---
_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. <i>Developmental Cell</i>. 2023;58(7):582-596.e7.
    doi:<a href="https://doi.org/10.1016/j.devcel.2023.02.016">10.1016/j.devcel.2023.02.016</a>
  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. <i>Developmental Cell</i>. Elsevier. <a href="https://doi.org/10.1016/j.devcel.2023.02.016">https://doi.org/10.1016/j.devcel.2023.02.016</a>
  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.” <i>Developmental
    Cell</i>. Elsevier, 2023. <a href="https://doi.org/10.1016/j.devcel.2023.02.016">https://doi.org/10.1016/j.devcel.2023.02.016</a>.
  ieee: K. Huljev <i>et al.</i>, “A hydraulic feedback loop between mesendoderm cell
    migration and interstitial fluid relocalization promotes embryonic axis formation
    in zebrafish,” <i>Developmental Cell</i>, 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.”
    <i>Developmental Cell</i>, vol. 58, no. 7, Elsevier, 2023, p. 582–596.e7, doi:<a
    href="https://doi.org/10.1016/j.devcel.2023.02.016">10.1016/j.devcel.2023.02.016</a>.
  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'
...
---
_id: '7888'
abstract:
- lang: eng
  text: Embryonic stem cell cultures are thought to self-organize into embryoid bodies,
    able to undergo symmetry-breaking, germ layer specification and even morphogenesis.
    Yet, it is unclear how to reconcile this remarkable self-organization capacity
    with classical experiments demonstrating key roles for extrinsic biases by maternal
    factors and/or extraembryonic tissues in embryogenesis. Here, we show that zebrafish
    embryonic tissue explants, prepared prior to germ layer induction and lacking
    extraembryonic tissues, can specify all germ layers and form a seemingly complete
    mesendoderm anlage. Importantly, explant organization requires polarized inheritance
    of maternal factors from dorsal-marginal regions of the blastoderm. Moreover,
    induction of endoderm and head-mesoderm, which require peak Nodal-signaling levels,
    is highly variable in explants, reminiscent of embryos with reduced Nodal signals
    from the extraembryonic tissues. Together, these data suggest that zebrafish explants
    do not undergo bona fide self-organization, but rather display features of genetically
    encoded self-assembly, where intrinsic genetic programs control the emergence
    of order.
article_number: e55190
article_processing_charge: No
article_type: original
author:
- first_name: Alexandra
  full_name: Schauer, Alexandra
  id: 30A536BA-F248-11E8-B48F-1D18A9856A87
  last_name: Schauer
  orcid: 0000-0001-7659-9142
- 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: Robert
  full_name: Hauschild, Robert
  id: 4E01D6B4-F248-11E8-B48F-1D18A9856A87
  last_name: Hauschild
  orcid: 0000-0001-9843-3522
- 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: Schauer A, Nunes Pinheiro DC, Hauschild R, Heisenberg C-PJ. Zebrafish embryonic
    explants undergo genetically encoded self-assembly. <i>eLife</i>. 2020;9. doi:<a
    href="https://doi.org/10.7554/elife.55190">10.7554/elife.55190</a>
  apa: Schauer, A., Nunes Pinheiro, D. C., Hauschild, R., &#38; Heisenberg, C.-P.
    J. (2020). Zebrafish embryonic explants undergo genetically encoded self-assembly.
    <i>ELife</i>. eLife Sciences Publications. <a href="https://doi.org/10.7554/elife.55190">https://doi.org/10.7554/elife.55190</a>
  chicago: Schauer, Alexandra, Diana C Nunes Pinheiro, Robert Hauschild, and Carl-Philipp
    J Heisenberg. “Zebrafish Embryonic Explants Undergo Genetically Encoded Self-Assembly.”
    <i>ELife</i>. eLife Sciences Publications, 2020. <a href="https://doi.org/10.7554/elife.55190">https://doi.org/10.7554/elife.55190</a>.
  ieee: A. Schauer, D. C. Nunes Pinheiro, R. Hauschild, and C.-P. J. Heisenberg, “Zebrafish
    embryonic explants undergo genetically encoded self-assembly,” <i>eLife</i>, vol.
    9. eLife Sciences Publications, 2020.
  ista: Schauer A, Nunes Pinheiro DC, Hauschild R, Heisenberg C-PJ. 2020. Zebrafish
    embryonic explants undergo genetically encoded self-assembly. eLife. 9, e55190.
  mla: Schauer, Alexandra, et al. “Zebrafish Embryonic Explants Undergo Genetically
    Encoded Self-Assembly.” <i>ELife</i>, vol. 9, e55190, eLife Sciences Publications,
    2020, doi:<a href="https://doi.org/10.7554/elife.55190">10.7554/elife.55190</a>.
  short: A. Schauer, D.C. Nunes Pinheiro, R. Hauschild, C.-P.J. Heisenberg, ELife
    9 (2020).
date_created: 2020-05-25T15:01:40Z
date_published: 2020-04-06T00:00:00Z
date_updated: 2023-08-21T06:25:49Z
day: '06'
ddc:
- '570'
department:
- _id: CaHe
- _id: Bio
doi: 10.7554/elife.55190
ec_funded: 1
external_id:
  isi:
  - '000531544400001'
  pmid:
  - '32250246'
file:
- access_level: open_access
  checksum: f6aad884cf706846ae9357fcd728f8b5
  content_type: application/pdf
  creator: dernst
  date_created: 2020-05-25T15:15:43Z
  date_updated: 2020-07-14T12:48:04Z
  file_id: '7890'
  file_name: 2020_eLife_Schauer.pdf
  file_size: 7744848
  relation: main_file
file_date_updated: 2020-07-14T12:48:04Z
has_accepted_license: '1'
intvolume: '         9'
isi: 1
language:
- iso: eng
month: '04'
oa: 1
oa_version: Published Version
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
- _id: 26B1E39C-B435-11E9-9278-68D0E5697425
  grant_number: '25239'
  name: 'Mesendoderm specification in zebrafish: The role of extraembryonic tissues'
- _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: eLife
publication_identifier:
  issn:
  - 2050-084X
publication_status: published
publisher: eLife Sciences Publications
quality_controlled: '1'
related_material:
  record:
  - id: '12891'
    relation: dissertation_contains
    status: public
scopus_import: '1'
status: public
title: Zebrafish embryonic explants undergo genetically encoded self-assembly
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: 9
year: '2020'
...
---
_id: '7227'
abstract:
- lang: eng
  text: Gastrulation entails specification and formation of three embryonic germ layers—ectoderm,
    mesoderm and endoderm—thereby establishing the basis for the future body plan.
    In zebrafish embryos, germ layer specification occurs during blastula and early
    gastrula stages (Ho & Kimmel, 1993), a period when the main morphogenetic movements
    underlying gastrulation are initiated. Hence, the signals driving progenitor cell
    fate specification, such as Nodal ligands from the TGF-β family, also play key
    roles in regulating germ layer progenitor cell segregation (Carmany-Rampey & Schier,
    2001; David & Rosa, 2001; Feldman et al., 2000; Gritsman et al., 1999; Keller
    et al., 2008). In this review, we summarize and discuss the main signaling pathways
    involved in germ layer progenitor cell fate specification and segregation, specifically
    focusing on recent advances in understanding the interplay between mesoderm and
    endoderm specification and the internalization movements at the onset of zebrafish
    gastrulation.
acknowledgement: We thank Alexandra Schauer, Nicoletta Petridou and Feyza Nur Arslan
  for comments on the manuscript. Research in the Heisenberg laboratory is supported
  by an ERC Advanced Grant (MECSPEC 742573), ANR/FWF (I03601) and FWF/DFG (I03196)
  International Cooperation Grants. D. Pinheiro acknowledges a fellowship from EMBO
  ALTF (850-2017) and is currently supported by HFSP LTF (LT000429/2018-L2).
alternative_title:
- Current Topics in Developmental Biology
article_processing_charge: No
author:
- 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: 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: 'Nunes Pinheiro DC, Heisenberg C-PJ. Zebrafish gastrulation: Putting fate in
    motion. In: <i>Gastrulation: From Embryonic Pattern to Form</i>. Vol 136. Elsevier;
    2020:343-375. doi:<a href="https://doi.org/10.1016/bs.ctdb.2019.10.009">10.1016/bs.ctdb.2019.10.009</a>'
  apa: 'Nunes Pinheiro, D. C., &#38; Heisenberg, C.-P. J. (2020). Zebrafish gastrulation:
    Putting fate in motion. In <i>Gastrulation: From Embryonic Pattern to Form</i>
    (Vol. 136, pp. 343–375). Elsevier. <a href="https://doi.org/10.1016/bs.ctdb.2019.10.009">https://doi.org/10.1016/bs.ctdb.2019.10.009</a>'
  chicago: 'Nunes Pinheiro, Diana C, and Carl-Philipp J Heisenberg. “Zebrafish Gastrulation:
    Putting Fate in Motion.” In <i>Gastrulation: From Embryonic Pattern to Form</i>,
    136:343–75. Elsevier, 2020. <a href="https://doi.org/10.1016/bs.ctdb.2019.10.009">https://doi.org/10.1016/bs.ctdb.2019.10.009</a>.'
  ieee: 'D. C. Nunes Pinheiro and C.-P. J. Heisenberg, “Zebrafish gastrulation: Putting
    fate in motion,” in <i>Gastrulation: From Embryonic Pattern to Form</i>, vol.
    136, Elsevier, 2020, pp. 343–375.'
  ista: 'Nunes Pinheiro DC, Heisenberg C-PJ. 2020.Zebrafish gastrulation: Putting
    fate in motion. In: Gastrulation: From Embryonic Pattern to Form. Current Topics
    in Developmental Biology, vol. 136, 343–375.'
  mla: 'Nunes Pinheiro, Diana C., and Carl-Philipp J. Heisenberg. “Zebrafish Gastrulation:
    Putting Fate in Motion.” <i>Gastrulation: From Embryonic Pattern to Form</i>,
    vol. 136, Elsevier, 2020, pp. 343–75, doi:<a href="https://doi.org/10.1016/bs.ctdb.2019.10.009">10.1016/bs.ctdb.2019.10.009</a>.'
  short: 'D.C. Nunes Pinheiro, C.-P.J. Heisenberg, in:, Gastrulation: From Embryonic
    Pattern to Form, Elsevier, 2020, pp. 343–375.'
date_created: 2020-01-05T23:00:46Z
date_published: 2020-06-01T00:00:00Z
date_updated: 2023-09-06T14:54:36Z
day: '01'
department:
- _id: CaHe
doi: 10.1016/bs.ctdb.2019.10.009
ec_funded: 1
external_id:
  isi:
  - '000611830600013'
  pmid:
  - '31959295'
intvolume: '       136'
isi: 1
language:
- iso: eng
month: '06'
oa_version: None
page: 343-375
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
- _id: 2646861A-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: I03601
  name: Control of embryonic cleavage pattern
- _id: 2608FC64-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: I03196
  name: Control of epithelial cell layer spreading in zebrafish
- _id: 266BC5CE-B435-11E9-9278-68D0E5697425
  grant_number: LT000429
  name: Coordination of mesendoderm fate specification and internalization during
    zebrafish gastrulation
- _id: 26520D1E-B435-11E9-9278-68D0E5697425
  grant_number: ALTF 850-2017
  name: Coordination of mesendoderm cell fate specification and internalization during
    zebrafish gastrulation
publication: 'Gastrulation: From Embryonic Pattern to Form'
publication_identifier:
  issn:
  - '00702153'
publication_status: published
publisher: Elsevier
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Zebrafish gastrulation: Putting fate in motion'
type: book_chapter
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 136
year: '2020'
...