Biophysical properties governing septin assembly

Woods, Benjamin; Seim, Ian; Liu, Jessica; McLaughlin, Grace A.; Cannon, Kevin S.; Gladfelter, Amy S.

doi:10.1101/2021.03.22.436414

Cited by 6 publications

(5 citation statements)

References 99 publications

(155 reference statements)

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“…The distribution of filament lengths for both Cdc11a- and Cdc11b-capped octamers at steady state could be approximated by a left truncated exponential function, consistent with isodesmic polymer growth models ( Fig. 3 D ; Romberg et al, 2001 ; Skillman et al, 2013 ; Woods et al, 2021 ). Interestingly, septin assembly on curved membranes has been shown to be a cooperative process, where membrane-bound septins drive the recruitment of septins from the solution onto the membrane ( Shi et al, 2022 ).…”

Section: Resultssupporting

confidence: 67%

A gene duplication of a septin reveals a developmentally regulated filament length control mechanism

Cannon

Vargas-Muñiz

Billington

et al. 2023

Journal of Cell Biology

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Septins are a family of conserved filament-forming proteins that function in multiple cellular processes. The number of septin genes within an organism varies, and higher eukaryotes express many septin isoforms due to alternative splicing. It is unclear if different combinations of septin proteins in complex alter the polymers’ biophysical properties. We report that a duplication event within the CDC11 locus in Ashbya gossypii gave rise to two similar but distinct Cdc11 proteins: Cdc11a and Cdc1b. CDC11b transcription is developmentally regulated, producing different amounts of Cdc11a- and Cdc11b-complexes in the lifecycle of Ashbya gossypii. Deletion of either gene results in distinct cell polarity defects, suggesting non-overlapping functions. Cdc11a and Cdc11b complexes have differences in filament length and membrane-binding ability. Thus, septin subunit composition has functional consequences on filament properties and cell morphogenesis. Small sequence differences elicit distinct biophysical properties and cell functions of septins, illuminating how gene duplication could be a driving force for septin gene expansions seen throughout the tree of life.

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Section: Resultssupporting

confidence: 67%

A gene duplication of a septin reveals a developmentally regulated filament length control mechanism

Cannon

Vargas-Muñiz

Billington

et al. 2023

Journal of Cell Biology

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“…We therefore reconstituted septin assembly with recombinant proteins and planar supported lipid bilayers (SLBs) (Figure 4C). The distribution of filament lengths for both Cdc11a and Cdc11b-capped octamers at steady state could be approximated by a single exponential function, consistent with isodesmic polymer growth models (Figure 4D) (Romberg, Simon and Erickson, 2001;Skillman et al, 2013;Woods et al, 2021). Fitting to a single exponential function also allowed us to calculate an average filament length despite the diffraction limit of the light microscope and for Cdc11a octamers was 0.72 µm (~23 octamers) and for Cdc11b octamers 0.52 µm (~16 octamers) (Figure 4D).…”

Section: Identity Of Terminal Subunit Changes the Biophysical Properties Of Septin Filamentssupporting

confidence: 67%

A gene duplication of a septin provides a developmentally-regulated filament length control mechanism

Ks¹,

Billington

et al. 2021

Preprint

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Septins are a family of conserved filament-forming proteins that function in a variety of processes including cell cycle progression, cell morphogenesis and autophagy. Despite their conservation from yeast to humans, the number of septin genes within an organism varies and higher eukaryotes express many septin isoforms due to alternative splicing. It is unclear how variability in septin complex composition influences the biophysical properties of septin polymers. Here we report that a complex duplication event within theCDC11locus in the fungus,Ashbya gossypii, gave rise to two similar, but distinct Cdc11 proteins, Cdc11a and Cdc1b.CDC11btranscription is developmentally regulated producing different ratios of Cdc11a and b complexes duringAshbya’slifecycle. Moreover, deletion of eitherCDC11aorCDC11bresults in distinct cell polarity defects. Remarkably, despite substantial identity in amino acid sequence, Cdc11a and Cdc11b complexes have distinct biophysical properties with clear filament length and membrane-binding ability differences. Thus, septin subunit composition has functional consequences for filament properties and such functional plasticity can be exploited for distinct biophysical properties and cell functions.

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“…To study the assembly process of membrane-bound septins, we used confocal microscopy and measured time-dependent septin adsorption onto membrane-coated beads with assays that were developed and used in our earlier studies ( 9 , 41 ). One main difference between our current and past studies is that here, the adsorption is measured over time, whereas in previous studies, we reported only the adsorption at steady state.…”

Section: Resultsmentioning

confidence: 99%

Curvature sensing as an emergent property of multiscale assembly of septins

Shi

Cannon

Curtis

et al. 2023

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

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The ability of cells to sense and communicate their shape is central to many of their functions. Much is known about how cells generate complex shapes, yet how they sense and respond to geometric cues remains poorly understood. Septins are GTP-binding proteins that localize to sites of micrometer-scale membrane curvature. Assembly of septins is a multistep and multiscale process, but it is unknown how these discrete steps lead to curvature sensing. Here, we experimentally examine the time-dependent binding of septins at different curvatures and septin bulk concentrations. These experiments unexpectedly indicated that septins’ curvature preference is not absolute but rather is sensitive to the combinations of membrane curvatures present in a reaction, suggesting that there is competition between different curvatures for septin binding. To understand the physical underpinning of this result, we developed a kinetic model that connects septins’ self-assembly and curvature-sensing properties. Our experimental and modeling results are consistent with curvature-sensitive assembly being driven by cooperative associations of septin oligomers in solution with the bound septins. When combined, the work indicates that septin curvature sensing is an emergent property of the multistep, multiscale assembly of membrane-bound septins. As a result, curvature preference is not absolute and can be modulated by changing the physicochemical and geometric parameters involved in septin assembly, including bulk concentration, and the available membrane curvatures. While much geometry-sensitive assembly in biology is thought to be guided by intrinsic material properties of molecules, this is an important example of how curvature sensing can arise from multiscale assembly of polymers.

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Biophysical properties governing septin assembly

Cited by 6 publications

References 99 publications

A gene duplication of a septin reveals a developmentally regulated filament length control mechanism

A gene duplication of a septin reveals a developmentally regulated filament length control mechanism

A gene duplication of a septin provides a developmentally-regulated filament length control mechanism

Curvature sensing as an emergent property of multiscale assembly of septins

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