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PMID: 8991092 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

AP-2-containing clathrin coats assemble on mature lysosomes.

The Journal of cell biology ·Vol. 135 ·No. 6 Pt 2 ·1996-12-00 ·Pages 1801-14

Traub LM, Bannykh SI, Rodel JE, Aridor M, Balch WE, Kornfeld S

Abstract

Coat proteins appear to play a general role in intracellular protein trafficking by coordinating a membrane budding event with cargo selection. Here we show that the AP-2 adaptor, a clathrin-associated coat-protein complex that nucleates clathrin-coated vesicle formation at the cell surface, can also initiate the assembly of normal polyhedral clathrin coats on dense lysosomes under physiological conditions in vitro. Clathrin coat formation on lysosomes is temperature dependent, displays an absolute requirement for ATP, and occurs in both semi-intact cells and on purified lysosomes, suggesting that clathrin-coated vesicles might regulate retrograde membrane traffic out of the lysosomal compartment.

MeSH Terms
Animals Antigens, CD/analysis,metabolism Brain/cytology Cell Membrane Permeability Cells, Cultured/chemistry,metabolism,ultrastructure Clathrin/analysis Coated Vesicles/chemistry,ultrastructure DNA-Binding Proteins/analysis,metabolism Fluorescent Antibody Technique Freeze Etching Kidney/cytology Liver/cytology Lysosome-Associated Membrane Glycoproteins Lysosomes/chemistry,metabolism,ultrastructure Membrane Glycoproteins/analysis,metabolism Membrane Proteins/analysis Microscopy, Electron Rats Transcription Factor AP-2 Transcription Factors/analysis,metabolism
Chemicals
Antigens, CD Clathrin DNA-Binding Proteins Lysosome-Associated Membrane Glycoproteins Membrane Glycoproteins Membrane Proteins Transcription Factor AP-2 Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Traub L M
Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Bannykh S I
Rodel J E
Aridor M
Balch W E
Kornfeld S
References (71)
71 references, click to expand
  1. A Chinese hamster ovary cell line with a temperature-conditional defect in receptor recycling is pleiotropically defective in lysosome biogenesis.
    J Biol Chem. 1993 Dec 5;268(34):25357-63 PMID: 8244967
  2. Cycling of two endogenous lysosomal membrane proteins, lamp-2 and acid phosphatase, between the cell surface and lysosomes in cultured rat hepatocytes.
    J Biochem. 1993 Oct;114(4):598-604 PMID: 8276775
  3. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF.
    Nature. 1992 Nov 26;360(6402):352-4 PMID: 1448152
  4. Binding of AP-1 Golgi adaptors to membranes requires phosphorylated cytoplasmic domains of the mannose 6-phosphate/insulin-like growth factor II receptor.
    J Biol Chem. 1993 Oct 25;268(30):22552-6 PMID: 8226766
  5. Comparative behavior of lysosomes and the pre-lysosome compartment (PLC) in in vivo cell fusion experiments.
    J Cell Sci. 1991 Jul;99 ( Pt 3):571-82 PMID: 1658017
  6. Targeting of membrane proteins to endosomes and lysosomes.
    Trends Cell Biol. 1994 Aug;4(8):292-7 PMID: 14731593
  7. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells.
    J Cell Biol. 1995 Aug;130(4):781-96 PMID: 7642697
  8. A novel class of clathrin-coated vesicles budding from endosomes.
    J Cell Biol. 1996 Jan;132(1-2):21-33 PMID: 8567724
  9. Golgi membrane dynamics imaged by freeze-etch electron microscopy: views of different membrane coatings involved in tubulation versus vesiculation.
    Cell. 1993 Oct 8;75(1):123-33 PMID: 8402891
  10. Osmotic swelling of endocytic compartments induced by internalized sucrose is restricted to mature lysosomes in cultured mammalian cells.
    Exp Cell Res. 1991 Jan;192(1):52-60 PMID: 1845800
  11. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators.
    Cell. 1992 Apr 3;69(1):129-38 PMID: 1555237
  12. Clathrin, adaptors, and sorting.
    Annu Rev Cell Biol. 1990;6:151-71 PMID: 2177341
  13. Expression and localization of alpha-adaptin isoforms.
    J Cell Sci. 1995 Aug;108 ( Pt 8):2865-75 PMID: 7593326
  14. Metabolic and morphological observations on the effect of surface-active agents of leukocytes.
    J Cell Biol. 1967 Mar;32(3):629-47 PMID: 6034482
  15. The biogenesis of lysosomes.
    Annu Rev Cell Biol. 1989;5:483-525 PMID: 2557062
  16. 100-kDa polypeptides in peripheral clathrin-coated vesicles are required for receptor-mediated endocytosis.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9289-93 PMID: 2574457
  17. 100-kD proteins of Golgi- and trans-Golgi network-associated coated vesicles have related but distinct membrane binding properties.
    J Cell Biol. 1992 Jun;117(6):1171-9 PMID: 1607381
  18. Phosphoinositide 3-kinases and membrane traffic.
    Trends Cell Biol. 1996 Mar;6(3):92-7 PMID: 15157484
  19. Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport.
    J Cell Biol. 1995 Nov;131(4):875-93 PMID: 7490291
  20. Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells.
    J Cell Sci. 1990 Mar;95 ( Pt 3):441-61 PMID: 2166740
  21. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein.
    Nature. 1992 Nov 26;360(6402):350-2 PMID: 1448151
  22. Freeze-fracture identification of sterol-digitonin complexes in cell and liposome membranes.
    J Cell Biol. 1978 Aug;78(2):577-96 PMID: 690180
  23. Liposome-encapsulated antigens are processed in lysosomes, recycled, and presented to T cells.
    Cell. 1991 Jan 25;64(2):393-401 PMID: 1899049
  24. Functions of coated vesicles during protein absorption in the rat vas deferens.
    J Cell Biol. 1967 Nov;35(2):357-76 PMID: 6055991
  25. Targeting and mistargeting of plasma membrane adaptors in vitro.
    J Cell Biol. 1993 Dec;123(5):1093-105 PMID: 8245120
  26. Folding and trimerization of clathrin subunits at the triskelion hub.
    Cell. 1992 Mar 6;68(5):899-910 PMID: 1547490
  27. Glycoproteins of the lysosomal membrane.
    J Cell Biol. 1985 Jun;100(6):1839-47 PMID: 3922993
  28. The mannose 6-phosphate receptor and the biogenesis of lysosomes.
    Cell. 1988 Feb 12;52(3):329-41 PMID: 2964276
  29. Degradation of epidermal growth factor receptor in rat liver. Membrane topology through the lysosomal pathway.
    J Biol Chem. 1991 Nov 5;266(31):21265-73 PMID: 1682317
  30. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane.
    EMBO J. 1988 Apr;7(4):919-29 PMID: 3402440
  31. Eukaryotic membrane traffic: retrieval and retention mechanisms to achieve organelle residence.
    Trends Biochem Sci. 1993 Oct;18(10):395-8 PMID: 8256290
  32. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling.
    J Cell Biol. 1992 Sep;118(6):1379-88 PMID: 1325974
  33. Morphological localization of a major lysosomal membrane glycoprotein in the endocytic membrane system.
    J Biochem. 1989 Oct;106(4):708-16 PMID: 2691512
  34. Effect of starvation and refeeding on autophagy and heterophagy in rat liver.
    J Biochem. 1986 Sep;100(3):623-32 PMID: 2430955
  35. The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane.
    J Cell Biol. 1996 Feb;132(4):565-76 PMID: 8647888
  36. Clathrin structure characterized with monoclonal antibodies. II. Identification of in vivo forms of clathrin.
    J Cell Biol. 1985 Dec;101(6):2055-62 PMID: 4066749
  37. Cytochemical studies of lysosomes, golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat.
    J Histochem Cytochem. 1968 May;16(5):320-36 PMID: 5656143
  38. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2.
    J Biol Chem. 1995 Jan 13;270(2):619-25 PMID: 7822287
  39. Purification, some properties, and tissue distribution of a major lysosome-associated membrane glycoprotein (r-lamp-2) of rat liver.
    J Biochem. 1991 Dec;110(6):922-7 PMID: 1794981
  40. Biochemical analysis of the movement of a major lysosomal membrane glycoprotein in the endocytic membrane system.
    J Biochem. 1989 Oct;106(4):717-22 PMID: 2606917
  41. Proton pumps populate the contractile vacuoles of Dictyostelium amoebae.
    J Cell Biol. 1993 Jun;121(6):1311-27 PMID: 8509452
  42. Down-regulation of the epidermal growth factor receptor in KB cells is due to receptor internalization and subsequent degradation in lysosomes.
    Proc Natl Acad Sci U S A. 1984 Apr;81(8):2384-8 PMID: 6326124
  43. Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the P58 containing compartment.
    J Cell Biol. 1992 Dec;119(5):1097-116 PMID: 1447290
  44. A monoclonal antibody to the heavy chain of clathrin.
    EMBO J. 1983;2(10):1655-64 PMID: 6357779
  45. Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes.
    J Biol Chem. 1994 Oct 21;269(42):26374-80 PMID: 7929357
  46. Biosynthetic transport of a major lysosomal membrane glycoprotein, lamp-1: convergence of biosynthetic and endocytic pathways occurs at three distinctive points.
    Exp Cell Res. 1995 Oct;220(2):464-73 PMID: 7556456
  47. Biochemical dissection of AP-1 recruitment onto Golgi membranes.
    J Cell Biol. 1993 Nov;123(3):561-73 PMID: 8227126
  48. Targeting signals and subunit interactions in coated vesicle adaptor complexes.
    J Cell Biol. 1995 Nov;131(3):619-30 PMID: 7593184
  49. Cycling of the integral membrane glycoprotein, LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis.
    Cell. 1987 Jun 5;49(5):669-77 PMID: 3107839
  50. Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis.
    J Cell Biol. 1987 Apr;104(4):875-86 PMID: 3031085
  51. Filipin-cholesterol complexes form in uncoated vesicle membrane derived from coated vesicles during receptor-mediated endocytosis of low density lipoprotein.
    J Cell Biol. 1983 May;96(5):1273-8 PMID: 6132922
  52. Cycling of an 85-kDa lysosomal membrane glycoprotein between the cell surface and lysosomes in cultured rat hepatocytes.
    J Biochem. 1994 Sep;116(3):670-6 PMID: 7852289
  53. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein.
    Cell. 1993 Jun 4;73(5):999-1005 PMID: 8500185
  54. TGN38/41: a molecule on the move.
    Trends Cell Biol. 1993 Aug;3(8):252-5 PMID: 14731742
  55. Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein.
    J Cell Biol. 1986 May;102(5):1593-605 PMID: 2871029
  56. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes.
    J Cell Biol. 1996 Mar;132(6):1011-23 PMID: 8601581
  57. Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment.
    J Cell Sci. 1994 Jan;107 ( Pt 1):145-57 PMID: 8175904
  58. Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment.
    J Biol Chem. 1995 Mar 3;270(9):4933-42 PMID: 7876268
  59. The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor-II receptor has two signals for lysosomal enzyme sorting in the Golgi.
    J Cell Biol. 1992 Oct;119(2):249-57 PMID: 1400571
  60. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation.
    J Cell Biol. 1993 Dec;123(5):1107-17 PMID: 8245121
  61. Coat proteins and vesicle budding.
    Science. 1996 Mar 15;271(5255):1526-33 PMID: 8599108
  62. Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins.
    J Cell Biol. 1987 Sep;105(3):1227-40 PMID: 2821012
  63. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking.
    J Biol Chem. 1991 Nov 15;266(32):21327-30 PMID: 1939168
  64. Transport of the lysosomal membrane glycoprotein lgp120 (lgp-A) to lysosomes does not require appearance on the plasma membrane.
    J Cell Biol. 1992 Apr;117(2):311-25 PMID: 1560028
  65. The effect of wortmannin on the localisation of lysosomal type I integral membrane glycoproteins suggests a role for phosphoinositide 3-kinase activity in regulating membrane traffic late in the endocytic pathway.
    J Cell Sci. 1996 Apr;109 ( Pt 4):749-62 PMID: 8718666
  66. Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles.
    J Cell Biol. 1988 Dec;107(6 Pt 2):2491-501 PMID: 2849607
  67. Digitonin induced alterations of the erythrocyte membrane as visible by freeze-fracturing.
    Exp Pathol (Jena). 1978;16(1-6):60-8 PMID: 102519
  68. 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies.
    J Cell Biol. 1987 Apr;104(4):887-95 PMID: 2881934
  69. Coated vesicles: a diversity of form and function.
    FASEB J. 1995 Nov;9(14):1445-53 PMID: 7589986
  70. Extracellular release as the major degradative pathway of the insulin-like growth factor II/mannose 6-phosphate receptor.
    J Biol Chem. 1991 Jul 5;266(19):12131-4 PMID: 1648081
  71. Cytoplasmic coat proteins involved in endosome function.
    Cell. 1995 Dec 1;83(5):703-13 PMID: 8521487
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-12-00
Pages
1801-14
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2133961
Subset
IM
Grants
NCI NIH HHS · CA 08759 · United States
NCI NIH HHS · CA 586689 · United States
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