Cysteine34 of the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor is reversibly palmitoylated and required for normal trafficking and lysosomal enzyme sorting

Journal of Cell Biology

Volumn 132, Issue 4, 1996, Pages 577-584

  Schweizer, Anja ^a   Kornfeld, Stuart ^a   Rohrer, Jack ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; CATHEPSIN D; CATION; CYSTEINE; LYSOSOME ENZYME; METHIONINE; PALMITIC ACID; SOMATOMEDIN B RECEPTOR; THIOESTER; CELL SURFACE RECEPTOR; LECTIN; MANNOSE BINDING LECTIN; MANNOSE PHOSPHATE; MANNOSE RECEPTOR; PALMITIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; CYTOPLASM; FLUOROGRAPHY; IMMUNOPRECIPITATION; LIPID BILAYER; LYSOSOME; MOUSE; MUTATION; NONHUMAN; PALMITOYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; GENE TRANSFER; GENETICS; METABOLISM; MOLECULAR GENETICS; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALIA;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CATIONS; CELL LINE; CYSTEINE; GENE TRANSFER TECHNIQUES; LECTINS, C-TYPE; LYSOSOMES; MANNOSE-BINDING LECTINS; MANNOSEPHOSPHATES; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PALMITATES; RECEPTORS, CELL SURFACE;

EID: 0029670903     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.132.4.577     Document Type: Article

References (42)

1. Balch, W.E., and J.E. Rothman. 1985. Characterization of protein transport between successive compartments of the Golgi apparatus: asymmetric properties of donor and acceptor activities in a cell-free system Arch Biochem. Biophys 240.413-425.
2. Crise, B., and J.K Rose. 1992. Identification of palmitoylation sites on CD4, the human immunodeficiency virus receptor. J. Biol Chem. 267:13593-13597
3. Faust. P.L , D.A Wall, E. Perara, V R. Lingappa, and S. Kornfeld 1987. Expression of human cathepsin D in Xenopus oocytes: phosphorylation and intracellular targeting. J. Cell Biol. 105:1937-1945.
4. Gabel, C.A , D.E. Goldberg, and S. Kornfeld 1983. Identification and characterization of cells deficient in the mannose 6-phosphate receptor: evidence for an alternate pathway for lysosomal enzyme targeting. Proc. Natl. Acad. Sci. USA. 80:775-779.
5. 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.
6. Hancock, J.F., A.I. Magee, J.E. Childs, and C.J. Marshall. 1989. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 57:1167-1177.
7. Hille-Rehfeld, A. 1995. Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta. 1241:177-194.
8. Ho, S.N , H.D. Hunt, R M Horton, J.K. Pullen, and L.R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene (Amst.) 77:51-59.
9. Jing, S.Q , and I.S. Trowbridge. 1987. Identification of the intermolecular disulfide bonds of the human transferrin receptor and its lipid-attachment site. EMBO (Eur. Mol. Biol Organ.) J. 6:327-331.
10. Jing, S.Q., and I.S. Trowbridge. 1990. Nonacylated human transferrin receptors are rapidly internalized and mediate iron uptake. J. Biol Chem. 265:11555-11559.
11. Johnson, K.F., and S. Kornfeld. 1992. 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. 267:17110-17115.
12. Johnson, K.F , W. Chan, and S. Kornfeld. 1990. Cation-dependent mannose 6-phosphate receptor contains two internalization signals in its cytoplasmic domain. Proc. Natl. Acad. Sci. USA 87:10010-10014.
13. Karnik, S.S., K.D. Ridge, S. Bhattacharya, and H.G. Khorana. 1993. Palmitoylation of bovine opsin and its cysteine mutants in COS cells. Proc. Natl Acad. Sci. USA. 90:40-44.
14. Kaufman, J.F., M.S. Krangel, and J.L. Strominger. 1984. Cysteines in the transmembrane region of major histocompatibility complex antigens are fatty acylated via thioester bonds. J. Biol. Chem. 259:7230-7238.
15. Kawate, N., and K.M. Menon. 1994. Palmitoylation of luteinizing hormone/human chonogonadotropin receptors in transfected cells. Abolition of palmitoylation by mutation of Cys-621 and Cys-622 residues in the cytoplasmic tail increases ligand-induced internalization of the receptor. J. Biol Chem. 269: 30651-30658
16. Koch, N., and G.J. Hammerling 1986. The HLA-D-associated invariant chain binds palmitic acid at the cysteine adjacent to the membrane segment J. Biol Chem. 261:3434-3440
17. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5:483-525.
18. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature (Lond.). 227:680-685.
19. Liu, Y., D.A. Fisher, and D.R. Storm. 1993. Analysis of the palmitoylation and membrane targeting domain of neuromodulin (GAP-43) by site-specific mutagenesis. Biochemistry. 32:10714-10719.
20. Ludwig, T., R. LeBorgne, and B. Hoflack. 1995. Rules for mannose 6-phosphate receptors in lysosomal enzyme sorting, IGF-II binding and clathrin coat assembly. Trends Cell Biol. 5:202-206.
21. Ma, Z.M., J.H. Grubb, and W.S. Sly. 1991. Cloning, sequencing, and functional characterization of the murine 46-kDa mannose 6-phosphate receptor. J. Biol. Chem 266 10589-10595.
22. Magee, A.I., L. Gutierrez, I.A. McKay, C.J Marshall, and A. Hall. 1987. Dynamic fatty acylation of p21N-ras. EMBO (Eur. Mol. Biol. Organ) J. 6:3353-3357.
23. Messner, D.J. 1993. The mannose receptor and the cation-dependent form of mannose 6-phosphate receptor have overlapping cellular and subcellular distributions in liver. Arch. Biochem Biophys 306:391-401.
24. O'Brien, P.J., R.S. St. Jules, T.S. Reddy, N.G. Bazan, and M. Zatz. 1987. Acylation of disc membrane rhodopsin may be nonenzymatic. J. Biol. Chem 262: 5210-5215.
25. O'Dowd, B.F., M. Hnatowich, M G. Caron, R.J. Lefkowitz, and M. Bouvier, 1989. Palmitoylation of the human β 2-adrenergic receptor. Mutation of Cys341 in the carboxyl tail leads to an uncoupled nonpalmitoylated form of the receptor. J. Biol Chem. 264.7564-7569.
26. Omary, M.B., and I.S. Trowbridge 1981. Biosynthesis of the human transferrin receptor in cultured cells. J. Biol. Chem. 256:12888-12892.
27. Ovchinnikov, Y.U.A., N.G. Abdulaev, and A.S. Bogachuk. 1988. Two adjacent cysteine residues in the C-terminal cytoplasmic fragment of bovine rhodopsin are palmitoylated. FEBS Lett. 230:1-5.
28. Papac, D.I., K.R. Thornburg, E.E. Bullesbach, R K. Crouch, and D.R. Knapp. 1992. Palmitoylation of a G-protein coupled receptor. Direct analysis by tandem mass spectrometry. J. Biol. Chem. 267:16889-16894.
29. Rohrer, J., A. Schweizer, K.F. Johnson, and S. Kornfeld. 1995. A determinant in the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor prevents trafficking to lysosomes. J. Cell Biol. 130:1297-1306
30. Rose, J.K , G.A. Adams, and C.J Gallione. 1984. The presence of cysteine in the cytoplasmic domain of the vesicular stomatitis virus glycoprotein is required for palmitate addition Proc. Natl. Acad. Sci. USA. 81:2050-2054
31. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
32. Schlesinger, M.J., A.I Magee, and M.F. Schmidt. 1980. Fatty acid acylation of proteins in cultured cells. J Biol Chem. 255:10021-10024.
33. Schweizer, A., J. Rohrer, and S. Kornfeld 1995. Determination of the structural requirements for palmitoylation of p63. J. Biol Chem. 270:9638-9644
34. Sefton, B.M., and J.E. Buss. 1987. The covalent modification of eukaryotic proteins with lipid. J Cell Biol. 104:1449-1453.
35. Skene, J.H., and I. Virag. 1989. Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J. Cell Biol. 108:613-624.
36. Staufenbiel, M. 1987. Ankyrin-bound fatty acid turns over rapidly at the erythrocyte plasma membrane. Mol. Cell. Biol. 7:2981-2984.
37. Stein, M., H.E. Meyer, A. Hasilik, and K. von Figura 1987 46-kDa mannose 6-phosphate-specific receptor: purification, subunit composition, chemical modification. Biol. Chem. Hoppe. Seyler. 368:927-936.
38. Towbin, H , T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and applications. Proc. Natl. Acad. Sci. USA. 70:4350-4354.
39. Veit, M , E. Kretzschmar, K. Kuroda, W. Garten, M.F. Schmidt, H.D. Klenk, and R. Rott. 1991. Site-specific mutagenesis identifies three cysteine residues in the cytoplasmic tail as acylation sites of influenza virus hemagglutinin. J. Virol. 65:2491-2500.
40. Wedegaertner, P.B., D.H. Chu, P.T. Wilson, M.J. Levis, and H.R. Bourne, 1993. Palmitoylation is required for signaling functions and membrane attachment of Gq α and Gs α. J. Biol. Chem. 268:25001-25008
41. Westcott, K R., and L.H. Rome. 1988. Cation-independent mannose 6-phosphate receptor contains covalently bound fatty acid. J. Cell. Biochem. 38:23-33.
42. Zuber, M.X., S.M. Strittmatter, and M.C Fishman. 1989. A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43. Nature (Lond.). 341.345-348.