The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
ATP-dependent membrane remodeling links EHD1 functions to endocytic recycling
Abstract
Endocytic and recycling pathways generate cargo-laden transport carriers by membrane fission. Classical dynamins, which generate transport carriers during endocytosis, constrict and cause fission of membrane tubes in response to GTP hydrolysis. Relatively, less is known about the ATP-binding Eps15-homology domain-containing protein1 (EHD1), a dynamin family member that functions at the endocytic-recycling compartment. Here, we show using cross complementation assays in C. elegans that EHD1’s membrane binding and ATP hydrolysis activities are necessary for endocytic recycling. Further, we show that ATP-bound EHD1 forms membrane-active scaffolds that bulge tubular model membranes. ATP hydrolysis promotes scaffold self-assembly, causing the bulge to extend and thin down intermediate regions on the tube. On tubes below 25 nm in radius, such thinning leads to scission. Molecular dynamics simulations corroborate this scission pathway. Deletion of N-terminal residues causes defects in stable scaffolding, scission and endocytic recycling. Thus, ATP hydrolysis-dependent membrane remodeling links EHD1 functions to endocytic recycling.
Overview
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.
Integrity signals
Registry
Cites
Statistics
Verification
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.
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?
In the citing paper
“Recent studies suggest that a dynamin-homolog, Eps15 homology domain protein 1, catalyzes fission and releases endosome-derived vesicles for recycling to the plasma membrane.”
From Sorting nexin 17 (SNX17) links endosomal sorting to Eps15 homology domain protein 1 (EHD1)–mediated fission machinery (2020) · cites this paper as [17]
In the citing paper
“The process of endosomal fission mediated by EHD1 is highly complex”
From Sorting nexin 17 (SNX17) links endosomal sorting to Eps15 homology domain protein 1 (EHD1)–mediated fission machinery (2020) · cites this paper as [17]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
A High Precision Survey of the Molecular Dynamics of Mammalian Clathrin-Mediated Endocytosis
Taylor, M. J., Perrais, D., & Merrifield, C. J. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000604 · Cited by 754
Bhattacharyya, S., Rainey, M. A., Arya, P., Mohapatra, B. C., Mushtaq, I., Dutta, S., George, M., Storck, M. D., McComb, R. D., Muirhead, D., et al. (2016) · Scientific Reports · doi:10.1038/srep20727 · Cited by 36
Flagged first, then by citations
Research works printed but not linked: 68
- Bonifacino, J. S. & Rojas, R. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7, 568–579 (2006). · DOI
- Grant, B. D. & Donaldson, J. G. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597–608 (2009). · DOI · Paper page
- Maxfield, F. R. & McGraw, T. E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121–132 (2004). · DOI · Paper page
- Caplan, S. et al. 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 (2002). · DOI · Paper page
- Grant, B. D. & Caplan, S. Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9, 2043–2052 (2008). · DOI · Paper page
- Lin, S. X., Grant, B., Hirsh, D. & Maxfield, F. R. Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3, 567–572 (2001). · DOI · Paper page
- Blume, J. J., Halbach, A., Behrendt, D., Paulsson, M. & Plomann, M. EHD proteins are associated with tubular and vesicular compartments and interact with specific phospholipids. Exp. Cell Res. 313, 219–231 (2007). · DOI
- Daumke, O. et al. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923–927 (2007). · DOI · Paper page
- Sharma, M., Naslavsky, N. & Caplan, S. A role for EHD4 in the regulation of early endosomal transport. Traffic 9, 995–1018 (2008). · DOI · Paper page
- Grant, B. et al. Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573–579 (2001). · DOI
- Olswang-Kutz, Y. et al. Drosophila Past1 is involved in endocytosis and is required for germline development and survival of the adult fly. J. Cell Sci. 122, 471–480 (2009). · DOI
- Rainey, M. A. et al. The endocytic recycling regulator EHD1 is essential for spermatogenesis and male fertility in mice. BMC Dev. Biol. 10, 1 (2010). · DOI · Paper page
- Lu, Q. et al. Early steps in primary cilium assembly require EHD1/EHD3-dependent ciliary vesicle formation. Nat. Cell Biol. 17, 531–531 (2015). · DOI
- Cai, B. et al. Differential roles of C-terminal Eps15 homology domain proteins as vesiculators and tubulators of recycling endosomes. J. Biol. Chem. 288, 30172–30180 (2013). · DOI
- Lee, S. et al. Transport through recycling endosomes requires EHD1 recruitment by a phosphatidylserine translocase. EMBO J. 34, 669–688 (2015). · DOI
- Cai, B., Caplan, S. & Naslavsky, N. cPLA2α and EHD1 interact and regulate the vesiculation of cholesterol-rich, GPI-anchored, protein-containing endosomes. Mol. Biol. Cell 23, 1874–1888 (2012). · DOI · Paper page
- Pant, S. et al. AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat. Cell Biol. 11, 1399–1410 (2009). · DOI · Paper page
- Rapaport, D. et al. Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7, 52–60 (2006). · DOI · Paper page
- George, M. et al. Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans. BMC Cell Biol. 8, 3 (2007). · DOI · Paper page
- Giridharan, S. S. P., Cai, B., Vitale, N., Naslavsky, N. & Caplan, S. Cooperation of MICAL-L1, syndapin2, and phosphatidic acid in tubular recycling endosome biogenesis. Mol. Biol. Cell 24, 1776–1790 (2013). · DOI
- Jović, M., Kieken, F., Naslavsky, N., Sorgen, P. L. & Caplan, S. Eps15 homology domain 1-associated tubules contain phosphatidylinositol-4-phosphate and phosphatidylinositol-(4,5)-bisphosphate and are required for efficient recycling. Mol. Biol. Cell 20, 2731–2743 (2009). · DOI · Paper page
- Simone, L. C., Caplan, S. & Naslavsky, N. Role of Phosphatidylinositol 4,5-Bisphosphate in regulating EHD2 plasma membrane localization. PLoS ONE 8, e74519 (2013). · DOI
- Ramachandran, R. & Schmid, S. L. Real-time detection reveals that effectors couple dynamin’s GTP-dependent conformational changes to the membrane. EMBO J. 27, 27–37 (2007). · DOI
- Stowell, M., Marks, B., Wigge, P. & McMahon, H. T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat. Cell Biol. 1, 27–32 (1999). · DOI
- Hoernke, M. et al. EHD2 restrains dynamics of caveolae by an ATP-dependent, membrane-bound, open conformation. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1614066114 (2017). · DOI
- Dar, S., Kamerkar, S. C. & Pucadyil, T. J. A high-throughput platform for real-time analysis of membrane fission reactions reveals dynamin function. Nat. Cell Biol. 17, 1588–1596 (2015). · DOI
- Dar, S., Kamerkar, S. C. & Pucadyil, T. J. Use of the supported membrane tube assay system for real-time analysis of membrane fission reactions. Nat. Protoc. 12, 390–400 (2017). · DOI
- Xie, S. et al. The endocytic recycling compartment maintains cargo segregation acquired upon exit from the sorting endosome. Mol. Biol. Cell 27, 108–126 (2016). · DOI
- Yeung, T. et al. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210–213 (2008). · DOI
- Lee, D.-W. et al. ATP binding regulates oligomerization and endosome association of RME-1 family proteins. J. Biol. Chem. 280, 17213–17220 (2005). · DOI
- Kunding, A. H., Mortensen, M. W., Christensen, S. M. & Stamou, D. A fluorescence-based technique to construct size distributions from single-object measurements: application to the extrusion of lipid vesicles. Biophys. J. 95, 1176–1188 (2008). · DOI
- Roux, A. et al. Membrane curvature controls dynamin polymerization. Proc. Natl Acad. Sci. USA 107, 4141–4146 (2010). · DOI
- Shnyrova, A. V. et al. Geometric catalysis of membrane fission driven by flexible dynamin rings. Science 339, 1433–1436 (2013). · DOI
- Chappie, J. S. et al. A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209–222 (2011). · DOI
- Shah, C. et al. Structural insights into membrane interaction and caveolar targeting of dynamin-like EHD2. Structure 22, 409–420 (2014). · DOI
- Zhao, H. et al. Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4, 1213–1223 (2013). · DOI
- Simunovic, M. et al. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 170, 172–184 (2017). e11. · DOI
- Kozlovsky, Y. & Kozlov, M. M. Membrane fission: model for intermediate structures. Biophys. J. 85, 85–96 (2003). · DOI
- Frolov, V. A., Escalada, A., Akimov, S. A. & Shnyrova, A. V. Geometry of membrane fission. Chem. Phys. Lipids 185, 129–140 (2015). · DOI
- Melikyan, G. B., Deriy, B. N., Ok, D. C. & Cohen, F. S. Voltage-dependent translocation of R18 and DiI across lipid bilayers leads to fluorescence changes. Biophys. J. 71, 2680–2691 (1996). · DOI
- Mattila, J.-P. et al. A hemi-fission intermediate links two mechanistically distinct stages of membrane fission. Nature 524, 109–113 (2015). · DOI
- Melo, A. A. et al. Structural insights into the activation mechanism of dynamin-like EHD ATPases. Proc. Natl Acad. Sci. USA 114, 5629–5634 (2017). · DOI
- Daumke, O., Roux, A. & Haucke, V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell 156, 882–892 (2014). · DOI
- McMahon, H. T. & Gallop, J. L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nat. Cell Biol. 438, 590–596 (2005).
- Jarsch, I. K., Daste, F. & Gallop, J. L. Membrane curvature in cell biology: an integration of molecular mechanisms. J. Cell Biol. 214, 375–387 (2016). · DOI
- Chappie, J. S., Acharya, S., Leonard, M., Schmid, S. L. & Dyda, F. G domain dimerization controls dynamin’s assembly-stimulated GTPase activity. Nature 465, 435–440 (2010). · DOI
- Carr, J. F. & Hinshaw, J. E. Dynamin assembles into spirals under physiological salt conditions upon the addition of GDP and gamma-phosphate analogues. J. Biol. Chem. 272, 28030–28035 (1997). · DOI
- Stoeber, M. et al. Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin. EMBO J. 31, 2350–2364 (2012). · DOI
- Yeow, I. et al. EHD proteins cooperate to generate caveolar clusters and to maintain caveolae during repeated mechanical stress. Curr. Biol. 27, 2951–2962 (2017). · DOI
- Braun, A. et al. EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol. Biol. Cell 16, 3642–3658 (2005). · DOI · Paper page
- Delevoye, C. et al. Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Rep. 6, 445–454 (2014). · DOI
- Hopkins, C. R. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 35, 321–330 (1983). · DOI
- Yamashiro, D. J., Tycko, B., Fluss, S. R. & Maxfield, F. R. Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37, 789–800 (1984). · DOI
- Antonny, B. et al. Membrane fission by dynamin: what we know and what we need to know. EMBO J. 35, 2270–2284 (2016). · DOI
- Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974). · DOI
- Mello, C. & Fire, A. DNA transformation. Methods Cell Biol. 48, 451–482 (1995). · DOI
- Baykov, A. A., Evtushenko, O. A. & Avaeva, S. M. A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal. Biochem. 171, 266–270 (1988). · DOI
- Dar, S. & Pucadyil, T. J. The pleckstrin-homology domain of dynamin is dispensable for membrane constriction and fission. Mol. Biol. Cell 28, 152–160 (2017). · DOI
- Yguerabide, J., Schmidt, J. A. & Yguerabide, E. E. Lateral mobility in membranes as detected by fluorescence recovery after photobleaching. Biophys. J. 40, 69–75 (1982). · DOI
- Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). · DOI · Paper page
- Srivastava, A. & Voth, G. A. Hybrid approach for highly coarse-grained lipid bilayer models. J. Chem. Theory Comput. 9, 750–765 (2012). · DOI
- Simunovic, M., Srivastava, A. & Voth, G. A. Linear aggregation of proteins on the membrane as a prelude to membrane remodeling. Proc. Natl Acad. Sci. USA 110, 20396–20401 (2013). · DOI
- Simunovic, M. & Voth, G. A. Membrane tension controls the assembly of curvature-generating proteins. Nat. Commun. 6, 7219 (2015). · DOI
- Izvekov, S. & Voth, G. A. A multiscale coarse-graining method for biomolecular systems. J. Phys. Chem. B 109, 2469–2473 (2005). · DOI
- Noid, W. G. et al. The multiscale coarse-graining method. I. A rigorous bridge between atomistic and coarse-grained models. J. Chem. Phys. 128, 244114 (2008). · DOI
- Fuhrmans, M. & Müller, M. Coarse-grained simulation of dynamin-mediated fission. Soft Matter 11, 1464–1480 (2015). · DOI
- Reynwar, B. J. et al. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447, 461–464 (2007). · DOI
- Plimpton, S. Fast Parallel Algorithms for short-range molecular dynamics. J. Comput. Phys. 117, 1–19 (1995). · DOI · Paper page
Cited by
Sorted by citations
Spoiled for Choice: Diverse Endocytic Pathways Function at the Cell Surface
Thottacherry, J. J., Sathe, M., Prabhakara, C., & Mayor, S. (2019) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062710 · Cited by 122
Dhawan, K., Naslavsky, N., & Caplan, S. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.011368 · Cited by 36
Metadata
- Authors
- Deo, R., Kushwah, M. S., Kamerkar, S. C., Kadam, N. Y., Dar, S., Babu, K., Srivastava, A., & Pucadyil, T. J.
- Venue
- Nature Communications
- Published
- 2018-12-05
- Volume
- 9
- Issue
- 1
- ISSN
- 2041-1723
- PMC
- PMC6281616
- Cited by
- 77
- 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