In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting

EMBO Journal

Volumn 15, Issue 11, 1996, Pages 2893-2899

  Heilker, Ralf ^a   Manning Krieg, Ute ^b   Zuber, Jean François ^b   Spiess, Martin ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b Sandoz Pharma Ltd   (Switzerland)

Author keywords

Adaptor complexes; Basolateral sorting; Clathrin coated vesicles; Endocytosis signals; Surface plasmon resonance

Indexed keywords

CLATHRIN; MEMBRANE PROTEIN; OLIGOPEPTIDE; TYROSINE; VIRUS HEMAGGLUTININ;

AMINO ACID COMPOSITION; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; BINDING AFFINITY; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; DISSOCIATION CONSTANT; ENDOCYTOSIS; GOLGI COMPLEX; INFLUENZA VIRUS; INTERNALIZATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

EID: 0029935911     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00650.x     Document Type: Article

References (44)

1. Ahle,S., Mann,A., Eichelsbacher,U. and Ungewickell,E. (1988) Structural relationships between clathrin assembly proteins from the Golgi anil the plasma membrane. EMBO J., 7, 919-930.
2. Backer,J.M., Shoelson,S.E., Weiss,M.A., Hua,Q.X., Cheatham,R.B., Haring,E., Cahill,D.C. and White,M.F. (1992) The insulin receptor juxtamembrane region contains 2 independent tyrosine/β-turn internalization signals. J. Cell Biol., 118, 831-839.
3. Bansal,A. and Gierasoh,L.M. (1991) The NPXY internalization signal of the LDL receptor adopts a reverse-turn conformation. Cell. 67, 1195-1201.
4. Beltzer,J.P. and Spiess,M. (1991) In vitro binding of the asialoglycoprotein receptor to the β-adaptin of plasma membrane coated vesicles. EMBO J., 10, 3735-3742.
5. Brewer,C.B. and Roth,M.G. (1991) A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J. Cell Biol., 114, 413-421.
6. Campbell,C., Squicciarini,J., Shia,M., Pilch,P.F. and Fine,R.E. (1984) Identification of a protein kinase as an intrinsic component of rat liver coated vesicles. Biochemistry, 23, 4420-4426.
7. Davis,C.G., van Driel,I.R., Russell,D.W., Brown,M.S. and Goldstein,J.L. (1987) The low density lipoprotein receptor. Identification of amino acids in the cytoplasmic domain required for rapid endocytosis. J. Biol Chem., 262, 4075-4082.
8. Eberle,W., Sander,C., Klaus,W., Schmidt,B., von Figura,K. and Peters,C (1991) The essential tyrosine of the internalization signal in lysosoma acid phosphatase is pan of a β-turn. Cell, 67, 1203-1209.
9. Fägerstamm,L. (1991) A Non-label Technology for Real-time Biospecific Interaction Analysis. Academic Press Inc., New York.
10. Fire,E., Zwart,D.E., Roth,M.G. and Henis,Y.I. (1991) Evidence from lateral mobility studies for dynamic interactions of a mutant influenza hemagglutinin with coated pits. J. Cell Biol., 115, 1585-1594.
11. Fire,E., Gutman,O., Roth,M.G. and Henis,Y.I. (1995) Dynamic or stable interactions of influenza hemagglutinin mutants with coated pits. Dependence on the imernalization signal but not on aggregation. J. Biol. Chem., 270, 21075-21081.
12. Futter,C.E., Connolly,C.N., Cutler,D.F. and Hopkins,C.R. (1995) Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface. J. Biol. Chem., 270, 10999-11003.
13. Glickman,J.N., Conibear,E. and Pearse,B.M.F. (1989) Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin-like growth factor-II receptor. EMBO J., 8, 1041-1047.
14. Hunziker,W. and Fumey,C. (1994) A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells. EMBO J., 13, 2963-2969.
15. Hunziker,W., Harter,C., Matter,K. and Mellman,I. (1991) Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell, 66, 907-920.
16. Johnson,K.F. and Kornfeld,S. (1992a) The cytoplasmic tail of the mannose 6-phosphate/insulin-like growth factor-II receptor has 2 signals for lysosomal enzyme sorting in the Golgi. J. Cell Biol., 119, 249-257.
17. Johnson,K.F. and Kornfeld,S. (1992b) A His-Leu-Leu sequence near the C-terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J. Biol. Chem., 267, 17110-17115.
18. Ktistakis,N.T., Thomas,D. and Roth,M.G. (1990) Characteristics of the tyrosine recognition signal for internalization of transmembrane surface glycoproteins. J. Cell Biol, 111, 1393-1407.
19. Lazarovits,J. and Roth,M. (1988) A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits. Cell, 53, 743-752.
20. Leitinger,B., Hille-Rehfeld,A. and Spiess,M. (1995) Biosynthetic transport of the asialoglycoprotein receptor H1 to the cell surface occurs via endosomes. Proc. Natl Acad. Sci. USA, 92, 10109-10113.
21. Letourneur,F. and Klausner,R.D. (1992) A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell, 69, 1143-1157.
22. Mahaffey,D.T., Peeler,J.S., Brodsky,F.M. and Anderson,R.G.W. (1990) Clathrin-coated pits contain an integral membrane protein that binds the AP-2 subunit with high affinity. J. Biol. Chem., 265, 16514-16520.
23. Naim,H.Y. and Roth,M.G. (1994) Characteristics of the internalization signal in the Y543 influenza virus hemagglutinin suggest a model for recognition of internalization signals containing tyrosine. J. Biol. Chem., 269, 3928-3933.
24. Naim,H.Y., Dodds,D.T., Brewer,C.B. and Roth,M.G. (1995) Apical and basolateral coated pits of MDCK cells differ in their rates of maturation into coated vesicles, but not in the ability to distinguish between mutant hemagglutinin proteins with different internalization signals. J. Cell Biol., 129, 1241-1250.
25. Nesterov,A., Wiley,H.S. and Gill,G.N. (1995) Ligand-induced endocytosis of epidermal growth factor receptors that are defective in binding adaptor proteins. Proc. Natl Acad. Sci. USA, 92, 8718-8723.
26. Ogata,S. and Fukuda,M. (1994) Lysosomal targeting of Limp II membrane glycoprotein requires a novel Leu-Ile motif at a particular position in its cytoplasmic tail. J. Biol. Chem., 269, 5210-5217.
27. Ohno,H. et al. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science, 269, 1872-1875.
28. Pearse,B.M.F. (1988) Receptors compete for adaptors found in plasma membrane coated pits. EMBO J., 1, 3331-3336.
29. Pearse,B.M.F. and Robinson,M.S. (1984) Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J., 3, 1951-1957.
30. Pearse,B.M.F. and Robinson,M.S. (1990) Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol., 6, 151-171.
31. Prill,V., Lehmann,L., von Figura,K. and Peters,C. (1993) The cytoplasmic tail of lysosomal acid phosphatase contains overlapping but distinct signals for basolateral sorting and rapid internalization in polarized MDCK cells. EMBO J., 12, 2181-2193.
32. Robinson,M.S. (1987) 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J. Cell Biol., 104, 887-895.
33. Rodriguez-Boulan,E., Paskiet,K.T., Salas,P.J.I. and Bard,E. (1984) Intracellular transport of influenza virus hemagglutinin to the apical surface of MDCK cells. J. Cell Biol., 98, 308-319.
34. Roth,M.G., Compans,R.W., Giusti,L., Davis,A.R., Nayak,D.P., Gething, M.J. and Sambrook,J. (1983) Influenza virus hemagglutinin expression is polarized in cells infected with recombinant SV40 viruses carrying cloned hemagglutinin DNA. Cell, 33, 435-443.
35. Sandoval,I.V., Arredondo,J.J., Alcalde,J., Gonzalez-Noriega,A., Vandekerckhove,J., Jimenez,M.A. and Rico,M. (1994) The residues Leu(Ile)475-Ile(Leu, Val, Ala)476, contained in the extended carboxyl cytoplasmic tail, are critical for targeting of the resident lysosomal membrane protein LIMP II to lysosomes. J. Biol. Chem., 269, 6622-6631.
36. Seaman,M.N.J., Ball,C.L. and Robinson,M.S. (1993) Targeting and mistargeting of plasma membrane adaptors in vitro. J. Cell Biol., 123, 1093-1105.
37. Sorkin,A. and Carpenter,G. (1993) Interaction of activated EGF receptors with coated pit adaptins. Science, 261, 612-615.
38. Sorkin,A., McKinsey,T., Shih,W., Kirchhausen,T. and Carpenter,G. (1995) Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2. J. Biol. Chem., 270, 619-625.
39. Sosa,M.A., Schmidt,B., von Figura,K. and Hille-Rehfeld,A. (1993) In vitro binding of plasma membrane-coated vesicle adaptors to the cytoplasmic domain of lysosomal acid phosphatase. J. Biol. Chem., 268, 12537-12543.
40. Stamnes,M.A. and Rothman,J.E. (1993) The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylalion factor, a small GTP-binding protein. Cell, 73, 999-1005.
41. Traub,L.M., Ostrom,J.A. and Kornfeld,S. (1993) Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol., 123, 561-573.
42. Trowbridge,I.S., Collawn,J.F. and Hopkins,C.R. (1993) Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell Biol., 9, 129-161.
43. Wang,L.H., Rothberg,K.G. and Anderson,R.G.W. (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol., 123, 1107-1117.
44. Zhang,J.Z., Davletov,B.A., Südhof,T.C. and Anderson,R.G.W. (1994) Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell, 78, 751-760.