Apical plasma membrane traffic in superficial cells of bladder urothelium

Annals of the New York Academy of Sciences

Volumn 1152, Issue , 2009, Pages 18-29

  Kreft, Mateja Erdani ^a   Jezernik, Kristijan ^a   Kreft, Marko ^a,b   Romih, Rok ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Celica Biomedical Sciences Center   (Slovenia)

Author keywords

Bladder pathology; Differentiation; Endocytosis; Exocytosis; Urothelium

Indexed keywords

UROPLAKIN;

ANIMAL CELL; APICAL MEMBRANE; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE TRANSPORT; CELL SURFACE; CONFERENCE PAPER; DOWN REGULATION; ENDOCYTOSIS; EXOCYTOSIS; NONHUMAN; UROTHELIUM;

EID: 58549087372     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2008.04004.x     Document Type: Conference Paper

References (95)

1. Romih, R. et al. 2005. Differentiation of epithelial cells in the urinary tract. Cell Tissue Res. 320 : 259 268.
2. Deng, F.M. et al. 2002. Uroplakin IIIb, a urothelial differentiation marker, dimerizes with uroplakin Ib as an early step of urothelial plaque assembly. J. Cell Biol. 159 : 685 694.
3. Lin, J.H. et al. 1994. Precursor sequence, processing, and urothelium-specific expression of a major 15-kDa protein subunit of asymmetric unit membrane. J. Biol. Chem. 269 : 1775 1784.
4. Wu, X-R. et al. 1990. Large scale purification and immunolocalization of bovine uroplakins I, II, and III: molecular markers of urothelial differentiation. J. Biol. Chem. 265 : 19170 19179.
5. Wu, X-R. & T-T. Sun. 1993. Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell surface glycoprotein. J. Cell Sci. 106 : 31 43.
6. Yu, J. et al. 1994. Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins. J. Cell Biol. 125 : 171 182.
7. Berditchevski, F. 2001. Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 114 : 4143 4151.
8. Boucheix, C. & E. Rubinstein. 2004. Tetraspanins. Cell Mol. Life Sci. 58 : 1189 1205.
9. Boucheix, C. et al. 2004. A tiny thread towards a tetraspanin function. Pathol. Biol. (Paris) 52 : 55 57.
10. Hemler, M.E. 2003. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 19 : 397 422.
11. Levy, S. & T. Shoham. 2005. The tetraspanin web modulates immune-signalling complexes. Nat. Rev. Immunol. 5 : 136 148.
12. Maecker, H.T., S.C. Todd & S. Levy. 1997. The tetraspanin superfamily: molecular facilitators. FASEB J. 11 : 428 442.
13. Wu, X-R., T-T. Sun & J.J. Medina. 1996. In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proc. Nat. Acad. Sci. USA 93 : 9630 9635.
14. Zhou, G. et al. 2001. Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J. Cell Sci. 114 : 4095 4103.
15. Adachi, W., K. Okubo & S. Kinoshita. 2000. Human uroplakin Ib in ocular surface epithelium. Invest. Ophthalmol. Vis. Sci. 41 : 2900 2905.
16. Lobban, E.D. et al. 1998. Uroplakin gene expression by normal and neoplastic human urothelium. Am. J. Pathol. 153 : 1957 1967.
17. Olsburgh, J. et al. 2003. Uroplakin gene expression in normal human tissues and locally advanced bladder cancer. J. Pathol. 199 : 41 49.
18. Apodaca, G. 2004. The uroepithelium: not just a passive barrier. Traffic 5 : 117 128.
19. Staehelin, L.A., F.J. Chlapowski & M.A. Bonneville. 1972. Lumenal plasma membrane of the urinary bladder: Three-dimensional reconstruction from freeze-etch images. J. Cell Biol. 53 : 73 91.
20. Severs, N.J. & R.M. Hicks. 1979. Analysis of membrane sructure in the transitional epithelium of rat urinary bladder. The discoidal vesicles and Golgi apparatus: their role in luminal membrane biogenesis. J. Ultrastr. Res. 69 : 279 296.
21. Minsky, B.D. & F.J. Chlapowski. 1978. Morphometric analysis of the translocation of lumenal membrane between cytoplasm and cell surface of transitional epithelial cells during the expansion-contraction cycles of mammalian urinary bladder. J. Cell Biol. 77 : 685 697.
22. Hicks, R.M. & J. Chowaniec. 1978. Experimental induction, histology, and ultrastructure of hyperplasia and neoplasia of the urinary bladder epithelium. Int. Rev. Exp. Pathol. 18 : 199 280.
23. Kreft, M.E. et al. 2005. Urothelial injuries and the early wound healing response: tight junctions and urothelial differentiation. Histochem. Cell Biol. 123 : 529 539.
24. Kreft, M.E., M. Sterle & K. Jezernik. 2006. Distribution of junction- and differentiation-related proteins in urothelial cells at the leading edge of primary explant outgrowths. Histochem. Cell Biol. 125 : 475 485.
25. Romih, R. et al. 2001. Restoration of the rat urothelium after cyclophosphamide treatment. Cell Biol. Int. 25 : 531 537.
26. Romih, R., P. Veranič & K. Jezernik. 2002. Appraisal of differentiation markers in urothelial cells. Appl. Immunohistochem. Mol. Morphol. 10 : 339 343.
27. Huang, H.Y. et al. 2007. Persistent uroplakin expression in advanced urothelial carcinomas: implications in urothelial tumor progression and clinical outcome. Hum. Pathol. 38 : 1703 1713.
28. Sun, T-T. 2006. Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing. Am. J. Physiol. Renal. Physiol. 291 : F9 F21.
29. Zhang, Z.T. et al. 2001. Role of Ha-ras activation in superficial papillary pathway of urothelial tumor formation. Oncogene 20 : 1973 1980.
30. Wu, R-L. et al. 1998. Uroplakin II gene is expressed in transitional cell carcinoma but not in bilharzial bladder squamous cell carcinoma: alternative pathways of bladder epithelial differentiation and tumor formation. Cancer Res. 58 : 1291 1297.
31. Hu, C-C. et al. 2005. Assembly of urothelial plaques: tetraspanin function in membrane protein trafficking. Mol. Biol. Cell 16 : 3937 3950.
32. Tu, L., T-T. Sun & G. Kreibich. 2002. Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol. Biol. Cell 13 : 4221 4230.
33. Wu, X-R., J.J. Medina & T-T. Sun. 1995. Selective interactions of UPIa and UPIb, two members of the transmembrane 4 superfamily, with distinct single transmembrane-domained proteins in differentiated urothelial cells. J. Biol. Chem. 270 : 29752 29759.
34. Hicks, R.M. & B. Ketterer. 1969. Hexagonal lattice of subunits in the thick luminal membrane of the rat urinary bladder. Nature 224 : 1304 1305.
35. Vergara, J.A., W. Longley & J.D. Robertson. 1969. A hexagonal arrangement of subunits in membrane of mouse urinary bladder. J. Mol. Biol. 46 : 593 596.
36. Brisson, A. & R.H. Wade. 1983. Three-dimensional structure of luminal plasma membrane protein from urinary bladder. J. Mol. Biol. 166 : 21 36.
37. Hu, C-C. et al. 2008. Assembly of a membrane receptor complex: roles of the uroplakin II prosequence in regulating uroplakin bacterial receptor oligomerization. Biochem. J. doi :.
38. Hicks, R.M. 1966. The function of the Golgi complex in transitional epithelium: Synthesis of the thick cell membrane. J. Cell Biol. 30 : 623 643.
39. Koss, L.G. 1969. The asymmetric unit membranes of the epithelium of the urinary bladder of the rat. An electron microscopic study of a mechanism of epithelial maturation and function. Lab. Invest. 21 : 154 168.
40. Alroy, J. et al. 1982. Membrane differentiation in the Golgi apparatus of mammalian urinary bladder epithelium. Anat. Rec. 203 : 429 440.
41. Hicks, R.M. 1965. The fine structure of the transitional epithelium of rat ureter. J. Cell Biol. 26 : 25 48.
42. Porter, K.R., K. Kenyon & S. Badenhausen. 1967. Specialization of the unit membrane. Protoplasma 63 : 262 274.
43. Chlapowski, F.J., M.A. Bonneville & L.A. Staehelin. 1972. Lumenal plasma membrane of the urinary bladder: Isolation and structure of membrane components. J. Cell Biol. 53 : 92 104.
44. Kachar, B. et al. 1999. Three-dimensional analysis of the 16 nm urothelial plaque particle: luminal surface exposure, preferential head-to-head interaction, and hinge formation. J. Mol. Biol. 285 : 595 608.
45. Hu, P. et al. 2000. Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J. Cell Biol. 151 : 961 972.
46. Sarikas, S.N. & F.J. Chlapowski. 1989. The effect of thioglycolate on intermediate filaments and membrane translocation in rat urothelium during the expansion-contraction cycle. Cell Tissue Res. 258 : 393 401.
47. Sarikas, S.N. & F.J. Chlapowski. 1986. Effect of ATP inhibitors on the translocation of luminal membrane between cytoplasm and cell surface of transitional epithelial cells during the expansion-contraction cycle of the rat urinary bladder. Cell Tissue Res. 246 : 109 117.
48. Hicks, R.M. 1975. The mammalian urinary bladder: an accommodating organ. Biol. Rev. 50 : 215 246.
49. Truschel, S.T. et al. 2002. Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol. Biol. Cell 13 : 830 846.
50. Yu, W. et al. 2006. Adenosine receptor expression and function in bladder uroepithelium. Am. J. Physiol. Cell Physiol. 291 : C254 C265.
51. Wang, E., S.T. Truschel & G. Apodaca. 2003. Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods 30 : 207 217.
52. Wang, E.C. et al. 2005. ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J. Clin. Invest. 115 : 2412 2422.
53. Chen, Y. et al. 2003. Rab 27b is associated with fusiform vesicles and may be involved in targeting uroplakins to urothelial apical membranes. Proc. Nat. Acad. Sci. USA 100 : 14012 14017.
54. Born, M. et al. 2003. The maintenance of the permeability barrier of bladder facet cells requires a continuous fusion of discoid vesicles with the apical plasma membrane. Eur. J. Cell Biol. 82 : 343 350.
55. Veranič, P., R. Romih & K. Jezernik. 2004. What determinates differentiation of urothelial umbrella cells? Eur. J. Cell Biol. 83 : 27 34.
56. Romih, R, K. Jezernik & A. Mašera. 1998. Uroplakins and cytokeratins in the regenerating rat urothelium after sodium saccharin treatment. Histochem. Cell Biol. 109 : 263 269.
57. Romih, R., P. Veranič & K. Jezernik. 1999. Actin filaments during terminal differentiation of urothelial cells in the rat urinary bladder. Histochem. Cell Biol. 112 : 375 380.
58. Lewis, S.A. & J.L. de Moura. 1982. Incorporation of cytoplasmic vesicles into apical membrane of mammalian urinary bladder epithelium. Nature 297 : 685 688.
59. Amano, O., S. Kataoka & T.Y. Yamamoto. 1988. Derivation and termination of fusiform vesicles in the transitional epithelium of the rat urinary bladder. Tohoku. J. Exp. Med. 156 : 117 118.
60. Amano, O., S. Kataoka & T.Y. Yamamoto. 1991. Turnover of asymmetric unit membranes in the transitional epithelial superficial cells of the rat urinary bladder. Anat. Rec. 229 : 9 15.
61. Jezernik, K. & M. Sterle. 1992. Multivesicular bodies in the transitional epithelium of the neonatal mouse urinary border. Cell Biol. Int. Rep. 16 : 1219 1228.
62. Romih, R. & K. Jezernik. 1994. Endocytosis during postnatal differentiation in superficial cells of the mouse urinary bladder epithelium. Cell Biol. Int. 18 : 663 668.
63. Zhang, S.X. & H. Seguchi. 1994. The fate of the luminal asymmetric unit membrane of the superficial cell of the rat transitional epithelium. Histol. Histopathol. 9 : 315 323.
64. Martinez, J.J. et al. 2000. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J. 19 : 2803 2812.
65. Mysorekar, I.U. et al. 2002. Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J. Biol. Chem. 277 : 7412 7419.
66. Justice, S.S. et al. 2004. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. PNAS 101 : 1333 1338.
67. Duncan, M.J. et al. 2004. Bacterial penetration of bladder epithelium through lipid rafts. J. Biol. Chem. 279 : 18944 18951.
68. Eto, D.S., J.L. Sundsbak & M.M. Mulvey. 2006. Actin-gated intracellular growth and resurgence of uropathogenic Echerichia coli. Cell Microbiol. 8 : 704 717.
69. Kreplak, L. et al. 2007. Atomic force microscopy of mammalian urothelial surface. J. Mol. Biol. 374 : 365 373.
70. Bishop, B.L. et al. 2007. Cyclic AMP-regulated exocytosis of Escherichia coli from infected bladder epithelial cells. Nat. Med. 13 : 625 630.
71. Wang, H., F-X. Liang & X-P. Kong. 2008. Characteristics of phagocytic cup induced by uropathogenic Escherichia coli. J. Histochem. Cytochem. 56 : 597 604.
72. Kreft, M.E. et al. 2009. Endocytotic activity of bladder superficial urothelial cells is inversely related to their differentiation stage. Differentiation. 77 : 48 59.
73. McTaggart, L.A., R.C. Rigby & T.S. Elliott. 1990. The pathogenesis of urinary tract infections associated with Escherichia coli, Staphylococcus saprophyticus and S. epidermidis. J. Med. Microbiol. 32 : 135 141.
74. Hultgren, S.J. et al. 1993. Pilus and nonpilus bacterial adhesins: assembly and function in cell recognition. Cell 73 : 887 901.
75. Langermann, S. et al. 1997. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276 : 607 611.
76. Deborde, S. et al. 2008. Clathrin is a key regulator of basolateral polarity. Nature 452 : 719 723.
77. Barresi, V. et al. 2006. Caveolin-1 immuno-expression in human fetal tissues during mid and late gestation. Eur. J. Histochem. 50 : 183 190.
78. Fong, A. et al. 2003. Expression of caveolin-1 and caveolin-2 in urothelial carcinoma of the urinary bladder correlates with tumor grade and squamous differentiation. Am. J. Clin. Pathol. 120 : 93 100.
79. Parton, R.G. & K. Simons. 2007. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8 : 185 194.
80. Acharya, P. et al. 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.
81. Maples, C.J., W.G. Ruiz & G. Apodaca. 1997. Both microtubules and actin filaments are required for efficient postendocytotic traffic of the polymeric immunoglobulin receptor in polarized Madin-Darbay canine kidney cells. J. Biol. Chem. 272 : 6741 6751.
82. Gottlieb, T.A. et al. 1993. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120 : 695 710.
83. Fukata, M., M. Nakagawa & K. Kaibuchi. 2003. Roles of Rho-family GTPases in cell polarisation and directional migration. Curr. Opin. Cell Biol. 15 : 590 597.
84. Symons, M. & N. Rusk. 2003. Control of vesicular trafficking by Rho GTPases. Curr. Biol. 13 : R409 R418.
85. Foerg, C. et al. 2007. Differentiation restricted endocytosis of cell penetrating peptides in MDCK cells corresponds with activities of Rho-GTPases. Pharm. Res. 24 : 628 642.
86. + channel density at the apical surface of rabbit urinary bladder epithelium. Eur. J. Pharmacol. 448 : 215 223. m
87. Sachse, M. et al. 2002. Endosomes: multipurpose designs for integrating housekeeping and specialized tasks. Histochem. Cell Biol. 117 : 91 104.
88. Hu, P. et al. 2002. Role of membrane proteins in permeability barrier function: uroplakin ablation elevates urothelial permeability. Am. J. Physiol. Renal. Physiol. 283 : F1200 F1207.
89. Giltay, J.C. et al. 2004. No pathogenic mutations in the uroplakin III gene of 25 patients with primary vesicoureteral reflux. J. Urol. 171 : 931 932.
90. Kong, X-T. et al. 2004. Roles of uroplakins in plaque formation, umbrella cell enlargement, and urinary tract diseases. J. Cell Biol. 167 : 1195 1204.
91. Jiang, S. et al. Lack of major involvement of human uroplakin genes in vesicoureteral reflux: implications for disease heterogeneity. Kidney Int. 66 : 10 19.
92. Kelly, H. et al. 2005. Uroplakin III is not a major candidate gene for primary vesicoureteral reflux. Eur. J. Hum. Genet. 13 : 500 502.
93. Romih, R. et al. 2003. Inverse expression of uroplakins and inducible nitric oxide synthase in the urothelium of patients with bladder outlet obstruction. BJU Int. 91 : 507 512.
94. Romih, R. et al. 2008. Mitochondrial localization of nitric oxide synthase in partially differentiated urothelial cells of urinary bladder lesions. Appl. Immunohistochem. Mol. Morphol. 16 : 239 245.
95. Litwin, M.S. et al. 2005. Urologic diseases in America Project: analytical methods and principal findings. J. Urol. 173 : 933 937.