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The cytoskeletal mechanics of brain morphogenesis

Cell state splitters cause primary neural induction

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“Eye of newt, and toe of frog, Wool of bat, and tongue of dog, Adder’s fork, and blind-worm’s sting, Lizard’s leg, and howlet’s wing, For a charm of powerful trouble, Like a hell-broth boil and bubble.” (W. Shakespeare,Macbeth, 1623).

Abstract

There is a functional device in embryonic ectodermal cells that we propose causes them to differentiate into either neuroepithelial or epidermal tissue during the process called primary neural induction. We call this apparatus the “cell state splitter”. Its main components are the apical microfilament ring and the coplanar apical mat of microtubules, which exert forces in opposite radial directions. We analyze the mechanical interaction between these cytoskeletal components and show that they are in anunstable mechanical equilibrium. The role of the cell state splitter is thus to create a mechanical instability corresponding to the embryonic state of “competence” in an otherwise mechanically stable cell. When the equilibrium of the cell state splitter is disturbed so as to produce a slight contraction of the apical end, apical contraction continues and the distinctive columnar neuroepithelial cells are produced. A slight expansion from the equilibrium state, on the other hand, results in flattened epidermal cells. The calculated forces are consistent with the know constitutive and force-generating properties and morphology of microfilaments and microtubules, and with free tubulin concentration. There are no free parameters in the analysis.

The first cells to assume the neuroepithelial state lie over the notochord. Propagation of the neuroepithelial state (homoiogenetic induction) then proceeds via stretch-induced constriction of the apical microfilament rings, until ahemisphere is covered, at which point the high rate of change of the meridional stress component necessary for further propagation vanishes. The remaining cells are stretched somewhat by this process and become epidermis. A sharp boundary between the tissues is thus formed (explaining “compartmentalization” and the binary nature of differentiation in general).

Normal induction apparently involves setup of the cell state splitters in all of the ectoderm cells, perhaps synchronously timed by global embryo tension. The initial transition of cells from the ectodermal to the neuroepithelial state begins at the notoplate, where cell attachments to the notochord may both cause basal actin deposition and significantly reduce the stress induced in the ectoderm by the global tension, biasing the notoplate cell state splitters toward the neuroepithelial state. Introduction of an organizer or other solid substrate (artificial inducer) elsewhere, to which ectodermal cells can adhere, may likewise have both of these effects.

Differentiation to either epidermis or neuroepithelium is thus a machanical eventfollowed by the synthesis of specific proteins. This model of differentiation suggests that the genome responds to, rather than directly causes, differentiation.

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Abbreviations

MAP:

microtubule associated protein

mRNA:

messenger ribonucleic acid

MTOC:

microtubule organizing centre

N-CAM:

neural cell adhesion molecule

RNA:

ribonucleic acid

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  1. Department of Botany and Radiology, University of Manitoba, R3T 2N2, Winnipeg, Canada

    Richard Gordon

  2. Department of Civil Engineering, University of Waterloo, N2L 3G1, Waterloo, Canada

    G. Wayne Brodland

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Dedication for Festschrift Issue Dedicated with affection and deep respect to Terrell L. Hill on his 70th birthday, and to his namesake, Leland Terrell Gordon, on the joyous occasion of his Bar Mitzvah.

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Gordon, R., Brodland, G.W. The cytoskeletal mechanics of brain morphogenesis. Cell Biophysics 11, 177–238 (1987). https://doi.org/10.1007/BF02797122

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