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Cell sociology and the problem of automation in the development of pluricellular animals

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Abstract

The principles of automation (automatism and programming) in the unfolding of spatio-temporal patterns during animal development are deduced from experimental data reconsidered from the point of view of cell sociology. The developmental programme in the egg is not part of the genetic information but a part of the cytoplasmic information. Throughout development cells store extra-cellular information released by their neighbours in the form of cytoplasmic information. Successive determinations cannot be considered as successive reprogrammings of cells: each one consists of a selection of one specific programme from the total information previously stored. This programme specifies cell interactions in the determined population as a whole; it is very imprecise and is progressively completed during the course of further differentiation by information released by neighbouring cell populations. Complicated patterns may emerge from only two homogeneous populations involved in distinct differentiation pathways and confronting each other. Consequently the ‘egg developmental programme’ provides gene effectors and specific physico-chemical conditions necessary for the starting of at least two distinct differentation pathways. Experimental data suggest that there are two components in this programme. One is a molecular machinery which starts at fertilization in the whole cytoplasm. It yields two programmes of differentiation, typically first an endodermal and then an ectodermal one. The other component of the egg developmental programme, which does not require specific information, allows the interception of the first (endodermal) programme. The application of informatics to developmental automatism is discussed in the latter part of the paper.

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References

  • Apter, M.J. (1966). Cybernetics and development. - Oxford, Pergamon Press, 188 pp.

    Google Scholar 

  • Apter, M.J. & L. Wolpert (1965). Cybernetics and development. - J. Theor. Biol. 8, p. 244–257.

    Google Scholar 

  • Arbib, M.A. (1972). Automata theory in the context of theoretical embryology. - In: R. Rosen, Ed., Foundations of mathematical biology. Vol. 2: Cellular systems, p. 141–215. - New York & London, Academic Press.

    Google Scholar 

  • Ashby, W.R. (1958) Requisite variety and its implication for the control of complex systems. - Cybernetica 1, p. 83–99.

    Google Scholar 

  • Atlan, H. (1972). L'organisation biologique et la théorie de l'information. (Actualités scientifiques et industrielles). - Paris, Hermann, 300 pp.

    Google Scholar 

  • Auerbach, R. (1960). The organization and reorganization of embryonic cells. - In: Self-organizing systems, p. 101–107. - Oxford, Pergamon Press.

    Google Scholar 

  • Beermann, W. (1966). Differentiation at the level of the chromosomes. - In: Cell differentiation and morphogenesis, International Lecture Course, Wageningen, p. 24–54. - Amsterdam, North-Holland Publishing Comp.

    Google Scholar 

  • Boon-Niermeijer, E.K. (1975). The effect of puromycin on the early cleavage cycles and morphogenesis of the Pond Snail Lymnaea stagnalis. - Roux Arch. EntwMech. Organ. 177, p. 20–40.

    Google Scholar 

  • Brachet, J. (1960). The biochemistry of development. - In: International Series of Monographs in pure and applied Biology. Vol.2. - London, Pergamon Press, 320 pp.

    Google Scholar 

  • Brandhorst, B.P. (1976). Two-dimensional gel patterns of protein synthesis before and after fertilization of sea-urchin eggs. - Dev. Biol. 52, p. 310–317.

    Google Scholar 

  • Brien, P. (1968). Blastogenesis and morphogenesis. - Adv. Morphogenesis 7, p. 151–203.

    Google Scholar 

  • Brien, P. (1974). Propos d'un zoologiste: Le vivant: épigenèse, évolution épigénétique. - Bruxelles, Editions Universitaires, 155 pp.

    Google Scholar 

  • Chandebois, R. (1976a). Cell sociology: a way of reconsidering the current concepts of morphogenesis. - Acta biotheor., Leiden 25 p. 71–102.

    Google Scholar 

  • Chandebois, R. (1976b). Morphogénétique des animaux pluricellulaires. - Paris, Maloine Ed., 461 pp.

    Google Scholar 

  • Chandebois, R. (1977). Cell sociology and the problem of position effect: pattern formation, origin and role of gradients. - Acta biotheor., Leiden 26, p. 203–238.

    Google Scholar 

  • Counce, S.J. (1973). The causal analysis of insect embryogenesis. - In: S.J. Counce & C.H. Waddington, Ed., Developmental systems: Insects, 2, p. 1–156. - London, Academic Press.

    Google Scholar 

  • Counce, S.J. & D.A. Ede (1957). The effect on embryogenesis of a sex-linked femalesterility factor in Drosophila melanogaster. - J. Embryol. exp. Morph. 5, p.404–421.

    Google Scholar 

  • Czihak, G. (1965). Evidences for inductive properties of the micromeres RNA in seaurchin embryos. - Naturwissenschaften 52, p. 141–142.

    Google Scholar 

  • Czihak, G. (1977). Kinetics of RNA synthesis in the 16-cell stage of the sea-urchin Paracentrotus lividus. - Roux Arch. EntwMech. Organ. 182, p. 59–68.

    Google Scholar 

  • Dalcq, A.M. (1961). A comparison of the various types of egg organization. - Symp. Germ cells and Development, p. 704–713.

  • Dan, K. (1972). Modified cleavage pattern after suppression of one mitotic division. - Exp. Cell Res. 72, p. 69–73.

    Google Scholar 

  • Dettlaff, T.A. (1964). Cell divisions, duration of interkinetic states of differentiation in early stages of embryonic development. - Adv. Morph. 3, p. 323–362.

    Google Scholar 

  • Devriès, J. (1973a). Détermination précoce du dévelopment embryonnaire chez le lombricien Eisenia foetida. - Bull. Soc. Zool. Fr. 98, p. 405–417.

    Google Scholar 

  • Devriès, J. (1973b). Aspect du déterminisme embryonnaire au cours des premiers stades de la segmentation chez le lombricien Eisenia foetida. - Ann. Embryol. Morph. 6, p. 95–108.

    Google Scholar 

  • Devriès, J. (1976). Activité génétique au cours de l'embryogenèse de l'oligochète Eisenia foetida (Autoradiographie à l'uracile 3H et traitement à l'actinomycine D). - J. Embrvol. exp. Moroh. 35. p. 403–424.

    Google Scholar 

  • Ebert, J.D. & M.E. Kaighn (1966). Keys to change factors regulating differentiation. - in: M. Locke, ed., Major problems in developmental Biology, p. 20–84. - New York and London, Academic Press.

    Google Scholar 

  • Ede, D. (1971). Control of form and pattern in the vertebrate limb. - Symp. Soc. exp. Biol. 25 (Control mechanisms of growth and differentiation), p. 235–254.

    Google Scholar 

  • Elsdale, T. & Jones K. (1963). The independence and interdependence of cells in the amphibian embryo. - Symp. Soc. exp. Biol. 17, p. 257–272.

    Google Scholar 

  • Freeman, G. (1976). The role of cleavage in the localization of developmental potential in the ctenophore Mniemiopsis leidvi. - Develop. Biol. 49, p. 143–177.

    Google Scholar 

  • Graham, C.F. & S.J. Kelly (1977). Interactions between embryonic cells during early development of the mouse. - In: L. Saxen & L. Weiss, Ed., Cell interactions in differentiation; 6th Sigrid Juselius Found. Symp. Helsinki; August 1976, pp. 45–57. - London, Academic Press.

    Google Scholar 

  • Guerrier, P. (1970a). Les caractères de la segmentation et la détermination de la polarité dorsoventrale dans le développement de quelques Spiralia. I. Les formes à premier clivage ál. - J. Embryol. exp. Morph. 23, p. 611–637.

    Google Scholar 

  • Guerrier, P. (1970b). Les caractères de la segmentation et la détermination de la polarité dorsoventrale dans le développement de quelques Spiralia. II. Sabellaria alveolata (Anníde polychè). - J. Embryol. exp. Morph. 23, p. 639–665.

    Google Scholar 

  • Guerrier, P. (1970c). Les caractères de la segmentation et la détermination de la polarité dorsoventrale dans le développement de quelques Spiralia. III. Pholas dactylus et Spisula subtruncata (Mollusques Lamellibranches). - J. Embryol. exp. Morph. 23, p. 667–692.

    Google Scholar 

  • Gustafson, T. (1965). Morphogenetic significance and biochemical patterns in sea-urchin embryo. - R. Weber, ed., The biochemistry of animal development, I, p. 140–202. - New York, Academic Press.

    Google Scholar 

  • Hara, K. (1977). The cleavage pattern of the Axolotl egg studied by cinematography and cell counting. - Roux Arch. EntwMech. Organ. 181, p. 73–87.

    Google Scholar 

  • Hörstadius, S. (1935). Ueber die Determination im Verlaufe der Eiachse bei Seeigeln. - Publ. Staz. Zool. Napoli, 14, p. 251–279.

    Google Scholar 

  • Hörstadius, S., J.I. Lorch & J.F. Danielli (1953). The effect of enucleation on the development of sea-urchin eggs. II. Enucleation of animal and vegetal halves. - Exp. Cell Res. 4, p. 263–274.

    Google Scholar 

  • Lallier, R. (1964). Biochemical aspects of animalization and vegetalization in the seaurchin embryo. - Adv. Morphogenesis 3, p. 147–196.

    Google Scholar 

  • Lash, J.W. (1963). Tissue interaction and specific metabolic responses: chondrogenic induction and differentiation. - In: M. Locke, ed., Cytodifferentiation and macromolecular synthesis, p. 253–260. - New York and London, Academic Press.

    Google Scholar 

  • Lehmann, F.E. (1958). Phases of dependent and autonomous morphogenesis in the so-called mosaic-egg of Tubifex. In: W.D. McElroy & B. Glass, ed., A symposium on the chemical basis of development, p. 73–84. - Baltimore, Johns Hopkins Press.

    Google Scholar 

  • Levak-Svajger, B. & A. Svajger (1970). Differentiation in homografts of isolated germ layers of the rat embryo. - Arch. Sci. Biol. 22, p. 25–32.

    Google Scholar 

  • Lopashov, G.V. & O.G. Stroeva (1964). Development of the eye. Experimental studies. (Transl. from Russian). - Jerusalem, Israel Programme for Scientific Translations.

    Google Scholar 

  • Mc Carthy (1966). Information. - In: Information. A Scientific American book, p. 1–16, - San Francisco, London, W.H. Freeman.

    Google Scholar 

  • Martin, G.R. (1975). Teratocarcinoma as model system for the study of embryogenesis and neoplasia. A review. - Cell 5 p. 229–236.

    Google Scholar 

  • Morgan, T.H. (1934). Embryology and genetics. - New York, Columbia Univ. Press. 238 pp.

    Google Scholar 

  • Nieuwkoop, P.D. (1969). The formation of the mesodern in urodelean amphibians. I. The induction by the endoderm. - Roux Arch. EntwMech. Organ. 162, p. 341–373.

    Google Scholar 

  • Nieuwkoop, P.D. (1977). Origin and establishment of embryonic polar axes in amphibian development. - In: Current topics in developmental Biology 11, p. 115–132. - New York, San Francisco, London, Acad. Press.

    Google Scholar 

  • Ortolani, G. (1958). Cleavage and development of egg fragments in ascidians. - Acta Embryol. Morphol. exp. 1, p. 247–272.

    Google Scholar 

  • Parisi, E., S. Filosa, B. De Petrocellis & A. Monroy (1978). The pattern of cell division in the early development of the sea-urchin Paracentrotus lividus. - Dev. Biol. 65, p. 38–49.

    Google Scholar 

  • Pasteels, J. (1934). Recherches sur le morphogenèse et le dérminisme des segmentations ináles chez les Spiralia. - Arch. Anat. mocro. 30, p. 161–197.

    Google Scholar 

  • Pasteels, J. (1938). Recherches sur les facteurs initiaux de la morphogenèse chez les amphibiens anoures. - Arch. Biol. 49, p. 629–667.

    Google Scholar 

  • Pasteels J. (1964). The morphogenetic role of the cortex of the amphibian egg. - Adv. Morphogenesis 3, p. 363–388.

    Google Scholar 

  • Raven, C.P. (1961). Oogenesis: The storage of developmental information. (International Series of Monographs on pure and applied Biology, vol. 10). - Oxford, London, New York & Paris, Pergamon Press, viii+ 274 pp.

    Google Scholar 

  • Reverberi, G. (1961). The embryology of ascidians. - Adv. Morphogenesis 1, p. 55–101.

    Google Scholar 

  • Reverberi, G. (1968). La mánique du développement de l'oeuf des Ascidies. - Année biol. 7, p. 557–576.

    Google Scholar 

  • Reverberi, G. (1970). The ultrastructure of the ripe oocyte of Dentalium. - Acta Embryol. exp. 3, p. 225–279.

    Google Scholar 

  • Reverberi, G. & A. Minganti (1946). Fenomeni di evocazione nelle sviluppo dell'uovo di Ascidie. - Publ. Staz. Zool. Napoli 20, p. 199–252.

    Google Scholar 

  • Rossant, J. (1975). Investigation of the determinative state of the mouse inner cell masses transferred to the oviduct. - J. Embryol. exp. Morph. 33, p. 991–1001.

    Google Scholar 

  • Sala, M. (1955). Distribution of activating and transforming influences in the archenteron roof during the induction of the nervous system in amphibians. - Proc. Acad. Sci. Amst. Ser.C 58, p. 635–647.

    Google Scholar 

  • Saxen, L.O. Koskimies, A. Lahtii, H. Miettinin, J. Rapola & J. Wartiovaara (1968). Differentiation of kidney mesenchyme in an experimental model system. - Adv. Morphogenesis 7, p. 251–294.

    Google Scholar 

  • Smith, L.D. & R.E. Ecker (1970). Regulatory processes in the maturation and early cleavage of amphibian eggs. - In: A.A. Moscona & A. Monroy, ed., Current Topics in Developmental Biology, p. 1–38. - New York, Academic Press.

    Google Scholar 

  • Stevens, L.C. (1967). The biology of teratomas. - Adv. Morphogenesis 6, p. 1–31.

    Google Scholar 

  • Waddington, C.H. (1940). Organizers and genes. - Cambridge, Cambridge University Press, 160 pp.

    Google Scholar 

  • Waddington, C.H. (1956). Principles of embryology. - New York, Macmillan, 510 pp.

    Google Scholar 

  • Waddington, C.H. (1966). Fields and gradients. - In: M. Locke, ed., Major problems in developmental biology, p. 105–124. - New York, Academic Press.

    Google Scholar 

  • Wolpert, L. (1969). Positional information and the spatial pattern of cell differentiation. - J. theor. Biol. 25, p. 1–47.

    Google Scholar 

  • Yamada, T. (1967). Cellular synthetic activities in induction of tissue transformation. - In: A.V.S. De Reuck and J. Krugel, eds., Cell differentiation, CIBA Fnd. Symp., p. 116–130. - Boston, Little, Brown and Comp.

    Google Scholar 

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Chandebois, R. Cell sociology and the problem of automation in the development of pluricellular animals. Acta Biotheor 29, 1–35 (1980). https://doi.org/10.1007/BF00045880

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