Sulfatide-tenascin interaction mediates binding to the extracellular matrix and endocytic uptake of liposomes in glioma cells

Cellular and Molecular Life Sciences

Volumn 64, Issue 4, 2007, Pages 506-515

  Shao, K ^a   Hou, Q ^a   Go, M L ^b   Duan, W ^c   Cheung, N S ^a   Feng, S S ^b   Wong, K P ^a   Yoram, A ^d   Zhang, W ^a   Huang, Z ^a   Li, Q T ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DEAKIN UNIVERSITY   (Australia)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Extracellular matrix; Ligand targeted drug delivery; Liposomes; Sulfatide; Tenascin C

Indexed keywords

CLATHRIN; GLYCOPROTEIN; LIPOSOME; SULFATIDE; TENASCIN;

ARTICLE; CAVEOLA; CONTROLLED STUDY; DRUG BINDING; DRUG PROTEIN BINDING; EXPERIMENTAL STUDY; EXTRACELLULAR MATRIX; GLIOMA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LIPID RAFT; LIPOSOMAL DELIVERY; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TARGET CELL; TUMOR CELL;

ANTIBODIES; BETA-CYCLODEXTRINS; CALCITRIOL; CLATHRIN; ENDOCYTOSIS; EXTRACELLULAR MATRIX; GLIOMA; HUMANS; LIPOSOMES; PHOSPHOLIPASE C; PROTEIN BINDING; RNA, SMALL INTERFERING; SPHINGOSINE; SUCROSE; SULFOGLYCOSPHINGOLIPIDS; TENASCIN; TUMOR CELLS, CULTURED;

EID: 33847251041     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-6419-1     Document Type: Article

References (40)

1. Allen, T. M. (2002) Ligand-targeted therapeutics in anticancer therapy. Nat. Rev. Cancer 2, 750-663.
2. Allen, T. M. and Cullis, P. R. (2004) Drug delivery systems: Entering the mainstream. Science 303, 1818-1822.
3. Chiquet-Ehrismann, R. and Chiquet, M. (2003) Tenascins: regulation and putative functions during pathological stress. J. Pathol. 200, 488-499.
4. Jones, F. S. and Jones, P. L. (2000) The tenascin family of ECM glycoproteins: Structure, function, and regulation during embryonic development and tissue remodeling. Dev. Dyn. 218, 235-259.
5. Marty, C., Odermatt, B., Schott, H., Neri, D., Ballmer-Hofer, K., Klemenz, R. and Schwendener, R. A. (2002) Cytotoxic targeting of F9 teratocarcinoma tumours with anti-ED-B fibronectin scFv antibody modified liposomes. Br. J. Cancer 87, 106-112.
6. Hallahan, D., Geng, L., Qu, S., Scarfone, C., Giorgio, T., Donnelly, E., Gao, X. and Clanton, J. (2003) Integrin-mediated targeting of drug delivery to irradiated tumor blood vessels. Cancer Cell 3, 63-74.
7. Dunehoo, A. L., Anderson, M., Majumdar, S., Kobayashi, N., Berkland, C. and Siahaan, T. J. (2006) Cell adhesion molecules for targeted drug delivery. J. Pharm. Sci. 95, 1856-1872.
8. Vos, J. P., Lopes-Cardozo, M. and Gadella, B. M. (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta 1211, 125-149.
9. Han, X., Holtzman, D. M., McKeel, D. W. Jr., Kelley, J. and Morris, J. C. (2002) Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer's disease: potential role in disease pathogenesis. J. Neurochem. 82, 809-818.
10. Merten, M. and Thiagarajan, P. (2001) Role for sulfatides in platelet aggregation. Circulation 104, 2955-2960.
11. Crossin, K. L. and Edelman, G. M. (1992) Specific binding of cytotactin to sulfated glycolipids. J. Neurosci. Res. 33, 631-638.
12. Pesheva, P., Gloor, S., Schachner, M. and Probstmeier, R. (1997) Tenascin-R is an intrinsic autocrine factor for oligodendrocyte differentiation and promotes cell adhension by a sulfatide-mediated mechanism. J. Neurosci.17, 4642-4651.
13. Miura, R., Aspberg, A., Ethell, I. M., Hagihara, K., Schnaar, R. L., Ruoslahti, E. and Yamaguchi, Y. (1999) The proteoglycan lectin domain binds sulfated cell surface glycolipids and promotes cell adhesion. J. Biol. Chem. 274, 11431-11438.
14. Roberts, D. D., Rao, C. N., Magnani, J. L., Spitalnik, S. L., Liotta, L. A. and Ginsburg,V. (1985) Laminin binds specifically to sulfated glycolipids. Proc. Natl. Acad. Sci. USA 82, 1306-1310.
15. Chen, D. S., Li, Q.-T. and Lee, K. H. (1993) Antinociceptive activity of liposome-entrapped calcitonin by systemic administration in mice. Brain Res. 603, 139-142.
16. Wu, X., Lee, K. H. and Li, Q.-T. (1996) Stability and pH sensitivity of sulfatide-containing phosphatidylethanolamine small unilamellar vesicles. Biochim. Biophys. Acta 1248, 13-19.
17. Wu,X. and Li,Q.-T. (1999) Hydration and stability of sulfatide-containing phosphatidylethanolamine small unilamellar vesicles. Biochim. Biophys. Acta 1416, 285-294.
18. Olson, F., Hunt, C. A., Szoka, F. C., Vail, W. J. and Papahadjopoulos, D. (1979) Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes. Biochim. Biophys. Acta 557, 9-23.
19. Alvarez-Dolado, M., Gonzalez-Sancho, J. M., Navarro-Yubero, C., Garcia-Fernandez, L. F. and Munoz, A. (1999) Retinoic acid and 1,25-dihydroxyvitamin D3 inhibit tenascin-C expression in rat glioma C6 cells. J. Neurosci. Res. 58, 293-300.
20. Gonzalez-Sancho, J. M., Alvarez-Dolado, M. and Munoz, A. (1998) 1,25-Dihydroxyvitamin D3 inhibits tenascin-C expression in mammary epithelial cells. FEBS Lett. 426, 225-228.
21. Wolf, A. A., Fujinaga, Y. and Lencer, W. I. (2002) Uncoupling of the cholera toxin-G (M1) ganglioside receptor complex from endocytosis, retrograde Golgi trafficking, and downstream signal transduction by depletion of membrane cholesterol. J. Biol. Chem. 277, 16249-16256.
22. Zenni, M. K., Giardina, P. C., Harvey, H.A., Shao, J., Ketterer, M. R., Lubaroff, D. M., Williams, R. D. and Apicella, M. A. (2000) Macropinocytosis as a mechanism of entry into primary human urethral epithelial cells by Neisseria gonorrhoeae. Infect. Immun. 688, 1696-1699.
23. Sofer, A. and Futerman, A. H. (1995) Cationic amphiphilic drugs inhibit the internalization of cholera toxin to the Golgi apparatus and the subsequent elevation of cyclic AMP. J. Biol. Chem. 270, 12117-12122.
24. Heuser, J. E. and Anderson, R. G. (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108, 389-400.
25. Ricci, V., Galmiche, A., Doye, A., Necchi, V., Solcia, E. and Boquet, P. (2000) High cell sensitivity to Helicobacter pylori VacA toxin depends on a GPI-anchored protein and is not blocked by inhibition of the clathrin-mediated pathway of endocytosis. Mol. Biol. Cell 11, 3897-3909.
26. Peters, P. J., Mironov, A. Jr., Peretz, D., van Donselaar, E., Leclerc, E., Erpel, S., DeArmond, S. J., Burton, D. R., Williamson, R. A., Vey, M. and Prusiner, S. B. (2003) Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J. Cell Biol. 162, 703-717.
27. Liu, S.-H., Marks, M. S. and Brodsky, F.M. (1998) A dominant-negative clathrin mutant differentially affects trafficking of molecules with distinct sorting motifs in the class II major histocompatibility complex (MHC) pathway. J. Cell Biol. 140, 1023-1037.
28. Marty, C., Meylan, C., Schott, H., Ballmer-Hofer, K. and Schwendener, R. A. (2004) Enhanced heparan sulfate proteoglycan-mediated uptake of cell-penetrating peptide-modified liposomes, Cell. Mol. Life Sci. 61, 1785-1794.
29. Sauer, I., Dunay, I. R., Weisgraber, K., Bienert, M. and Dathe, M. (2005) An apolipoprotein E-derived peptide mediates uptake of sterically stabilized liposomes into brain capillary endothelial cells. Biochemistry 44, 2021-2029.
30. Ventimiglia, J.B., Wiskstrand, C. J., Ostrowski, L. E., Bourdon, M. A., Lightner, V. A. and Bigner, D. D. (1992) Tenascin expression in human glioma cell lines and normal tissues. J. Neuroimmunol. 36, 41 -55.
31. Swanson, J. A. and Watts, C. (1995) Macropinocytosis. Trends Cell Biol. 5, 424-428.
32. Rodal, S. K., Skretting, G., Garred, O., Vilhard, F., van Deurs, B. and Sandvig, K. (1999) Extraction of cholesterol with methyl-β-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10, 961-974.
33. Rejman, J., Oberle, V., Zuhorn, I. S. and Hoekstra, D. (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolar-mediated endocytosis. Biochem. J. 377, 159-169.
34. Puri, V., Watanabe, R., Singh, R.D., Dominguez, M., Brown, J. C., Wheatley, C. L., Marks, D. L. and Pagano, R. E. (2001) Clathrin-dependent and -independent interaction of plasma membrane sphingolipids initiates two Golgi targeting pathways. J. Cell Biol. 154, 535-547.
35. Singh, R.D., Puri, V., Valiyaveettil, J.T., Marks, D.L., Bittman, R. and Pagano, R. E. (2003) Selective caveolin-1-dependent endocytosis of glycosphingolipids. Mol. Biol. Cell 14, 3254-3265.
36. Altschuler, Y., Liu, S.-H., Katz, L., Tang, K., Hardy, S., Brodsky, F., Apodaca, G. and Mostov, K. (1999) ADP-ribosylation factor 6 and endocytosis at the apical surface of Madin-Darby canine kidney cells. J. Cell Biol. 147, 7-12.
37. Enam, S.A., Rosenblum, M. L. and Edvardsen, K. (1998) Role of extracellular matrix in tumor invasion: migration of glioma cells along fibronectin-positive mesenchymal cell processes. Neurosurgery 42, 599-607.
38. Carver, L.A. and Schnitzer, J. E. (2003) Caveolae:mining little caves for new cancer targets. Nat. Rev. Cancer 3, 571-581.
39. Bathori, G., Cervenak, L. and Karadi, I. (2004) Caveolae - an alternative endocytotic pathway for targeted drug delivery. Crit. Rev. Ther. Drug Carrier Syst. 21, 67-95.
40. Shao, K., Hou, Q., Duan, W., Go, M. L., Wong, K. P. and Li, Q.-T. (2006) Intracellular drug delivery by sulfatide-mediated liposomes to gliomas. J. Control. Release 115, 150-157.