Structural basis for the recognition of tyrosine-based sorting signals by the μ3A subunit of the AP-3 adaptor complex

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 9563-9571

  Mardones, Gonzalo A ^a,b   Burgos, Patricia V ^a,b   Lin, Yimo ^b   Kloer, Daniel P ^c,d   Magadán, Javier G ^b   Hurley, James H ^c   Bonifacino, Juan S ^b  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

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

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^d JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL ANALYSIS; C-TERMINAL DOMAINS; INTRACELLULAR MEMBRANES; PHOSPHOINOSITIDES; SURFACE ELECTROSTATIC POTENTIAL; TRANS-GOLGI NETWORK PROTEINS; TRANS-MEMBRANE PROTEINS; X-RAY CRYSTALLOGRAPHIC ANALYSIS;

AMINO ACIDS; CELL MEMBRANES; COMPLEX NETWORKS; PHOSPHOLIPIDS; PROTEINS; X RAY CRYSTALLOGRAPHY;

BINDING SITES;

ADAPTOR PROTEIN; ADAPTOR PROTEIN 3 MU3A SUBUNIT; ALANINE; ASPARAGINE; CD63 ANTIGEN; CELL PROTEIN; LEUCINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PHENYLALANINE; SERINE; TRANS GOLGI NETWORK 38 PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN TARGETING; RAT; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ADAPTOR PROTEIN COMPLEX 3; ADAPTOR PROTEIN COMPLEX MU SUBUNITS; AMINO ACID SEQUENCE; ANIMALS; CALORIMETRY; CLATHRIN; ENDOSOMES; HUMANS; IMMUNOGLOBULINS; LYSOSOMES; MICE; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; RATS; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; TYROSINE;

EID: 84875971537     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.450775     Document Type: Article

References (48)

1. Kirchhausen, T., Bonifacino, J. S., and Riezman, H. (1997) Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol. 9, 488-495
2. Bonifacino, J. S., and Traub, L. M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447
3. Canfield, W. M., Johnson, K. F., Ye, R. D., Gregory, W., and Kornfeld, S. (1991) Localization of the signal for rapid internalization of the bovine cation-independent mannose 6-phosphate/insulin-like growth factor-II receptor to amino acids 24-29 of the cytoplasmic tail. J. Biol. Chem. 266, 5682-5688
4. Collawn, J. F., Stangel, M., Kuhn, L. A., Esekogwu, V., Jing, S. Q., Trowbridge, I. S., and Tainer, J. A. (1990) Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 63, 1061-1072
5. 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
6. Höning, S., and Hunziker, W. (1995) Cytoplasmic determinants involved in direct lysosomal sorting, endocytosis, and basolateral targeting of rat lgp120 (lamp-I) in MDCK cells. J. Cell Biol. 128, 321-332
7. Farías, G. G., Cuitino, L., Guo, X., Ren, X., Jarnik, M., Mattera, R., and Bonifacino, J. S. (2012) Signal-mediated, AP-1/clathrin-dependent sorting of transmembrane receptors to the somatodendritic domain of hippocampal neurons. Neuron 75, 810-823
8. 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, 1872-1875
9. Ohno, H., Aguilar, R. C., Yeh, D., Taura, D., Saito, T., and Bonifacino, J. S. (1998) The medium subunits of adaptor complexes recognize distinct but overlapping sets of tyrosine-based sorting signals. J. Biol. Chem. 273, 25915-25921
10. Stephens, D. J., and Banting, G. (1998) Specificity of interaction between adaptor-complex medium chains and the tyrosine-based sorting motifs of TGN38 and lgp120. Biochem. J. 335, 567-572
11. Hirst, J., Bright, N. A., Rous, B., and Robinson, M. S. (1999) Characterization of a fourth adaptor-related protein complex. Mol. Biol. Cell 10, 2787-2802
12. Aguilar, R. C., Boehm, M., Gorshkova, I., Crouch, R. J., Tomita, K., Saito, T., Ohno, H., and Bonifacino, J. S. (2001) Signal-binding specificity of the mu4 subunit of the adaptor protein complex AP-4. J. Biol. Chem. 276, 13145-13152
13. Aguilar, R. C., Ohno, H., Roche, K. W., and Bonifacino, J. S. (1997) Functional domain mapping of the clathrin-associated adaptor medium chains μ1 and μ2. J. Biol. Chem. 272, 27160-27166
14. Hirst, J., Barlow, L. D., Francisco, G. C., Sahlender, D. A., Seaman, M. N., Dacks, J. B., and Robinson, M. S. (2011) The fifth adaptor protein complex. PLoS Biol. 9, e1001170
15. Cosson, P., Démollière, C., Hennecke, S., Duden, R., and Letourneur, F. (1996) δ- and ζ-COP, two coatomer subunits homologous to clathrinassociated proteins, are involved in ER retrieval. EMBO J. 15, 1792-1798
16. Martina, J. A., Bonangelino, C. J., Aguilar, R. C., and Bonifacino, J. S. (2001) Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J. Cell Biol. 153, 1111-1120
17. Walther, K., Krauss, M., Diril, M. K., Lemke, S., Ricotta, D., Honing, S., Kaiser, S., and Haucke, V. (2001) Human stoned B interacts with AP-2 and synaptotagmin and facilitates clathrin-coated vesicle uncoating. EMBO Rep. 2, 634-640
18. Reider, A., Barker, S. L., Mishra, S. K., Im, Y. J., Maldonado- Báez, L., Hurley, J. H., Traub, L. M., and Wendland, B. (2009) Syp1 is a conserved endocytic adaptor that contains domains involved in cargo selection and membrane tubulation. EMBO J. 28, 3103-3116
19. Umasankar, P. K., Sanker, S., Thieman, J. R., Chakraborty, S., Wendland, B., Tsang, M., and Traub, L. M. (2012) Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning. Nat. Cell Biol. 14, 488-501
20. Owen, D. J., and Evans, P. R. (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282, 1327-1332
21. Burgos, P. V., Mardones, G. A., Rojas, A. L., daSilva, L. L., Prabhu, Y., Hurley, J. H., and Bonifacino, J. S. (2010) Sorting of the Alzheimer's disease amyloid precursor protein mediated by the AP-4 complex. Dev. Cell 18, 425-436
22. Jia, X., Singh, R., Homann, S., Yang, H., Guatelli, J., and Xiong, Y. (2012) Structural basis of evasion of cellular adaptive immunity by HIV-1 Nef. Nat. Struct. Mol. Biol. 19, 701-706
23. 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
24. Dell'Angelica, E. C., Ohno, H., Ooi, C. E., Rabinovich, E., Roche, K. W., and Bonifacino, J. S. (1997) AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J. 16, 917-928
25. 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
26. Peden, A. A., Oorschot, V., Hesser, B. A., Austin, C. D., Scheller, R. H., and Klumperman, J. (2004) Localization of the AP-3 adaptor complex defines a novel endosomal exit site for lysosomal membrane proteins. J. Cell Biol. 164, 1065-1076
27. Sheffield, P., Garrard, S., and Derewenda, Z. (1999) Overcoming expression and purification problems of RhoGDI using a family of "parallel" expression vectors. Protein Expr. Purif. 15, 34-39
28. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 276, 307-326
29. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
30. Heldwein, E. E., Macia, E., Wang, J., Yin, H. L., Kirchhausen, T., and Harrison, S. C. (2004) Crystal structure of the clathrin adaptor protein 1 core. Proc. Natl. Acad. Sci. U.S.A. 101, 14108-14113
31. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
32. Collins, B. M., McCoy, A. J., Kent, H. M., Evans, P. R., and Owen, D. J. (2002) Molecular architecture and functional model of the endocytic AP2 complex. Cell 109, 523-535
33. Kelly, B. T., McCoy, A. J., Späte, K., Miller, S. E., Evans, P. R., Höning, S., and Owen, D. J. (2008) A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456, 976-979
34. Jackson, L. P., Kelly, B. T., McCoy, A. J., Gaffry, T., James, L. C., Collins, B. M., Höning, S., Evans, P. R., and Owen, D. J. (2010) A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex. Cell 141, 1220-1229
35. Rohde, G., Wenzel, D., and Haucke, V. (2002) A phosphatidylinositol (4,5)-bisphosphate binding site within μ2-adaptin regulates clathrin-mediated endocytosis. J. Cell Biol. 158, 209-214
36. Wang, Y. J., Wang, J., Sun, H. Q., Martinez, M., Sun, Y. X., Macia, E., Kirchhausen, T., Albanesi, J. P., Roth, M. G., and Yin, H. L. (2003) Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299-310
37. Baust, T., Anitei, M., Czupalla, C., Parshyna, I., Bourel, L., Thiele, C., Krause, E., and Hoflack, B. (2008) Protein networks supporting AP-3 function in targeting lysosomal membrane proteins. Mol. Biol. Cell 19, 1942-1951
38. Dell'Angelica, E. C., Shotelersuk, V., Aguilar, R. C., Gahl, W. A., and Bonifacino, J. S. (1999) Altered trafficking of lysosomal proteins in Hermansky- Pudlak syndrome due to mutations in the μ 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21
39. Janvier, K., and Bonifacino, J. S. (2005) Role of the endocytic machinery in the sorting of lysosome-associated membrane proteins. Mol. Biol. Cell 16, 4231-4242
40. Feng, L., Seymour, A. B., Jiang, S., To, A., Peden, A. A., Novak, E. K., Zhen, L., Rusiniak, M. E., Eicher, E. M., Robinson, M. S., Gorin, M. B., and Swank, R. T. (1999) The μ3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky- Pudlak syndrome and night blindness. Hum. Mol. Genet. 8, 323-330
41. Kantheti, P., Qiao, X., Diaz, M. E., Peden, A. A., Meyer, G. E., Carskadon, S. L., Kapfhamer, D., Sufalko, D., Robinson, M. S., Noebels, J. L., and Burmeister, M. (1998) Mutation in AP-3 δ in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21, 111-122
42. Mullins, C., Hartnell, L. M., Wassarman, D. A., and Bonifacino, J. S. (1999) Defective expression of theμ3 subunit of the AP-3 adaptor complex in the Drosophila pigmentation mutant carmine. Mol. Gen. Genet. 262, 401-412
43. Boll, W., Ohno, H., Songyang, Z., Rapoport, 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
44. 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, 565-576
45. Carvajal-Gonzalez, J. M., Gravotta, D., Mattera, R., Diaz, F., Perez Bay, A., Roman, A. C., Schreiner, R. P., Thuenauer, R., Bonifacino, J. S., and Rodriguez- Boulan, E. (2012) Basolateral sorting of the coxsackie and adenovirus receptor through interaction of a canonical YXXPhi motif with the clathrin adaptors AP-1A and AP-1B. Proc. Natl. Acad. Sci. U.S.A. 109, 3820-3825
46. Gravotta, D., Carvajal-Gonzalez, J. M., Mattera, R., Deborde, S., Banfelder, J. R., Bonifacino, J. S., and Rodriguez-Boulan, E. (2012) The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell 22, 811-823
47. Ren, X., Farias, G. G., Canagarajah, B. J., Bonifacino, J. S., and Hurley, J. H. (2013) Structural basis for recruitment and activation of the AP-1 clathrin adaptor complex by Arf1. Cell 152, 755-767
48. Wallace, A. C., Laskowski, R. A., and Thornton, J. M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8, 127-134