Scaling of subcellular actin structures with cell length through decelerated growth

McInally, Shane G; Kondev, Jané; Goode, Bruce L.

doi:10.7554/elife.68424

Cited by 17 publications

(19 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…To distinguish between the uninduced and induced cdc28-13 ts cells, we used mother cell length to sort cells into bins containing either 'small' or 'large' cells. To validate this binning strategy, we plotted the cable lengths we measured from these cells and found that the mean cable length in each bin was consistent with our previous measurements (𝐿 𝑐𝑎𝑏𝑙𝑒, 𝑠𝑚𝑎𝑙𝑙 = 4.1 ± 0.3µm, 𝐿 𝑐𝑎𝑏𝑙𝑒, 𝑙𝑎𝑟𝑔𝑒 = 7.3 ± 0.8µm) (Figure 3B) (19).…”

Section: Actin Cables Taper In a Cell Length-dependent Mannersupporting

confidence: 79%

“…To determine how extension velocity changes as a function of cell size we referred to our prior quantification of cable extension rates from temperaturesensitive cdc28-13 ts cells. At the permissive temperature, cdc28-13 ts cells are similar in size to wildtype haploid budding yeast; however, their size increases when grown at the nonpermissive temperature (19,27,28). In our prior study, we quantified cable extension rates from these enlarged cells by tracking the tips of cables marked with the fluorescent cable reporter Abp140-GFP Envy .…”

Section: Cable Extension Velocity Is Independent Of Cell Sizementioning

confidence: 99%

See 1 more Smart Citation

Length control emerges from cytoskeletal network geometry

McInally,

Reading,

Rosario

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Many cytoskeletal networks consist of individual filaments that are organized into elaborate higher order structures. While it is appreciated that the size and architecture of these networks are critical for their biological functions, much of the work investigating control over their assembly has focused on mechanisms that regulate the turnover of individual filaments through size-dependent feedback. Here, we propose a very different, feedback-independent mechanism to explain how yeast cells control the length of their actin cables. Our findings, supported by quantitative cell imaging and mathematical modeling, indicate that actin cable length control is an emergent property that arises from the cross-linked and bundled organization of the filaments within the cable. Using this model, we further dissect the mechanisms that allow cables to grow longer in larger cells, and propose that cell length-dependent tuning of formin activity allows cells to scale cable length with cell length. This mechanism is a significant departure from prior models of cytoskeletal filament length control and presents a new paradigm to consider how cells control the size, shape, and dynamics of higher order cytoskeletal structures.Significance StatementCells control the sizes of their cytoskeletal networks to ensure that these structures can efficiently perform their cellular functions. Until now, this ability has been attributed to molecular feedback mechanisms that control the rates at which individual filaments are assembled and disassembled. We find that size control of cytoskeletal networks does not require this type of feedback and can instead be encoded through the physical arrangement of the filaments within that network. These findings have important implications for understanding how the underlying geometry of higher order cytoskeletal networks contributes to cellular control over these structures.

show abstract

Section: Actin Cables Taper In a Cell Length-dependent Mannersupporting

confidence: 79%

Section: Cable Extension Velocity Is Independent Of Cell Sizementioning

confidence: 99%

Length control emerges from cytoskeletal network geometry

McInally,

Reading,

Rosario

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Another possible use for such a gradient could be in controlling the self-assembly of linear structures such as actin cables and flagella, which are precisely scaled to the linear dimensions of the cell ( McInally et al, 2019 ; Bauer et al, 2021 ; Datta et al, 2020 ). For example, a recent study of actin cables in yeast found that when cells were mutated to grow abnormally large, the actin cables assembled to a length that was proportional to the cell radius ( McInally et al, 2021 ). A hypothesized explanation of this phenomena is the presence of a scale-invariant gradient of depolymerizing activity.…”

Section: Discussionmentioning

confidence: 99%

How to assemble a scale-invariant gradient

Datta

Ghosh

Kondev

2022

eLife

Self Cite

View full text Add to dashboard Cite

Intracellular protein gradients serve a variety of functions, such as the establishment of cell polarity or to provide positional information for gene expression in developing embryos. Given that cell size in a population can vary considerably, for the protein gradients to work properly they often have to be scaled to the size of the cell. Here, we examine a model of protein gradient formation within a cell that relies on cytoplasmic diffusion and cortical transport of proteins toward a cell pole. We show that the shape of the protein gradient is determined solely by the cell geometry. Furthermore, we show that the length scale over which the protein concentration in the gradient varies is determined by the linear dimensions of the cell, independent of the diffusion constant or the transport speed. This gradient provides scale-invariant positional information within a cell, which can be used for assembly of intracellular structures whose size is scaled to the linear dimensions of the cell, such as the cytokinetic ring and actin cables in budding yeast cells.

show abstract

“…Finally, although extensive work has been done on S. cerevisiae actin cables ( Alioto et al, 2016 ; Chesarone et al, 2009 ; Huckaba et al, 2004 ; McInally et al, 2021 ; Miao et al, 2016 , 2013 ; Yang and Pon, 2002 ), the dynamics of Tpm1 or Tpm2 in interphase cables has not been explored in live cells. Furthermore, an extensive body of work has been done on the interplay between actin patches, actin cables and endocytosis ( Drubin et al, 2005 ; Kaksonen et al, 2005 , 2006 ).…”

Section: Discussionmentioning

confidence: 99%

mNG-tagged fusion proteins and nanobodies to visualize tropomyosins in yeast and mammalian cells

Hatano

Lim

Billault-Chaumartin

et al. 2022

Journal of Cell Science

View full text Add to dashboard Cite

Tropomyosins are structurally conserved α-helical coiled-coil proteins that bind along the length of filamentous actin (F-actin) in fungi and animals. Tropomyosins play essential roles in the stability of actin filaments and in regulating myosin II contractility. Despite the crucial role of tropomyosin in actin cytoskeletal regulation, in vivo investigations of tropomyosin are limited, mainly due to the suboptimal live-cell imaging tools currently available. Here, we report on an mNeonGreen (mNG)-tagged tropomyosin, with native promoter and linker length configuration, that clearly reports tropomyosin dynamics in Schizosaccharomyces pombe (Cdc8), Schizosaccharomyces japonicus (Cdc8) and Saccharomyces cerevisiae (Tpm1 and Tpm2). We also describe a fluorescent probe to visualize mammalian tropomyosin (TPM2 isoform). Finally, we generated a camelid nanobody against S. pombe Cdc8, which mimics the localization of mNG–Cdc8 in vivo. Using these tools, we report the presence of tropomyosin in previously unappreciated patch-like structures in fission and budding yeasts, show flow of tropomyosin (F-actin) cables to the cytokinetic actomyosin ring and identify rearrangements of the actin cytoskeleton during mating. These powerful tools and strategies will aid better analyses of tropomyosin and F-actin cables in vivo.

show abstract

Scaling of subcellular actin structures with cell length through decelerated growth

Cited by 17 publications

References 37 publications

Length control emerges from cytoskeletal network geometry

Length control emerges from cytoskeletal network geometry

How to assemble a scale-invariant gradient

mNG-tagged fusion proteins and nanobodies to visualize tropomyosins in yeast and mammalian cells

Contact Info

Product

Resources

About