Tracking intracellular forces and mechanical property changes in mouse one-cell embryo development

Duch, Marta; Torras, Núria; Asami, Maki; Suzuki, Toru; Arjona, María Isabel; Gómez-Martínez, Rodrigo; VerMilyea, Matthew; Castilla, R.; Plaza, J.A.; Perry, Anthony C.F.

doi:10.1038/s41563-020-0685-9

Cited by 18 publications

(13 citation statements)

References 49 publications

(28 reference statements)

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“…The present data confirms the set pattern of shape changes of cytokinesis that have been described ( Duch et al, 2020 ). Sub-zona space distribution changed rapidly.…”

Section: Resultssupporting

confidence: 93%

Dynamic shapes of the zygote and two-cell mouse and human

et al. 2021

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Mouse zygote morphokinetics were measured during interphase, the mitotic period, cytokinesis, and two-cell stage. Sequences of rounder–distorted–rounder shapes were revealed, as were changing patterns of cross section area. A calcium chelator and an actin-disrupting agent inhibited the area changes that occurred between pronuclear envelope breakdown and cytokinesis. During cell division, two vortices developed in each nascent cell and they rotated in opposite directions at each end of the cell, a pattern that sometimes persisted for up to 10 h. Exchange with the environment may have been promoted by these shape and area cycles and persisting circulation in the cytoplasm may have a similar function between a cell's interior and periphery. Some of these movements were sporadically also seen in human zygotes with abnormal numbers of pronuclei and the two-cell stages that developed from these compromised human zygotes.

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“…The present data confirms the set pattern of shape changes of cytokinesis that have been described ( Duch et al, 2020 ). Sub-zona space distribution changed rapidly.…”

Section: Resultssupporting

confidence: 93%

Dynamic shapes of the zygote and two-cell mouse and human

et al. 2021

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“…Through the miniaturization and patterning of the microparticles, we also anticipate that barcoded microparticles will enhance labeling capabilities, already enabling extraordinarily volumetric coding densities of up to 1093 codes µm −3 . Already smaller than the volume of a cell, [27,50,51] with only a modest increase in the number of printed inks, much higher coding densities can be envisioned for applications at the microscale. Multiplexed analysis systems could also provide cumulative testing sites in a single device and the inclusion of more intricate domains and dimensions could inspire the development of more sophisticated microparticles.…”

Section: Resultsmentioning

confidence: 99%

Multidimensional Anisotropic Architectures on Polymeric Microparticles

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Arjona

Duch

et al. 2020

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microfluidics, [9] centrifugation, [10] electrohydrodynamics, [11] and two-photon lithography [6] have been developed to fabricate microparticles with selected physical traits. However, the combination of all of these physical traits and further customization of properties in a single microparticle to augment the functionality, are hindered by the limitations to combining complementary physical anisotropies. In parallel, research has also focused on chemical anisotropy. Extended anisotropy can be implemented with the addition of subdivisions during fabrication, albeit limited by the process, or with posterior functionalization which may be obstructed by the stochastic nature of suspended microparticles in a reactive solution or limited by the available orthogonal chemical reaction sites present on the surface of the microparticles. [12] Imaginative solutions have been used to fabricate multiple subdivided microparticles or chips, offering an attractive approach in the encoding [4,5] and anticounterfeiting [13] fields, yet their main utilization has centered on biomedical and bioengineering. [9,14] Nevertheless, the combination of different customized properties to increase functionality in a single microparticle is limited by the availability of reactive pathways that would otherwise allow the incorporation of complementary chemical anisotropies. Consolidation of these technologies has advanced considerably in the microparticle field, yet the constant trade-off between physical anisotropies, chemical anisotropies and their combination limits the library of possible customized microparticles, a problem that is aggravated by miniaturization. In this work, we aim to remove constraints placed by entangled physical and chemical anisotropies to fabricate polymeric microparticles with customized traits. We achieve this by combining physical attributes and surface chemical functionalization to obtain SU-8 microparticles with specific anisotropic signatures at coordinates established in selected dimensions or domains, [3,15] which collectively define the multidimensional anisotropic space. To do so, we exploit standard SU-8 photolithography to invest the required physical anisotropies on the resulting wafer-bound microparticles. We then incorporate chemical anisotropy with soft lithography on the top, bottom or both surfaces of the microparticles with multiple patterned molecular inks. This collective approach guarantees a highthroughput and low polydispersity fabrication protocol without the need for excessively specialized facilities. Furthermore, the Next generation life science technologies will require the integration of building blocks with tunable physical and chemical architectures at the microscale. A central issue is to govern the multidimensional anisotropic space that defines these microparticle attributes. However, this control is limited to one or few dimensions due to profound fabrication tradeoffs, a problem that is exacerbated by miniaturization. Here, a vast number of anisotropic dimensions are integrate...

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“…Contrary, we found no evidence of direct interaction between the SL‐500 devices and microtubules (Figure 2d), consistent with the behavior of polysilicon devices microinjected within mouse embryos. [ 15 ]…”

Section: High Rate Of Sl‐500 Device Internalization By Hela Cellsmentioning

confidence: 99%

“…Although the volume of a HeLa cell is more than an order of magnitude smaller than the volume of a one‐cell mouse embryo, we detected forces almost 10 times larger (114 vs 17.7 nN, respectively), and 1745 and 233 Pa when expressed in terms of pressure. [ 15 ] This led us to consider the role played by structural support of the devices at the cell membrane, understood as the structural support of the cantilevers in the cortex that limits the device displacements.…”

Section: Intracellular Mechanical Drugs Alter Cell Division and Provo...mentioning

confidence: 99%

Intracellular Mechanical Drugs Induce Cell‐Cycle Altering and Cell Death

et al. 2022

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physical terms, the combination of cell membrane-cortex system and cytoskeleton constitutes a mechanical system whose stability is based on a force balance between compression and tensileload-bearing components. [1] Any physical perturbation of this cellular mechanical system elicits a redistribution of forces and rearrangement of mechanical elements that can be disruptive. [3] Thus, it is not surprising that multiple chemical drugs for research and therapeutics target to alter the cellular mechanical performance. Anticancer drugs such as paclitaxel or colchicine affect the microtubules, provoking mitotic catastrophe to cause cell death. [4,5] Other compounds, including cytochalasin B, cytochalasin D, and latrunculin A disrupt actin filaments, also disturbing cell function and growth. [6] Intracellular mechanical cues induced by physiological internalization of large objects can also alter the redistribution of forces and the rearrangement of mechanical elements. Indeed, during entosis (the engulfment of one living cell by another), cytokinesis in the engulfing cell is perturbed, which can cause aneuploidy. [7,8] This has parallels to cell division perturbation when cells are exposed to natural or artificial "long" fibrous material such as asbestos fibers that can induce genomic changes and cancer by sterically blocking cytokinesis. [9] Current advances in materials science have demonstrated that extracellular mechanical cues can define cell function and cell fate. However, a fundamental understanding of the manner in which intracellular mechanical cues affect cell mechanics remains elusive. How intracellular mechanical hindrance, reinforcement, and supports interfere with the cell cycle and promote cell death is described here. Reproducible devices with highly controlled size, shape, and with a broad range of stiffness are internalized in HeLa cells. Once inside, they induce characteristic cell-cycle deviations and promote cell death. Device shape and stiffness are the dominant determinants of mechanical impairment. Device structural support to the cell membrane and centering during mitosis maximize their effects, preventing spindle centering, and correct chromosome alignment. Nanodevices reveal that the spindle generates forces larger than 114 nN which overcomes intracellular confinement by relocating the device to a less damaging position. By using intracellular mechanical drugs, this work provides a foundation to defining the role of intracellular constraints on cell function and fate, with relevance to fundamental cell mechanics and nanomedicine.

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Tracking intracellular forces and mechanical property changes in mouse one-cell embryo development

Cited by 18 publications

References 49 publications

Dynamic shapes of the zygote and two-cell mouse and human

Dynamic shapes of the zygote and two-cell mouse and human

Multidimensional Anisotropic Architectures on Polymeric Microparticles

Intracellular Mechanical Drugs Induce Cell‐Cycle Altering and Cell Death

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