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Model and movement: studying cell movement in early morphogenesis, 1900 to the present

Abstract

Morphogenesis is one of the fundamental processes of developing life. Gastrulation, especially, marks a period of major translocations and bustling rearrangements of cells that give rise to the three germ layers. It was also one of the earliest fields in biology where cell movement and behaviour in living specimens were investigated. This article examines scientific attempts to understand gastrulation from the point of view of cells in motion. It argues that the study of morphogenesis in the twentieth century faced a major dilemma, both epistemological and pictorial: representing form and understanding movement are mutually exclusive, as are understanding form and representing movement. The article follows various ways of modelling, imaging, and simulating gastrular processes, from the early twentieth century to present-day systems biology. The first section examines the tactile modelling of shape changes, the second cell cinematography, mainly the pioneering work of the German embryologists Friedrich Kopsch and Ernst Ludwig Gräper in the 1920s but also a series of classic, yet not widely known, studies of the 1960s. The third section deals with the changes that computer simulation and live-cell imaging introduced to the modelling of shape change and the study of cell movement at the turn of the twenty-first century. Although live-cell imaging promises to experiment upon and represent the living body simultaneously, I argue that the new visuals are an obstacle rather than a solution to the puzzle of understanding cell motion.

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Notes

  1. 1.

    Landecker and Kelty first elaborated on the “helix of the perceptible and the intelligible” in studying the animated organism in biology in a paper that still serves as a point of reference (Landecker and Kelty 2004, p. 33). Landecker also argued that live-cell imaging started out in the 1990s as a program in genetics to see the “genetic code unfolding itself” on the screen, but after 2000 surpassed and abandoned the gene, turning instead into the animation of biochemical knowledge (Landecker 2012, pp. 379, 390).

  2. 2.

    Unless otherwise noted, all translations from German are mine.

  3. 3.

    More precisely, the model consists of 20 hoops or circles altogether, six at the upper pole made of shorter slats 18 cm in length, followed on each side by two made from longer slats of 20 cm, three of 22 cm, and finally closing the ring with four circles made of 24 cm slats (Rhumbler 1902, p. 404).

  4. 4.

    During his long scientific career in embryology, Warren H. Lewis also used cinematography for his research, starting in 1929 at the Carnegie Institution of Washington (Landecker 2004). For this late study of invagination, Lewis teamed up with the physics department at the Wistar Institute in Philadelphia, his home institution at the time. Along with Rhumbler’s, his model continues to be a reference to this day (Davidson et al. 1995).

  5. 5.

    In amphibians, gastrulation starts in the marginal zone, an area surrounding the equator of the blastula, where the animal and the vegetal hemispheres meet. It begins with the invagination of the epithelial sheet inward to form the dorsal lip of the blastopore. Amphibian gastrulation varies across different species. For a detailed account, see Beetschen (2001).

  6. 6.

    The unequal size of the cells in the two hemispheres of the egg are the result of unequally rapid cell divisions at the animal and the vegetal pole (Kopsch 1895b, p. 22).

  7. 7.

    The invaginating cells change their shape and are called bottle cells due to their elongated shape. These invaginating bottle cells initiate the formation of the archenteron (primitive gut).

  8. 8.

    Today, the process Kopsch describes is known as involution. Involution describes the rolling inward of the epithelial sheet, forming an underlying layer: when the migrating cells reach the dorsal lip of the blastopore, they turn inward and travel along the inner surface of the outer animal hemisphere cells. At the dorsal lip, therefore, cells are constantly moving and new cells are entering the embryo. In the process, the blastopore lip expands, widens, and forms a circle, closed by a yolk plug which is eventually internalized as well. These movements bring the endodermal cells into the interior of the embryo; the ectoderm has encircled the surface and the mesoderm has been brought between the two layers (see Gilbert 2014).

  9. 9.

    He first showed his films at a 1926 meeting of the Anatomische Gesellschaft in Frankfurt. Kopsch applied the uncommon practice of exposing his films for almost the entire period of filming (Kopsch 1930, p. 245).

  10. 10.

    On stereocinematography, see Liesegang (1926, pp. 106–109, 1920, pp. 190–211). On Gräper’s stereocinematographic investigation, see Liesegang (1920, p. 288); Michaelis (1955, pp. 31–32, 58, 116). Gräper himself gives a detailed account (Gräper 1928b).

  11. 11.

    Gräper points out the same countercurrent movement in amphibians (Gräper 1929b, pp. 399–400).

  12. 12.

    More research remains to be done in this field. Beetschen holds that Kopsch’s findings, which ought to have changed the course of research, failed to convince his contemporaries (Beetschen 2001, p. 781). Kopsch and Gräper, on the other hand, were both devoted teachers, though we know little of their many students and their careers. Involvement with National Socialism may also be a reason why there has been little research on Gräper: he seems to have been a member of Stahlhelm and the SA, and from 1932 to 1938 the Jena Anatomical Institute was headed by a member of the Nazi Party and SS, Hans Böker (1886–1939), see Hoßfeld et al. (2003). Three of Gräper’s films were commissioned in 1936 and 1937 by the Reich Office for Educational Film, which was created in 1934.

  13. 13.

    Research on the scientific use of film in the period around 1900 far exceeds research on the period after World War II. On early film, see Curtis (2015), Gaycken (2015), Ostherr (2012), Wellmann (2011), in the context of cell culture Landecker (2007). On the pioneer Warren Lewis, see Landecker (2004), on Ronald Canti, Foxon (1976), on Julius Ries, Wellmann (2017), on Jean Comandon, De Pastre and Lefebvre (2012). On the technological advances in cinematographic research in biology after World War II, see Michaelis (1955, pp. 47–57, ch. 3); on Michael Abercrombie and the Strangeway Laboratories, Stramer and Dunn (2015); Landecker (2011).

  14. 14.

    http://thenode.biologists.com/forgotten-classics-principles-morphogenesis/research/, Accessed March 5, 2018.

  15. 15.

    For the mathematical formulation of the simulation, see Odell (1981, pp. 459–461).

  16. 16.

    The five hypotheses are (1) apical constriction of vegetal plate cells, (2) cell tractoring of cells lateral to the vegetal plate, (3) contraction of a cycoskeletal bundle, (4) apicobasally aligned contraction of the cell cortex within the vegetal plate (this contraction is a mechanical effect of the adhesion hypothesis put forward by Gustafson and Wolpert and was modelled instead of the adhesion hypothesis itself), (5) swelling of a polyelectrolyte gel secreted by vegetal plate cells (Davidson et al. 1995, pp. 2005–2006).

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Acknowledgements

Generous support by the Radcliffe Institute for Advanced Study at Harvard University during the academic year 2017/2018 and the DFG-Kollegforschergruppe “Medienkulturen der Computersimulation” made research on this topic possible. I am grateful to my colleagues and the anonymous reviewers for their invaluable comments and critique.

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Wellmann, J. Model and movement: studying cell movement in early morphogenesis, 1900 to the present. HPLS 40, 59 (2018). https://doi.org/10.1007/s40656-018-0223-0

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Keywords

  • Cell motion
  • Cinematography
  • Embryology
  • Gastrulation
  • Live-cell imaging
  • Simulation