oncol. 2014 9 1821 1825 10.1097/JTO.0000000000000368 25393796 · DOI
  160. [166]Ross T.S. Bernard O.A. Berger R. Gilliland D.G. Fusion of Huntingtin interacting protein 1 to platelet-derived growth factor beta receptor (PDGFbetaR) in chronic myelomonocytic leukemia with t(5;7)(q33;q11.2) Blood 1998 91 4419 4426 10.1182/blood.V91.12.4419 9616134 · DOI
  161. [167]Ramocki M.B. Bartnik M. Szafranski P. Kolodziejska K.E. Xia Z. Bravo J. Miller G.S. Rodriguez D.L. Williams C.A. Bader P.I. Recurrent distal 7q11.23 deletion including HIP1 and YWHAG identified in patients with intellectual disabilities, epilepsy, and neurobehavioral problems Am. J. Hum. Genet. 2010 87 857 865 10.1016/j.ajhg.2010.10.019 21109226 PMC2997378 · DOI
  162. [168]Wanker E.E. Rovira C. Scherzinger E. Hasenbank R. Walter S. Tait D. Colicelli J. Lehrach H. HIP-I: A huntingtin interacting protein isolated by the yeast two-hybrid system Hum. Mol. Genet. 1997 6 487 495 10.1093/hmg/6.3.487 9147654 · DOI
  163. [169]Fazioli F. Minichiello L. Matoskova B. Wong W.T. Di Fiore P.P. eps15, a novel tyrosine kinase substrate, exhibits transforming activity Mol. Cell Biol. 1993 13 5814 5828 10.1128/MCB.13.9.5814 7689153 PMC360326 · DOI
  164. [170]Milesi C. Alberici P. Pozzi B. Oldani A. Beznoussenko G.V. Raimondi A. Soppo B.E. Amodio S. Caldieri G. Malabarba M.G. Redundant and nonredundant organismal functions of EPS15 and EPS15L1 Life Sci. Alliance 2019 2 10.26508/lsa.201800273 PMC6350104 30692166 · DOI
  165. [171]Polo S. Sigismund S. Faretta M. Guidi M. Capua M.R. Bossi G. Chen H. De Camilli P. Di Fiore P.P. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins Nature 2002 416 451 455 10.1038/416451a 11919637 · DOI
  166. [172]Confalonieri S. Di Fiore P.P. The Eps15 homology (EH) domain FEBS Lett. 2002 513 24 29 10.1016/S0014-5793(01)03241-0 11911876 · DOI
  167. [173]Wong W.T. Schumacher C. Salcini A.E. Romano A. Castagnino P. Pelicci P.G. Di Fiore P.P. A protein-binding domain, EH, identified in the receptor tyrosine kinase substrate Eps15 and conserved in evolution Proc. Natl. Acad. Sci. USA 1995 92 9530 9534 10.1073/pnas.92.21.9530 7568168 PMC40835 · DOI
  168. [174]Mayer B.J. Endocytosis: EH domains lend a hand Curr. Biol. 1999 9 R70 R73 10.1016/S0960-9822(99)80014-1 10021353 · DOI
  169. [175]Polo S. Confalonieri S. Salcini A.E. Di Fiore P.P. EH and UIM: Endocytosis and more Sci. STKE 2003 2003 re17 10.1126/stke.2132003re17 14679291 · DOI
  170. [176]Salcini A.E. Confalonieri S. Doria M. Santolini E. Tassi E. Minenkova O. Cesareni G. Pelicci P.G. Di Fiore P.P. Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module Genes Dev. 1997 11 2239 2249 10.1101/gad.11.17.2239 9303539 PMC275390 · DOI · Paper page
  171. [177]Tebar F. Confalonieri S. Carter R.E. Di Fiore P.P. Sorkin A. Eps15 is constitutively oligomerized due to homophilic interaction of its coiled-coil region J. Biol. Chem. 1997 272 15413 15418 10.1074/jbc.272.24.15413 9182572 · DOI
  172. [178]Sengar A.S. Wang W. Bishay J. Cohen S. Egan S.E. The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15 EMBO J. 1999 18 1159 1171 10.1093/emboj/18.5.1159 10064583 PMC1171207 · DOI
  173. [179]Iannolo G. Salcini A.E. Gaidarov I. Goodman O.B. Jr. Baulida J. Carpenter G. Pelicci P.G. Di Fiore P.P. Keen J.H. Mapping of the molecular determinants involved in the interaction between eps15 and AP-2 Cancer Res. 1997 57 240 245 9000562
  174. [180]Evergren E. Cobbe N. McMahon H.T. Eps15R and clathrin regulate EphB2-mediated cell repulsion Traffic 2018 19 44 57 10.1111/tra.12531 28972287 PMC5836524 · DOI
  175. [181]Salcini A.E. Chen H. Iannolo G. De Camilli P. Di Fiore P.P. Epidermal growth factor pathway substrate 15, Eps15 Int. J. BioChem. Cell Biol. 1999 31 805 809 10.1016/S1357-2725(99)00042-4 10481267 · DOI
  176. [182]Torrisi M.R. Lotti L.V. Belleudi F. Gradini R. Salcini A.E. Confalonieri S. Pelicci P.G. Di Fiore P.P. Eps15 is recruited to the plasma membrane upon epidermal growth factor receptor activation and localizes to components of the endocytic pathway during receptor internalization Mol. Biol. Cell 1999 10 417 434 10.1091/mbc.10.2.417 9950686 PMC25178 · DOI
  177. [183]Carbone R. Fre S. Iannolo G. Belleudi F. Mancini P. Pelicci P.G. Torrisi M.R. Di Fiore P.P. eps15 and eps15R are essential components of the endocytic pathway Cancer Res. 1997 57 5498 5504 9407958
  178. [184]de Melker A.A. van der Horst G. Borst J. c-Cbl directs EGF receptors into an endocytic pathway that involves the ubiquitin-interacting motif of Eps15 J. Cell Sci. 2004 117 5001 5012 10.1242/jcs.01354 15383614 · DOI
  179. [185]Girao H. Catarino S. Pereira P. Eps15 interacts with ubiquitinated Cx43 and mediates its internalization Exp. Cell Res. 2009 315 3587 3597 10.1016/j.yexcr.2009.10.003 19835873 · DOI
  180. [186]Lin A. Man H.Y. Endocytic adaptor epidermal growth factor receptor substrate 15 (Eps15) is involved in the trafficking of ubiquitinated alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors J. Biol. Chem. 2014 289 24652 24664 10.1074/jbc.M114.582114 25023288 PMC4148888 · DOI
  181. [187]Parachoniak C.A. Park M. Distinct recruitment of Eps15 via Its coiled-coil domain is required for efficient down-regulation of the met receptor tyrosine kinase J. Biol. Chem. 2009 284 8382 8394 10.1074/jbc.M807607200 19109251 PMC2659196 · DOI
  182. [188]Chi S. Cao H. Chen J. McNiven M.A. Eps15 mediates vesicle trafficking from the trans-Golgi network via an interaction with the clathrin adaptor AP-1 Mol. Biol. Cell 2008 19 3564 3575 10.1091/mbc.e07-10-0997 18524853 PMC2488291 · DOI
  183. [189]Kent H.M. McMahon H.T. Evans P.R. Benmerah A. Owen D.J. Gamma-adaptin appendage domain: Structure and binding site for Eps15 and gamma-synergin Structure 2002 10 1139 1148 10.1016/S0969-2126(02)00801-8 12176391 · DOI
  184. [190]Poupon V. Polo S. Vecchi M. Martin G. Dautry-Varsat A. Cerf-Bensussan N. Di Fiore P.P. Benmerah A. Differential nucleocytoplasmic trafficking between the related endocytic proteins Eps15 and Eps15R J. Biol. Chem. 2002 277 8941 8948 10.1074/jbc.M108385200 11777906 · DOI
  185. [191]Salcini A.E. Hilliard M.A. Croce A. Arbucci S. Luzzi P. Tacchetti C. Daniell L. De Camilli P. Pelicci P.G. Di Fiore P.P. The Eps15 C. elegans homologue EHS-1 is implicated in synaptic vesicle recycling Nat. Cell Biol. 2001 3 755 760 10.1038/35087075 11483962 · DOI
  186. [192]Koh T.W. Korolchuk V.I. Wairkar Y.P. Jiao W. Evergren E. Pan H. Zhou Y. Venken K.J. Shupliakov O. Robinson I.M. Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development J. Cell Biol. 2007 178 309 322 10.1083/jcb.200701030 17620409 PMC2064449 · DOI
  187. [193]Majumdar A. Ramagiri S. Rikhy R. Drosophila homologue of Eps15 is essential for synaptic vesicle recycling Exp. Cell Res. 2006 312 2288 2298 10.1016/j.yexcr.2006.03.030 16709407 · DOI
  188. [194]Seiler C. Gebhart N. Zhang Y. Shinton S.A. Li Y.S. Ross N.L. Liu X. Li Q. Bilbee A.N. Varshney G.K. Mutagenesis Screen Identifies agtpbp1 and eps15L1 as Essential for T lymphocyte Development in Zebrafish PLoS ONE 2015 10 e0131908 10.1371/journal.pone.0131908 26161877 PMC4498767 · DOI
  189. [195]Pozzi B. Amodio S. Lucano C. Sciullo A. Ronzoni S. Castelletti D. Adler T. Treise I. Betsholtz I.H. Rathkolb B. The endocytic adaptor Eps15 controls marginal zone B cell numbers PLoS ONE 2012 7 e50818 10.1371/journal.pone.0050818 23226392 PMC3511280 · DOI
  190. [196]Dai X. Liu Z. Zhang S. Over-expression of EPS15 is a favorable prognostic factor in breast cancer Mol. Biosyst. 2015 11 2978 2985 10.1039/C5MB00219B 26289382 · DOI
  191. [197]Bens S. Haake A. Tonnies H. Vater I. Stephani U. Holterhus P.M. Siebert R. Caliebe A. A de novo 1.1Mb microdeletion of chromosome 19p13.11 provides indirect evidence for EPS15L1 to be a strong candidate for split hand split foot malformation Eur. J. Med. Genet. 2011 54 e501 e504 10.1016/j.ejmg.2011.05.004 21700002 · DOI
  192. [198]Umair M. Ullah A. Abbas S. Ahmad F. Basit S. Ahmad W. First direct evidence of involvement of a homozygous loss-of-function variant in the EPS15L1 gene underlying split-hand/split-foot malformation Clin. Genet. 2018 93 699 702 10.1111/cge.13152 29023680 · DOI
  193. [199]Spradling K.D. Burke T.J. Lohi J. Pilcher B.K. Cloning and initial characterization of human epsin 3, a novel matrix-induced keratinocyte specific transcript J. Investig. Dermatol. 2000 115 332 10.1046/j.1523-1747.2000.00abs-4.x 10951261 · DOI
  194. [200]Ko G. Paradise S. Chen H. Graham M. Vecchi M. Bianchi F. Cremona O. Di Fiore P.P. De Camilli P. Selective high-level expression of epsin 3 in gastric parietal cells, where it is localized at endocytic sites of apical canaliculi Proc. Natl. Acad. Sci. USA 2010 107 21511 21516 10.1073/pnas.1016390107 21115825 PMC3003030 · DOI
  195. [201]Chen H. Fre S. Slepnev V.I. Capua M.R. Takei K. Butler M.H. Di Fiore P.P. De Camilli P. Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis Nature 1998 394 793 797 10.1038/29555 9723620 · DOI
  196. [202]Drake M.T. Downs M.A. Traub L.M. Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites J. Biol. Chem. 2000 275 6479 6489 10.1074/jbc.275.9.6479 10692452 · DOI
  197. [203]Shih S.C. Katzmann D.J. Schnell J.D. Sutanto M. Emr S.D. Hicke L. Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis Nat. Cell Biol. 2002 4 389 393 10.1038/ncb790 11988742 · DOI
  198. [204]Kalthoff C. Alves J. Urbanke C. Knorr R. Ungewickell E.J. Unusual structural organization of the endocytic proteins AP180 and epsin 1 J. Biol. Chem. 2002 277 8209 8216 10.1074/jbc.M111587200 11756460 · DOI
  199. [205]Ford M.G. Mills I.G. Peter B.J. Vallis Y. Praefcke G.J. Evans P.R. McMahon H.T. Curvature of clathrin-coated pits driven by epsin Nature 2002 419 361 366 10.1038/nature01020 12353027 · DOI · Paper page
  200. [206]Chen B. Dores M.R. Grimsey N. Canto I. Barker B.L. Trejo J. Adaptor protein complex-2 (AP-2) and epsin-1 mediate protease-activated receptor-1 internalization via phosphorylation- and ubiquitination-dependent sorting signals J. Biol. Chem. 2011 286 40760 40770 10.1074/jbc.M111.299776 21965661 PMC3220480 · DOI

200 of 370 shown

Cited by

Sorted by citations

Authors
Azarnia Tehran, D., López-Hernández, T., & Maritzen, T.
Affiliations
  • Leibniz-Forschungsinstitut für Molekulare Pharmakologie (FMP), 13125 Berlin, Germany
  • Leibniz-Forschungsinstitut für Molekulare Pharmakologie (DE)
Corresponding author
Maritzen, Tanja
ORCID
Venue
Cells
Publisher
MDPI AG
Published
2019-10-29
Volume
8
Issue
11
Pages
1345
ISSN
2073-4409 (ISSN-L)
DOI
10.3390/cells8111345
PMC
PMC6912373
OpenAlex
W2982434028
Cited by
44
References
9
Citations by year
2026: 8 · 2025: 3 · 2024: 7 · 2023: 3 · 2022: 7 · 2021: 7 · 2020: 7 · 2019: 1 · 2018: 1
FWCI
0.64
Type
journal article
Language
en
Open access
Licence
Locations
  • Cells (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Padua Research Archive (University of Padova) (submittedVersion, cc-by)
Funders
DFG to T.M. (MA 4735/2-1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords
endocytic adaptor proteins, endocytosis, AP-2, cell surface receptors, receptor internalization, nutrient uptake, signal transduction, neurotransmission, metabolic disorders, encephalopathy, human mutations, model organisms
MeSH terms
Animals, Disease, Endocytosis, Health, Humans, Membrane Proteins, Mutation, Clathrin-Coated Vesicles, Models, Animal, Adaptor Proteins, Signal Transducing

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review