Release of extracellular membrane vesicles from microvilli of epithelial cells is enhanced by depleting membrane cholesterol

FEBS Letters

Volumn 583, Issue 5, 2009, Pages 897-902

  Marzesco, Anne Marie ^a   Wilsch Bräuninger, Michaela ^a   Dubreuil, Véronique ^a   Janich, Peggy ^b   Langenfeld, Katja ^a   Thiele, Christoph ^a   Huttner, Wieland B ^a   Corbeil, Denis ^b  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Cancer; CD133; Cholesterol; Epithelial cell; Microvilli; Prominin

Indexed keywords

BETA CYCLODEXTRIN; CELL PROTEIN; CHOLESTEROL; PROMININ 1; UNCLASSIFIED DRUG;

ARTICLE; CELL SHAPE; CELL STRAIN CACO 2; CELL ULTRASTRUCTURE; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MEMBRANE VESICLE; MICROVILLUS; NORMAL HUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SALIVA;

CACO-2 CELLS; CELL MEMBRANE; CHOLESTEROL; EPITHELIAL CELLS; EXTRACELLULAR SPACE; HUMANS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, ELECTRON; MICROVILLI; PROTEIN BINDING; SECRETORY VESICLES;

EID: 60749127775     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.01.048     Document Type: Article

References (34)

1. Lakkaraju A., and Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell. Biol. 18 (2008) 199-209
2. Bachy I., Kozyraki R., and Wassef M. The particles of the embryonic cerebrospinal fluid: how could they influence brain development?. Brain Res. Bull. 75 (2008) 289-294
3. Marzesco A.M., Janich P., Wilsch-Brauninger M., Dubreuil V., Langenfeld K., Corbeil D., and Huttner W.B. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 118 (2005) 2849-2858
4. Dubreuil V., Marzesco A.M., Corbeil D., Huttner W.B., and Wilsch-Brauninger M. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J. Cell Biol. 176 (2007) 483-495
5. Huttner H.B., et al. The stem cell marker prominin-1/CD133 on membrane particles in human cerebrospinal fluid offers novel approaches for studying central nervous system disease. Stem Cells 26 (2008) 698-705
6. Florek M., et al. Prominin-2 is a cholesterol-binding protein associated with apical and basolateral plasmalemmal protrusions in polarized epithelial cells and released into urine. Cell Tissue Res. 328 (2007) 31-47
7. Weigmann A., Corbeil D., Hellwig A., and Huttner W.B. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc. Natl. Acad. Sci. USA 94 (1997) 12425-12430
8. Yin A.H., et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90 (1997) 5002-5012
9. Fargeas C.A., Fonseca A.-V., Huttner W.B., and Corbeil D. Prominin-1 (CD133): from progenitor cells to human diseases. Future Lipidol. 1 (2006) 213-225
10. Karbanová J., et al. The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J. Histochem. Cytochem. 56 (2008) 977-993
11. Corbeil D., et al. The human AC133 hematopoietic stem cell antigen is also expressed in epithelial cells and targeted to plasma membrane protrusions. J. Biol. Chem. 275 (2000) 5512-5520
12. Röper K., Corbeil D., and Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2 (2000) 582-592
13. Janich P., and Corbeil D. GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett. 581 (2007) 1783-1787
14. Wang Y., Thiele C., and Huttner W.B. Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1 (2000) 952-962
15. Schmidt K., Schrader M., Kern H.-F., and Kleene R. Regulated apical secretion of zymogens in rat pancreas. Involvement of the glycosylphosphatidylinositol-anchored glycoprotein GP-2, the lectin ZG16p, and cholesterol-glycosphingolipid-enriched microdomains. J. Biol. Chem. 276 (2001) 14315-14323
16. Rodal S.K., Skretting G., Garred O., Vilhardt F., van Deurs B., and Sandvig K. Extraction of cholesterol with methyl-b-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10 (1999) 961-974
17. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., and McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. USA 96 (1999) 6775-6780
18. Thiele C., Hannah M.J., Fahrenholz F., and Huttner W.B. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol. 2 (2000) 42-49
19. Corbeil D., Fargeas C.A., and Huttner W.B. Rat prominin, like its mouse and human orthologues, is a pentaspan membrane glycoprotein. Biochem. Biophys. Res. Commun. 285 (2001) 939-944
20. Florek M., Haase M., Marzesco A.M., Freund D., Ehninger G., Huttner W.B., and Corbeil D. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res. 319 (2005) 15-26
21. Hobbs D.G. The origin and distribution of membrane-bound vesicles associated with the brush border of chick intestinal mucosa. J. Anat. 131 (1980) 635-642
22. Bar-Ziv R., Tlusty T., Moses E., Safran S.A., and Bershadsky A. Pearling in cells: a clue to understanding cell shape. Proc. Natl. Acad. Sci. USA 96 (1999) 10140-10145
23. Baumgart T., Hess S.T., and Webb W.W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425 (2003) 821-824
24. Roux A., Cuvelier D., Nassoy P., Prost J., Bassereau P., and Goud B. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J. 24 (2005) 1537-1545
25. Hansen G.H., Niels-Christiansen L.L., Thorsen E., Immerdal L., and Danielsen E.M. Cholesterol depletion of enterocytes. Effect on the Golgi complex and apical membrane trafficking. J. Biol. Chem. 275 (2000) 5136-5142
26. Needham D., and Nunn R.S. Elastic-deformation and failure of lipid bilayer-membranes containing cholesterol. Biophys. J. 58 (1990) 997-1009
27. Evans E., and Rawicz W. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64 (1990) 2094-2097
28. Chen Z., and Rand R. The influence of cholesterol on phospholipid membrane curvature and bending elasticity. Biophys. J. 73 (1997) 267-276
29. Wang W., Yang L., and Huang H.W. Evidence of cholesterol accumulated in high curvature regions: implication to the curvature elastic energy for lipid mixtures. Biophys. J. 92 (2007) 2819-2830
30. Yanagisawa M., Imai M., and Taniguchi T. Shape deformation of ternary vesicles coupled with phase separation. Phys. Rev. Lett. 100 (2008) 148102-1-148102-4
31. Jindrichova S., Novakova O., Bryndova J., Tvrzicka E., Lisa V., Novak F., and Pacha J. Corticosteroid effect on Caco-2 cell lipids depends on cell differentiation. J. Steroid Biochem. Mol. Biol. 87 (2003) 157-165
32. Tyska M.J., Mackey A.T., Huang J.-D., Copeland N.G., Jenkins N.A., and Mooseker M.S. Myosin-1a is critical for normal brush border structure and composition. Mol. Biol. Cell 16 (2005) 2443-2457
33. Tyska M.J., and Mooseker M.S. A role for myosin-1A in the localization of a brush border disaccharidase. J. Cell Biol. 165 (2004) 395-405
34. McConnell R.E., and Tyska M.J. Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J. Cell Biol. 177 (2007) 671-681