Structural basis of urothelial permeability barrier function as revealed by Cryo-EM studies of the 16 nm uroplakin particle

Journal of Cell Science

Volumn 116, Issue 20, 2003, Pages 4087-4094

  Min, Guangwei ^a   Zhou, Ge ^a   Schapira, Matthieu ^a   Sun, Tung Tien ^a   Kong, Xiang Peng ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Electron cryo microscopy; Permeability barrier; Plasma membrane; Tetraspanin; Uroplakin; Urothelium

Indexed keywords

LIPID; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; PROTEIN SUBUNIT; RECEPTOR PROTEIN; UROPLAKIN;

ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; CELL ACTIVATION; CELL MEMBRANE; CELL STRUCTURE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; LIPID COMPOSITION; MEMBRANE FLUIDITY; NONHUMAN; PARTICLE SIZE; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; UROTHELIUM;

ANIMALS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; IMAGING, THREE-DIMENSIONAL; LIPID METABOLISM; MEMBRANE FLUIDITY; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MODELS, STRUCTURAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; URINARY BLADDER; UROTHELIUM;

ANIMALIA; ESCHERICHIA COLI; MAMMALIA;

EID: 0242287924     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00811     Document Type: Review

References (67)

1. Agard, D. A. (1983). A least-squares method for determining structure factors in three- dimensional tilted-view reconstructions. J. Mol. Biol. 167, 849-852.
2. Bienstock, R. J. and Barrett, J. C. (2001). KAI1, a prostate metastasis suppressor: prediction of solvated structure and interactions with binding partners; integrins, cadherins, and cell-surface receptor proteins. Mol. Carcinogen. 32, 139-153.
3. Boucheix, C. and Rubinstein, E. (2001). Tetraspanins. Cell. Mol. Life Sci. 58, 1189-1205.
4. Brisson, A. and Wade, R. H. (1983). Three-dimensional structure of luminal plasma membrane protein from urinary bladder. J. Mol. Biol. 166, 21-36.
5. Brown, D. A. and London, E. (2000). Structure and function of sphingolipid-and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224.
6. CCP4 (1994). The CCP4 suite: programs for protein crystallography. Acta Cryst. D50, 760-763.
7. Chang, A., Hammond, T. G., Sun, T. T. and Zeidel, M. L. (1994). Permeability properties of the mammalian bladder apical membrane. Am. J. Physiol. 267, C1483-C1492.
8. Crowther, R. A., Henderson, R. and Smith, J. M. (1996). MRC image processing programs. J. Struct. Biol. 116, 9-16.
9. Deng, F. M., Liang, F. X., Tu, L., Resing, K. A., Hu, P., Supino, M., Hu, C. C., Zhou, G., Ding, M., Kreibich, G. 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.
10. Hagberg, L., Jodal, U., Korbonen, T. K., Lidin-Janson, G., Lindberg, U. and Svanborg Eden, C. (1981). Adhesion, hemagglutination, and virulence of Escherichia coli causing urinary tract infections. Infect. Immun. 31, 564-570.
11. Hemler, M. E. (2001). Specific tetraspanin functions. J. Cell Biol. 155, 1103-1108.
12. Henderson, R., Baldwin, J. M., Ceska, T. A., Zemlin, F., Beckmann, E. and Downing, K. H. (1990). Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 213, 899-929.
13. Hicks, R. M. (1975). The mammalian urinary bladder: an accommodating organ. Biol. Rev. Camb. Philos. Soc. 50, 215-246.
14. Hicks, R. M. and Ketterer, B. (1969). Hexagonal lattice of subunits in the thick luminal membrane of the rat urinary bladder. Nature 224, 1304-1305.
15. Hicks, R. M., Ketterer, B. and Warren, R. C. (1974). The ultrastructure and chemistry of the luminal plasma membrane of the mammalian urinary bladder: a structure with low permeability to water and ions. Philos. Trans. R. Soc. London. Ser. B 268, 23-38.
16. Hill, W. G., Rivers, R. L. and Zeidel, M. L. (1999). Role of leaflet asymmetry in the permeability of model biological membranes to protons, solutes, and gases. J. Gen. Physiol. 114, 405-414.
17. Hill, W. G. and Zeidel, M. L. (2000). Reconstituting the barrier properties of a water-tight epithelial membrane by design of leaflet-specific liposomes. J Biol. Chem. 275, 30176-30185.
18. Hooton, T. M. and Stamm, W. E. (1997). Diagnosis and treatment of uncomplicated urinary tract infection. Infect. Disease Clinics North America 11, 551-81.
19. Hu, P., Deng, F. M., Liang, F. X., Hu, C. M., Auerbach, A. B., Shapiro, E., Wu, X. R., Kachar, B. and Sun, T. T. (2000). Ablation of uroplakin III gene results in small urothelial plaques, urothelial leakage, and vesicoureteral reflux. J Cell Biol, 151, 961-972.
20. 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 urothelial permeability. Am. J. Physiol. Renal Physiol. 283, F1200-F1207.
21. Johnson, J. R. (1991). Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 4, 80-128.
22. Jones, T. A., Zou, J. Y., Cowan, S. W. and Kjeldgaad, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A47, 110-119.
23. Kachar, B., Liang, F., Lins, U., Ding, M., Wu, X. R., Stoffler, D., Aebi, U. and Sun, T. T. (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.
24. Kitadokoro, K., Bordo, D., Galli, G., Petracca, R., Falugi, F., Abrignani, S., Grandi, G. and Bolognesi, M. (2001). CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. EMBO J. 20, 12-18.
25. 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.
26. Krylov, A. V., Pohl, P., Zeidel, M. L. and Hill, W. G. (2001). Water permeability of asymmetric planar lipid bilayers: leaflets of different composition offer independent and additive resistances to permeation. J. Gen. Physiol. 118, 333-340.
27. Lande, M. B., Donovan, J. M. and Zeidel, M. L. (1995). The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J. Gen. Physiol. 106, 67-84.
28. Langermann, S., Palaszynski, S., Barnhart, M., Auguste, G., Pinkner, J. S., Burlein, J., Barren, P., Koenig, S., Leath, S., Jones, C. H. et al. (1997). Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 276, 607-611.
29. Lewis, S. A. (2000). Everything you wanted to know about the bladder epithelium but were afraid to ask. Am. J. Physiol. Renal Physiol. 278, F867-F874.
30. Lewis, S. A. and de Moura, J. L. (1982). Incorporation of cytoplasmic vesicles into apical membrane of mammalian urinary bladder epithelium. Nature 297, 685-688.
31. Liang, F., Kachar, B., Ding, M., Zhai, Z., Wu, X. R. and Sun, T. T. (1999). Urothelial hinge as a highly specialized membrane: detergent- insolubility, urohingin association, and in vitro formation. Differentiation 65, 59-69.
32. 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.
33. Lin, J. H., Wu, X. R., Kreibich, G. and Sun, T. T. (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.
34. Maecker, H. T., Todd, S. C. and Levy, S. (1997). The tetraspanin superfamily: molecular facilitators. FASEB J. 11, 428-442.
35. Min, G., Stolz, M., Zhou, G., Liang, F., Sebbel, P., Stoffler, D., Glockshuber, R., Sun, T. T., Aebi, U. and Kong, X. P. (2002). Localization of uroplakin Ia, the urothelial receptor for bacterial adhesin FimH, on the six inner domains of the 16 nm urothelial plaque particle. J. Mol. Biol. 317, 697-706.
36. Minsky, B. D. and Chlapowski, F. J. (1978). Morphometric analysis of the translocation of luminal 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.
37. Mulvey, M. A., Lopez-Boado, Y. S., Wilson, C. L., Roth, R., Parks, W. C., Heuser, J. and Hultgren, S. J. (1998). Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 282, 1494-1497.
38. Mulvey, M. A., Schilling, J. D., Martinez, J. J. and Hultgren, S. J. (2000). From the Cover: Bad bugs and beleaguered bladders: Interplay between uropathogenic Escherichia coli and innate host defenses. Proc. Natl. Acad. Sci. USA 97, 8829-8835.
39. Negrete, H. O., Lavelle, J. P., Berg, J., Lewis, S. A. and Zeidel, M. L. (1996a). Permeability properties of the intact mammalian bladder epithelium. Am. J. Physiol. 271, F886-F894.
40. Negrete, H. O., Rivers, R. L., Goughs, A. H., Colombini, M. and Zeidel, M. L. (1996b). Individual leaflets of a membrane bilayer can independently regulate permeability. J. Biol. Chem. 271, 11627-11630.
41. Oostergetel, G. T., Keegstra, W. and Brisson, A. (2001). Structure of the major membrane protein complex from urinary bladder epithelial cells by cryo-electron crystallography. J. Mol. Biol. 314, 245-252.
42. Porter, K. R., Kenyon, K. and Badenhausen, S. (1967). Specialization of the unit membrane. Protoplasma 63, 262-274.
43. Robertson, J. D. and Vergara, J. (1980). Analysis of the structure of intramembrane particles of the mammalian urinary bladder. J. Cell Biol. 86, 514-528.
44. Schilling, J. D. and Hultgren, S. J. (2002). Recent advances into the pathogenesis of recurrent urinary tract infections: the bladder as a reservoir for uropathogenic Escherichia coli. Int. J. Antimicrob. Agents 19, 457-460.
45. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
46. Simons, K. and van Meer, G. (1988). Lipid sorting in epithelial cells. Biochemistry 27, 6197-6202.
47. Staehelin, L. A., Chlapowski, F. J. and Bonneville, M. A. (1972). Lumenal plasma membrane of the urinary bladder. I. Three-dimensional reconstruction from freeze-etch images. J. Cell Biol. 53, 73-91.
48. Stubbs, C. D., Ketterer, B. and Hicks, R. M. (1979). The isolation and analysis of the luminal plasma membrane of calf urinary bladder epithelium. Biochim. Biophys. Acta 558, 58-72.
49. Sun, T. T., Liang, F. X. and Wu, X. R. (1999). Uroplakins as markers of urothelial differentiation. Adv. Exp. Med. Biol. 462, 7-18.
50. Svanborg, C. and de Man, P. (1987). Bacterial virulence in urinary tract infection. Infect. Disease Clinics North America 1, 731-750.
51. Taylor, K. A. and Robertson, J. D. (1984). Analysis of the three-dimensional structure of the urinary bladder epithelial cell membranes. J. Ultrastruct. Res. 87, 23-30.
52. Tu, L., Sun, T. T. and Kreibich, G. (2002). Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol. Biol. Cell 13, 4221-4230.
53. Unger, V. M. and Schertler, G. F. (1995). Low resolution structure of bovine rhodopsin determined by electron cryo-microscopy. Biophys. J. 68, 1776-1786.
54. van Meer, G. and Lisman, Q. (2002). Sphingolipid transport: rafts and translocators. J. Biol. Chem. 277, 25855-25858.
55. Vergara, J., Longley, W. and Robertson, J. D. (1969). A hexagonal arrangement of subunits in membrane of mouse urinary bladder. J. Mol. Biol. 46, 593-596.
56. Vergara, J., Zambrano, F., Robertson, J. D. and Elrod, H. (1974). Isolation and characterization of luminal membranes from urinary bladder. J. Cell Biol. 61, 83-94.
57. Walz, T., Haner, M., Wu, X. R., Henn, C., Engel, A., Sun, T. T. and Aebi, U. (1995). Towards the molecular architecture of the asymmetric unit membrane of the mammalian urinary bladder epithelium: a closed "twisted ribbon" structure. J. Mol. Biol. 248, 887-900.
58. Wang, D. N. and Kuhlbrandt, W. (1991). High-resolution electron crystallography of light-harvesting chlorophyll a/b-protein complex in three different media. J. Mol. Biol. 217, 691-699.
59. Warren, R. C. and Hicks, R. M. (1978). Chemical dissection and negative staining of the bladder luminal membrane. J. Ultrastruct. Res. 64, 327-340.
60. Wu, X. R., Lin, J. H., Walz, T., Haner, M., Yu, J., Aebi, U. and Sun, T. T. (1994). Mammalian uroplakins. A group of highly conserved urothelial differentiation-related membrane proteins. J. Biol. Chem. 269, 13716-13724.
61. 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 urothelial differentiation. J. Biol. Chem. 265, 19170-19179.
62. Wu, X. R., Medina, J. J. and Sun, T. T. (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.
63. Wu, X. R. and Sun, T. T. (1993). Molecular cloning of a 47 kDa tissue-specific and differentiation- dependent urothelial cell surface glycoprotein. J. Cell Sci. 106, 31-43.
64. Wu, X. R., Sun, T. T. and Medina, J. J. (1996). In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proc. Natl. Acad. Sci. USA 93, 9630-9635.
65. Yu, J., Lin, J. H., Wu, X. R. and Sun, T. T. (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.
66. Yu, J., Manabe, M., Wu, X. R., Xu, C., Surya, B. and Sun, T. T. (1990). Uroplakin I: a 27-kD protein associated with the asymmetric unit membrane of mammalian urothelium. J. Cell Biol. 111, 1207-1216.
67. Zhou, G., Mo, W. J., Min, G. W., Sebbel, P., Neubert, T. A., Glockshuber, R., Wu, X. R., Sun, T. T. and Kong, X. P. (2001). Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J. Cell Sci. 114, 4095-4103.