Role of membrane traffic in the generation of epithelial cell asymmetry

Nature Cell Biology

Volumn 14, Issue 12, 2012, Pages 1235-1243

  Apodaca, Gerard ^a   Gallo, Luciana I ^a   Bryant, David M ^b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

APICAL MEMBRANE; BASOLATERAL MEMBRANE; CELL CONTACT; CELL MATURATION; CELL MEMBRANE TRANSPORT; CELL POLARITY; CELL SELECTION; CELL STRUCTURE; CELL SURFACE; CELLULAR DISTRIBUTION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; EUKARYOTIC FLAGELLUM; GOLGI COMPLEX; INTERNALIZATION; INTRACELLULAR SIGNALING; MEMBRANE STRUCTURE; MICROVILLUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL MEMBRANE; CELL POLARITY; EPITHELIAL CELLS; HUMANS; MICE; MODELS, BIOLOGICAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84870576679     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2635     Document Type: Review

References (139)

1. Mellman, I. & Nelson, W. J. Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845 (2008).
2. Cao, X., Surma, M. A. & Simons, K. Polarized sorting and trafficking in epithelial cells. Cell Res. 22, 793-805 (2012).
3. Martin-Belmonte, F. et al. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383-397 (2007). (Pubitemid 46123512)
4. 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). (Pubitemid 44314727)
5. Jacob, R. & Naim, H. Y. Apical membrane proteins are transported in distinct vesicular carriers. Curr. Biol. 11, 1444-1450 (2001). (Pubitemid 32863195)
6. Kreitzer, G. et al. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells. Nat. Cell Biol. 5, 126-136 (2003). (Pubitemid 36204195)
7. 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).
8. Fukuda, M. Regulation of secretory vesicle traffic by Rab small GTPases. Cell. Mol. Life Sci. 65, 2801-2813 (2008).
9. 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).
10. 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). (Pubitemid 39489060)
11. Cresawn, K. O. et al. Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J. 26, 3737-3748 (2007). (Pubitemid 47295880)
12. 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).
13. 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). (Pubitemid 46214630)
14. Traub, L. M. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596 (2009).
15. 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).
16. 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). (Pubitemid 20017977)
17. 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). (Pubitemid 24177792)
18. Zeigerer, A. et al. Rab5 is necessary for the biogenesis of the endolysosomal system in vivo. Nature 485, 465-470 (2012).
19. 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). (Pubitemid 29177680)
20. 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).
21. 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). (Pubitemid 43993517)
22. Henry, L. & Sheff, D. R. Rab8 regulates basolateral secretory, but not recycling, traffic at the recycling endosome. Mol. Biol. Cell 19, 2059-2068 (2008).
23. 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). (Pubitemid 30408069)
24. 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).
25. 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). (Pubitemid 47025733)
26. Jerdeva, G. V. et al. Comparison of FcRn- and pIgR-mediated transport in MDCK cells by fluorescence confocal microscopy. Traffic 11, 1205-1220 (2010).
27. Ait Slimane, T. & Hoekstra, D. Sphingolipid trafficking and protein sorting in epithelial cells. FEBS Lett. 529, 54-59 (2002). (Pubitemid 35283912)
28. Gonzalez, A. & Rodriguez-Boulan, E. Clathrin and AP1B: key roles in basolateral trafficking through trans-endosomal routes. FEBS Lett. 583, 3784-3795 (2009).
29. Deborde, S. et al. Clathrin is a key regulator of basolateral polarity. Nature 452, 719- 723 (2008). (Pubitemid 351521081)
30. 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). (Pubitemid 29491785)
31. 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). (Pubitemid 34141482)
32. 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). (Pubitemid 34526204)
33. Ohno, H. et al. μ1B, a novel adaptor medium chain expressed in polarized epithelial cells. FEBS Lett. 449, 215-220 (1999). (Pubitemid 29192909)
34. Gravotta, D. et al. The clathrin adaptor AP-1A mediates basolateral polarity. Dev. Cell 22, 811-823 (2012).
35. Takahashi, D. et al. The epithelia-specific membrane trafficking factor AP-1B controls gut immune homeostasis in mice. Gastroenterology 141, 621-632 (2011).
36. Schreiner, R. et al. The absence of a clathrin adapter confers unique polarity essential to proximal tubule function. Kidney Int. 78, 382-388 (2010).
37. 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). (Pubitemid 34280241)
38. 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). (Pubitemid 34831341)
39. Kelly, B. T. et al. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456, 976-979 (2008).
40. 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).
41. 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).
42. 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). (Pubitemid 47076465)
43. 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). (Pubitemid 47519489)
44. 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). (Pubitemid 28257580)
45. 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). (Pubitemid 37363135)
46. 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).
47. 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).
48. 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). (Pubitemid 35462755)
49. 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). (Pubitemid 37363134)
50. 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).
51. Shteyn, E., Pigati, L. & Folsch, H. Arf6 regulates AP-1B-dependent sorting in polarized epithelial cells. J. Cell Biol. 194, 873-887 (2011).
52. 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). (Pubitemid 37363134)
53. 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). (Pubitemid 46588405)
54. 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). (Pubitemid 46718276)
55. Sato, T. et al. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448, 366-369 (2007). (Pubitemid 47080335)
56. 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).
57. Feng, S. et al. A Rab8 guanine nucleotide exchange factor-effector interaction network regulates primary ciliogenesis. J. Biol. Chem. 287, 15602-15609 (2012).
58. 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).
59. Knodler, A. et al. Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl Acad. Sci. USA 107, 6346-6351 (2010).
60. 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).
61. 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). (Pubitemid 39122019)
62. Li, C. et al. Naked2 acts as a cargo recognition and targeting protein to ensure proper delivery and fusion of TGFαα containing exocytic vesicles at the lower lateral membrane of polarized MDCK cells. Mol. Biol. Cell 18, 3081-3093 (2007). (Pubitemid 47235313)
63. 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). (Pubitemid 47443799)
64. 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).
65. 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).
66. Weisz, O. A. & Rodriguez-Boulan, E. Apical trafficking in epithelial cells: signals, clusters and motors. J. Cell Sci. 122, 4253-4266 (2009).
67. 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). (Pubitemid 27399842)
68. Rodriguez-Boulan, E. & Gonzalez, A. Glycans in post-Golgi apical targeting: sorting signals or structural props? Trends Cell Biol. 9, 291-294 (1999). (Pubitemid 29339143)
69. Boscher, C., Dennis, J. W. & Nabi, I. R. Glycosylation, galectins and cellular signaling. Curr. Opin. Cell Biol. 23, 383-392 (2011).
70. Delacour, D. et al. Requirement for galectin-3 in apical protein sorting. Curr. Biol. 16, 408-414 (2006). (Pubitemid 43259352)
71. Delacour, D. et al. Loss of galectin-3 impairs membrane polarisation of mouse enterocytes in vivo. J. Cell Sci. 121, 458-465 (2008). (Pubitemid 351405054)
72. Mattila, P. E. et al. Multiple biosynthetic trafficking routes for apically secreted proteins in MDCK cells. Traffic 13, 433-442 (2012).
73. Delacour, D. et al. Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J. Cell Biol. 169, 491-501 (2005). (Pubitemid 40686699)
74. Stechly, L. et al. Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10, 438-450 (2009).
75. 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).
76. Delacour, D. et al. Apical sorting by galectin-3-dependent glycoprotein clustering. Traffic 8, 379-388 (2007). (Pubitemid 46421620)
77. 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).
78. Jacob, R. et al. Annexin II is required for apical transport in polarized epithelial cells. J. Biol. Chem. 279, 3680-3684 (2004). (Pubitemid 38140610)
79. Magal, L. G. et al. Clustering and lateral concentration of raft lipids by the MAL protein. Mol. Biol. Cell 20, 3751-3762 (2009).
80. 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).
81. 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). (Pubitemid 35191516)
82. Simons, K. & Gerl, M. J. Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 11, 688-699 (2010).
83. 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).
84. Zhang, H. et al. Apicobasal domain identities of expanding tubular membranes depend on glycosphingolipid biosynthesis. Nat. Cell Biol. 13, 1189-1201 (2011).
85. Hutagalung, A. H. & Novick, P. J. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119-149 (2011).
86. 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).
87. 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).
88. 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). (Pubitemid 28298193)
89. 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).
90. 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). (Pubitemid 47500806)
91. 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). (Pubitemid 34286209)
92. 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). (Pubitemid 44524522)
93. Ameen, N. & Apodaca, G. Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8, 998-1006 (2007). (Pubitemid 47074034)
94. 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). (Pubitemid 44796395)
95. Roland, J. T. et al. Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc. Natl Acad. Sci. USA 108, 2789-2794 (2011).
96. 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).
97. 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). (Pubitemid 36944163)
98. 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).
99. 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). (Pubitemid 352015207)
100. 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). (Pubitemid 36014455)
101. Low, S. H. et al. Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 7, 2007-2018 (1996).
102. 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).
103. 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).
104. Bryant, D. M. & Mostov, K. E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 9, 887-901 (2008).
105. Schluter, M. A. & Margolis, B. Apicobasal polarity in the kidney. Exp. Cell Res. 318, 1033-1039 (2012).
106. 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).
107. 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). (Pubitemid 39298486)
108. -/- mice. Dev. Cell 13, 338-350 (2007). (Pubitemid 47308679)
109. +-ATPase form a novel group of epithelial polarity proteins. Nature 459, 1141-1145 (2009).
110. 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). (Pubitemid 36432294)
111. Laprise, P. & Tepass, U. Novel insights into epithelial polarity proteins in Drosophila. Trends Cell Biol. 21, 401-408 (2011).
112. Shivas, J. M., Morrison, H. A., Bilder, D. & Skop, A. R. Polarity and endocytosis: reciprocal regulation. Trends Cell Biol. 20, 445-452 (2010).
113. 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).
114. Schluter, M. A. et al. Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation. Mol. Biol. Cell 20, 4652-4663 (2009).
115. 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).
116. 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).
117. Xu, K. et al. Blood vessel tubulogenesis requires Rasip1 regulation of GTPase signaling. Dev. Cell 20, 526-539 (2011).
118. Herwig, L. et al. Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21, 1942-1948 (2011).
119. Schluter, M. A. & Margolis, B. Apical lumen formation in renal epithelia. J. Am. Soc. Nephrol. 20, 1444-1452 (2009).
120. Willenborg, C. et al. Interaction between FIP5 and SNX18 regulates epithelial lumen formation. J. Cell Biol. 195, 71-86 (2011).
121. 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).
122. 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).
123. Zhang, H. et al. Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development 139, 2071-2083 (2012).
124. 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).
125. Nelson, W. J. Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. Cold Spring Harb. Perspect. Biol. 1, a000513 (2009).
126. Wang, Q., Chen, X. W. & Margolis, B. PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol. Biol. Cell 18, 874-885 (2007). (Pubitemid 46399493)
127. 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). (Pubitemid 47076467)
128. 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). (Pubitemid 46198893)
129. 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). (Pubitemid 40471945)
130. 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). (Pubitemid 38240197)
131. Garcia-Gonzalo, F. R. & Reiter, J. F. Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J. Cell Biol. 197, 697-709 (2012).
132. 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).
133. Sato, T. et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
134. O'Brien, L. E. et al. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838 (2001). (Pubitemid 32842689)
135. O'Brien, L. E. et al. Morphological and biochemical analysis of Rac1 in three-dimensional epithelial cell cultures. Methods Enzymol. 406, 676-691 (2006). (Pubitemid 43207478)
136. 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). (Pubitemid 36677560)
137. 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). (Pubitemid 36351532)
138. 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). (Pubitemid 36237029)
139. Apodaca, G. Opening ahead: early steps in lumen formation revealed. Nat. Cell Biol. 12, 1026-1028 (2010).