Golgi apparatus fragmentation as a mechanism responsible for uniform delivery of uroplakins to the apical plasma membrane of uroepithelial cells

Biology of the Cell

Volumn 102, Issue 11, 2010, Pages 593-607

  Kreft, Mateja Erdani ^a   Di Giandomenico, Daniele ^b   Beznoussenko, Galina V ^b   Resnik, Nataša ^a   Mironov, Alexander A ^b   Jezernik, Kristijan ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Laboratory of Electron Microscopy   (Italy)

Author keywords

Cytoskeleton; Differentiation; Fragmentation; Golgi apparatus; Uroepithelium

Indexed keywords

ALPHA TUBULIN; CELL MARKER; CYTOKERATIN 20; CYTOKERATIN 7; GALACTOSYLTRANSFERASE; NOCODAZOLE; UROPLAKIN;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BLADDER; CELL DIFFERENTIATION; CELL MEMBRANE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EPITHELIUM CELL; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETIC TRANSFECTION; GOLGI COMPLEX; IMMUNOFLUORESCENCE; INTERMEDIATE FILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT;

ANIMALS; CELL DIFFERENTIATION; CELL MEMBRANE; CELLS, CULTURED; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GOLGI APPARATUS; HYPERTROPHY; INTERMEDIATE FILAMENTS; KERATIN-20; KERATIN-7; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MICROTUBULES; N-ACETYLLACTOSAMINE SYNTHASE; NOCODAZOLE; PROTEIN TRANSPORT; SWINE; UROTHELIUM;

EID: 78149448259     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20100024     Document Type: Article

References (39)

1. Acharya, P., Beckel, J., Ruiz, W.G., Wang, E., Rojas, R., Birder, L. and Apodaca, G. (2004) Distribution of the tight junction proteins ZO-1, occludin, and claudin-4, -8, and -12 in bladder epithelium. Am. J. Physiol. Renal. Physiol. 287, F305-F318
2. Apodaca, G. (2004) The uroepithelium: not just a passive barrier. Traffic 5, 117-128
3. Calkins, C.C., Setzer, S.V., Jennings, J.M., Summers, S., Tsunoda, K., Amagai, M. and Kowalczyk, A.P. (2006) Desmoglein endocytosis and desmosome disassembly are coordinated responses to pemphigus autoantibodies. J. Biol. Chem. 281, 7623-7634
4. Cole, N.B., Smith, C.L., Sciaky, N., Terasaki, M., Edidin, M. and Lippincott-Schwartz, J. (1996) Diffusional mobility of Golgi proteins in membranes of living cells. Science 273, 797-801 (Pubitemid 26271525)
5. Eto, D.S., Sundsbak, J.L. and Mulvey, M.M. (2006) Actin-gated intracellular growth and resurgence of uropathogenic Echerichia coli. Cell Microbiol. 8, 704-717
6. Gekle, M., Mildenberger, S., Freudinger, R., Schwerdt, G. and Silbernagl, S. (1997) Albumin endocytosis in OK cells: dependence on actin and microtubules and regulation by protein kinases. Am. J. Physiol. 272, F668-F677
7. Gruenberg, J., Griffiths, G. and Howell, K.E. (1989) Characterization of the early endosome and putative endocytotic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108, 1301-1316 (Pubitemid 19097039)
8. Hicks, R.M. (1975) The mammalian urinary bladder: an accommodating organ. Biol. Rev. 50, 215-246
9. Hu, P., Meyers, S., Liang, F.X., Deng, F.M., Kachar, B., Zeidel, M.L. and Sun, T.T. (2002) Role of membrane proteins in permeability barrier function: uroplakin ablation elevates uroepithelial permeability. Am. J. Physiol. Renal. Physiol. 283, F1200-F1207
10. Hudoklin, S., Zupancic, D. and Romih, R. (2009) Maturation of the Golgi apparatus in uroepithelial cells. Cell Tissue Res. 336, 453-463
11. Jaworski, J., Hoogenraad, C.C. and Akhmanova, A. (2008) Microtubule plus-end tracking proteins in differentiated mammalian cells. Int. J. Biochem. Cell Biol. 40, 619-637
12. Kachar, B., Liang, F.X., Lins, U., Ding,M., Wu, X.R., Stoffler, D., Aebi, U. and Sun, T.T. (1999) Three-dimensional analysis of the 16 nm uroepithelial plaque particle: luminal surface exposure, preferential head-to-head interaction, and hinge formation. J. Mol. Biol. 285, 595-608
13. Khandelwal, P., Ruiz, W.G., Balestreire-Hawryluk, E., Weisz, O.A., Goldenring, J.R. and Apodaca, G. (2008) Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc. Natl. Acad. Sci. U.S.A. 105, 15773-15778
14. Khandelwal, P., Abraham, S.N. and Apodaca, G. (2009) Cell biology and physiology of the uroepithelium. Am. J. Physiol. Renal. Physiol. 297, F1477-F14501
15. Kong, X.T., Deng, F.M., Hu, P., Liang, F.X., Zhou, G., Auerbach, A.B., Genieser, N., Nelson, P.K., Robbins, E.S., Shapiro, E., Kachar, B. and Sun, T.T. (2004) Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J. Cell Biol. 167, 1195-1204 (Pubitemid 40066633)
16. Kreft, M.E., Romih, R. and Sterle, M. (2002) Antigenic and ultrastructural markers associated with uroepithelial cytodifferentiation in primary explant outgrowths of mouse bladder. Cell Biol. Int. 26, 63-74
17. Kreft, M.E., Hudoklin, S. and Sterle, M. (2005a) Establishment and characterization of primary and subsequent subcultures of normal mouse uroepithelial cells. Folia Biologica (Praha) 51, 126-132 (Pubitemid 41645212)
18. Kreft, M.E., Sterle, M., Veranic, P. and Jezernik, K. (2005b) Uroepithelial injuries and the early wound healing response: tight junctions and uroepithelial cytodifferentiation. Histochem. Cell Biol. 123, 529-539
19. Kreft, M.E., Romih, R., Kreft, M. and Jezernik, K. (2009a) Endocytotic activity of bladder superficial uroepithelial cells is inversely related to their differentiation stage. Differentiation 77, 48-59
20. Kreft, M.E., Jezernik, K., Kreft, M. and Romih, R. (2009b) Apical plasma membrane traffic in superficial cells of bladder urothelium. Ann. N. Y. Acad. Sci. 1152, 18-29
21. Kreft, M.E., Hudoklin, S., Jezernik, K. and Romih, R. (2010) Formation and maintenance of blood-urine barrier in urothelium. Protoplasma, doi:10.1007/s00709-010-0112-1
22. Liang, F.X., Riedel, I., Deng, F.M., Zhou, G., Xu, C., Wu, X.R., Kong, X.P., Moll, R. and Sun, T.T. (2001) Organization of uroplakin subunits: transmembrane topology, pair formation and plaque composition. Biochem. J. 355, 13-18 (Pubitemid 32304230)
23. Mironov, A.A. and Beznoussenko, G.V. (2010), Molecular mechanisms responsible for formation of Golgi ribbon. Histol. Histopathol., in the press
24. Mironov, A.A., Beznoussenko, G.V., Nicoziani, P., Martella, O., Trucco, A., Kweon, H.S., Di, Giandomenico.D., Polishchuk, R.S., Fusella, A. and Lupetti, P. (2001) Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155, 1225-1238 (Pubitemid 34286272)
25. Mironov, A.A., Beznoussenko, G.V., Luini, A. and Polishchuk, R.S. (2005) Visualizing intracellular events in vivo by combined video fluorescence and 3-D electron microscopy. Methods Enzymol. 404, 43-57
26. Negrete, H.O., Lavelle, J.P., Berg, J., Lewis, S.A. and Zeidel, M.L. (1996) Permeability properties of the intact mammalian bladder epithelium. Am. J. Physiol. Renal Fluid Electrolyte Physiol. 271, F886-F894
27. Phair, R.D., Gorski, S.A. and Misteli, T. (2004) Measurement of dynamic protein binding to chromatin in vivo, using photobleaching microscopy. Methods Enzymol. 375, 393-414
28. Piasek, A. and Thyberg, J. (1980) Effect of colchicine on endocytosis of horseradish peroxidise by rat peritoneal macrophages. J. Cell Sci. 45, 59-71 (Pubitemid 11208490)
29. Presley, J.F., Cole, N.B., Schroer, T.A., Hirschberg, K., Zaal, K.J. and Lippincott-Schwartz, J. (1997) ER-to-Golgi transport visualized in living cells. Nature 389, 81-85 (Pubitemid 27387695)
30. Polishchuk, R.S., Polishchuk, E.V. and Mironov, A.A. (1999) Coalescence of Golgi fragments in microtubule-deprived living cells. Eur. J. Cell Biol. 78, 170-185
31. Rhodin, J.A.G. (1974) Histology. A Text and Atlas, University Press, New York, http://projects.galter.northwestern.edu/rhodin/ Rogalski, A.A. and Singer, S.J. (1984) Associations of elements of the Golgi apparatus with microtubules. J. Cell Biol. 99, 1092-1100 (Pubitemid 14043367)
32. Romih, R., Veranič, P. and Jezernik, K. (1999) Actin filaments during terminal differentiation of uroepithelial cells in the rat urinary bladder. Histochem. Cell Biol. 112, 375-380
33. Scales, S.J., Pepperkok, R. and Kreis, T.E. (1997) Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90, 1137-1148 (Pubitemid 27408527)
34. Sterle, M., Kreft, M.E. and Batista, U. (1997) The effect of epidermal growth factor and transforming growth factor beta 1 on proliferation and differentiation of urothelial cells in urinary bladder explant culture. Biol. Cell 89, 263-271 (Pubitemid 28022437)
35. Trucco, A., Polishchuk, R.S., Martella, O., Di Pentima, A., Fusella, A., Di Giandomenico, D., San Pietro, E., Beznoussenko, G.V., Polishchuk, E.V., Baldassarre, M. et al. (2004) Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat. Cell Biol. 6, 1071-1081
36. Truschel, S.T., Wang, E., Ruiz, W.G., Leung, S.M., Rojas, R., Lavelle, J., Zeidel, M., Stoffer, S. and Apodaca, G. (2002) Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol. Biol. Cell 13, 830-846
37. Tu, L., Sun, T.T. and Kreibich, G. (2002) Specific heterodimer formation is a prerequisite for uroplakins to exit from endoplasmic reticulum. Mol. Biol. Cell 13, 4221-4230
38. Veranič, P. and Jezernik, K. (2002) Trajectorial organisation of cytokeratins within the subapical region of umbrella cells. Cell Motil. Cytoskeleton 53, 317-325 (Pubitemid 35332730)
39. Wu, X.R., Manabe, M., Yu, J. and Sun, T.T. (1990) Large scale purification and immunolocalization of bovine uroplakins I, II, and III: molecular markers of uroepithelial differentiation. J. Biol. Chem. 265, 19170-19179