A rim-and-spoke hypothesis to explain the biomechanical roles for cytoplasmic intermediate filament networks

Quinlan, Roy A.; Schwarz, Nicole; Windoffer, Reinhard; Richardson, Christine; Hawkins, Tim J.; Broussard, Joshua A.; Green, Kathleen J.; Leube, Rudolf E.

doi:10.1242/jcs.202168

Cited by 50 publications

(69 citation statements)

References 127 publications

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“…We propose that intermediate filaments provide the MC mechanical strength to support the plasma membrane to withstand the pressure from the forming vitelline membrane around over longer time period. This is in agreement with the structural role of intermediate filaments in providing mechanical strength, including plasma membrane support to cells (reviewed in Loschke et al, 2015;Quinlan et al, 2017). In addition, we observe enrichment in acetylated tubulin in the MC cytoplasmic process that pushes on the oolemma (Fig.…”

Section: What Are the Events Downstream Of Taz Driving Differentiatiosupporting

confidence: 91%

The Hippo pathway effector Taz is required for cell fate specification and fertilization in zebrafish

Dingare

Niedzwetzki

Klemmt

et al. 2018

Preprint

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In the last decade, Hippo signaling has emerged as a critical pathway integrating extrinsic and intrinsic mechanical cues to regulate cell proliferation and survival, tissue morphology and organ size in vivo. Despite its essential role in organogenesis, surprisingly much less is known about how it connects biomechanical signals to control of cell fate and cell size during development. Here we unravel a novel and unexpected role of the Hippo pathway effector Taz (wwtr1) in the control of cell size and cell fate specification. In teleosts, fertilization occurs through a specific structure at the animal pole, called the micropyle. This opening in the chorion is formed during oogenesis by a specialized somatic follicle cell, the micropylar cell (MC). The MC has a peculiar shape and is much larger than its neighboring follicle cells but the mechanisms underlying its specification and cell shape acquisition are not known.Here we show that Taz is essential for the specification of the MC and subsequent micropyle formation in zebrafish. We identify Taz as the first bona fide MC marker and show that Taz is specifically and strongly enriched in the MC precursor before the cell can be identified morphologically. Altogether, our genetic data and molecular characterization of the MC lead us to propose that Taz is a key regulator of the MC fate activated by physical cues emanating from the oocyte to initiate the MC morphogenetic program. We describe here for the first time the mechanism underlying the specification of the MC fate. Abstract word count: 248 words Main text word count: 8639 words Bally-Cuif, L., Schatz, W. J. and Ho, R. K. (1998). Characterization of the zebrafish Orb/CPEB-related RNA binding protein and localization of maternal components in the zebrafish oocyte. Mech Dev 77, 31-47. . Cadherin-catenin complexes during zebrafish oogenesis: heterotypic junctions between oocytes and follicle cells. Biol. Reprod. 61, 692-704. . (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39, e82. Chaigne, A., Campillo, C., Gov, N. S., Voituriez, R., Sykes, C., Verlhac, M. H. and Terret, M. E. (2015). A narrow window of cortical tension guides asymmetric spindle positioning in the mouse oocyte. Nat Commun 6, 6027.Compagnon, J., Barone, V., Rajshekar, S., Kottmeier, R., Pranjic-Ferscha, K., Behrndt, M. and Heisenberg, C.-P. (2014). The notochord breaks bilateral symmetry by controlling cell shapes in the zebrafish laterality organ. Dev Cell 31, 774-783.

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Section: What Are the Events Downstream Of Taz Driving Differentiatiosupporting

confidence: 91%

The Hippo pathway effector Taz is required for cell fate specification and fertilization in zebrafish

Dingare

Niedzwetzki

Klemmt

et al. 2018

Preprint

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“…Taken together, these results indicate that desmin has no influence on the mechanical properties of the cell cortex. This was expected, as the cortex structure is mainly composed of actin and actin binding proteins, and desmin is excluded from it (see Figure ), although in some cell types a subplasmalemmal IF network has been identified [Quinlan et al., ]. However, when myoblasts overexpress functional or mutated desmin that is polymerised into networks, we show an increase in global and local stiffness as measured with the SCR and the MT.…”

Section: Resultssupporting

confidence: 70%

The desmin network is a determinant of the cytoplasmic stiffness of myoblasts

Charrier

Montel

Asnacios

et al. 2018

Biology of the Cell

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Desminopathies are associated with muscular weaknesses attributed to a disorganisation of the structure of striated muscle that impairs the active force generation. The present study evidences for the first time the key role of desmin in the rheological properties of myoblasts, raising the hypothesis that desmin mutations could also alter the passive mechanical properties of muscles, thus participating to the lack of force build up in muscle tissue.

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“…In cells, interactions between intermediate filaments are mediated by a variety of accessory proteins that crosslink the filaments to each other, 76 to actin and microtubules, 13 and to cell-matrix and cell-cell adhesions. 66 Rheological studies on reconstituted networks of intermediate filaments have furthermore shown that they are inherently associative due to ionic interactions, 63 particularly between their highly charged carboxy-terminal tail domains which act as crosslinkers. 52 As a result of this crosslinking, intermediate filament networks exhibit nonlinear stress stiffening over several decades of applied stress.…”

Section: Introductionmentioning

confidence: 99%

Stiffening and inelastic fluidization in vimentin intermediate filament networks

Aufderhorst-Roberts

Koenderink

2019

Soft Matter

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Intermediate filaments are cytoskeletal proteins that are key regulators of cell mechanics, a role which is intrinsically tied to their hierarchical structure and their unique ability to accommodate large axial strains. However, how the single-filament response to applied strains translates to networks remains unclear, particularly with regards to the crosslinking role played by the filaments' disordered "tail" domains. Here we test the role of these noncovalent crosslinks in the nonlinear rheology of reconstituted networks of the intermediate filament protein vimentin, probing their stress-and rate-dependent mechanics. Similarly to previous studies we observe elastic stressstiffening but unlike previous work we identify a characteristic yield stress σ * , above which the networks exhibit rate-dependent softening of the network, referred to as inelastic fluidization. By investigating networks formed from tail-truncated vimentin, in which noncovalent crosslinking is suppressed, and glutaraldehyde-treated vimentin, in which crosslinking is made permanent, we show that rate-dependent inelastic fluidization is a direct consequence of vimentin's transient crosslinking. Surprisingly, although the tail-tail crosslinks are individually weak, the effective timescale for stress relaxation of the network exceeds 1000s at σ * . Vimentin networks can therefore maintain their integrity over a large range of strains (up to ∼1000%) and loading rates (10 −3 to 10 3 s −1 ). Our results provide insight into how the hierarchical structure of vimentin networks contributes to the cell's ability to be deformable yet strong. * Present address: School of Physics and Astronomy, University of Leeds, Leeds LS2 9JT, United Kingdom. 1 † Electronic Supplementary Information (ESI) available: Onset stress and linear modulus at all loading rates (S1), Representative stress vs. strain curve indicating rupture criteria (S2), loading rate dependent contributions to differential storage modulus (S3), affine entropic simulation data of vimentin networks (S4), frequency sweeps of vimentin networks with different crosslink modifications (S5), linear and nonlinear rheology of tailless vimentin (S6).

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A rim-and-spoke hypothesis to explain the biomechanical roles for cytoplasmic intermediate filament networks

Cited by 50 publications

References 127 publications

The Hippo pathway effector Taz is required for cell fate specification and fertilization in zebrafish

The Hippo pathway effector Taz is required for cell fate specification and fertilization in zebrafish

The desmin network is a determinant of the cytoplasmic stiffness of myoblasts

Stiffening and inelastic fluidization in vimentin intermediate filament networks

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