CoChat
Sign Up
Cited by 218Cellular transport and secretionAutophagy in Disease and TherapyCaveolin-1 and cellular processes

AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling

Open access
Pant, Saumya, Sharma, Mahak, Patel, Kruti, Caplan, Steve, Carr, Chavela M., Grant, Barth D.·2009·Nature Cell Biology
DOI 10.1038/ncb1986PMC PMC2788952
Open this paper in CoChat — free account

Abstract

RME-1/EHD1 (receptor mediated endocytosis/Eps15 homology-domain containing 1) family proteins are key residents of the recycling endosome, which are required for endosome-to-plasma membrane transport in Caenorhabditis elegans and mammals. Recent studies suggest similarities between the RME-1/EHD proteins and the Dynamin GTPase superfamily of mechanochemical pinchases, which promote membrane fission. Here we show that endogenous C. elegans AMPH-1, the only C. elegans member of the Amphiphysin/BIN1 family of BAR (Bin1-Amphiphysin-Rvs161p/167p)-domain-containing proteins, colocalizes with RME-1 on recycling endosomes in vivo, that amph-1-deletion mutants are defective in recycling endosome morphology and function, and that binding of AMPH-1 Asn-Pro-Phe(Asp/Glu) sequences to the RME-1 EH-domain promotes the recycling of transmembrane cargo. We also show a requirement for human BIN1 (also known as Amphiphysin 2) in EHD1-regulated endocytic recycling. In vitro, we find that purified recombinant AMPH-1-RME-1 complexes produce short, coated membrane tubules that are qualitatively distinct from those produced by either protein alone. Our results indicate that AMPH-1 and RME-1 cooperatively regulate endocytic recycling, probably through functions required for the production of cargo carriers that exit the recycling endosome for the cell surface.

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 · 10.1038/ncb1986

Cites

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?

  • EHD proteins regulate BIN1 activity and are required for endocytic vesicle recycling together with Rab8a, Rab11-FIP2 and MICAL-L1.

    “EHD proteins regulate BIN1 activity and are required for endocytic vesicle recycling together with Rab8a, Rab11-FIP2 and MICAL-L1 (16,43,44).”

    From BIN1 regulates BACE1 intracellular trafficking and amyloid-β production (2016) · cites this paper as [16]

    The Results section (‘Mammalian Bin1/Amphiphysin2 functions in recycling’; page not provided) reports that BIN1 is present on EHD1-positive recycling tubules and that BIN1 depletion delays recycling. The paper describes BIN1 as functioning in EHD1-regulated recycling, but does not establish that EHD proteins regulate BIN1 activity. It also does not show recycling involving Rab8a, Rab11-FIP2 and MICAL-L1 together; Rab11-FIP2 appears in a reference title, not in that finding. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Depletion of Bin1 in HeLa cells impaired recycling of transferrin, but not endocytosis, and cellular transferrin accumulated in the juxtanuclear compartment.

    “In addition, the depletion of Bin1 in HeLa cells impaired the recycling of transferrin, but not endocytosis, and cellular transferrin was accumulated in the juxtanuclear compartment (16).”

    From BIN1 regulates BACE1 intracellular trafficking and amyloid-β production (2016) · cites this paper as [16]

Self-check

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

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

The citation lists haven’t been fetched yet

References 50 · Cited by 218

Research works printed but not linked: 46

  1. [1]Grant B Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling Nature cell biology 2001 3 573 579 11389442
  2. [2]Lin SX Grant B Hirsh D Maxfield FR Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells Nature cell biology 2001 3 567 572 11389441
  3. [3]Caplan S A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane The EMBO journal 2002 21 2557 2567 12032069 PMC126039
  4. [4]Lee DW ATP binding regulates oligomerization and endosome association of RME-1 family proteins The Journal of biological chemistry 2005 280 17213 17220 15710626
  5. [5]Naslavsky N Rahajeng J Sharma M Jovic M Caplan S Interactions between EHD proteins and Rab11-FIP2: a role for EHD3 in early endosomal transport Molecular biology of the cell 2006 17 163 177 16251358 PMC1345656
  6. [6]Sharma M Naslavsky N Caplan S A role for EHD4 in the regulation of early endosomal transport Traffic (Copenhagen, Denmark) 2008 9 995 1018 PMC2795359 18331452
  7. [7]Shao Y Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes The Journal of cell biology 2002 157 679 691 12011113 PMC2173850
  8. [8]Guilherme A EHD2 and the novel EH domain binding protein EHBP1 couple endocytosis to the actin cytoskeleton The Journal of biological chemistry 2004 279 10593 10605 14676205
  9. [9]Daumke O Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling Nature 2007 449 923 927 17914359
  10. [10]Sever S Dynamin and endocytosis Current opinion in cell biology 2002 14 463 467 12383797
  11. [11]Roux A Antonny B The long and short of membrane fission Cell 2008 135 1163 1165 19109885
  12. [12]Salcini AE Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module Genes & development 1997 11 2239 2249 9303539 PMC275390
  13. [13]Grant BD Caplan S Mechanisms of EHD/RME-1 Protein Function in Endocytic Transport Traffic (Copenhagen, Denmark) 2008 PMC2766864 18801062
  14. [14]Kieken F Jovic M Naslavsky N Caplan S Sorgen PL EH domain of EHD1 Journal of biomolecular NMR 2007 39 323 329 17899392
  15. [15]Takei K Slepnev VI Haucke V De Camilli P Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis Nature cell biology 1999 1 33 39 10559861
  16. [16]David C McPherson PS Mundigl O de Camilli P A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals Proceedings of the National Academy of Sciences of the United States of America 1996 93 331 335 8552632 PMC40232
  17. [17]Shi A A novel requirement for C. elegans Alix/ALX-1 in RME-1-mediated membrane transport Curr Biol 2007 17 1913 1924 17997305 PMC2175126
  18. [18]Sato K Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools Proceedings of the National Academy of Sciences of the United States of America 2009 106 1139 1144 19151157 PMC2633560
  19. [19]Chen CC RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine Molecular biology of the cell 2006 17 1286 1297 16394106 PMC1382317
  20. [20]Zhang B Zelhof AC Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin-Rvsp Traffic (Copenhagen, Denmark) 2002 3 452 460 12047553
  21. [21]Razzaq A Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila Genes & development 2001 15 2967 2979 11711432 PMC312829
  22. [22]Zelhof AC Drosophila Amphiphysin is implicated in protein localization and membrane morphogenesis but not in synaptic vesicle endocytosis Development (Cambridge, England) 2001 128 5005 5015 11748137
  23. [23]Leventis PA Drosophila Amphiphysin is a post-synaptic protein required for normal locomotion but not endocytosis Traffic (Copenhagen, Denmark) 2001 2 839 850 11733051
  24. [24]Grabs D The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence The Journal of biological chemistry 1997 272 13419 13425 9148966
  25. [25]Burack MA Silverman MA Banker G The role of selective transport in neuronal protein sorting Neuron 2000 26 465 472 10839364
  26. [26]Naslavsky N Weigert R Donaldson JG Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements Molecular biology of the cell 2004 15 3542 3552 15146059 PMC491817
  27. [27]Naslavsky N Weigert R Donaldson JG Convergence of non-clathrin-and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides Molecular biology of the cell 2003 14 417 431 12589044 PMC149982
  28. [28]Farsad K A putative role for intramolecular regulatory mechanisms in the adaptor function of amphiphysin in endocytosis Neuropharmacology 2003 45 787 796 14529717
  29. [29]McMahon HT Wigge P Smith C Clathrin interacts specifically with amphiphysin and is displaced by dynamin FEBS letters 1997 413 319 322 9280305
  30. [30]Olesen LE Solitary and repetitive binding motifs for the AP2 complex alpha-appendage in amphiphysin and other accessory proteins The Journal of biological chemistry 2008 283 5099 5109 17986441
  31. [31]Owen DJ Crystal structure of the amphiphysin-2 SH3 domain and its role in the prevention of dynamin ring formation The EMBO journal 1998 17 5273 5285 9736607 PMC1170855
  32. [32]Slepnev VI De Camilli P Accessory factors in clathrin-dependent synaptic vesicle endocytosis Nature reviews 2000 1 161 172 11257904
  33. [33]Yoshida Y The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature The EMBO journal 2004 23 3483 3491 15318165 PMC516627
  34. [34]Lee E Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle Science (New York, N.Y 2002 297 1193 1196 12183633
  35. [35]Muller AJ Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation Molecular and cellular biology 2003 23 4295 4306 12773571 PMC156129
  36. [36]Jovic M Kieken F Naslavsky N Sorgen PL Caplan S Eps15 homology domain 1-associated tubules contain phosphatidylinositol-4-phosphate and phosphatidylinositol-(4,5)-bisphosphate and are required for efficient recycling Molecular biology of the cell 2009 20 2731 2743 19369419 PMC2688552
  37. [37]Yamashiro DJ Tycko B Fluss SR Maxfield FR Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway Cell 1984 37 789 800 6204769
  38. [38]Takei K Slepnev VI De Camilli P Interactions of dynamin and amphiphysin with liposomes Methods in enzymology 2001 329 478 486 11210568
  39. [39]Brown FD Rozelle AL Yin HL Balla T Donaldson JG Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic The Journal of cell biology 2001 154 1007 1017 11535619 PMC2196179
  40. [40]Pucadyil TJ Schmid SL Real-time visualization of dynamin-catalyzed membrane fission and vesicle release Cell 2008 135 1263 1275 19084268 PMC2673235
  41. [41]Bashkirov PV GTPase Cycle of Dynamin Is Coupled to Membrane Squeeze and Release, Leading to Spontaneous Fission Cell 2008 PMC2768395 19084269
  42. [42]Braun A EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling Molecular biology of the cell 2005 16 3642 3658 15930129 PMC1182304
  43. [43]Roux A Uyhazi K Frost A De Camilli P GTP-dependent twisting of dynamin implicates constriction and tension in membrane fission Nature 2006 441 528 531 16648839
  44. [44]Kamath RS Ahringer J Genome-wide RNAi screening in Caenorhabditis elegans Methods (San Diego, Calif 2003 30 313 321 12828945
  45. [45]Balklava Z Pant S Fares H Grant BD Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic Nature cell biology 2007 9 1066 1073 17704769
  46. [46]Edelhoch H Spectroscopic determination of tryptophan and tyrosine in proteins Biochemistry 1967 6 1948 1954 6049437

Authors
Pant, S., Sharma, M., Patel, K., Caplan, S., Carr, C. M., & Grant, B. D.
Affiliations
  • Rutgers, The State University of New Jersey (US)
  • University of Nebraska Medical Center (US)
Corresponding author
Grant, Barth D.
ORCID
Venue
Nature Cell Biology
Publisher
Springer Science and Business Media LLC
Published
2009-11-15
Volume
11
Issue
12
Pages
1399-1410
ISSN
  • 1465-7392 (ISSN-L)
  • 1476-4679
DOI
10.1038/ncb1986
PMC
PMC2788952
OpenAlex
W2007118279
Cited by
218
References
50
Citations by year
2026: 4 · 2025: 13 · 2024: 11 · 2023: 5 · 2022: 20 · 2021: 8 · 2020: 11 · 2019: 11 · 2018: 10 · 2017: 9 · 2016: 15 · 2015: 16 · 2014: 17 · 2013: 18 · 2012: 20
FWCI
7.27
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature Cell Biology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of General Medical Sciences (R01GM067237, GM074876, GM67237, R01GM074876)
  • National Center for Research Resources (R24RR022234, R24RR22234)
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 › Cell Biology › Caveolin-1 and cellular processes
Keywords
amphiphysin, BIN1, EHD1, endocytic recycling, recycling endosomes, BAR domain proteins, EH domain, Caenorhabditis elegans, cargo carriers, membrane fission
MeSH terms
Animals, Endocytosis, HeLa Cells, Humans, Microscopy, Electron, Nerve Tissue Proteins, Nuclear Proteins, Protein Binding, Caenorhabditis elegans, Tumor Suppressor Proteins, Caenorhabditis elegans Proteins, RNA Interference, 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