Phosphoinositide 3-kinase regulates the role of retromer in transcytosis of the polymeric immunoglobulin receptor

Experimental Cell Research

Volumn 313, Issue 4, 2007, Pages 707-718

  Vergés, Marcel ^a,b   Sebastián, Isabel ^b   Mostov, Keith E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

LY294002; MDCK; Phosphatidylinositol; Phosphoinositide; pIgR; Receptor; Retromer; Sorting nexin; Transcytosis; Vps35

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEASE NEXIN I; PROTEIN; PROTEIN SNX 1; PROTEIN SNX 2; PROTEIN VPS35; RETROMER; SECRETORY COMPONENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME INHIBITION; GENE OVEREXPRESSION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; TRANSCYTOSIS;

EID: 33846657408     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.11.010     Document Type: Article

References (50)

1. Mostov K., Su T., and ter Beest M. Polarized epithelial membrane traffic: conservation and plasticity. Nat. Cell Biol. 5 (2003) 287-293
2. Tuma P.L., and Hubbard A.L. Transcytosis: crossing cellular barriers. Physiol. Rev. 83 (2003) 871-932
3. Rojas R., and Apodaca G. Immunoglobulin transport across polarized epithelial cells. Nat. Rev., Mol. Cell Biol. 3 (2002) 944-956
4. Seaman M.N., McCaffery J.M., and Emr S.D. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142 (1998) 665-681
5. Seaman M.N., Marcusson E.G., Cereghino J.L., and Emr S.D. Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137 (1997) 79-92
6. Arighi C.N., Hartnell L.M., Aguilar R.C., Haft C.R., and Bonifacino J.S. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165 (2004) 123-133
7. Seaman M.N. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165 (2004) 111-122
8. Seaman M.N. Recycle your receptors with retromer. Trends Cell Biol. 15 (2005) 68-75
9. Vergés M., Luton F., Gruber C., Tiemann F., Reinders L.G., Huang L., Burlingame A.L., Haft C.R., and Mostov K.E. The mammalian retromer regulates transcytosis of the polymeric immunoglobulin receptor. Nat. Cell Biol. 6 (2004) 763-769
10. Bonifacino J.S., and Rojas R. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev., Mol. Cell Biol. 7 (2006) 568-579
11. Seaman M.N., and Williams H.P. Identification of the functional domains of yeast sorting nexins Vps5p and Vps17p. Mol. Biol. Cell 13 (2002) 2826-2840
12. Horazdovsky B.F., Davies B.A., Seaman M.N., McLaughlin S.A., Yoon S., and Emr S.D. 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 (1997) 1529-1541
13. Nothwehr S.F., Bruinsma P., and 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 (1999) 875-890
14. Nothwehr S.F., Ha S.A., and 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 (2000) 297-310
15. Reddy J.V., and Seaman M.N. Vps26p, a component of retromer, directs the interactions of Vps35p in endosome-to-Golgi retrieval. Mol. Biol. Cell 12 (2001) 3242-3256
16. Haft C.R., de la Luz Sierra M., Bafford R., Lesniak M.A., Barr V.A., and Taylor S.I. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35: assembly into multimeric complexes. Mol. Biol. Cell 11 (2000) 4105-4116
17. Collins B.M., Skinner C.F., Watson P.J., Seaman M.N., and Owen D.J. Vps29 has a phosphoesterase fold that acts as a protein interaction scaffold for retromer assembly. Nat. Struct. Mol. Biol. 12 (2005) 594-602
18. Wang D., Guo M., Liang Z., Fan J., Zhu Z., Zang J., Li X., Teng M., Niu L., Dong Y., and Liu P. Crystal structure of human vacuolar protein sorting protein 29 reveals a phosphodiesterase/nuclease-like fold and two protein-protein interaction sites. J. Biol. Chem. 280 (2005) 22962-22967
19. Shi H., Rojas R., Bonifacino J.S., and Hurley J.H. The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat. Struct. Mol. Biol. 13 (2006) 540-548
20. Burda P., Padilla S.M., Sarkar S., and Emr S.D. Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps34 PtdIns 3-kinase. J. Cell Sci. 115 (2002) 3889-3900
21. Zhong Q., Lazar C.S., Tronchere H., Sato T., Meerloo T., Yeo M., Songyang Z., Emr S.D., and Gill G.N. Endosomal localization and function of sorting nexin 1. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6767-6772
22. Hansen S.H., Olsson A., and Casanova J.E. Wortmannin, an inhibitor of phosphoinositide 3-kinase, inhibits transcytosis in polarized epithelial cells. J. Biol. Chem. 270 (1995) 28425-28432
23. Cardone M., and Mostov K. Wortmannin inhibits transcytosis of dimeric IgA by the polymeric immunoglobulin receptor. FEBS Lett. 376 (1995) 74-76
24. Barth A.I., Pollack A.L., Altschuler Y., Mostov K.E., and Nelson W.J. NH2-terminal deletion of beta-catenin results in stable colocalization of mutant beta-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion. J. Cell Biol. 136 (1997) 693-706
25. Breitfeld P.P., Casanova J.E., McKinnon W.C., and Mostov K.E. Deletions in the cytoplasmic domain of the polymeric immunoglobulin receptor differentially affect endocytotic rate and postendocytotic traffic. J. Biol. Chem. 265 (1990) 13750-13757
26. Singer K.L., and Mostov K.E. Dimerization of the polymeric immunoglobulin receptor controls its transcytotic trafficking. Mol. Biol. Cell 9 (1998) 901-915
27. Luton F., Cardone M.H., Zhang M., and Mostov K.E. Role of tyrosine phosphorylation in ligand-induced regulation of transcytosis of the polymeric Ig receptor. Mol. Biol. Cell 9 (1998) 1787-1802
28. Vlahos C.J., Matter W.F., Hui K.Y., and Brown R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269 (1994) 5241-5248
29. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 296 (2002) 1655-1657
30. Patki V., Virbasius J., Lane W.S., Toh B.H., Shpetner H.S., and Corvera S. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 7326-7330
31. Chen X., and Wang Z. Regulation of epidermal growth factor receptor endocytosis by wortmannin through activation of Rab5 rather than inhibition of phosphatidylinositol 3-kinase. EMBO Rep. 2 (2001) 842-849
32. Tuma P.L., Finnegan C.M., Yi J.H., and Hubbard A.L. Evidence for apical endocytosis in polarized hepatic cells: phosphoinositide 3-kinase inhibitors lead to the lysosomal accumulation of resident apical plasma membrane proteins. J. Cell Biol. 145 (1999) 1089-1102
33. Futter C.E., Collinson L.M., Backer J.M., and Hopkins C.R. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J. Cell Biol. 155 (2001) 1251-1264
34. Christoforidis S., McBride H.M., Burgoyne R.D., and Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397 (1999) 621-625
35. Davidson H.W. Wortmannin causes mistargeting of procathepsin D. Evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol. 130 (1995) 797-805
36. Brown W.J., DeWald D.B., Emr S.D., Plutner H., and Balch W.E. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol. 130 (1995) 781-796
37. Apodaca G., Katz L.A., and Mostov K.E. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125 (1994) 67-86
38. Brunn G.J., Williams J., Sabers C., Wiederrecht G., Lawrence Jr. J.C., and Abraham R.T. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15 (1996) 5256-5267
39. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95-105
40. Orzech E., Schlessinger K., Weiss A., Okamoto C.T., and Aroeti B. Interactions of the AP-1 Golgi adaptor with the polymeric immunoglobulin receptor and their possible role in mediating brefeldin A-sensitive basolateral targeting from the trans-Golgi network. J. Biol. Chem. 274 (1999) 2201-2215
41. Walker E.H., Pacold M.E., Perisic O., Stephens L., Hawkins P.T., Wymann M.P., and Williams R.L. Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol. Cell 6 (2000) 909-919
42. Shpetner H., Joly M., Hartley D., and Corvera S. Potential sites of PI-3 kinase function in the endocytic pathway revealed by the PI-3 kinase inhibitor, wortmannin. J. Cell Biol. 132 (1996) 595-605
43. Worby C.A., and Dixon J.E. Sorting out the cellular functions of sorting nexins. Nat. Rev., Mol. Cell Biol. 3 (2002) 919-931
44. Carlton J., Bujny M., Rutherford A., and Cullen P. Sorting nexins-unifying trends and new perspectives. Traffic 6 (2005) 75-82
45. Seet L.F., and Hong W. The Phox (PX) domain proteins and membrane traffic. Biochim. Biophys. Acta 1761 (2006) 878-896
46. Stack J.H., DeWald D.B., Takegawa K., and Emr S.D. Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol. 129 (1995) 321-334
47. Carlton J., Bujny M., Peter B.J., Oorschot V.M., Rutherford A., Mellor H., Klumperman J., McMahon H.T., and Cullen P.J. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr. Biol. 14 (2004) 1791-1800
48. Carlton J.G., Bujny M.V., Peter B.J., Oorschot V.M., Rutherford A., Arkell R.S., Klumperman J., McMahon H.T., and Cullen P.J. 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 (2005) 4527-4539
49. Gullapalli A., Wolfe B.L., Griffin C.T., Magnuson T., and Trejo J. An essential role for SNX1 in lysosomal sorting of protease-activated receptor-1: evidence for retromer-, Hrs-, and Tsg101-independent functions of sorting nexins. Mol. Biol. Cell 17 (2006) 1228-1238
50. Oliviusson P., Heinzerling O., Hillmer S., Hinz G., Tse Y.C., Jiang L., and Robinson D.G. Plant retromer, localized to the prevacuolar compartment and microvesicles in Arabidopsis, may interact with vacuolar sorting receptors. Plant Cell 18 (2006) 1239-1252