Epiboly

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Epiboly describes one of the five major types of cell movements that occur in the gastrulation stage of embryonic development of some organisms. [1] Epiboly is the spreading and thinning of the ectoderm while the endoderm and mesoderm layers move to the inside of the embryo. [2]

Contents

When undergoing epiboly, a monolayer of cells must undergo a physical change in shape in order to spread. Alternatively, multiple layers of cells can also undergo epiboly as the position of cells is changed or the cell layers undergo intercalation. While human embryos do not experience epiboly, this movement can be studied in sea urchins, tunicates, amphibians, and most commonly zebrafish.

Epibolic movement of cells during gastrulation Epiboly svg hariadhi.svg
Epibolic movement of cells during gastrulation

Zebrafish

General movements

Epiboly in zebrafish is the first coordinated cell movement, beginning at the dome stage late in the blastula period and continuing throughout gastrulation. [3] At this point the zebrafish embryo contains three portions: an epithelial monolayer known as the enveloping layer (EVL), a yolk syncytial layer (YSL) which is a membrane-enclosed group of nuclei that lie on top of the yolk cell, and the deep cells (DEL) of the blastoderm which will eventually form the embryo's three germ layers (ectoderm, mesoderm, and endoderm). The EVL, YSL, and DEL all undergo epiboly.

Schematic of Zebra Fish epiboly Epiboly process in zebra fish svg hariadhi.svg
Schematic of Zebra Fish epiboly
Cartoon of a 4-hour post fertilization zebrafish embryo, before the initiation of epiboly Zfish midblastula stage embryo.jpg
Cartoon of a 4-hour post fertilization zebrafish embryo, before the initiation of epiboly

Radial intercalation occurs in the DEL. Interior cells of the blastoderm move towards the outer cells, thus "intercalating" with each other. The blastoderm begins to thin as it spreads toward the vegetal pole of the embryo until it has completely engulfed the yolk cell. [4] The EVL also moves vegetally during epiboly, increasing its surface area as it spreads. Work in the ray-finned fish fundulus has shown that no large rearrangements occur in the EVL; instead, cells at the leading edge of the EVL align and constrict. [5] [6] The YSL also moves towards the vegetal pole, spreading along the surface of the yolk and migrating slightly ahead of the blastomeres. [7] Once epiboly is complete, the DEL, EVL, and YSL have engulfed the yolk cell, forming a closure known as the blastopore.

Molecular mechanisms of epiboly

Cytoskeletal and cell adhesion components

Completion of epiboly requires the coordination of cytoskeletal changes across the embryo. The YSL appears to play a prominent role in this process. Studies on fundulus demonstrated that the YSL is capable of undergoing epiboly even when the blastoderm has been removed, however, the blastoderm cannot undergo epiboly in the absence of the YSL. [8] In zebrafish, there is a microtubule array in the yolk that extends from the animal to the vegetal pole of the embryo, and that contracts as epiboly progresses. [9] Treating embryos with the microtubule depolymerizing agent nocodazole completely blocks epiboly of the YSL and partially blocks epiboly of the blastoderm, while treating with the microtubule stabilizing agent taxol blocks epiboly of all cell layers. [9] There is also evidence for the importance of actin-based structures in epiboly. Ring-like structures of filamentous actin have been observed at the leading edge of the enveloping layer, where it contacts the yolk cell. [10] It is thought that a network of filamentous actin in the yolk might constrict in a myosin-II dependent manner to close the blastopore at the end of epiboly, via a "purse-string mechanism". [11] Treating embryos with the actin destabilizer cytochalasin b results in delayed or arrested epiboly. [10]

There is still debate on the extent to which the DEL and EVL epibolic movements are active movements. [12] The EVL contacts the YSL by means of tight junctions. It is thought that these contacts allow the YSL to "tow" the EVL towards the vegetal pole. [8] Claudin E is a molecule found in tight junctions that appears to be expressed in the EVL and required for normal zebrafish epiboly, supporting this hypothesis. [13] Additionally, zebrafish embryos that fail to make a fully differentiated EVL show defects in epibolic movements of the DEL, EVL, and YSL, suggesting a requirement for a normal EVL for the epiboly of all three cell layers. [14]

The cell-cell adhesion molecule E-cadherin has been shown to be required for the radial intercalation of the deep cells. [4] Many other molecules involved in cell-cell contact are implicated in zebrafish epiboly, including G alpha (12/13) which interacts with E-cadherin and actin, as well as the cell adhesion molecule EpCam in the EVL, which may modulate adhesion with the underlying deep cells. [15] [16]

Signaling

The molecule fibronectin has been found to play a role in radial intercalation. [17] Other signaling pathways that appear to function in epiboly include the Wnt/PCP pathway, [18] PDGF-PI3K pathway, [19] Eph-Ephrin signaling, [20] JAK-STAT signaling, [21] and the MAP kinase cascade. [22]

Other vertebrates

Epibolic movements have been conserved in vertebrates. Though most work on epiboly has been done in fish, there is also a body of work concerning epiboly in the African clawed frog, Xenopus laevis . Comparisons of epiboly in amniotes, teleosts and X. laevis show that the key movement of epiboly in the fish and frog is radial intercalation while in amniotes it would appear to be cell division in the plane of the epithelium. All groups undergo cell shape changes such as the characteristic flattening of cells to increase surface area. [23]

Related Research Articles

Morphogenesis is the biological process that causes a cell, tissue or organism to develop its shape. It is one of three fundamental aspects of developmental biology along with the control of tissue growth and patterning of cellular differentiation.

<span class="mw-page-title-main">Embryo</span> Multicellular diploid eukaryote in its earliest stage of development

An embryo is the initial stage of development for a multicellular organism. In organisms that reproduce sexually, embryonic development is the part of the life cycle that begins just after fertilization of the female egg cell by the male sperm cell. The resulting fusion of these two cells produces a single-celled zygote that undergoes many cell divisions that produce cells known as blastomeres. The blastomeres are arranged as a solid ball that when reaching a certain size, called a morula, takes in fluid to create a cavity called a blastocoel. The structure is then termed a blastula, or a blastocyst in mammals.

<span class="mw-page-title-main">Blastulation</span> Sphere of cells formed during early embryonic development in animals

Blastulation is the stage in early animal embryonic development that produces the blastula. In mammalian development, the blastula develops into the blastocyst with a differentiated inner cell mass and an outer trophectoderm. The blastula is a hollow sphere of cells known as blastomeres surrounding an inner fluid-filled cavity called the blastocoel. Embryonic development begins with a sperm fertilizing an egg cell to become a zygote, which undergoes many cleavages to develop into a ball of cells called a morula. Only when the blastocoel is formed does the early embryo become a blastula. The blastula precedes the formation of the gastrula in which the germ layers of the embryo form.

<span class="mw-page-title-main">Gastrulation</span> Stage in embryonic development in which germ layers form

Gastrulation is the stage in the early embryonic development of most animals, during which the blastula, or in mammals the blastocyst, is reorganized into a two-layered or three-layered embryo known as the gastrula. 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, and internalized one or more cell types including the prospective gut.

<span class="mw-page-title-main">Ectoderm</span> Outer germ layer of embryonic development

The ectoderm is one of the three primary germ layers formed in early embryonic development. It is the outermost layer, and is superficial to the mesoderm and endoderm. It emerges and originates from the outer layer of germ cells. The word ectoderm comes from the Greek ektos meaning "outside", and derma meaning "skin".

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<span class="mw-page-title-main">Blastocoel</span> Fluid-filled or yolk-filled cavity that forms in the blastula

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<span class="mw-page-title-main">Neural fold</span> Structure arising during embryonic development of birds and mammals

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<span class="mw-page-title-main">Epiblast</span> Embryonic inner cell mass tissue that forms the embryo itself, through the three germ layers

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<span class="mw-page-title-main">Hypoblast</span> Embryonic inner cell mass tissue that forms the yolk sac and, later, chorion

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<span class="mw-page-title-main">SNAI1</span> Protein

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<span class="mw-page-title-main">Nodal homolog</span> Mammalian protein found in Homo sapiens

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References

  1. ↑ Developmental Biology, 10e. Sinauer Associates, Inc. 2014. Table 5.2.
  2. ↑ Principles of development (Fifth ed.). Oxford, United Kingdom. 2015. p. 383. ISBN   978-0-19-967814-3.{{cite book}}: CS1 maint: location missing publisher (link)
  3. ↑ Warga RM, Kimmel CB (April 1990). "Cell movements during epiboly and gastrulation in zebrafish". Development. 108 (4): 569–80. doi:10.1242/dev.108.4.569. PMID   2387236.
  4. 1 2 Donald A. Kane; Karen N. McFarland; Rachel M. Warga (2005-03-01). "Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly". Development. 132 (5): 1105–16. doi: 10.1242/dev.01668 . PMID   15689372.
  5. ↑ Kimmel CB, Warga RM (November 1987). "Indeterminate cell lineage of the zebrafish embryo". Dev. Biol. 124 (1): 269–80. doi:10.1016/0012-1606(87)90478-7. PMID   3666309.
  6. ↑ C.B. Kimmel; R.M. Warga; T.F. Schilling (1990-04-01). "Origin and organization of the zebrafish fate map". Development. 108 (4): 581–94. doi:10.1242/dev.108.4.581. PMID   2387237.
  7. ↑ D'Amico LA, Cooper MS (December 2001). "Morphogenetic domains in the yolk syncytial layer of axiating zebrafish embryos". Dev. Dyn. 222 (4): 611–24. doi:10.1002/dvdy.1216. PMID   11748830. S2CID   41436032. Archived from the original on 2013-01-05.
  8. 1 2 Betchaku T, Trinkaus JP (December 1978). "Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of fundulus before and during epiboly". J. Exp. Zool. 206 (3): 381–426. doi:10.1002/jez.1402060310. PMID   568653.
  9. 1 2 L. Solnica-Krezel; W. Driever (1994-09-01). "Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly". Development. 120 (9): 2443–55. doi:10.1242/dev.120.9.2443. PMID   7956824.
  10. 1 2 Cheng JC, Miller AL, Webb SE (October 2004). "Organization and function of microfilaments during late epiboly in zebrafish embryos". Dev. Dyn. 231 (2): 313–23. doi: 10.1002/dvdy.20144 . PMID   15366008.
  11. ↑ Mathias Köppen; Beatriz García Fernández; Lara Carvalho; Antonio Jacinto; Carl-Philipp Heisenberg (2006-07-15). "Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila". Development. 133 (14): 2671–81. doi: 10.1242/dev.02439 . PMID   16794032.
  12. ↑ A. Bruce and R. Winklbauer 03-P005 Zebra fish epiboly as a model of vertebrate cell rearrangement, Mechanisms of Development 126 (2009)
  13. ↑ Siddiqui M, Sheikh H, Tran C, Bruce A (2010). "The tight junction component claudin E is required for zebra fish epiboly". Developmental Dynamics. 239 (2): 715–722. doi: 10.1002/dvdy.22172 . PMID   20014098.[ dead link ]
  14. ↑ Fukazawa C, Santiago C, Park K, Deery W, Gomez de la Torre Canny S, Holterhoff C, Wagner DS (October 2010). "poky/chuk/ikk1 is required for differentiation of the zebrafish embryonic epidermis". Developmental Biology. 346 (2): 272–83. doi:10.1016/j.ydbio.2010.07.037. PMC   2956273 . PMID   20692251.
  15. ↑ Fang Lin; Songhai Chen; Diane S. Sepich; Jennifer Ray Panizzi; Sherry G. Clendenon; James A. Marrs; Heidi E. Hamm; Solnica-Krezel, L. (2009-03-23). "Gα12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton". The Journal of Cell Biology. 184 (6): 909–21. doi:10.1083/jcb.200805148. PMC   2664974 . PMID   19307601.
  16. ↑ Slanchev K; Carney TJ; Stemmler MP; et al. (July 2009). Mullins, Mary C (ed.). "The Epithelial Cell Adhesion Molecule EpCAM Is Required for Epithelial Morphogenesis and Integrity during Zebrafish Epiboly and Skin Development". PLOS Genet. 5 (7): e1000563. doi: 10.1371/journal.pgen.1000563 . PMC   2700972 . PMID   19609345.
  17. ↑ Mungo Marsden; Douglas W. DeSimone (2001-09-15). "Regulation of cell polarity, radial intercalation and epiboly in Xenopus: novel roles for integrin and fibronectin". Development. 128 (18): 3635–47. doi:10.1242/dev.128.18.3635. PMID   11566866.
  18. ↑ M. Hammerschmidt; F. Pelegri; M.C. Mullins; D.A. Kane; M. Brand; F.J. van Eeden; M. Furutani-Seiki; Granato, M; Haffter, P (1996-12-01). "Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio". Development. 123 (1): 143–51. doi:10.1242/dev.123.1.143. PMID   9007236.
  19. ↑ Martina Nagel; Emilios Tahinci; Karen Symes; Rudolf Winklbauer (2004-06-01). "Guidance of mesoderm cell migration in the Xenopus gastrula requires PDGF signaling". Development. 131 (11): 2727–36. doi: 10.1242/dev.01141 . PMID   15128658.
  20. ↑ Oates AC; Lackmann M; Power MA; et al. (May 1999). "An early developmental role for eph-ephrin interaction during vertebrate gastrulation". Mech. Dev. 83 (1–2): 77–94. doi: 10.1016/S0925-4773(99)00036-2 . PMID   10381569.
  21. ↑ Conway G, Margoliath A, Wong-Madden S, Roberts RJ, Gilbert W (April 1997). "Jak1 kinase is required for cell migrations and anterior specification in zebrafish embryos". Proc. Natl. Acad. Sci. U.S.A. 94 (7): 3082–7. Bibcode:1997PNAS...94.3082C. doi: 10.1073/pnas.94.7.3082 . PMC   20325 . PMID   9096349.
  22. ↑ Holloway BA, Gomez de la Torre Canny S, Ye Y, Slusarski DC, Freisinger CM, Dosch R, Chou MM, Wagner DS, Mullins MC (March 2009). Barsh GS (ed.). "A Novel Role for MAPKAPK2 in Morphogenesis during Zebrafish Development". PLOS Genetics. 5 (3): e1000413. doi: 10.1371/journal.pgen.1000413 . PMC   2652113 . PMID   19282986.
  23. ↑ Solnica-Krezel L (March 2005). "Conserved patterns of cell movements during vertebrate gastrulation". Curr. Biol. 15 (6): R213–28. doi: 10.1016/j.cub.2005.03.016 . PMID   15797016.
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