Formation of the apical pole of epithelial (Madin-Darby canine kidney) cells: polarity of an apical protein is independent of tight junctions while segregation of a basolateral marker requires cell-cell interactions

doi:10.1083/jcb.104.4.905

This Article

	Full Text (PDF, 3221K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Vega-Salas, D. E.
	Articles by Rodriguez-Boulan, E.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Vega-Salas, D. E.
	Articles by Rodriguez-Boulan, E.


Social Bookmarking

	What's this?

ARTICLES

Formation of the apical pole of epithelial (Madin-Darby canine kidney) cells: polarity of an apical protein is independent of tight junctions while segregation of a basolateral marker requires cell-cell interactions

DE Vega-Salas, PJ Salas, D Gundersen and E Rodriguez-Boulan

The time course of development of polarity of an apical (184-kD) and a basolateral (63-kD) plasma membrane protein of Madin-Darby canine kidney cells was followed using semiquantitative immunofluorescence on semithin (approximately 0.5-micron) frozen sections and monoclonal antibody probes. The 184-kD protein became highly polarized to the apical pole within the initial 24 h both in normal medium and in 1-5 microM Ca2+, which results in well-spread, dome-shaped cells, lacking tight junctions and other lateral membrane interactions. In contrast, the basolateral 63-kD membrane protein developed full polarity only after incubation in normal Ca2+ concentrations for greater than 72 h, a time much longer than that required for the formation of tight junctions (approximately 18 h) and failed to polarize in 1-5 microM Ca2+. These results demonstrate that intradomain restriction mechanisms independent of tight junctions, such as self-aggregation or specific interactions with the submembrane cytoskeleton, participate in the regionalization of at least some epithelial plasma membrane proteins. The full operation of these mechanisms depends on the presence of normal cell-cell interactions in the case of the basolateral 63-kD antigen but not in the case of the apical 184-kD protein.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Masuda-Hirata, M., Suzuki, A., Amano, Y., Yamashita, K., Ide, M., Yamanaka, T., Sakai, M., Imamura, M., Ohno, S. (2009). Intracellular polarity protein PAR-1 regulates extracellular laminin assembly by regulating the dystroglycan complex. GENES CELLS 14: 835-850 [Abstract] [Full Text]
Konopka, G., Tekiela, J., Iverson, M., Wells, C., Duncan, S. A. (2007). Junctional Adhesion Molecule-A Is Critical for the Formation of Pseudocanaliculi and Modulates E-cadherin Expression in Hepatic Cells. J. Biol. Chem. 282: 28137-28148 [Abstract] [Full Text]
Nejsum, L. N., Nelson, W. J. (2007). A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. JCB 178: 323-335 [Abstract] [Full Text]
Gravotta, D., Deora, A., Perret, E., Oyanadel, C., Soza, A., Schreiner, R., Gonzalez, A., Rodriguez-Boulan, E. (2007). AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells. Proc. Natl. Acad. Sci. USA 104: 1564-1569 [Abstract] [Full Text]
Schneider, M., Khalil, A. A., Poulton, J., Castillejo-Lopez, C., Egger-Adam, D., Wodarz, A., Deng, W.-M., Baumgartner, S. (2006). Perlecan and Dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization. Development 133: 3805-3815 [Abstract] [Full Text]
Mak, G. Z., Kavanaugh, G. M., Buschmann, M. M., Stickley, S. M., Koch, M., Goss, K. H., Waechter, H., Zuk, A., Matlin, K. S. (2006). Regulated Synthesis and Functions of Laminin 5 in Polarized Madin-Darby Canine Kidney Epithelial Cells. Mol. Biol. Cell 17: 3664-3677 [Abstract] [Full Text]
Hua, W., Sheff, D., Toomre, D., Mellman, I. (2006). Vectorial insertion of apical and basolateral membrane proteins in polarized epithelial cells revealed by quantitative 3D live cell imaging.. JCB 172: 1035-1044 [Abstract] [Full Text]
Utech, M., Ivanov, A. I., Samarin, S. N., Bruewer, M., Turner, J. R., Mrsny, R. J., Parkos, C. A., Nusrat, A. (2005). Mechanism of IFN-{gamma}-induced Endocytosis of Tight Junction Proteins: Myosin II-dependent Vacuolarization of the Apical Plasma Membrane. Mol. Biol. Cell 16: 5040-5052 [Abstract] [Full Text]
Yu, W., Datta, A., Leroy, P., O'Brien, L. E., Mak, G., Jou, T.-S., Matlin, K. S., Mostov, K. E., Zegers, M. M.P. (2005). {beta}1-Integrin Orients Epithelial Polarity via Rac1 and Laminin. Mol. Biol. Cell 16: 433-445 [Abstract] [Full Text]
Bazzoni, G., Dejana, E. (2004). Endothelial Cell-to-Cell Junctions: Molecular Organization and Role in Vascular Homeostasis. Physiol. Rev. 84: 869-901 [Abstract] [Full Text]
Prahalad, P., Calvo, I., Waechter, H., Matthews, J. B., Zuk, A., Matlin, K. S. (2004). Regulation of MDCK cell-substratum adhesion by RhoA and myosin light chain kinase after ATP depletion. Am. J. Physiol. Cell Physiol. 286: C693-C707 [Abstract] [Full Text]
Yeaman, C., Grindstaff, K. K., Nelson, W. J. (2004). Mechanism of recruiting Sec6/8 (exocyst) complex to the apical junctional complex during polarization of epithelial cells. J. Cell Sci. 117: 559-570 [Abstract] [Full Text]
Nelson, W. J. (2003). Epithelial Cell Polarity From the Outside Looking In. Physiology 18: 143-146 [Abstract] [Full Text]
Wald, F. A., Figueroa, Y., Oriolo, A. S., Salas, P. J. I. (2003). Membrane repolarization is delayed in proximal tubules after ischemia-reperfusion: possible role of microtubule-organizing centers. Am. J. Physiol. Renal Physiol. 285: F230-F240 [Abstract] [Full Text]
Nakamura, K., Hirano, J., Itazawa, S.-I., Kubokawa, M. (2002). Protein kinase G activates inwardly rectifying K+ channel in cultured human proximal tubule cells. Am. J. Physiol. Renal Physiol. 283: F784-F791 [Abstract] [Full Text]
Magyar, C. E., White, K. E., Rojas, R., Apodaca, G., Friedman, P. A. (2002). Plasma membrane Ca2+-ATPase and NCX1 Na+/Ca2+ exchanger expression in distal convoluted tubule cells. Am. J. Physiol. Renal Physiol. 283: F29-F40 [Abstract] [Full Text]
Yeaman, C., Grindstaff, K. K., Wright, J. R., Nelson, W. J. (2001). Sec6/8 complexes on trans-Golgi network and plasma membrane regulate late stages of exocytosis in mammalian cells. JCB 155: 593-604 [Abstract] [Full Text]
Ojakian, G., Ratcliffe, D., Schwimmer, R (2001). Integrin regulation of cell-cell adhesion during epithelial tubule formation. J. Cell Sci. 114: 941-952 [Abstract]
Yanez-Mo, M, Tejedor, R, Rousselle, P, Sanchez -Madrid, F (2001). Tetraspanins in intercellular adhesion of polarized epithelial cells: spatial and functional relationship to integrins and cadherins. J. Cell Sci. 114: 577-587 [Abstract]
Tanentzapf, G., Smith, C., McGlade, J., Tepass, U. (2000). Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis. JCB 151: 891-904 [Abstract] [Full Text]
Salas, P. J.I. (1999). Insoluble {gamma}-Tubulin-Containing Structures Are Anchored to the Apical Network of Intermediate Filaments in Polarized Caco-2 Epithelial Cells. JCB 146: 645-658 [Abstract] [Full Text]
Le, T. L., Yap, A. S., Stow, J. L. (1999). Recycling of E-Cadherin: A Potential Mechanism for Regulating Cadherin Dynamics. JCB 146: 219-232 [Abstract] [Full Text]
Gallicano, G. I., Kouklis, P., Bauer, C., Yin, M., Vasioukhin, V., Degenstein, L., Fuchs, E. (1998). Desmoplakin Is Required Early in Development for Assembly of Desmosomes and Cytoskeletal Linkage. JCB 143: 2009-2022 [Abstract] [Full Text]
Takada, M., Yai, H., Komazaki, S. (1998). Effect of calcium on development of amiloride-blockable Na+ transport in axolotl in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 275: R69-R75 [Abstract] [Full Text]
Grindstaff, K. K., Bacallao, R. L., Nelson, W. J. (1998). Apiconuclear Organization of Microtubules Does Not Specify Protein Delivery from the Trans-Golgi Network to Different Membrane Domains in Polarized Epithelial Cells. Mol. Biol. Cell 9: 685-699 [Abstract] [Full Text]
Herrera, R (1998). Modulation of hepatocyte growth factor-induced scattering of HT29 colon carcinoma cells. Involvement of the MAPK pathway. J. Cell Sci. 111: 1039-1049 [Abstract]
Hobert, M. E., Kil, S. J., Medof, M. E., Carlin, C. R. (1997). The Cytoplasmic Juxtamembrane Domain of the Epidermal Growth Factor Receptor Contains a Novel Autonomous Basolateral Sorting Determinant. J. Biol. Chem. 272: 32901-32909 [Abstract] [Full Text]
Weigmann, A., Corbeil, D., Hellwig, A., Huttner, W. B. (1997). 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: 12425-12430 [Abstract] [Full Text]
Salas, P. J.I., Rodriguez, M. L., Viciana, A. L., Vega-Salas, D. E., Hauri, H.-P. (1997). The Apical Submembrane Cytoskeleton Participates in the Organization of the Apical Pole in Epithelial Cells. JCB 137: 359-375 [Abstract] [Full Text]
Lo, S. H., Yu, Q.-C., Degenstein, L., Chen, L. B., Fuchs, E. (1997). Progressive Kidney Degeneration in Mice Lacking Tensin. JCB 136: 1349-1361 [Abstract] [Full Text]
Ojakian, G., Nelson, W., Beck, K. (1997). Mechanisms for de novo biogenesis of an apical membrane compartment in groups of simple epithelial cells surrounded by extracellular matrix. J. Cell Sci. 110: 2781-2794 [Abstract]
Zuk, A, Matlin, K. (1996). Apical beta 1 integrin in polarized MDCK cells mediates tubulocyst formation in response to type I collagen overlay. J. Cell Sci. 109: 1875-1889 [Abstract]
Schwimmer, R, Ojakian, G. (1995). The alpha 2 beta 1 integrin regulates collagen-mediated MDCK epithelial membrane remodeling and tubule formation. J. Cell Sci. 108: 2487-2498 [Abstract]
Brignoni, M, Pignataro, O., Rodriguez, M., Alvarez, A, Vega-Salas, D., Rodriguez-Boulan, E, Salas, P. (1995). Cyclic AMP modulates the rate of 'constitutive' exocytosis of apical membrane proteins in Madin-Darby canine kidney cells. J. Cell Sci. 108: 1931-1943 [Abstract]
Rodriguez, M., Brignoni, M, Salas, P. (1994). A specifically apical sub-membrane intermediate filament cytoskeleton in non-brush-border epithelial cells. J. Cell Sci. 107: 3145-3151 [Abstract]
Ojakian, G., Schwimmer, R (1994). Regulation of epithelial cell surface polarity reversal by beta 1 integrins. J. Cell Sci. 107: 561-576 [Abstract]
Schoenenberger, C., Zuk, A, Zinkl, G., Kendall, D, Matlin, K. (1994). Integrin expression and localization in normal MDCK cells and transformed MDCK cells lacking apical polarity. J. Cell Sci. 107: 527-541 [Abstract]
Baumann, O, Takeyasu, K (1993). Polarized distribution of Na,K-ATPase in honeybee photoreceptors is maintained by interaction with glial cells. J. Cell Sci. 105: 287-301 [Abstract]
Nelson, W. (1992). Regulation of cell surface polarity from bacteria to mammals. Science 258: 948-955 [Abstract]
Ojakian, G. K., Schwimmer, R. (1992). Antimicrotubule drugs inhibit the polarized insertion of an intracellular glycoprotein pool into the apical membrane of Madin-Darby canine kidney (MDCK) cells. J. Cell Sci. 103: 677-687 [Abstract]
Rodriguez-Boulan, E, Nelson, W. (1989). Morphogenesis of the polarized epithelial cell phenotype. Science 245: 718-725 [Abstract]
Jetten, A., Yankaskas, JR, Stutts, M., Willumsen, N., Boucher, R. (1989). Persistence of abnormal chloride conductance regulation in transformed cystic fibrosis epithelia. Science 244: 1472-1475 [Abstract]