In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting (original) (raw)

. 1996 Jun 3;15(11):2893–2899.

Abstract

To analyze the interaction of sorting signals with clathrin-associated adaptor complexes, we developed an in vitro assay based on surface plasmon resonance analysis. This method monitors the binding of purified adaptors to immobilized oligopeptides in real time and determines binding kinetics and affinities. A peptide corresponding to the cytoplasmic domain of wild-type influenza hemagglutinin, an apical membrane protein that is not endocytosed, did not significantly bind adaptor complexes. However, peptide sequences containing a tyrosine residue that has previously been shown to induce endocytosis and basolateral sorting were specifically recognized by adaptor complexes. The in vitro rates of adaptor association with these peptides correlated with the internalization rates of the corresponding hemagglutinin variants in vivo. Binding was observed both for purified AP-2 adaptors of the plasma membrane and for AP-1 adaptors of the Golgi, with similar apparent equilibrium dissociation constants in the range 10(-7)-10(-6) M. Adaptor binding was also demonstrated for a sequence containing a C-terminal di-leucine sequence, the second major motif of endocytosis/basolateral sorting signals. These results confirm the concept that interaction of cytoplasmic signals with plasma membrane adaptors determines the endocytosis rate of membrane proteins, and suggest the model that clathrin-coated vesicles of the trans-Golgi network are involved in basolateral sorting.

2893

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahle S., Mann A., Eichelsbacher U., Ungewickell E. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J. 1988 Apr;7(4):919–929. doi: 10.1002/j.1460-2075.1988.tb02897.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Backer J. M., Shoelson S. E., Weiss M. A., Hua Q. X., Cheatham R. B., Haring E., Cahill D. C., White M. F. The insulin receptor juxtamembrane region contains two independent tyrosine/beta-turn internalization signals. J Cell Biol. 1992 Aug;118(4):831–839. doi: 10.1083/jcb.118.4.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bansal A., Gierasch L. M. The NPXY internalization signal of the LDL receptor adopts a reverse-turn conformation. Cell. 1991 Dec 20;67(6):1195–1201. doi: 10.1016/0092-8674(91)90295-a. [DOI] [PubMed] [Google Scholar]
  4. Beltzer J. P., Spiess M. In vitro binding of the asialoglycoprotein receptor to the beta adaptin of plasma membrane coated vesicles. EMBO J. 1991 Dec;10(12):3735–3742. doi: 10.1002/j.1460-2075.1991.tb04942.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brewer C. B., Roth M. G. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol. 1991 Aug;114(3):413–421. doi: 10.1083/jcb.114.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campbell C., Squicciarini J., Shia M., Pilch P. F., Fine R. E. Identification of a protein kinase as an intrinsic component of rat liver coated vesicles. Biochemistry. 1984 Sep 11;23(19):4420–4426. doi: 10.1021/bi00314a028. [DOI] [PubMed] [Google Scholar]
  7. Davis C. G., van Driel I. R., Russell D. W., Brown M. S., Goldstein J. L. The low density lipoprotein receptor. Identification of amino acids in cytoplasmic domain required for rapid endocytosis. J Biol Chem. 1987 Mar 25;262(9):4075–4082. [PubMed] [Google Scholar]
  8. Eberle W., Sander C., Klaus W., Schmidt B., von Figura K., Peters C. The essential tyrosine of the internalization signal in lysosomal acid phosphatase is part of a beta turn. Cell. 1991 Dec 20;67(6):1203–1209. doi: 10.1016/0092-8674(91)90296-b. [DOI] [PubMed] [Google Scholar]
  9. Fire E., Gutman O., Roth M. G., Henis Y. I. Dynamic or stable interactions of influenza hemagglutinin mutants with coated pits. Dependence on the internalization signal but not on aggregation. J Biol Chem. 1995 Sep 8;270(36):21075–21081. doi: 10.1074/jbc.270.36.21075. [DOI] [PubMed] [Google Scholar]
  10. Fire E., Zwart D. E., Roth M. G., Henis Y. I. Evidence from lateral mobility studies for dynamic interactions of a mutant influenza hemagglutinin with coated pits. J Cell Biol. 1991 Dec;115(6):1585–1594. doi: 10.1083/jcb.115.6.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Futter C. E., Connolly C. N., Cutler D. F., Hopkins C. R. Newly synthesized transferrin receptors can be detected in the endosome before they appear on the cell surface. J Biol Chem. 1995 May 5;270(18):10999–11003. doi: 10.1074/jbc.270.18.10999. [DOI] [PubMed] [Google Scholar]
  12. Glickman J. N., Conibear E., Pearse B. M. Specificity of binding of clathrin adaptors to signals on the mannose-6-phosphate/insulin-like growth factor II receptor. EMBO J. 1989 Apr;8(4):1041–1047. doi: 10.1002/j.1460-2075.1989.tb03471.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hunziker W., Fumey C. A di-leucine motif mediates endocytosis and basolateral sorting of macrophage IgG Fc receptors in MDCK cells. EMBO J. 1994 Jul 1;13(13):2963–2969. doi: 10.1002/j.1460-2075.1994.tb06594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hunziker W., Harter C., Matter K., Mellman I. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell. 1991 Sep 6;66(5):907–920. doi: 10.1016/0092-8674(91)90437-4. [DOI] [PubMed] [Google Scholar]
  15. Johnson K. F., Kornfeld S. A His-Leu-Leu sequence near the carboxyl terminus of the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor is necessary for the lysosomal enzyme sorting function. J Biol Chem. 1992 Aug 25;267(24):17110–17115. [PubMed] [Google Scholar]
  16. Johnson K. F., Kornfeld S. 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):249–257. doi: 10.1083/jcb.119.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ktistakis N. T., Thomas D., Roth M. G. Characteristics of the tyrosine recognition signal for internalization of transmembrane surface glycoproteins. J Cell Biol. 1990 Oct;111(4):1393–1407. doi: 10.1083/jcb.111.4.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lazarovits J., Roth M. A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits. Cell. 1988 Jun 3;53(5):743–752. doi: 10.1016/0092-8674(88)90092-x. [DOI] [PubMed] [Google Scholar]
  19. Leitinger B., Hille-Rehfeld A., Spiess M. Biosynthetic transport of the asialoglycoprotein receptor H1 to the cell surface occurs via endosomes. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10109–10113. doi: 10.1073/pnas.92.22.10109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Letourneur F., Klausner R. D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 1992 Jun 26;69(7):1143–1157. doi: 10.1016/0092-8674(92)90636-q. [DOI] [PubMed] [Google Scholar]
  21. Mahaffey D. T., Peeler J. S., Brodsky F. M., Anderson R. G. 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):16514–16520. [PubMed] [Google Scholar]
  22. Naim H. Y., Dodds D. T., Brewer C. B., Roth M. G. 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. 1995 Jun;129(5):1241–1250. doi: 10.1083/jcb.129.5.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Naim H. Y., Roth M. G. Characteristics of the internalization signal in the Y543 influenza virus hemagglutinin suggest a model for recognition of internalization signals containing tyrosine. J Biol Chem. 1994 Feb 11;269(6):3928–3933. [PubMed] [Google Scholar]
  24. Nesterov A., Wiley H. S., Gill G. N. Ligand-induced endocytosis of epidermal growth factor receptors that are defective in binding adaptor proteins. Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8719–8723. doi: 10.1073/pnas.92.19.8719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ogata S., Fukuda M. Lysosomal targeting of Limp II membrane glycoprotein requires a novel Leu-Ile motif at a particular position in its cytoplasmic tail. J Biol Chem. 1994 Feb 18;269(7):5210–5217. [PubMed] [Google Scholar]
  26. Ohno H., Stewart J., Fournier M. C., Bosshart H., Rhee I., Miyatake S., Saito T., Gallusser A., Kirchhausen T., Bonifacino J. S. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science. 1995 Sep 29;269(5232):1872–1875. doi: 10.1126/science.7569928. [DOI] [PubMed] [Google Scholar]
  27. Pearse B. M. Receptors compete for adaptors found in plasma membrane coated pits. EMBO J. 1988 Nov;7(11):3331–3336. doi: 10.1002/j.1460-2075.1988.tb03204.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pearse B. M., Robinson M. S. Clathrin, adaptors, and sorting. Annu Rev Cell Biol. 1990;6:151–171. doi: 10.1146/annurev.cb.06.110190.001055. [DOI] [PubMed] [Google Scholar]
  29. Pearse B. M., Robinson M. S. Purification and properties of 100-kd proteins from coated vesicles and their reconstitution with clathrin. EMBO J. 1984 Sep;3(9):1951–1957. doi: 10.1002/j.1460-2075.1984.tb02075.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Prill V., Lehmann L., von Figura K., Peters C. The cytoplasmic tail of lysosomal acid phosphatase contains overlapping but distinct signals for basolateral sorting and rapid internalization in polarized MDCK cells. EMBO J. 1993 May;12(5):2181–2193. doi: 10.1002/j.1460-2075.1993.tb05866.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Robinson M. S. 100-kD coated vesicle proteins: molecular heterogeneity and intracellular distribution studied with monoclonal antibodies. J Cell Biol. 1987 Apr;104(4):887–895. doi: 10.1083/jcb.104.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rodriguez-Boulan E., Paskiet K. T., Salas P. J., Bard E. Intracellular transport of influenza virus hemagglutinin to the apical surface of Madin-Darby canine kidney cells. J Cell Biol. 1984 Jan;98(1):308–319. doi: 10.1083/jcb.98.1.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Roth M. G., Compans R. W., Giusti L., Davis A. R., Nayak D. P., Gething M. J., Sambrook J. Influenza virus hemagglutinin expression is polarized in cells infected with recombinant SV40 viruses carrying cloned hemagglutinin DNA. Cell. 1983 Jun;33(2):435–443. doi: 10.1016/0092-8674(83)90425-7. [DOI] [PubMed] [Google Scholar]
  34. Sandoval I. V., Arredondo J. J., Alcalde J., Gonzalez Noriega A., Vandekerckhove J., Jimenez M. A., Rico M. 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. 1994 Mar 4;269(9):6622–6631. [PubMed] [Google Scholar]
  35. Seaman M. N., Ball C. L., Robinson M. S. Targeting and mistargeting of plasma membrane adaptors in vitro. J Cell Biol. 1993 Dec;123(5):1093–1105. doi: 10.1083/jcb.123.5.1093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sorkin A., Carpenter G. Interaction of activated EGF receptors with coated pit adaptins. Science. 1993 Jul 30;261(5121):612–615. doi: 10.1126/science.8342026. [DOI] [PubMed] [Google Scholar]
  37. Sorkin A., McKinsey T., Shih W., Kirchhausen T., Carpenter G. Stoichiometric interaction of the epidermal growth factor receptor with the clathrin-associated protein complex AP-2. J Biol Chem. 1995 Jan 13;270(2):619–625. doi: 10.1074/jbc.270.2.619. [DOI] [PubMed] [Google Scholar]
  38. Sosa M. A., Schmidt B., von Figura K., Hille-Rehfeld A. In vitro binding of plasma membrane-coated vesicle adaptors to the cytoplasmic domain of lysosomal acid phosphatase. J Biol Chem. 1993 Jun 15;268(17):12537–12543. [PubMed] [Google Scholar]
  39. Stamnes M. A., Rothman J. E. 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. doi: 10.1016/0092-8674(93)90277-w. [DOI] [PubMed] [Google Scholar]
  40. Traub L. M., Ostrom J. A., Kornfeld S. Biochemical dissection of AP-1 recruitment onto Golgi membranes. J Cell Biol. 1993 Nov;123(3):561–573. doi: 10.1083/jcb.123.3.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Trowbridge I. S., Collawn J. F., Hopkins C. R. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu Rev Cell Biol. 1993;9:129–161. doi: 10.1146/annurev.cb.09.110193.001021. [DOI] [PubMed] [Google Scholar]
  42. Wang L. H., Rothberg K. G., Anderson R. G. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J Cell Biol. 1993 Dec;123(5):1107–1117. doi: 10.1083/jcb.123.5.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zhang J. Z., Davletov B. A., Südhof T. C., Anderson R. G. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell. 1994 Sep 9;78(5):751–760. doi: 10.1016/s0092-8674(94)90442-1. [DOI] [PubMed] [Google Scholar]