Role of membrane traffic in the generation of epithelial cell asymmetry (original) (raw)

• Mellman, I. & Nelson, W. J. Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833–845 (2008).
  CAS PubMed PubMed Central Google Scholar
• Cao, X., Surma, M. A. & Simons, K. Polarized sorting and trafficking in epithelial cells. Cell Res. 22, 793–805 (2012).
  CAS PubMed PubMed Central Google Scholar
• Martin-Belmonte, F. et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383–397 (2007).
  CAS PubMed PubMed Central Google Scholar
• Gassama-Diagne, A. et al. Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat. Cell Biol. 8, 963–970 (2006).
  CAS PubMed Google Scholar
• Jacob, R. & Naim, H. Y. Apical membrane proteins are transported in distinct vesicular carriers. Curr. Biol. 11, 1444–1450 (2001).
  CAS PubMed Google Scholar
• Kreitzer, G. et al. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells. Nat. Cell Biol. 5, 126–136 (2003).
  CAS PubMed Google Scholar
• Farr, G. A., Hull, M., Mellman, I. & Caplan, M. J. Membrane proteins follow multiple pathways to the basolateral cell surface in polarized epithelial cells. J. Cell Biol. 186, 269–282 (2009).
  CAS PubMed PubMed Central Google Scholar
• Fukuda, M. Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci. 65, 2801–2813 (2008).
  CAS PubMed Google Scholar
• Tveit, H., Akslen, L. K., Fagereng, G. L., Tranulis, M. A. & Prydz, K. A secretory Golgi bypass route to the apical surface domain of epithelial MDCK cells. Traffic 10, 1685–1695 (2009).
  CAS PubMed Google Scholar
• Ang, A. L. et al. Recycling endosomes can serve as intermediates during transport from the Golgi to the plasma membrane of MDCK cells. J. Cell Bio. 167, 531–543 (2004).
  CAS Google Scholar
• Cresawn, K. O. et al. Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J. 26, 3737–3748 (2007).
  CAS PubMed PubMed Central Google Scholar
• Cramm-Behrens, C. I., Dienst, M. & Jacob, R. Apical cargo traverses endosomal compartments on the passage to the cell surface. Traffic 9, 2206–2220 (2008).
  CAS PubMed Google Scholar
• Gravotta, D. et al. AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells. Proc. Natl Acad. Sci. USA 104, 1564–1569 (2007).
  CAS PubMed PubMed Central Google Scholar
• Traub, L. M. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583–596 (2009).
  CAS PubMed Google Scholar
• Khandelwal, P., Ruiz, W. G. & Apodaca, G. Compensatory endocytosis in bladder umbrella cells occurs through an integrin-regulated and RhoA- and dynamin-dependent pathway. EMBO J. 29, 1961–1975 (2010).
  CAS PubMed PubMed Central Google Scholar
• Parton, R. G., Prydz, K., Bomsel, M., Simons, K. & Griffiths, G. Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes. J. Cell Biol. 109, 3259–3272 (1989).
  CAS PubMed Google Scholar
• Bucci, C. et al. Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells. Proc. Natl Acad. Sci. USA 91, 5061–5065 (1994).
  CAS PubMed PubMed Central Google Scholar
• Zeigerer, A. et al. Rab5 is necessary for the biogenesis of the endolysosomal system in vivo . Nature 485, 465–470 (2012).
  CAS PubMed Google Scholar
• Sheff, D. R., Daro, E. A., Hull, M. & Mellman, I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145, 123–139 (1999).
  CAS PubMed PubMed Central Google Scholar
• Wang, E. et al. Apical and basolateral pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1, 480–493 (2000).
  CAS PubMed Google Scholar
• Babbey, C. M. et al. Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 17, 3156–3175 (2006).
  CAS PubMed PubMed Central Google Scholar
• Henry, L. & Sheff, D. R. Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol. Biol. Cell 19, 2059–2068 (2008).
  CAS PubMed PubMed Central Google Scholar
• Leung, S.-M., Ruiz, W. G. & Apodaca, G. Sorting of membrane and fluid at the apical pole of polarized MDCK cells. Mol. Biol. Cell 11, 2131–2150 (2000).
  CAS PubMed PubMed Central Google Scholar
• Tzaban, S. et al. The recycling and transcytotic pathways for IgG transport by FcRn are distinct and display an inherent polarity. J. Cell Biol. 185, 673–684 (2009).
  CAS PubMed PubMed Central Google Scholar
• Thompson, A. et al. Recycling endosomes of polarized epithelial cells actively sort apical and basolateral cargos into separate subdomains. Mol. Biol. Cell 18, 2687–2697 (2007).
  CAS PubMed PubMed Central Google Scholar
• Jerdeva, G. V. et al. Comparison of FcRn- and pIgR-mediated transport in MDCK cells by fluorescence confocal microscopy. Traffic 11, 1205–1220 (2010).
  CAS PubMed PubMed Central Google Scholar
• Ait Slimane, T. & Hoekstra, D. Sphingolipid trafficking and protein sorting in epithelial cells. FEBS Lett. 529, 54–59 (2002).
  CAS PubMed Google Scholar
• Gonzalez, A. & Rodriguez-Boulan, E. Clathrin and AP1B: key roles in basolateral trafficking through trans-endosomal routes. FEBS Lett. 583, 3784–3795 (2009).
  CAS PubMed PubMed Central Google Scholar
• Deborde, S. et al. Clathrin is a key regulator of basolateral polarity. Nature 452, 719–723 (2008).
  CAS PubMed PubMed Central Google Scholar
• Fölsch, H., Ohno, H., Bonifacino, J. S. & Mellman, I. A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99, 189–198 (1999).
  PubMed Google Scholar
• Simmen, T., Höning, S., Icking, A., Tikkanen, R. & Hunziker, W. AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nature Cell Biol. 4, 154–159 (2002).
  CAS PubMed Google Scholar
• Nishimura, N., Plutner, H., Hahn, K. & Balch, W. E. The delta subunit of AP-3 is required for efficient transport of VSV-G from the trans-Golgi network to the cell surface. Proc. Natl Acad. Sci. USA 99, 6755–6760 (2002).
  CAS PubMed PubMed Central Google Scholar
• Ohno, H. et al. μ1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449, 215–220 (1999).
  CAS PubMed Google Scholar
• Gravotta, D. et al. The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell 22, 811–823 (2012).
  CAS PubMed PubMed Central Google Scholar
• Takahashi, D. et al. The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice. Gastroenterology 141, 621–632 (2011).
  CAS PubMed Google Scholar
• Schreiner, R. et al. The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int. 78, 382–388 (2010).
  CAS PubMed PubMed Central Google Scholar
• Fölsch, H., Pypaert, M., Schu, P. & Mellman, I. Distribution and function of AP-1 clathrin adaptor complexes in polarized epithelial cells. J. Cell Biol. 152, 595–606 (2001).
  PubMed PubMed Central Google Scholar
• Sugimoto, H. et al. Differential recognition of tyrosine-based basolateral signals by AP-1B subunit μ1B in polarized epithelial cells. Mol. Biol. Cell 13, 2374–2382 (2002).
  CAS PubMed PubMed Central Google Scholar
• Kelly, B. T. et al. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456, 976–979 (2008).
  CAS PubMed PubMed Central Google Scholar
• Carvajal-Gonzalez, J. M. et al. Basolateral sorting of the coxsackie and adenovirus receptor through interaction of a canonical YXXPhi motif with the clathrin adaptors AP-1A and AP-1B. Proc. Natl Acad. Sci. USA 109, 3820–3825 (2012).
  CAS PubMed PubMed Central Google Scholar
• Xiong, X. et al. An association between type Iγ PI4P 5-kinase and Exo70 directs E-cadherin clustering and epithelial polarization. Mol. Biol. Cell 23, 87–98 (2012).
  CAS PubMed PubMed Central Google Scholar
• Sun, Y., Ling, K., Wagoner, M. P. & Anderson, R. A. Type I gamma phosphatidylinositol phosphate kinase is required for EGF-stimulated directional cell migration. J. Cell Biol. 178, 297–308 (2007).
  CAS PubMed PubMed Central Google Scholar
• Oztan, A. et al. Exocyst requirement for endocytic traffic directed toward the apical and basolateral poles of polarized MDCK cells. Mol. Biol. Cell 18, 3978–3992 (2007).
  CAS PubMed PubMed Central Google Scholar
• Grindstaff, K. K. et al. Sec6/8 complex is recruited to cell–cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 93, 731–740 (1998).
  CAS PubMed Google Scholar
• Folsch, H., Pypaert, M., Maday, S., Pelletier, L. & Mellman, I. The AP-1A and AP-1B clathrin adaptor complexes define biochemically and functionally distinct membrane domains. J. Cell Biol. 163, 351–362 (2003).
  PubMed PubMed Central Google Scholar
• Miranda, K. C. et al. A dileucine motif targets E-cadherin to the basolateral cell surface in Madin-Darby canine kidney and LLC-PK1 epithelial cells. J. Biol. Chem. 276, 22565–22572 (2001).
  CAS PubMed Google Scholar
• Kang, R. S. & Folsch, H. ARH cooperates with AP-1B in the exocytosis of LDLR in polarized epithelial cells. J. Cell Biol. 193, 51–60 (2011).
  CAS PubMed PubMed Central Google Scholar
• Mishra, S. K., Watkins, S. C. & Traub, L. M. The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc. Natl Acad. Sci. USA 99, 16099–16104 (2002).
  CAS PubMed PubMed Central Google Scholar
• Ang, A. L., Folsch, H., Koivisto, U. M., Pypaert, M. & Mellman, I. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J. Cell Biol. 163, 339–350 (2003).
  CAS PubMed PubMed Central Google Scholar
• Fields, I. C., King, S. M., Shteyn, E., Kang, R. S. & Folsch, H. Phosphatidylinositol 3,4,5-trisphosphate localization in recycling endosomes is necessary for AP-1B-dependent sorting in polarized epithelial cells. Mol. Biol. Cell 21, 95–105 (2010).
  CAS PubMed PubMed Central Google Scholar
• Shteyn, E., Pigati, L. & Folsch, H. Arf6 regulates AP-1B-dependent sorting in polarized epithelial cells. J. Cell Biol. 194, 873–887 (2011).
  CAS PubMed PubMed Central Google Scholar
• Ang, A. L., Folsch, H., Koivisto, U. M., Pypaert, M. & Mellman, I. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J. Cell Biol. 163, 339–350 (2003).
  CAS PubMed PubMed Central Google Scholar
• Au, J. S., Puri, C., Ihrke, G., Kendrick-Jones, J. & Buss, F. Myosin VI is required for sorting of AP-1B-dependent cargo to the basolateral domain in polarized MDCK cells. J. Cell Biol. 177, 103–114 (2007).
  CAS PubMed PubMed Central Google Scholar
• Fields, I. C. et al. v-SNARE cellubrevin is required for basolateral sorting of AP-1B-dependent cargo in polarized epithelial cells. J. Cell Biol. 177, 477–488 (2007).
  CAS PubMed PubMed Central Google Scholar
• Sato, T. et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448, 366–369 (2007).
  CAS PubMed Google Scholar
• Bryant, D. M. et al. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035–1045 (2010).
  CAS PubMed PubMed Central Google Scholar
• Feng, S. et al. A Rab8 guanine nucleotide exchange factor-effector interaction network regulates primary ciliogenesis. J. Biol. Chem. 287, 15602–15609 (2012).
  CAS PubMed PubMed Central Google Scholar
• Kim, J., Krishnaswami, S. R. & Gleeson, J. G. CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet. 17, 3796–3805 (2008).
  CAS PubMed PubMed Central Google Scholar
• Knodler, A. et al. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl Acad. Sci. USA 107, 6346–6351 (2010).
  CAS PubMed PubMed Central Google Scholar
• Omori, Y. et al. Elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat. Cell Biol. 10, 437–444 (2008).
  CAS PubMed Google Scholar
• Deora, A. A. et al. The basolateral targeting signal of CD147 (EMMPRIN) consists of a single leucine and is not recognized by retinal pigment epithelium. Mol. Biol. Cell 15, 4148–4165 (2004).
  CAS PubMed PubMed Central Google Scholar
• Li, C. et al. Naked2 acts as a cargo recognition and targeting protein to ensure proper delivery and fusion of TGF-α containing exocytic vesicles at the lower lateral membrane of polarized MDCK cells. Mol. Biol. Cell 18, 3081–3093 (2007).
  PubMed PubMed Central Google Scholar
• Kizhatil, K. et al. Ankyrin-G is a molecular partner of E-cadherin in epithelial cells and early embryos. J. Biol. Chem. 282, 26552–26561 (2007).
  CAS PubMed Google Scholar
• Sorrosal, G., Perez, L., Herranz, H. & Milan, M. Scarface, a secreted serine protease-like protein, regulates polarized localization of laminin A at the basement membrane of the Drosophila embryo. EMBO Rep. 11, 373–379 (2010).
  CAS PubMed PubMed Central Google Scholar
• Denef, N., Chen, Y., Weeks, S. D., Barcelo, G. & Schupbach, T. Crag regulates epithelial architecture and polarized deposition of basement membrane proteins in Drosophila . Dev. Cell 14, 354–364 (2008).
  CAS PubMed PubMed Central Google Scholar
• Weisz, O. A. & Rodriguez-Boulan, E. Apical trafficking in epithelial cells: signals, clusters and motors. J. Cell Sci. 122, 4253–4266 (2009).
  CAS PubMed PubMed Central Google Scholar
• Scheiffele, P., Roth, M. G. & Simons, K. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16, 5501–5508 (1997).
  CAS PubMed PubMed Central Google Scholar
• Rodriguez-Boulan, E. & Gonzalez, A. Glycans in post-Golgi apical targeting: sorting signals or structural props? Trends Cell Biol. 9, 291–294 (1999).
  CAS PubMed Google Scholar
• Boscher, C., Dennis, J. W. & Nabi, I. R. Glycosylation, galectins and cellular signaling. Curr. Opin. Cell Biol. 23, 383–392 (2011).
  CAS PubMed Google Scholar
• Delacour, D. et al. Requirement for galectin-3 in apical protein sorting. Curr. Biol. 16, 408–414 (2006).
  CAS PubMed Google Scholar
• Delacour, D. et al. Loss of galectin-3 impairs membrane polarisation of mouse enterocytes in vivo . J. Cell Sci. 121, 458–465 (2008).
  CAS PubMed Google Scholar
• Mattila, P. E. et al. Multiple biosynthetic trafficking routes for apically secreted proteins in MDCK cells. Traffic 13, 433–442 (2012).
  CAS PubMed Google Scholar
• Delacour, D. et al. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J. Cell Biol. 169, 491–501 (2005).
  CAS PubMed PubMed Central Google Scholar
• Stechly, L. et al. Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10, 438–450 (2009).
  CAS PubMed Google Scholar
• Mishra, R., Grzybek, M., Niki, T., Hirashima, M. & Simons, K. Galectin-9 trafficking regulates apical-basal polarity in Madin–Darby canine kidney epithelial cells. Proc. Natl Acad. Sci. USA 107, 17633–17638 (2010).
  CAS PubMed PubMed Central Google Scholar
• Delacour, D. et al. Apical sorting by galectin-3-dependent glycoprotein clustering. Traffic 8, 379–388 (2007).
  CAS PubMed Google Scholar
• Astanina, K., Delebinski, C. I., Delacour, D. & Jacob, R. Annexin XIIIb guides raft-dependent and -independent apical traffic in MDCK cells. Eur. J. Cell Biol. 89, 799–806 (2010).
  CAS PubMed Google Scholar
• Jacob, R. et al. Annexin II is required for apical transport in polarized epithelial cells. J. Biol. Chem. 279, 3680–3684 (2004).
  CAS PubMed Google Scholar
• Magal, L. G. et al. Clustering and lateral concentration of raft lipids by the MAL protein. Mol. Biol. Cell 20, 3751–3762 (2009).
  CAS PubMed PubMed Central Google Scholar
• Zhou, G. et al. MAL facilitates the incorporation of exocytic uroplakin-delivering vesicles into the apical membrane of urothelial umbrella cells. Mol. Biol. Cell 23, 1354–1366 (2012).
  CAS PubMed PubMed Central Google Scholar
• de Marco, M. C. et al. MAL2, a novel raft protein of the MAL family, is an essential component of the machinery for transcytosis in hepatoma HepG2 cells. J. Cell Biol. 159, 37–44 (2002).
  CAS PubMed PubMed Central Google Scholar
• Simons, K. & Gerl, M. J. Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11, 688–699 (2010).
  CAS PubMed Google Scholar
• Klemm, R. W. et al. Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J. Cell Biol. 185, 601–612 (2009).
  CAS PubMed PubMed Central Google Scholar
• Zhang, H. et al. Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat. Cell Biol. 13, 1189–1201 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hutagalung, A. H. & Novick, P. J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119–149 (2011).
  CAS PubMed Google Scholar
• Nokes, R. L., Fields, I. C., Collins, R. N. & Folsch, H. Rab13 regulates membrane trafficking between TGN and recycling endosomes in polarized epithelial cells. J. Cell Biol. 182, 845–853 (2008).
  CAS PubMed PubMed Central Google Scholar
• Galvez-Santisteban, M. et al. Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells. Nat. Cell Biol. 14, 838–849 (2012).
  CAS PubMed PubMed Central Google Scholar
• Hunziker, W. & Peters, P. J. Rab17 localizes to recycling endosomes and regulates receptor-mediated transcytosis in epithelial cells. J. Biol. Chem. 273, 15734–15741 (1998).
  CAS PubMed Google Scholar
• Jaulin, F. & Kreitzer, G. KIF17 stabilizes microtubules and contributes to epithelial morphogenesis by acting at MT plus ends with EB1 and APC. J. Cell Biol. 190, 443–460 (2010).
  CAS PubMed PubMed Central Google Scholar
• Jaulin, F., Xue, X., Rodriguez-Boulan, E. & Kreitzer, G. Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev. Cell 13, 511–522 (2007).
  CAS PubMed PubMed Central Google Scholar
• Noda, Y. et al. KIFC3, a microtubule minus end-directed motor for the apical transport of annexin XIIIb-associated Triton-insoluble membranes. J. Cell Biol. 155, 77–88 (2001).
  CAS PubMed PubMed Central Google Scholar
• Yeh, T. Y., Peretti, D., Chuang, J. Z., Rodriguez-Boulan, E. & Sung, C. H. Regulatory dissociation of Tctex-1 light chain from dynein complex is essential for the apical delivery of rhodopsin. Traffic 7, 1495–1502 (2006).
  CAS PubMed Google Scholar
• Ameen, N. & Apodaca, G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8, 998–1006 (2007).
  CAS PubMed Google Scholar
• Eichler, T. W., Kogel, T., Bukoreshtliev, N. V. & Gerdes, H. H. The role of myosin Va in secretory granule trafficking and exocytosis. Biochem. Soc. Trans. 34, 671–674 (2006).
  CAS PubMed Google Scholar
• Roland, J. T. et al. Rab GTPase–Myo5B complexes control membrane recycling and epithelial polarization. Proc. Natl Acad. Sci. USA 108, 2789–2794 (2011).
  CAS PubMed PubMed Central Google Scholar
• Bond, L. M., Brandstaetter, H., Sellers, J. R., Kendrick-Jones, J. & Buss, F. Myosin motor proteins are involved in the final stages of the secretory pathways. Biochem. Soc. Trans. 39, 1115–1119 (2011).
  CAS PubMed PubMed Central Google Scholar
• Born, M., Pahner, I., Ahnert-Hilger, G. & Jons, T. 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 (2003).
  CAS PubMed Google Scholar
• Nielsen, S. et al. Expression of VAMP-2-like protein in kidney collecting duct intracellular vesicles. Colocalization with Aquaporin-2 water channels. J. Clin. Invest. 96, 1834–1844 (1995).
  CAS PubMed PubMed Central Google Scholar
• Procino, G. et al. AQP2 exocytosis in the renal collecting duct — involvement of SNARE isoforms and the regulatory role of Munc18b. J. Cell Sci. 121, 2097–2106 (2008).
  CAS PubMed Google Scholar
• Karvar, S., Yao, X., Crothers, J. M. Jr, Liu, Y. & Forte, J. G. Localization and function of soluble _N_-ethylmaleimide-sensitive factor attachment protein-25 and vesicle-associated membrane protein-2 in functioning gastric parietal cells. J. Biol. Chem. 277, 50030–50035 (2002).
  CAS PubMed Google Scholar
• Low, S. H. et al. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 7, 2007–2018 (1996).
  CAS PubMed PubMed Central Google Scholar
• Reales, E., Sharma, N., Low, S. H., Folsch, H. & Weimbs, T. Basolateral sorting of syntaxin 4 is dependent on its N-terminal domain and the AP1B clathrin adaptor, and required for the epithelial cell polarity. PLoS ONE 6, e21181 (2011).
  CAS PubMed PubMed Central Google Scholar
• Sharma, N., Low, S. H., Misra, S., Pallavi, B. & Weimbs, T. Apical targeting of syntaxin 3 is essential for epithelial cell polarity. J. Cell Biol. 173, 937–948 (2006).
  CAS PubMed PubMed Central Google Scholar
• Bryant, D. M. & Mostov, K. E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9, 887–901 (2008).
  CAS PubMed PubMed Central Google Scholar
• Schluter, M. A. & Margolis, B. Apicobasal polarity in the kidney. Exp. Cell Res. 318, 1033–1039 (2012).
  PubMed PubMed Central Google Scholar
• Tepass, U. The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu. Rev. Cell Dev. Biol. 28, 655–685 (2012).
  CAS PubMed Google Scholar
• Cohen, D., Rodriguez-Boulan, E. & Musch, A. Par-1 promotes a hepatic mode of apical protein trafficking in MDCK cells. Proc. Natl Acad. Sci. USA 101, 13792–13797 (2004).
  CAS PubMed PubMed Central Google Scholar
• Nechiporuk, T., Fernandez, T. E. & Vasioukhin, V. Failure of epithelial tube maintenance causes hydrocephalus and renal cysts in Dlg5 −/− mice. Dev. Cell 13, 338–350 (2007).
  CAS PubMed PubMed Central Google Scholar
• Laprise, P. et al. Yurt, Coracle, Neurexin IV and the Na+,K+-ATPase form a novel group of epithelial polarity proteins. Nature 459, 1141–1145 (2009).
  CAS PubMed Google Scholar
• Plant, P. J. et al. A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5, 301–308 (2003).
  CAS PubMed Google Scholar
• Laprise, P. & Tepass, U. Novel insights into epithelial polarity proteins in Drosophila . Trends Cell Biol. 21, 401–408 (2011).
  CAS PubMed Google Scholar
• Shivas, J. M., Morrison, H. A., Bilder, D. & Skop, A. R. Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 20, 445–452 (2010).
  CAS PubMed PubMed Central Google Scholar
• Winter, J. F. et al. Caenorhabditis elegans screen reveals role of PAR-5 in RAB-11-recycling endosome positioning and apicobasal cell polarity. Nat. Cell Biol. 14, 666–676 (2012).
  CAS PubMed Google Scholar
• Schluter, M. A. et al. Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol. Biol. Cell 20, 4652–4663 (2009).
  CAS PubMed PubMed Central Google Scholar
• Bryant, D. M. et al. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035–1045 (2010).
  CAS PubMed PubMed Central Google Scholar
• Ferrari, A., Veligodskiy, A., Berge, U., Lucas, M. S. & Kroschewski, R. ROCK-mediated contractility, tight junctions and channels contribute to the conversion of a preapical patch into apical surface during isochoric lumen initiation. J. Cell Sci. 121, 3649–3663 (2008).
  CAS PubMed Google Scholar
• Xu, K. et al. Blood vessel tubulogenesis requires Rasip1 regulation of GTPase signaling. Dev. Cell 20, 526–539 (2011).
  CAS PubMed PubMed Central Google Scholar
• Herwig, L. et al. Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21, 1942–1948 (2011).
  CAS PubMed Google Scholar
• Schluter, M. A. & Margolis, B. Apical lumen formation in renal epithelia. J. Am. Soc. Nephrol. 20, 1444–1452 (2009).
  PubMed Google Scholar
• Willenborg, C. et al. Interaction between FIP5 and SNX18 regulates epithelial lumen formation. J. Cell Biol. 195, 71–86 (2011).
  CAS PubMed PubMed Central Google Scholar
• Jin, Y. et al. Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev. Cell 21, 1156–1170 (2011).
  CAS PubMed PubMed Central Google Scholar
• Horikoshi, Y. et al. Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J. Cell Sci. 122, 1595–1606 (2009).
  CAS PubMed Google Scholar
• Zhang, H. et al. Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development 139, 2071–2083 (2012).
  PubMed PubMed Central Google Scholar
• Shafaq-Zadah, M., Brocard, L., Solari, F. & Michaux, G. AP-1 is required for the maintenance of apico-basal polarity in the C. elegans intestine. Development 139, 2061–2070 (2012).
  CAS PubMed Google Scholar
• Nelson, W. J. Remodeling epithelial cell organization: transitions between front–rear and apical–basal polarity. Cold Spring Harb. Perspect. Biol. 1, a000513 (2009).
  PubMed PubMed Central Google Scholar
• Wang, Q., Chen, X. W. & Margolis, B. PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol. Biol. Cell 18, 874–885 (2007).
  PubMed PubMed Central Google Scholar
• Nejsum, L. N. & Nelson, W. J. A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. J. Cell Biol. 178, 323–335 (2007).
  CAS PubMed PubMed Central Google Scholar
• Shaw, R. M. et al. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 128, 547–560 (2007).
  CAS PubMed PubMed Central Google Scholar
• Lock, J. G. & Stow, J. L. Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin. Mol. Biol. Cell 16, 1744–1755 (2005).
  CAS PubMed PubMed Central Google Scholar
• Yeaman, C., Grindstaff, K. K. & Nelson, W. J. Mechanism of recruiting Sec6/8 (exocyst) complex to the apical junctional complex during polarization of epithelial cells. J. Cell Sci. 117, 559–570 (2004).
  CAS PubMed Google Scholar
• Garcia-Gonzalo, F. R. & Reiter, J. F. Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J. Cell Biol. 197, 697–709 (2012).
  CAS PubMed PubMed Central Google Scholar
• ten Klooster, J. P. et al. Mst4 and Ezrin induce brush borders downstream of the Lkb1/Strad/Mo25 polarization complex. Dev. Cell 16, 551–562 (2009).
  CAS PubMed Google Scholar
• Sato, T. et al. Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature 459, 262–265 (2009).
  CAS PubMed Google Scholar
• O'Brien, L. E. et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831–838 (2001).
  CAS PubMed Google Scholar
• O'Brien, L. E. et al. Morphological and biochemical analysis of Rac1 in three-dimensional epithelial cell cultures. Methods Enzymol. 406, 676–691 (2006).
  CAS PubMed Google Scholar
• Debnath, J., Muthuswamy, S. K. & Brugge, J. S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256–268 (2003).
  CAS PubMed Google Scholar
• Zegers, M. M., O'Brien, L. E., Yu, W., Datta, A. & Mostov, K. E. Epithelial polarity and tubulogenesis in vitro . Trends Cell Biol. 13, 169–176 (2003).
  CAS PubMed Google Scholar
• Yu, W. et al. Hepatocyte growth factor switches orientation of polarity and mode of movement during morphogenesis of multicellular epithelial structures. Mol. Biol. Cell 14, 748–763 (2003).
  CAS PubMed PubMed Central Google Scholar
• Apodaca, G. Opening ahead: early steps in lumen formation revealed. Nat. Cell Biol. 12, 1026–1028 (2010).
  CAS PubMed Google Scholar