Endocytosis of megalin by visceral endoderm cells requires the Dab2 adaptor protein

Journal of Cell Science

Volumn 118, Issue 22, 2005, Pages 5345-5355

  Maurer, Meghan E ^a   Cooper, Jonathan A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Dab2; Endocytic adaptor protein; Endocytosis; Lipoprotein receptor traffic; Megalin; Visceral endoderm

Indexed keywords

ADAPTOR PROTEIN; CELL PROTEIN; CUBILIN; ISOPROTEIN; LIGAND; MEGALIN; PROTEIN DAB2; PROTEIN P67; PROTEIN P96; TRANSFERRIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BRUSH BORDER; CELL VACUOLE; CONTROLLED STUDY; CORRELATION ANALYSIS; EMBRYO; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ENDODERM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TRANSPORT; VISCERA; YOLK SAC;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ALTERNATIVE SPLICING; ANIMALS; CELL SURVIVAL; EMBRYO; EMBRYONIC DEVELOPMENT; ENDOCYTOSIS; ENDODERM; LDL-RECEPTOR RELATED PROTEIN 2; MICE; ORGAN SPECIFICITY; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; RNA, MESSENGER; TRANSGENES;

ANIMALIA; MAMMALIA;

EID: 29244461395     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02650     Document Type: Article

References (47)

1. Beddington, R. S. and Robertson, E. J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.
2. Bielinska, M., Narita, N. and Wilson, D. B. (1999). Distinct roles for visceral endoderm during embryonic mouse development. Int. J. Dev. Biol. 43, 183-205.
3. Bohnsack, B. L., Lai, L., Dolle, P. and Hirschi, K. K. (2004). Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev. 18, 1345-1358.
4. Bork, P. and Margolis, B. (1995). A phosphotyrosine interaction domain. Cell 80, 693-694.
5. Buss, F., Luzio, J. P. and Kendrick-Jones, J. (2001). Myosin VI, a new force in clathrin mediated endocytosis. FEBS Lett. 508, 295-299.
6. Chen, W. J., Goldstein, J. L. and Brown, M. S. (1990). NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265, 3116-3123.
7. Cho, S. Y., Lee, S. H. and Park, S. S. (1999). Differential expression of mouse Disabled 2 gene in retinoic acid-treated F9 embryonal carcinoma cells and early mouse embryos. Mol. Cell 9, 179-184.
8. Christensen, E. I. and Birn, H. (2002). Megalin and cubilin: multifunctional endocytic receptors. Nat. Rev. Mol. Cell. Biol. 3, 256-266.
9. Coucouvanis, E. and Martin, G. R. (1999). BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126, 535-546.
10. Dance, A. L., Miller, M., Seragaki, S., Aryal, P., White, B., Aschenbrenner, L. and Hasson, T. (2004). Regulation of myosin-VI targeting to endocytic compartments. Traffic 5, 798-813.
11. Drake, B. L. and Head, J. R. (1990). Transferrin receptor expression in early postimplantation mouse trophoblast and associated tissues. Placenta 11, 535-547.
12. Drake, C. J., Fleming, P. A., Larue, A. C., Barth, J. L., Chintalapudi, M. R. and Argraves, W. S. (2004). Differential distribution of cubilin and megalin expression in the mouse embryo. Anat. Rec. 277A, 163-170.
13. Farese, R. V., Jr, Ruland, S. L., Flynn, L. M., Stokowski, R. P. and Young, S. G. (1995). Knockout of the mouse apolipoprotein B gene results in embryonic lethality in homozygotes and protection against diet-induced hypercholesterolemia in heterozygotes. Proc. Natl. Acad. Sci. USA 92, 1774-1778.
14. Farese, R. V., Jr, Cases, S., Ruland, S. L., Kayden, H. J., Wong, J. S., Young, S. G. and Hamilton, R. L. (1996). A novel function for apolipoprotein B: lipoprotein synthesis in the yolk sac is critical for maternal-fetal lipid transport in mice. J. Lipid Res. 37, 347-360.
15. Fiering, S., Bender, M. A. and Groudine, M. (1999). Analysis of mammalian cis-regulatory DNA elements by homologous recombination. Methods Enzymol. 306, 42-66.
16. Garcia, C. K., Wilund, K., Arca, M., Zuliani, G., Fellin, R., Maioli, M., Calandra, S., Bertolini, S., Cossu, F., Grishin, N. et al. (2001). Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 292, 1394-1398.
17. Hasson, T. (2003). Myosin VI: two distinct roles in endocytosis. J. Cell Sci. 116, 3453-3461.
18. He, G., Gupta, S., Yi, M., Michaely, P., Hobbs, H. H. and Cohen, J. C. (2002). ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin, and AP-2. J. Biol. Chem. 277, 44044-44049.
19. Herz, J., Clouthier, D. E. and Hammer, R. E. (1992). LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 71, 411-421.
20. Herz, J., Couthier, D. E. and Hammer, R. E. (1993). Correction: LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 73, 428.
21. Inoue, A., Sato, O., Homma, K. and Ikebe, M. (2002). DOC-2/DAB2 is the binding partner of myosin VI. Biochem. Biophys. Res. Commun. 292, 300-307.
22. Johnson, M. S., Thomson, S. C. and Speakman, J. R. (2001). Limits to sustained energy intake. III. Effects of concurrent pregnancy and lactation in Mus musculus. J. Exp. Biol. 204, 1947-1956.
23. Jones, C., Hammer, R. E., Li, W. P., Cohen, J. C., Hobbs, H. H. and Herz, J. (2003). Normal sorting but defective endocytosis of the low density lipoprotein receptor in mice with autosomal recessive hypercholesterolemia. J. Biol. Chem. 278, 29024-29030.
24. Kamikura, D. M. and Cooper, J. A. (2003). Lipoprotein receptors and a disabled family cytoplasmic adaptor protein regulate EGL-17/FGF export in C. elegans. Genes Dev. 17, 2798-2811.
25. Kibbey, R. G., Rizo, J., Gierasch, L. M. and Anderson, R. G. (1998). The LDL receptor clustering motif interacts with the clathrin terminal domain in a reverse turn conformation. J. Cell Biol. 142, 59-67.
26. Koutsourakis, M., Langeveld, A., Patient, R., Beddington, R. and Grosveld, F. (1999). The transcription factor GATA6 is essential for early extraembryonic development. Development 126, 723-732.
27. Kozyraki, R., Fyfe, J., Verroust, P. J., Jacobsen, C., Dautry-Varsat, A., Gburek, J., Willnow, T. E., Christensen, E. I. and Moestrup, S. K. (2001). Megalin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc. Natl. Acad. Sci. USA 98, 12491-12496.
28. Krieger, M. and Herz, J. (1994). Structures and functions of multiligand lipoprotein receptors: macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu. Rev. Biochem. 63, 601-637.
29. Li, Y., Marzolo, M. P., van Kerkhof, P., Strous, G. J. and Bu, G. (2000). The YXXL motif, but not the two NPXY motifs, serves as the dominant endocytosis signal for low density lipoprotein receptor-related protein. J. Biol. Chem. 275, 17187-17194.
30. Matter, K., Hunziker, W. and Mellman, I. (1992). Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell 71, 741-753.
31. McCarthy, R. A., Barth, J. L., Chintalapudi, M. R., Knaak, C. and Argraves, W. S. (2002). Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 277, 25660-25667.
32. Mishra, S. K., Keyel, P. A., Hawryluk, M. J., Agostinelli, N. R., Watkins, S. C. and Traub, L. M. (2002). Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21, 4915-4926.
33. Morris, S. M. and Cooper, J. A. (2001). Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2, 111-123.
34. Morris, S. M., Arden, S. D., Roberts, R. C., Kendrick-Jones, J., Cooper, J. A., Luzio, J. P. and Buss, F. (2002a). Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3, 331-341.
35. Morris, S. M., Tallquist, M. D., Rock, C. O. and Cooper, J. A. (2002b). Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J. 21, 1555-1564.
36. Morrisey, E. E., Tang, Z., Sigrist, K., Lu, M. M., Jiang, F., Ip, H. S. and Parmacek, M. S. (1998). GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 12, 3579-3590.
37. Morrisey, E. E., Musco, S., Chen, M. Y., Lu, M. M., Leiden, J. M. and Parmacek, M. S. (2000). The gene encoding the mitogen-responsive phosphoprotein Dab2 is differentially regulated by GATA-6 and GATA-4 in the visceral endoderm. J. Biol. Chem. 275, 19949-19954.
38. Nagai, J., Christensen, E. I., Morris, S. M., Willnow, T. E., Cooper, J. A. and Nielsen, R. (2005). Mutually-dependent localization of megalin and Dab2 in the renal proximal tubule. Am J. Physiol. Renal Physiol. 289, F569-F576.
39. Norman, D., Sun, X. M., Bourbon, M., Knight, B. L., Naoumova, R. P. and Soutar, A. K. (1999). Characterization of a novel cellular defect in patients with phenotypic homozygous familial hypercholesterolemia. J. Clin. Invest. 104, 619-628.
40. Oleinikov, A. V., Zhao, J. and Makker, S. P. (2000). Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem. J. 347, 613-621.
41. Rossant, J. and Tam, P. P. (2004). Emerging asymmetry and embryonic patterning in early mouse development. Dev. Cell 7, 155-164.
42. Snow, M. H. L. (1977). Gastrulation in the mouse: Growth and regionalization of the epiblast. J. Embryol. Exp. Morph. 42, 293-303.
43. Spoelgen, R., Hammes, A., Anzenberger, U., Zechner, D., Andersen, O., Jerchow, B. and Willnow, T. E. (2005). LRP2/Megalin is required for patterning of the ventral telencephalon. Development 132, 405-414.
44. Strope, S., Rivi, R., Metzger, T., Manova, K. and Lacy, E. (2004). Mouse amnionless, which is required for primitive streak assembly, mediates cell-surface localization and endocytic function of cubilin on visceral endoderm and kidney proximal tubules. Development 131, 4787-4795.
45. Willnow, T. E., Hilpert, J., Armstrong, S. A., Rohlmann, A., Hammer, R. E., Burns, D. K. and Herz, J. (1996). Defective forebrain development in mice lacking gp330/megalin. Proc. Natl. Acad. Sci. USA 93, 8460-8464.
46. Xu, X. X., Yang, W., Jackowski, S. and Rock, C. O. (1995). Cloning of a novel phosphoprotein regulated by colony-stimulating factor 1 shares a domain with the Drosophila disabled gene product. J. Biol. Chem. 270, 14184-14191.
47. Yang, D. H., Smith, E. R., Roland, I. H., Sheng, Z., He, J., Martin, W. D., Hamilton, T. C., Lambeth, J. D. and Xu, X. X. (2002). Disabled-2 is essential for endodermal cell positioning and structure formation during mouse embryogenesis. Dev. Biol. 251, 27-44.