Fertilization-induced cytoplasmic flows are a conserved feature of eggs in many species. However, until now the importance of cytoplasmic flows for the development of mammalian embryos has been unknown. Here, by combining a rapid imaging of the freshly fertilized mouse egg with advanced image analysis based on particle image velocimetry, we show that fertilization induces rhythmical cytoplasmic movements that coincide with pulsations of the protrusion forming above the sperm head. We find that these movements are caused by contractions of the actomyosin cytoskeleton triggered by Ca(2+) oscillations induced by fertilization. Most importantly, the relationship between the movements and the events of egg activation makes it possible to use the movements alone to predict developmental potential of the zygote. In conclusion, this method offers, thus far, the earliest and fastest, non-invasive way to predict the viability of eggs fertilized in vitro and therefore can potentially improve greatly the prospects for IVF treatment

Ajduk, Anna

Bomphrey, Richard J

Graham, Chris

Ilozue, Tagbo

Seres, K Bianka

Swann, Karl

Thomas, Adrian

Tom, Brian D

Windsor, Shane

Yu, Yuansong

Zernicka-Goetz, Magdalena

Nature Communications

English

PubMed

Fertilization-induced cytoplasmic flows are a conserved feature of eggs in many species. However, until now the importance of cytoplasmic flows for the development of mammalian embryos has been unknown. Here, by combining a rapid imaging of the freshly fertilized mouse egg with advanced image analysis based on particle image velocimetry, we show that fertilization induces rhythmical cytoplasmic movements that coincide with pulsations of the protrusion forming above the sperm head. We find that these movements are caused by contractions of the actomyosin cytoskeleton triggered by Ca2+ oscillations induced by fertilization. Most importantly, the relationship between the movements and the events of egg activation makes it possible to use the movements alone to predict developmental potential of the zygote. In conclusion, this method offers, thus far, the earliest and fastest, non-invasive way to predict the viability of eggs fertilized in vitro and therefore can potentially improve greatly the prospects for IVF treatment

Seres, K. Bianka

Bomphrey, Richard J.

Tom, Brian D.

Online Research @ Cardiff

Rhythmic actomyosin-driven contractions induced by sperm entry predict mammalian embryo viability

Fertilization-induced cytoplasmic flows are a conserved feature of eggs in many species. However, until now the importance of cytoplasmic flows for the development of mammalian embryos has been unknown. Here, by combining a rapid imaging of the freshly fertilized mouse egg with advanced image analysis based on particle image velocimetry, we show that fertilization induces rhythmical cytoplasmic movements that coincide with pulsations of the protrusion forming above the sperm head. We find that these movements are caused by contractions of the actomyosin cytoskeleton triggered by Ca^(2+) oscillations induced by fertilization. Most importantly, the relationship between the movements and the events of egg activation makes it possible to use the movements alone to predict developmental potential of the zygote. In conclusion, this method offers, thus far, the earliest and fastest, non-invasive way to predict the viability of eggs fertilized in vitro and therefore can potentially improve greatly the prospects for IVF treatment

Caltech Authors - Main

SUPPLEMENTARY INFORMATION 
for: 
Rhythmic actomyosin-driven contractions induced by sperm entry predict mammalian 
embryo viability 
 
Anna Ajduk, Tagbo Ilozue, Shane Windsor,
 Yuansong Yu, K. Bianka Seres, Richard J. 
Bomphrey,
 
 
Brian D. Tom, Karl Swann, Adrian Thomas, Chris Graham and Magdalena 
Zernicka-Goetz 
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Supplementary Figure. S1
Cytoplasmic movements in the zygote
Mean cytoplasmic speed in a zygote imaged in a plane above the FC (a), a plane bisecting the FC (c) 
and a plane below the FC (e). (b), (d) and (f) Cytoplasmic speeds in a timepoints marked by an arrow 
in (a), (c) and (e) respectively. Colour of the background represents local speed values. FC visible 
at 5 o’clock. Scale bar 10µm .(g) Speed-peaks recorded during the first and second Ca2+ transients in 
the egg injected 
with sperm. 
00:02:53
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Gap43-RFP UtrCH-GFP DIC Gap43/UtrCH
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UtrCH-GFPa b
Supplementary Figure. S2
Reorganization of actin in the cortex of the fertilization cone.
(a) Still images from a time-lapse movie showing reorganization of actin (labeled with UtrCH-EGFP)
in the FC. UtrCH-EGFP intensity in the FC cortex changes in accordance to the change in the FC shape.
As the FC flattens (beginning of the flattening marked with a red line) intensity of UtrCH-EGFP, labeling
F-actin, weakens. When the FC starts gradually protruding, intensity of UtrCH-EGFP increases again. 
Gap43-RFP served as a membrane marker. Images were taken every 20s, every 4th image is shown. 
(b) Zoomed images of the FC cortical region indicated in (a). Scale bar 10 µm.
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Gap43-RFP MyoRLC-GFP DIC Gap43/MyoRLC
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Supplementary Figure. S3
Reorganization of myosin in the cortex of the fertilization cone.
(a) Still images from a time-lapse movie showing reorganization of myosin (labeled with MyoRLC-GFP) 
in the FC. MyoRLC-GFP intensity in the cortex of the FC shoulders changes in accordance to the change 
in the FC shape. As the FC flattens (beginning of the flattening marked with a red line) intensity 
of MyoRLC-GFP weakens. When the FC starts gradually protruding, intensity of MyoRLC-GFP increases 
again. Gap43-RFP served as a membrane marker. Images were taken every 20s, every 2nd image is shown. 
(b) and (c) Zoomed images of the FC cortical region indicated in (a) by numbers 1 and 2 respectively.
Scale bar 10 µm.
20 + 0 min 20 + 90 min 20 + 180 min
Tubulin β actin    DNA
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Supplementary Figure. S4
Effect of Ca2+ chelatation and cytoskeletal inhibitors on microtubules and actomyosin in 
mouse zygotes.
Fertilized in vitro eggs were transferred to the inhibitors when anaphase bulges appeared. Images show 
projections prepared from confocal Z-stacks of representative zygotes fixed immediately after 20 minutes 
of preincubation with the drug (20 + 0 min) or 1.5 or 3 hours later (0 + 90 min and 0+180 min, respectively). 
Experimental and contro zygotes were scanned using the same settings . Phalloidin staining 
of jasplakinolide-treated zygotes failed to show F-actin (third panel from the bottom), because 
jasplakinolide competes with phalloidin for the same binding sites and thus prevents proper staining. 
Staining with anti-actin antibody revealed that jasplakinolide leads to formation of a thicker cortical layer 
of actin (2 bottom panels). Female chromatin indicated by f, male chromatin indicated by m. 
Scale bar 10 µm.
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mean basal speed - 1 SD (8.3 nm/s)
mean basal speed + 1 SD (16.1 nm/s)
e f
Supplementary Figure. S5
DIC imaging does not affect development of the mouse embryos.
(a) Mathematical model correlating probability of achieving blastocyt stage with mean basal
speed with an adjustment for mean inter-peak intervals. (b) Mathematical model correlating 
probability of achieving blastocyt stage (i.e ≥ 32 cells) with mean inter-peak interval with an 
adjustment for mean basal speed. (c) Mean number of cells in 4-day-old embryos imaged at 
different times after fertilisation. (d) Distribution of 4-day-old embryos with different number 
of cells in relation to the time of pronuclear formation. (e) Mean number of cells in 4-day-old 
embryos imaged or not in the zygote stage. (f) Distribution of 4-day-old embryos with different
number of cells depending on whether they were or were not imaged in the zygote stage. Error
bars represent standard deviations. Data comes from 13 independent experiments.
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Supplementary Figure. S6
Subpixel resolution of the PIV method
Accuracy of PIV for measuring sub-pixel 
displacements of artificially shifted and down 
sampled images.  (a) Error in pixels.  (a) 
Error as a percentage of the displacement.
 1 
Supplementary Table S1  
Direction of vectors during speed-peaks at different post-fertilization stages 
 
Post-
fertilization 
stages
Total no. 
of 
analysed 
speed 
peaks 
† 
No. of speed peaks with vectors pointing in a 
specified direction* (%): 
 
Towards 
2PB 
 
Between 
2PB and 
FC 
 
 
Towards 
FC 
 
No 
predominant 
direction 
Stage 1 
(11 zygotes) 
25 17‡
(66.7) 
  6  
(25.9) 
2
(7.4) 
§ 
 
0 
Stage 2 
(19 zygotes) 
65 1
(1.5) 
‡ 22 
(33.8) 
42
(64.6) 
§ 
 
0 
Stage 3 
(19 zygotes) 
34 7 
(20.6) 
4 
(11.8) 
8 
(23.5) 
15 
(44.1) 
 
*The direction of movement was judged as described in the Materials and Methods. 
†Stages of the zygote development are described in the main text. 
‡,§
 
 p<0.0001 
 
 
 
 2 
Supplementary Table S2 
Influence of Ca2+
 
 chelation and cytoskeleton inhibitors on completion of meiosis in in 
vivo fertilized mouse eggs 
 
 Total no. of  zygotes* 
Zygotes that failed 
to extrude 2PB (%) 
Zygotes that 
extruded 2PB (%) 
Control zygotes 
 
52 0 52 (100) 
BAPTA-treated 
zygotes 
 
6 2 (33.3) 4 (66.7) 
Nocodazole-treated 
zygotes 
 
12 7 (58.3) 5 (41.7) 
Taxol-treated 
zygotes  
 
12 12 (100) 0 
Cytochalasin D-
treated zygotes 
 
10 10 (100) 0 
Jasplakinolide-
treated zygotes  
 
23 23 (100) 0 
ML-7-treated 
zygotes 
 
13 4 (30.8) 9 (69.2) 
 
*Only zygotes that did not extrude 2PB before the onset of recording were included to this 
analysis. 
 
 
 
 3 
Supplementary Table S3 Comparison between predicted quality and actual developmental potential of the embryos 
 
No. 
No. of 
embryos 
transferred 
Mean 
basal 
speed 
(nm/s) 
Mean 
interval 
between 
speed-
peaks 
(min) 
Predicted 
no. of 
cells after 
4-day 
culture 
(mean +/- 
s.d.) 
Predicted 
probability of 
achieving 
blastocyst 
stage after 
4-day culture 
(%) 
(mean +/- s.d.) 
 
Estimated 
likehood of 
developmental 
success 
(high or low) 
Time of 
dissection 
(dpc) 
No. of 
embryos/
pups 
No. of 
resorptions 
Efficiency 
of the 
transfer 
(%) 
1 2 3 4 5 6 7 8 9 10 11 
 
1 
 
6 
 
11.2 
12.3 
11.1 
13.2 
16.0 
14.1 
 
21.4 
19.1 
25.9 
20.1 
20.3 
33.2 
 
28 
29 
32 
33 
39-40 
52 
(36+/-9) 
 
35-40 
40 
45-50 
50-55 
65-70 
85-90 
(56+/-19) 
 
high 
 
6.5 
 
5 
 
- 
 
83.3 
 
2 
 
6 
 
6.7 
8.6 
10.5 
10.4 
11.2 
9.4 
 
9.4 
13.6 
9.2 
13.1 
9.7 
23.2 
 
9-10 
15-16 
17 
19 
19 
23-24 
(17+/-5) 
 
0-5 
5-10 
5-10 
10-15 
10-15 
20-25 
(11+/-7) 
 
low 
 
6.5 
 
1 
 
- 
 
16.7 
 
3 
 
5 
 
12.5 
11.4 
14.0 
13.5 
13.5 
 
15.3 
18.7 
13.1 
16.1 
18.1 
 
 
25-26 
26 
27-28 
29-30 
31-32 
(28+/-3) 
 
30-35 
30-35 
35-40 
40-45 
45-50 
(39 +/-7) 
 
high 
 
19.5 
 
4 
 
-
 
* 80 
           
          cont’d 
 4 
1 2 3 4 5 6 7 8 9 10 11 
 
4 
 
9 
 
11.2 
11.4 
9.8 
12.8 
13.9 
13.8 
14.7 
16.2 
16.8 
 
18.8 
17.8 
24.6 
16.7 
17 
17.9 
17.3 
17.2 
19.1 
 
 
25-26  
25-26  
26-27  
28-29  
31  
32  
33-34  
36  
38-39 
(31+/-5) 
 
25-30 
25-30 
30-35 
35-40 
45-50 
50 
50-55 
60-65 
65-70 
(45+/-15) 
 
high 
 
19.5 
 
7 
 
-
 
* 77.8 
 
5 
 
5 
 
18.2 
17.2 
15.6 
16.2 
15.9 
 
14.6 
17.6 
20.0 
20.7 
29.7 
 
35-40 
38 
38-39 
40-41 
53-54 
(42+/-7) 
 
60-70 
65-70 
65-70 
70-75 
80-90 
(72+/-8) 
 
high 
 
19.5 
 
5 
  
-* 100 
 
6 
 
5 
 
12.3 
12.7 
13.7 
12.4 
12.8 
 
 
20.5 
21.9 
19.7 
24.8 
23.7 
 
30-31 
33 
33-34 
35-36 
36-37 
(34+/-2) 
 
40-45 
50 
50-55 
55-60 
55-60 
(52+/-6) 
 
high 
 
19.5 
 
5 
 
-
 
* 100 
 
7 
 
5 
 
10.0 
11.3 
10.4 
10.2 
10.5 
 
5.5 
7.4 
11.5 
16.8 
18.3 
 
 
10-15  
18 
18  
21-22  
22-23 
(19+/-4) 
 
5 
10 
10 
15-20 
20 
(13+/-6) 
 
low 
 
19.5 
 
3 
 
0 
 
60 
           
 
 
          
cont’d. 
 5 
 
1 2 3 4 5 6 7 8 9 10 11 
 
8 
 
6 
 
8.1 
9.4 
9.2 
10.1 
10.2 
13.3 
 
6.4 
6.4 
17.1 
16.4 
16.0 
7.4 
 
 
11-12  
13-14  
18-19  
20-21  
20-21  
21-22  
 (18+/-4) 
 
0-5 
0-5 
10-15 
15-20 
15-20 
20 
(12+/-8) 
 
low 
 
19.5 
 
1 
 
2 
 
16.7 
 
9 
 
4 
 
9.5 
9.2 
9.8 
7.2 
 
7.3 
9.7 
13.3 
8.0 
 
 
10 
14-15 
14-15 
18-19 
(14+/-3) 
 
0-5 
0-5 
5-10 
10-15 
(6+/-5) 
 
low 
 
19.5 
 
1
 
# 1 
 
25 
 
10 
 
4 
 
6.6 
10.1 
13.5 
12.1 
 
6.7 
5.5 
4.4 
10.1 
 
13-14 
14-15 
19-20 
20-22 
(17+/-4) 
 
0-5 
0-5 
10-20 
15-20 
(9+/-8) 
 
low 
 
19.5 
 
1
 
# 3 
 
25 
* Delivered naturally on 19.5 dpc. 
# 
 
Found dead after 2 days. 
 6 
Supplementary Table S4  
Optical specifications of the imaging systems used in experiments 
 
 Zeiss LSM 510 Meta Zeiss Axiovert Deltavision 
 
Objective 
magnification 
 
20x 20x * 20x 
Objective NA 
 
0.8 0.75 0.75 
Condenser NA 
 
0.55 0.55 0.55 
Chip size of the 
camera (pixels) 
 
- 1024x1344 # 512x512 
Binning - 2x2 1x1 
 
* With digital magnification 0.7x (final magnification 14x) 
#
 
 Images were scanned with 1800 x 1800 pixel resolution.  
 7 
SUPPLEMENTARY METHODS 
Particle Image Velocimetry (PIV) analysis 
DIC images of fertilized eggs were analyzed using custom written software in 
MATLAB (The Mathworks Inc., Natick, MA, USA) using algorithms adapted from MatPIV 
v1.6.150
The accuracy of using PIV to measure very small (subpixal) displacements, such as 
observed in the periods between the speed-peaks, was tested by using images of eggs taken at 
a higher magnification (x252, i.e. objective magnification x63, digital magnification 4x) and 
artificially shifting the image and then reducing the magnification and resolution of the image 
.  The algorithm was based on that used in PIV, a standard analysis technique that 
involves the use of pattern matching techniques based on cross-correlating sub-regions 
between sequential pairs of images (see Methods in the main text and Fig. 1a). To calculate a 
displacement for each analysed interrogation region two subsequent PIV iterations were used. 
First, the displacement was calculated for a larger interrogation area and then it was used as 
an estimate of where to centre the search area for the next iteration with a smaller 
interrogation region. The area in which the algorithm looked for the best fit was twice as 
large as the interrogation region itself. In Fig. 1a the figure represents a single iteration of the 
PIV algorithm.  For experiments conducted on Zeiss LSM 510 Meta confocal microscope, an 
initial interrogation region size of 64 x 64 pixels was used in the first iteration and then an 
interrogation region of 32 x 32 pixels was used in the second iteration. The pixel size for this 
imaging system was 0.35 µm. For experiments conducted on Zeiss Axiovert and Deltavision 
microscopes, due to bigger pixel sizes (0.64 and 0.83 µm respectively), in the first iteration 
an initial interrogation region size of 32 x 32 pixels was used and then an interrogation region 
of 16 x 16 pixels was used in the second iteration. The mean speed of cytoplasmic movement 
was calculated by taking the mean magnitude of a square of 11 by 11 vectors in the centre of 
each cell.  
 8 
to the same as that used in experiments (x14, i.e. objective magnification x20, digital 
magnification 0.7x).  The shift was then measured using PIV.  It was found that the error was 
approximately linearly proportional to displacement for displacements of less than 
approximately 0.3 pixels (Supplementary Fig. S6), which includes most of the range of the 
basal movements measured experimentally.  This is in agreement with other studies that 
looked at the accuracy of PIV when measuring small displacements24,26,51
 
.  Displacements of 
the order of the basal movements (between 0.1 and 0.3 pixels/frame or 3.5 - 10.6 nm/s for 
Zeiss LSM 510 Meta, 6.4 - 19.2 nm/s for Zeiss Axiovert and 8.3 - 24.9 nm/s for Deltavision) 
had an error between -18.1% to -15.5% (Supplementary Fig. S6). As the PIV measurements 
are being used for comparative purposes these systematic underestimates had little effect on 
the results or their interpretation.  
Immunostaining 
Embryos were fixed in 4% PFA (30 min, RT or 4ºC overnight), permeabilised with 
0.2–0.5% Triton-X100 (30 min, RT) and blocked with 3% BSA or 10% FCS. Subsequently, 
they were stained with following antibodies and dyes: 
1) mouse anti-tubulin β antibody labeled with FITC (Sigma-Aldrich; dilution 1:50 in 3% 
BSA, 1.5h at RT);  
2) mouse anti-actin β antibody labeled with FITC (Sigma-Aldrich; dilution 1:100 in 3% BSA, 
1.5h at RT);  
3) goat anti-Gata4 primary antibody (Santa Cruz; 1:200 in 10% FCS, overnight in 4ºC) 
followed by a secondary antibody labeled with AlexaFluor 568 (Molecular Probes; 1:1000 in 
10% FCS, 1.5h at RT);  
4) phalloidin labeled with TexasRed or OregonGreen (Invitrogen; 1:100, 30 min, RT or 
overnight, 4ºC);  
 9 
5) Hoechst 33342 (Molecular Probes; 100ng/ul in PBS, 30 min, RT or overnight, 4ºC). 
Embryos were scanned using an inverted confocal microscope (Zeiss LSM 510 Meta).  
 
 
 


Ajduk, A

Ilozue, T

Windsor, S

Yu, Y

Seres, KB

Bomphrey, RJ

Tom, BD

Swann, K

Thomas, A

Graham, C

Zernicka-Goetz, M

Oxford University Research Archive (ORA)

Bomphrey, Richard

Oxford University Research Archive

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An introduction to MatPIV v.1.6.1. In eprint series.

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Ca2+ is required for mouse sperm capacitation and fertilization in vitro.

Ca2+ oscillatory pattern in fertilized mouse eggs affects gene expression and development to term.

Ca2+ signal blockers can inhibit M/A transition in mammalian cells by interfering with the spindle checkpoint.

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Cell cycle-dependent regulation of structure of endoplasmic reticulum and inositol 1,4,5-trisphosphate-induced Ca2+ release in mouse oocytes and embryos.

Changes in actin distribution during fertilization of the mouse egg.

Conventional PKCs regulate the temporal pattern of Ca2+ oscillations at fertilization in mouse eggs.

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https://www.repository.cam.ac.uk/bitstream/handle/1810/278681/Rhythmic%20actomyosin-driven%20contractions%20induced%20by%20sperm%20entry%20predict%20mammalian%20embryo%20viability.pdf?sequence=1&isAllowed=y

Rhythmic actomyosin-driven contractions induced by sperm entry predict mammalian embryo viability.

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