Sorting out the cellular functions of sorting nexins

Nature Reviews Molecular Cell Biology

Volumn 3, Issue 12, 2002, Pages 919-931

  Worby, Carolyn A ^a   Dixon, Jack E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOLIPID; PROTEASE NEXIN;

CELL MEMBRANE TRANSPORT; COMPLEX FORMATION; HUMAN; HYDROPHILICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; CYTOPLASMIC VESICLES; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHOLIPIDS; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; VESICULAR TRANSPORT PROTEINS; YEASTS;

EID: 0036904274     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm974     Document Type: Review

References (91)

1. Mellman, I. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625 (1996).
2. Teasdale, R. D., Loci, D., Houghton, F., Karlsson, L. & Gleeson, P A, A large family of endosome-localized proteins related to sorting nexin 1. Biochem. J. 358, 7-16 (2001).
3. Miaczynska, M. & Zenal, M. Mosaic organization of the endocytic pathway Exp. Cell Res. 272, 8-14 (2002).
4. Simonsen, A., Wurmser, A. E., Emr S. D. & Stenmark, H. The role of phosphoinositides in membrane transport. Curr Opin. Cell Biol. 13, 485-492 (2001).
5. Xu, Y., Seet, L F., Hanson, B, & Hong, W. The Phox homology (PX) domain, a new player in phosphoinositide signalling. Biochem J. 360, 513-530 (2001).
6. Ponting, C. P. Novel domains in NADPH oxidase subunits, sorting nexins, and Ptdlns3-kinases: Binding partners of SH3 domains? Protein Sci. 5, 2353-2357 (1996). This paper was the first to define the PX domain.
7. Cheever, M. L. et al. Phox domain interaction with Ptdlns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nature Cell Biol. 3, 613-618 (2001).
8. Ellson, C. D. et al. Ptdlns(3)P regulates the neutrophil oxidase complex by binding to the PX domain of P40(phox). Nature Cell Biol. 3, 679-682 (2001).
9. phox bind to lipid products of PI(3)K. Nature Cell Biol. 3, 675-678 (2001). This paper was one of the first to show that PX domains bind phosphorylated phosphoinositides.
10. Kurten, R. C., Cadena, D. L. & Gill, G. N. Enhanced degradation of EGF receptors by a sorting nexin, SNX1, Science 272, 1008-1110 (1996). This was the first report of a mammalian sorting nexin.
11. Rothman, J. H. & Stevens, T. H. & Stevens, TH. Protein sorting in yeast: Mutants defective in vacuole biogenesis mislocalize vacuolar proteins into the late secretory pathway, Cell 47, 1041-1051 (1986).
12. Rothman, J. H., Raymond, C. K., Gilbert, T., O'Hara, P. J. & Stevens, T. H. A putative GTP binding protein homologous to interferon-inducible Mx proteins performs an essential function in yeast protein sorting. Cell 61, 1063-1074 (1990).
13. Nothwehr S. F., Conibear, E. & Stevens, T. H. Golgi and vacuolar membrane proteins reach the vacuole in vps 1 mutant yeast cells via the plasma membrane. J. Cell Biol. 129, 35-46 (1995).
14. Ekena, K. & Stevens, T. H. The Saccharomyces cerevisiae MVP1 gene interacts with VPS1 and is required for vacuolar protein sorting, Mol. Cell. Biol. 15, 1671-1678 (1995).
15. Horazdovsky, B. F. et al. 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 (1997).
16. Schultz, J., Copley R. R., Doerks, T., Ponting C. P. & Bork, P. SMART a web-based tool for the study of genetically mobile domains, Nucleic Acids Res. 28, 231-234 (2000).
17. Lupas, A Coiled coils: New structures and new functions. Trends Biochem. Sci. 21, 375-382 (1996).
18. Mayer, B, J. SH3 domains: Complexity in moderation, J. Cell Sci. 114, 1253-1263 (2001).
19. Goebl, M. & Yanagida, M. The TPR snap helix: A novel protein repeat motif from mitosis to transcription. Trends Biochem. Sci. 16, 173-177 (1991).
20. Lamb, J. R., Tugendreich, S. & Hieter, R Tetratrico peptide repeat interactions: To TPR or not to TPR? Trends Biochem. Sci. 20, 257-259 (1995).
21. Shaw, R. J., Henry, M., Solomon, F. & Jacks, T RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol. Biol. Cell 9, 403-419 (1998).
22. Tsukita, S & Yonemura, S. ERM proteins: Head-to-tail regulation of actin-plasma membrane interaction, Trends Biochem. Sci. 22, 53-58 (1997).
23. Hollinger, S. & Hepler, J. R. Cellular regulation of RGS proteins: Modulators and integrators of G protein signaling. Pharmacol. Rev. 54, 527-559 (2002).
24. Zheng, B. et al. RGS-PX1, a GAP for GαS and sorting nexin in vesicular trafficking. Science 294, 1939-1942 (2001).
25. Ponting, C. P. & Benjamin, D. R. A novel family of Ras-binding domains. Trends Biochem. Sci. 21, 422-425 (1996).
26. Shaw, G. The pleckstrin homology domain: An Intriguing multifunctional protein module. Bioessays 18, 35-46 (1996).
27. Harlan, J. E., Hajduk, P. J., Yoon, H. S. & Fesik, S. W. Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371, 168-170 (1994).
28. Itoh, T et al. Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291, 1047-1051 (2001).
29. Patki, V., Lawe, D. C., Corvera, S., Virbasius, J. V. & Chawla, A. A functional Ptdlns(3)P-binding motif Nature 394, 433-434 (1998).
30. 2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes Science 291, 1051-1055 (2001).
31. Lemmon, M. A. & Ferguson, K. M Pleckstrin homology domains Curr. Top. Microbiol. Immunol. 228, 39-74 (1998).
32. Lemmon, M. A., Ferguson, K. M. & Abrams, C. S, Pleckstrin homology domains and the cytoskeleton FEBS Lett, 513, 71-76 (2002).
33. Lemmon, M. A., & Ferguson, K. M. Molecular determinants in pleckstrin homology domains that allow specific recognition of phosphoinositides. Biochem. Soc. Trans. 29, 377-384 (2001).
34. Gillooly, D. J., Simonsen, A. & Stenmark, H. Cellular Junctions of phosphatidylinositol 3-phosphate and FYVE domain proteins. Biochem. J. 355, 249-258 (2001).
35. Ago, T. et al. The PX domain as a novel phosphoinositide-binding module. Biochem. Biophys. Res. Commun 287, 733-738 (2001).
36. Matsui, Y., Matsui, R., Akada, R. & Toh-e, A. Yeast src homology region 3 domain-binding proteins involved in bud formation. J. Cell Biol. 133, 865-878 (1996).
37. Nothwehr, S. F. & Hindes, A. E. 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 (1997).
38. Schwarz, D. G., Griffin, C. T., Schneider, E. A., Yee, D & Magnuson, T. Genetic analysis of sorting nexins 1 and 2 reveals a redundant and essential function in mice. Mol. Biol. Cell 13, 3588-3600 (2002).
39. Voos, W. & Stevens, T. H. Retrieval of resident late-Golgi membrane proteins from the prevacuolar compartment of Saccharomyces cerevisiae is dependent on the function of Grd19p. J. Cell Biol. 140, 577-590 (1998).
40. phox bound to phosphatidylinositol 3-phosphate Mol. Cell 8, 829-839 (2001). This paper reports the first crystal structure of a PX domain.
41. Xu, Y., Hortsman, H., Seet, L., Wong, S. H. & Hong, W. SNX3 regulates endosomal function through its PX-domain-mediated interaction with Ptdlns(3)P. Nature Cell Biol 3, 658-666 (2001).
42. Xu, J., Liu, D., Gill, G. & Songyang, Z. Regulation of cytokine-independent survival kinase (CISK) by the Phox homology domain and phosphoinositides J. Cell Biol. 154, 699-705 (2001).
43. Song, X. et al. Phox homology domains specificaly bind phosphatidylinositol phosphates. Biochemistry 40, 8940-8944 (2001).
44. Wishart, M. J., Taylor, G. S. & Dixon, J. E. Phoxy lipids: Revealing PX domains as phosphoinositide binding modules. Cell 105, 817-820 (2001).
45. Hiroaki, H., Ago, T., Ito T., Sumimoto, H. & Kohda, D. Solution structure of the PX domain, a target of the SH3 domain. Nature Struct. Biol. 8, 526-530 (2001).
46. phox to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J. 21, 5057-5068 (2002).
47. Lu, J., Garcia, J., Dulubova, I., Sudhof, T. C. & Rizo, J. Solution structure of the Vam7p PX domain. Biochemistry 41, 5956-5962 (2002).
48. Seaman, M. N., McCaffery, J. M. & Emr, S, D. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142, 665-681 (1998).
49. Kurten, R. C. et al. Self-assembly and binding of a sorting nexin to sorting endosomes. J. Cell Sci, 114, 1743-1756 (2001).
50. Haft, C. R. et al. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: Assembly into multimeric complexes. Mol. Biol. Sci. 11, 4105-4116 (2000).
51. Haft, C. R., de la Luz Sierra, M., Barr, V. A., Haft, D. H. & Taylor, S. I. Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol. Cell. Biol. 18, 7278-7287 (1998).
52. Mu, F. T. et al. EEA1, an early endosome-associated protein EEA1 is a conserved α-helical peripheral membrane protein flanked by cysteine 'fingers' and contains a calmodulin-binding IQ motif. J. Biol. Chem. 270, 13503-13511 (1995).
53. Raiborg, C. et al. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nature Cell Biol. 4, 394-398 (2002).
54. Chin, L. S., Raynor, M. C., Wei, X., Chen, H. Q. & Li, L. Hrs interacts with sorting nexin 1 and regulates degradation of epidermal growth factor receptor. J. Biol. Chem. 276, 7069-7078 (2001).
55. Zhong, Q. et al. Endosomal localization and function of sorting nexin 1. Proc. Natl. Acad. Sci. USA 99, 6767-6772 (2002).
56. Yu, J. W. & Lemmon, M. A. All phox homology (PX) domains from Saccharomyces cerevisiae specifically recognize phosphatidylinositol 3-phosphate. J. Biol. Chem. 276, 44179-44184 (2001).
57. Watton, S. J. & Downward, J. Akt/PKB localisation and 3′ phosphoinositide generation at sites of epithelial cell-matrix and cell-cell interaction. Curr. Biol. 9, 433-436 (1999).
58. Oatey, P. B. et al. Confocal imaging of the subcellular distnbution of phosphatidylinositol 3,4,5-trisphosphate in insulin- and PDGF-stimulated 3T3-L1 abipocytes. Biochem. J. 344. 511-518 (1999).
59. Cozier, G. E. et al. The 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. 2002 Aug 26 (DOI 10 1074/bc. M206986200).
60. Otsuki, T., Kaligaya, S., Ozawa, K & Liu, J. M. SNX5, a new member of the sorting nexin family, binds to the Fanconi anemia complementation group A protein. Biochem. Biophys. Res Commun. 265, 630-635 (1999).
61. Liu, J. M., Buchwald, M., Walsh, C. E. & Young, N. S. Fanconi anemia and novel strategies for therapy. Blood 84, 3995-4007 (1994).
62. Joenje, H. et al. Evidence for at least eight Fancon anemia genes. Am. J. Hum. Genet. 61, 940-944 (1997).
63. Parks, W. T et al. Sorting nexin 6, a novel SNX, interacts with the transforming growth factor-β family of receptor serine-threonine kinases. J. Biol. Chem. 276, 19332-19339 (2001).
64. Ishibashi, Y. et al. Pm-1 translocates sorting nexin 6/TRAF4-associated factor 2 from cytoplasm to nucleus. FEBS Lett. 506, 33-38 (2001).
65. Howard, L., Nelson, K. K., Maciewicz, R. A. & Blobel, C. P. Interaction of the metalloprotease disintegrins MDC9 and MDC15 with two SH3 domain-containing proteins, endophilin I and SH3PX1. J. Biol. Chem. 274, 31693-31699 (1999).
66. Lundmark, R. & Carlsson, S. R. The β-appendages of the four adaptor-protein (AP) complexes: Structure and binding properties, and identification of sorting nexin 9 as an accessory protein to AP-2. Biochem. J. 362, 597-607 (2002).
67. Worby, C. A. et al. The sorting nexin, DSH3PX1, connects the axonal guidance receptor, Dscam, to the actin cytoskeleton. J Biol. Chem. 276, 41782-41789 (2001).
68. Robinson, M. S. & Bonifacino, J S. Adaptor-related proteins. Curr. Opin. Cell Biol. 13, 444-453 (2001).
69. Worby, C. A. et al. Drosophila Ack targets its substrate, the sorting nexin DSH3PX1, to a protein complex involved in axonal guidance. J. Biol. Chem. 277, 9422-9428 (2002).
70. Lin, Q., Lo, C. G., Cerione, R. A. & Yang, W. The Cdc42 target ACK2 interacts with sorting nexin 9 (SH3PX1) to regulate epidermal growth factor receptor degradation. J. Biol. Chem. 277, 10134-10138 (2002).
71. Schafer, D. A. Coupling actin dynamics and membrane dynamics during endocytosis. Curr. Opin. Cell Biol. 14, 76-81 (2002).
72. De Vries, L., Zheng, B., Fischer, T., Elenko, E. & Farquhar, M. G. The regulator of G protein signaling family. Annu. Rev. Pharmacol. Toxicol. 40, 235-271 (2000).
73. von Zastrow, M. & Mostov, K. Signal transduction A new thread in an intricate web. Science 294, 1845-1847 (2001).
74. Phillips, S. A., Barr, V. A., Haft, D. H., Taylor, S. I. & Haft, C. R. Identification and characterizaton of SNX 15, a novel sorting nexin involved in protein trafficking. J. Biol. Chem. 276, 5074-5084 (2001).
75. Barr, V. A., Phillips, S. A., Taylor, S. I. & Haft, C. R. Overexpression of a novel sorting nexin, SNX 15, affects endosome morphology and protein trafficking. Traffic 1, 904-916 (2000).
76. Komada, M, et al. Proteolytic processing of the hepatocyte growth factor/scatter factor receptor by furin. FEBS Lett. 328, 25-29 (1993).
77. Ghosh, R. N., Mallet, W. G., Soe, T. T., McGraw, T. E. & Maxfield, F. R. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol. 142, 923-936 (1998).
78. Mallet, W. G. & Maxfield, F. R. Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146, 345-359 (1999).
79. Florian, V., Schluter, T. & Bohnensack, R. A new member of the sorting nexin family interacts with the C-terminus of P-selectin. Biochem. Biophys. Res. Commun. 281, 1045-1050 (2001).
80. Straley, K. S. & Green, S. A. Rapid transport of internalized P-selectin to late endosomes and the TGN: Roles in regulating cell surface expression and recycling to secretory granules. J. Cell Biol. 151, 107-116 (2000).
81. Stockinger, W. et al. The PX-domain protein SNX17 interacts with members of the LDL receptor family and modulates endecytosis of the LDL receptor. EMBO J. 21, 4259-4267 (2002).
82. phox), thereby activating the oxidase. J. Biol. Chem. 274, 33644-33653 (1999).
83. Chanock, S. J. el Benna, J., Smith, R. M. & Babior, B. M. The respiratory burst oxidase. J. Biol. Chem. 269, 24519-24522 (1994).
84. Noack, D. et al. Autosomal recessive chronic granulomatous disease caused by defects in NCF-1, the gene encoding the phagocyte p47-phox: Mutations not arising in the NCF-1 pseudogenes. Blood 97, 305-311 (2001).
85. Nothwehr, S. F., Ha, S. A. & Bruinsma. P. Sorting of yeast membrane proteins into an endosome-to-Golgi pathway involves direct interaction of their cytosolic domains with Vps35p. J. Cell. Biol. 151, 297-310 (2000).
86. Seaman, M. N., Marcusson, E. G., Cereghino, J. L. & Emr, S. D. Endosome to Golgi retrieval of the vacuolar protien sorting receptor, Vps 10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137, 79-92 (1997).
87. Nothwehr, S. F., Bruinsma, P. & Strawn, L. A. Distinct domains within Vps35p mediate the retrieval of two different cargo proteins from the yeast prevacuolar/endosomal compartment. Mol. Biol. Cell 10, 875-890 (1999).
88. Reddy, J. V. & Seaman, M. N. Vps26p, a component of retromer, directs the interactions of Vps35p in endosome-to-Golgi retrieval. Mol. Biol. Cell 12, 3242-3256 (2001).
89. Seaman, M. N. & Williams, H. P. Identification of the functional domains of yeast sorting nexins vps5p and vps17p. Mol. Biol. Cell 13, 2826-2840 (2002).
90. Felsenstein, J. An alternating least squares approach to inferring phylogenies from pairwise distances. Syst. Biol. 46, 101-111 (1997).
91. Carson, M. Ribbons 2.0. J. Appl. Cryst. 24, 956-961 (1991).