An α-helical signal in the cytosolic domain of the interleukin 2 receptor β chain mediates sorting towards degradation after endocytosis

Journal of Cell Biology

Volumn 136, Issue 3, 1997, Pages 583-595

  Subtil, Agathe ^a   Delepierre, Muriel ^b   Dautry Varsat, Alice ^a,b  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2 RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; BETA CHAIN; CIRCULAR DICHROISM; ENDOCYTOSIS; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; AMINO ACIDS; CELL MEMBRANE; CLATHRIN; CYTOSOL; ENDOCYTOSIS; HELA CELLS; HELIX-TURN-HELIX MOTIFS; HUMANS; MOLECULAR SEQUENCE DATA; RECEPTORS, INTERLEUKIN-2; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TIME FACTORS; TRANSFERRIN; TUMOR CELLS, CULTURED;

EID: 0031045008     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.136.3.583     Document Type: Article

References (61)

1. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1993. Current Protocols in Molecular Biology. K. Janssen, editor. Wiley, J. & Sons, Inc.
2. Aiken, C., J. Konner, N.R. Landau, M.E. Lenburg, and D. Trono, 1994. Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell. 76:853-864.
3. Aniento, F., F. Gu, R.G. Parton, and J. Gruenberg. 1996. An endosomal βCOP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133:29-41.
4. Bansal, A., and L.M. Gierasch. 1991. The NPXY internalization signal of the LDL receptor adopts a reverse-turn conformation. Cell. 67:1195-1201.
5. Bazan, J.F. 1990. Haemopoietic receptors and helical cytokines. Immunology Today. 11:350-354.
6. Bothner-By, A., R.L. Stephens, and J.-M. Lee. 1984. Structure determination of a tetrasaccharide: transient nuclear overhauser effects in the rotating frame. J. Am. Chem. Soc. 106:811-813.
7. Braun, M., A. Waheed, and K. von Figura. 1989. Lysosomal acid phosphatase is transported to lysosomes via the cell surface. EMBO (Eur. Mol. Biol. Organ.) J. 8:3633-3640.
8. Collawn, J.F., M. Stangel, L.A. Kuhn, V. Esekogwu, S. Jing, I.S. Trowbridge, and J.A. Tainer. 1990. Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell. 63:1061-1072.
9. DiSanto, J.P., A. Dautry-Varsat, S. Certain, A. Fischer, and G. de Saint Basile. 1994. IL-2Rγ chain mutations in SCIDX1 result in the loss of high-affinity IL-2 receptor binding. Eur. J. Immunol. 24:475-479.
10. DiSanto, J.P., F. Rieux-Laucat, A. Dautry-Varsat, A. Fischer, and G. de Saint Basile. 1994. Defective human interleukin 2 receptor γ chain in an atypical X chromosome-linked severe combined immunodeficiency with peripheral T cells. Proc. Natl. Acad. Sci. USA. 91:9466-9470.
11. Duprez, V., and A. Dautry-Varsat. 1986. Receptor mediated endocytosis of interleukin 2 in a human tumor T cell line: degradation of interleukin 2 and evidence for the absence of recycling of interleukin 2 receptors. J. Biol. Chem. 261:15450-15454.
12. Duprez, V., V. Cornet, and A. Dautry-Varsat. 1988. Down regulation of high affinity interleukin 2 receptors in a human tumor T cell line: IL2 increases the rate of surface receptor decay. J. Biol. Chem. 263:12860-12865.
13. Dyson, H.J., M. Rance, R.A. Houghten, R.A. Lerner, and P.E. Wright. 1988. Folding of immunogenic peptide fragments of proteins in water solution. J. Mol. Biol. 201:161-200.
14. Eberle, W., C. Sander, W. Klaus, B. Schmidt, K. von Figura, and C. Peters. 1991. The essential tyrosine of the internalization signal in lysosomal acid phosphatase is part of a β turn. Cell. 67:1203-1209.
15. Green, S.A., H. Setiadi, R.P. McEver, and R.B. Kelly. 1994. The cytoplasmic domain of P-selectin contains a sorting determinant that mediates rapid degradation in lysosomes. J. Cell Biol. 124:435-448.
16. 1H spin system identification in macromolecules. J. Am. Chem. Soc. 110:7870-7872.
17. Grote, E., J.C. Hao, M.K. Bennett, and R.B. Kelly. 1995. A targeting signal in VAMP regulating transport to synaptic vesicles. Cell. 81:581-589.
18. Gruenberg, J., and F.R. Maxfield. 1995. Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7:552-563.
19. Hansen, S.H., K. Sandvig, and B. van Deurs. 1993. Molecules internalized by clathrin-independent endocytosis are delivered to endosomes containing transferrin receptors. J. Cell Biol. 123:89-97.
20. Harter, C., and I. Mellman. 1992. Transport of the lysosomal membrane glycoprotein Igp120 (Igp-A) to lysosomes does not require appearance on the plasma membrane. J. Cell Biol. 117:311-325.
21. Hémar, A., and A. Dautry-Varsat. 1990. Cyclosporin A inhibits the interleukin 2 receptor a chain gene transcription but not its cell surface expression: the a chain stability can explain this discrepancy. Eur. J. Immunol. 20:2629-2635.
22. Hémar, A., M. Lieb, A. Subtil, J.P. DiSanto, and A. Dautry-Varsat. 1994. Endocytosis of the β chain of interleukin 2 receptor requires neither interleukin 2 nor the γ chain. Eur. J. Immunol. 24:1951-1955.
23. Hémar, A., A. Subtil, M. Lieb, E. Morelon, R. Hellio, and A. Dautry-Varsat. 1995. Endocytosis of interleukin 2 receptors in human T lymphocytes: distinct intracellular localization and fate of the receptor α, β, and γ chains. J. Cell Biol. 129:55-64.
24. Höning, S., and W. Hunziker. 1995. Cytoplasmic determinants involved in direct lysosomal sorting, endocytosis, and basolateral targeting of rat Igp120 (lamp-1) in MDCK cells. J. Cell Biol. 128:321-332.
25. Huang, Z., Y. Chen, and R.A. Nissenson. 1995. The cytoplasmic tail of the G-protein-coupled receptor for parathyroid hormone and parathyroid hormone-related protein contains positive and negative signals for endocytosis. J. Biol. Chem. 270:151-156.
26. Hunziker, W., and H.J. Geuze. 1996. Intracellular trafficking of lysosomal membrane proteins. BioEssays. 18:379-389.
27. Jing, S., T. Spencer, K. Miller, C. Hopkins, and I.S. Trowbridge. 1990. Role of the human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J. Cell Biol. 110:283-294.
28. Lamaze, C., and S.L. Schmid. 1995. The emergence of clathrin-independent pinocytic pathways. Curr. Opin. Cell Biol. 7:573-580.
29. Letourneur, F., and R.D. Klausner. 1992. A novel di-leucine motif and a tyrosine based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 69:1143-1157.
30. Macura, S., and R.R. Ernst. 1980. Elucidation of cross relaxation in liquids by two-dimensional N.M.R. spectroscopy. Mol. Phys. 41:95-117.
31. Mallabiabarrena, A., M.A. Jiménez, M. Rico, and B. Alarcon. 1995. A tyrosine-containing motif mediates ER retention of CD3∈ and adopts a helix-turn structure. EMBO (Eur. Mol. Biol. Organ.) J. 14:2257-2268.
32. Marks, M.S., P.A. Roche, E. van Donselaar, L. Woodruff, P.J. Peters, and J.S. Bonifacino. 1995. A lysosomal targeting signal in the cytoplasmic tail of the β chain directs HLA-DM to MHC class II compartments. J. Cell Biol. 131:351-369.
33. Mathews, P.M., J.B. Martinie, and D.M. Fambrough. 1992. The pathway and targeting signal for delivery of the integral membrane glycoprotein LEP100 to lysosomes. J. Cell Biol. 118:1027-1040.
34. Mayor, S., J.F. Presley, and F.R. Maxfield. 1993. Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process. J. Cell Biol. 121:1257-1269.
35. Merrifield, R.B. 1963. Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J. Am. Chem. Soc. 85:2149-2154.
36. Minami, Y., T. Kono, T. Miyazaki, and T. Taniguchi. 1993. The IL2 receptor complex: its structure, function, and target genes. Annu. Rev. Immunol. 11:245-267.
37. Minamoto, S., H. Mori, M. Hatakeyama, T. Kono, T. Doi, T. Ide, T. Uede, and T. Taniguchi. 1990. Characterization of the heterodimeric complex of human IL2 receptor α β chains reconstituted in a mouse fibroblast cell line, L929. J. Immunol. 145:2177-2182.
38. Motta, A., B. Bremnes, M.A. Castiglione Morelli, R.W. Frank, G. Saviano, and O. Bakke. 1995. Structure-activity relationship of the leucine-based sorting motifs in the cytosolic tail of the major histocompatibility complex-associated invariant chain. J. Biol. Chem. 270:27165-27171.
39. Nelson, J.W., and N.R. Kallenbach. 1986. Stabilization of the ribonuclease S-peptide α-helix by trifluoroethanol. Proteins. 1:211-217.
40. Noguchi, M., H. Yi, H.M. Rosenblatt, A.H. Filipovich, S. Adelstein, W.S. Modi, O.W. McBride, and W.J. Leonard. 1993. Interleukin-2 receptor γ chain mutation results in X-linked severe combined immunodeficiency in humans. Cell. 73:147-157.
41. Odorizzi, C.G., I.S. Trowbridge, L. Xue, C. Hopkins, C.D. Davis, and J.F. Collawn. 1994. Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment. J. Cell Biol. 126:317-330.
42. Padmanabhan, S., S. Marqusee, T. Ridgeway, T.M. Laue, and R.L. Baldwin. 1990. Relative helix-forming tendencies of nonpolar amino acids. Nature (Lond.). 344:268-270.
43. Peters, C., M. Braun, B. Weber, M. Wendland, B. Schmidt, R. Pohlmann, A. Waheed, and K. von Figura. 1990. Targeting of a lysosomal membrane protein: a tyrosine-containing endocytosis signal in the cytoplasmic tail of lysosomal acid phosphatase is necessary and sufficient for targeting to lysosomes. EMBO (Eur. Mol. Biol. Organ.) J. 9:3497-3506.
44. 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117:479-485.
45. Robinson, M.S. 1994. The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6:538-544.
46. Robinson, M.S., C. Watts, and M. Zerial. 1996. Membrane dynamics in endocytosis. Cell. 84:13-21.
47. Rohrer, J., A. Schweizer, D. Russell, and S. Kornfeld. 1996. 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. 132:565-576.
48. Rubin, L.A., C.C. Kutman, M.E. Fritz, W.E. Biddison, B. Boutin, R. Yarchoan, and D.L. Nelson. 1985. Soluble interleukin 2 receptors are released from activated human lymphoid cells in vitro. J. Immunol. 135:3172-3177.
49. Sandoval, I.V., and O. Bakke. 1994. Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4:292-297.
50. States, D.J., R.A. Haberkorn, and D.J. Ruben. 1982. A two-dimensional nuclear overhauser experiment with pure absorption phase in four quadrants. J. Magn. Reson. 48:286-292.
51. Subtil, A., A. Hémar, and A. Dautry-Varsat. 1994. Rapid endocytosis of interleukin 2 receptors when clathrin-coated pit endocytosis is inhibited. J. Cell Sci. 107:3461-3468.
52. Sugamura, K., H. Asao, M. Kondo, N. Tanaka, N. Ishii, K. Ohbo, M. Nakamura, and T. Takeshita. 1996. The interleukin 2 receptor γ chain: its role in the multiple cytokine receptor complexes and T cell development in XSCID. Annu. Rev. Immunol. 14:179-205.
53. Sutherland, R., D. Delia, C. Schneider, R. Newman, J. Kemshead, and M. Greaves. 1981. Ubiquitous cell-surface glycoprotein on tumor cells is proliferation-associated receptor for transferrin. Immunology. 78:4515-4519.
54. Trowbridge, I.S., and C.R. Hopkins. 1993. Signal-dependent membrane protein trafficking in the endocytic pathway. Annu. Rev. Cell. Biol. 9:129-161.
55. Vijayasaradhi, S., Y. Xu, B. Bouchard, and A.N. Houghton. 1995. Intracellular sorting and targeting of melanosomal membrane proteins: identification of signals for sorting of the human brown locus protein, GP75. J. Cell Biol. 130:807-820.
56. Voss, S.D., T.P. Leary, P.M. Sondel, and R.J. Robb. 1993. Identification of a direct interaction between interleukin 2 and the p64 interleukin 2 receptor γ chain. Proc. Natl. Acad. Sci. USA. 90:2428-2432.
57. 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.
58. Wilde, A., C. Dempsey, and G. Banting. 1994. The tyrosine-containing internalization motif in the cytoplasmic domain of TGN38/41 lies within a nascent helix. J. Biol. Chem. 269:7131-7136.
59. Williams, M.A., and M. Fukuda. 1990. Accumulation of membrane glycoproteins in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J. Cell Biol. 111:955-966.
60. Wishart, D.S., B.D. Sykes, and P.M. Richards. 1991. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222:311-333.
61. Zwart, D.E., C.B. Brewer, J. Lazarovits, Y.I. Henis, and M.G. Roth. 1996. Degradation of mutant influenza virus hemagglutinins is influenced by cytoplasmic sequences independent of internalization signals. J. Biol. Chem. 271:907-917.