Abstract
This bibliographical review of the modelling of the mitotic apparatus covers a period of one hundred and twenty years, from the discovery of the bipolar mitotic spindle up to the present day. Without attempting to be fully comprehensive, it will describe the evolution of the main ideas that have left their mark on a century of experimental and theoretical research. Fol and Bütschli's first writings date back to 1873, at a time when Schleiden and Schwann's cell theory was rapidly gaining ground throughout Germany. Both mitosis and chromosomes were to be discovered within the space of thirty years, along with the two key events in the animal and plant reproductive cycle, namely fecondation and meiosis. The mitotic pole, a term still in use to this day, was employed to describe a morphological fact which was noted as early as 1876, namely that the lines and the dots of the karyokinetic figure, with its spindle and asters, looks remarkably like the lines of force around a bar magnet. This was to lead to models designed to explain the movements of chromosomes which take place when the cell nucleus appears to cease to exist as an organelle during mitosis. The nature of those mechanisms and the origin of the forces behind the chromosomes' ordered movements were central to the debate. Auguste Prenant, in a remarkable bibliographical synthesis published in 1910, summed up the opposing viewpoints of the ‘vitalists’, on the one hand, who favoured the theory of contractility or extensility in spindle fibres, and of those who believed in models based on physical phenomena, on the other. The latter subdivided into two groups: some, like Bütschli, Rhumbler or Leduc, referred to diffusion, osmosis and superficial tension, whilst the others, led by Gallardo and Hartog, focussed on the laws of electromagnetism. Lillie, Kuwada and Darlington followed up this line of research. The mid-20th century was a major turning point. Most of the modelling mentioned above was criticized and fell into disuse after disappearing from research publications and textbooks.
This marked the onset of a new era, as electron microscopes made possible the materialization and detailed study of the macromolecular elements of the fibres, filaments and microtubules of the cytoskeleton. The successive phases of (a) de Harven and Bernhard's 1956 discovery of the centriole's ultrastructure, (b) its identification with the basal body of the cilia and flagella, confirming the theory set out by Henneguy and von Lenhossek (1898–99), (c) the universal presence of microtubules in animal, vegetal and eukaryotic protist cells, (d) the polymerization-depolymerization induced reversible transformations of the tubulin pool in mitosing cells (Inoue, 1960), (e) ultrastructural comparative studies of the mitotic apparatus of eukaryotes illustrating the Pickett-Heaps integrating concept of the MTOC (microtubule-organizing centre), (f) the possibility ofin vitro experiments on mtocs or on microtubules, brings us upon the present day, which has seen the focus placed on the concept of motor-proteins (kinesin, dynein) and on cell cycle models. The latter are based on a close coincidence between the observable modifications of the mitotic apparatus and the periodic variations in intracellular concentrations of calcium or of certain enzymes (cyclins, Cdc2) during the main transitions of the cell cycle.
The potential role of biophysics in the construction of a unified mitosis theory is examined.
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References
Alberts, B., D. Bray, J. Lewis, M. Raff, K. Roberts and J. Watson (1983). Molecular biology of the cell. New York, London, Garland Publ.
Belar, K. (1929a). Beiträge zur Kausalanalyse der Mitose. II. Arch. Entw. 118: 359–480.
Belar, K. (1929b). Beiträge zur Kausalanalyse der Mitose. III. Z. Zellf. 10: 73–134.
Beneden E. van (1883). Recherches sur la maturation de l'oeuf et la fécondation. Ascaris megalocephala. Arch. de Biologie. 4: 266–640.
Beneden E. van, and A. Neyt (1887). Nouvelles recherches sur la fécondation et la division mitosique chez l'ascaride mégalocéphale. Bull. Acad. Roy. Belgique 3. Ser. 7.
Berkaloff, A., J. Bourguet P. and N. Favard and J. Lacroix (1981). Biologie et Physiologie Cellulaire. Coll. Méthodes, tomes 3 et 4. Paris, Hermann.
Bernhard, W. and E. de Harven (1956). Sur la présence dans certaines cellules de mammifères d'un organite de nature probablement centriolaire. Etude au microscope électronique. C. R. Acad. Sci. Paris 242: 288–290.
Bjerknes, C.A. (1902). Hydronynamische Fernkrafte. 2 vols. Leipzig, J.A. Barth.
Bjerkens, M. (1986). Physical theory of the orientation of astral mitotic spindles. Science 234: 1413–1416.
Bornens, M. (1979). The centriole as a gyroscopic oscillator. Implications for cell organisation and some other consequences. Biol. Cell. 35: 115–132.
Boveri, T. (1887–1888). Zellstudien. H.1. Die Bildung der Richtungs körper bei Ascaris megalocephala und Ascaris lumbricoïdes. H2. Die Befruchtung und Teilung des Eies von Ascaris megalocephala. Jenaische Zeit schr. f. Naturw.XXI., XXII.
Boveri, T. (1895–1896). Also references cited by Prenant (1910).
Bobretzky, N. (1876). Studien über die embryonale Entwickelung der Gasteropoden. Arch. f. mikr. Anat. XIII 1re livr. Juillet.
Bütschli, O. (1874). Beiträge zur Kenntniss der freilebenden Nematoden. Nova Acta Leop. Carol. Bd 36.
Bütschli, O. (1892). Über die künstlich Nachahmung der karyokinetischen Figur. Verh. Medizin Nat. Ver, in Heidelberg, V.
Bütschli, O. (1892–1901). Also references cited by Prenant (1910).
Darlington, C.D. (1965) Cytology. Part IA Reprint of “Recent advances in cytology”, 2nd ed. (1937). Part II “Recent advances in cytology” 1937–1964; London, J. et A. Churchill.
Drüner (1894). Zur Morphologie der Centralspindel. Jenaische. Zeitschr. f. Naturw. XXVIII (N.F.XXI).
Drüner (1895). Studien über den Mechanismus der Zelltheilung. Jenaische Zeitschr. f. Naturw. XXIX (N.F.XXII).
Fawcett, D.W. and K.R. Porter (1954). A study of the fine structure of ciliated epithelia. J. Morphol. 94: 221–281.
Flemming, W. (1874). Über den ersten Entwicklungserscheinungen am der Teichmuschel., II. 125 Pl.II.
Flemming, W. (1882). Zellsubstanz, Kern und Zelltheilung. Leipzig.
Fisher (1899). Fixirung, Förbung und Bau des Protoplasmas. Jena.
Fol. H. (1873). Die erste Entwickelung des Geryonideneis. Jenaische Zeitschr. f. Naturw.: 471–492.
Fol, H. (1976) Sur les phénomènes intimes de la division cellulaire. Comptes Rendus Hebd. Acad. Sci. Paris 83: 667–669.
Fol, H. (1976) Sur les phénomènes intimes de la fécondation. Comptes Rendus Hebd. Acad. Sci. Paris 84: 268–273.
Fol, H. (1879). Recherches sur la fécondation et le commencement de l'hénogénie chez divers animaux. Mém. Soc. de Physique et d'Histoire Naturelle de Genève. 26.
Fuge, H. (1977) Ultrastructure of the mitotic spindle. Int. Rev. Cytol. Suppl. 6: 1–52
Fuller, M.S. (1976). Mitosis in Fungi. Int. Rev. Cytol. 45: 113–153.
Gallardo, A. (1896). Essai d'interprétation des figures karyocinétiques. Anal. Mus. Nac. Buenos Aires 5: 11–22.
Giudice E. del, S. Doglia and M. Milani (1982). Self focusing of Fröhlich waves and cytoskeleton dynamics. Physics Letters 90A, 1–2: 104–106.
Goldbeter, A. (1991) A minimal cascade model for the mitotic oscillator involving cyclin and cdc2 kinase. Proc. Natl. Acad. Sci. USA 88: 9107–9111.
Goldbeter, A., G. Dupont and M. Berridge (1990) Minimal model for signal-induced Ca++ oscillations and for their frequency encoding through protein phosphorylation. Proc. Natl. Acad. Sci. USA 87: 1461–1465.
Goodwin, B.C. and L.E.H. Trainor (1980). A field description of the cleavage process in embryogenesis. J. Theor. Biol. 86: 757–790.
Gorsky, G.J. (1992). Chromosome motion in mitosis. BioEssays 14: 73–80.
Guyader, H. Le (1988) Théories et histoire en Biologie. Publ. Institut Interdisciplinaire d'Etudes Epistémologiques. Lyon.
Hartog, M. (1902). Dynamic interpretation of cell-division. Nature LXVII.
Hartog, M. (1904). Des chaines de forces et d'un nouveau modèle magnétique des mitoses cellulaires. C. R. Acad. Sci. Paris CXXXVIII.
Hartog, M. (1905). The dual force of the dividing cell. Part I. The achromatic spindle figure illustrated by magnetic chains of force. Proc. Roy. Soc. SB. 76.
Hartog, M. (1907). The dual force of the dividing cell. Science Progress II.
Harven E. de, and W. Bernhard (1956) Etude au microscope électronique de l'ultrastructure du centriole chez les vertébrés. Z Zellforsch. mikr. Anat. 45: 378–398.
Heath, I.B. (1980) Variant mitosis in lower eukaryotes: indicators of the evolution of mitosis? Int. Rev. Cytol. 32: 93–137
Heidenhain, M. (1894). Neue Untersuchungen über die Centralkörper und ihre Beziehungen zum Kern und Zellenprotoplasma. Arch. f. mikr. Anat. XLIII.
Heidenhain, M. (1894). Cytomechanische Studien. Arch. Entwickl. Mech. I.
Heidenhain, M. (1896). Ein Neues, Modell zum Spannungsgesetz der centrierten Systeme. Verh. d. Anat. Ges.
Henneguy, L.F. (1898) Sur les rapports des cils vibratiles avec les centrosomes. Arch. Anat Microscop. Morph. Expl. 1: 481–496.
Hertwig, O. (1875). Beiträge zur Kenntniss der Bildung, Befruchtung und Theilung des thierischen. Eies. 1ere partie Morphol. Jahrb. Bd. I.
Hertwig, O. (1877). Beiträge zur Kenntniss der Bildung, Befruchtung und Theilung des thierischen. Eies. 2eme partie Morphol.Jahr Bd II. 3eme partie Morphol. Jahr Bd IV.
Inoué, S. (1960) On the physical properties of the mitotic spindle. Ann. N. Y. Acad. Sci. 90: 529–530.
Inoué, S. and H. Sato. (1967) Cell motility by labile association of molecules. The nature of the mitotic spindle fibers and their role in chromosome movement. J. Gen. Physiol 50: 259–292.
Klebs (1874). Über die Regeneration des Plattenepithels. Arch. f. Experim. Pathol. u. Pharmacol.; I 125 Pl. II.
Kubai, D.F. (1975) The evolution of the mitotic spindle.. Int. Rev Cytol. 43: 167–227.
Kuryama, R. and C. Nislow (1992) Molecular components of the mitotic spindle. BioEssays 4: 81–88
Kuwada, Y. (1929). Chromosome arrangement: Model experiments with floating magnets and some theoretical considerations on the problem. Mem. Coll. Sci. Kyoto Imp. Univ. 4: 199–264.
Lamb, A.B. (1908). A new explanation of the mechanics of mitosis. J.Exp. Zool. V: 27–33.
Leduc, S. (1901) Diffusion dans la gélatine. C. R. Acad. Sci. Paris CXXXII: 1500–1501.
Leduc, S. (1902). Champs de forces moléculaires. C. R. Acad. Sci. Paris CXXXIV: 423–425
Leduc, S. (1902). Champs de diffusion bipolaire. C. R. Acad. Sci. Paris CXXXIV: 1202–1204.
Leduc, S. (1901 & 1906). Also references cited by Prenant (1910).
Lenhossek, M. von (1899). Das Mikrocentrum des glatten Muskelzellen. Anat. Anzeiger 18: 334–342.
Lillie, F.R. (1902). The organization of the egg of Unio based on a study of its maturation, fertilization and cleavage. J. Morphol. XXVII.
Lillie, F.R. (1909). Karyokinetic figures of centrifuged eggs. An experimental test of the center of force hypothesis. Biological Bulletin. XVII: 101–119.
Lillie, F.R. (1903-1904-1905). Also references cited by Lillie (1909) and Prenant (1910).
Manton, I., B. Clarke and A.D. Greenwood (1955). Observations with the electron microscope on biciliate and quadriciliate zoospores in green algae. J. Expl. Bot. 6: 126–128.
Margolis, R.L., L. Wilson and B.I. Kiefer (1978). Mitotic mechanism based on intrinsic microtubule behavior. Nature 272: 450.
Margolis, R.L. and L. Wilson (1981). Microtubule treadmills: possible molecular machinery. Nature 293: 705–710.
Masui, Y. and C.L. Markert (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177: 129–145.
Maxwell, J.C. (1885) Traité d'électricité et de magnétisme. Translated from English from 2nd edition by G. Seligmann-Lui Paris, Gauthiers Villars.
Mazia, D. (1961). Mitosis and the physiology of cell division. In: J. Brachet and A.E. Mirsky, eds., The Cell Biochemistry, Physiology, Morphology. Academic Press.
Mazia, D. and K. Dan (1952) The isolation and biochemical characterization of the mitotic apparatus of dividing cells. Proc. Natl. Acad. Sci. USA 38: 826–838.
McIntosh, J.R. (1984). Microtubule catastrophe. Nature 312: 196–197.
McIntosh, J.R., P.K. Hepler and D.G. Van Wie (1969). Model for mitosis. Nature 224: 659.
Meves (1897–1898). Zelltheilung. Ergebn. d. Anat. u. Entw. VII and VIII.
Meves (1896–1898). Also references cited by Prenant (1910).
Milovidov, P. (1936). La constitution chimique et physico-chimique du noyau cellulaire. Fondation Masaryk près le Conseil National Tchécoslovaque de Recherches.
Morin, E. (1991). La Méthode. Tome 4. Les Idées. Leur habitat, leur vie, leurs moeurs, leur organisation Paris, Ed. Seuil.
Mota, M. (1956). A new hypothesis of the anaphase movement. Suppl. Cytologia Proc. Internat. Genetics Symposia: 113–116
Murray, A. and T. Hunt (1993). The Cell Cycle: An introduction. New York, Oxford, Ed. Freeman.
Östergren, G., J. Molé-Bajer and A. Bajer (1960). An interpretation of transport phenomena at mitosis Ann. N. Y. Acad. Sci. 90: 381–408.
Paintrand, M., M. Moudjou, H. Delacroix and M. Bornens (1992). Centrosome organization and centriole architecture: their relative sensitivity to divalent cations. J. Struct. Biol. 108: 107–128.
Pethig, R. (1979). Dielectric and electronic properties of biological materials. Chichester, Wiley
Pickett-Heaps, J.D. (1969). The evolution of the mitotic apparatus: an attempt at comparative ultrastructural cytology in dividing plant cell. Cytobios. 3: 257–280.
Pickett-Heaps, J.D. (1971). The autonomy of the centriole: fact or fallacy? Cytobios. 3: 205–214.
Pickett-Heaps, J.D. (1975). Aspects of spindle evolution. Ann. N.Y. Acad. Sci 253: 352–361.
Prenant, A. (1910). Théories et interprétations physiques de la mitose. J. Anat. Physiol. 46: 511–578.
Rhumbler, L. (1896). Versuch einer mechanischen Erklärung der indirecten Zell-und Kerntheilung I; Theil. Die Cytokinese. Arch. f. Entw. Mech. III.
Rhumbler, L. (1897–1903). Also references cited by Prenant (1910)
Salmon, E.D. (1976). Pressure induced depolymerization of spindle microtubules. II Thermodynamics ofin vivo spindle assembly. J. Cell Biol 66: 114–127.
Shafer, F.W. (1969) Centriole of a human cancer: intercellular order and intracellular disorder. Science 164: 1300–1303.
Slautterback, D.B. (1963). Cytoplamic microtubules. J. Cell Biol. 18: 367–388.
Strasburger, E. (1875). Zellbildung und Zellteilung. Jena.
Strasburger, E. (1875). Etudes sur la formation et la division des cellules. Edition revue et corrigée, traduite de l'allemand, par J.J. Kicks Paris 1876.
Turing, A.M. (1952). The chemical basis of morphogenesis. Phil. Trans. Roy. Soc. London 2378: 37–72.
Wade, R.H. (1992). Un regard glacial sur les microtubules. Regards sur la biochimie 2: 24–31.
White, J.G. (1985). The astral relaxation theory of cytokinesis revisited. BioEssays 2: 267–272.
Wilson, E.B. (1925). The cell in development and heredity. 3rd Ed. New York, MacMillan Co.
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Gourret, JP. Modelling the mitotic apparatus. Acta Biotheor 43, 127–142 (1995). https://doi.org/10.1007/BF00709438
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DOI: https://doi.org/10.1007/BF00709438