Dynamic clustering of dynamin-amphiphysin helices regulates membrane constriction and fission coupled with GTP hydrolysis

Takeda, Tetsuya; Kozai, Toshiya; Yang, Huiran; Ishikuro, Daiki; Seyama, Kaho; Kumagai, Yusuke; Abe, Tadashi; Yamada, Hiroshi; Uchihashi, Takayuki; Ando, Toshio; Takei, Kohji

doi:10.7554/elife.30246

Cited by 42 publications

(42 citation statements)

References 52 publications

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“…4G). This establishes an interesting similarity between FtsZ and dynamin, in which GTP hydrolysis also triggers a super-constricted state, favoring fragmentation and clustering (19,20). We conclude that these torques represent a robust constriction mechanism for cylindrically shaped membranes.…”

supporting

confidence: 55%

Bidirectional FtsZ filament treadmilling transforms lipid membranes via torsional stress

Ramirez-Diaz

Merino‐Salomón

Heymann

et al. 2019

Preprint

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FtsZ is a key component in bacterial cell division, being the primary protein of the presumably contractile Z ring. Reconstituted in vitro, it shows two distinctive features that could so far however not be mechanistically linked: self-organization into directionally treadmilling vortices on solid supported membranes, and shape deformation of flexible liposomes. In cells, circumferential treadmilling of FtsZ was shown to recruit septum-building enzymes, but an active force production remains elusive. To determine direct contributions of FtsZ to membrane constriction, we designed a novel in vitro assay based on soft lipid tubes pulled from FtsZ decorated giant lipid vesicles (GUVs) by optical tweezers. FtsZ actively transformed these tubes into spring-like structures, where GTPase activity promoted spring compression. Operating the optical tweezers in lateral vibration mode and assigning spring constants to FtsZ coated tubes, we found that that FtsZ indeed exerts pN forces upon GTP hydrolysis, through torsional stress induced by bidirectional treadmilling.

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supporting

confidence: 55%

Bidirectional FtsZ filament treadmilling transforms lipid membranes via torsional stress

Ramirez-Diaz

Merino‐Salomón

Heymann

et al. 2019

Preprint

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“…In fluorescence experiments with pre-formed tubules pulled with optical tweezers from GUVs, the membrane coverages 44 ± 27% of endophilin N-BAR domains and 37 ± 9% of β2 centaurin BAR domains have been measured along the tubules (45). Sparse but regular arrangements on membrane tubules have been recently observed for dynamin-amphiphysin complexes (46).…”

Section: Discussionmentioning

confidence: 91%

Membrane Morphologies Induced by Arc-Shaped Scaffolds Are Determined by Arc Angle and Coverage

Bonazzi

Weikl

2019

Biophysical Journal

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The intricate shapes of biological membranes such as tubules and membrane stacks are induced by proteins. In this article, we systematically investigate the membrane shapes induced by arc-shaped scaffolds such as proteins and protein complexes with coarse-grained modeling and simulations. We find that arc-shaped scaffolds induce membrane tubules at membrane coverages larger than a threshold of about 40%, irrespective of their arc angle. The membrane morphologies at intermediate coverages below this tubulation threshold, in contrast, strongly depend on the arc angle. Scaffolds with arc angles of about 60°akin to N-BAR domains do not change the membrane shape at coverages below the tubulation threshold, while scaffolds with arc angles larger than about 120°induce double-membrane stacks at intermediate coverages. The scaffolds stabilize the curved membrane edges that connect the membrane stacks, as suggested for complexes of reticulon proteins. Our results provide general insights on the determinants of membrane shaping by arc-shaped scaffolds .

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“…In recent years, several structural and theoretical models have proposed that tilting of the PH domains promotes membrane fission by applying torque to the lipid bilayer and therefore, plays a key role in the membrane fission function of dynamin (20)(21)(22). Additionally, evidence, such as decrease in the fluorescence of labeled dynamin scaffolds (11), variations in the conductance of dynamin-coated tubes (12), and clustering of dynamin-amphiphysin complexes (23), suggests that GTP hydrolysis results in a partial breakup of the dynamin helix, indicating that the equilibrium length of the constricted oligomer is reduced (24).…”

mentioning

confidence: 99%

“…Recently, high-speed atomic force microscopy (AFM) has been utilized to characterize the morphology of the membranedynamin system (23,25). The high spatial and temporal resolutions of these measurements have revealed that GTP hydrolysis results in a dynamic alteration of the oligomer's shape (25).…”

mentioning

confidence: 99%

The tilted helix model of dynamin oligomers

Kadosh

Colom

Yellin

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Dynamin proteins assemble into characteristic helical structures around necks of clathrin-coated membrane buds. Hydrolysis of dynamin-bound GTP results in both fission of the membrane neck and partial disruption of the dynamin oligomer. Imaging by atomic force microscopy reveals that, on GTP hydrolysis, dynamin oligomers undergo a dynamic remodeling and lose their distinctive helical shape. While breakup of the dynamin helix is a critical stage in clathrin-mediated endocytosis, the mechanism for this remodeling of the oligomer has not been resolved. In this paper, we formulate an analytical, elasticity-based model for the reshaping and disassembly of the dynamin scaffold. We predict that the shape of the oligomer is modulated by the orientation of dynamin’s pleckstrin homology (PH) domain relative to the underlying membrane. Our results indicate that tilt of the PH domain drives deformation and fragmentation of the oligomer, in agreement with experimental observations. This model motivated the introduction of the tilted helix: a curve that maintains a fixed angle between its normal and the normal of the embedding surface. Our findings highlight the importance of tilt as a key regulator of size and morphology of membrane-bound oligomers.

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Dynamic clustering of dynamin-amphiphysin helices regulates membrane constriction and fission coupled with GTP hydrolysis

Cited by 42 publications

References 52 publications

Bidirectional FtsZ filament treadmilling transforms lipid membranes via torsional stress

Bidirectional FtsZ filament treadmilling transforms lipid membranes via torsional stress

Membrane Morphologies Induced by Arc-Shaped Scaffolds Are Determined by Arc Angle and Coverage

The tilted helix model of dynamin oligomers

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