Trafficking of Crumbs3 during cytokinesis is crucial for lumen formation

Molecular Biology of the Cell

Volumn 20, Issue 22, 2009, Pages 4652-4663

  Schlüter, Marc A ^a,b   Pfarr, Catherine S ^a,b   Pieczynski, Jay ^a   Whiteman, Eileen L ^a   Hurd, Toby W ^a   Fan, Shuling ^a   Liu, Chia Jen ^a   Margolis, Ben ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL DIVISION; CELL STRAIN; CYTOKINESIS; DAUGHTER CELL; ENDOSOME; MICROTUBULE; MITOSIS; MITOSIS SPINDLE; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; CELL CYCLE PROTEINS; CELL LINE; CELL POLARITY; CYTOKINESIS; CYTOSKELETON; DOGS; ENDOCYTOSIS; ENDOSOMES; MEMBRANE PROTEINS; MICROTUBULES; MORPHOGENESIS; MULTIPROTEIN COMPLEXES; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS;

EID: 73949111285     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-02-0137     Document Type: Article

References (46)

1. Benton, R., and St. Johnston, D. (2003). Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115, 691-704.
2. Bhartur, S. G., Calhoun, B. C., Woodrum, J., Kurkjian, J., Iyer, S., Lai, F., and Goldenring, J. R. (2000). Genomic structure of murine Rab11 family members. Biochem. Biophys. Res. Commun. 269, 611-617.
3. Boutet, A., De Frutos, C. A., Maxwell, P. H., Mayol, M. J., Romero, J., and Nieto, M. A. (2006). Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J. 25, 5603-5613.
4. Cheng, H. Y., et al. (2005). Molecular identification of canine podocalyxin-like protein 1 as a renal tubulogenic regulator. J. Am. Soc. Nephrol. 16, 1612-1622.
5. Cresawn, K. O., Potter, B. A., Oztan, A., Guerriero, C. J., Ihrke, G., Goldenring, J. R., Apodaca, G., and Weisz, O. A. (2007). Differential involvement of endocytic compartments in the biosynthetic traffic of apical proteins. EMBO J. 26, 3737-3748.
6. Fan, S., Fogg, V., Wang, Q., Chen, X. W., Liu, C. J., and Margolis, B. (2007). A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J. Cell Biol. 178, 387-398.
7. Ferrari, A., Veligodskiy, A., Berge, U., Lucas, M. S., and Kroschewski, R. (2008). 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.
8. Fogg, V. C., Liu, C. J., and Margolis, B. (2005). Multiple regions of Crumbs3 are required for tight junction formation in MCF10A cells. J. Cell Sci. 118, 2859-2869.
9. Hobdy-Henderson, K. C., Hales, C. M., Lapierre, L. A., Cheney, R. E., and Goldenring, J. R. (2003). Dynamics of the apical plasma membrane recycling system during cell division. Traffic 4, 681-693.
10. Horgan, C. P., Walsh, M., Zurawski, T. H., and McCaffrey, M. W. (2004). Rab11-FIP3 localises to a Rab11-positive pericentrosomal compartment during interphase and to the cleavage furrow during cytokinesis. Biochem. Biophys. Res. Commun. 319, 83-94.
11. Horikoshi, Y., Suzuki, A., Yamanaka, T., Sasaki, K., Mizuno, K., Sawada, H., Yonemura, S., and Ohno, S. (2009). 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.
12. Hurd, T. W., Fan, S., Liu, C. J., Kweon, H. K., Hakansson, K., and Margolis, B. (2003a). Phosphorylation-dependent binding of 14-3-3 to the polarity protein Par3 regulates cell polarity in mammalian epithelia. Curr. Biol. 13, 2082-2090.
13. Hurd, T. W., Gao, L., Roh, M. H., Macara, I. G., and Margolis, B. (2003b). Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat. Cell Biol 5, 137-142.
14. Hurov, J. B., Watkins, J. L., and Piwnica-Worms, H. (2004). Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Curr. Biol. 14, 736-741.
15. Ikenouchi, J., Matsuda, M., Furuse, M., and Tsukita, S. (2003). Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J. Cell Sci. 116, 1959-1967.
16. Jaffe, A. B., Kaji, N., Durgan, J., and Hall, A. (2008). Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183, 625-633.
17. Lemmers, C., Medina, E., Lane-Guermonprez, L., Arsanto, J. P., and Le Bivic, A. (2004a). [Role of Crumbs proteins in the control of epithelial cell and photoreceptor morphogenesis]. Med. Sci. (Paris) 20, 663-667.
18. Lemmers, C., Michel, D., Lane-Guermonprez, L., Delgrossi, M. H., Medina, E., Arsanto, J. P., and Le Bivic, A. (2004b). CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol. Biol. Cell 15, 1324-1333.
19. Lubarsky, B., and Krasnow, M. A. (2003). Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28.
20. Makarova, O., Roh, M. H., Liu, C. J., Laurinec, S., and Margolis, B. (2003). Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene 302, 21-29.
21. Martin-Belmonte, F., Gassama, A., Datta, A., Yu, W., Rescher, U., Gerke, V., and Mostov, K. (2007). PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383-397.
22. Martin-Belmonte, F., and Mostov, K. (2008). Regulation of cell polarity during epithelial morphogenesis. Curr. Opin. Cell Biol. 20, 227-234.
23. Martin-Belmonte, F., Yu, W., Rodriguez-Fraticelli, A. E., Ewald, A., Werb, Z., Alonso, M. A., and Mostov, K. (2008). Cell-polarity dynamics controls the mechanism of lumen formation in epithelial morphogenesis. Curr. Biol. 18, 507-513.
24. Martinez-Estrada, O. M., Culleres, A., Soriano, F. X., Peinado, H., Bolos, V., Martinez, F. O., Reina, M., Cano, A., Fabre, M., and Vilaro, S. (2006). The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 394, 449-457.
25. Meder, D., Shevchenko, A., Simons, K., and Fullekrug, J. (2005). Gp135/ podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. J. Cell Biol. 168, 303-313.
26. Nokes, R. L., Fields, I. C., Collins, R. N., and Folsch, H. (2008). Rab13 regulates membrane trafficking between TGN and recycling endosomes in polarized epithelial cells. J. Cell Biol. 182, 845-853.
27. O'Brien, L. E., Zegers, M. M., and Mostov, K. E. (2002). Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 3, 531-537.
28. Omori, Y., and Malicki, J. (2006). oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr. Biol. 16, 945-957.
29. Plant, P. J., Fawcett, J. P., Lin, D. C., Holdorf, A. D., Binns, K., Kulkarni, S., and Pawson, T. (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5, 301-308.
30. Roh, M. H., Fan, S., Liu, C. J., and Margolis, B. (2003). The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J. Cell Sci. 116, 2895-2906.
31. Roh, M. H., Makarova, O., Liu, C. J., Shin, K., Lee, S., Laurinec, S., Goyal, M., Wiggins, R., and Margolis, B. (2002). The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J. Cell Biol. 157, 161-172.
32. Sato, T., et al. (2007). The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448, 366-369. Saxen, L. (1987). Organogenesis of The Kidney, Cambridge: Cambridge University Press.
33. Schlüter, M. A., and Margolis, B. (2009). Apical lumen formation in renal epithelia. J. Am. Soc. Nephrol. 20, 1444-1452.
34. Shin, K., Fogg, V. C., and Margolis, B. (2006). Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22, 207-235.
35. Shin, K., Straight, S., and Margolis, B. (2005). PATJ regulates tight junction formation and polarity in mammalian epithelial cells. J. Cell Biol. 168, 705-711.
36. Straight, S. W., Shin, K., Fogg, V. C., Fan, S., Liu, C. J., Roh, M., and Margolis, B. (2004). Loss of PALS1 expression leads to tight junction and polarity defects. Mol. Biol. Cell 15, 1981-1990.
37. Suzuki, A., et al. (2004). aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr. Biol. 14, 1425-1435.
38. Tawk, M., Araya, C., Lyons, D. A., Reugels, A. M., Girdler, G. C., Bayley, P. R., Hyde, D. R., Tada, M., and Clarke, J. D. (2007). A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446, 797-800.
39. Thiery, J. P., and Sleeman, J. P. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142.
40. Torkko, J. M., Manninen, A., Schuck, S., and Simons, K. (2008). Depletion of apical transport proteins perturbs epithelial cyst formation and ciliogenesis. J. Cell Sci. 121, 1193-1203.
41. van Ijzendoorn, S. C. (2006). Recycling endosomes. J. Cell Sci. 119, 1679-1681.
42. Vega-Salas, D. E., Salas, P. J., and Rodriguez-Boulan, E. (1987). Modulation of the expression of an apical plasma membrane protein of Madin-Darby canine kidney epithelial cells: cell-cell interactions control the appearance of a novel intracellular storage compartment. J. Cell Biol. 104, 1249-1259.
43. Wang, Q., and Margolis, B. (2007). Apical junctional complexes and cell polarity. Kidney Int. 72, 1448-1458.
44. Wang, X., Kumar, R., Navarre, J., Casanova, J. E., and Goldenring, J. R. (2000). Regulation of vesicle trafficking in madin-darby canine kidney cells by Rab11a and Rab25. J. Biol. Chem. 275, 29138-29146.
45. Whiteman, E. L., Liu, C. J., Fearon, E. R., and Margolis, B. (2008). The transcription factor snail represses Crumbs3 expression and disrupts apicobasal polarity complexes. Oncogene 27, 3875-3879.
46. Wodarz, A., Hinz, U., Engelbert, M., and Knust, E. (1995). Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76.