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Pulsatile cell-autonomous contractility drives compaction in the mouse embryo

A Corrigendum to this article was published on 01 August 2017

This article has been updated

Abstract

Mammalian embryos initiate morphogenesis with compaction, which is essential for specifying the first lineages of the blastocyst. The 8-cell-stage mouse embryo compacts by enlarging its cell–cell contacts in a Cdh1-dependent manner. It was therefore proposed that Cdh1 adhesion molecules generate the forces driving compaction. Using micropipette aspiration to map all tensions in a developing embryo, we show that compaction is primarily driven by a twofold increase in tension at the cell–medium interface. We show that the principal force generator of compaction is the actomyosin cortex, which gives rise to pulsed contractions starting at the 8-cell stage. Remarkably, contractions emerge as periodic cortical waves when cells are disengaged from adhesive contacts. In line with this, tension mapping of mzCdh1−/− embryos suggests that Cdh1 acts by redirecting contractility away from cell–cell contacts. Our study provides a framework to understand early mammalian embryogenesis and original perspectives on evolutionary conserved pulsed contractions.

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Figure 1: Spatiotemporal map of tensions during compaction.
Figure 2: Role of cell–cell contacts in regulating tensions during compaction.
Figure 3: Role of Cdh1 in regulating tensions during compaction.
Figure 4: Role of contractility in generating tensions during compaction.
Figure 5: Non-cell-autonomous control of contractility by Cdh1.
Figure 6: Phase diagram of compaction.
Figure 7: Periodic contractions.
Figure 8: Periodic cortical waves.

Change history

  • 05 July 2017

    In the version of this Article originally published, the wave velocity reported in the sentence beginning 'In the absence of cell–cell contacts...' was incorrectly calculated and should have read '0.8 ± 0.1 μm s–1'. The wave velocity is calculated by dividing the cell perimeter by the oscillation period, and further dividing this by two as there are two waves travelling around the cell. The number of waves was not taken into account in the originally published version of the Article. This mistake does not affect the main conclusions of the paper, as this sentence only describes a property of the phenomenon identified. This error has been corrected in the online version of the Article.

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Acknowledgements

We are grateful to all members of the Hiiragi laboratory and EMBL animal facility for their support. We thank J. E. Dietrich for providing images used for volume measurement. We thank A. G. Clark, A. Aulehla and C-P. Heisenberg for comments on an earlier version of the manuscript. J-L.M. is supported by EMBO (ALTF1195-2012), R.N. by HumboldtStiftung (JAN-1149654-STP-2), H.T. by EIPOD, and the Hiiragi group by VolkswagenStiftung.

Author information

Authors and Affiliations

Authors

Contributions

J-L.M. and T.H. designed the project. J-L.M. designed, performed and analysed the experiments. R.N. implemented the image analysis. H.T. conceived the supporting theory. All authors discussed the significance of the results and helped write the manuscript.

Corresponding authors

Correspondence to Jean-Léon Maître or Takashi Hiiragi.

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Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 2 Blastomeres volume during the 8-cell stage.

a, Images of cell volume reconstruction showing 6 cells of an 8-cell stage embryo expressing mTmG (grey) artificially labelled in distinct colours using Bitplane Imaris. Scale bar, 10 μm. b, Volume of blastomeres at the beginning (30 min after the last 4- to 8-cell stage division) and end (30 min before rounding up of the first 8- to 16-cell stage division) of the 8-cell stage. Individual examples from (a) are shown in colour while the whisker plot in black shows the minimum and maximum values, and upper and lower quartiles of n = 32 blastomeres pooled from 4 embryos from 1 representative experiment. p value indicates the result of Student’s t-test.

Supplementary Figure 3 Theoretical modelling of surface energy minimization during compaction of 2/8th doublets.

a, Diagram of two blastomeres from 8-cell stage mouse embryo forming a 2/8th doublet shaped by surface tension γcm at the cell–medium interface and interfacial tension γcc at the cell–cell interface. The shape of each blastomere is characterized by a radius of curvature Rc, an area of cell–medium interface A and a volume V0. The shape of the cell–cell contact is characterized by its radius r and contact angle θe. The 2/8th doublet is symmetric with respect to a rotational axis Φ and to the cell–cell contact. b, Rescaled energy E/E0 as a function of the contact angle θe/2 for different values of the dimensionless parameter 0 ≤ α = γcc/2γcm ≤ 1. The minimum of the surface energy, overlaid as a diagram, corresponds to the mechanical equilibrium α = cos(θe/2) for the 2/8th doublet.

Supplementary Figure 4 Natural variation in shape and tensions during compaction.

ad, Mean ± s.d. are shown for the blastomeres and contacts of 3 individual embryos. Embryo shown in Fig. 1b is shown in red. a, Radius of curvature Rc over time. b, Contact angle θe over time. c, Surface tension γcm over time. d, Interfacial tension γcc/2 over time. e, Plot of each surface tension γcm of each contacting blastomeres against one another. N = 233 contacting blastomeres pooled from 28 embryos from 11 representative experiments, Pearson correlation R = 0.778 (p < 0.001). f, Plot of each contact angle θi of each contacting blastomeres against one another. N = 233 contacting blastomeres pooled from 28 embryos, Pearson correlation R = 0.603 (p < 0.001).

Supplementary Figure 5 Surface tension at the 4-cell stage.

a, Surface tension measurements of an early (top) and late (bottom) 4-cell stage embryo. bc, Contact angles θi and θe (b) and tensions γcm and γcc/2 (c) of n = 42 and 46 contacting blastomeres pooled from 6 embryos early and late in the 4-cell stage from 2 representative experiments. d, Surface tension measurements (n = 88)γcm of a 4-cell stage embryo as a function of the contact angle θi in blue, together with 8-cell stage measurements shown in Fig. 1c in grey. p value indicates the result of Student’s t-test.

Supplementary Figure 6 Role of contractility in generating tensions during compaction.

a, Immunostaining of Myh9 early and late in the 8-cell stage. Red arrowheads point at cell–medium interfaces, green ones at cell–cell contacts. Scale bar, 10 μm. b, Mean ± s.d. contact/cortex ratio, n = 194 contacting blastomeres pooled from 22 embryos from 2 representative experiments, Pearson correlation R = −0.538 (p < 0.001). c, Phalloidin staining of F-actin early and late in the 8-cell stage. Red arrowheads point at cell–medium interfaces, green ones at cell–cell contacts. d, Mean ± s.d. contact/cortex ratio, 113 embryos from 9 representative experiments, Pearson correlation R = −0.752 (p < 0.001). e, Time-lapse of mTmG expressing embryo. Time post-division (hh:mm), Supplementary Video 3 . f, Contact/cortex ratio of mTmG and LifeAct-GFP over time. Mean ± s.d. of n = 23 contacts pooled from 8 embryos from 3 representative experiments followed every 30 min for 5–8 h. g, Surface tension measurement of DMSO or 1 μM CCD treated embryos. Scale bar, 10 μm. h, Surface tension γcm as a function of the contact angle θi of n = 10 and 42 contacting blastomeres pooled from 2 and 3 embryos treated with DMSO (black) or CCD (yellow) respectively from 1 representative experiment. Pearson correlation R = −0.028 for DMSO and −0.005 for CCD with (p > 0.1). WT (grey) shown in Fig. 1c.

Supplementary Figure 7 Examples of PIV and Fourier analysis of periodic contractions in different conditions.

af, Four examples of PIV and Fourier analysis are shown for 8-cell stage embryos (a, black), 4-cell stage embryos (b, blue), 8-cell stage embryos without zona pellucida (c, no ZP, purple), 8-cell stage embryos treated with 25 μM Bb (−) (d, orange) or 1 μM CCD (e, yellow), and mzCdh1−/− 8-cell stage embryos (f, green) are shown. The left column shows the velocity of one vector in one direction over time. The middle column shows the corresponding power spectrum. The right column shows the amplitude as a function of the period.

Supplementary Figure 8 Periodic contractions in different conditions.

ad, Mean ± s.d. amplitude of periodic contractions as a function of the oscillation period for control 8-cell stage embryos (ad, in black, n = 23 from 6 representative experiments), 1 μM CCD-treated 8-cell stage embryos (a, in yellow, n = 14 from 2 representative experiments), 4-cell stage embryos (b, in blue, n = 8 from 2 representative experiments), 8-cell stage embryos without zona pellucida (c, No ZP, in purple, n = 6 from 2 representative experiments). mzCdh1−/− 8-cell stage embryos (d, in green, n = 7 from 3 representative experiments). e, After Fourier analysis, the mean power spectra are analysed for the presence of a distinct peak of amplitude at a specific frequency. Distinct peaks could be observed in 16 out of n = 23 embryos at 8-cell stage, 1 out of n = 8 embryos at 4-cell stage, 0 out of n = 17 embryos at 8-cell stage with 25 μM Bb (−), 0 out of n = 14 embryos at 8-cell stage with 1 μM CCD, 6 out of n = 6 embryos at 8-cell stage without zona pellucida (ZP), 7 out of n = 7 mzCdh1−/− embryos at 8-cell stage, 7 out of n = 7 blastomeres isolated at the 8-cell stage. f, Periods that could be extracted are plotted as mean ± s.d. for embryos at 8-cell stage after PIV analysis (n = 16) and LifeAct-GFP intensity changes (n = 4), n = 6 embryos at 8-cell stage without zona pellucida (ZP) after PIV analysis, n = 7 mzCdh1−/− embryos at 8-cell stage after PIV analysis, n = 7 blastomeres isolated at the 8-cell stage after curvature analysis and LifeAct-GFP intensity changes.

Supplementary Figure 9 Examples of periodic cortical waves.

Three examples of 1/8th blastomeres showing periodic cortical waves. Left column shows the curvature computed from the segmented membrane signal. 2nd column shows LifeAct-GFP. 3rd column shows a kymograph of the curvature along the cell perimeter (y-axis, arbitrary unit) as a function of time (x-axis over 15 min). 4th column shows a kymograph of LifeAct-GFP signal along the cell perimeter (y-axis, arbitrary unit) as a function of time (x-axis over 15 min).

Supplementary Table 1 a, mean ± s.d. of contact angles and surface tensions over time shown in Fig. 1c. b, mean ± s.d. of contact angles and surface tensions over time for whole 8-cell embryos, 2/8th doublets and 1/8th single blastomeres shown in Fig. 2e. c, mean ± s.d. of contact angles and surface tensions over time for mCdh1+/− and mzCdh1−/− embryos shown in Fig. 3d. d, mean ± s.d. of contact angles and surface tensions over time for 25 μM Bb (+) or Bb (−) treated embryos shown in Fig. 4g.

Supplementary information

Supplementary Information

Supplementary Information (PDF 2459 kb)

Pre-implantation development.

Brightfield (BF) images of a developing zygote with mechanically removed ZP until blastocyst stage. At the 8-cell stage, compaction starts at 68:00 and ends at 76:00. Images are taken every 30 min and shown at 10 frames per second (fps). Time post-division (hh:mm), scale bar, 10 μm. (MOV 7225 kb)

Mapping of surface tension in space and time.

BF images of surface tension mapping of an embryo. Each blastomeres is measured 5 times throughout the 8-cell stage (from 3:00 to 10:30 post-division). A picture is taken for each pressure step when the deformation reached a stable shape and shown at 10 fps. Time post-division (hh:mm), scale bar, 10 μm. (MOV 6198 kb)

LifeAct-GFP and mTmG compaction.

Fluorescent confocal imaging of an mTmG (right) and LifeAct-GFP (left) expressing transgenic embryo throughout the 8-cell stage. Timelapse imaging consists of a picture taken every 30 min and is displayed at 5 fps. Time post-division (hh:mm), scale bar, 10 μm. (MOV 1643 kb)

PIV analysis of control 8-cell stage embryo.

BF images of an 8-cell stage embryo undergoing pulsed contractions. Pictures are acquired every 5 s and PIV analysis is performed between two successive images. Resulting PIV vectors are overlaid on top of the first of the two images analysed with vectors pointing up in green and vectors pointing down in red. Pictures are displayed at 10 fps. Scale bar, 10 μm. (MOV 1537 kb)

PIV analysis of 4-cell stage embryo.

BF images of a 4-cell stage embryo. Pictures are acquired every 2 s and PIV analysis is performed between two successive images. Resulting PIV vectors are overlaid on top of the first of the two images analysed with vectors pointing up in green and vectors pointing down in red and half of the images are shown to match Supplementary Videos 4, 710 display. Pictures are displayed at 10 fps. Scale bar, 10 μm. (MOV 1953 kb)

LifeAct-GFP pulses.

En face confocal slice of the cortex of an 8-cell stage embryo undergoing pulsed contractions. On the left, LifeAct-GFP shows patchy accumulation of signal at the cortex of cells. In the middle, mT shows membrane movements while the cell remains in focus. On the right, LifeAct-GFP (green) and mT (red) signals are merged. Timelapse imaging consists of a picture taken every 5 s and is displayed at 20 fps. Scale bar, 5 μm. (MOV 4468 kb)

PIV analysis of 8-cell stage embryo treated with 25 μM Bb (-).

BF images of an 8-cell stage embryo treated with 25 μM Bb (-). Pictures are acquired every 5 s and PIV analysis is performed between two successive images. Resulting PIV vectors are overlaid on top of the first of the two images analysed with vectors pointing up in green and vectors pointing down in red. Pictures are displayed at 10 fps. Scale bar, 10 μm. (MOV 1421 kb)

PIV analysis of 8-cell stage embryo treated with 1 μM CCD.

BF images of an 8-cell stage embryo treated with 1 μM CCD. Pictures are acquired every 5 s and PIV analysis is performed between two successive images. Resulting PIV vectors are overlaid on top of the first of the two images analysed with vectors pointing up in green and vectors pointing down in red. Pictures are displayed at 10 fps. Scale bar, 10 μm. (MOV 1432 kb)

PIV analysis of 8-cell stage embryo without zona pellucida

BF images of an 8-cell stage embryo without ZP. Pictures are acquired every 5 s and PIV analysis is performed between two successive images. Resulting PIV vectors are overlaid on top of the first of the two images analysed with vectors pointing up in green and vectors pointing down in red. Pictures are displayed at 10 fps. Scale bar, 10 μm. (MOV 1287 kb)

PIV analysis of mzCdh1−/− embryo.

BF images of an 8-cell stage mzCdh1−/− embryo. Pictures are acquired every 5 s and PIV analysis is performed between two successive images. Resulting PIV vectors are overlaid on top of the first of the two images analysed with vectors pointing up in green and vectors pointing down in red. Pictures are displayed at 10 fps. Scale bar, 10 μm. (MOV 1818 kb)

Periodic cortical waves.

Montage of BF (top left), mTmG (top right), LifeAct-GFP (bottom left) and local curvature measurement (bottom right) of a 1/8th blastomeres undergoing periodic cortical waves. Timelapse imaging consists of a picture taken every 5 s and is displayed at 10 fps. Scale bar, 10 μm. (MOV 14777 kb)

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Maître, JL., Niwayama, R., Turlier, H. et al. Pulsatile cell-autonomous contractility drives compaction in the mouse embryo. Nat Cell Biol 17, 849–855 (2015). https://doi.org/10.1038/ncb3185

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