Curvature-driven feedback on aggregation–diffusion of proteins in lipid bilayers

Mahapatra, Arijit; Saintillan, David; Rangamani, Padmini

doi:10.1039/d1sm00502b

Cited by 21 publications

(19 citation statements)

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“…Energy minimization results in where is an effective tension. This relationship is reminiscent of the radius of a tube extruded using a pulling force, ( 4 ), with an effective tension λ eff that accounts for the tension contributions from the protein coat ( 27, 37–39 ). We compared our theoretical prediction against simulations for two different values of κ (Figure 5a).…”

Section: Resultsmentioning

confidence: 99%

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Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Mahapatra

Rangamani

2022

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Plasma membrane tubes are ubiquitous in cellular membranes and in the membranes of intracellular organelles. They play crucial roles in trafficking, ion transport, and cellular motility. The formation of plasma membrane tubes can be due to localized forces acting on the membrane or by curvature-induced by membrane-bound proteins. Here, we present a mathematical framework to model cylindrical tubular protrusions formed by proteins that induce anisotropic spontaneous curvature. Our analysis revealed that the tube radius depends on an effective tension that includes contributions from the bare membrane tension and the protein-induced curvature. We also found that the length of the tube undergoes an abrupt transition from a short, dome-shaped membrane to a long cylinder and this transition is characteristic of a snapthrough instability. Finally, we show that the snapthrough instability depends on the different parameters including coat area, bending modulus, and extent of protein-induced curvature. Our findings have implications for tube formation due to BAR-domain proteins in processes such as endocytosis, t-tubule formation in myocytes, and cristae formation in mitochondria.1Significance StatementCylindrical tubes are ubiquitous on cellular membranes and many studies have focused on how forces can give rise to tubes. How do curvature-inducing proteins, in the absence of forces, form cylindrical tubes on lipid bilayers? The answer to this question relies on minimizing the bending energy of the membrane to accommodate two different principal curvatures such that a cylindrical shape is an energy minimizer. Here, we build on previous works to develop such a model and show that the formation of an elongated cylindrical tube is accompanied by a snapthrough transition in the bending energy. Furthermore, we identify how this transition depends on different membrane properties, providing a landscape for comparing with different experimental observations. These findings have implications for our understanding how tubes forms in different cellular processes including trafficking, mitochondrial inner membrane cristae formation, and T-tubule formation in myocytes.

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Section: Resultsmentioning

confidence: 99%

“…The tangential force balance relation reduces to ( 22, 29, 35, 36 ) where λ is the Lagrange multiplier for area constraints. Physically it represents the tension in the plane of the membrane ( 28, 37–39 ). W , α | exp in Equation (7) represents the explicit dependence of the energy on the coordinates ( 35, 36 ).…”

Section: Model Developmentmentioning

confidence: 99%

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Mahapatra

Rangamani

2022

Preprint

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“…The bulk-surface coupling between the cytosol and the synaptic membrane is likely a crucial mediator of AMPAR density [45,[60][61][62]. Additionally, surface diffusion is also an important parameter for governing the receptor dynamics [63][64][65][66]. Here, we developed a spatiotemporal model to investigate how spine morphology, trafficking, and signaling interact to regulate AMPAR density at the PSD.…”

Section: • Role Of Traffickingmentioning

confidence: 99%

Spatiotemporal modeling reveals geometric dependence of AMPAR dynamics on dendritic spine morphology

Bell

Lee

Rangamani

2022

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The modification of neural circuits depends on the strengthening and weakening of synaptic connections. Synaptic strength is often correlated to the density of the ionotropic, glutamateric receptors, AMPAR, (α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor) at the postsynaptic density (PSD). While AMPAR density is known to change based on complex biological signaling cascades, the effect of geometric factors such as dendritic spine shape, size, and curvature remain poorly understood. In this work, we developed a deterministic, spatiotemporal model to study the dynamics of AMPAR during long term potentiation (LTP). This model includes a minimal set of biochemical events that represent the upstream signaling events, trafficking of AMPAR to and from the PSD, lateral diffusion in the plane of the spine membrane, and the presence of an extrasynaptic AMPAR pool. Using idealized and realistic spine geometries, we show that the dynamics and increase of bound AMPAR at the PSD depends on a combination of endo- and exocytosis, membrane diffusion, availability of free AMPAR, and intracellular signaling interactions. We also found non-monotonic relationships between spine volume and change in AMPAR at the PSD, suggesting that spines restrict changes in AMPAR to optimize resources and prevent runaway potentiation.

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“…In general, there are many ways to implement such a coupling. For example, the local concentration of proteins can drive shape deformations as well as protein transport on and onto the manifold through local bending of the membrane [30,37,57], active stresses in the form of myosin contractility [39,58,59] or actin polymerization [47,58].…”

Section: Self-organized Mechanochemical Couplingmentioning

confidence: 99%

Geometry-induced patterns through mechanochemical coupling

Würthner¹,

Goychuk²,

Frey³

2022

Preprint

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Curvature-driven feedback on aggregation–diffusion of proteins in lipid bilayers

Abstract: Membrane bending is an extensively studied problem from both modeling and experimental perspectives because of the wide implications of curvature generation in cell biology. Many of the curvature generating aspects...

Cited by 21 publications

References 64 publications

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Formation of protein-mediated bilayer tubes is governed by a snapthrough transition

Spatiotemporal modeling reveals geometric dependence of AMPAR dynamics on dendritic spine morphology

Geometry-induced patterns through mechanochemical coupling

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