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PMID: 2010466 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cell cycle control of microtubule-based membrane transport and tubule formation in vitro.

The Journal of cell biology ·Vol. 113 ·No. 2 ·1991-04-00 ·Pages 347-59

Allan VJ, Vale RD

Abstract

When higher eukaryotic cells enter mitosis, membrane organization changes dramatically and traffic between membrane compartments is inhibited. Since membrane transport along microtubules is involved in secretion, endocytosis, and the positioning of organelles during interphase, we have explored whether the mitotic reorganization of membrane could involve a change in microtubule-based membrane transport. This question was examined by reconstituting organelle transport along microtubules in Xenopus egg extracts, which can be converted between interphase and metaphase states in vitro in the absence of protein synthesis. Interphase extracts support the microtubule-dependent formation of abundant polygonal networks of membrane tubules and the transport of small vesicles. In metaphase extracts, however, the plus end- and minus end-directed movements of vesicles along microtubules as well as the formation of tubular membrane networks are all reduced substantially. By fractionating the extracts into soluble and membrane components, we have shown that the cell cycle state of the supernatant determines the extent of microtubule-based membrane movement. Interphase but not metaphase Xenopus soluble factors also stimulate movement of membranes from a rat liver Golgi fraction. In contrast to above findings with organelle transport, the minus end-directed movements of microtubules on glass surfaces and of latex beads along microtubules are similar in interphase and metaphase extracts, suggesting that cytoplasmic dynein, the predominant soluble motor in frog extracts, retains its force-generating activity throughout the cell cycle. A change in the association of motors with membranes may therefore explain the differing levels of organelle transport activity in interphase and mitotic extracts. We propose that the regulation of organelle transport may contribute significantly to the changes in membrane structure and function observed during mitosis in living cells.

MeSH Terms
Animals Biological Transport Cell Cycle Cell Membrane/metabolism,ultrastructure Female Golgi Apparatus/metabolism Male Microtubules/metabolism,ultrastructure Organelles/metabolism Rats Solubility Xenopus
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Allan V J
Department of Pharmacology, University of California, San Francisco 94143.
Vale R D
References (64)
64 references, click to expand
  1. Polarized intracellular particle transport: saltatory movements and cytoplasmic streaming.
    Int Rev Cytol. 1972;32:93-137 PMID: 4114619
  2. Light and electron microscopy of rat kangaroo cells in mitosis. I. Formation and breakdown of the mitotic apparatus.
    Chromosoma. 1973;40(1):43-82 PMID: 4344486
  3. Surface functions during Mitosis I: phagocytosis, pinocytosis and mobility of surface-bound Con A.
    Cell. 1978 Oct;15(2):327-41 PMID: 719746
  4. A latent adenosine triphosphatase form of dynein 1 from sea urchin sperm flagella.
    J Biol Chem. 1979 Jan 10;254(1):187-96 PMID: 214440
  5. Mitosis in rat thyroid epithelial cells in vivo. I. Ultrastructural changes in cytoplasmic organelles during the mitotic cycle.
    J Ultrastruct Res. 1979 Jan;66(1):53-77 PMID: 423323
  6. Membrane distribution in dividing endosperm cells of Haemanthus.
    J Cell Biol. 1982 Sep;94(3):637-43 PMID: 7130275
  7. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation.
    J Cell Biol. 1983 May;96(5):1374-88 PMID: 6404912
  8. Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis.
    J Cell Biol. 1983 Nov;97(5 Pt 1):1623-8 PMID: 6355124
  9. A time-lapse video image intensification analysis of cytoplasmic organelle movements during endosome translocation.
    J Cell Biol. 1984 Feb;98(2):565-76 PMID: 6693496
  10. Direct visualization of protein transport and processing in the living cell by microinjection of specific antibodies.
    Cell. 1984 Nov;39(1):99-109 PMID: 6091920
  11. Recycling of transferrin receptors in A431 cells is inhibited during mitosis.
    EMBO J. 1984 Oct;3(10):2217-25 PMID: 6209129
  12. Membranes in the mitotic apparatus: their structure and function.
    Int Rev Cytol. 1984;90:169-238 PMID: 6389413
  13. Meiotic maturation in Xenopus oocytes: a link between the cessation of protein secretion and the polarized disappearance of Golgi apparati.
    J Cell Biol. 1985 Jul;101(1):313-8 PMID: 4008532
  14. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility.
    Cell. 1985 Aug;42(1):39-50 PMID: 3926325
  15. Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts.
    J Cell Biol. 1985 Aug;101(2):518-23 PMID: 3926780
  16. Newly synthesized G protein of vesicular stomatitis virus is not transported to the Golgi complex in mitotic cells.
    J Cell Biol. 1985 Dec;101(6):2036-46 PMID: 2999158
  17. Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro.
    Cell. 1985 Dec;43(3 Pt 2):623-32 PMID: 2416467
  18. Microtubules and the endoplasmic reticulum are highly interdependent structures.
    J Cell Biol. 1986 Oct;103(4):1557-68 PMID: 3533956
  19. Bidirectional pigment granule movements of melanophores are regulated by protein phosphorylation and dephosphorylation.
    Cell. 1986 Dec 26;47(6):1061-70 PMID: 3022941
  20. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA.
    Cell. 1987 Jan 30;48(2):205-17 PMID: 3026635
  21. Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes.
    Cell. 1987 Jan 30;48(2):219-30 PMID: 3026636
  22. Myosin movement in vitro: a quantitative assay using oriented actin cables from Nitella.
    Methods Enzymol. 1986;134:531-44 PMID: 3821577
  23. Accumulation of adrenocorticotropin secretory granules in the midbody of telophase AtT20 cells: evidence that secretory granules move anterogradely along microtubules.
    J Cell Biol. 1987 Apr;104(4):1047-57 PMID: 3031082
  24. Tubular lysosomes accompany stimulated pinocytosis in macrophages.
    J Cell Biol. 1987 May;104(5):1217-22 PMID: 3571329
  25. Translocation and clustering of endosomes and lysosomes depends on microtubules.
    J Cell Biol. 1987 Sep;105(3):1253-65 PMID: 3308906
  26. MAP 1C is a microtubule-activated ATPase which translocates microtubules in vitro and has dynein-like properties.
    J Cell Biol. 1987 Sep;105(3):1273-82 PMID: 2958482
  27. Intracellular transport using microtubule-based motors.
    Annu Rev Cell Biol. 1987;3:347-78 PMID: 3120763
  28. Myosin structure and function in cell motility.
    Annu Rev Cell Biol. 1987;3:379-421 PMID: 3318880
  29. Rotation and translocation of microtubules in vitro induced by dyneins from Tetrahymena cilia.
    Cell. 1988 Feb 12;52(3):459-69 PMID: 2964278
  30. Coated pits in interphase and mitotic A431 cells.
    Eur J Cell Biol. 1987 Dec;45(1):23-9 PMID: 2894988
  31. The microtubule-dependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts.
    Cell. 1988 Jul 1;54(1):27-35 PMID: 3289756
  32. Dynamic behavior of endoplasmic reticulum in living cells.
    Cell. 1988 Jul 1;54(1):37-46 PMID: 3383243
  33. The role of kinesin and other soluble factors in organelle movement along microtubules.
    J Cell Biol. 1988 Nov;107(5):1785-92 PMID: 3141429
  34. Formation of membrane networks in vitro by kinesin-driven microtubule movement.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2233-41 PMID: 3143735
  35. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH.
    J Cell Biol. 1989 Mar;108(3):855-64 PMID: 2921284
  36. Dynein is the motor for retrograde axonal transport of organelles.
    Proc Natl Acad Sci U S A. 1989 Mar;86(5):1548-52 PMID: 2466291
  37. Cytoplasmic dynein is a minus end-directed motor for membranous organelles.
    Cell. 1989 Mar 24;56(6):937-46 PMID: 2522353
  38. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro.
    J Cell Biol. 1989 Apr;108(4):1301-16 PMID: 2538480
  39. Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells.
    J Cell Biol. 1989 Apr;108(4):1453-63 PMID: 2522455
  40. Cyclin synthesis drives the early embryonic cell cycle.
    Nature. 1989 May 25;339(6222):275-80 PMID: 2566917
  41. Reclustering of scattered Golgi elements occurs along microtubules.
    Eur J Cell Biol. 1989 Apr;48(2):250-63 PMID: 2743999
  42. Mitotic Golgi fragments in HeLa cells and their role in the reassembly pathway.
    J Cell Biol. 1989 Aug;109(2):463-74 PMID: 2503521
  43. Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts.
    Cell. 1990 Aug 10;62(3):579-89 PMID: 2379239
  44. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells.
    Cell. 1990 Aug 24;62(4):719-31 PMID: 2143699
  45. Radial extension of macrophage tubular lysosomes supported by kinesin.
    Nature. 1990 Aug 30;346(6287):864-6 PMID: 1697403
  46. Severing of stable microtubules by a mitotically activated protein in Xenopus egg extracts.
    Cell. 1991 Feb 22;64(4):827-39 PMID: 1671762
  47. Taxol-induced microtubule asters in mitotic extracts of Xenopus eggs: requirement for phosphorylated factors and cytoplasmic dynein.
    J Cell Biol. 1991 Mar;112(6):1177-87 PMID: 1671864
  48. THE ULTRASTRUCTURE OF A MAMMALIAN CELL DURING THE MITOTIC CYCLE.
    J Cell Biol. 1964 Jun;21:429-63 PMID: 14189913
  49. Construction of the endoplasmic reticulum.
    J Cell Biol. 1989 Nov;109(5):2045-55 PMID: 2478561
  50. Dominoes and clocks: the union of two views of the cell cycle.
    Science. 1989 Nov 3;246(4930):614-21 PMID: 2683077
  51. A post-ribosomal supernatant from activated Xenopus eggs that displays post-translationally regulated oscillation of its cdc2+ mitotic kinase activity.
    EMBO J. 1989 Oct;8(10):3059-69 PMID: 2573514
  52. The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs.
    Nature. 1989 Nov 30;342(6249):512-8 PMID: 2531292
  53. Inhibition of endocytic vesicle fusion in vitro by the cell-cycle control protein kinase cdc2.
    Nature. 1989 Dec 21-28;342(6252):942-5 PMID: 2556645
  54. Regulation of microtubule dynamics by cdc2 protein kinase in cell-free extracts of Xenopus eggs.
    Nature. 1990 Jan 18;343(6255):233-8 PMID: 2405278
  55. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway.
    Cell. 1990 Mar 9;60(5):821-36 PMID: 2178778
  56. Tubulovesicular processes emerge from trans-Golgi cisternae, extend along microtubules, and interlink adjacent trans-golgi elements into a reticulum.
    Cell. 1990 Apr 6;61(1):135-45 PMID: 2180583
  57. Universal control mechanism regulating onset of M-phase.
    Nature. 1990 Apr 5;344(6266):503-8 PMID: 2138713
  58. Cytoplasmic dynein is localized to kinetochores during mitosis.
    Nature. 1990 May 17;345(6272):263-5 PMID: 2139717
  59. Biochemistry of interorganelle transport. A new frontier in enzymology emerges from versatile in vitro model systems.
    J Biol Chem. 1989 Oct 15;264(29):16965-8 PMID: 2507534
  60. Protein transport from endoplasmic reticulum to the Golgi complex can occur during meiotic metaphase in Xenopus oocytes.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1439-44 PMID: 2793929
  61. Localization of cytoplasmic dynein to mitotic spindles and kinetochores.
    Nature. 1990 May 17;345(6272):266-8 PMID: 2139718
  62. Substrates for p34cdc2: in vivo veritas?
    Cell. 1990 May 18;61(4):549-51 PMID: 2188729
  63. Three-dimensional electron microscopy: structure of the Golgi apparatus.
    Eur J Cell Biol. 1990 Apr;51(2):189-200 PMID: 2190832
  64. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum.
    Nature. 1990 Jul 26;346(6282):335-9 PMID: 2374607
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.113.2.347
Published
1991-04-00
Pages
347-59
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2288932
Subset
IM
Grants
NIGMS NIH HHS · R01 GM038499 · United States
NIGMS NIH HHS · GM38499 · United States
External Links
PubMed source DOI: 10.1083/jcb.113.2.347 PMC Full Text View journal details
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