Molecular mediators for raft-dependent endocytosis of syndecan-1, a highly conserved, multifunctional receptor

Journal of Biological Chemistry

Volumn 288, Issue 20, 2013, Pages 13988-13999

  Chen, Keyang ^a   Williams, Kevin Jon ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE-SCANNING MUTAGENESIS; ALZHEIMER DISEASE; CYTOPLASMIC REGIONS; HEPARAN SULFATES; MOLECULAR EVENTS; SRC-FAMILY KINASE; TRANSMEMBRANES; TYROSINE PHOSPHORYLATION;

AMINO ACIDS; CELL MEMBRANES; ENZYMES; LIGANDS; MOLECULES; PROTEINS;

MOLECULAR BIOLOGY;

ALPHA TUBULIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN TYROSINE KINASE; PROTEOHEPARAN SULFATE; SYNDECAN 1; TYROSINE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; RAT;

ERK; LIPID RAFT; LIPOPROTEIN RECEPTOR; PROTEOGLYCAN; RECEPTOR ENDOCYTOSIS; SRC;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL MEMBRANE; CLUSTER ANALYSIS; CORTACTIN; CYTOPLASM; ENDOCYTOSIS; HUMANS; IMMUNOGLOBULIN G; LIGANDS; MEMBRANE MICRODOMAINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOSPHORYLATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RATS; SEQUENCE HOMOLOGY, AMINO ACID; SYNDECAN-1; TUBULIN;

EID: 84877901149     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.444737     Document Type: Article

References (58)

1. Nichols, B. J., and Lippincott-Schwartz, J. (2001) Endocytosis without clathrin coats. Trends Cell Biol. 11, 406-412 (Pubitemid 32903989)
2. Anderson, R. G., and Jacobson, K. (2002) A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 1821-1825 (Pubitemid 34596260)
3. Kirkham, M., and Parton, R. G. (2005) Clathrin-independent endocytosis: new insights into caveolae and noncaveolar lipid raft carriers. Biochim. Biophys. Acta 1745, 273-286 (Pubitemid 41330782)
4. Römer, W., Pontani, L. L., Sorre, B., Rentero, C., Berland, L., Chambon, V., Lamaze, C., Bassereau, P., Sykes, C., Gaus, K., and Johannes, L. (2010) Actin dynamics drive membrane reorganization and scission in clathrinindependent endocytosis. Cell 140, 540-553
5. Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E., and Zerial, M. (2005) Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436, 78-86 (Pubitemid 40966188)
6. Kartenbeck, J., Stukenbrok, H., and Helenius, A. (1989) Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109, 2721-2729 (Pubitemid 20011899)
7. Stang, E., Kartenbeck, J., and Parton, R. G. (1997) Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 8, 47-57 (Pubitemid 27294796)
8. Bonifacino, J. S., and Traub, L. M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72, 395-447 (Pubitemid 36930451)
9. Michaely, P., Zhao, Z., Li, W. P., Garuti, R., Huang, L. J., Hobbs, H. H., and Cohen, J. C. (2007) Identification of a VLDL-induced, FDNPVY-independent internalization mechanism for the LDLR. EMBO J. 26, 3273-3282 (Pubitemid 47123534)
10. Benmerah, A., and Lamaze, C. (2007) Clathrin-coated pits: vive la différence? Traffic 8, 970-982
11. Fuki, I. V., Kuhn, K. M., Lomazov, I. R., Rothman, V. L., Tuszynski, G. P., Iozzo, R. V., Swenson, T. L., Fisher, E. A., and Williams, K. J. (1997) The syndecan family of proteoglycans: novel receptors mediating internalization of atherogenic lipoproteins in vitro. J. Clin. Invest. 100, 1611-1622 (Pubitemid 27425789)
12. Fuki, I. V., Meyer, M. E., and Williams, K. J. (2000) Transmembrane and cytoplasmic domains of syndecan mediate a multistep endocytic pathway involving detergent-insoluble membrane rafts. Biochem. J. 351, 607-612
13. Williams, K. J., and Fuki, I. V. (1997) Cell-surface heparan sulfate proteoglycans: dynamic molecules mediating ligand catabolism. Curr. Opin. Lipidol. 8, 253-262 (Pubitemid 27462431)
14. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J., and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777 (Pubitemid 29449208)
15. Gingis-Velitski, S., Zetser, A., Kaplan, V., Ben-Zaken, O., Cohen, E., Levy-Adam, F., Bashenko, Y., Flugelman, M. Y., Vlodavsky, I., and Ilan, N. (2004) Heparanase uptake is mediated by cell membrane heparan sulfate proteoglycans. J. Biol. Chem. 279, 44084-44092 (Pubitemid 39390718)
16. Chen, K., Liu, M.-L., Schaffer, L., Li, M., Boden, G., Wu, X., and Williams, K. J. (2010) Type 2 diabetes in mice induces hepatic overexpression of sulfatase 2, a novel factor that suppresses uptake of remnant lipoproteins. Hepatology 52, 1957-1967
17. Sarrazin, S., Lamanna, W. C., and Esko, J. D. (2011) Heparan sulfate proteoglycans. Cold Spring Harbor Perspect. Biol. 3, a004952
18. Spring, J., Paine-Saunders, S. E., Hynes, R. O., and Bernfield, M. (1994) Drosophila syndecan: Conservation of a cell-surface heparan sulfate proteoglycan. Proc. Natl. Acad. Sci. U.S.A. 91, 3334-3338 (Pubitemid 24130231)
19. Zimmermann, P., and David, G. (1999) The syndecans, tuners of transmembrane signaling. FASEB J. 13, S91-S100 (Pubitemid 29220679)
20. Williams, K. J., and Chen, K. (2010) Recent insights into factors affecting remnant lipoprotein uptake. Curr. Opin. Lipidol. 21, 218-228
21. Granés, F., Berndt, C., Roy, C., Mangeat, P., Reina, M., and Vilaró, S. (2003) Identification of a novel ezrin-binding site in syndecan-2 cytoplasmic domain. FEBS Lett. 547, 212-216
22. Chakravarti, R., Sapountzi, V., and Adams, J. C. (2005) Functional role of syndecan-1 cytoplasmic V region in lamellipodial spreading, actin bundling, and cell migration. Mol. Biol. Cell 16, 3678-3691 (Pubitemid 41077078)
23. Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Dürr, J., and David, G. (1997) Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. U.S.A. 94, 13683-13688 (Pubitemid 28009643)
24. Cohen, A. R., Woods, D. F., Marfatia, S. M., Walther, Z., Chishti, A. H., and Anderson, J. M. (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 142, 129-138 (Pubitemid 28341145)
25. Zimmermann, P., Zhang, Z., Degeest, G., Mortier, E., Leenaerts, I., Coomans, C., Schulz, J., N'Kuli, F., Courtoy, P. J., and David, G. (2005) Syndecan recycling is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 9, 377-388 (Pubitemid 41235807)
26. Chen, K., Liu, M.-L., and Williams, K. J. (2008) Molecular determinants of endocytosis and tyrosine phosphorylation within the cytoplasmic tail of human syndecan-1, a receptor for remnant lipoproteins. Circulation 118, S-453
27. Chen, K., and Williams, K. J. (2011) Tyrosine phosphorylation of synde-can- 1, a receptor for remnant lipoproteins, triggers its binding to cortactin, an essential intracellular mediator of a novel endocytic pathway. Circulation 124, A10838
28. Wu, X., and Williams, K. J. (2012) NOX4 pathway as a source of selective insulin resistance and responsiveness. Arterioscler. Thromb. Vasc. Biol. 32, 1236-1245
29. Williams, K. J. (2001) Interactions of lipoproteins with proteoglycans. Methods Mol. Biol. 171, 457-477
30. Rauch, B. H., Millette, E., Kenagy, R. D., Daum, G., Fischer, J. W., and Clowes, A. W. (2005) Syndecan-4 is required for thrombin-induced migration and proliferation in human vascular smooth muscle cells. J. Biol. Chem. 280, 17507-17511 (Pubitemid 41389223)
31. Li, X., Herz, J., and Monard, D. (2006) Activation of ERK signaling upon alternative protease nexin-1 internalization mediated by syndecan-1. J. Cell Biochem. 99, 936-951 (Pubitemid 44522010)
32. Kinnunen, T., Kaksonen, M., Saarinen, J., Kalkkinen, N., Peng, H. B., and Rauvala, H. (1998) Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J. Biol. Chem. 273, 10702-10708 (Pubitemid 28227685)
33. Cosen-Binker, L. I., and Kapus, A. (2006) Cortactin: the gray eminence of the cytoskeleton. Physiology 21, 352-361 (Pubitemid 44511763)
34. Rothberg, K. G., Heuser, J. E., Donzell, W. C., Ying, Y. S., Glenney, J. R., and Anderson, R. G. (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682
35. Holowka, D., Gosse, J. A., Hammond, A. T., Han, X., Sengupta, P., Smith, N. L., Wagenknecht-Wiesner, A., Wu, M., Young, R. M., and Baird, B. (2005) Lipid segregation and IgE receptor signaling: a decade of progress. Biochim. Biophys. Acta 1746, 252-259 (Pubitemid 41815020)
36. 2 and plays an integral role in insulin signal transduction. Mol. Cell. Biol. 24, 1844-1854
37. Wu, X., Chen, K., and Williams, K. J. (2012) The role of pathway-selective insulin resistance and responsiveness in diabetic dyslipoproteinemia. Curr. Opin. Lipidol. 23, 334-344
38. Rhee, S. G., Kang, S. W., Jeong, W., Chang, T. S., Yang, K. S., and Woo, H. A. (2005) Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr. Opin. Cell Biol. 17, 183-189 (Pubitemid 40380942)
39. Liberali, P., Rämö, P., and Pelkmans, L. (2008) Protein kinases: starting a molecular systems view of endocytosis. Annu. Rev. Cell Dev. Biol. 24, 501-523
40. Ingley, E. (2008) Src family kinases: regulation of their activities, levels, and identification of new pathways. Biochim. Biophys. Acta 1784, 56-65
41. Wittrup, A., Zhang, S. H., Svensson, K. J., Kucharzewska, P., Johansson, M. C., Mörgelin, M., and Belting, M. (2010) Magnetic nanoparticle-based isolation of endocytic vesicles reveals a role of the heat shock protein GRP75 in macromolecular delivery. Proc. Natl. Acad. Sci. U.S.A. 107, 13342-13347
42. Giannoni, E., Taddei, M. L., and Chiarugi, P. (2010) Src redox regulation: again in the front line. Free Radic. Biol. Med. 49, 516-527
43. Wittrup, A., Zhang, S. H., ten Dam, G. B., van Kuppevelt, T. H., Bengtson, P., Johansson, M., Welch, J., Mörgelin, M., and Belting, M. (2009) ScFv antibody-induced translocation of cell-surface heparan sulfate proteoglycan to endocytic vesicles: evidence for heparan sulfate epitope specificity and role of both syndecan and glypican. J. Biol. Chem. 284, 32959-32967
44. Williams, K. J. (2008) Molecular processes that handle- and mishandle-dietary lipids. J. Clin. Invest. 118, 3247-3259
45. Hassing, H. C., Mooij, H., Guo, S., Monia, B. P., Chen, K., Kulik, W., Dallinga-Thie, G. M., Nieuwdorp, M., Stroes, E. S., and Williams, K. J. (2012) Inhibition of hepatic sulfatase-2 in vivo: A novel strategy to correct diabetic dyslipidemia. Hepatology 55, 1746-1753
46. Saphire, A. C., Bobardt, M. D., Zhang, Z., David, G., and Gallay, P. A. (2001) Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J. Virol. 75, 9187-9200 (Pubitemid 32851923)
47. de Parseval, A., Bobardt, M. D., Chatterji, A., Chatterji, U., Elder, J. H., David, G., Zolla-Pazner, S., Farzan, M., Lee, T. H., and Gallay, P. A. (2005) A highly conserved arginine in gp120 governs HIV-1 binding to both syndecans and CCR5 via sulfated motifs. J. Biol. Chem. 280, 39493-39504 (Pubitemid 41713907)
48. Mañes, S., del Real, G., Lacalle, R. A., Lucas, P., Gómez-Moutón, C., Sán-chez-Palomino, S., Delgado, R., Alcamí, J., Mira, E., and Martínez-A, C. (2000) Membrane raft microdomains mediate lateral assemblies required for HIV-1 infection. EMBO Rep. 1, 190-196
49. Liao, Z., Cimakasky, L. M., Hampton, R., Nguyen, D. H., and Hildreth, J. E. (2001) Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS Res. Hum. Retroviruses 17, 1009-1019 (Pubitemid 32881320)
50. Rawat, S. S., Viard, M., Gallo, S. A., Blumenthal, R., and Puri, A. (2006) Sphingolipids, cholesterol, and HIV-1: a paradigm in viral fusion. Glycoconj. J. 23, 189-197 (Pubitemid 43725198)
51. Yang, X., and Gabuzda, D. (1999) Regulation of human immunodeficiency virus type 1 infectivity by the ERK mitogen-activated protein kinase signaling pathway. J. Virol. 73, 3460-3466 (Pubitemid 29135742)
52. Furler, R. L., and Uittenbogaart, C. H. (2010) Signaling through the p38 and ERK pathways: a common link between HIV replication and the immune response. Immunol. Res. 48, 99-109
53. Stanford, K. I., Bishop, J. R., Foley, E. M., Gonzales, J. C., Niesman, I. R., Witztum, J. L., and Esko, J. D. (2009) Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J. Clin. Invest. 119, 3236-3245
54. Hayashi, K., Hayashi, M., Jalkanen, M., Firestone, J. H., Trelstad, R. L., and Bernfield, M. (1987) Immunocytochemistry of cell surface heparan sulfate proteoglycan in mouse tissue. A light and electron microscopic study. J. Histochem. Cytochem. 35, 1079-1088
55. Roskams, T., Moshage, H., De Vos, R., Guido, D., Yap, P., and Desmet, V. (1995) Heparan sulfate proteoglycan expression in normal human liver. Hepatology 21, 950-958
56. Williams, K. J., Liu, M.-L., Zhu, Y., Xu, X., Davidson, W. R., McCue, P., and Sharma, K. (2005) Loss of heparan N-sulfotransferase in diabetic liver: role of angiotensin II. Diabetes 54, 1116-1122 (Pubitemid 40446326)
57. Boyanovsky, B. B., Shridas, P., Simons, M., van der Westhuyzen, D. R., and Webb, N. R. (2009) Syndecan-4 mediates macrophage uptake of group V secretory phospholipase A2-modified low density lipoprotein. J. Lipid Res. 50, 641-650
58. Pelkmans, L., and Zerial, M. (2005) Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436, 128-133 (Pubitemid 40966198)