Utilization of the indirect lysosome targeting pathway by lysosome-associated membrane proteins (LAMPs) is influenced largely by the C-terminal residue of their GYXXΦ targeting signals

Journal of Cell Science

Volumn 112, Issue 23, 1999, Pages 4257-4269

  Gough, Nancy R ^a   Zweifel, Mark E ^a   Martinez Augustin, Olga ^a   Aguilar, Ruben C ^b   Bonifacino, Juan S ^b   Fambrough, Douglas M ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Adaptor; Endocytosis; LAMP; Lysosome; Lysosome associated membrane protein; Protein targeting

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; ASSAY; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; GENE MUTATION; HYDROPHOBICITY; IMMUNOFLUORESCENCE MICROSCOPY; INTERNALIZATION; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; BINDING SITES, ANTIBODY; BUTYRATES; CELL MEMBRANE; CYCLOHEXIMIDE; GENE EXPRESSION REGULATION; GENES, REPORTER; L CELLS (CELL LINE); LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MICE; MICROSCOPY, CONFOCAL; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

ANIMALIA; AVES;

EID: 0033491059     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (40)

1. Aguilar, R. C., Ohno, H., Roche, K. W. and Bonifacino, J. S. (1997). Functional domain mapping of the clathrin-associated adaptor medium chains mu1 and mu2. J. Biol. Chem. 272, 27160-27166.
2. Akasaki, K., Fukuzawa, M., Kinoshita, H., Furuno, K. and Tsuji, H. (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.
3. Akasaki, K., Michihara, A., Mibuka, K., Fujiwara, Y. and Tsuji, H. (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.
4. Boll, W., Ohno, H., Songyang, Z., Rapaport, I., Cantley, L. C., Bonifacino, J. S. and Kirchhausen, T. (1996). Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J. 15, 5789-5795.
5. Chen, J. W., Murphy, T. L., Willingham, M. C., Pastan, I. and August, J. T. (1985). Identification of two lysosomal membrane glycoproteins. J. Cell Biol. 101, 85-95.
6. Dell'Angelica, E. C., Klumperman, J., Stoorvogel, W. and Bonifacino, J. S. (1998). Association of the AP-3 adaptor complex with clathrin. Science 280, 431-434.
7. Dell'Angelica, E., Shotelersuk, V., Aguilar, R., Gahl, W. and Bonifacino, J. (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21.
8. Fambrough, D. M., Takeyasu, K., Lippincott-Schwarz, J. and Siegel, N. R. (1988). Structure of LEP100, a glycoprotein that shuttles between lysosomes and the plasma membrane, deduced from the nucleotide sequence of the encoding cDNA. J. Cell Biol. 106, 61-67.
9. Fukuda, M. (1991). Lysosomal membrane glycoproteins. Structure, biosynthesis and intracellular trafficking. J. Biol. Chem. 266, 21327-21330.
10. Furuno, K., Ishikawa, T., Akasaki, K., Yano, S., Tanaka, Y., Yamaguchi, Y., Tsujji, H., Himeno, M. and Kato, K. (1989a). Morphological localization of a major lysosomal membrane glycoprotein in the endocytic membrane system. J. Biochem. (Tokyo) 106, 708-716.
11. Furuno, K., Yano, S., Akasaki, K., Tanaka, Y., Yamaguchi, Y., Tsujji, H., Himeno, M. and Kato, K. (1989b). Biochemical analysis of the movement of a major lysosomal membrane glycoprotein in the endocytic membrane system. J. Biochem. (Tokyo) 106, 717-722.
12. Gough, N. R., Hatem, C. L. and Fambrough, D. M. (1995). The family of LAMP-2 proteins arises by alternative splicing from a single gene: characterization of the avian LAMP-2 gene and identification of mammalian homologs of LAMP-2b and LAMP-2c. DNA Cell Biol. 14, 863-867.
13. Gough, N. R. and Fambrough, D. M. (1997). Different steady state subcellular distributions of the three splice variants of lysosome-associated membrane protein LAMP-2 are determined largely by the COOH-terminal amino acid residue. J. Cell Biol. 137, 1161-1169.
14. Guarnieri, F. G., Arterburn, L. M., Penno, M. B., Cha, Y. and August, J. T. (1993). The motif Tyr-X-X-hydrophobic residue mediates lysosomal membrane targeting of lysosome-associated membrane protein 1. J. Biol. Chem. 268, 1941-1946.
15. Harter, C. and Mellman, I. (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.
16. Hatem, C. L., Gough, N. R. and Fambrough, D. M. (1995). Multiple mRNAs encode the avian lysosomal membrane protein LAMP-2, resulting in alternative transmembrane and cytoplasmic domains. J. Cell Sci. 108, 2093-2100.
17. Höning, S. and Hunziker, W. (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.
18. Höning, S., Griffith, J., Geuze, H. J. and Hunziker, W. (1996). The tyrosine-based lysosomal targeting signal in lamp-1 mediates sorting into Golgi-derived clathrin-coated vesicles. EMBO J 15, 5230-5239.
19. 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.
20. Hunziker, W. and Geuze, H. J. (1996). Intracellular trafficking of lysosomal membrane proteins. BioEssays 18, 379-389.
21. Konecki, D. S., Foetisch, K., Zimmer, K. P., Schlotter, M. and Lichter-Konecki, U. (1995). An alternatively spliced form of the human lysosome-associated membrane protein-2 gene is expressed in a tissue-specific manner. Biochem. Biophys. Res. Commun. 215, 757-767.
22. Kyte, J. and Doolittle, R. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
23. Le Borgne, R., Alconaca, A., Bauer, U. and Hoflack, B. (1998). The mammalian AP-3 adaptor-like complex mediates the intracellular transport of lysosomal membrane glycoproteins. J. Biol. Chem. 273, 29451-29461.
24. Lesley, J., Domingo, D., Schulte, R. and Trowbridge, I. (1984). Effect of an anti-murine transferrin receptor-ricin A conjugate on bone marrow stem and progenitor cells treated in vitro. Exp. Cell Res. 150, 400-407.
25. Lippincott-Schwartz, J. and Fambrough, D. M. (1986). Lysosomal membrane dynamics: structure and interorganellar movement of a major lysosomal membrane glycoprotein. J. Cell Biol. 102, 1593-1602.
26. Lippincott-Schwartz, J. and Fambrough, D. M. (1987). Cycling of the integral membrane glycoprotein. LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis. Cell 49, 669-677.
27. Marks, M. S., Woodruff, L., Ohno, H. and Bonifacino, J. S. (1996). Protein targeting by lyrosine- and di-leucine-based signals: evicence for distinct saturable components. J. Cell Biol. 135, 341-354.
28. Odorizzi, G., Cowles, C. and Emr, S. (1998). The AP-3 complex: a coat of many colours. Trends Cell Biol. 8, 282-288.
29. Ohno, H., Stewart, J., Fournier, M.-C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T. and Bonifacino, J. S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1874.
30. Ohno, H., Fournier, M.-C., Poy, G. and Bonifacino, J. S. (1996). Structural determinants of interaction of tyrosine-based sorting signals with the adaptor medium chains. J. Biol. Chem. 271, 29009-29015.
31. Owen, D. and Evans, R (1998). A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1127-1332.
32. Peters, C. and von Figura, K. (1994). Biogenesis of lysosomal membranes. FEBS. Lett. 346, 108-114.
33. Robinson, M. (1997). Coats and vesicle budding. Trends Cell Biol. 7, 99-102.
34. Rohrer, J., Schweizer, A., Russell, D. and Kornfeld, S. (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, 565-76.
35. Salicinski. P. R. P., McLean, C., Sykes, J. E., Clement-Jones, V. V. and Lowry, P. J. (1981). Iodinaition of proteins, glycoproteins and peptides using a solid-phase oxidising agent. 1, 3, 4, 6-tetrachloro-3α. 6α-diphenyl glycoluril (lodogen). Anal. Biochem. 117, 136-146.
36. Sandoval, I. V. and Bakke, O. (1994). Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol. 4, 292-297.
37. Sweet, R. and Eisenberg, D. (1983). Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structure. J. Mol. Biol. 171, 479-488.
38. Uthayakumar, S. and Granger, B. L. (1995). Cell surface accumulation of overexpressed hamster lysosomal membrane glycoproteins. Cell. Mol. Biol. Res. 41, 405-420.
39. Williams, M. A. and Fukuda, M. (1990). Accumulation of membrane glycoproteins in lysosomes requires a tyrosine residue at a particular position in the cytoplasmic tail. J. Cell Biol. 111, 955-66.
40. Zot, A. S. and Fambrough, D. M. (1990). Structure of a gene fora lysosomal membrane glycoprotein (LEP100). Housekeeping gene with unexpected exon organization. J. Biol. Chem. 265, 20988-20995.