Summary
Video-enhanced microscopy was used to study the behavior of cytoplasmic microtubules in flattened reticulopodia of the marine protistAllogromia. Linear microtubule bundles were observed bending to various degrees and then straightening. When microtubules bent sufficiently to contact the plasma membrane, protuberances extended from the pseudopodial margins. These protuberances withdrew as the bent microtubules straightened. In extreme cases, microtubules formed c-shaped loops which moved laterally through the cytoplasm and contacted fenestrae formed within the flattened pseudopodia. A given fenestra first deformed at the site of microtubule contact and then closed as the loop continued its motion; reversal of the microtubule motion reopened the fenestra. By electron microscopy, microtubules are consistently seen within 20 nm of the plasma membrane and are often connected to the membrane by detergent-resistant crosslinks. Together, these observations indicate that microtubule movements can deform the plasma membrane and thus mediate certain aspects of cellular morphogenesis.
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References
Allen RD, Allen NS, Travis JL (1981) Video-enhanced contrast differential interference contrast (AVEC-DIC) microscopy: a new method capable of analyzing microtubule-related motility in the reticulopodial network ofAllogromia laticollaris. Cell Motil 1: 291–302
—, Weiss DG, Hayden JH, Brown DT, Fujiwake H, Simpson M (1985) Gliding movement of and bidirectional transport along single microtubules from squid axoplasm: evidence for a role of microtubules in cytoplasmic transport. J Cell Biol 100: 1736–1752
Bloodgood RA (1977) Motility occurring in association with the surface of theChlamydomonas flagellum. J Cell Biol 75: 983–989
Bowser SS, DeLaca TE (1985) Rapid intracellular motility and dynamic membrane events in an Antarctic foraminifer. Cell Biol Int Rep 9: 901–910
—, Rieder CL (1985) Evidence that cell surface motility inAllogromia is mediated by cytoplasmic microtubules. Can J Biochem Cell Biol 63: 608–620
—, McGee-Russell SM, Rieder CL (1985) Digestion of prey in foraminifera is not anomalous: a correlation of light microscopic, cytochemical and HVEM technics to study phagotrophy in two allogromiids. Tissue Cell 17: 823–839
—, Travis JL, Rieder CL (1988) Microtubules associate with actincontaining filaments at discrete sites along the ventral surface ofAllogromia reticulopods. J Cell Sci 89: 297–307
Bray D, Heath J, Moss D (1986) The membrane-associated “cortex” of animal cells: Its structure and mechanical properties. J Cell Sci [Suppl 4]: 71–88
Cassimeris L, Pryer NK, Salmon ED (1988) Real-time observations of microtubule dynamic instability in living cells. J Cell Biol 107: 2223–2231
Dentler WL (1981 a) Microtubule-membrane interactions in ctenophore swimming plate cilia. Tissue Cell 13: 197–208
— (1981 b) Microtubule-membrane interactions in cilia and flagella. Int Rev Cytol 72: 1–47
Jensen CG, Smaill BH (1986) Analysis of the spatial organization of microtubule-associated proteins. J Cell Biol 103: 559–569
McGee-Russell SM, Allen RD (1971) Reversible stabilization of labile microtubules in the reticulopodial network ofAllogromia. Adv Cell Mol Biol 1: 153–184
McIntosh JR (1974) Bridges between microtubules. J Cell Biol 61: 166–187
Sammak PJ, Borisy GG (1988) Direct observation of microtubule dynamics in living cells. Nature 332: 724–726
Schliwa M, van Blerkom J (1981) Structural interaction of cytoskeletal components. J Cell Biol 90: 222–235
Schultze E, Kirschner M (1988) New features of microtubule behaviour observed in vivo. Nature 334: 356–359
Sommer JR (1977) To cationize glass. J Cell Biol 75: 245a
Travis JL, Allen RD (1981) Studies on the motility of the foraminifera: I. Ultrastructure of the reticulopodial network ofAllogromia laticollaris. J Cell Biol 90: 211–221
—, Bowser SS (1986) A new model of reticulopodial motility and shape: evidence of a microtubule-based motor and an actin skeleton. Cell Motil Cytoskeleton 6: 2–14
— — (1988) Optical approaches to the study of foraminiferan motility. Cell Motil Cytoskeleton 10: 126–136
—, Kenealy JFX, Allen RD (1983) Studies on the motility of the foraminifera: II. The dynamic microtubular cytoskeleton of the reticulopodial network ofAllogromia laticollaris. J Cell Biol 97: 1669–1676
Vasiliev JM (1982) Spreading and locomotion of tissue cells; factors controlling the distribution of pseudopodia. Philos Trans R Soc Lond [B] 299: 185–197
— (1987) Actin cortex and microtubular system in morphogenesis: cooperation and competition. J Cell Sci 8: 1–18
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Travis, J.L., Bowser, S.S. Microtubule-membrane interactions in vivo: direct observation of plasma membrane deformation mediated by actively bending cytoplasmic microtubules. Protoplasma 154, 184–189 (1990). https://doi.org/10.1007/BF01539847
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DOI: https://doi.org/10.1007/BF01539847