---
_id: '14846'
abstract:
- lang: eng
text: Contraction and flow of the actin cell cortex have emerged as a common principle
by which cells reorganize their cytoplasm and take shape. However, how these cortical
flows interact with adjacent cytoplasmic components, changing their form and localization,
and how this affects cytoplasmic organization and cell shape remains unclear.
Here we show that in ascidian oocytes, the cooperative activities of cortical
actomyosin flows and deformation of the adjacent mitochondria-rich myoplasm drive
oocyte cytoplasmic reorganization and shape changes following fertilization. We
show that vegetal-directed cortical actomyosin flows, established upon oocyte
fertilization, lead to both the accumulation of cortical actin at the vegetal
pole of the zygote and compression and local buckling of the adjacent elastic
solid-like myoplasm layer due to friction forces generated at their interface.
Once cortical flows have ceased, the multiple myoplasm buckles resolve into one
larger buckle, which again drives the formation of the contraction pole—a protuberance
of the zygote’s vegetal pole where maternal mRNAs accumulate. Thus, our findings
reveal a mechanism where cortical actomyosin network flows determine cytoplasmic
reorganization and cell shape by deforming adjacent cytoplasmic components through
friction forces.
acknowledged_ssus:
- _id: EM-Fac
- _id: Bio
- _id: NanoFab
acknowledgement: We would like to thank A. McDougall, E. Hannezo and the Heisenberg
lab for fruitful discussions and reagents. We also thank E. Munro for the iMyo-YFP
and Bra>iMyo-mScarlet constructs. This research was supported by the Scientific
Service Units of the Institute of Science and Technology Austria through resources
provided by the Electron Microscopy Facility, Imaging and Optics Facility and the
Nanofabrication Facility. This work was supported by a Joint Project Grant from
the FWF (I 3601-B27).
article_processing_charge: Yes (in subscription journal)
article_type: original
author:
- first_name: Silvia
full_name: Caballero Mancebo, Silvia
id: 2F1E1758-F248-11E8-B48F-1D18A9856A87
last_name: Caballero Mancebo
orcid: 0000-0002-5223-3346
- first_name: Rushikesh
full_name: Shinde, Rushikesh
last_name: Shinde
- first_name: Madison
full_name: Bolger-Munro, Madison
id: 516F03FA-93A3-11EA-A7C5-D6BE3DDC885E
last_name: Bolger-Munro
orcid: 0000-0002-8176-4824
- first_name: Matilda
full_name: Peruzzo, Matilda
id: 3F920B30-F248-11E8-B48F-1D18A9856A87
last_name: Peruzzo
orcid: 0000-0002-3415-4628
- first_name: Gregory
full_name: Szep, Gregory
id: 4BFB7762-F248-11E8-B48F-1D18A9856A87
last_name: Szep
- first_name: Irene
full_name: Steccari, Irene
id: 2705C766-9FE2-11EA-B224-C6773DDC885E
last_name: Steccari
- first_name: David
full_name: Labrousse Arias, David
id: CD573DF4-9ED3-11E9-9D77-3223E6697425
last_name: Labrousse Arias
- first_name: Vanessa
full_name: Zheden, Vanessa
id: 39C5A68A-F248-11E8-B48F-1D18A9856A87
last_name: Zheden
orcid: 0000-0002-9438-4783
- first_name: Jack
full_name: Merrin, Jack
id: 4515C308-F248-11E8-B48F-1D18A9856A87
last_name: Merrin
orcid: 0000-0001-5145-4609
- first_name: Andrew
full_name: Callan-Jones, Andrew
last_name: Callan-Jones
- first_name: Raphaël
full_name: Voituriez, Raphaël
last_name: Voituriez
- first_name: Carl-Philipp J
full_name: Heisenberg, Carl-Philipp J
id: 39427864-F248-11E8-B48F-1D18A9856A87
last_name: Heisenberg
orcid: 0000-0002-0912-4566
citation:
ama: Caballero Mancebo S, Shinde R, Bolger-Munro M, et al. Friction forces determine
cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization.
Nature Physics. 2024. doi:10.1038/s41567-023-02302-1
apa: Caballero Mancebo, S., Shinde, R., Bolger-Munro, M., Peruzzo, M., Szep, G.,
Steccari, I., … Heisenberg, C.-P. J. (2024). Friction forces determine cytoplasmic
reorganization and shape changes of ascidian oocytes upon fertilization. Nature
Physics. Springer Nature. https://doi.org/10.1038/s41567-023-02302-1
chicago: Caballero Mancebo, Silvia, Rushikesh Shinde, Madison Bolger-Munro, Matilda
Peruzzo, Gregory Szep, Irene Steccari, David Labrousse Arias, et al. “Friction
Forces Determine Cytoplasmic Reorganization and Shape Changes of Ascidian Oocytes
upon Fertilization.” Nature Physics. Springer Nature, 2024. https://doi.org/10.1038/s41567-023-02302-1.
ieee: S. Caballero Mancebo et al., “Friction forces determine cytoplasmic
reorganization and shape changes of ascidian oocytes upon fertilization,” Nature
Physics. Springer Nature, 2024.
ista: Caballero Mancebo S, Shinde R, Bolger-Munro M, Peruzzo M, Szep G, Steccari
I, Labrousse Arias D, Zheden V, Merrin J, Callan-Jones A, Voituriez R, Heisenberg
C-PJ. 2024. Friction forces determine cytoplasmic reorganization and shape changes
of ascidian oocytes upon fertilization. Nature Physics.
mla: Caballero Mancebo, Silvia, et al. “Friction Forces Determine Cytoplasmic Reorganization
and Shape Changes of Ascidian Oocytes upon Fertilization.” Nature Physics,
Springer Nature, 2024, doi:10.1038/s41567-023-02302-1.
short: S. Caballero Mancebo, R. Shinde, M. Bolger-Munro, M. Peruzzo, G. Szep, I.
Steccari, D. Labrousse Arias, V. Zheden, J. Merrin, A. Callan-Jones, R. Voituriez,
C.-P.J. Heisenberg, Nature Physics (2024).
date_created: 2024-01-21T23:00:57Z
date_published: 2024-01-09T00:00:00Z
date_updated: 2024-03-05T09:33:38Z
day: '09'
department:
- _id: CaHe
- _id: JoFi
- _id: MiSi
- _id: EM-Fac
- _id: NanoFab
doi: 10.1038/s41567-023-02302-1
has_accepted_license: '1'
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
main_file_link:
- open_access: '1'
url: https://doi.org/10.1038/s41567-023-02302-1
month: '01'
oa: 1
oa_version: Published Version
project:
- _id: 2646861A-B435-11E9-9278-68D0E5697425
call_identifier: FWF
grant_number: I03601
name: Control of embryonic cleavage pattern
publication: Nature Physics
publication_identifier:
eissn:
- 1745-2481
issn:
- 1745-2473
publication_status: epub_ahead
publisher: Springer Nature
quality_controlled: '1'
related_material:
link:
- description: News on ISTA Website
relation: press_release
url: https://ista.ac.at/en/news/stranger-than-friction-a-force-initiating-life/
scopus_import: '1'
status: public
title: Friction forces determine cytoplasmic reorganization and shape changes of ascidian
oocytes upon fertilization
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2024'
...
---
_id: '13229'
abstract:
- lang: eng
text: Dynamic reorganization of the cytoplasm is key to many core cellular processes,
such as cell division, cell migration, and cell polarization. Cytoskeletal rearrangements
are thought to constitute the main drivers of cytoplasmic flows and reorganization.
In contrast, remarkably little is known about how dynamic changes in size and
shape of cell organelles affect cytoplasmic organization. Here, we show that within
the maturing zebrafish oocyte, the surface localization of exocytosis-competent
cortical granules (Cgs) upon germinal vesicle breakdown (GVBD) is achieved by
the combined activities of yolk granule (Yg) fusion and microtubule aster formation
and translocation. We find that Cgs are moved towards the oocyte surface through
radially outward cytoplasmic flows induced by Ygs fusing and compacting towards
the oocyte center in response to GVBD. We further show that vesicles decorated
with the small Rab GTPase Rab11, a master regulator of vesicular trafficking and
exocytosis, accumulate together with Cgs at the oocyte surface. This accumulation
is achieved by Rab11-positive vesicles being transported by acentrosomal microtubule
asters, the formation of which is induced by the release of CyclinB/Cdk1 upon
GVBD, and which display a net movement towards the oocyte surface by preferentially
binding to the oocyte actin cortex. We finally demonstrate that the decoration
of Cgs by Rab11 at the oocyte surface is needed for Cg exocytosis and subsequent
chorion elevation, a process central in egg activation. Collectively, these findings
unravel a yet unrecognized role of organelle fusion, functioning together with
cytoskeletal rearrangements, in orchestrating cytoplasmic organization during
oocyte maturation.
acknowledgement: This work was supported by funding from the European Union (European
Research Council Advanced grant 742573) to C.-P.H. The funders had no role in study
design, data collection and analysis, decision to publish, or preparation of the
manuscript.
article_processing_charge: No
article_type: original
author:
- first_name: Shayan
full_name: Shamipour, Shayan
id: 40B34FE2-F248-11E8-B48F-1D18A9856A87
last_name: Shamipour
- first_name: Laura
full_name: Hofmann, Laura
id: b88d43f2-dc74-11ea-a0a7-e41b7912e031
last_name: Hofmann
- first_name: Irene
full_name: Steccari, Irene
id: 2705C766-9FE2-11EA-B224-C6773DDC885E
last_name: Steccari
- first_name: Roland
full_name: Kardos, Roland
id: 4039350E-F248-11E8-B48F-1D18A9856A87
last_name: Kardos
- first_name: Carl-Philipp J
full_name: Heisenberg, Carl-Philipp J
id: 39427864-F248-11E8-B48F-1D18A9856A87
last_name: Heisenberg
orcid: 0000-0002-0912-4566
citation:
ama: Shamipour S, Hofmann L, Steccari I, Kardos R, Heisenberg C-PJ. Yolk granule
fusion and microtubule aster formation regulate cortical granule translocation
and exocytosis in zebrafish oocytes. PLoS Biology. 2023;21(6):e3002146.
doi:10.1371/journal.pbio.3002146
apa: Shamipour, S., Hofmann, L., Steccari, I., Kardos, R., & Heisenberg, C.-P.
J. (2023). Yolk granule fusion and microtubule aster formation regulate cortical
granule translocation and exocytosis in zebrafish oocytes. PLoS Biology.
Public Library of Science. https://doi.org/10.1371/journal.pbio.3002146
chicago: Shamipour, Shayan, Laura Hofmann, Irene Steccari, Roland Kardos, and Carl-Philipp
J Heisenberg. “Yolk Granule Fusion and Microtubule Aster Formation Regulate Cortical
Granule Translocation and Exocytosis in Zebrafish Oocytes.” PLoS Biology.
Public Library of Science, 2023. https://doi.org/10.1371/journal.pbio.3002146.
ieee: S. Shamipour, L. Hofmann, I. Steccari, R. Kardos, and C.-P. J. Heisenberg,
“Yolk granule fusion and microtubule aster formation regulate cortical granule
translocation and exocytosis in zebrafish oocytes,” PLoS Biology, vol.
21, no. 6. Public Library of Science, p. e3002146, 2023.
ista: Shamipour S, Hofmann L, Steccari I, Kardos R, Heisenberg C-PJ. 2023. Yolk
granule fusion and microtubule aster formation regulate cortical granule translocation
and exocytosis in zebrafish oocytes. PLoS Biology. 21(6), e3002146.
mla: Shamipour, Shayan, et al. “Yolk Granule Fusion and Microtubule Aster Formation
Regulate Cortical Granule Translocation and Exocytosis in Zebrafish Oocytes.”
PLoS Biology, vol. 21, no. 6, Public Library of Science, 2023, p. e3002146,
doi:10.1371/journal.pbio.3002146.
short: S. Shamipour, L. Hofmann, I. Steccari, R. Kardos, C.-P.J. Heisenberg, PLoS
Biology 21 (2023) e3002146.
date_created: 2023-07-16T22:01:09Z
date_published: 2023-06-08T00:00:00Z
date_updated: 2023-08-02T06:33:14Z
day: '08'
ddc:
- '570'
department:
- _id: CaHe
doi: 10.1371/journal.pbio.3002146
ec_funded: 1
external_id:
isi:
- '001003199100005'
pmid:
- '37289834'
file:
- access_level: open_access
checksum: 8e88cb0e5a6433a2f1939a9030bed384
content_type: application/pdf
creator: dernst
date_created: 2023-07-18T07:59:58Z
date_updated: 2023-07-18T07:59:58Z
file_id: '13246'
file_name: 2023_PloSBiology_Shamipour.pdf
file_size: 4431723
relation: main_file
success: 1
file_date_updated: 2023-07-18T07:59:58Z
has_accepted_license: '1'
intvolume: ' 21'
isi: 1
issue: '6'
language:
- iso: eng
month: '06'
oa: 1
oa_version: Published Version
page: e3002146
pmid: 1
project:
- _id: 260F1432-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '742573'
name: Interaction and feedback between cell mechanics and fate specification in
vertebrate gastrulation
publication: PLoS Biology
publication_identifier:
eissn:
- 1545-7885
publication_status: published
publisher: Public Library of Science
quality_controlled: '1'
scopus_import: '1'
status: public
title: Yolk granule fusion and microtubule aster formation regulate cortical granule
translocation and exocytosis in zebrafish oocytes
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 21
year: '2023'
...
---
_id: '12830'
abstract:
- lang: eng
text: Interstitial fluid (IF) accumulation between embryonic cells is thought to
be important for embryo patterning and morphogenesis. Here, we identify a positive
mechanical feedback loop between cell migration and IF relocalization and find
that it promotes embryonic axis formation during zebrafish gastrulation. We show
that anterior axial mesendoderm (prechordal plate [ppl]) cells, moving in between
the yolk cell and deep cell tissue to extend the embryonic axis, compress the
overlying deep cell layer, thereby causing IF to flow from the deep cell layer
to the boundary between the yolk cell and the deep cell layer, directly ahead
of the advancing ppl. This IF relocalization, in turn, facilitates ppl cell protrusion
formation and migration by opening up the space into which the ppl moves and,
thereby, the ability of the ppl to trigger IF relocalization by pushing against
the overlying deep cell layer. Thus, embryonic axis formation relies on a hydraulic
feedback loop between cell migration and IF relocalization.
acknowledged_ssus:
- _id: PreCl
- _id: Bio
acknowledgement: We thank Andrea Pauli (IMP) and Edouard Hannezo (ISTA) for fruitful
discussions and support with the SPIM experiments; the Heisenberg group, and especially
Feyza Nur Arslan and Alexandra Schauer, for discussions and feedback; Michaela Jović
(ISTA) for help with the quantitative real-time PCR protocol; the bioimaging and
zebrafish facilities of ISTA for continuous support; Stephan Preibisch (Janelia
Research Campus) for support with the SPIM data analysis; and Nobuhiro Nakamura
(Tokyo Institute of Technology) for sharing α1-Na+/K+-ATPase antibody. This work
was supported by funding from the European Union (European Research Council Advanced
grant 742573 to C.-P.H.), postdoctoral fellowships from EMBO (LTF-850-2017) and
HFSP (LT000429/2018-L2) to D.P., and a PhD fellowship from the Studienstiftung des
deutschen Volkes to F.P.
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Karla
full_name: Huljev, Karla
id: 44C6F6A6-F248-11E8-B48F-1D18A9856A87
last_name: Huljev
- first_name: Shayan
full_name: Shamipour, Shayan
id: 40B34FE2-F248-11E8-B48F-1D18A9856A87
last_name: Shamipour
- first_name: Diana C
full_name: Nunes Pinheiro, Diana C
id: 2E839F16-F248-11E8-B48F-1D18A9856A87
last_name: Nunes Pinheiro
orcid: 0000-0003-4333-7503
- first_name: Friedrich
full_name: Preusser, Friedrich
last_name: Preusser
- first_name: Irene
full_name: Steccari, Irene
id: 2705C766-9FE2-11EA-B224-C6773DDC885E
last_name: Steccari
- first_name: Christoph M
full_name: Sommer, Christoph M
id: 4DF26D8C-F248-11E8-B48F-1D18A9856A87
last_name: Sommer
orcid: 0000-0003-1216-9105
- first_name: Suyash
full_name: Naik, Suyash
id: 2C0B105C-F248-11E8-B48F-1D18A9856A87
last_name: Naik
orcid: 0000-0001-8421-5508
- first_name: Carl-Philipp J
full_name: Heisenberg, Carl-Philipp J
id: 39427864-F248-11E8-B48F-1D18A9856A87
last_name: Heisenberg
orcid: 0000-0002-0912-4566
citation:
ama: Huljev K, Shamipour S, Nunes Pinheiro DC, et al. A hydraulic feedback loop
between mesendoderm cell migration and interstitial fluid relocalization promotes
embryonic axis formation in zebrafish. Developmental Cell. 2023;58(7):582-596.e7.
doi:10.1016/j.devcel.2023.02.016
apa: Huljev, K., Shamipour, S., Nunes Pinheiro, D. C., Preusser, F., Steccari, I.,
Sommer, C. M., … Heisenberg, C.-P. J. (2023). A hydraulic feedback loop between
mesendoderm cell migration and interstitial fluid relocalization promotes embryonic
axis formation in zebrafish. Developmental Cell. Elsevier. https://doi.org/10.1016/j.devcel.2023.02.016
chicago: Huljev, Karla, Shayan Shamipour, Diana C Nunes Pinheiro, Friedrich Preusser,
Irene Steccari, Christoph M Sommer, Suyash Naik, and Carl-Philipp J Heisenberg.
“A Hydraulic Feedback Loop between Mesendoderm Cell Migration and Interstitial
Fluid Relocalization Promotes Embryonic Axis Formation in Zebrafish.” Developmental
Cell. Elsevier, 2023. https://doi.org/10.1016/j.devcel.2023.02.016.
ieee: K. Huljev et al., “A hydraulic feedback loop between mesendoderm cell
migration and interstitial fluid relocalization promotes embryonic axis formation
in zebrafish,” Developmental Cell, vol. 58, no. 7. Elsevier, p. 582–596.e7,
2023.
ista: Huljev K, Shamipour S, Nunes Pinheiro DC, Preusser F, Steccari I, Sommer CM,
Naik S, Heisenberg C-PJ. 2023. A hydraulic feedback loop between mesendoderm cell
migration and interstitial fluid relocalization promotes embryonic axis formation
in zebrafish. Developmental Cell. 58(7), 582–596.e7.
mla: Huljev, Karla, et al. “A Hydraulic Feedback Loop between Mesendoderm Cell Migration
and Interstitial Fluid Relocalization Promotes Embryonic Axis Formation in Zebrafish.”
Developmental Cell, vol. 58, no. 7, Elsevier, 2023, p. 582–596.e7, doi:10.1016/j.devcel.2023.02.016.
short: K. Huljev, S. Shamipour, D.C. Nunes Pinheiro, F. Preusser, I. Steccari, C.M.
Sommer, S. Naik, C.-P.J. Heisenberg, Developmental Cell 58 (2023) 582–596.e7.
date_created: 2023-04-16T22:01:07Z
date_published: 2023-04-10T00:00:00Z
date_updated: 2023-08-01T14:10:38Z
day: '10'
ddc:
- '570'
department:
- _id: CaHe
- _id: Bio
doi: 10.1016/j.devcel.2023.02.016
ec_funded: 1
external_id:
isi:
- '000982111800001'
file:
- access_level: open_access
checksum: c80ca2ebc241232aacdb5aa4b4c80957
content_type: application/pdf
creator: dernst
date_created: 2023-04-17T07:41:25Z
date_updated: 2023-04-17T07:41:25Z
file_id: '12842'
file_name: 2023_DevelopmentalCell_Huljev.pdf
file_size: 7925886
relation: main_file
success: 1
file_date_updated: 2023-04-17T07:41:25Z
has_accepted_license: '1'
intvolume: ' 58'
isi: 1
issue: '7'
language:
- iso: eng
month: '04'
oa: 1
oa_version: Published Version
page: 582-596.e7
project:
- _id: 260F1432-B435-11E9-9278-68D0E5697425
call_identifier: H2020
grant_number: '742573'
name: Interaction and feedback between cell mechanics and fate specification in
vertebrate gastrulation
- _id: 26520D1E-B435-11E9-9278-68D0E5697425
grant_number: ALTF 850-2017
name: Coordination of mesendoderm cell fate specification and internalization during
zebrafish gastrulation
- _id: 266BC5CE-B435-11E9-9278-68D0E5697425
grant_number: LT000429
name: Coordination of mesendoderm fate specification and internalization during
zebrafish gastrulation
publication: Developmental Cell
publication_identifier:
eissn:
- 1878-1551
issn:
- 1534-5807
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: A hydraulic feedback loop between mesendoderm cell migration and interstitial
fluid relocalization promotes embryonic axis formation in zebrafish
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 58
year: '2023'
...