Temperature Dependence of Cell Division Timing Accounts for a Shift in the Thermal Limits of C. elegans and C. briggsae

Begasse, Maria L.; Leaver, Mark; Vázquez, Federico; Grill, Stephan W.; Hyman, Anthony A.

doi:10.1016/j.celrep.2015.01.006

Cited by 104 publications

(100 citation statements)

References 39 publications

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“…Manual lineaging was performed at 23°C. To compare cell cycle times between manual lineaging and automated imaging, manually obtained values were scaled to presumptive 20°C values via an Arrhenius law extracted from the molting data at different temperatures in (Hirsh et al, 1976) (scaling factor 1.24, (see also (Begasse et al, 2015)).…”

Section: Methodsmentioning

confidence: 99%

Long-Term High-Resolution Imaging of Developing C. elegans Larvae with Microfluidics

et al. 2017

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Long-term studies of C. elegans larval development traditionally require tedious manual observations as larvae must move to develop, and existing immobilization techniques either perturb development or are unsuited for young larvae. Here, we present a simple microfluidic device to simultaneously follow development of 10 C. elegans larvae at high spatiotemporal resolution from hatching to adulthood (~3 days). Animals grown in micro-chambers are periodically immobilized by compression to allow high-quality imaging of even weak fluorescence signals. Using the device, we obtain cell-cycle statistics for C. elegans vulval development, a paradigm for organogenesis. We combine Nomarski and multi-channel fluorescence microscopy to study processes such as cell-fate specification, cell death, and trans-differentiation throughout postembryonic development. Finally, we generate time-lapse movies of complex neural arborization through automated image registration. Our technique opens the door to quantitative analysis of time-dependent phenomena governing cellular behavior during C. elegans larval development.

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Section: Methodsmentioning

confidence: 99%

Long-Term High-Resolution Imaging of Developing C. elegans Larvae with Microfluidics

et al. 2017

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“…Above 258C, the rate of defective cell divisions rapidly increases with increasing temperature and adult animals become progressively sterile. Asymmetry during cell divisions-which is highly precise between 12 and 258C-becomes tenuous; with 19.4% embryos failing to divide asymmetrically (Begasse et al, 2015). These findings indicate that certain aspects of polarity maintenance and hence the first asymmetric cell division are heat-labile ( Fig.…”

Section: Introductionmentioning

confidence: 90%

“…In poikilotherms, the body temperature is not subject to thermal homeostasis, thus, these organisms have to search for ambient temperatures that match their physiological requirements. It has been recently shown that the optimal ambient temperature range for the nematode C. elegans is 8 2 258C (Begasse et al, 2015;Neves et al, 2015). Above 258C, the rate of defective cell divisions rapidly increases with increasing temperature and adult animals become progressively sterile.…”

Section: Introductionmentioning

confidence: 99%

Acute heat shock leads to cortical domain internalization and polarity loss in the C. elegans embryo

Singh

Odedra

Lehmann

et al. 2016

Genesis

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Summary: Many developmental processes are inherently robust due to network organization of the participating factors and functional redundancy. The heterogeneity of the factors involved and their connectivity puts these processes at risk of abrupt system collapse under stress. The polarization of the one-cell C. elegans embryo constitutes such an inherently robust process with functional redundancy. However, how polarization is affected by acute stress has not been thoroughly investigated. Here, we report that heat shock (348C, 1 h) triggers a highly reproducible loss of the anterior and collapse of the posterior polarity domains. Temperature-dependent loss of cortical nonmuscle myosin II drastically reduces cortical tension and leads to internalization of large plasma membrane domains including the membrane-associated polarity factor PAR-2. After internalization, plasma membrane vesicles and associated factors cluster around centrosomes and are thereby withdrawn from the polarization process. Transient formation of the posterior polarity domain suggests that microtubule-induced self-organization of this domain is not compromised after heat shock. Hence, our data uncover that the polarization system undergoes a temperature-dependent collapse under acute stress. genesis 54:220-228, 2016. V C 2016Wiley Periodicals, Inc.

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“…The impact of vitelline membrane as a mechanical confinement on embryonic cell division has never been investigated. Previous works have shown the effects of temperature on mechanical properties of fiber-rich biological gels (Tempel, Isenberg & Sackmann, 1996;Xu, Wirtz & Pollard, 1998;Semmrich et al, 2007), suspended (Chan et al, 2014) and embryonic cells (Marsland & Landau, 1954;Mitchison & Swann, 1954) as well as timing of cell division (Begasse et al, 2015). However, the effects of temperature on division of vitelline-confined embryonic cells have not been investigated.…”

Section: Introductionmentioning

confidence: 99%

On the embryonic cell division beyond the contractile ring mechanism: experimental and computational investigation of effects of vitelline confinement, temperature and egg size

2015

Draw Science

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Embryonic cell division is a mechanical process which is predominantly driven by contraction of the cleavage furrow and response of the remaining cellular matter. While most previous studies focused on contractile ring mechanisms of cytokinesis, effects of environmental factors such as pericellular vitelline membrane and temperature on the mechanics of dividing cells were rarely studied. Here, we apply a model-based analysis to the time-lapse imaging data of two species (Saccoglossus kowalevskii and Xenopus laevis) with relatively large eggs, with the goal of revealing the effects of temperature and vitelline envelope on the mechanics of the first embryonic cell division. We constructed a numerical model of cytokinesis to estimate the effects of vitelline confinement on cellular deformation and to predict deformation of cellular contours. We used the deviations of our computational predictions from experimentally observed cell elongation to adjust variable parameters of the contractile ring model and to quantify the contribution of other factors (constitutive cell properties, spindle polarization) that may influence the mechanics and shape of dividing cells. We find that temperature affects the size and rate of dilatation of the vitelline membrane surrounding fertilized eggs and show that in native (not artificially devitellinized) egg cells the effects of temperature and vitelline envelope on mechanics of cell division are tightly interlinked. In particular, our results support the view that vitelline membrane fulfills an important role of micromechanical environment around the early embryo the absence or improper function of which under moderately elevated temperature impairs normal development. Furthermore, our findings suggest the existence of scale-dependent mechanisms that contribute to cytokinesis in species with different egg size, and challenge the view of mechanics of embryonic cell division as a scale-independent phenomenon. Subjects Biophysics, Cell Biology, Computational Biology, Developmental Biology Keywords Embryonic cell division, Contractile ring mechanism, Cell mechanics, Mitotic spindle, Vitelline envelope, Temperature effects, Scale effects, Finite Element Method How to cite this article Gladilin et al. (2015), On the embryonic cell division beyond the contractile ring mechanism: experimental and computational investigation of effects of vitelline confinement, temperature and egg size.

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Temperature Dependence of Cell Division Timing Accounts for a Shift in the Thermal Limits of C. elegans and C. briggsae

Cited by 104 publications

References 39 publications

Long-Term High-Resolution Imaging of Developing C. elegans Larvae with Microfluidics

Long-Term High-Resolution Imaging of Developing C. elegans Larvae with Microfluidics

Acute heat shock leads to cortical domain internalization and polarity loss in the C. elegans embryo

On the embryonic cell division beyond the contractile ring mechanism: experimental and computational investigation of effects of vitelline confinement, temperature and egg size

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