Triggering a Cell Shape Change by Exploiting Preexisting Actomyosin Contractions

Roh-Johnson, Minna; Shemer, Gidi; Higgins, Christopher D.; McClellan, Joseph H.; Werts, Adam D.; Tulu, U. Serdar; Gao, Liang; Betzig, Eric; Kiehart, Daniel P.; Goldstein, Bob

doi:10.1126/science.1217869

Cited by 247 publications

(280 citation statements)

References 44 publications

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“…Laser ablation was used to analyse in vivo the forces generated by actomyosin structures organized in apical layers or cables 29,37,38 . Only a few studies have focused on the cortical actomyosin mesh of rounded cells, but these were done in cultured cells or in vivo-isolated cells, and none were done in mitotic cells 26,39 .…”

Section: Discussionmentioning

confidence: 99%

Mitotic cell rounding and epithelial thinning regulate lumen growth and shape

et al. 2015

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Many organ functions rely on epithelial cavities with particular shapes. Morphogenetic anomalies in these cavities lead to kidney, brain or inner ear diseases. Despite their relevance, the mechanisms regulating lumen dimensions are poorly understood. Here, we perform live imaging of zebrafish inner ear development and quantitatively analyse the dynamics of lumen growth in 3D. Using genetic, chemical and mechanical interferences, we identify two new morphogenetic mechanisms underlying anisotropic lumen growth. The first mechanism involves thinning of the epithelium as the cells change their shape and lose fluids in concert with expansion of the cavity, suggesting an intra-organ fluid redistribution process. In the second mechanism, revealed by laser microsurgery experiments, mitotic rounding cells apicobasally contract the epithelium and mechanically contribute to expansion of the lumen. Since these mechanisms are axis specific, they not only regulate lumen growth but also the shape of the cavity.

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Section: Discussionmentioning

confidence: 99%

Mitotic cell rounding and epithelial thinning regulate lumen growth and shape

et al. 2015

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“…This makes it difficult to extract information even close to the approximately 3× axial resolution gain that it theoretically provides over conventional wide-field microscopy. Nevertheless, it can still address important biological questions 18,19 when the side lobe background is not a concern. The TP mode (TP Bessel beam plane illumination) offers high-speed and near-isotropic 3D resolution, but with limited multicolor capability 20 .…”

Section: Implementing Multiple Scanning Beams To Reduce Photobleachinmentioning

confidence: 99%

3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy

et al. 2014

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3D live imaging is important for a better understanding of biological processes, but it is challenging with current techniques such as spinning-disk confocal microscopy. Bessel beam plane illumination microscopy allows high-speed 3D live fluorescence imaging of living cellular and multicellular specimens with nearly isotropic spatial resolution, low photobleaching and low photodamage. unlike conventional fluorescence imaging techniques that usually have a unique operation mode, Bessel plane illumination has several modes that offer different performance with different imaging metrics. to achieve optimal results from this technique, the appropriate operation mode needs to be selected and the experimental setting must be optimized for the specific application and associated sample properties. Here we explain the fundamental working principles of this technique, discuss the pros and cons of each operational mode and show through examples how to optimize experimental parameters. We also describe the procedures needed to construct, align and operate a Bessel beam plane illumination microscope by using our previously reported system as an example, and we list the necessary equipment to build such a microscope. assuming all components are readily available, it would take a person skilled in optical instrumentation ~1 month to assemble and operate a microscope according to this protocol. accompanied by slower imaging speed, faster photobleaching and higher photodamage, thereby limiting the number of time points for live imaging. TP fluorescence microscopy achieves optical sectioning and simultaneously avoids an out-of-focus background through nonlinear absorption of the excitation, but the imaging speed is still limited by point-scanned detection using the photomultiplier tube (PMT), and nonlinear mechanisms introduce additional photodamage. It also has a limited multicolor imaging capability. In practice, confocal and, more recently, spinning-disk confocal microscopy have been the most common methods for live 3D imaging of cellular-scale specimens. Selective plane illumination microscopy (SPIM)Although the technique is a century old 1 , the rapid development of SPIM over the last decade 2-9 was driven by the need for highspeed, low-photobleaching and noninvasive 3D live imaging. SPIM minimizes the out-of-focus excitation by using two objectives with optical axes orthogonal to each other separately for excitation and detection. The sample is illuminated from the side by sending a sheet of excitation light into the sample, so that the illumination is confined near the focal plane of the orthogonal detection objective (Fig. 1a). In comparison with epi-illumination methods, SPIM has the following advantages. First, the confined excitation provides optical sectioning automatically by producing minimal out-of-focus fluorescence background. Second, the method is as fast as conventional wide-field detection, as fluorescence is imaged across the entire excitation plane simultaneously. Third, if the sheet thickness is comparable...

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“…Following A/P polarization, chiral cortical actomyosin activity patterns the D/V and L/R axes [187,188,191,192,197] (see above), and cortical contractility drives cell internalization and most likely also cell sorting during gastrulation [197,[262][263][264][265][266][267]. The central inductive cue(s) that drives non-muscle myosin II activation during gastrulation is constituted by Wnt signaling [200,265].…”

Section: Actomyosinmentioning

confidence: 99%

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

Pohl

2015

Symmetry

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Animal development relies on repeated symmetry breaking, e.g., during axial specification, gastrulation, nervous system lateralization, lumen formation, or organ coiling. It is crucial that asymmetry increases during these processes, since this will generate higher morphological and functional specialization. On one hand, cue-dependent symmetry breaking is used during these processes which is the consequence of developmental signaling. On the other hand, cells isolated from developing animals also undergo symmetry breaking in the absence of signaling cues. These spontaneously arising asymmetries are not well understood. However, an ever growing body of evidence suggests that these asymmetries can originate from spontaneous symmetry breaking and self-organization of molecular assemblies into polarized entities on mesoscopic scales. Recent discoveries will be highlighted and it will be discussed how actomyosin and microtubule networks serve as common biomechanical systems with inherent abilities to drive spontaneous symmetry breaking.

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Triggering a Cell Shape Change by Exploiting Preexisting Actomyosin Contractions

Cited by 247 publications

References 44 publications

Mitotic cell rounding and epithelial thinning regulate lumen growth and shape

Mitotic cell rounding and epithelial thinning regulate lumen growth and shape

3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

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