An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: Evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins

Molecular Biology of the Cell

Volumn 17, Issue 3, 2006, Pages 1228-1238

  Gullapalli, Anuradha ^a   Wolfe, Breann L ^a   Griffin, Courtney T ^a   Magnuson, Terry ^a   Trejo, JoAnn ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CELL SURFACE RECEPTOR; G PROTEIN COUPLED RECEPTOR; PROTEASE NEXIN; PROTEIN HRS; PROTEIN SNX1; PROTEIN SNX2; PROTEINASE ACTIVATED RECEPTOR 1; SMALL INTERFERING RNA; THROMBIN; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOSOME; GOLGI COMPLEX; HELA CELL; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

CARRIER PROTEINS; DNA-BINDING PROTEINS; ENDOSOMES; GENE EXPRESSION; HELA CELLS; HUMANS; LYSOSOMES; MUTATION; PHOSPHOPROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECEPTOR, PAR-1; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; VESICULAR TRANSPORT PROTEINS;

MAMMALIA;

EID: 33644861535     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-09-0899     Document Type: Article

References (35)

1. Arighi, C. N., Hartnell, L. M., Aguilar, R. C., Haft, C. R., and Bonifacino, J. S. (2004). Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell. Biol. 165, 123-133.
2. Bishop, N., Horman, A., and Woodman, P. (2002). Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates. J. Cell Biol. 157, 91-101.
3. Carlton, J., Bujny, M., Peter, B. J., Oorschot, V.M.J., and Rutherford, A. (2005). Sorting nexin-2 is associated with tubular elements of the early endosome, but is not essential for retromer-mediated endosome-to-TGN transport. J. Cell Sci. 118, 4527-4539.
4. Carlton, J., Bujny, M., Peter, B. J., Oorschot, V.M.J., Rutherford, A., Meller, H., Klumperman, J., McMahon, H. T., and Cullen, P. J. (2004). Sorting Nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high curvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800.
5. Chin, L. S., Raynor, M. C., Wei, X., Chen, H. Q., and Li, L. (2001). Hrs interacts with sorting Nexin 1 and regulates degradation of epidermal growth factor receptor. J. Biol. Chem. 276, 7069-7078.
6. Connolly, A. J., Ishihara, H., Kahn, M. L., Farese, R. V., and Coughlin, S. R. (1996). Role of the thrombin receptor in development and evidence for a second receptor. Nature 381, 516-519.
7. Cozier, G. E., Carlton, J., McGregor, A. H., Gleeson, P. A., Teasdale, R. D., Mellor, H., and Cullen, P. J. (2002). The Phox homology (PX) domain-dependent, 3-phosphoinositide-mediated association of sorting nexin-1 with an early sorting endosomal compartment is required for its ability to regulate epidermal growth factor receptor degradation. J. Biol. Chem. 277, 48730-48736.
8. Griffin, C. T., Srinivasan, Y., Zheng, Y.-W., Huang, W., and Coughlin, S. R. (2001). A role for thrombin receptor signaling in endothelial cells during embryonic development. Science 293, 1666-1670.
9. Griffin, C. T., Trejo, J., and Magnuson, T. (2005). Genetic evidence for a mammalian retromer complex containing sorting nexins 1 and 2. Proc. Natl. Acad. Sci. USA 102, 15173-15177.
10. Gullapalli, A., Garrett, T. A., Paing, M. M., Griffin, C. T., Yang, Y., and Trejo, J. (2004). A role for sorting nexin 2 in epidermal growth factor receptor down-regulation: evidence for distinct functions of sorting nexin 1 and 2 in protein trafficking. Mol. Biol. Cell 15, 2143-2155.
11. Haft, C. R., Sierra, M., Bafford, R., Lesniak, M. A., Barr, V. A., and Taylor, S. I. (2000). Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35, assembly into multimeric complexes. Mol. Biol. Cell 11, 4105-4116.
12. Haft, C. R., Sierra, M., Barr, V. A., Haft, D. H., and Taylor, S. I. (1998). Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol. Cell. Biol. 18, 7278-7287.
13. Heydorn, A., Sondergaard, B. P., Ersboll, B., Holst, B., Nielsen, F. C., Haft, C. R., Whistler, J., and Schwartz, T. W. (2004). A library of 7TM receptor C-terminal tails. J. Biol. Chem. 279, 54291-54303.
14. Hislop, J. N., Marley, A., and von Zastrow, M. (2004). Role of mammalian vacuolar protein-sorting proteins in endocytic trafficking of a non-ubiquitinated G protein-coupled receptor to lysosomes. J. Biol. Chem. 279, 22522-22531.
15. Horazdovsky, B. F., Davies, B. A., Seaman, M.N.J., McLaughin, S. A., Yoon, S.-H., and Emr, S. D. (1997). A sorting nexin-1 homologue, Vps5p, forms a complex with Vps17p and is required for recycling the vacuolar protein-sorting receptor. Mol. Biol. Cell 8, 1529-1541.
16. Hung, D. T., Vu, T.-K.H., Wheaton, V. I., Charo, I. F., Nelken, N. A., Esmon, C. T., and Coughlin, S. R. (1992). "Mirror image" antagonists of thrombin-induced platelet activation based on thrombin receptor structure. J. Clin. Invest. 89, 444-450.
17. Ihrke, G., Kyttala, A., Russell, M.R.G., Rous, B. A., and Luzio, J. P. (2004). Differential use of two AP-3-mediated pathways by lysosomal membrane proteins. Traffic 5, 946-962.
18. Kurten, R. C., Cadena, D. L., and Gill, G. N. (1996). Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272, 1008-1010.
19. Lu, Q., Hope, L. W., Brasch, M., Reinhard, C., and Cohen, S. N. (2003). TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation. Proc. Natl. Acad. Sci. USA 200, 7626-7631.
20. Nothwehr, S. F., and Hindes, A. E. (1997). The yeast VPS5/GRD2 gene encodes a sorting nexin-1-like protein required for localizing membrane proteins to the late Golgi. J. Cell Sci. 110, 1063-1072.
21. Paing, M. M., Johnston, C. A., Siderovski, D. P., and Trejo, J. (2006). Clathrin adaptor AP-2 regulates thrombin receptor constitutive internalization and endothelial cell resensitization. Mol. Cell. Biol. (in press).
22. 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.
23. Pierce, K. L., Premont, R. T., and Lefkowitz, R. J. (2002). Seven-transmembrane receptors. Nat. Rev. Mol. Cell. Biol. 3, 639-650.
24. Raiborg, C, Bache, K. G., Mehlum, A., Stang, E., and Stenmark, H. (2001). Hrs recruits clathrin to early endosomes. EMBO J. 20, 5008-5021.
25. Schwarz, D. G., Griffin, C. T., Schneider, E. A., Yee, D., and Magnuson, T. (2002). Genetic analysis of sorting nexins 1 and 2 reveals a redundant and essential function in mice. Mol. Biol. Cell 13, 3588-3600.
26. Seaman, M.N.J. (2004). Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.
27. Seaman, M.N.J., McCaffery, J. M., and Emr, S. D. (1998). A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142, 665-681.
28. Tanowitz, M., and Von Zastrow, M. (2002). Ubiquitination-independent trafficking of G protein-coupled receptors to lysosomes. J. Biol. Chem. 277, 50219-50222.
29. Trejo, J., Altschuler, Y., Fu, H.-W., Mostov, K. E., and Coughlin, S. R. (2000). Protease-activated receptor downregulation: a mutant HeLa cell line suggests novel requirements for PAR1 phosphorylation and recruitment to clathrincoated pits. J. Biol. Chem. 275, 31255-31265.
30. Trejo, J., and Coughlin, S. R. (1999). The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J. Biol. Chem. 274, 2216-2224.
31. Trejo, J., Hammes, S. R., and Coughlin, S. R. (1998). Termination of signaling by protease-activated receptor-1 is linked to lysosomal sorting. Proc. Natl. Acad. Sci. USA 95, 13698-13702.
32. Verges, M., Luton, F., Gruber, C., Tiemann, F., Reinders, L. G., Huang, L., Burlingame, A., Haft, C. R., and Mostov, K. E. (2004). The mammalian retromer regulates transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol. 6, 763-769.
33. Wang, Y., Zhou, Y., Szabo, K., Haft, C. R., and Trejo, J. (2002). Down-regulation of protease-activated receptor-1 is regulated by sorting nexin 1. Mol. Biol. Cell 13, 1965-1976.
34. Worby, C. A., and Dixon, J. E. (2002). Sorting out the cellular functions of sorting nexins. Nat. Rev. 3, 919-931.
35. Zhong, Q., Lasar, C. S., Tronchere, H., Sato, T., Meerloo, T., Yeo, M., Songyang, Z., Emr, S. D., and Gill, G. N. (2002). Endosomal localization and function of sorting nexin 1. Proc. Natl. Acad. Sci. USA 99, 6767-6772.