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Gastrulation

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Gastrulation
Gastrulation occurs when a blastula, made up of one layer, folds inward and enlarges to create a gastrula. This diagram is color-coded: ectoderm, blue; endoderm, green; blastocoel (the yolk sac), yellow; and archenteron (the primary gut), purple.
Identifiers
MeSHD054262
Anatomical terminology

Gastrulation is the stage in the early embryonic development of most animals, during which the blastula (a single-layered hollow sphere of cells), or in mammals the blastocyst, is reorganized into a two-layered or three-layered embryo known as the gastrula.[1] Before gastrulation, the embryo is a continuous epithelial sheet of cells; by the end of gastrulation, the embryo has begun differentiation to establish distinct cell lineages, set up the basic axes of the body (e.g. dorsal–ventral, anterior–posterior), and internalized one or more cell types including the prospective gut.[2]

Gastrula layers

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In triploblastic organisms, the gastrula is trilaminar (three-layered). These three germ layers are the ectoderm (outer layer), mesoderm (middle layer), and endoderm (inner layer).[3][4] In diploblastic organisms, such as Cnidaria and Ctenophora, the gastrula has only ectoderm and endoderm. The two layers are also sometimes referred to as the hypoblast and epiblast.[5] Sponges do not go through the gastrula stage.

Gastrulation takes place after cleavage and the formation of the blastula, or blastocyst. Gastrulation is followed by organogenesis, when individual organs develop within the newly formed germ layers.[6] Each layer gives rise to specific tissues and organs in the developing embryo.

Following gastrulation, cells in the body are either organized into sheets of connected cells (as in epithelia), or as a mesh of isolated cells, such as mesenchyme.[4][8]

Basic cell movements

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Although gastrulation patterns exhibit enormous variation throughout the animal kingdom, they are unified by the five basic types of cell movements that occur during gastrulation:[2][9]

  1. Invagination
  2. Involution
  3. Ingression
  4. Delamination
  5. Epiboly

Etymology

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The terms "gastrula" and "gastrulation" were coined by Ernst Haeckel, in his 1872 work "Biology of Calcareous Sponges".[10] Gastrula (literally, "little belly") is a neo-Latin diminutive based on the Ancient Greek γαστήρ gastḗr ("a belly").

Importance

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Lewis Wolpert, pioneering developmental biologist in the field, has been credited for noting that "It is not birth, marriage, or death, but gastrulation which is truly the most important time in your life."[2][11]

A description of the gastrulation process in a human embryo in three dimensions

Model systems

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Gastrulation is highly variable across the animal kingdom but has underlying similarities. Gastrulation has been studied in many animals, but some models have been used for longer than others. Furthermore, it is easier to study development in animals that develop outside the mother. Model organisms whose gastrulation is understood in the greatest detail include the mollusc, sea urchin, frog, and chicken. A human model system is the gastruloid.

Protostomes versus deuterostomes

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The distinction between protostomes and deuterostomes is based on the direction in which the mouth (stoma) develops in relation to the blastopore. Protostome derives from the Greek word protostoma meaning "first mouth" (πρῶτος + στόμα) whereas Deuterostome's etymology is "second mouth" from the words second and mouth (δεύτερος + στόμα).[citation needed]

The major distinctions between deuterostomes and protostomes are found in embryonic development:

Sea urchins

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Sea urchins have been important model organisms in developmental biology since the 19th century.[12] Their gastrulation is often considered the archetype for invertebrate deuterostomes.[13] Experiments along with computer simulations have been used to gain knowledge about gastrulation in the sea urchin. Recent simulations found that planar cell polarity is sufficient to drive sea urchin gastrulation.

Shortly after the blastula hatches from its fertilization envelope, a group cells derived from the micromeres undergoes an epithelial-to-mesenchymal transformation. These cells change their cytoskeleton, become bottle-shaped, lose their adhesions to the cells lateral to them, and then break away from the apical layer to enter the blastocoel.

These micromere-derived cells are called the primary mesenchyme. Since they will form the larval skeleton, they are sometimes called the skeletogenic mesenchyme. These mesenchyme cells begin extending and contracting long, thin (250 nm in diameter and 25 μm long) processes called filopodia. At first the cells appear to move randomly along the inner blastocoel surface, actively making and breaking filopodial connections to the wall of the blastocoel. Eventually, however, they become localized within the prospective ventrolateral region of the blastocoel. Here they fuse into syncytial cables, which will form the axis of the calcium carbonate spicules of the larval skeletal rods

First stage of archenteron invagination As the primary mesenchyme cells leave the vegetal region of the spherical embryo, important changes are occurring in the cells that remains there .These cells thicken and flattened to form a vegetal plate, changing the shape of the blastula, these vegetal plate cells remain bound to one another and to the hyaline layer of the egg ,and they move to fill the gaps caused by ingression of the primary mesenchyme. Moreover, the vegetal plate bends inward and invaginates about one-fourth to one half the way into the blastocoel. Then invagination suddenly ceases. The invaginated region is called the archenteron (primitive gut), and the opening of the archenteron at the vegetal pole is called the blastopore. Invagination appears to be caused by shape changes in the vegetal plate cells and in the extracellular matrix underlying them. Kimberly and Hardin (1998) have shown that a group of vegetal plate cells surrounding the 2-8 cells at the vegetal pole become bottle-shaped, constricting their apical ends. This change causes the cells to pucker inward. Destroying these cells with lasers retards gastrulation. In addition, the hyaline layer at the vegetal plate buckles inward due to changes in its composition .The hyaline layer is actually made up of two layers, an outer lamina made primarily of hyalin protein and an inner lamina composed of fibropellin proteins. Fibropellins are stored in secretory granules within the oocyte and are secreted from those granules after cortical granule exocytosis releases the hyalin protein. By the blastula stage, the fibropellins have formed a mesh like network over the embryo surface. At the time of invagination, the vegetal plate cells (and only those cells) secrete a chondroitin sulfate proteoglycan into the inner lamina of the hyaline layer directly beneath them. This hygroscopic (water absorbing) molecule swells the inner lamina, but not the outer lamina, which causes the vegetal region of the hyaline layer to buckle. Slightly later a second force, arising from the movements of epithelial cells adjacent to the vegetal plate, may facilitate invagination by drawing the buckled layer inward (Burke et al. 1991).At the stage when the skeletogenic mesenchyme cells begin ingressing into the blastocoel, the fates of the vegetal plate cells have already been specified (Ruffins and Ettensohn 1996). The secondary mesenchyme is the first group of cells invaginating, and it forms the tip of the archenteron, leading the way into the blastocoel. It will form the pigment cells, the musculature around the gut, and the coelomic pouches. The endodermal cells adjacent to the micromere-derived mesenchyme become foregut, migrating the farthest distance into the blastocoel. The next layer of endodermal cells becomes midgut, and the last circumferential row to invaginate forms the hindgut and anus.

Second and third stages of archenteron invagination The invagination of the vegetal cells occurs in discrete stages. After a brief pause following the initial invagination, the second phase of archenteron formation begins. During this stage, the archenteron extends dramatically, sometimes tripling its length. In this process of extension, the wide, short gut rudiment is transformed into a long ,thin tube. To accomplish this extension, the cells of the archenteron rearrange themselves by migrating over one another and by flattening themselves (Ettensohn 1985; Hardin and Cheng 1986). This phenomenon, where cells intercalate to narrow the tissue and at the same time move it forward, is called convergent extension (Martins et al. 1998). In all species of sea urchins observed, a third stage of archenteron elongation occurs. This final phase is initiated by the tension provided by secondary mesenchyme cells, which form at the tip of the archenteron and remain there. These cells extend filopodia through the blastocoel fluid to contact the inner surface of the blastocoel wall (Dan and Okazaki 1956; Schroeder 1981). The filopodia attach to the wall at the junctions between the blastomeres and then shorten, pulling up the archenteron. The secondary mesenchyme cells with a laser, with the result that the archenteron could elongate to only about two-thirds of the normal length. If a few secondary mesenchyme cells were left, elongation continued, although at a slower rate. The secondary mesenchyme cells, in this species, play an essential role in pulling the archenteron up to the blastocoel wall during the last phase of invagination. But can the secondary mesenchyme filopodia attach to any part of the blastocoel wall, or is there a specific target in the animal hemisphere that must be present for attachment to occur? Is there a region of the blastocoel wall that is already committed to becoming the ventral side of the larva? Studies by Hardin and McClay (1990) show that there is a specific target site for the filopodia that differs from other regions of the animal hemisphere. The filopodia extend, touch the blastocoel wall at random sites, and then retract. However, when the filopodia contact a particular region of the wall, they remain attached there, flatten out against this region, and pull the archenteron toward it. When Hardin and McClay poked in the other side of the blastocoel wall so that contacts were made most readily with that region, the filopodia continued to extend and retract after touching it. Only when the filopodia found their target tissue did they cease these movements. If the gastrula was constricted so that the filopodia never reached the target area, the secondary mesenchyme cells continued to explore until they eventually moved off the archenteron and found the target as freely migrating cells. There appears, then, to be a target region on what is to become the ventral side of the larva that is recognized by the secondary mesenchyme cells, and which positions the archenteron in the region where the mouth will form. As the top of the archenteron meets the blastocoel wall in the target region, the secondary mesenchyme cells disperse into the blastocoel, where they proliferate to form the mesodermal organs. Where the archenteron contacts the wall, a mouth is eventually formed. The mouth fuses with the archenteron to create a continuous digestive tube. Thus, as is characteristic of deuterostomes, the blastopore marks the position of the anus. As the pluteus larva elongates, the coelomic cavities form from secondary mesenchyme. Under the influence of Nodal protein, as described on page 221, the right coelomic sac remains rudimentary. However, the left coelomic sac undergoes extensive development to form many of the structures of the adult sea urchin. The left sac splits into three smaller sacs. An invagination from the ectoderm fuses with the middle sac to form the imaginal rudiment. This rudiment develops a fivefold symmetry, and skeletogenic mesenchyme cells enter the rudiment to synthesize the first skeletal plates of the shell. The left side of the pluteus becomes, in effect, the future oral surface of the adult sea urchin (Bury 1895; Aihara and Amemiya2001). During metamorphosis, the imaginal rudiment separates from the larva, which then degenerates. While the imaginal rudiment (now called a juvenile) is re-forming its digestive tract and settling on the ocean floor, it is dependent on the nutrition it received from the jettisoned larva. The echinoderm pattern of gastrulation provides the evolutionary prototype for deuterostome development. In deuterostomes (echinoderms, tunicates, cephalochordates, and vertebrates), the first opening becomes the anus while the second opening becomes the mouth.Moreover,in sea urchins we see the phenomena of convergent extension and the use of Nodal gene expression for the establishment of axes. Reference :Development Biology. Eighth Edition by Scott F Gilbert

[14]

Germ layer determination

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Sea urchins exhibit highly stereotyped cleavage patterns and cell fates. Maternally deposited mRNAs establish the organizing center of the sea urchin embryo. Canonical Wnt and Delta-Notch signaling progressively segregate progressive endoderm and mesoderm.[15]

Cell internalization

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In sea urchins the first cells to internalize are the primary mesenchyme cells (PMCs), which have a skeletogenic fate, which ingress during the blastula stage. Gastrulation – internalization of the prospective endoderm and non-skeletogenic mesoderm – begins shortly thereafter with invagination and other cell rearrangements the vegetal pole, which contribute approximately 30% to the final archenteron length. The gut's final length depends on cell rearrangements within the archenteron.[16]

Amphibians

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The frog genus Xenopus has been used as a model organism for the study of gastrulation.[17]

Symmetry breaking

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The sperm contributes one of the two mitotic asters needed to complete first cleavage. The sperm can enter anywhere in the animal half of the egg but its exact point of entry will break the egg's radial symmetry by organizing the cytoskeleton. Prior to first cleavage, the egg's cortex rotates relative to the internal cytoplasm by the coordinated action of microtubules, in a process known as cortical rotation. This displacement brings maternally loaded determinants of cell fate from the equatorial cytoplasm and vegetal cortex into contact, and together these determinants set up the organizer. Thus, the area on the vegetal side opposite the sperm entry point will become the organizer.[18] Hilde Mangold, working in the lab of Hans Spemann, demonstrated that this special "organizer" of the embryo is necessary and sufficient to induce gastrulation.[19][20][21]

Germ layer determination

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Specification of endoderm depends on rearrangement of maternally deposited determinants, leading to nuclearization of Beta-catenin. Mesoderm is induced by signaling from the presumptive endoderm to cells that would otherwise become ectoderm.[18]

Cell internalization

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The dorsal lip of the blastopore is the mechanical driver of gastrulation. The first sign of invagination seen in the frog is the dorsal lip.[citation needed]

Cell signaling

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In the frog, Xenopus, one of the signals is retinoic acid (RA).[22] RA signaling in this organism can affect the formation of the endoderm and depending on the timing of the signaling, it can determine the fate whether its pancreatic, intestinal, or respiratory. Other signals such as Wnt and BMP also play a role in respiratory fate of the Xenopus by activating cell lineage tracers.[22]

Amniotes

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Overview

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In amniotes (reptiles, birds and mammals), gastrulation involves the creation of the blastopore, an opening into the archenteron. Note that the blastopore is not an opening into the blastocoel, the space within the blastula, but represents a new inpocketing that pushes the existing surfaces of the blastula together. In amniotes, gastrulation occurs in the following sequence: (1) the embryo becomes asymmetric; (2) the primitive streak forms; (3) cells from the epiblast at the primitive streak undergo an epithelial to mesenchymal transition and ingress at the primitive streak to form the germ layers.[7]

Symmetry breaking

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In preparation for gastrulation, the embryo must become asymmetric along both the proximal-distal axis and the anteroposterior axis. The proximal-distal axis is formed when the cells of the embryo form the "egg cylinder", which consists of the extraembryonic tissues, which give rise to structures like the placenta, at the proximal end and the epiblast at the distal end. Many signaling pathways contribute to this reorganization, including BMP, FGF, nodal, and Wnt. Visceral endoderm surrounds the epiblast. The distal visceral endoderm (DVE) migrates to the anterior portion of the embryo, forming the anterior visceral endoderm (AVE). This breaks anterior-posterior symmetry and is regulated by nodal signaling.[7]

Epithelial–mesenchymal transition – loss of cell adhesion leads to constriction and extrusion of newly formed mesenchymal cell.

Germ layer determination

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The primitive streak is formed at the beginning of gastrulation and is found at the junction between the extraembryonic tissue and the epiblast on the posterior side of the embryo and the site of ingression.[23] Formation of the primitive streak is reliant upon nodal signaling[7] in the Koller's sickle within the cells contributing to the primitive streak and BMP4 signaling from the extraembryonic tissue.[23][24] Furthermore, Cer1 and Lefty1 restrict the primitive streak to the appropriate location by antagonizing nodal signaling.[25] The region defined as the primitive streak continues to grow towards the distal tip.[7]

During the early stages of development, the primitive streak is the structure that will establish bilateral symmetry, determine the site of gastrulation and initiate germ layer formation.[26] To form the streak, reptiles, birds and mammals arrange mesenchymal cells along the prospective midline, establishing the first embryonic axis, as well as the place where cells will ingress and migrate during the process of gastrulation and germ layer formation.[27] The primitive streak extends through this midline and creates the antero-posterior body axis,[28] becoming the first symmetry-breaking event in the embryo, and marks the beginning of gastrulation.[29] This process involves the ingression of mesoderm and endoderm progenitors and their migration to their ultimate position,[28][30] where they will differentiate into the three germ layers.[27] The localization of the cell adhesion and signaling molecule beta-catenin is critical to the proper formation of the organizer region that is responsible for initiating gastrulation.

Cell internalization

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In order for the cells to move from the epithelium of the epiblast through the primitive streak to form a new layer, the cells must undergo an epithelial to mesenchymal transition (EMT) to lose their epithelial characteristics, such as cell–cell adhesion. FGF signaling is necessary for proper EMT. FGFR1 is needed for the up regulation of SNAI1, which down regulates E-cadherin, causing a loss of cell adhesion. Following the EMT, the cells ingress through the primitive streak and spread out to form a new layer of cells or join existing layers. FGF8 is implicated in the process of this dispersal from the primitive streak.[25]

Cell signaling

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There are certain signals that play a role in determination and formation of the three germ layers, such as FGF, RA, and Wnt.[22] In mammals such as mice, RA signaling can play a role in lung formation. If there is not enough RA, there will be an error in the lung production. RA also regulates the respiratory competence in this mouse model.[citation needed]

Cell signaling driving gastrulation

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During gastrulation, the cells are differentiated into the ectoderm or mesendoderm, which then separates into the mesoderm and endoderm.[22] The endoderm and mesoderm form due to the nodal signaling. Nodal signaling uses ligands that are part of TGFβ family. These ligands will signal transmembrane serine/threonine kinase receptors, and this will then phosphorylate Smad2 and Smad3. This protein will then attach itself to Smad4 and relocate to the nucleus where the mesendoderm genes will begin to be transcribed. The Wnt pathway along with β-catenin plays a key role in nodal signaling and endoderm formation.[31] Fibroblast growth factors (FGF), canonical Wnt pathway, bone morphogenetic protein (BMP), and retinoic acid (RA) are all important in the formation and development of the endoderm.[22] FGF are important in producing the homeobox gene which regulates early anatomical development. BMP signaling plays a role in the liver and promotes hepatic fate. RA signaling also induce homeobox genes such as Hoxb1 and Hoxa5. In mice, if there is a lack in RA signaling the mouse will not develop lungs.[22] RA signaling also has multiple uses in organ formation of the pharyngeal arches, the foregut, and hindgut.[22]

Gastrulation in vitro

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There have been a number of attempts to understand the processes of gastrulation using in vitro techniques in parallel and complementary to studies in embryos, usually though the use of 2D[32][33][34] and 3D cell (Embryonic organoids) culture techniques[35][36][37][38] using embryonic stem cells (ESCs) or induced pluripotent stem cells (iPSCs). These are associated with number of clear advantages in using tissue-culture based protocols, some of which include reducing the cost of associated in vivo work (thereby reducing, replacing and refining the use of animals in experiments; the 3Rs), being able to accurately apply agonists/antagonists in spatially and temporally specific manner[36][37] which may be technically difficult to perform during Gastrulation. However, it is important to relate the observations in culture to the processes occurring in the embryo for context.

To illustrate this, the guided differentiation of mouse ESCs has resulted in generating primitive streak–like cells that display many of the characteristics of epiblast cells that traverse through the primitive streak[32] (e.g. transient brachyury up regulation and the cellular changes associated with an epithelial to mesenchymal transition[32]), and human ESCs cultured on micro patterns, treated with BMP4, can generate spatial differentiation pattern similar to the arrangement of the germ layers in the human embryo.[33][34] Finally, using 3D embryoid body- and organoid-based techniques, small aggregates of mouse ESCs (Embryonic Organoids, or Gastruloids) are able to show a number of processes of early mammalian embryo development such as symmetry-breaking, polarisation of gene expression, gastrulation-like movements, axial elongation and the generation of all three embryonic axes (anteroposterior, dorsoventral and left-right axes).[35][36][37][39]

In vitro fertilization occurs in a laboratory. The process of in vitro fertilization is when mature eggs are removed from the ovaries and are placed in a cultured medium where they are fertilized by sperm. In the culture the embryo will form.[40] 14 days after fertilization the primitive streak forms. The formation of the primitive streak has been known to some countries as "human individuality".[41] This means that the embryo is now a being itself, it is its own entity. The countries that believe this have created a 14-day rule in which it is illegal to study or experiment on a human embryo after the 14-day period in vitro. Research has been conducted on the first 14 days of an embryo, but no known studies have been done after the 14 days.[42] With the rule in place, mice embryos are used understand the development after 14 days; however, there are differences in the development between mice and humans.

See also

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References

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Notes

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  1. ^ Urry, Lisa (2016). Campbell Biology (11th ed.). Pearson. p. 1047. ISBN 978-0134093413.
  2. ^ a b c d e f Gilbert, Scott F.; Michael J. F. Barresi (2016). Developmental biology (Eleventh ed.). Sunderland, Massachusetts: Sinauer. ISBN 978-1-60535-470-5. OCLC 945169933.
  3. ^ Mundlos 2009: p. 422
  4. ^ a b McGeady, 2004: p. 34
  5. ^ Jonathon M.W., Slack (2013). Essential Developmental Biology. West Sussex, UK: Wiley-Blackwell. p. 122. ISBN 978-0-470-92351-1.
  6. ^ Hall, 1998: pp. 132-134
  7. ^ a b c d e Arnold & Robinson, 2009
  8. ^ Hall, 1998: p. 177
  9. ^ Gilbert, Scott F. (2000). "Figure 8.6, [Types of cell movements during...]". www.ncbi.nlm.nih.gov. Retrieved 11 May 2022.
  10. ^ Ereskovsky 2010: p. 236
  11. ^ Wolpert L (2008) The triumph of the embryo. Courier Corporation, page 12. ISBN 978-0-486-46929-4
  12. ^ Laubichler, M.D. and Davidson, E. H. (2008). "Boveri's long experiment: sea urchin merogones and the establishment of the role of nuclear chromosomes in development". Developmental Biology. 314(1):1–11. doi:10.1016/j.ydbio.2007.11.024.
  13. ^ McClay, David R.; Gross, J.M.; Range, Ryan; Peterson, R.E.; Bradham, Cynthia (2004). "Chapter 9: Sea Urchin Gastrulation". In Stern, Claudio D. (ed.). Gastrulation: From Cells to Embryos. Cold Spring Harbor Laboratory Press. pp. 123–137. ISBN 978-0-87969-707-5.
  14. ^ Nielsen, Bjarke Frost; Nissen, Silas Boye; Sneppen, Kim; Mathiesen, Joachim; Trusina, Ala (February 21, 2020). "Model to Link Cell Shape and Polarity with Organogenesis". iScience. 23 (2): 100830. Bibcode:2020iSci...23j0830N. doi:10.1016/j.isci.2020.100830. PMC 6994644. PMID 31986479. S2CID 210934521.
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  19. ^ Gilbert, Scott F. (2000). "Figure 10.20, [Organization of a secondary axis...]". www.ncbi.nlm.nih.gov. Retrieved 1 June 2020.
  20. ^ Spemann H., Mangold H. (1924). "Über Induktion von Embryonanlagen durch Implantation artfremder Organisatoren". Roux' Arch. F. Entw. Mech. 100 (3–4): 599–638. doi:10.1007/bf02108133. S2CID 12605303.
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  22. ^ a b c d e f g Zorn A, Wells J (2009). "Vertebrate Endoderm Development and Organ Formation". Annu Rev Cell Dev Biol. 25: 221–251. doi:10.1146/annurev.cellbio.042308.113344. PMC 2861293. PMID 19575677.
  23. ^ a b Tam & Behringer, 1997
  24. ^ Catala, 2005: p. 1535
  25. ^ a b Tam, P.P.; Loebel, D.A (2007). "Gene function in mouse embryogenesis: get set for gastrulation". Nat Rev Genet. 8 (5): 368–81. doi:10.1038/nrg2084. PMID 17387317. S2CID 138874.
  26. ^ Sheng, Guojun; Arias, Alfonso Martinez; Sutherland, Ann (2021-12-03). "The primitive streak and cellular principles of building an amniote body through gastrulation". Science. 374 (6572): abg1727. doi:10.1126/science.abg1727. PMID 34855481. S2CID 244841366.
  27. ^ a b Mikawa T, Poh AM, Kelly KA, Ishii Y, Reese DE (2004). "Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote". Dev Dyn. 229 (3): 422–32. doi:10.1002/dvdy.10458. PMID 14991697. S2CID 758473.
  28. ^ a b Downs KM. (2009). "The enigmatic primitive streak: prevailing notions and challenges concerning the body axis of mammals". BioEssays. 31 (8): 892–902. doi:10.1002/bies.200900038. PMC 2949267. PMID 19609969.
  29. ^ Chuai M, Zeng W, Yang X, Boychenko V, Glazier JA, Weijer CJ (2006). "Cell movement during chick primitive streak formation". Dev. Biol. 296 (1): 137–49. doi:10.1016/j.ydbio.2006.04.451. PMC 2556955. PMID 16725136.
  30. ^ Chuai M, Weijer CJ (2008). "The mechanisms underlying primitive streak formation in the chick embryo.". Current Topics in Developmental Biology. Vol. 81. pp. 135–56. doi:10.1016/S0070-2153(07)81004-0. ISBN 978-0-12-374253-7. PMID 18023726.
  31. ^ Grapin-Botton, A.; Constam, D. (2007). "Evolution of the mechanisms and molecular control of endoderm formation". Mechanisms of Development. 124 (4): 253–78. doi:10.1016/j.mod.2007.01.001. PMID 17307341. S2CID 16552755.
  32. ^ a b c Turner, David A.; Rué, Pau; Mackenzie, Jonathan P.; Davies, Eleanor; Martinez Arias, Alfonso (2014-01-01). "Brachyury cooperates with Wnt/β-catenin signalling to elicit primitive-streak-like behaviour in differentiating mouse embryonic stem cells". BMC Biology. 12: 63. doi:10.1186/s12915-014-0063-7. ISSN 1741-7007. PMC 4171571. PMID 25115237.
  33. ^ a b Warmflash, Aryeh; Sorre, Benoit; Etoc, Fred; Siggia, Eric D; Brivanlou, Ali H (2014). "A method to recapitulate early embryonic spatial patterning in human embryonic stem cells". Nature Methods. 11 (8): 847–854. doi:10.1038/nmeth.3016. PMC 4341966. PMID 24973948.
  34. ^ a b Etoc, Fred; Metzger, Jakob; Ruzo, Albert; Kirst, Christoph; Yoney, Anna; Ozair, M. Zeeshan; Brivanlou, Ali H.; Siggia, Eric D. (2016). "A Balance between Secreted Inhibitors and Edge Sensing Controls Gastruloid Self-Organization". Developmental Cell. 39 (3): 302–315. doi:10.1016/j.devcel.2016.09.016. PMC 5113147. PMID 27746044.
  35. ^ a b Brink, Susanne C. van den; Baillie-Johnson, Peter; Balayo, Tina; Hadjantonakis, Anna-Katerina; Nowotschin, Sonja; Turner, David A.; Arias, Alfonso Martinez (2014-11-15). "Symmetry breaking, germ layer specification and axial organisation in aggregates of mouse embryonic stem cells". Development. 141 (22): 4231–4242. doi:10.1242/dev.113001. ISSN 0950-1991. PMC 4302915. PMID 25371360.
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Bibliography

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Further reading

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