Gastrulation

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Introduction

Human embryo primitive streak
Hans Spemann (1869 - 1941)

Gastrulation means the formation of gut (Greek, gastrula = belly), but has now a more broad sense to to describe the formation of the trilaminar embryo. The epiblast layer, consisting of totipotential cells, derives all 3 embryo layers: endoderm, mesoderm and ectoderm. The primitive streak is the visible feature which represents the site of cell migration to form the additional layers.

Historically, gastrulation was one of the earliest observable morphological event occurring in the frog embryo. Currently, the molecular and physical mechanisms that regulate patterning and migration during this key event are being investigated in several different animal models. This region was also called the "Spemann's organiser" after Hans Spemann (1869 - 1941) who identified the region in amphibia. The same region in birds it is known as "Hensen's node" named for Victor Hensen (1835 – 1924) and is also known generally as the primitive node or knot. In humans, it is proposed that similar mechanisms regulate gastrulation to those found in other vertebrates.


  • primitive node - region in the middle of the early embryonic disc epiblast from which the primitive streak extends caudally (tail)
    • nodal cilia establish the embryo left/right axis
    • axial process extends from the nodal epiblast
  • primitive streak - region of cell migration from the epiblast layer forming sequentially the two germ cell layers (endoderm and mesoderm)

Epithelial to Mesenchymal Transition

Gastrulation cartoon

Epithelial cells (organised cellular layer) which loose their organisation and migrate/proliferate as a mesenchymal cells (disorganised cellular layers) are said to have undergone an Epithelial Mesenchymal Transition (EMT). Mesenchymal cells have an embryonic connective tissue-like cellular arrangement, that have undergone this process may at a later time and under specific signaling conditions undergo the opposite process, mesenchyme to epithelia. In development, this process can be repeated several times during tissue differentiation.

This process occurs at the primitive streak where epiblast cells undergo an epithelial to mesenchymal transition in order to delaminate and migrate.


Links: Gastrulation | Lecture - Week 3 | Week 3 | stage 7 | stage 8 | Endoderm | Mesoderm | Ectoderm | Epithelial Mesenchymal Transition | Notochord
Historic Embryology - Gastrulation 
Historic Papers: 1910 Gastrulation | 1935 Nobel Lecture | 1951 Frog Gastrulation

Some Recent Findings

  • Review - Molecular specification of germ layers in vertebrate embryos[1] "In order to generate the tissues and organs of a multicellular organism, different cell types have to be generated during embryonic development. The first step in this process of cellular diversification is the formation of the three germ layers: ectoderm, endoderm and mesoderm. The ectoderm gives rise to the nervous system, epidermis and various neural crest-derived tissues, the endoderm goes on to form the gastrointestinal, respiratory and urinary systems as well as many endocrine glands, and the mesoderm will form the notochord, axial skeleton, cartilage, connective tissue, trunk muscles, kidneys and blood. Classic experiments in amphibian embryos revealed the tissue interactions involved in germ layer formation and provided the groundwork for the identification of secreted and intracellular factors involved in this process."
  • Rho kinase activity controls directional cell movements during primitive streak formation in the rabbit embryo[2] "During animal gastrulation, the specification of the embryonic axes is accompanied by epithelio-mesenchymal transition (EMT), the first major change in cell shape after fertilization. EMT takes place in disparate topographical arrangements, such as the circular blastopore of amphibians, the straight primitive streak of birds and mammals or in intermediate gastrulation forms of other amniotes such as reptiles. Planar cell movements are prime candidates to arrange specific modes of gastrulation but there is no consensus view on their role in different vertebrate classes. Here, we test the impact of interfering with Rho kinase-mediated cell movements on gastrulation topography in blastocysts of the rabbit, which has a flat embryonic disc typical for most mammals. Time-lapse video microscopy, electron microscopy, gene expression and morphometric analyses of the effect of inhibiting ROCK activity showed - besides normal specification of the organizer region - a dose-dependent disruption of primitive streak formation; this disruption resulted in circular, arc-shaped or intermediate forms, reminiscent of those found in amphibians, fishes and reptiles. Our results reveal a crucial role of ROCK-controlled directional cell movements during rabbit primitive streak formation and highlight the possibility that temporal and spatial modulation of cell movements were instrumental for the evolution of gastrulation forms." Rabbit Development
  • Generation of organized germ layers from a single mouse embryonic stem cell[3] "Mammalian inner cell mass cells undergo lineage-specific differentiation into germ layers of endoderm, mesoderm and ectoderm during gastrulation. It has been a long-standing challenge in developmental biology to replicate these organized germ layer patterns in culture. Here we present a method of generating organized germ layers from a single mouse embryonic stem cell cultured in a soft fibrin matrix." Stem Cells
  • Deficiency in crumbs homolog 2 (Crb2) affects gastrulation and results in embryonic lethality in mice[4] "The Crumbs family of transmembrane proteins has an important role in the differentiation of the apical membrane domain in various cell types, regulating such processes as epithelial cell polarization. The mammalian Crumbs protein family is composed of three members. Here, we inactivated the mouse Crb2 gene with gene-targeting techniques and found that the protein is crucial for early embryonic development with severe abnormalities appearing in Crb2-deficient embryos at late-gastrulation. Our findings indicate that the primary defect in the mutant embryos is disturbed polarity of the epiblast cells at the primitive streak, which affects epithelial to mesenchymal transition (EMT) during gastrulation, resulting in impaired mesoderm and endoderm formation, and embryonic lethality by embryonic day 12.5. These findings therefore indicate a novel role for the Crumbs family of proteins."
  • Zebrafish eve1 regulates the lateral and ventral fates of mesodermal progenitor cells at the onset of gastrulation[5] "Our data show that Eve1 functions together with Ved, Vent and Vox in a transcriptional network to prevent the spread of anti-Bmp gene activity from the dorsal side, leading to the establishment of the Bmp gradient activity along the dorsoventral axis to induce distinct transcriptional outputs in mesodermal progenitor cells (MPCs) to maintain the lateral and ventral MPC fates during gastrulation."
More recent papers
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This table shows an automated computer PubMed search using the listed sub-heading term.

  • Therefore the list of references do not reflect any editorial selection of material based on content or relevance.
  • References appear in this list based upon the date of the actual page viewing.

References listed on the rest of the content page and the associated discussion page (listed under the publication year sub-headings) do include some editorial selection based upon both relevance and availability.

Links: References | Discussion Page | Pubmed Most Recent | Journal Searches


Search term: Gastrulation

Yuko Komiya, Zhiyong Bai, Na Cai, Liping Lou, Namariq Al-Saadi, Courtney Mezzacappa, Raymond Habas, Loren W Runnels A Nonredundant Role for the TRPM6 Channel in Neural Tube Closure. Sci Rep: 2017, 7(1);15623 PubMed 29142255

Vani Joshi, Pancharatna Katti Developmental Toxicity Assay for Food Additive Tartrazine Using Zebrafish ( Danio rerio) Embryo Cultures. Int. J. Toxicol.: 2017;1091581817735227 PubMed 29130832

A M Abdol, Andrew Bedard, Imke Lansky, J A Kaandorp High-throughput method for extracting and visualizing the spatial gene expressions from in situ hybridization images: A case study of the early development of the sea anemone Nematostella vectensis. Gene Expr. Patterns: 2017; PubMed 29122675

Megan L Norris, Andrea Pauli, James A Gagnon, Nathan D Lord, Katherine W Rogers, Christian Mosimann, Leonard I Zon, Alexander F Schier Toddler signaling regulates mesodermal cell migration downstream of Nodal signaling. Elife: 2017, 6; PubMed 29117894

Xiao-Ning Cheng, Ming Shao, Ji-Tong Li, Yan-Fei Wang, Jing Qi, Zhi-Gang Xu, De-Li Shi Leucine repeat adaptor protein 1 interacts with Dishevelled to regulate gastrulation cell movements in zebrafish. Nat Commun: 2017, 8(1);1353 PubMed 29116181

Gastrulation Movies

Animation showing the secondary spread of mesoderm following the migration of endoderm through the primitive streak.
Mesoderm 001 icon.jpg
 ‎‎Week 3 Mesoderm
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Nodal-cilia-001-icon.jpg
 ‎‎Nodal Cilia
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Quail HH stage 2 fibronectin movement.jpg
 ‎‎Gastrulation ECM
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Gastrulation planar cell move icon.jpg
 ‎‎Planar Movement
Page | Play
Mesoderm migration movie 1 icon.jpg
 ‎‎Mesoderm Move
Page | Play
mesoderm spread mouse cilia quail extracellular matrix Planar cell movement Mesoderm migration

Human Gastrulation

The site of gastrulation, the primitive streak is visible during week 3 on the epiblast dorsal surface of the embryonic disc.

Stage 7

Stage7-sem4.jpg Stage7-bf4.jpg

Stage7 primitive streak labelled.jpg


Links: Carnegie stage 7

Stage 8

Stage8 bf10.jpg

Primitive pit

Stage8 bf11.jpg

Primitive groove and primitive streak


Links: Carnegie stage 8

Gastrulation Concepts

Chicken-gastrulation2.jpg


Chicken-gastrulation3.jpg


Links: Chicken Development


Germ Layer Markers

Stem cell researchers have used the following markers to identify early differentiation of cells in the three germ layer in embryoid bodies.[6]


Links: Induced Stem Cells | Alpha-Fetoprotein

Frog Gastrulation

Rugh 071.jpg Frog Gastrulation[7]

(A) The blastula stage, prior to any gastrulation movement.

(B) Movement of the blastula cells preliminary to gastrulation.

(C) Blastoporal view of successive phases of gastrulation; (solid line) lip of blastopore, {dotted line) germ ring, to be subsequently incorporated into the blastoporal lips.

(D) Lateral view of sagittal section during late gastrulation showing the origin of the mesial notochord, and the lateral mesoderm from the proliferated chorda-mesoderm cells at the dorsal lip.

(E) Composite drawing to illustrate the germ layer relations in the later gastrula of the frog. The medullary plate (ectoderm) is not indicated; {alternate dots and dashes) notochord, {heavy stippling) notochord, {sparse stippling) mesoderm, (cellular markings) ectoderm.

Links: Frog Development

Zebrafish Gastrulation

Kupffer's vesicle (ciliated organ of asymmetry, primitive node) a transient epithelial fluid-filled sac located midventrally posterior to the yolk cell or its extension. The vesicle has been described as equivalent to the primitive node for establishing embryo left-right (L-R) axis.[8]

Links: Zebrafish Development

Additional Images

References

  1. Clemens Kiecker, Thomas Bates, Esther Bell Molecular specification of germ layers in vertebrate embryos. Cell. Mol. Life Sci.: 2015; PubMed 26667903
  2. Viktoria Stankova, Nikoloz Tsikolia, Christoph Viebahn Rho kinase activity controls directional cell movements during primitive streak formation in the rabbit embryo. Development: 2015, 142(1);92-8 PubMed 25516971
  3. Yeh-Chuin Poh, Junwei Chen, Ying Hong, Haiying Yi, Shuang Zhang, Junjian Chen, Douglas C Wu, Lili Wang, Qiong Jia, Rishi Singh, Wenting Yao, Youhua Tan, Arash Tajik, Tetsuya S Tanaka, Ning Wang Generation of organized germ layers from a single mouse embryonic stem cell. Nat Commun: 2014, 5;4000 PubMed 24873804
  4. Zhijie Xiao, Jaakko Patrakka, Masatoshi Nukui, Lijun Chi, Dadi Niu, Christer Betsholtz, Timo Pikkarainen, Timo Pikkarainan, Seppo Vainio, Karl Tryggvason Deficiency in Crumbs homolog 2 (Crb2) affects gastrulation and results in embryonic lethality in mice. Dev. Dyn.: 2011, 240(12);2646-56 PubMed 22072575
  5. Jamie L Seebald, Daniel P Szeto Zebrafish eve1 regulates the lateral and ventral fates of mesodermal progenitor cells at the onset of gastrulation. Dev. Biol.: 2011, 349(1);78-89 PubMed 20950598
  6. Mari Pekkanen-Mattila, Markku Pelto-Huikko, Ville Kujala, Riitta Suuronen, Heli Skottman, Katriina Aalto-Setälä, Erja Kerkelä Spatial and temporal expression pattern of germ layer markers during human embryonic stem cell differentiation in embryoid bodies. Histochem. Cell Biol.: 2010, 133(5);595-606 PubMed 20369364
  7. Rugh, R. The Frog Its Reproduction and Development (1951)
  8. Wei Gao, Linjie Xu, Rui Guan, Xinxing Liu, Yuxiang Han, Qian Wu, Yi Xiao, Fei Qi, Zuoyan Zhu, Shuo Lin, Bo Zhang Wdr18 is required for Kupffer's vesicle formation and regulation of body asymmetry in zebrafish. PLoS ONE: 2011, 6(8);e23386 PubMed 21876750


Reviews

Clemens Kiecker, Thomas Bates, Esther Bell Molecular specification of germ layers in vertebrate embryos. Cell. Mol. Life Sci.: 2015; PubMed 26667903

Sonja Nowotschin, Anna-Katerina Hadjantonakis Cellular dynamics in the early mouse embryo: from axis formation to gastrulation. Curr. Opin. Genet. Dev.: 2010, 20(4);420-7 PubMed 20566281

Josh G Chenoweth, Ronald D G McKay, Paul J Tesar Epiblast stem cells contribute new insight into pluripotency and gastrulation. Dev. Growth Differ.: 2010, 52(3);293-301 PubMed 20298258

Jean Paul Thiery, Hervé Acloque, Ruby Y J Huang, M Angela Nieto Epithelial-mesenchymal transitions in development and disease. Cell: 2009, 139(5);871-90 PubMed 19945376

Isabelle Roszko, Atsushi Sawada, Lilianna Solnica-Krezel Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin. Cell Dev. Biol.: 2009, 20(8);986-97 PubMed 19761865

Monica R Rohrschneider, Jeremy Nance Polarity and cell fate specification in the control of Caenorhabditis elegans gastrulation. Dev. Dyn.: 2009, 238(4);789-96 PubMed 19253398

Carl-Philipp Heisenberg, Lilianna Solnica-Krezel Back and forth between cell fate specification and movement during vertebrate gastrulation. Curr. Opin. Genet. Dev.: 2008, 18(4);311-6 PubMed 18721878

Christopher Watters Video views and reviews: gastrulation and the fashioning of animal embryos. Cell Biol Educ: 2005, 4(4);273-8 PubMed 16344860

C Viebahn Hensen's node. Genesis: 2001, 29(2);96-103 PubMed 11170350

M Leptin Gastrulation in Drosophila: the logic and the cellular mechanisms. EMBO J.: 1999, 18(12);3187-92 PubMed 10369659


Articles

Manli Chuai, David Hughes, Cornelis J Weijer Collective epithelial and mesenchymal cell migration during gastrulation. Curr. Genomics: 2012, 13(4);267-77 PubMed 23204916

Viktoriya Halacheva, Mathias Fuchs, Jürgen Dönitz, Tobias Reupke, Bernd Püschel, Christoph Viebahn Planar cell movements and oriented cell division during early primitive streak formation in the mammalian embryo. Dev. Dyn.: 2011, 240(8);1905-16 PubMed 21761476

Bakhtier Vasiev, Ariel Balter, Mark Chaplain, James A Glazier, Cornelis J Weijer Modeling gastrulation in the chick embryo: formation of the primitive streak. PLoS ONE: 2010, 5(5);e10571 PubMed 20485500


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Cite this page: Hill, M.A. 2017 Embryology Gastrulation. Retrieved November 18, 2017, from https://embryology.med.unsw.edu.au/embryology/index.php/Gastrulation

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