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Movement of membrane tubules along microtubules in vitro: evidence for specialised sites of motor attachment
V. Allan, R. Vale
Journal of Cell Science 1994 107: 1885-1897;

Summary

We have studied the microtubule-dependent formation of tubular membrane networks in vitro, using a heterologous system composed of Xenopus egg cytosol combined with rat liver membrane fractions enriched in either Golgi stacks or rough endoplasmic reticulum. The first step in membrane network construction involves the extension of membrane tubules along microtubules by the action of microtubule-based motor proteins. We have observed for both membrane fractions that 80–95% of moving tubule tips possess a distinct globular domain. These structures do not form simply as a consequence of motor protein activity, but are stable domains that appear to be enriched in active microtubule motors. Negative stain electron microscopy reveals that the motile globular domains associated with the RER networks are generally smaller than those observed in networks derived from a crude Golgi stack fraction. The globular domains from the Golgi fraction are often packed with very low density lipoprotein particles (the major secretory product of hepatocytes) and albumin, which suggests that motor proteins may be specifically enriched in organelle regions where proteins for export are accumulated. These data raise the possibility that the concentration of active motor proteins into specialised membrane domains may be an important feature of the secretory pathway.

REFERENCES

    1. Alexander, C. A.,
    2. Hamilton, R. L. and
    3. Havel, R. J.
    (1976). Subcellular localization of B apoprotein of plasma lipoproteins in rat liver. J. Cell Biol 69, 241–263
    OpenUrlAbstract/FREE Full Text
    1. Allan, V. J. and
    2. Vale, R. D.
    (1991). Cell cycle control of microtubule-based membrane transport and tubule formation in vitro. J. Cell Biol 113, 347–359
    OpenUrlAbstract/FREE Full Text
    1. Burkhardt, J. K.,
    2. McIlvain, J. M.,
    3. Sheetz, M. P. and
    4. Argon, Y.
    (1993). Lytic granules from cytotoxic T cells exhibit kinesin-dependent motility on microtubules in vitro. J. Cell Sci 104, 151–162
    OpenUrlAbstract/FREE Full Text
    1. Claude, A.
    (1970). Growth and differentiation of cytoplasmic membranes in the course of lipoprotein granule synthesis in the hepatic cell. I. Elaboration of elements of the Golgi complex. J. Cell Biol 47, 745–766
    OpenUrlAbstract/FREE Full Text
    1. Cooper, M. S.,
    2. Cornell-Bell, A. H.,
    3. Chernjavsky, A.,
    4. Dani, J. W. and
    5. Smith, S. J.
    (1990). Tubulovesicular processes emerge from trans-Golgi cisternae, extend along microtubules, and interlink adjacent trans-Golgi elements into a reticulum. Cell 61, 135–145
    OpenUrlCrossRefPubMedWeb of Science
    1. Corthesy-Theulaz, I.,
    2. Pauloin, A. and
    3. Pfeffer, A. R.
    (1992). Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol 118, 1333–1345
    OpenUrlAbstract/FREE Full Text
    1. Dabora, S. L. and
    2. Sheetz, M. P.
    (1988). Microtubule dependent formation of a tubularvesicular network with characteristics of the endoplasmic reticulum from cultured cell extracts. Cell 54, 27–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Gill, S. R.,
    2. Schroer, T. A.,
    3. Szilak, I.,
    4. Steuer, E. R. and
    5. Sheetz, M. P.
    (1991). Dynactin, a conserved, ubiquitously expressed component of an activator of vesicle motility mediated by cytoplasmic dynein. J. Cell Biol 115, 1639–1650
    OpenUrlAbstract/FREE Full Text
    1. Goltz, J. S.,
    2. Wolkoff, A. W.,
    3. Novikoff, P. M.,
    4. Stockert, R. J. and
    5. Satir, P.
    (1992). A role for microtubules in sorting endocytic vesicles in rat hepatocytes. Proc. Nat. Acad. Sci. USA 89, 7026–7030
    OpenUrlAbstract/FREE Full Text
    1. Graham, D. L.,
    2. Knott, T. J.,
    3. Jones, T. C.,
    4. Pease, R. J.,
    5. Pullinger, C. R. and
    6. Scott, J.
    (1991). Carboxyl-terminal truncation of apolipoprotein B results in gradual loss of the ability to form buoyant lipoproteins in cultured human and rat liver cell lines. Biochemistry 30, 5616–5621
    OpenUrlCrossRefPubMed
    1. Henson, J. H.,
    2. Nesbitt, D.,
    3. Wright, B. D. and
    4. Scholey, J. M.
    (1992). Immunolocalization of kinesin in sea urchin coelomocytes. Association of kinesin with intracellular organelles. J. Cell Sci 103, 309–320
    OpenUrlAbstract/FREE Full Text
    1. Ho, W. C.,
    2. Allan, V. J.,
    3. van Meer, G.,
    4. Berger, E. G. and
    5. Kreis, T. E.
    (1989). Reclustering of scattered Golgi elements occurs along microtubules. Eur. J. Cell Biol 48, 250–263
    OpenUrlPubMedWeb of Science
    1. Hollenbeck, P. J. and
    2. Swanson, J. A.
    (1990). Radial extension of macrophage tubular lysosomes supported by kinesin. Nature 346, 864–866
    OpenUrlCrossRefPubMedWeb of Science
    1. Hopkins, C. R.,
    2. Gibson, A.,
    3. Shipman, M. and
    4. Miller, K.
    (1990). Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 346, 335–339
    OpenUrlCrossRefPubMed
    1. Iida, H.,
    2. Barron, W. M. and
    3. Page, E.
    (1988). Monensin turns on microtubule-associated translocation of secretory granules in cultured rat atrial myocytes. Circul. Res 62, 1159–1170
    OpenUrlAbstract/FREE Full Text
    1. Koonce, M. P. and
    2. McIntosh, J. R.
    (1990). Identification and immunolocalization of cytoplasmic dynein in Dictyostelium. Cell Motil. Cytoskel 15, 51–62
    OpenUrlCrossRefPubMed
    1. Kreis, T. E.,
    2. Matteoni, R.,
    3. Hollinshead, M. and
    4. Tooze, J.
    (1989). Secretory granules and endosomes show saltatory movement biased to the anterograde and retrograde directions, respectively, along microtubules in AtT20 cells. Eur. J. Cell Biol 49, 128–139
    OpenUrlPubMedWeb of Science
    1. Lacey, M. L. and
    2. Haimo, L. T.
    (1992). Cytoplasmic dynein is a vesicle protein. J. Biol. Chem 267, 4793–4798
    OpenUrlAbstract/FREE Full Text
    1. Lee, C. H. and
    2. Chen, L. B.
    (1988). Behavior of endoplasmic reticulum in living cells. Cell 54, 37–46
    OpenUrlCrossRefPubMedWeb of Science
    1. Leopold, P. L.,
    2. McDowall, A. W.,
    3. Pfister, K. K.,
    4. Bloom, G. S. and
    5. Brady, S. T.
    (1992). Association of kinesin with characterized membrane-bounded organelles. Cell Motil. Cytoskel 23, 19–33
    OpenUrlCrossRefPubMedWeb of Science
    1. Lin, S. X. H. and
    2. Collins, C. A.
    (1992). Immunolocalization of cytoplasmic dynein to lysosomes in cultured cells. J. Cell Sci 101, 125–137
    OpenUrlAbstract/FREE Full Text
    1. Lippincott-Schwartz, J.,
    2. Donaldson, J. G.,
    3. Schweizer, A.,
    4. Berger, E. G.,
    5. Hauri, H.-P.,
    6. Yuan, L. C. and
    7. Klausner, R. D.
    (1990). Microtubule-dependent retrograde transport of proteins into the ER in the presence of Brefeldin A suggests an ER recycling pathway. Cell 60, 821–836
    OpenUrlCrossRefPubMedWeb of Science
    1. Lippincott-Schwartz, J.,
    2. Yuan, L.,
    3. Tipper, C.,
    4. Amherdt, M.,
    5. Orci, L. and
    6. Klausner, R. D.
    (1991). Brefeldin A's effects on endosomes, lysosomes and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67, 601–616
    OpenUrlCrossRefPubMedWeb of Science
    1. Mahley, R. M.,
    2. Gray, M. E.,
    3. Hamilton, R. L. and
    4. LeQuire, V. S.
    (1968). Lipid transport in liver. II. Electron microscopic and biochemical studies of alterations in lipoprotein transport induced by cortisone in the rabbit. Lab. Invest 19, 358–369
    OpenUrlPubMedWeb of Science
    1. Mahley, R. W.,
    2. Bersot, T. P.,
    3. LeQuire, V. S.,
    4. Levy, R. I.,
    5. Windmueller, H. G. and
    6. Brown, W. V.
    (1970). Identity of very low density lipoprotein apoproteins of plasma and liver Golgi apparatus. Science 168, 380–382
    OpenUrlAbstract/FREE Full Text
    1. Murray, A.
    (1991). Cell cycle extracts. Meth. Cell Biol 36, 581–605
    OpenUrlCrossRefPubMedWeb of Science
    1. Newmeyer, D. D. and
    2. Wilson, K. L.
    (1991). Egg extracts for nuclear import and nuclear assembly reactions. Meth. Cell Biol 36, 607–634
    OpenUrlCrossRefPubMedWeb of Science
    1. Osborn, M. and
    2. Weber, K.
    (1982). Immunofluorescence and immunocytochemical procedures with affinity purified antibodies: tubulin containing structures. Meth. Cell Biol 24, 97–132
    OpenUrlCrossRefPubMedWeb of Science
    1. Paschal, B. M.,
    2. Shpetner, H. S. and
    3. Vallee, R. B.
    (1987). MAP1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties. J. Cell Biol 105, 1273–1282
    OpenUrlAbstract/FREE Full Text
    1. Paschal, B. M. and
    2. Vallee, R. B.
    (1987). Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330, 181–183
    OpenUrlCrossRefPubMedWeb of Science
    1. Pelham, H. R. B.
    (1991). Multiple targets for Brefeldin A. Cell 67, 449–451
    OpenUrlCrossRefPubMedWeb of Science
    1. Pfarr, C. M.,
    2. Coue, M.,
    3. Grissom, P. M.,
    4. Hays, T. S.,
    5. Porter, M. E. and
    6. McIntosh, J. R.
    (1990). Cytoplasmic dynein is localized to kinetochores during mitosis. Nature 345, 263–265
    OpenUrlCrossRefPubMed
    1. Pfister, K. K.,
    2. Wagner, M. C.,
    3. Stenoien, D. L.,
    4. Brady, S. T. and
    5. Bloom, G. S.
    (1989). Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells. J. Cell Biol 108, 1453–1464
    OpenUrlAbstract/FREE Full Text
    1. Rothwell, S. W.,
    2. Nath, J. and
    3. Wright, D. G.
    (1989). Interactions of cytoplasmic granules with microtubule in human neutrophils. J. Cell Biol 108, 2313–2326
    OpenUrlAbstract/FREE Full Text
    1. Rusiñol, A.,
    2. Verkade, H. and
    3. Vance, J. E.
    (1993). Assembly of rat hepatic very low density lipoproteins in the endoplasmic reticulum. J. Biol. Chem 268, 3555–3562
    OpenUrlAbstract/FREE Full Text
    1. Schmid, S. L.
    (1993). Biochemical requirements for the formation of clathrin-and COP-coated transport vesicles. Curr. Biol 5, 621–627
    OpenUrlCrossRef
    1. Schnapp, B. J.,
    2. Reese, T. S. and
    3. Bechtold, R.
    (1992). Kinesin is bound with high affinity to squid axon organelles that move to the plus-end of microtubules. J. Cell Biol 119, 389–399
    OpenUrlAbstract/FREE Full Text
    1. Stein, O. and
    2. Stein, Y.
    (1967). Lipid synthesis, intracellular transport, storage, and secretion. I. Electron microscopic radioautographic study of liver after injection of tritiated palmitate or glycerol in fasted and ethanol-treated rats. J. Cell Biol 33, 319–339
    OpenUrlAbstract/FREE Full Text
    1. Swanson, J.,
    2. Bushnell, A. and
    3. Silverstein, S. C.
    (1987). Tubular lysosome morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules. Proc. Nat. Acad. Sci. USA 84, 1921–1925
    OpenUrlAbstract/FREE Full Text
    1. Terasaki, M.,
    2. Chen, L. B. and
    3. Fujiwara, K.
    (1986). Microtubules and the endoplasmic reticulum are highly interdependent structures. J. Cell Biol 103, 1557–1568
    OpenUrlAbstract/FREE Full Text
    1. Toyoshima, I.,
    2. Yu, H.,
    3. Steuer, E. R. and
    4. Sheetz, M. P.
    (1992). Kinectin, a major kinesin-binding protein on ER. J. Cell Biol 118, 1121–1131
    OpenUrlAbstract/FREE Full Text
    1. Vale, R. D.,
    2. Reese, T. S. and
    3. Sheetz, M. P.
    (1985). Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Vale, R. D.,
    2. Schnapp, B. J.,
    3. Mitchison, T.,
    4. Steuer, E.,
    5. Reese, T. S. and
    6. Sheetz, M. P.
    (1985). Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell 43, 623–632
    OpenUrlCrossRefPubMedWeb of Science
    1. Vale, R. D. and
    2. Hotani, H.
    (1988). Formation of membrane networks in vitro by kinesin-driven microtubule movement. J. Cell Biol 107, 2233–2242
    OpenUrlAbstract/FREE Full Text
    1. Wood, S. A.,
    2. Park, J. E. and
    3. Brown, W. J.
    (1991). Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 67, 591–600
    OpenUrlCrossRefPubMedWeb of Science
    1. Wright, B. D.,
    2. Henson, J. H.,
    3. Wedaman, K. P.,
    4. Willy, P. J.,
    5. Morand, J. N. and
    6. Scholey, J. M.
    (1991). Subcellular localization and sequence of sea urchin kinesin heavy chain: evidence for its association with membranes in the mitotic apparatus and interphase cytoplasm. J. Cell Biol 113, 817–833
    OpenUrlAbstract/FREE Full Text
    1. Yu, H.,
    2. Toyoshima, I.,
    3. Steuer, E. R. and
    4. Sheetz, M. P.
    (1992). Kinesin and cytoplasmic dynein binding to brain microsomes. J. Biol. Chem 267, 20457–20464
    OpenUrlAbstract/FREE Full Text
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Journal Article
Movement of membrane tubules along microtubules in vitro: evidence for specialised sites of motor attachment
V. Allan, R. Vale
Journal of Cell Science 1994 107: 1885-1897;
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