---
_id: '15048'
abstract:
- lang: eng
text: Embryogenesis results from the coordinated activities of different signaling
pathways controlling cell fate specification and morphogenesis. In vertebrate
gastrulation, both Nodal and BMP signaling play key roles in germ layer specification
and morphogenesis, yet their interplay to coordinate embryo patterning with morphogenesis
is still insufficiently understood. Here, we took a reductionist approach using
zebrafish embryonic explants to study the coordination of Nodal and BMP signaling
for embryo patterning and morphogenesis. We show that Nodal signaling triggers
explant elongation by inducing mesendodermal progenitors but also suppressing
BMP signaling activity at the site of mesendoderm induction. Consistent with this,
ectopic BMP signaling in the mesendoderm blocks cell alignment and oriented mesendoderm
intercalations, key processes during explant elongation. Translating these ex
vivo observations to the intact embryo showed that, similar to explants, Nodal
signaling suppresses the effect of BMP signaling on cell intercalations in the
dorsal domain, thus allowing robust embryonic axis elongation. These findings
suggest a dual function of Nodal signaling in embryonic axis elongation by both
inducing mesendoderm and suppressing BMP effects in the dorsal portion of the
mesendoderm.
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
acknowledgement: "We thank Patrick Müller for sharing the chordintt250 mutant zebrafish
line as well as the plasmid for chrd-GFP, Katherine Rogers for sharing the bmp2b
plasmid and Andrea Pauli for sharing the draculin plasmid. Diana Pinheiro generated
the MZlefty1,2;Tg(sebox::EGFP) line. We are grateful to Patrick Müller, Diana Pinheiro
and Katherine Rogers and members of the Heisenberg lab for discussions, technical
advice and feedback on the manuscript. We also thank Anna Kicheva and Edouard Hannezo
for discussions. We thank the Imaging and Optics Facility as well as the Life Science
facility at IST Austria for support with microscopy and fish maintenance.\r\nThis
work was supported by a European Research Council Advanced Grant\r\n(MECSPEC 742573
to C.-P.H.). A.S. is a recipient of a DOC Fellowship of the Austrian\r\nAcademy
of Sciences at IST Austria. Open Access funding provided by Institute of\r\nScience
and Technology Austria. "
article_processing_charge: Yes (via OA deal)
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: Kornelija
full_name: Pranjic-Ferscha, Kornelija
id: 4362B3C2-F248-11E8-B48F-1D18A9856A87
last_name: Pranjic-Ferscha
- 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, Pranjic-Ferscha K, Hauschild R, Heisenberg C-PJ. Robust axis elongation
by Nodal-dependent restriction of BMP signaling. Development. 2024;151(4):1-18.
doi:10.1242/dev.202316
apa: Schauer, A., Pranjic-Ferscha, K., Hauschild, R., & Heisenberg, C.-P. J.
(2024). Robust axis elongation by Nodal-dependent restriction of BMP signaling.
Development. The Company of Biologists. https://doi.org/10.1242/dev.202316
chicago: Schauer, Alexandra, Kornelija Pranjic-Ferscha, Robert Hauschild, and Carl-Philipp
J Heisenberg. “Robust Axis Elongation by Nodal-Dependent Restriction of BMP Signaling.”
Development. The Company of Biologists, 2024. https://doi.org/10.1242/dev.202316.
ieee: A. Schauer, K. Pranjic-Ferscha, R. Hauschild, and C.-P. J. Heisenberg, “Robust
axis elongation by Nodal-dependent restriction of BMP signaling,” Development,
vol. 151, no. 4. The Company of Biologists, pp. 1–18, 2024.
ista: Schauer A, Pranjic-Ferscha K, Hauschild R, Heisenberg C-PJ. 2024. Robust axis
elongation by Nodal-dependent restriction of BMP signaling. Development. 151(4),
1–18.
mla: Schauer, Alexandra, et al. “Robust Axis Elongation by Nodal-Dependent Restriction
of BMP Signaling.” Development, vol. 151, no. 4, The Company of Biologists,
2024, pp. 1–18, doi:10.1242/dev.202316.
short: A. Schauer, K. Pranjic-Ferscha, R. Hauschild, C.-P.J. Heisenberg, Development
151 (2024) 1–18.
date_created: 2024-03-03T23:00:50Z
date_published: 2024-02-01T00:00:00Z
date_updated: 2024-03-04T07:28:25Z
day: '01'
ddc:
- '570'
department:
- _id: CaHe
- _id: Bio
doi: 10.1242/dev.202316
ec_funded: 1
file:
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checksum: 6961ea10012bf0d266681f9628bb8f13
content_type: application/pdf
creator: dernst
date_created: 2024-03-04T07:24:43Z
date_updated: 2024-03-04T07:24:43Z
file_id: '15050'
file_name: 2024_Development_Schauer.pdf
file_size: 14839986
relation: main_file
success: 1
file_date_updated: 2024-03-04T07:24:43Z
has_accepted_license: '1'
intvolume: ' 151'
issue: '4'
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
page: 1-18
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'
publication: Development
publication_identifier:
eissn:
- 1477-9129
issn:
- 0950-1991
publication_status: published
publisher: The Company of Biologists
quality_controlled: '1'
related_material:
record:
- id: '14926'
relation: research_data
status: public
scopus_import: '1'
status: public
title: Robust axis elongation by Nodal-dependent restriction of BMP signaling
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
volume: 151
year: '2024'
...
---
_id: '12891'
abstract:
- lang: eng
text: "The tight spatiotemporal coordination of signaling activity determining embryo\r\npatterning
and the physical processes driving embryo morphogenesis renders\r\nembryonic development
robust, such that key developmental processes can unfold\r\nrelatively normally
even outside of the full embryonic context. For instance, embryonic\r\nstem cell
cultures can recapitulate the hallmarks of gastrulation, i.e. break symmetry\r\nleading
to germ layer formation and morphogenesis, in a very reduced environment.\r\nThis
leads to questions on specific contributions of embryo-specific features, such
as\r\nthe presence of extraembryonic tissues, which are inherently involved in
gastrulation\r\nin the full embryonic context. To address this, we established
zebrafish embryonic\r\nexplants without the extraembryonic yolk cell, an important
player as a signaling\r\nsource and for morphogenesis during gastrulation, as
a model of ex vivo development.\r\nWe found that dorsal-marginal determinants
are required and sufficient in these\r\nexplants to form and pattern all three
germ layers. However, formation of tissues,\r\nwhich require the highest Nodal-signaling
levels, is variable, demonstrating a\r\ncontribution of extraembryonic tissues
for reaching peak Nodal signaling levels.\r\nBlastoderm explants also undergo
gastrulation-like axis elongation. We found that this\r\nelongation movement shows
hallmarks of oriented mesendoderm cell intercalations\r\ntypically associated
with dorsal tissues in the intact embryo. These are disrupted by\r\nuniform upregulation
of BMP signaling activity and concomitant explant ventralization,\r\nsuggesting
that tight spatial control of BMP signaling is a prerequisite for explant\r\nmorphogenesis.
This control is achieved by Nodal signaling, which is critical for\r\neffectively
downregulating BMP signaling in the mesendoderm, highlighting that Nodal\r\nsignaling
is not only directly required for mesendoderm cell fate specification and\r\nmorphogenesis,
but also by maintaining low levels of BMP signaling at the dorsal side.\r\nCollectively,
we provide insights into the capacity and organization of signaling and\r\nmorphogenetic
domains to recapitulate features of zebrafish gastrulation outside of\r\nthe full
embryonic context."
acknowledged_ssus:
- _id: Bio
- _id: LifeSc
alternative_title:
- ISTA Thesis
article_processing_charge: No
author:
- first_name: Alexandra
full_name: Schauer, Alexandra
id: 30A536BA-F248-11E8-B48F-1D18A9856A87
last_name: Schauer
orcid: 0000-0001-7659-9142
citation:
ama: 'Schauer A. Mesendoderm formation in zebrafish gastrulation: The role of extraembryonic
tissues. 2023. doi:10.15479/at:ista:12891'
apa: 'Schauer, A. (2023). Mesendoderm formation in zebrafish gastrulation: The
role of extraembryonic tissues. Institute of Science and Technology Austria.
https://doi.org/10.15479/at:ista:12891'
chicago: 'Schauer, Alexandra. “Mesendoderm Formation in Zebrafish Gastrulation:
The Role of Extraembryonic Tissues.” Institute of Science and Technology Austria,
2023. https://doi.org/10.15479/at:ista:12891.'
ieee: 'A. Schauer, “Mesendoderm formation in zebrafish gastrulation: The role of
extraembryonic tissues,” Institute of Science and Technology Austria, 2023.'
ista: 'Schauer A. 2023. Mesendoderm formation in zebrafish gastrulation: The role
of extraembryonic tissues. Institute of Science and Technology Austria.'
mla: 'Schauer, Alexandra. Mesendoderm Formation in Zebrafish Gastrulation: The
Role of Extraembryonic Tissues. Institute of Science and Technology Austria,
2023, doi:10.15479/at:ista:12891.'
short: 'A. Schauer, Mesendoderm Formation in Zebrafish Gastrulation: The Role of
Extraembryonic Tissues, Institute of Science and Technology Austria, 2023.'
date_created: 2023-05-05T08:48:20Z
date_published: 2023-05-05T00:00:00Z
date_updated: 2023-08-21T06:25:48Z
day: '05'
ddc:
- '570'
degree_awarded: PhD
department:
- _id: GradSch
- _id: CaHe
doi: 10.15479/at:ista:12891
ec_funded: 1
file:
- access_level: closed
checksum: 59b0303dc483f40a96a610a90aab7ee9
content_type: application/pdf
creator: aschauer
date_created: 2023-05-05T13:01:14Z
date_updated: 2023-05-05T13:01:14Z
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embargo_to: open_access
file_id: '12907'
file_name: Thesis_Schauer_final.pdf
file_size: 31434230
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content_type: application/vnd.openxmlformats-officedocument.wordprocessingml.document
creator: aschauer
date_created: 2023-05-05T13:04:15Z
date_updated: 2023-05-05T13:04:15Z
file_id: '12908'
file_name: Thesis_Schauer_final.docx
file_size: 43809109
relation: source_file
file_date_updated: 2023-05-05T13:04:15Z
has_accepted_license: '1'
language:
- iso: eng
month: '05'
oa_version: Published Version
page: '190'
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'
publication_identifier:
issn:
- 2663 - 337X
publication_status: published
publisher: Institute of Science and Technology Austria
related_material:
record:
- id: '8966'
relation: part_of_dissertation
status: public
- id: '7888'
relation: part_of_dissertation
status: public
status: public
supervisor:
- 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
title: 'Mesendoderm formation in zebrafish gastrulation: The role of extraembryonic
tissues'
type: dissertation
user_id: 8b945eb4-e2f2-11eb-945a-df72226e66a9
year: '2023'
...
---
_id: '8966'
abstract:
- lang: eng
text: During development, a single cell is transformed into a highly complex organism
through progressive cell division, specification and rearrangement. An important
prerequisite for the emergence of patterns within the developing organism is to
establish asymmetries at various scales, ranging from individual cells to the
entire embryo, eventually giving rise to the different body structures. This becomes
especially apparent during gastrulation, when the earliest major lineage restriction
events lead to the formation of the different germ layers. Traditionally, the
unfolding of the developmental program from symmetry breaking to germ layer formation
has been studied by dissecting the contributions of different signaling pathways
and cellular rearrangements in the in vivo context of intact embryos. Recent efforts,
using the intrinsic capacity of embryonic stem cells to self-assemble and generate
embryo-like structures de novo, have opened new avenues for understanding the
many ways by which an embryo can be built and the influence of extrinsic factors
therein. Here, we discuss and compare divergent and conserved strategies leading
to germ layer formation in embryos as compared to in vitro systems, their upstream
molecular cascades and the role of extrinsic factors in this process.
acknowledgement: We thank Nicoletta Petridou, Diana Pinheiro, Cornelia Schwayer and
Stefania Tavano for feedback on the manuscript. Research in the Heisenberg lab is
supported by an ERC Advanced Grant (MECSPEC 742573) to C.-P.H. A.S. is a recipient
of a DOC Fellowship of the Austrian Academy of Science.
article_processing_charge: Yes (via OA deal)
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: 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, Heisenberg C-PJ. Reassembling gastrulation. Developmental Biology.
2021;474:71-81. doi:10.1016/j.ydbio.2020.12.014
apa: Schauer, A., & Heisenberg, C.-P. J. (2021). Reassembling gastrulation.
Developmental Biology. Elsevier. https://doi.org/10.1016/j.ydbio.2020.12.014
chicago: Schauer, Alexandra, and Carl-Philipp J Heisenberg. “Reassembling Gastrulation.”
Developmental Biology. Elsevier, 2021. https://doi.org/10.1016/j.ydbio.2020.12.014.
ieee: A. Schauer and C.-P. J. Heisenberg, “Reassembling gastrulation,” Developmental
Biology, vol. 474. Elsevier, pp. 71–81, 2021.
ista: Schauer A, Heisenberg C-PJ. 2021. Reassembling gastrulation. Developmental
Biology. 474, 71–81.
mla: Schauer, Alexandra, and Carl-Philipp J. Heisenberg. “Reassembling Gastrulation.”
Developmental Biology, vol. 474, Elsevier, 2021, pp. 71–81, doi:10.1016/j.ydbio.2020.12.014.
short: A. Schauer, C.-P.J. Heisenberg, Developmental Biology 474 (2021) 71–81.
date_created: 2020-12-22T09:53:34Z
date_published: 2021-06-01T00:00:00Z
date_updated: 2023-08-07T13:30:01Z
day: '01'
ddc:
- '570'
department:
- _id: CaHe
doi: 10.1016/j.ydbio.2020.12.014
ec_funded: 1
external_id:
isi:
- '000639461800008'
file:
- access_level: open_access
checksum: fa2a5731fd16ab171b029f32f031c440
content_type: application/pdf
creator: kschuh
date_created: 2021-08-11T10:28:06Z
date_updated: 2021-08-11T10:28:06Z
file_id: '9880'
file_name: 2021_DevBiology_Schauer.pdf
file_size: 1440321
relation: main_file
success: 1
file_date_updated: 2021-08-11T10:28:06Z
has_accepted_license: '1'
intvolume: ' 474'
isi: 1
keyword:
- Developmental Biology
- Cell Biology
- Molecular Biology
language:
- iso: eng
month: '06'
oa: 1
oa_version: Published Version
page: 71-81
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'
publication: Developmental Biology
publication_identifier:
issn:
- 0012-1606
publication_status: published
publisher: Elsevier
quality_controlled: '1'
related_material:
record:
- id: '12891'
relation: dissertation_contains
status: public
scopus_import: '1'
status: public
title: Reassembling gastrulation
tmp:
image: /images/cc_by_nc_nd.png
legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
(CC BY-NC-ND 4.0)
short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 474
year: '2021'
...
---
_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. eLife. 2020;9. doi:10.7554/elife.55190
apa: Schauer, A., Nunes Pinheiro, D. C., Hauschild, R., & Heisenberg, C.-P.
J. (2020). Zebrafish embryonic explants undergo genetically encoded self-assembly.
ELife. eLife Sciences Publications. https://doi.org/10.7554/elife.55190
chicago: Schauer, Alexandra, Diana C Nunes Pinheiro, Robert Hauschild, and Carl-Philipp
J Heisenberg. “Zebrafish Embryonic Explants Undergo Genetically Encoded Self-Assembly.”
ELife. eLife Sciences Publications, 2020. https://doi.org/10.7554/elife.55190.
ieee: A. Schauer, D. C. Nunes Pinheiro, R. Hauschild, and C.-P. J. Heisenberg, “Zebrafish
embryonic explants undergo genetically encoded self-assembly,” eLife, 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.” ELife, vol. 9, e55190, eLife Sciences Publications,
2020, doi:10.7554/elife.55190.
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:
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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'
...