Distinct apical and basolateral membrane requirements for stretch-induced membrane traffic at the apical surface of bladder umbrella cells

Molecular Biology of the Cell

Volumn 20, Issue 1, 2009, Pages 282-295

  Yu, Weiqun ^a   Khandelwal, Puneet ^a   Apodaca, Gerard ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; SODIUM CHANNEL; ION CHANNEL;

ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; BASOLATERAL MEMBRANE; BLADDER EPITHELIUM; BLADDER UMBRELLA CELL; CONTROLLED STUDY; CYTOSKELETON; EPITHELIUM CELL; EXOCYTOSIS; HYDROSTATIC PRESSURE; ION TRANSPORT; MECHANOTRANSDUCTION; MEMBRANE ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RABBIT; TEMPERATURE; TENSION; TURNOVER TIME; ANIMAL; BIOLOGICAL MODEL; BLADDER; CELL MEMBRANE; CHANNEL GATING; CHEMISTRY; CYTOLOGY; ELECTROPHYSIOLOGY; ENDOCYTOSIS; MECHANICAL STRESS; METABOLISM; PHYSIOLOGY; RAT; UROTHELIUM;

ANIMALS; CELL MEMBRANE; CYTOSKELETON; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EPITHELIAL CELLS; HYDROSTATIC PRESSURE; ION CHANNEL GATING; ION CHANNELS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; RATS; STRESS, MECHANICAL; URINARY BLADDER; UROTHELIUM;

EID: 63049102324     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-04-0439     Document Type: Article

References (50)

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. Alenghat, F. J., Nauli, S. M., Kolb, R., Zhou, J., and Ingber, D. E. (2004). Global cytoskeletal control of mechanotransduction in kidney epithelial cells. Exp. Cell Res. 301, 23-30.
3. Althaus, M., Bogdan, R., Clauss, W. G., and Fronius, M. (2007). Mechano- sensitivity of epithelial sodium channels (ENaCs): laminar shear stress increases ion channel open probability. FASEB J. 21, 2389-2399.
4. Apodaca, G. (2002). Modulation of membrane traffic by mechanical stimuli. Am. J. Physiol. Renal Physiol. 282, F179 -F190.
5. Apodaca, G. (2004). The uroepithelium: not just a passive barrier. Traffic 5, 117-128.
6. Balestreire, E. M., and Apodaca, G. (2007). Apical EGF receptor signaling: regulation of stretch-dependent exocytosis in bladder umbrella cells. Mol. Biol. Cell 18, 1312-1323.
7. Barg, S., and Machado, J. D. (2008). Compensatory endocytosis in chromaffin cells. Acta Physiol. 192, 195-201.
8. Blankson, H., Holen, I., and Seglen, P. O. (1995). Disruption of the cytokeratin cytoskeleton and inhibition of hepatocytic autophagy by okadaic acid. Exp. Cell Res. 218, 522-530.
9. Bonev, A. D., and Nelson, M. T. (1993). ATP-sensitive potassium channels in smooth muscle cells from guinea pig urinary bladder. Am. J. Physiol. 264, C1190-C1200.
10. + channels are activated by laminar shear stress. J. Biol. Chem. 279, 4120-4126.
11. Effler, J. C., Iglesias, P. A., and Robinson, D. N. (2007). A mechanosensory system controls cell shape changes during mitosis. Cell Cycle 6, 30-35.
12. Elliot, G., and O'Hare, P. (1997). Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88, 223-233.
13. Ferguson, D. R. (1999). Urothelial function. B.J.U. Int. 84, 235-242.
14. Ferguson, D. R., Kennedy, I., and Burton, T. J. (1997). ATP is released from rabbit urinary bladder epithelial cells by hydrostatic pressure changes-a possible sensory mechanism? J. Physiol. 505(Pt 2), 503-511.
15. Frey, M. T., Tsai, I. Y., Russell, T. P., Hanks, S. K., and Wang, Y. L. (2006). Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. Biophys. J. 90, 3774-3782.
16. Gillespie, P. G., and Walker, R. G. (2001). Molecular basis of mechanosensory transduction. Nature 413, 194-202.
17. Gopalakrishnan, M. et al. (1999). Characterization of the ATP-sensitive potassium channels (KATP) expressed in guinea pig bladder smooth muscle cells. J. Pharmacol. Exp. Ther. 289, 551-558.
18. Henquin, J.C. (2004). Pathways in beta-cell stimulus-secretion coupling as targets for therapeutic insulin secretagogues. Diabetes 53(Suppl. 3), S48-S58.
19. Ibraghimov-Beskrovnaya, O. et al. (1997). Polycystin: in vitro synthesis, in vivo tissue expression, and subcellular localization identifies a large membrane-associated protein. Proc Natl Acad Sci USA 94, 6397-6402.
20. Ingber, D. E. (2003). Tensegrity II. How structural networks influence cellular information processing networks. J. Cell Sci. 116, 1397-1408.
21. Ingber, D. E. (2006). Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20, 811-827.
22. Jiao, J. H., Baumann, P., Baron, A., Roatti, A., Pence, R. A., and Baertschi, A. J. (2000). Sulfonylurea receptor ligands modulate stretch-induced ANF secretion in rat atrial myocyte culture. Am. J. Physiol. Heart Circ. Physiol. 278, H2028-H2038.
23. Khandelwal,P.,Ruiz,G.,Balestreire-Hawryluk,E.,Weisz,O. A.,and Goldenring, J. A. (2008). Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc. Natl. Acad. Sci. USA 105, 15773-15778.
24. 2+ channel modulation. Pfluegers Arch. 434, 362-372.
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. Kwak, B. R., Silacci, P., Stergiopulos, N., Hayoz, D., and Meda, P. (2005). Shear stress and cyclic circumferential stretch, but not pressure, alter connexin43 expression in endothelial cells. Cell Commun. Adhes. 12, 261-270.
27. Laine, M., Arjamaa, O., Vuolteenaho, O., Ruskoaho, H., and Weckstrom, M. (1994). Block of stretch-activated atrial natriuretic peptide secretion by gadolinium in isolated rat atrium. J. Physiol. 480, 553-561.
28. Lewis, S., and de Moura, J. (1984). Apical membrane area of rabbit urinary bladder increases by fusion of intracellular vesicle: an electrophysiological study. J. Membr. Biol. 82, 123-136.
29. 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.
30. Lewis, S. A., Eaton, D. C., Clausen, C., and Diamond, J. M. (1977). Nystatin as a probe for investigating the electrical properties of a tight epithelium. J. Gen. Physiol. 70, 427-440.
31. Lewis, S. A., and Hanrahan, J. W. (1990). Physiological approaches for studying mammalian urinary bladder epithelium. Methods Enzymol. 192, 632-650.
32. Lewis, S. A., and Lewis, J. R. (2006). Kinetics of urothelial ATP release. Am. J. Physiol. Renal. Physiol. 291, F332-F340.
33. Lewis, S. A., and Wills, N. K. (1983). Apical membrane permeability and kinetic properties of the sodium pump in rabbit urinary bladder. J. Physiol. 341, 169-184.
34. Moe, P., and Blount, P. (2005). Assessment of potential stimuli for mechano- dependent gating of MscL: effects of pressure, tension, and lipid headgroups. Biochemistry 44, 12239-12244.
35. Mohanty, M. J., and Li, X. (2002). Stretch-induced Ca(2 + ) release via an IP(3)-insensitive Ca(2 + ) channel. Am. J. Physiol. Cell Physiol. 283, C456-C462.
36. Ormond, C. J., Orgeig, S., Daniels, C. B., and Milsom, W. K. (2003). Thermal acclimation of surfactant secretion and its regulation by adrenergic and cholinergic agonists in type II cells isolated from warm-active and torpid golden-mantled ground squirrels, Spermophilus lateralis. J. Exp. Biol. 206, 3031-3041.
37. Rentsendorj, A., Agadjanian, H., Chen, X., Cirivello, M., Macveigh, M., Kedes, L., Hamm-Alvarez, S., and Medina-Kauwe, L. K. (2005). The Ad5 fiber mediates nonviral gene transfer in the absence of whole virus, utilizing a novel cell entry pathway. Gene Ther. 12, 225-237.
38. Richard, J. P., Melikov, K., Brooks, H., Prevot, P., Lebleu, B., and Chernomordik, L. V. (2005). Cellular uptake of unconjugated TAT peptide involves clathrin- independent endocytosis and heparan sulfate receptors. J. Biol. Chem. 280, 15300-15306.
39. + channel in human colonic crypt cells. Acta Physiol. Scand. 182, 361-368.
40. Sarikas, S. N., and Chlapowski, F. J. (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.
41. Staehelin, L., Chlapowski, F., and Bonneville, M. (1972). Lumenal plasma membrane of the urinary bladder I. Three-dimensional reconstruction from freeze-etch images. J. Cell Biol. 53, 73-91.
42. Swingle, M., Ni, L., and Honkanen, R. E. (2007). Small-molecule inhibitors of ser/thr protein phosphatases, use and common forms of abuse. Methods Mol. Biol. 365, 23-38.
43. 2+. J. Physiol. 565, 743-750.
44. Tonosaki, Y., Cruijsen, P.M.J.M., Nishiyama, K., Yaninuma, H., and Roubos, E. W. (2004). Low temperature stimulates alpha-melanophore-stimulating hormone secretion and inhibits background adaptation in Xenopus laevis. J. Neuroendocrinol. 16, 894-905.
45. Truschel, S. T., Wang, E., Ruiz, W. G., Leung, S. M., Rojas, R., Lavelle, J., Zeidel, M., Stoffer, D., and Apodaca, G. (2002). Stretch-regulated exocytosis/endocytosis in bladder umbrella cells. Mol. Biol. Cell 13, 830-846.
46. Veranic, P., and Jezernik, K. (2002). Trajectorial organisation of cytokeratins within the subapical region of umbrella cells. Cell Motil. Cytoskelet. 53, 317-325.
47. Wang, E., Truschel, S., and Apodaca, G. (2003a). Analysis of hydrostatic pressure-induced changes in umbrella cell surface area. Methods 30, 207-217.
48. Wang, E. C., Lee, J. M., Johnson, J. P., Kleyman, T. R., Bridges, R., and Apodaca, G. (2003b). Hydrostatic pressure-regulated ion transport in bladder uroepithelium. Am. J. Physiol. Renal. Physiol. 285, F651-F663.
49. Wang, E. C., Lee, J. M., Ruiz, W. G., Balestreire, E. M., von Bodungen, M., Barrick, S., Cockayne, D. A., Birder, L. A., and Apodaca, G. (2005). ATP and purinergic receptor-dependent membrane traffic in bladder umbrella cells. J Clin. Invest. 115, 2412-2422.
50. Yu, W., Zacharia, L. C., Jackson, E. K., and Apodaca, G. (2006). Adenosine receptor expression and function in bladder uroepithelium. Am. J. Physiol. Cell Physiol. 291, C254-C265.