Galectin-4-mediated transcytosis of transferrin receptor

Journal of Cell Science

Volumn 127, Issue 20, 2014, Pages 4457-4469

  Perez Bay, Andres E ^a   Schreiner, Ryan ^a   Benedicto, Ignacio ^a   Rodriguez Boulan, Enrique J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Galectin; Glycan; Rab11a; Transcytosis; Transferrin receptor

Indexed keywords

GALECTIN 4; TRANSFERRIN RECEPTOR; ADAPTOR PROTEIN; AP1B1 PROTEIN, HUMAN; BETA ADAPTIN; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; BASOLATERAL MEMBRANE; CELL MEMBRANE; KIDNEY PROXIMAL TUBULE; NONHUMAN; PIGMENT EPITHELIUM; PROTEIN LOCALIZATION; TRANSCYTOSIS; ANIMAL; CELL LINE; CELL POLARITY; DOG; ENDOSOME; EPITHELIUM CELL; GENE SILENCING; GENETICS; HUMAN; LYSOSOME; MDCK CELL LINE; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT;

ADAPTOR PROTEIN COMPLEX 1; ADAPTOR PROTEIN COMPLEX BETA SUBUNITS; ANIMALS; CELL LINE; CELL MEMBRANE; CELL POLARITY; DOGS; ENDOSOMES; EPITHELIAL CELLS; GALECTIN 4; GENE KNOCKDOWN TECHNIQUES; HUMANS; LYSOSOMES; MADIN DARBY CANINE KIDNEY CELLS; MUTATION; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECEPTORS, TRANSFERRIN; TRANSCYTOSIS;

EID: 84918541122     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.153437     Document Type: Article

References (53)

1. Ang, A. L., Taguchi, T., Francis, S., Fölsch, H., Murrells, L. J., Pypaert, M., Warren, G. and Mellman, I. (2004). Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Biol. 167, 531-543.
2. Apodaca, G., Katz, L. A. and Mostov, K. E. (1994). Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125, 67-86.
3. Bell, R. D. and Ehlers, M. D. (2014). Breaching the blood-brain barrier for drug delivery. Neuron 81, 1-3.
4. Bomsel, M., Prydz, K., Parton, R. G., Gruenberg, J. and Simons, K. (1989). Endocytosis in filter-grown Madin-Darby canine kidney cells. J. Cell Biol. 109, 3243-3258.
5. Bonifacino, J. S. (2014). Adaptor proteins involved in polarized sorting. J. Cell Biol. 204, 7-17.
6. Chen, R., Jiang, X., Sun, D., Han, G., Wang, F., Ye, M., Wang, L. and Zou, H. (2009). Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J. Proteome Res. 8, 651-661.
7. Dai, J., Li, J., Bos, E., Porcionatto, M., Premont, R. T., Bourgoin, S., Peters, P. J. and Hsu, V. W. (2004). ACAP1 promotes endocytic recycling by recognizing recycling sorting signals. Dev. Cell 7, 771-776.
8. Deborde, S., Perret, E., Gravotta, D., Deora, A., Salvarezza, S., Schreiner, R. and Rodriguez-Boulan, E. (2008). Clathrin is a key regulator of basolateral polarity. Nature 452, 719-723.
9. Delacour, D., Cramm-Behrens, C. I., Drobecq, H., Le Bivic, A., Naim, H. Y. and Jacob, R. (2006). Requirement for galectin-3 in apical protein sorting. Curr. Biol. 16, 408-414.
10. Delacour, D., Greb, C., Koch, A., Salomonsson, E., Leffler, H., Le Bivic, A. and Jacob, R. (2007). Apical sorting by galectin-3-dependent glycoprotein clustering. Traffic 8, 379-388.
11. Deora, A. A., Diaz, F., Schreiner, R. and Rodriguez-Boulan, E. (2007). Efficient electroporation of DNA and protein into confluent and differentiated epithelial cells in culture. Traffic 8, 1304-1312.
12. Diaz, F., Gravotta, D., Deora, A., Schreiner, R., Schoggins, J., Falck-Pedersen, E. and Rodriguez-Boulan, E. (2009). Clathrin adaptor AP1B controls adenovirus infectivity of epithelial cells. Proc. Natl. Acad. Sci. USA 106, 11143-11148.
13. Dunn, K. W., Kamocka, M. M. and McDonald, J. H. (2011). A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. 300, C723-C742.
14. Fiedler, K. and Simons, K. (1995). The role of N-glycans in the secretory pathway. Cell 81, 309-312.
15. Fölsch, H. (2008). Regulation of membrane trafficking in polarized epithelial cells. Curr. Opin. Cell Biol. 20, 208-213.
16. Fölsch, H., Ohno, H., Bonifacino, J. S. and Mellman, I. (1999). A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99, 189-198.
17. Fölsch, H., Pypaert, M., Maday, S., Pelletier, L. and Mellman, I. (2003). The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J. Cell Biol. 163, 351-362.
18. Gan, Y., McGraw, T. E. and Rodriguez-Boulan, E. (2002). The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane. Nat. Cell Biol. 4, 605-609.
19. Gonzalez, A. and Rodriguez-Boulan, E. (2009). Clathrin and AP1B: key roles in basolateral trafficking through trans-endosomal routes. FEBS Lett. 583, 3784-3795.
20. Gravotta, D., Deora, A., Perret, E., Oyanadel, C., Soza, A., Schreiner, R., Gonzalez, A. and Rodriguez-Boulan, E. (2007). AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells. Proc. Natl. Acad. Sci. USA 104, 1564-1569.
21. 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.
22. Guo, X., Mattera, R., Ren, X., Chen, Y., Retamal, C., González, A. and Bonifacino, J. S. (2013). The adaptor protein-1 m1B subunit expands the repertoire of basolateral sorting signal recognition in epithelial cells. Dev. Cell 27, 353-366.
23. Hoepfner, S., Severin, F., Cabezas, A., Habermann, B., Runge, A., Gillooly, D., Stenmark, H. and Zerial, M. (2005). Modulation of receptor recycling and degradation by the endosomal kinesin KIF16B. Cell 121, 437-450.
24. Hosoya, K., Tomi, M. and Tachikawa, M. (2011). Strategies for therapy of retinal diseases using systemic drug delivery: relevance of transporters at the bloodretinal barrier. Expert Opin. Drug Deliv. 8, 1571-1587.
25. Hughes, R. C. (1999). Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473, 172-185.
26. Hughson, E. J. and Hopkins, C. R. (1990). Endocytic pathways in polarized Caco-2 cells: identification of an endosomal compartment accessible from both apical and basolateral surfaces. J. Cell Biol. 110, 337-348.
27. Hunt, R. C., Dewey, A. and Davis, A. A. (1989). Transferrin receptors on the surfaces of retinal pigment epithelial cells are associated with the cytoskeleton. J. Cell Sci. 92, 655-666.
28. Iezzi, R., Guru, B. R., Glybina, I. V., Mishra, M. K., Kennedy, A. and Kannan, R. M. (2012). Dendrimer-based targeted intravitreal therapy for sustained attenuation of neuroinflammation in retinal degeneration. Biomaterials 33, 979-988.
29. Iriyama, A., Inoue, Y., Takahashi, H., Tamaki, Y., Jang, W. D. and Yanagi, Y. (2009). A2E, a component of lipofuscin, is pro-angiogenic in vivo. J. Cell. Physiol. 220, 469-475.
30. Jacob, R., Alfalah, M., Grünberg, J., Obendorf, M. and Naim, H. Y. (2000). Structural determinants required for apical sorting of an intestinal brush-border membrane protein. J. Biol. Chem. 275, 6566-6572.
31. Luton, F., Hexham, M. J., Zhang, M. and Mostov, K. E. (2009). Identification of a cytoplasmic signal for apical transcytosis. Traffic 10, 1128-1142.
32. Mattila, P. E., Youker, R. T., Mo, D., Bruns, J. R., Cresawn, K. O., Hughey, R. P., Ihrke, G. and Weisz, O. A. (2012). Multiple biosynthetic trafficking routes for apically secreted proteins in MDCK cells. Traffic 13, 433-442.
33. Maxfield, F. R. and McGraw, T. E. (2004). Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5, 121-132.
34. Mellman, I. and Nelson, W. J. (2008). Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845.
35. Mishra, R., Grzybek, M., Niki, T., Hirashima, M. and Simons, K. (2010). Galectin-9 trafficking regulates apical-basal polarity in Madin-Darby canine kidney epithelial cells. Proc. Natl. Acad. Sci. USA 107, 17633-17638.
36. Mostov, K. E., Verges, M. and Altschuler, Y. (2000). Membrane traffic in polarized epithelial cells. Curr. Opin. Cell Biol. 12, 483-490.
37. Nickel, W. (2005). Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 6, 607-614.
38. Odorizzi, G. and Trowbridge, I. S. (1997). Structural requirements for basolateral sorting of the human transferrin receptor in the biosynthetic and endocytic pathways of Madin-Darby canine kidney cells. J. Cell Biol. 137, 1255-1264.
39. Ohno, H., Tomemori, T., Nakatsu, F., Okazaki, Y., Aguilar, R. C., Foelsch, H., Mellman, I., Saito, T., Shirasawa, T. and Bonifacino, J. S. (1999). Mu1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449, 215-220.
40. Perez Bay, A. E., Schreiner, R., Mazzoni, F., Carvajal-Gonzalez, J. M., Gravotta, D., Perret, E., Lehmann Mantaras, G., Zhu, Y. S. and Rodriguez-Boulan, E. J. (2013). The kinesin KIF16B mediates apical transcytosis of transferrin receptor in AP-1B-deficient epithelia. EMBO J. 32, 2125-2139.
41. Poland, P. A., Rondanino, C., Kinlough, C. L., Heimburg-Molinaro, J., Arthur, C. M., Stowell, S. R., Smith, D. F. and Hughey, R. P. (2011). Identification and characterization of endogenous galectins expressed in Madin Darby canine kidney cells. J. Biol. Chem. 286, 6780-6790.
42. Rodriguez-Boulan, E. and Macara, I. G. (2014). Organization and execution of the epithelial polarity programme. Nat. Rev. Mol. Cell Biol. 15, 225-242.
43. Rodriguez-Boulan, E., Kreitzer, G. and Müsch, A. (2005). Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 6, 233-247.
44. Rodriguez-Boulan, E., Perez-Bay, A., Schreiner, R. and Gravotta, D. (2013). Response: the ''tail'' of the twin adaptors. Dev. Cell 27, 247-248.
45. Scheiffele, P., Roth, M. G. and Simons, K. (1997). Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16, 5501-5508.
46. Schreiner, R., Frindt, G., Diaz, F., Carvajal-Gonzalez, J. M., Perez Bay, A. E., Palmer, L. G., Marshansky, V., Brown, D., Philp, N. J. and Rodriguez-Boulan, E. (2010). The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int. 78, 382-388.
47. Stechly, L., Morelle, W., Dessein, A. F., André, S., Grard, G., Trinel, D., Dejonghe, M. J., Leteurtre, E., Drobecq, H., Trugnan, G. et al. (2009). Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10, 438-450.
48. Straube, T., von Mach, T., Hönig, E., Greb, C., Schneider, D. and Jacob, R. (2013). pH-dependent recycling of galectin-3 at the apical membrane of epithelial cells. Traffic 14, 1014-1027.
49. Traer, C. J., Rutherford, A. C., Palmer, K. J., Wassmer, T., Oakley, J., Attar, N., Carlton, J. G., Kremerskothen, J., Stephens, D. J. and Cullen, P. J. (2007). SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment. Nat. Cell Biol. 9, 1370-1380.
50. Tzaban, S., Massol, R. H., Yen, E., Hamman, W., Frank, S. R., Lapierre, L. A., Hansen, S. H., Goldenring, J. R., Blumberg, R. S. and Lencer, W. I. (2009). The recycling and transcytotic pathways for IgG transport by FcRn are distinct and display an inherent polarity. J. Cell Biol. 185, 673-684.
51. Wang, X., Kumar, R., Navarre, J., Casanova, J. E. and Goldenring, J. R. (2000). Regulation of vesicle trafficking in madin-darby canine kidney cells by Rab11a and Rab25. J. Biol. Chem. 275, 29138-29146.
52. Weisz, O. A. and Rodriguez-Boulan, E. (2009). Apical trafficking in epithelial cells: signals, clusters and motors. J. Cell Sci. 122, 4253-4266.
53. Yeaman, C., Le Gall, A. H., Baldwin, A. N., Monlauzeur, L., Le Bivic, A. and Rodriguez-Boulan, E. (1997). The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J. Cell Biol. 139, 929-940.