CoChat
Sign Up
Cited by 151

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

EHD Proteins Associate with Syndapin I and II and Such Interactions Play a Crucial Role in Endosomal Recycling

Braun, Anne, Pinyol, Roser, Dahlhaus, Regina, Koch, Dennis, Fonarev, Paul, Grant, Barth D., Kessels, Michael M., Qualmann, Britta·2005·Molecular Biology of the Cell
DOI 10.1091/mbc.e05-01-0076
Open this paper in CoChat — free account

Abstract

EHD proteins were shown to function in the exit of receptors and other membrane proteins from the endosomal recycling compartment. Here, we identify syndapins, accessory proteins in vesicle formation at the plasma membrane, as differential binding partners for EHD proteins. These complexes are formed by direct eps15-homology (EH) domain/asparagine proline phenylalanine (NPF) motif interactions. Heterologous and endogenous coimmunoprecipitations as well as reconstitutions of syndapin/EHD protein complexes at intracellular membranes of living cells demonstrate the in vivo relevance of the interaction. The combination of mutational analysis and coimmunoprecipitations performed under different nucleotide conditions strongly suggest that nucleotide binding by EHD proteins modulates the association with syndapins. Colocalization studies and subcellular fractionation experiments support a role for syndapin/EHD protein complexes in membrane trafficking. Specific interferences with syndapin–EHD protein interactions by either overexpression of the isolated EHD-binding interface of syndapin II or of the EHD1 EH domain inhibited the recycling of transferrin to the plasma membrane, suggesting that EH domain/NPF interactions are critical for EHD protein function in recycling. Consistently, both inhibitions were rescued by co-overexpression of the attacked protein component. Our data thus reveal that, in addition to a crucial role in endocytic internalization, syndapin protein complexes play an important role in endocytic receptor recycling.

Overview

Integrity signals

Registry

Crossref · 10.1091/mbc.e05-01-0076

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

  • EHD1 has been implicated in the internalization of certain receptors.

    “EHD1 has been implicated in: (I) recycling of receptors to the plasma membrane [ 15,16,18], and (II) in the internalization of certain receptors [29]”

    From EHD1 regulates cholesterol homeostasis and lipid droplet storage (2007) · cites this paper as [29]

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 33

  1. Caplan, S., Naslavsky, N., Hartnell, L. M., Lodge, R., Polishchuk, R. S., Donaldson, J. G., and Bonifacino, J. S. (2002). A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane.EMBO J.21, 2557–2567. · DOI · Paper page
  2. Carroll, R. C., Beattie, E. C., Xia, H., Luscher, C., Altschuler, Y., Nicoll, R. A., Malenka, R. C., and von Zastrow, M. (1999). Dynamin-dependent endocytosis of ionotropic glutamate receptors.Proc. Natl. Acad. Sci. USA96, 14112–14117. · DOI
  3. 10.1091/mbc.9.11.3241 · DOI
  4. de Beer, T., Hoofnagle, A. N., Enmon, J. L., Bowers, R. C., Yamabhai, M., Kay, B. K., and Overduin, M. (2000). Molecular mechanism of NPF recognition by EH domains.Nat. Struct. Biol.7, 1018–1022. · DOI
  5. de Renzis, S., Sonnichsen, B., and Zerial, M. (2002). Divalent Rab effectors regulate the sub-compartmental organization and sorting of early endosomes.Nat. Cell Biol.4, 124–133. · DOI
  6. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H., and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling.Nat. Cell Biol.3, 573–579. · DOI
  7. 10.1091/mbc.11.1.393 · DOI
  8. Kessels, M. M., Engqvist-Goldstein, A. E., Drubin, D. G., and Qualmann, B. (2001). Mammalian Abp1, a signal-responsive F-actin-binding protein, links the actin cytoskeleton to endocytosis via the GTPase dynamin.J. Cell Biol.153, 351–366. · DOI
  9. Kessels, M. M., and Qualmann, B. (2002). Syndapins integrate N-WASP in receptor-mediated endocytosis.EMBO J.21, 6083–6094. · DOI
  10. Kessels, M. M., and Qualmann, B. (2004). The syndapin protein family: linking membrane trafficking with the cytoskeleton.J. Cell Sci.117, 3077–3086. · DOI
  11. Lee, D. W., Zhao, X., Scarselletta, S., Schweinsberg, P. J., Eisenberg, E., Grant, B. D., and Greene, L. E. (2005). Interaction of RME-1/EHD1 with nucleotide.J. Biol. Chem.280, 17213–17220. · DOI
  12. Lin, S. X., Grant, B., Hirsh, D., and Maxfield, F. R. (2001). Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells.Nat. Cell Biol.3, 567–572. · DOI · Paper page
  13. Maxfield, F. R., and McGraw, T. E. (2004). Endocytic recycling.Nat. Rev. Mol. Cell. Biol.5, 121–132. · DOI · Paper page
  14. Merrifield, C. J., Feldman, M. E., Wan, L., and Almers, W. (2002). Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits.Nat. Cell Biol.4, 691–698. · DOI · Paper page
  15. Merrifield, C. J., Qualmann, B., Kessels, M. M., and Almers, W. (2004). Neural Wiskott Aldrich Syndrome Protein (N-WASP) and the Arp2/3 complex are recruited to sites of clathrin-mediated endocytosis in cultured fibroblasts.Eur. J. Cell Biol.83, 13–18. · DOI
  16. Mintz, L., Galperin, E., Pasmanik-Chor, M., Tulzinsky, S., Bromberg, Y., Kozak, C. A., Joyner, A., Fein, A., and Horowitz, M. (1999). EHD1–an EH-domain-containing protein with a specific expression pattern.Genomics59, 66–76. · DOI · Paper page
  17. 10.1091/mbc.e03-10-0733 · DOI
  18. Picciano, J. A., Ameen, N., Grant, B. D., and Bradbury, N. A. (2003). Rme-1 regulates the recycling of the cystic fibrosis transmembrane conductance regulator.Am. J. Physiol.285, C1009–C1018. · DOI
  19. Pohl, U., Smith, J. S., Tachibana, I., Ueki, K., Lee, H. K., Ramaswamy, S., Wu, Q., Mohrenweiser, H. W., Jenkins, R. B., and Louis, D. N. (2000). EHD2, EHD3, and EHD4 encode novel members of a highly conserved family of EH domain-containing proteins.Genomics63, 255–262. · DOI
  20. Qualmann, B., Boeckers, T. M., Jeromin, M., Gundelfinger, E. D., and Kessels, M. M. (2004). Linkage of the actin cytoskeleton to the postsynaptic density via direct interactions of Abp1 with the ProSAP/Shank family.J. Neurosci.24, 2481–2495. · DOI · Paper page
  21. Qualmann, B., and Kelly, R. B. (2000). Syndapin isoforms participate in receptor-mediated endocytosis and actin organization.J. Cell Biol.148, 1047–1062. · DOI
  22. Qualmann, B., and Kessels, M. M. (2002). Endocytosis and the cytoskeleton.Int. Rev. Cytol.220, 93–144. · DOI
  23. Qualmann, B., Kessels, M. M., and Kelly, R. B. (2000). Molecular links between endocytosis and the actin cytoskeleton.J. Cell Biol.150, F111–F116. · DOI
  24. 10.1091/mbc.10.2.501 · DOI
  25. Ren, M., Xu, G., Zeng, J., De Lemos-Chiarandini, C., Adesnik, M., and Sabatini, D. D. (1998). Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes.Proc. Natl. Acad. Sci. USA95, 6187–6192. · DOI · Paper page
  26. Salcini, A. E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P. G., and Di Fiore, P. P. (1997). Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module.Genes Dev.11, 2239–2249. · DOI · Paper page
  27. Schneider, C., Newman, R. A., Sutherland, D. R., Asser, U., and Greaves, M. F. (1982). A one-step purification of membrane proteins using a high efficiency immunomatrix.J. Biol. Chem.257, 10766–10769. · DOI
  28. Seidenbecher, C. I.et al. (2004). Caldendrin but not calmodulin binds to light chain 3 of MAP1A/B: an association with the microtubule cytoskeleton highlighting exclusive binding partners for neuronal Ca(2+)-sensor proteins.J. Mol. Biol.336, 957–970. · DOI
  29. Simpson, F., Hussain, N. K., Qualmann, B., Kelly, R. B., Kay, B. K., McPherson, P. S., and Schmid, S. L. (1999). SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation.Nat. Cell Biol.1, 119–124. · DOI
  30. Slepnev, V. I., and De Camilli, P. (2000). Accessory factors in clathrin-dependent synaptic vesicle endocytosis.Nat. Rev. Neurosci.1, 161–172. · DOI
  31. Stoorvogel, W., Oorschot, V., and Geuze, H. J. (1996). A novel class of clathrin-coated vesicles budding from endosomes.J. Cell Biol.132, 21–33. · DOI
  32. van Dam, E. M., Ten Broeke, T., Jansen, K., Spijkers, P., and Stoorvogel, W. (2002). Endocytosed transferrin receptors recycle via distinct dynamin and phosphatidylinositol 3-kinase-dependent pathways.J. Biol. Chem.277, 48876–48883. · DOI
  33. Xu, Y., Shi, H., Wei, S., Wong, S. H., and Hong, W. (2004). Mutually exclusive interactions of EHD1 with GS32 and syndapin II.Mol. Membr. Biol.21, 269–277. · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Braun, A., Pinyol, R., Dahlhaus, R., Koch, D., Fonarev, P., Grant, B. D., Kessels, M. M., & Qualmann, B.
Affiliations
  • Department of Neurochemistry and Molecular Biology, Leibniz Institute for Neurobiology, D-39118 Magdeburg, Germany
  • Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, NJ 08854
Venue
Molecular Biology of the Cell
Publisher
American Society for Cell Biology (ASCB)
Published
2005-08
Volume
16
Issue
8
Pages
3642-3658
ISSN
  • 1059-1524
  • 1939-4586
DOI
10.1091/mbc.e05-01-0076
Cited by
151
References
2
Language
en

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