Cellular organelle transport and positioning by plasma streaming

• Autorzy: Wanka F , Van Zoelen E.J.J.
• Języki publikacji: EN

Abstrakty

EN

Our analysis of known data reveals that translocations of passively movable cellular organelles from tiny granules up to large cell nuclei can be ascribed to transport by streaming cytoplasm. The various behaviours, such as velocity changes during more or less interrupted movements, forth and back shuttling and particle rotation result from different types of plasma circulation. Fast movements over long distances, as observed in the large characean internodial cells occur in strong streams generated by myosin in bundles of actin filaments in the direction of the barbed filament ends. Slow movements with frequent reversions of the direction are typical for neuronal axons, in which an anterograde plasma flow, produced in a thin layer of membrane-attached actin filaments, is compensated by a retrograde stream, produced by dynein activity in the central bundle of microtubules. Here particle rotation is due to steep flow velocity gradients, and frequent changes of particle movements result from minor particle displacements in radial directions. Similar shuttling of pigment granules in the lobes of epidermal chromatophores results from the same mechanism, whereby the centrifugal movement along astral microtubules is due to flow generated by excess of kinesin activity and the centripetal movement to the plasma recycling through the intermicrotubular space. If the streaming pattern is reversed by switching to excess dynein activity, the moving granules are trapped in the high microtubule density at the aster center. The presence of larger bodies in asters disturbs the regular, kinesin-dependent microtubule distribution in such a way that a superimposed centrifugal plasma flow develops in the microtubule-dense layer along them, which is recycled in the microtubule-free space, created by their presence. Consequently, at excess kinesin activity, nuclei, mitochondria as well as chromosome fragments move towards the aster center until they reach a dynamically stabilized position that depends on the local microtubule density. These various behaviours are not rationally explainable by models based on a mechanical stepping along microtubules or actin filaments.

Słowa kluczowe

EN

cell organelle; living cell; plasma; intracellular transport; microtubule; actin filament; organelle positoning

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2003
• Tom: 08
• Numer: 4
• Opis fizyczny: p.1035-1045,fig.

Twórcy

autor

Wanka F

• University of Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands

autor

Van Zoelen E.J.J.

Bibliografia

• 1. Schnitzer, M.J., Visscher, K. and Block, S.M. Force production by single kinesin motors. Nat. Cell Biol. 2 (2000) 718-723.
• 2. Bajer, A. and Molé-Bajer, J. Spindle dynamics and chromosome movements. Int. Rev. Cytol. 34 (1972, suppl 3) 1-217.
• 3. Wanka, F. and Van Zoelen, E.J.J. Force generation by cellular motors. Cell. Mol. Biol. Lett. 8 (2003) 1017-1033.
• 4. Williamson, R.E.. Cytoplasmic streaming in Chara: a cell model activated by ATP and inhibited by cytochalasin. J. Cell Sci. 17 (1975) 655-668.
• 5. Kersey, Y.M., Hepler, P.K., Palevitz, B.A. and Wessels, N.K. Polarity of actin filaments in Characean algae. Proc. Natl. Acad. Sci. U.S.A. 73 (1976) 165-167.
• 6. Hayama, T., Shimmen, T. and Tazawa, M. Participation of Ca2+ in cessation of plasma streaming induced by membrane excitation in characean internodial cells. Protoplasma 99 (1979) 303-321.
• 7. Oldenbourg, R., Katoh, K. and Danuser, G. Mechanism of lateral movement of filopodia and radial actin bundles across neuronal growth cones. Biophysical J. 78 (2000) 1176-1182.
• 8. Forer, A. Characterization of the mitotic traction system, and evidence that birefringent spindle fibers neither produce nor transmit force for chromosome movement. Chromosoma 19 (1966) 55-98.
• 9. Schibler, M.J. and Pickett-Heaps, J.D. The kinetochore fiber structure in the acentric spindles of the green alga Oedogonium. Protoplasma 137 (1987) 718-723.
• 10.Euteneuer, V. and McIntosh, J.R. Polarity of some mobility related microtubules. Proc. Natl. Acad. Sci. U.S.A. 78 (1978) 372-376.
• 11.Heidemann, S.R., Landers, J.M. and Hamborg, A.M. Polarity orientation of axonal microtubules. J. Cell Biol. 91 (1981) 661-665.
• 12.Sekine, Y., Okada, Y., Kondo, S., Aizawa, H., Takemura, R. and Hirokawa, N. A novel microtubule based motor (KIF4) for organelle transport, whose expression is regulated developmentally. J. Cell Biol. 137 (1994) 187-201.
• 13.Hollenbeck, P.J. and Bray, D. Rapidly transporting organelles containing membrane and cytoskeletal components: their relation to axonal growth. J. Cell Biol. 105 (1987) 2827-2835.
• 14.Hollenbeck, P.J. Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 121 (1993) 305-315.
• 15.Black, M.M. and Lasek, R.J. Slow components of axonal transport: two cytoskeletal networks. J. Cell Biol. 96 (1983) 354-362.
• 16.Lasek, R.J., Paggi, P. and Katz, M.J. Slow axonal transport mechanisms move neurofilaments relentlessly in mouse optic axons. J. Cell Biol. 117 (1992) 707-616.
• 17.Tanaka, E.M. and Kirschner, M.W. Microtubule behavior in the growth cones of living neurons during axon elongation. J. Cell Biol. 115 (1991) 345-363.
• 18.Rodionov, V.I., Gyoeva, L.K. and Gelfand, V.I. Kinesin is responsible for centrifugal movement of pigment granules in melanophores. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 4956-4960.
• 19.McNiven, M.A., Wang, M. and Porter, K.R. Microtubule polarity and the direction of pigment reverse simultaneously in surgical severed melanophore arms. Cell 37 (1984) 753-765.
• 20.Rebhuhn, L.I. Polarized intracellular particle transport: saltatory movement and cytoplasmic streaming. Int. Rev. Cytol. 32 (1972) 93-137.
• 21.Beckerle, M. and Porter, K.R. Analysis of the role of microtubules and actin in erythrophore intracellular motility. J. Cell Biol. 96 (1983) 354-362.
• 22.Ogawa, K., Hosoya, H., Yokota, E., Kabayashi, T., Wakamatsu, Y., Ozato, K., Negishi, S. and Obika, M. Melanoma dynein: evidence that dynein is a general “motor” for microtubule associated cell motilities. Eur. J. Cell Biol. 43 (1987) 3-9.
• 23.Nilson, H., Steffens W. and Palazzo, R.E. In vitro reconstitution of fish melanophore pigment aggregation. Cell Motil. Cytoskel. 48 (2000) 1-10.
• 24.Rouvière, C., Houliston, E., Carré, D., Chang, P. and Sardet, C. Characteristics of pronuclear migration in Beroe ovata. Cell Motil. Cytoskel. 29 (1994) 301-311.
• 25.Meluh, P.B. and Rose, M.D. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell 60 (1990) 1029-1041.
• 26.Terasaki, M. and Jaffe, L.A. Organization of the sea urchin egg cytoplasmic reticulum and its reorganization at fertilization. J. Cell Biol. 114 (1991) 929-940.
• 27.Riparbelli, M.G., Callaini, G. and Glover, D.M. Failure of pronuclear migration and repeated division of polar body nuclei associated with MTOC defects in polo eggs of Drosophila. J. Cell Sci. 113 (2000) 3341-3350.
• 28.Roos, U.-P. Light and electron microscopy of rat kangaroo cells in mitosis. I. Formation and break down of the mitotic apparatus. Chromosoma 40 (1973) 43-82.
• 29.Harris, P. and Bajer, A. Fine structure studies on mitosis in endosperm metaphase of Haemanthus Katharinae Bak. Chromosoma 16 (1965) 624-636.
• 30.LaFountain, J.R. Changes in patterns of birefringence and filament development in the mitotic spindle of Nephrotoma suturalis. Protoplasma 75 (1972) 2-17.
• 31.Visscher, K., Schnitzer, M.J. and Block, S.M. Single kinesin molecules studied with a molecular force clamp. Nature 400 (1999) 184-189.