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ATP-dependent membrane remodeling links EHD1 functions to endocytic recycling

Deo, Raunaq, Kushwah, Manish S., Kamerkar, Sukrut C., Kadam, Nagesh Y., Dar, Srishti, Babu, Kavita, Srivastava, Anand, Pucadyil, Thomas J.·2018·Nature Communications
DOI 10.1038/s41467-018-07586-zPMC PMC6281616
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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.

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Figures

Fig. 1 Functional determinants in EHD1 required for endocytic recycling. a Representative DIC and fluorescence images of worms injected with fluorescent BSA. Asterisks mark vacuoles. Scale bars = 50 μm. b Plot showing vacuole numbers per worm for the indicated numbers of worms. Red line denotes the mean. Statistical significance was assessed using an unpaired two-tailed t-test and ****P < 0.0001
Fig. 1 Functional determinants in EHD1 required for endocytic recycling. a Representative DIC and fluorescence images of worms injected with fluorescent BSA. Asterisks mark vacuoles. Scale bars = 50 μm. b Plot showing vacuole numbers per worm for the indicated numbers of worms. Red line denotes the mean. Statistical significance was assessed using an unpaired two-tailed t-test and ****P < 0.0001CC BY · PubMed Central
Fig. 2 Membrane binding and ATPase activity of EHD1. a Representative gel showing results from a sedimentation assay with EHD1 added to liposomes of increasing PS content and spun down to separate the supernatant (S) and pellet (P) fractions. M denotes the marker lane. b Bound fraction and ATPase activity of EHD1 with liposomes of increasing PS content. Data represent mean ± SD for N = 3. c Bound fraction and ATPase activity of EHD1(F322A) with liposomes of increasing PS content. Data represent mean ± SD for N = 3. d Bound fraction and ATPase activity of EHD1 on liposomes of the indicated compositions. Data represent mean ± SD for N = 3. e Liposome-bound fraction of EHD1 with increasing PS with different nucleotides (mean ± SD, N = 3 for Apo, N = 3 for ADP, N = 3 for AMP-PNP, N = 5 for ATP-γ-S). Statistical significance was assessed using an unpaired two-tailed t-test and **P = 0.003, ***P = 0.0001
Fig. 2 Membrane binding and ATPase activity of EHD1. a Representative gel showing results from a sedimentation assay with EHD1 added to liposomes of increasing PS content and spun down to separate the supernatant (S) and pellet (P) fractions. M denotes the marker lane. b Bound fraction and ATPase activity of EHD1 with liposomes of increasing PS content. Data represent mean ± SD for N = 3. c Bound fraction and ATPase activity of EHD1(F322A) with liposomes of increasing PS content. Data represent mean ± SD for N = 3. d Bound fraction and ATPase activity of EHD1 on liposomes of the indicated compositions. Data represent mean ± SD for N = 3. e Liposome-bound fraction of EHD1 with increasing PS with different nucleotides (mean ± SD, N = 3 for Apo, N = 3 for ADP, N = 3 for AMP-PNP, N = 5 for ATP-γ-S). Statistical significance was assessed using an unpaired two-tailed t-test and **P = 0.003, ***P = 0.0001CC BY · PubMed Central
Fig. 3 ATP- and curvature-sensitive membrane binding of EHD1. a Schematic of generation of membrane templates used in the study. b Distribution of tube radii from five independent preparations of templates. c Representative fluorescence micrographs showing distribution of EGFP-LactC2 on SLBs and tubes. Asteriks mark the bare glass surface. Scale bars = 5 μm. d Protein:membrane fluorescence ratios of EHD1-EGFP with various nucleotides (blue) and GFP-LactC2 (red) for the indicated numbers of tubes and SLBs sampled. Black lines denote means. Statistical significance was assessed using Mann–Whitney test and ****P < 0.0001. e Protein:membrane fluorescence ratios of AMP-PNP-bound EHD1-EGFP on tubes of varying starting sizes for the indicated numbers of tubes. Red lines denote means. Statistical significance was assessed using Mann–Whitney’s two-tailed test and *P = 0.010, **P = 0.005, ****P < 0.0001
Fig. 3 ATP- and curvature-sensitive membrane binding of EHD1. a Schematic of generation of membrane templates used in the study. b Distribution of tube radii from five independent preparations of templates. c Representative fluorescence micrographs showing distribution of EGFP-LactC2 on SLBs and tubes. Asteriks mark the bare glass surface. Scale bars = 5 μm. d Protein:membrane fluorescence ratios of EHD1-EGFP with various nucleotides (blue) and GFP-LactC2 (red) for the indicated numbers of tubes and SLBs sampled. Black lines denote means. Statistical significance was assessed using Mann–Whitney test and ****P < 0.0001. e Protein:membrane fluorescence ratios of AMP-PNP-bound EHD1-EGFP on tubes of varying starting sizes for the indicated numbers of tubes. Red lines denote means. Statistical significance was assessed using Mann–Whitney’s two-tailed test and *P = 0.010, **P = 0.005, ****P < 0.0001CC BY · PubMed Central
Fig. 4 EHD1 distribution and dynamics on membranes. Representative fluorescence micrographs showing the distribution of EHD1-EGFP in the Apo, ADP-bound, and AMP-PNP-bound states on SLBs (a) and tubes (b). White and yellow arrowheads mark oligomers of EHD1-EGFP on the SLB and tubes, respectively. Scale bars = 5 μm. c Representative fluorescence micrographs showing the distribution of EHD1-EGFP with ATP-γ-S on the SLB and tubes. Yellow arrowheads mark oligomers of EHD1-EGFP on the tubes. Scale bars = 5 μm. d Representative fluorescence micrographs showing the effect of ATP addition to EHD1-EGFP assembled with ATP-γ-S on the SLB and tubes. Plot shows quantitation of fluorescence intensities of EHD1-EGFP on the SLB and tubes. Data represent mean ± SD of n = 3 ROIs on the SLB and tubes
Fig. 4 EHD1 distribution and dynamics on membranes. Representative fluorescence micrographs showing the distribution of EHD1-EGFP in the Apo, ADP-bound, and AMP-PNP-bound states on SLBs (a) and tubes (b). White and yellow arrowheads mark oligomers of EHD1-EGFP on the SLB and tubes, respectively. Scale bars = 5 μm. c Representative fluorescence micrographs showing the distribution of EHD1-EGFP with ATP-γ-S on the SLB and tubes. Yellow arrowheads mark oligomers of EHD1-EGFP on the tubes. Scale bars = 5 μm. d Representative fluorescence micrographs showing the effect of ATP addition to EHD1-EGFP assembled with ATP-γ-S on the SLB and tubes. Plot shows quantitation of fluorescence intensities of EHD1-EGFP on the SLB and tubes. Data represent mean ± SD of n = 3 ROIs on the SLB and tubesCC BY · PubMed Central
Fig. 5 Membrane remodeling by EHD1. a Representative images and fluorescence line profiles of tubes showing scaffolds of AMP-PNP-bound EHD1-EGFP. b Representative images showing coincidence between GFP and membrane fluorescence in response to formation of extended EHD1 scaffolds with ATP-γ-S. Red arrowheads mark sites of tube thinning. c Representative images and fluorescence line profiles of tubes showing Alexa488-labeled dynamin1 scaffolds. d Pearson’s correlation between protein and membrane fluorescence for the indicated numbers of tubes. Red lines denote means. e Bulged tube radius (Rb) under AMP-PNP-bound EHD1 scaffolds as a function of the starting tube radius for the indicated numbers of tubes. Red lines denote means. f Constricted tube radius (Rc) under dynamin scaffolds as a function of the starting tube radius for the indicated numbers of tubes. Red line denotes means. g Representative images and associated line profiles acquired in the membrane channel showing remodeling of a tube by AMP-PNP-bound EHD1 scaffolds. Green arrowheads mark bulged regions and blue lines mark thinned-down regions on the tube
Fig. 5 Membrane remodeling by EHD1. a Representative images and fluorescence line profiles of tubes showing scaffolds of AMP-PNP-bound EHD1-EGFP. b Representative images showing coincidence between GFP and membrane fluorescence in response to formation of extended EHD1 scaffolds with ATP-γ-S. Red arrowheads mark sites of tube thinning. c Representative images and fluorescence line profiles of tubes showing Alexa488-labeled dynamin1 scaffolds. d Pearson’s correlation between protein and membrane fluorescence for the indicated numbers of tubes. Red lines denote means. e Bulged tube radius (Rb) under AMP-PNP-bound EHD1 scaffolds as a function of the starting tube radius for the indicated numbers of tubes. Red lines denote means. f Constricted tube radius (Rc) under dynamin scaffolds as a function of the starting tube radius for the indicated numbers of tubes. Red line denotes means. g Representative images and associated line profiles acquired in the membrane channel showing remodeling of a tube by AMP-PNP-bound EHD1 scaffolds. Green arrowheads mark bulged regions and blue lines mark thinned-down regions on the tubeCC BY · PubMed Central
Fig. 6 Membrane fission induced by ATP hydrolysis. a Representative fluorescence micrograph after 5 min of adding EHD1-EGFP with ATP to templates (see Supplementary Movie 1). Red arrowheads mark cut ends of tubes and white arrowheads mark tubes that remain uncut. Scale bar = 10 μm. b Tube remodeling and fission probability as a function of starting tube radius for the indicated numbers of tubes. c Representative montage of tube images acquired in the GFP channel showing the nucleation (white arrowheads) and growth of EHD1-EGFP scaffolds in presence of ATP (see Supplementary Movie 3). d Representative montage of tube images acquired in the membrane channel showing the expansion of bulges (white arrowheads). White arrowheads mark the site of onset of bulging and green arrowheads mark sites of tube thinning. e Frames and associated line profiles from a representative movie acquired in the membrane channel showing the bulged (white arrowheads) and thinned-down (green arrowheads) sites on a tube, before fission (yellow arrowheads)
Fig. 6 Membrane fission induced by ATP hydrolysis. a Representative fluorescence micrograph after 5 min of adding EHD1-EGFP with ATP to templates (see Supplementary Movie 1). Red arrowheads mark cut ends of tubes and white arrowheads mark tubes that remain uncut. Scale bar = 10 μm. b Tube remodeling and fission probability as a function of starting tube radius for the indicated numbers of tubes. c Representative montage of tube images acquired in the GFP channel showing the nucleation (white arrowheads) and growth of EHD1-EGFP scaffolds in presence of ATP (see Supplementary Movie 3). d Representative montage of tube images acquired in the membrane channel showing the expansion of bulges (white arrowheads). White arrowheads mark the site of onset of bulging and green arrowheads mark sites of tube thinning. e Frames and associated line profiles from a representative movie acquired in the membrane channel showing the bulged (white arrowheads) and thinned-down (green arrowheads) sites on a tube, before fission (yellow arrowheads)CC BY · PubMed Central
Fig. 7 Intermediates in the membrane-remodeling pathway. a Bulge density per unit length of the tube upon addition of EHD1 with AMP-PNP, ATP-γ-S and ATP for the indicated numbers of tubes. Red line denotes the mean. Statistical significance was assessed using Mann–Whitney’s two-tailed test and ***P < 0.005, ****P < 0.0001. b Plot showing cumulative cuts seen as a function of time (fission rate) upon adding EHD1 with ATP or ATP-γ-S to a collection of tubes. c Plot showing the time interval between membrane bulging and scission (fission time) upon adding EHD1 with ATP or ATP-γ-S to tubes for the indicated numbers of events. Red line denotes the mean. Statistical significance was assessed using Mann–Whitney’s two-tailed test and ****P < 0.0001. d STED microscopic images of EHD1-EGFP scaffolds with ATP-γ-S. White arrowheads mark the possible orientation of helical rungs. e Representative kymograph showing FRAP of an RhPE-containing tube displaying EHD1 scaffolds with ATP-γ-S. f Fluorescence recovery kinetics of RhPE for the indicated conditions. Numbers represent mobile fraction (mean ± SD for n(tubes) as indicated). g Representative kymograph showing fusion and spreading of R18 on a tube displaying EHD1 scaffolds with ATP-γ-S. h Schematic showing growth-induced tube thinning leading to the formation of a hemifused intermediate. Black and red lines depict the outer and inner monolayers, respectively of the tube
Fig. 7 Intermediates in the membrane-remodeling pathway. a Bulge density per unit length of the tube upon addition of EHD1 with AMP-PNP, ATP-γ-S and ATP for the indicated numbers of tubes. Red line denotes the mean. Statistical significance was assessed using Mann–Whitney’s two-tailed test and ***P < 0.005, ****P < 0.0001. b Plot showing cumulative cuts seen as a function of time (fission rate) upon adding EHD1 with ATP or ATP-γ-S to a collection of tubes. c Plot showing the time interval between membrane bulging and scission (fission time) upon adding EHD1 with ATP or ATP-γ-S to tubes for the indicated numbers of events. Red line denotes the mean. Statistical significance was assessed using Mann–Whitney’s two-tailed test and ****P < 0.0001. d STED microscopic images of EHD1-EGFP scaffolds with ATP-γ-S. White arrowheads mark the possible orientation of helical rungs. e Representative kymograph showing FRAP of an RhPE-containing tube displaying EHD1 scaffolds with ATP-γ-S. f Fluorescence recovery kinetics of RhPE for the indicated conditions. Numbers represent mobile fraction (mean ± SD for n(tubes) as indicated). g Representative kymograph showing fusion and spreading of R18 on a tube displaying EHD1 scaffolds with ATP-γ-S. h Schematic showing growth-induced tube thinning leading to the formation of a hemifused intermediate. Black and red lines depict the outer and inner monolayers, respectively of the tubeCC BY · PubMed Central
Fig. 8 Molecular dynamics simulations of scaffold-induced tube bulging and fission. a Frames from simulations of a 4 nm-long scaffold (magenta) on a 100 nm-long membrane tube. Cream and green spheres represent headgroups of DOPS and DOPC lipids, respectively. Light and dark spheres represent headgroups of lipids on the outer and inner leaflet, respectively. Only lipid head groups are shown for clarity (see Supplementary Movie 4). b Lumen radius along the tube length upon placement of a 4 nm-long scaffold. Data represent the mean with variance. Gray lines represent scaffold boundaries. c Frames from simulations of a 20 nm-long scaffold on a 100 nm-long membrane tube. Cream and green spheres represent headgroups of DOPS and DOPC lipids, respectively. Light and dark spheres represent headgroups of lipids on the outer and inner leaflet, respectively. Only lipid head groups are shown for clarity (see Supplementary Movie 5). d Evolution of lumen radius at the middle (blue) and at the site of maximum thinning (red) after placement of a 20 nm-long scaffold. X-axis is in units of 10,000 τ, where τ is a CG time step. e Lumen radius along the tube length upon placement of a 20 nm-long scaffold. Data represent the mean with variance. Gray lines represent scaffold boundaries
Fig. 8 Molecular dynamics simulations of scaffold-induced tube bulging and fission. a Frames from simulations of a 4 nm-long scaffold (magenta) on a 100 nm-long membrane tube. Cream and green spheres represent headgroups of DOPS and DOPC lipids, respectively. Light and dark spheres represent headgroups of lipids on the outer and inner leaflet, respectively. Only lipid head groups are shown for clarity (see Supplementary Movie 4). b Lumen radius along the tube length upon placement of a 4 nm-long scaffold. Data represent the mean with variance. Gray lines represent scaffold boundaries. c Frames from simulations of a 20 nm-long scaffold on a 100 nm-long membrane tube. Cream and green spheres represent headgroups of DOPS and DOPC lipids, respectively. Light and dark spheres represent headgroups of lipids on the outer and inner leaflet, respectively. Only lipid head groups are shown for clarity (see Supplementary Movie 5). d Evolution of lumen radius at the middle (blue) and at the site of maximum thinning (red) after placement of a 20 nm-long scaffold. X-axis is in units of 10,000 τ, where τ is a CG time step. e Lumen radius along the tube length upon placement of a 20 nm-long scaffold. Data represent the mean with variance. Gray lines represent scaffold boundariesCC BY · PubMed Central
Fig. 9 N-terminal residues are critical for EHD1 function. a Alignment of the N-terminal region in EHD proteins. b Representative DIC and fluorescence images of worms injected with fluorescent BSA. Asterisks mark vacuoles. Scale bar = 50 μm. c Plot showing vacuole numbers per worm for the indicated numbers of worms. Red line denotes mean. Data for WT, rme-1 and EHD1rescue are shown for comparison. Statistical significance was assessed using an unpaired two-tailed t-test and ****P < 0.0001. d Bound fraction of EHD1(Δ2–9) with liposomes of increasing PS content (mean ± SD, n = 3). Data for WT is shown for comparison. e ATPase activity of EHD1(Δ2–9) with liposomes of increasing PS content (mean ± SD, n = 3). Data for WT is shown for comparison. f Representative micrograph showing EHD1(Δ2–9) added to templates with ATP after 5 min (see Supplementary Movie 6). Scale bar = 10 μm. g Representative kymograph of tube images acquired in the membrane fluorescence channel showing the formation and dissolution of membrane bulges (white arrowheads)
Fig. 9 N-terminal residues are critical for EHD1 function. a Alignment of the N-terminal region in EHD proteins. b Representative DIC and fluorescence images of worms injected with fluorescent BSA. Asterisks mark vacuoles. Scale bar = 50 μm. c Plot showing vacuole numbers per worm for the indicated numbers of worms. Red line denotes mean. Data for WT, rme-1 and EHD1rescue are shown for comparison. Statistical significance was assessed using an unpaired two-tailed t-test and ****P < 0.0001. d Bound fraction of EHD1(Δ2–9) with liposomes of increasing PS content (mean ± SD, n = 3). Data for WT is shown for comparison. e ATPase activity of EHD1(Δ2–9) with liposomes of increasing PS content (mean ± SD, n = 3). Data for WT is shown for comparison. f Representative micrograph showing EHD1(Δ2–9) added to templates with ATP after 5 min (see Supplementary Movie 6). Scale bar = 10 μm. g Representative kymograph of tube images acquired in the membrane fluorescence channel showing the formation and dissolution of membrane bulges (white arrowheads)CC BY · PubMed Central
Fig. 10 Functional differences between EHD2 and EHD1. a Bound fraction of EHD2 with liposomes of increasing PS content (mean ± SD, N = 3). Data for EHD1 are shown for comparison. b ATPase activity of EHD2 with and without PS liposomes (mean ± SD, N = 3). Data for EHD1 are shown for comparison. c Frames from representative movie showing EHD2 added to templates with ATP acquired at the indicated time periods. Scale bar = 10 μm. d Plot showing the number of tubes cut (as percentage of the total tubes analyzed) with the indicated proteins. Data represent the mean ± SD
Fig. 10 Functional differences between EHD2 and EHD1. a Bound fraction of EHD2 with liposomes of increasing PS content (mean ± SD, N = 3). Data for EHD1 are shown for comparison. b ATPase activity of EHD2 with and without PS liposomes (mean ± SD, N = 3). Data for EHD1 are shown for comparison. c Frames from representative movie showing EHD2 added to templates with ATP acquired at the indicated time periods. Scale bar = 10 μm. d Plot showing the number of tubes cut (as percentage of the total tubes analyzed) with the indicated proteins. Data represent the mean ± SDCC BY · PubMed Central

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Metadata

Authors
Deo, R., Kushwah, M. S., Kamerkar, S. C., Kadam, N. Y., Dar, S., Babu, K., Srivastava, A., & Pucadyil, T. J.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2018-12-05
Volume
9
Issue
1
ISSN
2041-1723
DOI
10.1038/s41467-018-07586-z
PMC
PMC6281616
Cited by
77
References
2
Language
en
Licence

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