Embryonic differentiation waves

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Schematic of cell state splitter organelle Schematic of Cell State Splitter Organelle.jpg
Schematic of cell state splitter organelle
How embryonic differentiation waves create gradients How Embryonic Differentiation Waves Create Gradients.jpg
How embryonic differentiation waves create gradients
Differentiation tree of the Axolotl Differentiation Tree of the Axolotl.jpg
Differentiation tree of the Axolotl
Signal transduction model for embryonic differentiation waves Signal Transduction Model for Embryonic Differentiation Waves.png
Signal transduction model for embryonic differentiation waves

A mechanochemical based model for primary neural induction was first proposed in 1985 by Brodland and Gordon. [1] They proposed that there is a mechanically sensitive bistable organelle made of microtubules and microfilaments in the apical ends of cells within cell sheets that are about to differentiate (that are competent) and these cells are under mechanical tension. The microtubules and microfilaments are in mechanical opposition in a proposed embryonic organelle they called the cell state splitter. Depending on where the cell is within a sheet, the tension will be resolved by either the apical end contracting or the apical end expanding. The resolution will begin at one point and spread over the rest of the tissue limited by other mechanical forces at boundaries. An actual physical wave of contraction has been found which traverses the presumptive neural epithelium of the developing salamander, the axolotl (Ambystoma mexicanum). The contraction wave's trajectory was more complex than predicted in the original model however it did originate from the precise location of the Spemann organizer and traversed only the presumptive neural epithelium. [2] Electron microscopy showed intermediate filaments are also present in the cell state splitter. [3] Additional waves of both contraction and expansion were also discovered by time lapse photography of axolotl gastrulation. Among them was a wave of expansion that occurs in ectoderm only in the presumptive epithelium. When the trajectories of the waves were superimposed on the fate map of the axolotl it was shown that there is a unique combination of expansion and contraction waves that correlates with the tissue types determined during gastrulation and that this set of wave trajectories could explain the shape of the fate map. [4]

A biochemical basis for the signal transduction from the cytoskeleton to the nucleus resulting in changes in gene expression was first proposed by Björklund (now Gordon) and Gordon in 1993 [5] This would result in a biochemical transduction of the biomechanical signal from the cytoskeleton that is thereby passed on to the nucleus. This then signals the changes in gene expression. If the cell has experienced contraction, one signal is sent and if the cell has experienced expansion then another signal is sent. The signal from the cytoskeleton is what causes determination of cell fate. The phenomena of gene gradients during development is dismissed as an epiphenomena resulting from the passage of the biomechanical wave initiating changes in gene expression in individual cells as the wave passes through a cell sheet. [6] They have outlined their research and their theory of differentiation waves in detail in their book Embryogenesis Explained. For example, the first differentiation that takes place during mammalian compaction is explained in terms of their differentiation waves model thus; Cells on the outside of the morula expand due to the effect of their position on the outside of the early ball of cells and they become determined to be trophoblast. Cells on the inside of the ball contract instead due to the mechanical force of being on the inside and they become determined to be the inner cell mass. All the other activity, such as changes in gene expression, signalling proteins, release of morphogens, and epigenetic changes, are considered the result of differentiation after the response of the cytoskeleton to mechanical signals which then determines cell fate using purely mechanical signals. [7] [8] Failure of neural tube closure is explained as a failure of methylation of cytoskeleton of developing neural tissue for those neural tube defects which are folate sensitive and prevented by folic acid supplementation. [9]

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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.

Mesoderm Middle germ layer that forms muscle, bone, blood vessels and more

In all bilaterian animals, the mesoderm is one of the three primary germ layers in the very early embryo. The other two layers are the ectoderm and endoderm, with the mesoderm as the middle layer between them.

Gastrulation Stage in embryonic development in which germ layers form

In developmental biology, gastrulation is a phase early in the embryonic development of most animals, during which the blastula is reorganized into a multilayered structure 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.

Axolotl Species of salamander amphibian

The axolotl, Ambystoma mexicanum, also known as the Mexican walking fish, is a neotenic salamander related to the tiger salamander. Although colloquially known as a "walking fish", the axolotl is not a fish but an amphibian. The species was originally found in several lakes, such as Lake Xochimilco underlying Mexico City. Axolotls are unusual among amphibians in that they reach adulthood without undergoing metamorphosis. Instead of developing lungs and taking to the land, adults remain aquatic and gilled.

Ectoderm Outside germ layer that forms the brain, spinal cord, epidermis and more

The ectoderm is the most exterior of the three primary germ layers formed in the very early embryo. The other two layers are 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."

Neurulation Embryological process forming the neural tube

Neurulation refers to the folding process in vertebrate embryos, which includes the transformation of the neural plate into the neural tube. The embryo at this stage is termed the neurula.

Organogenesis is the phase of embryonic development that starts at the end of gastrulation and continues until birth. During organogenesis, the three germ layers formed from gastrulation form the internal organs of the organism.

The Wnt signaling pathways are a group of signal transduction pathways which begin with proteins that pass signals into a cell through cell surface receptors. The name Wnt is a portmanteau created from the names Wingless and Int-1. Wnt signaling pathways use either nearby cell-cell communication (paracrine) or same-cell communication (autocrine). They are highly evolutionarily conserved in animals, which means they are similar across animal species from fruit flies to humans.

Neurula

A neurula is a vertebrate embryo at the early stage of development in which neurulation occurs. The neurula stage is preceded by the gastrula stage; consequentially, neurulation is preceded by gastrulation. Neurulation marks the beginning of the process of organogenesis.

Neural crest Embyronic group of cells giving rise to diverse cell lineages

Neural crest cells are a temporary group of cells unique to vertebrates that arise from the embryonic ectoderm germ layer, and in turn give rise to a diverse cell lineage—including melanocytes, craniofacial cartilage and bone, smooth muscle, peripheral and enteric neurons and glia.

The primitive node is the organizer for gastrulation in the vertebrate embryo. The organizer is determined by the Nieuwkoop center in amphibians or the Posterior Marginal zone in amniotes.

Mesenchyme Type of connective tissue found mostly during the embryonic development of bilateral triploblast animals

Mesenchyme is a type of connective tissue found mostly during the embryonic development of bilateral triploblast animals.

Eye development Formation of the eye during embryonic development

Eye formation in the human embryo begins at approximately three weeks into embryonic development and continues through the tenth week. Cells from both the mesodermal and the ectodermal tissues contribute to the formation of the eye. Specifically, the eye is derived from the neuroepithelium, surface ectoderm, and the extracellular mesenchyme which consists of both the neural crest and mesoderm.

In the field of developmental biology, regional differentiation is the process by which different areas are identified in the development of the early embryo. The process by which the cells become specified differs between organisms.

Fish development

The development of fishes is unique in some specific aspects compared to the development of other animals.

French flag model Biological model

The French flag model is a conceptual definition of a morphogen, described by Lewis Wolpert in the 1960s. A morphogen is defined as a signaling molecule that acts directly on cells to produce specific cellular responses dependent on morphogen concentration. During early development, morphogen gradients generate different cell types in distinct spatial order. French flag patterning is often found in combination with others: vertebrate limb development is one of the many phenotypes exhibiting Turing overlapped with a complementary pattern.

Ectoderm specification

In Xenopus laevis, the specification of the three germ layers occurs at the blastula stage. Great efforts have been made to determine the factors that specify the endoderm and mesoderm. On the other hand, only a few examples of genes that are required for ectoderm specification have been described in the last decade. The first molecule identified to be required for the specification of ectoderm was the ubiquitin ligase Ectodermin ; later, it was found that the deubiquitinating enzyme, FAM/USP9x, is able to overcome the effects of ubiquitination made by Ectodermin in Smad4. Two transcription factors have been proposed to control gene expression of ectodermal specific genes: POU91/Oct3/4 and FoxIe1/Xema. A new factor specific for the ectoderm, XFDL156, has shown to be essential for suppression of mesoderm differentiation from pluripotent cells.

Richard Gordon (theoretical biologist)

Richard (Dick) Gordon is an American theoretical biologist. He was born in Brooklyn, New York, the eldest son of Jack Gordon, a salesman and American handball champion, and artist Diana Gordon. He is married to retired scientist Natalie K Björklund with whom he cowrote his second book and several academic publications. He has three sons, Leland, Bryson and Chason Gordon and three stepchildren Justin, Alan and Lana Hunstad. Gordon was a professor at the University of Manitoba in Winnipeg, Manitoba from 1978 to 2011. He is retired and currently volunteers as a scientist for the Gulf Specimen Marine Laboratory in Panacea, Florida where he winters, and he holds an adjunct position in the Department of Obstetrics & Gynecology, Wayne State University. Gordon lives in Alonsa, Manitoba, Canada.

The Spemann-Mangold organizer is a group of cells that are responsible for the induction of the neural tissues during development in amphibian embryos. First described in 1924 by Hans Spemann and Hilde Mangold, the introduction of the organizer provided evidence that the fate of cells can be influenced by factors from other cell populations. This discovery significantly impacted the world of developmental biology and fundamentally changed the understanding of early development.

Dorsal lip

The dorsal lip of the blastopore is a structure that forms during early embryonic development and is important for its role in organizing the germ layers. The dorsal lip is formed during early gastrulation as folding of tissue along the involuting marginal zone of the blastocoel forms an opening known as the blastopore. It is particularly important for its role in neural induction through the default model, where signaling from the dorsal lip protects a region of the epiblast from becoming epidermis, thus allowing it to develop to its default neural tissue.

References

  1. ↑ Gordon, R. Brodland, GW. The cytoskeletal mechanics of brain morphogenesis: cell state splitters cause primary neural induction. Gell Biophys. 11: 177-238. (1987)
  2. ↑ Brodland, GW” Gordon, R, Scott MJ, Bjorklund NK, Luchka KB, Martin, CC, Matuga, C., Globus, M., Vethamany-Globus S. and Shu, D. Furrowing surface contraction wave coincident with primary neural induction in amphibian embryos. J Morphol. 219: 131-142. 1994
  3. ↑ Martin, C.C. & R. Gordon. Ultrastructural analysis of the cell state splitter in ectoderm cells differentiating to neural plate and epidermis during gastrulation in embryos of the axolotl Ambystoma mexicanum. Russian J. Dev. Biol. 28(2), 71-80 1997
  4. ↑ Björklund, N.K. & R. Gordon (1994). Surface contraction and expansion waves correlated with differentiation in axolotl embryos. I. Prolegomenon and differentiation during the plunge through the blastopore, as shown by the fate map. Computers & Chemistry 18(3), 333- 345 [Appendix VI].
  5. ↑ Björklund, N.K. & R. Gordon. [Nuclear state splitting: a working model for the mechanochemical coupling of differentiation "waves" with the controlling genes (master genes)] [Russian]. Ontogenez 24(2), 5-23 1993
  6. ↑ Gordon, R., Björklund, N, Nieuwkoop, PD, International Review of Cytology, Appendix: Dialogue on Embryonic Induction and Differentiation Waves, Vol 150 1994/02/01, Pg 373-420
  7. ↑ Gordon, N. Gordon, R.Embryogenesis Explained World Scientific Publishing, Singapore, 2016
  8. ↑ Gordon, NK, Gordon R The organelle of differentiation in embryos: the cell state splitter Theor Biol Med Model (2016) 13: 11. https://doi.org/10.1186/s12976-016-0037-2
  9. ↑ Björklund NK, Gordon R A hypothesis linking low folate intake to neural tube defects due to failure of post-translation methylations of the cytoskeleton Int. J. Dev. Biol. 50: 135 - 141 2006
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