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PMID: 7962076 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Induction of mutant dynamin specifically blocks endocytic coated vesicle formation.

The Journal of cell biology ·Vol. 127 ·No. 4 ·1994-11-00 ·Pages 915-34

Damke H, Baba T, Warnock DE, Schmid SL

Abstract

Dynamin is the mammalian homologue to the Drosophila shibire gene product. Mutations in this 100-kD GTPase cause a pleiotropic defect in endocytosis. To further investigate its role, we generated stable HeLa cell lines expressing either wild-type dynamin or a mutant defective in GTP binding and hydrolysis driven by a tightly controlled, tetracycline-inducible promoter. Overexpression of wild-type dynamin had no effect. In contrast, coated pits failed to become constricted and coated vesicles failed to bud in cells overexpressing mutant dynamin so that endocytosis via both transferrin (Tfn) and EGF receptors was potently inhibited. Coated pit assembly, invagination, and the recruitment of receptors into coated pits were unaffected. Other vesicular transport pathways, including Tfn receptor recycling, Tfn receptor biosynthesis, and cathepsin D transport to lysosomes via Golgi-derived coated vesicles, were unaffected. Bulk fluid-phase uptake also continued at the same initial rates as wild type. EM immunolocalization showed that membrane-bound dynamin was specifically associated with clathrin-coated pits on the plasma membrane. Dynamin was also associated with isolated coated vesicles, suggesting that it plays a role in vesicle budding. Like the Drosophila shibire mutant, HeLa cells overexpressing mutant dynamin accumulated long tubules, many of which remained connected to the plasma membrane. We conclude that dynamin is specifically required for endocytic coated vesicle formation, and that its GTP binding and hydrolysis activities are required to form constricted coated pits and, subsequently, for coated vesicle budding.

MeSH Terms
Animals Base Sequence Blotting, Western Cell Membrane/metabolism Clathrin/analysis,biosynthesis Coated Pits, Cell-Membrane/physiology DNA, Complementary Drosophila/genetics Drosophila Proteins Dynamins Endocytosis Enzyme Induction Fluorescent Antibody Technique GTP Phosphohydrolases/analysis,biosynthesis,metabolism HeLa Cells Humans Kinetics Mammals Molecular Sequence Data Mutagenesis Oligoribonucleotides Protein Processing, Post-Translational Receptors, Transferrin/biosynthesis,metabolism Transfection
Chemicals
Clathrin DNA, Complementary Drosophila Proteins Oligoribonucleotides Receptors, Transferrin GTP Phosphohydrolases Dynamins shi protein, Drosophila
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Damke H
Department of Cell Biology, Scripps Research Institute, La Jolla, California 92037.
Baba T
Warnock D E
Schmid S L
References (72)
72 references, click to expand
  1. Formation of coated vesicles from coated pits in broken A431 cells.
    J Cell Biol. 1989 Mar;108(3):843-53 PMID: 2564003
  2. A novel member of the dynamin family of GTP-binding proteins is expressed specifically in the testis.
    J Cell Sci. 1993 May;105 ( Pt 1):1-5 PMID: 8360266
  3. Identification of dynamin 2, an isoform ubiquitously expressed in rat tissues.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):644-8 PMID: 8290576
  4. GTPases: multifunctional molecular switches regulating vesicular traffic.
    Annu Rev Biochem. 1994;63:949-90 PMID: 7979258
  5. Signal-dependent membrane protein trafficking in the endocytic pathway.
    Annu Rev Cell Biol. 1993;9:129-61 PMID: 8280459
  6. Recruitment of epidermal growth factor and transferrin receptors into coated pits in vitro: differing biochemical requirements.
    Mol Biol Cell. 1993 Jul;4(7):715-27 PMID: 8400457
  7. Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures.
    J Cell Biol. 1993 Dec;123(6 Pt 2):1845-55 PMID: 8276902
  8. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5547-51 PMID: 1319065
  9. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules.
    Cell. 1989 Nov 3;59(3):421-32 PMID: 2529977
  10. The GTPase dynamin binds to and is activated by a subset of SH3 domains.
    Cell. 1993 Oct 8;75(1):25-36 PMID: 8402898
  11. Clathrin-coated pits contain an integral membrane protein that binds the AP-2 subunit with high affinity.
    J Biol Chem. 1990 Sep 25;265(27):16514-20 PMID: 1975814
  12. Coated vesicles from pig brain: purification and biochemical characterization.
    J Mol Biol. 1975 Sep 5;97(1):93-8 PMID: 1177317
  13. Reversible blockage of membrane retrieval and endocytosis in the garland cell of the temperature-sensitive mutant of Drosophila melanogaster, shibirets1.
    J Cell Biol. 1983 Aug;97(2):499-507 PMID: 6411734
  14. Simultaneous visualization of LDL receptor distribution and clathrin lattices on membranes torn from the upper surface of cultured cells.
    J Histochem Cytochem. 1991 Aug;39(8):1017-24 PMID: 1906908
  15. Synchronized endocytosis studied in the oocyte of a temperature-sensitive mutant of Drosophila melanogaster.
    Cell Tissue Res. 1990 Feb;259(2):199-207 PMID: 1692513
  16. Temperature-sensitive mutations in Drosophila melanogaster. XIV. A selection of immobile adults.
    Mol Gen Genet. 1973 Jan 24;120(2):107-14 PMID: 4631264
  17. The protein translocation apparatus of the rough endoplasmic reticulum, its associated proteins, and the mechanism of translocation.
    Curr Opin Cell Biol. 1991 Aug;3(4):580-4 PMID: 1772653
  18. Depletion of intracellular potassium disrupts coated pits and reversibly inhibits cell polarization during fibroblast spreading.
    J Cell Biol. 1993 Mar;120(6):1449-59 PMID: 8449988
  19. Possible temperature-dependent blockage of synaptic vesicle recycling induced by a single gene mutation in Drosophila.
    J Neurobiol. 1983 May;14(3):207-25 PMID: 6304244
  20. The biogenesis of lysosomes.
    Annu Rev Cell Biol. 1989;5:483-525 PMID: 2557062
  21. ATP is required for receptor-mediated endocytosis in intact cells.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2307-18 PMID: 2126013
  22. Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum.
    Cell. 1994 Mar 11;76(5):841-52 PMID: 8124720
  23. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval.
    J Neurosci. 1989 Nov;9(11):3844-60 PMID: 2573698
  24. Refined crystal structure of the triphosphate conformation of H-ras p21 at 1.35 A resolution: implications for the mechanism of GTP hydrolysis.
    EMBO J. 1990 Aug;9(8):2351-9 PMID: 2196171
  25. Three-dimensional visualization of coated vesicle formation in fibroblasts.
    J Cell Biol. 1980 Mar;84(3):560-83 PMID: 6987244
  26. Activation of dynamin GTPase by acidic phospholipids and endogenous rat brain vesicles.
    J Biol Chem. 1993 Aug 15;268(23):17240-6 PMID: 8349610
  27. Exocytosis of pinocytosed fluid in cultured cells: kinetic evidence for rapid turnover and compartmentation.
    J Cell Biol. 1981 Dec;91(3 Pt 1):716-27 PMID: 7328118
  28. Assembly of clathrin-coated pits onto purified plasma membranes.
    Science. 1987 May 1;236(4801):558-63 PMID: 2883727
  29. Temperature sensitivity of muscle and neuron differentiation in embryonic cell cultures from the Drosophila mutant, shibire.
    Dev Biol. 1978 Oct;66(2):442-56 PMID: 100358
  30. The structure and function of proline-rich regions in proteins.
    Biochem J. 1994 Jan 15;297 ( Pt 2):249-60 PMID: 8297327
  31. Coated-vesicle formation in vitro: conflicting results using different assays.
    Trends Cell Biol. 1993 May;3(5):145-8 PMID: 14731608
  32. Mutations in human dynamin block an intermediate stage in coated vesicle formation.
    J Cell Biol. 1993 Aug;122(3):553-63 PMID: 8101525
  33. Transformational process of the endosomal compartment in nephrocytes of Drosophila melanogaster.
    Cell Tissue Res. 1990 Nov;262(2):233-44 PMID: 2127554
  34. Differential expression and regulation of multiple dynamins.
    J Biol Chem. 1994 Feb 11;269(6):4547-54 PMID: 8308025
  35. Predominant and developmentally regulated expression of dynamin in neurons.
    Neuron. 1991 Sep;7(3):461-9 PMID: 1832879
  36. Efficient transformation of mammalian cells with constructs containing a puromycin-resistance marker.
    Gene. 1988;62(1):121-6 PMID: 3371661
  37. Reversible alteration in the neuromuscular junctions of Drosophila melanogaster bearing a temperature-sensitive mutation, shibire.
    J Cell Biol. 1979 Jun;81(3):520-7 PMID: 110817
  38. Dynamin: motor protein or regulatory GTPase.
    J Muscle Res Cell Motil. 1992 Oct;13(5):493-6 PMID: 1460079
  39. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane.
    EMBO J. 1988 Apr;7(4):919-29 PMID: 3402440
  40. Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins.
    Nature. 1990 Sep 20;347(6290):256-61 PMID: 2144893
  41. Inhibition of GTP hydrolysis by Sar1p causes accumulation of vesicles that are a functional intermediate of the ER-to-Golgi transport in yeast.
    J Cell Biol. 1994 Feb;124(4):425-34 PMID: 8106544
  42. Membrane pinch-off and reinsertion observed in living cells of Drosophila.
    J Cell Physiol. 1989 Nov;141(2):383-91 PMID: 2808544
  43. Reversible blockage of neurite development and growth cone formation in neuronal cultures of a temperature-sensitive mutant of Drosophila.
    J Neurosci. 1987 Oct;7(10):3245-55 PMID: 3117981
  44. The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains.
    J Cell Biol. 1992 Nov;119(4):773-86 PMID: 1429836
  45. Membranous intermediates in endocytosis are labile, as shown in a temperature-sensitive mutant.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):4968-72 PMID: 2472637
  46. Interaction of dynamin with microtubules: its structure and GTPase activity investigated by using highly purified dynamin.
    Mol Biol Cell. 1992 Oct;3(10):1181-94 PMID: 1421574
  47. Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis.
    Nature. 1991 Jun 13;351(6327):583-6 PMID: 1828536
  48. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals.
    Nature. 1993 Sep 9;365(6442):163-6 PMID: 8371759
  49. Biochemical and immunochemical analysis of rat brain dynamin interaction with microtubules and organelles in vivo and in vitro.
    J Cell Biol. 1990 Dec;111(6 Pt 2):3023-33 PMID: 2148566
  50. Adaptins.
    Trends Cell Biol. 1992 Oct;2(10):293-7 PMID: 14731924
  51. Cytosol- and clathrin-dependent stimulation of endocytosis in vitro by purified adaptors.
    J Cell Biol. 1992 Dec;119(5):1163-71 PMID: 1447294
  52. Kinetics of internalization and recycling of transferrin and the transferrin receptor in a human hepatoma cell line. Effect of lysosomotropic agents.
    J Biol Chem. 1983 Aug 25;258(16):9681-9 PMID: 6309781
  53. Coated pits in interphase and mitotic A431 cells.
    Eur J Cell Biol. 1987 Dec;45(1):23-9 PMID: 2894988
  54. The structure of an antigenic determinant in a protein.
    Cell. 1984 Jul;37(3):767-78 PMID: 6204768
  55. Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis.
    J Cell Biol. 1987 Apr;104(4):875-86 PMID: 3031085
  56. A role for clathrin in the sorting of vacuolar proteins in the Golgi complex of yeast.
    EMBO J. 1992 Aug;11(8):2811-8 PMID: 1639056
  57. Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system.
    Mol Cell Biol. 1994 Mar;14(3):1669-79 PMID: 8114703
  58. A quantitative analysis of the endocytic pathway in baby hamster kidney cells.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2703-20 PMID: 2592402
  59. Biosynthesis of the human transferrin receptor in cultured cells.
    J Biol Chem. 1981 Dec 25;256(24):12888-92 PMID: 6273413
  60. The ways of endocytosis.
    Int Rev Cytol. 1989;117:131-77 PMID: 2573583
  61. Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae.
    EMBO J. 1993 Aug;12(8):3049-59 PMID: 8344247
  62. Microtubules and Src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11468-72 PMID: 7505438
  63. Dynamin: a novel microtubule-associated GTPase.
    Trends Cell Biol. 1991 Aug;1(2-3):57-60 PMID: 14731567
  64. Receptor-mediated endocytosis in semiintact cells.
    Methods Enzymol. 1992;219:223-34 PMID: 1487996
  65. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis.
    J Cell Biol. 1993 Jan;120(1):37-45 PMID: 8416994
  66. Effects of mutant rat dynamin on endocytosis.
    J Cell Biol. 1993 Aug;122(3):565-78 PMID: 8335685
  67. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A.
    Anal Biochem. 1981 Apr;112(2):195-203 PMID: 6266278
  68. Stage-specific assays for coated pit formation and coated vesicle budding in vitro.
    J Cell Biol. 1991 Sep;114(5):869-80 PMID: 1908470
  69. Rab GTPases in vesicular transport.
    Curr Opin Cell Biol. 1993 Aug;5(4):613-20 PMID: 8257602
  70. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic.
    Nature. 1991 May 30;351(6325):411-4 PMID: 1674590
  71. Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins.
    J Cell Biol. 1989 May;108(5):1863-72 PMID: 2497106
  72. Dynamin is a GTPase stimulated to high levels of activity by microtubules.
    Nature. 1992 Feb 20;355(6362):733-5 PMID: 1311055
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-11-00
Pages
915-34
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2200053
Subset
IM
Grants
NCI NIH HHS · CA58689 · United States
NIGMS NIH HHS · GM42445 · United States
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