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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

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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Research works printed but not linked: 68

  1. Bonifacino, J. S. & Rojas, R. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7, 568–579 (2006). · DOI
  2. Grant, B. D. & Donaldson, J. G. Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597–608 (2009). · DOI · Paper page
  3. Maxfield, F. R. & McGraw, T. E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121–132 (2004). · DOI · Paper page
  4. 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
  5. Grant, B. D. & Caplan, S. Mechanisms of EHD/RME-1 protein function in endocytic transport. Traffic 9, 2043–2052 (2008). · DOI · Paper page
  6. 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
  7. 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
  8. Daumke, O. et al. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 449, 923–927 (2007). · DOI · Paper page
  9. 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
  10. 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
  11. 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
  12. 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
  13. 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
  14. 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
  15. Lee, S. et al. Transport through recycling endosomes requires EHD1 recruitment by a phosphatidylserine translocase. EMBO J. 34, 669–688 (2015). · DOI
  16. 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
  17. 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
  18. Rapaport, D. et al. Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 7, 52–60 (2006). · DOI · Paper page
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. Yeung, T. et al. Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210–213 (2008). · DOI
  30. 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
  31. 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
  32. Roux, A. et al. Membrane curvature controls dynamin polymerization. Proc. Natl Acad. Sci. USA 107, 4141–4146 (2010). · DOI
  33. Shnyrova, A. V. et al. Geometric catalysis of membrane fission driven by flexible dynamin rings. Science 339, 1433–1436 (2013). · DOI
  34. Chappie, J. S. et al. A pseudoatomic model of the dynamin polymer identifies a hydrolysis-dependent powerstroke. Cell 147, 209–222 (2011). · DOI
  35. Shah, C. et al. Structural insights into membrane interaction and caveolar targeting of dynamin-like EHD2. Structure 22, 409–420 (2014). · DOI
  36. Zhao, H. et al. Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep. 4, 1213–1223 (2013). · DOI
  37. Simunovic, M. et al. Friction mediates scission of tubular membranes scaffolded by BAR proteins. Cell 170, 172–184 (2017). e11. · DOI
  38. Kozlovsky, Y. & Kozlov, M. M. Membrane fission: model for intermediate structures. Biophys. J. 85, 85–96 (2003). · DOI
  39. Frolov, V. A., Escalada, A., Akimov, S. A. & Shnyrova, A. V. Geometry of membrane fission. Chem. Phys. Lipids 185, 129–140 (2015). · DOI
  40. 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
  41. Mattila, J.-P. et al. A hemi-fission intermediate links two mechanistically distinct stages of membrane fission. Nature 524, 109–113 (2015). · DOI
  42. 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
  43. Daumke, O., Roux, A. & Haucke, V. BAR domain scaffolds in dynamin-mediated membrane fission. Cell 156, 882–892 (2014). · DOI
  44. McMahon, H. T. & Gallop, J. L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nat. Cell Biol. 438, 590–596 (2005).
  45. 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
  46. 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
  47. 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
  48. 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
  49. 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
  50. 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
  51. Delevoye, C. et al. Recycling endosome tubule morphogenesis from sorting endosomes requires the kinesin motor KIF13A. Cell Rep. 6, 445–454 (2014). · DOI
  52. Hopkins, C. R. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 35, 321–330 (1983). · DOI
  53. 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
  54. Antonny, B. et al. Membrane fission by dynamin: what we know and what we need to know. EMBO J. 35, 2270–2284 (2016). · DOI
  55. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974). · DOI
  56. Mello, C. & Fire, A. DNA transformation. Methods Cell Biol. 48, 451–482 (1995). · DOI
  57. 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
  58. 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
  59. 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
  60. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012). · DOI · Paper page
  61. Srivastava, A. & Voth, G. A. Hybrid approach for highly coarse-grained lipid bilayer models. J. Chem. Theory Comput. 9, 750–765 (2012). · DOI
  62. 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
  63. Simunovic, M. & Voth, G. A. Membrane tension controls the assembly of curvature-generating proteins. Nat. Commun. 6, 7219 (2015). · DOI
  64. Izvekov, S. & Voth, G. A. A multiscale coarse-graining method for biomolecular systems. J. Phys. Chem. B 109, 2469–2473 (2005). · DOI
  65. 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
  66. Fuhrmans, M. & Müller, M. Coarse-grained simulation of dynamin-mediated fission. Soft Matter 11, 1464–1480 (2015). · DOI
  67. Reynwar, B. J. et al. Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447, 461–464 (2007). · DOI
  68. Plimpton, S. Fast Parallel Algorithms for short-range molecular dynamics. J. Comput. Phys. 117, 1–19 (1995). · DOI · Paper page

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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.
Venue
Nature Communications
Published
2018-12-05
Volume
9
Issue
1
ISSN
2041-1723
Cited by
77
References
2
Language
en

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