AP-2-containing clathrin coats assemble on mature lysosomes

Journal of Cell Biology

Volumn 135, Issue 6 II, 1996, Pages 1801-1814

  Traub, Linton M ^a   Bannykh, Sergei I ^b   Rodel, Jill E ^a   Aridor, Meir ^b   Balch, William E ^b   Kornfeld, Stuart ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHALASIN D; PHALLOIDIN; SPECTRIN;

AFFINITY CHROMATOGRAPHY; ANTIGEN ANTIBODY REACTION; ARTICLE; CELL FUNCTION; CELL MIGRATION; CENTROSOME; GENETIC TRANSFECTION; GOLGI COMPLEX; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALS; ANTIGENS, CD; BRAIN; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CLATHRIN; COATED VESICLES; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; FREEZE ETCHING; KIDNEY; LIVER; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; RATS; TRANSCRIPTION FACTOR AP-2; TRANSCRIPTION FACTORS;

EID: 0030449536     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.6.1801     Document Type: Article

References (72)

1. Ahle, S., A. Mann, U. Eichelsbacher, and U. Ungewickell. 1988. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO (Eur Mol. Biol. Organ.) J. 7:919-929.
2. Akasaki, K., Y. Yamaguchi, K. Furuno, and H. Tsuji. 1991. Purification, some properties, and tissue distribution of a major lysosome-associated membrane glycoprotein (r-lamp-2) of rat liver. J. Biochem. (Tokyo). 110:922-927.
3. Akasaki, K., M. Fukuzawa, H. Kinoshita, K. Furuno, and H. Tsuji. 1993. Cycling of two endogenous lysosomal membrane proteins, lamp-2 and acid phosphatase. between the cell surface and lysosomes in cultured rat hepatocytes. J. Biochem. (Tokyo). 114:598-604.
4. Akasaki, K., A. Michihara, M. Fukuzawa, H. Kinoshita, and H. Tsuji. 1994. Cycling of an 85-kDa lysosomal membrane glycoprotein between the cell surface and lysosomes in cultured rat hepatocytes. J. Biochem. (Tokyo). 116:670-676.
5. Akasaki, K., A. Michihara, K. Mikuba, Y. Fujiwara, and H. Tsuji. 1995. Biosynthetic transport of a major lysosomal membrane glycoprotein. lamp-1: convergence of biosynthetic and endocytic pathways occurs at three distinctive points. Exp. Cell Res. 220:464-473.
6. Aridor, M., S.I. Bannykh, T. Rowe, and W.E. Balch. 1995. Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131:875-893.
7. Ball, C.L., S.P. Hunt, and M.S. Robinson. 1995. Expression and localization of α-adaptin isoforms. J. Cell Sci. 108:2865-2875.
8. Beguinot, L., R.M. Lyall, M.C. Willingham, and I.H. Pastan. 1984. 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. USA. 81:2384-2388.
9. Brodsky, F.M. 1985. Clathrin structure characterized with monoclonal antibodies. II. Identification of in vivo forms of clathrin. J. Cell Biol. 101:2055-2062.
10. Brown, W.J., D.B. Dewald, S.D. Emr, H. Plutner, and W.E. Balch. 1995. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol. 130:781-796.
11. Chin, D. J., R. M. Straubinger, S. Acton, I. Nathke, and F. M. Brodsky. 1989. 100-kDa polypeplides in peripheral clathrin-coated vesicles are required for receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA. 86:9289-9293.
12. Clairmont, K.B., and M.P. Czech. 1991. Extracellular release as the major degradative pathway of the insulin-like growth factor II/mannose 6-phosphate receptor. J. Biol. Chem. 266:12131-12134.
13. Cuervo, A.M., S.R. Terlecky, J.F. Dice, and E. Knecht. 1994. Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes. J. Biol. Chem. 269:26374-26380.
14. de Duve, C. 1963. The lysosome concept. In Lysosomes. A.V.S. de Reuck and M.P. Cameron, editors. Little, Brown, and Co., Boston, MA. 1-35.
15. DeCourcy, K., and B. Storrie. 1991. Osmotic swelling of endocytic compartments induced by internalized sucrose is restricted to mature lysosomes in cultures mammalian cells. Exp. Cell Res. 192:52-60.
16. Deng, Y., G. Griffiths, and B. Storrie. 1991. Comparative behavior of lysosomes and the pre-lysosomal compartment (PLC) in in vivo cell fusion experiments. J. Cell Sci. 99:571-582.
17. Donaldson, J.G., D. Finazzi, and R.D. Klausner. 1992. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature (Lond.). 360:350-352.
18. Elias, P.M., J. Goerke, D.S. Friend, and E.B. Brown. 1978. Freeze-fracture identification of sterol-digitonin complexes in cell and liposome membranes. J. Cell Biol. 78:577-596.
19. Friend, D.S., and M.G. Farquhar. 1967. Functions of coated vesicles during protein absorption in the rat vas deference. J. Cell Biol. 35:357-376.
20. Fukuda, M. 1991. Lysosomal membrane glycoproteins. structure, biosynthesis, and intracellular trafficking. J. Biol. Chem. 266:21327-21330.
21. Furuno, K., T. Ishikawa, K. Akasaki, S. Yano, Y. Tanaka, Y. Yamaguchi, H. Tsuji, M. Himeno, and K. Kato. 1989. Morphological localization of a major lysosomal membrane glycoprotein in the endocytic membrane system. J. Biochem. (Tokyo). 106:708-716.
22. Furuno, K., S. Yano, K. Akasaki, Y. Tanaka, Y. Yamaguchi, H. Tsuji, M. Himeno, and K. Kato. 1989. Biochemical analysis of the movement of a major lysosomal membrane glycoprotein in the endocytic membrane system. J. Biochem. (Tokyo). 106:717-722.
23. Futter, C.E., A. Pearse, L.J. Hewlett, and C.R. Hopkins. 1996. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 132:1011-1023.
24. Geuze, H.J., W. Stoorvogel, G.J. Strous, J.W. Slot, J.E. Bleekemolen, and I. Mellman. 1988. Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J. Cell Biol. 107:2491-2501.
25. Graham, R.C., M.J. Karnovsky, A.W. Shafer, E.A. Glass, and M.L. Karnovsky. 1967. Metabolic and morphological observations on the effect of surface-active agents on leukocytes. J. Cell Biol. 32:629-647.
26. Green, S.A., K.-P. Zimmer, G. Griffiths, and I. Mellman. 1987. Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins. J. Cell Biol. 105:1227-1240.
27. Griffiths, G., B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52:329-341.
28. Griffiths, G., R. Matteoni, R. Back, and B. Hoflack. 1990. Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J. Cell Sci. 95:441-461.
29. Harding, C. V., D. S. Collins, J. W. Slot, H. J. Geuze, and E. R. Unanue. 1991. Liposome-encapsulated antigens are processed in lysosomes, recycled, and presented to T cells. Cell. 64:393-401.
30. Harter, C., and I. Mellman. 1992. Transport of the lysosomal membrane glycoprotein lgp120 (lgp-A) does not require appearance on the plasma membrane. J. Cell Biol. 117:311-325.
31. Helms, J.B., and J.E. Rothman. 1992. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature (Lond.). 360:352-354.
32. Heuser, J., Q. Zhu, and M. Clarke. 1993. Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J. Cell Biol. 121:1311-1327.
33. Holtzman, E., and R. Dominitz. 1968. Cytochemical studies of lysosomes, Golgi apparatus and endoplasmic reticulum in secretion and protein uptake by adrenal medulla cells of the rat. J. Histochem. Cytochem. 16:320-336.
34. Jahraus, A., B. Storrie, G. Griffiths, and M. Desjardins. 1994, Evidence for retrograde traffic between terminal lysosomes and the prelysosomal/late endosome compartment. J. Cell Sci. 107:145-157.
35. Johnson, K.F., and S. Kornfeld. 1992. 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. 119:249-257.
36. Kornfeld, S., and I. Mellman. 1987. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
37. Le Borgne, R., A. Schmidt, F. Mauxion, G. Griffiths, and B. Hoflack. 1993. 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. 268:22552-22556.
38. Lewis, V., S.A. Green, M. Marsh, P. Vikho, A. Helenius, and I. Mellman. 1985. Glycoproteins of the lysosomal membrane. J. Cell Biol. 100:1839-1847.
39. Lippincott-Schwartz, J., and D.M. Fambrough. 1986. Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein. J. Cell Biol. 102:1593-1605.
40. Lippincott-Schwartz, J., and D. M. Fambrough. 1987. Cycling of the integral membrane glycoprotein. LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis. Cell. 49:669-677.
41. Louvard, D., C. Morris, G. Warren, K. Stanley, F. Winkler, and H. Reggio. 1983. A monoclonal antibody to the heavy chain of clathrin. EMBO (Eur. Mol. Biol. Organ.) J. 2:1655-1664.
42. Luzio, J.P., and G. Banting. 1993. Eukaryotic membrane traffic: retrieval and retention mechanisms to achieve organelle residence. Trends Biochem. Sci. 18:395-398.
43. Marsh, M., S. Schmid, H. Kern, E. Harms, P. Male, I. Mellman, and A. Helenius. 1987. Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis. J. Cell Biol. 104:875-886.
44. Maycox, P.R., E. Link, A. Reetz, S.A. Morris, and R. Jahn. 1992. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118:1379-1388.
45. McGookey, D.J., K. Fagerberg, and R.G.W. Anderson. 1983. Filipin-cholesterol complexes form in uncoated membrane derived from coated vesicles during receptor-mediated endocytosis of low density lipoprotein. J. Cell Biol. 96:1273-1278.
46. Meyer, H.W., H. Winkelmann, and W. Richter. 1978. Digitonin induced alterations of the erythrocyte membrane as visible by freeze-fracturing. Exp. Pathol. (Jena). 16:60-68.
47. Nathke, I.S., J. Heuser, A. Lupas, J. Stock, C.W. Turck, and P.M. Brodsky. 1992. Folding and trimerization of clathrin subunits at the triskelion hub. Cell. 68:899-910.
48. Ohshita, T., E. Kominami, K. Ii, and N. Katunuma. 1986. Effect of starvation and refeeding on autophagy and heterophagy in rat liver. J. Biochem. (Tokyo). 100:623-632.
49. Page, L., and M. Robinson. 1995. Targeting signals and subunit interactions in coaled vesicle adaptor complexes. J. Cell Biol. 131:619-630.
50. Pearse, B.M.F., and M.S. Robinson. 1990. Clathrin. adaptors and sorting. Annu. Rev. Cell Biol. 6:151-171.
51. Plutner, H., H.W. Davidson, J. Saraste, and W.E. Balch. 1992. Morphological analysis of protein transport from the ER to Golgi membranes in digitonin-permeabilized cells: role of the p58 containing compartment. J. Cell Biol. 119:1097-1116.
52. Reaves, B.J., N. A. Bright, B.M. Mullock, and J.P. Luzio. 1996. 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. 109:749-762.
53. Renfrew, C.A., and A.L. Hubbard. 1991. Degradation of epidermal growth factor receptor in rat liver: membrane topology through the lysosomal pathway. J. Biol. Chem. 266:21265-21273.
54. Robinson, M.S. 1987. 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J. Cell Riol. 104:887-895.
55. Robinson, M.S., and T.E. Kreis. 1992. Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell. 69:129-138.
56. Rohrer, J., A. Schweizer, D. Russell, and S. Kornfeld. 1996. The targeting of lamp1 to lysosomes is dependent on the spacing of its cytoplamic tail tyrosine sorting motif relative to the membrane. J. Cell Biol. 132:565-576.
57. Sandoval, I.V., and O. Bakke. 1994. Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4:292-297.
58. Schekman, R., and L. Orci. 1996. Coat proteins and vesicle budding. Science (Wash. DC). 271:1526-1533.
59. Schmid, S. L., and H. Damke. 1995. Coated vesicles: a diversity of form and function. FASEB (Fed. Am. Soc. Exp. Biol.)] 9:1445-1453.
60. Seaman, M.N.J., C.L. Ball, and M.S. Robinson. 1993. Targeting and mistargeting of plasma membrane adaptors in vitro. J. Cell Biol. 123:1093-1105.
61. Shepherd, P.R., B.J. Reaves, and H.W. Davidson. 1996. Phosphoinositide 3-kinases and membrane traffic. Trends Cell Biol. 6:92-97.
62. Sorkin, A., T. McKinsey, W. Shih, T. Kirchhausen, and G. Carpenter. 1995. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2. J. Biol. Chem. 270:619-625.
63. Stamnes, M.A., and J.E. Rothman. 1993. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell. 73:999-1005.
64. Stanley, K.K., and K.E. Howell. 1993. TGN38/41: a molecule on the move. Trends Cell Biol. 3:252-255.
65. Stoorvogel, W., V. Oorschot, and H.J. Geuze. 1996. A novel class of clathrin-coated vesicles budding from endosomes. J. Cell Biol. 132:21-33.
66. Traub, L.M., J.A. Ostrom, and S. Kornfeld. 1993. Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol. 123:561-573.
67. Traub, L.M., S. Kornfeld, and E. Ungewickell. 1995. Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment. J. Biol. Chem. 270:4933-4942.
68. Wang, L.-H., K. G. Rothberg, and R. G. W. Anderson. 1993. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 123:1107-1117.
69. Weidman, P., R. Roth, and J. Heuser. 1993. Golgi membrane dynamics imaged by freeze-etch electron microscopy: views of different membrane coatings involved in tubulation versus vesiculation. Cell. 75:123-133.
70. Whitney, J.A., M. Gomez, D. Sheff, T.E. Kreis, and I. Mellman. 1995. Cytoplasmic coat proteins involved in endosome function. Cell. 83:703-713.
71. Wilson, R.B., C.C. Mastick, and R.F. Murphy. 1993. A Chinese hamster ovary cell line with a temperature-conditional defect in receptor recycling is pleiotropically defective in lysosome biogenesis. J. Biol. Chem. 268:25357-25363.
72. Wong, D.H., and F.M. Brodsky. 1992. 100-kD proteins of Golgi- and trans-Golgi network-associated coated vesicles have related but distinct membrane binding properties. J. Cell Biol. 117:1171-1179.