Generation of high curvature membranes mediated by direct endophilin bilayer interactions

By K. Farsad, N. Ringstad, K. Takei, Scott R. Floyd, K. Rose, P. De Camilli. Journal of Cell Biology, 2001

615 citations recorded by the source corpus.

Endophilin 1 is a presynaptically enriched protein which binds the GTPase dynamin and the polyphosphoinositide phosphatase synptojanin. Perturbation of endophilin function in cell-free systems and in a living synapse has implicated endophilin in endocytic vesicle budding (Ringstad, N., H. Gad, P. Low, G. Di Paolo, L. Brodin, O. Shupliakov, and P. De Camilli. 1999. Neuron. 24:143–154; Schmidt, A., M. Wolde, C. Thiele, W. Fest, H. Kratzin, A.V. Podtelejnikov, W. Witke, W.B. Huttner, and H.D. Soling. 1999. Nature. 401:133–141; Gad, H., N. Ringstad, P. Low, O. Kjaerulff, J. Gustafsson, M. Wenk, G. Di Paolo, Y. Nemoto, J. Crun, M.H. Ellisman, et al. 2000. Neuron. 27:301–312). Here, we show that purified endophilin can directly bind and evaginate lipid bilayers into narrow tubules similar in diameter to the neck of a clathrin-coated bud, providing new insight into the mechanisms through which endophilin may participate in membrane deformation and vesicle budding. This property of endophilin is independent of its putative lysophosphatydic acid acyl transferase activity, is mediated by its NH2-terminal region, and requires an amino acid stretch homologous to a corresponding region in amphiphysin, a protein previously shown to have similar effects on lipid bilayers (Takei, K., V.I. Slepnev, V. Haucke, and P. De Camilli. 1999. Nat. Cell Biol. 1:33–39). Endophilin cooligomerizes with dynamin rings on lipid tubules and inhibits dynamin's GTP-dependent vesiculating activity. Endophilin B, a protein with homology to endophilin 1, partially localizes to the Golgi complex and also deforms lipid bilayers into tubules, underscoring a potential role of endophilin family members in diverse tubulovesicular membrane-trafficking events in the cell.

Subfields: Cell Biology, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/38bdc751bd9ef9642f2383244b0a09a06214c400

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In Cell Biology

1. H. McMahon
2. M. Lemmon
3. Michael M. Kozlov
4. Aurélien Roux
5. J. Gallop
6. D. Suen
7. Sean D. Conner
8. R. Youle

In Molecular Biology

1. R. Youle
2. H. McMahon
3. M. Lemmon
4. D. Suen
5. M. Karbowski
6. Kristi L. Norris
7. Michael M. Kozlov
8. Aurélien Roux

Citations in the corpus

• Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis (2007, background): “Although Bif-1 has liposome tubulation activity in vitro , it seems that this protein does not localize to transferrin-positive endosome”
• Dynamin, a membrane remodelling GTPase (2012, background): “The potential role of BAR domain-containing proteins has acquired interest with the realization that the GTPase activity of dynamin involves interactions between dynamin rungs because the intercalation of BAR domains between rungs could hinder such an interactio”
• Mitochondrial dynamics and apoptosis. (2008, background): “2004) and deforms lipid bilayers into tubules in vitro (Farsad et al. 2001).”
• Membrane curvature and mechanisms of dynamic cell membrane remodelling (2005, background): “All these N-BAR domains lead to membrane tubulation in vitro”
• Dynamics of mitochondrial morphology in healthy cells and during apoptosis (2003, background): “Interestingly, Bif1, as well as endophilin 1, can directly tubulate liposomes.(87) Bif1-mediated OMM deformations may somehow facilitate Bax interactions”
• How proteins produce cellular membrane curvature (2006, background): “Presumably, the amphipathic N-terminal region of endophilin functions in a similar fashion, independently of its putative enzymatic activit”
• Mitochondrial fission in apoptosis (2005, background): “It binds to dynamin through a Src-homology-3 (SH3) domain and co-spirals with dynamin around lipid tubules in vitro”
• Curvature of clathrin-coated pits driven by epsin (2002, background): “Role of helix 0 in membrane curvature Tubulation of liposomes has been observed with a number of protein”
• Membrane recognition by phospholipid-binding domains (2008, background): “A BAR domain at the N terminus of endophilin has similar membrane-deforming propertie”
• A general amphipathic α-helical motif for sensing membrane curvature (2007, background): “, or as a promoter of membrane curvature in the case of protein coat”
• Regulated portals of entry into the cell (2003, background): “Insight into their specific functions in CCV formation has been gained through in vivo analyses after interfering with protein interactions by overexpression of truncated mutants or peptide microinjection, and more recently through in vitro analysis of their behaviour on model liposome”
• Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. (2005, methodology): “F-BAR Domains Have Powerful Bilayer-Deforming Activity In Vitro BAR domain proteins induce massive tubulation of liposomes in vitro (Farsad et al., 2001; Peter et al., 2004; Takei et al., 1999).”