Crumbs proteins in epithelial morphogenesis

Frontiers in Bioscience

Volumn 14, Issue 6, 2009, Pages 2149-2169

  Bazellieres, Elsa ^a   Assemat, Emeline ^a   Arsanto, Jean Pierre ^a   Le Bivic, Andre ^a   Massey Harroche, Dominique ^b  

^a CNRS   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Epithelium; Mupp1; Pals1; Par6; Patj; Polarity; Review; Stardust

Indexed keywords

ANIMALIA; EUKARYOTA; METAZOA;

CRB1 PROTEIN, HUMAN; EYE PROTEIN; MEMBRANE PROTEIN; NERVE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; HUMAN; MOLECULAR GENETICS; MORPHOGENESIS; PHYLOGENY; PHYSIOLOGY; REVIEW; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; EYE PROTEINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; NERVE TISSUE PROTEINS; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 63849245005     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3368     Document Type: Article

References (154)

1. Brennwald, P. & G. Rossi: Spatial regulation of exocytosis and cell polarity: yeast as a model for animal cells. FEBS Lett, 581, 2119-24 (2007). (Pubitemid 46709909)
2. Wang, Q. & B. Margolis: Apical junctional complexes and cell polarity. Kidney Int, 72, 1448-58 (2007). (Pubitemid 350197955)
3. Kemphues, K. J., J. R. Priess, D. G. Morton & N. S. Cheng: Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell, 52, 311-20 (1988).
4. Dow, L. E. & P. O. Humbert: Polarity regulators and the control of epithelial architecture, cell migration, and tumorigenesis. Int Rev Cytol, 262, 253-302 (2007). (Pubitemid 47031311)
5. Muller, H. A. & O. Bossinger: Molecular networks controlling epithelial cell polarity in development. Mech Dev, 120, 1231-56 (2003). (Pubitemid 37421160)
6. Tepass, U. & E. Knust: Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev Biol, 159, 311-26 (1993). (Pubitemid 23287244)
7. Tepass, U., C. Theres & E. Knust: crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell, 61, 787-99 (1990).
8. Jürgens, G., E. Wieschaus, C. Nüsslein-Volhard & H. Kluding: Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Development Genes and Evolution 193, 283-295 (1984).
9. Wodarz, A., F. Grawe & E. Knust: CRUMBS is involved in the control of apical protein targeting during Drosophila epithelial development. Mech Dev, 44, 175-87 (1993). (Pubitemid 24028880)
10. Wodarz, A., U. Hinz, M. Engelbert & E. Knust: Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell, 82, 67-76 (1995).
11. Klebes, A. & E. Knust: A conserved motif in Crumbs is required for E-cadherin localisation and zonula adherens formation in Drosophila. Curr Biol, 10, 76-85 (2000). (Pubitemid 30079192)
12. Sotillos, S., M. T. Diaz-Meco, E. Caminero, J. Moscat & S. Campuzano: DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. J Cell Biol, 166, 549-57 (2004). (Pubitemid 39097174)
13. den Hollander, A. I., J. B. ten Brink, Y. J. de Kok, S. van Soest, L. I. van den Born, M. A. van Driel, D. J. van de Pol, A. M. Kellner, C. B. Hoyng, A. Westerveld, H. G. Brunner, E. M. Bleeker-Wagemakers, A. F. Deutman, J. R. Heckenlively, F. P. Cremers & A. A. Bergen: Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet, 23, 217-21 (1999). Payne, S. S. Bhattacharya, U. (Pubitemid 29455397)
14. Lemmers, C., E. Medina, M. H. Delgrossi, D. Michel, J. P. Arsanto & A. Le Bivic: hINADl/PATJ, a homolog of discs lost, interacts with crumbs and localizes to tight junctions in human epithelial cells. J Biol Chem, 277, 25408-15 (2002). (Pubitemid 34951853)
15. Watanabe, T., S. Miyatani, I. Katoh, S. Kobayashi & Y. Ikawa: Expression of a novel secretory form (Crb1s) of mouse Crumbs homologue Crb1 in skin development. Biochem Biophys Res Commun, 313, 263-70 (2004). (Pubitemid 37543580)
16. Katoh, M. & M. Katoh: Identification and characterization of Crumbs homolog 2 gene at human chromosome 9q33.3. Int J Oncol, 24, 743-9 (2004).
17. van den Hurk, J. A., P. Rashbass, R. Roepman, J. Davis, K. E. Voesenek, M. L. Arends, M. N. Zonneveld, M. H. van Roekel, K. Cameron, K. Rohrschneider, J. R. Heckenlively, R. K. Koenekoop, C. B. Hoyng, F. P. Cremers & A. I. den Hollander: Characterization of the Crumbs homolog 2 (CRB2) gene and analysis of its role in retinitis pigmentosa and Leber congenital amaurosis. Mol Vis, 11, 263-73 (2005). (Pubitemid 41358283)
18. Fan, S., V. Fogg, Q. Wang, X. W. Chen, C. J. Liu & B. Margolis: A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J Cell Biol, 178, 387-98 (2007). (Pubitemid 47196148)
19. Hung, A. Y. & M. Sheng: PDZ domains: structural modules for protein complex assembly. J Biol Chem, 277, 5699-702 (2002). (Pubitemid 34968344)
20. den Hollander, A. I., M. Ghiani, Y. J. de Kok, J. Wijnholds, A. Ballabio, F. P. Cremers & V. Broccoli: Isolation of Crb1, a mouse homologue of Drosophila crumbs, and analysis of its expression pattern in eye and brain. Mech Dev, 110, 203-7 (2002). (Pubitemid 34020642)
21. Bossinger, O., A. Klebes, C. Segbert, C. Theres & E. Knust: Zonula adherens formation in Caenorhabditis elegans requires dlg-1, the homologue of the Drosophila gene discs large. Dev Biol, 230, 29-42 (2001). (Pubitemid 32121557)
22. Omori, Y. & J. Malicki: oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr Biol, 16, 945-57 (2006). (Pubitemid 43744366)
23. Bachmann, A., M. Schneider, E. Theilenberg, F. Grawe & E. Knust: Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity. Nature, 414, 638-43 (2001). (Pubitemid 33151259)
24. Hong, Y., B. Stronach, N. Perrimon, L. Y. Jan & Y. N. Jan: Drosophila Stardust interacts with Crumbs to control polarity of epithelia but not neuroblasts. Nature, 414, 634-8 (2001). (Pubitemid 33151258)
25. Bhat, M. A., S. Izaddoost, Y. Lu, K. O. Cho, K. W. Choi & H. J. Bellen: Discs Lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity. Cell, 96, 833-45 (1999). (Pubitemid 29165086)
26. Roh, M. H., O. Makarova, C. J. Liu, K. Shin, S. Lee, S. Laurinec, M. Goyal, R. Wiggins & B. Margolis: The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. J Cell Biol, 157, 161-72 (2002). (Pubitemid 34847838)
27. Kempkens, O., E. Medina, G. Fernandez-Ballester, S. Ozuyaman, A. Le Bivic, L. Serrano & E. Knust: Computer modelling in combination with in vitro studies reveals similar binding affinities of Drosophila Crumbs for the PDZ domains of Stardust and DmPar-6. Eur J Cell Biol, 85, 753-67 (2006). (Pubitemid 44070573)
28. Bose, R. & J. L. Wrana: Regulation of Par6 by extracellular signals. Curr Opin Cell Biol, 18, 206-12 (2006). (Pubitemid 43375890)
29. Kaltschmidt, J. A. & A. H. Brand: Asymmetric cell division: microtubule dynamics and spindle asymmetry. J Cell Sci, 115, 2257-64 (2002). (Pubitemid 34752969)
30. Suzuki, A. & S. Ohno: The PAR-aPKC system: lessons in polarity. J Cell Sci, 119, 979-87 (2006).
31. Medina, E., J. Williams, E. Klipfell, D. Zarnescu, G. Thomas & A. Le Bivic: Crumbs interacts with moesin and beta (Heavy)-spectrin in the apical membrane skeleton of Drosophila. J Cell Biol, 158, 941-51 (2002). (Pubitemid 35001084)
32. Laprise, P., S. Beronja, N. F. Silva-Gagliardi, M. Pellikka, A. M. Jensen, C. J. McGlade & U. Tepass: The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev Cell, 11, 363-74 (2006). (Pubitemid 44283938)
33. Medina, E., C. Lemmers, L. Lane-Guermonprez & A. Le Bivic: Role of the Crumbs complex in the regulation of junction formation in Drosophila and mammalian epithelial cells. Biol Cell, 94, 305-13 (2002). (Pubitemid 35402314)
34. Bachmann, A., M. Timmer, J. Sierralta, G. Pietrini, E. D. Gundelfinger, E. Knust & U. Thomas: Cell type-specific recruitment of Drosophila Lin-7 to distinct MAGUK-based protein complexes defines novel roles for Sdt and Dlg-S97. J Cell Sci, 117, 1899-909 (2004). (Pubitemid 38745124)
35. Bachmann, A., F. Grawe, K. Johnson & E. Knust: Drosophila Lin-7 is a component of the Crumbs complex in epithelia and photoreceptor cells and prevents light-induced retinal degeneration. Eur J Cell Biol, 87, 123-136 (2008).
36. Wang, Q., T. W. Hurd & B. Margolis: Tight junction protein Par6 interacts with an evolutionarily conserved region in the amino terminus of PALS1/stardust. J Biol Chem, 279, 30715-21 (2004). (Pubitemid 38938004)
37. Nam, S. C. & K. W. Choi: Interaction of Par-6 and Crumbs complexes is essential for photoreceptor morphogenesis in Drosophila. Development, 130, 4363-72 (2003).
38. Djiane, A., S. Yogev & M. Mlodzik: The apical determinants aPKC and dPatj regulate Frizzled-dependent planar cell polarity in the Drosophila eye. Cell, 121, 621-31 (2005). (Pubitemid 40720014)
39. Schulte, G. & V. Bryja: The Frizzled family of unconventional G-protein-coupled receptors. Trends Pharmacol Sci, 28, 518-25 (2007). (Pubitemid 47488504)
40. Assemat, E., E. Bazellieres, E. Pallesi-Pocachard, A. Le Bivic & D. Massey-Harroche: Polarity complex proteins. Biochim Biophys Acta, 1778, 614-30 (2008). (Pubitemid 351317801)
41. den Hollander, A. I., K. Johnson, Y. J. de Kok, A. Klebes, H. G. Brunner, E. Knust & F. P. Cremers: CRB1 has a cytoplasmic domain that is functionally conserved between human and Drosophila. Hum Mol Genet, 10, 2767-73 (2001). (Pubitemid 34026458)
42. Makarova, O., M. H. Roh, C. J. Liu, S. Laurinec & B. Margolis: Mammalian Crumbs3 is a small transmembrane protein linked to protein associated with Lin-7 (Pals1). Gene, 302, 21-9 (2003). (Pubitemid 36078394)
43. Lemmers, C., D. Michel, L. Lane-Guermonprez, M. H. Delgrossi, E. Medina, J. P. Arsanto & A. Le Bivic: CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells. Mol Biol Cell, 15, 1324-33 (2004). (Pubitemid 38316238)
44. Fogg, V. C., C. J. Liu & B. Margolis: Multiple regions of Crumbs3 are required for tight junction formation in MCF10A cells. J Cell Sci, 118, 2859-69 (2005). (Pubitemid 41136363)
45. Roh, M. H., S. Fan, C. J. Liu & B. Margolis: The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells. J Cell Sci, 116, 2895-906 (2003). (Pubitemid 36926979)
46. Kamberov, E., O. Makarova, M. Roh, A. Liu, D. Karnak, S. Straight & B. Margolis: Molecular cloning and characterization of Pals, proteins associated with mLin-7. J Biol Chem, 275, 11425-31 (2000). (Pubitemid 30212796)
47. Li, Y., D. Karnak, B. Demeler, B. Margolis & A. Lavie: Structural basis for L27 domain-mediated assembly of signaling and cell polarity complexes. Embo J, 23, 2723-33 (2004). (Pubitemid 39013545)
48. Feng, W., J. F. Long & M. Zhang: A unified assembly mode revealed by the structures of tetrameric L27 domain complexes formed by mLin-2/mLin-7 and Patj/Pals1 scaffold proteins. Proc Natl Acad Sci U S A, 102, 6861-6 (2005). (Pubitemid 40675407)
49. Feng, W., J. F. Long, J. S. Fan, T. Suetake & M. Zhang: The tetrameric L27 domain complex as an organization platform for supramolecular assemblies. Nat Struct Mol Biol, 11, 475-80 (2004). (Pubitemid 38568953)
50. Philipp, S. & V. Flockerzi: Molecular characterization of a novel human PDZ domain protein with homology to INAD from Drosophila melanogaster. FEBS Lett, 413, 243-8 (1997). (Pubitemid 27353277)
51. Roh, M. H., C. J. Liu, S. Laurinec & B. Margolis: The carboxyl terminus of zona occludens-3 binds and recruits a mammalian homologue of discs lost to tight junctions. J Biol Chem, 277, 27501-9 (2002). (Pubitemid 34951771)
52. Ullmer, C., K. Schmuck, A. Figge & H. Lubbert: Cloning and characterization of MUPP1, a novel PDZ domain protein. FEBS Lett, 424, 63-8 (1998). (Pubitemid 28130353)
53. van de Pavert, S. A., A. Kantardzhieva, A. Malysheva, J. Meuleman, I. Versteeg, C. Levelt, J. Klooster, S. Geiger, M. W. Seeliger, P. Rashbass, A. Le Bivic & J. Wijnholds: Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci, 117, 4169-77 (2004). (Pubitemid 39328304)
54. Straight, S. W., J. N. Pieczynski, E. L. Whiteman, C. J. Liu & B. Margolis: Mammalian lin-7 stabilizes polarity protein complexes. J Biol Chem, 281, 37738-47 (2006). (Pubitemid 46042077)
55. Kantardzhieva, A., I. Gosens, S. Alexeeva, I. M. Punte, I. Versteeg, E. Krieger, C. A. Neefjes-Mol, A. I. den Hollander, S. J. Letteboer, J. Klooster, F. P. Cremers, R. Roepman & J. Wijnholds: MPP5 recruits MPP4 to the CRB1 complex in photoreceptors. Invest Ophthalmol Vis Sci, 46, 2192-201 (2005).
56. McGee, A. W., S. R. Dakoji, O. Olsen, D. S. Bredt, W. A. Lim & K. E. Prehoda: Structure of the SH3-guanylate kinase module from PSD-95 suggests a mechanism for regulated assembly of MAGUK scaffolding proteins. Mol Cell, 8, 1291-301 (2001). (Pubitemid 34085000)
57. Gosens, I., A. Sessa, A. I. den Hollander, S. J. Letteboer, V. Belloni, M. L. Arends, A. Le Bivic, F. P. Cremers, V. Broccoli & R. Roepman: FERM protein EPB41L5 is a novel member of the mammalian CRB-MPP5 polarity complex. Exp Cell Res, 313, 3959-70 (2007). (Pubitemid 350001292)
58. Hsu, Y. C., J. J. Willoughby, A. K. Christensen & A. M. Jensen: Mosaic Eyes is a novel component of the Crumbs complex and negatively regulates photoreceptor apical size. Development, 133, 4849-59 (2006). (Pubitemid 46085051)
59. Massey-Harroche, D., M. H. Delgrossi, L. Lane-Guermonprez, J. P. Arsanto, J. P. Borg, M. Billaud & A. Le Bivic: Evidence for a molecular link between the tuberous sclerosis complex and the Crumbs complex. Hum Mol Genet, 16, 529-36 (2007). (Pubitemid 46522615)
60. Yang, Q. & K. L. Guan: Expanding mTOR signaling. Cell Res, 17, 666-81 (2007). (Pubitemid 47255937)
61. Shaw, R. J. & L. C. Cantley: Ras, PI (3)K and mTOR signalling controls tumour cell growth. Nature, 441, 424-30 (2006). (Pubitemid 44050136)
62. De Virgilio, C. & R. Loewith: The TOR signalling network from yeast to man. Int J Biochem Cell Biol, 38, 1476-81 (2006). (Pubitemid 43729300)
63. Martin, D. E. & M. N. Hall: The expanding TOR signaling network. Curr Opin Cell Biol, 17, 158-66 (2005). (Pubitemid 40380939)
64. Kwiatkowski, D. J. & B. D. Manning: Tuberous sclerosis: a GAP at the crossroads of multiple signaling pathways. Hum Mol Genet, 14 Spec No. 2, R251-8 (2005). (Pubitemid 41631882)
65. Sugihara-Mizuno, Y., M. Adachi, Y. Kobayashi, Y. Hamazaki, M. Nishimura, T. Imai, M. Furuse & S. Tsukita: Molecular characterization of angiomotin/JEAP family proteins: interaction with MUPP1/Patj and their endogenous properties. Genes Cells, 12, 473-86 (2007). (Pubitemid 46488583)
66. Troyanovsky, B., T. Levchenko, G. Mansson, O. Matvijenko & L. Holmgren: Angiomotin: an angiostatin binding protein that regulates endothelial cell migration and tube formation. J Cell Biol, 152, 1247-54 (2001). (Pubitemid 34280181)
67. Bratt, A., W. J. Wilson, B. Troyanovsky, K. Aase, R. Kessler, E. G. Van Meir & L. Holmgren: Angiomotin belongs to a novel protein family with conserved coiledcoil and PDZ binding domains. Gene, 298, 69-77 (2002). (Pubitemid 35284264)
68. Patrie, K. M.: Identification and characterization of a novel tight junction-associated family of proteins that interacts with a WW domain of MAGI-1. Biochim Biophys Acta, 1745, 131-44 (2005). (Pubitemid 41111976)
69. Wells, C. D., J. P. Fawcett, A. Traweger, Y. Yamanaka, M. Goudreault, K. Elder, S. Kulkarni, G. Gish, C. Virag, C. Lim, K. Colwill, A. Starostine, P. Metalnikov & T. Pawson: A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells. Cell, 125, 535-48 (2006).
70. Hamazaki, Y., M. Itoh, H. Sasaki, M. Furuse & S. Tsukita: Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem, 277, 455-61 (2002). (Pubitemid 34952079)
71. Haskins, J., L. Gu, E. S. Wittchen, J. Hibbard & B. R. Stevenson: ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J Cell Biol, 141, 199-208 (1998). (Pubitemid 28182652)
72. Peng, B. H., M. A. White, G. A. Campbell, J. J. Robert, J. C. Lee & R. B. Sutton: Crystallization and preliminary X-ray diffraction of the ZO-binding domain of human occludin. Acta Crystallogr Sect F Struct Biol Cryst Commun, 61, 369-71 (2005). (Pubitemid 44210892)
73. Mazumdar, A. & M. Mazumdar: How one becomes many: blastoderm cellularization in Drosophila melanogaster. Bioessays, 24, 1012-22 (2002). (Pubitemid 35326159)
74. Tepass, U., G. Tanentzapf, R. Ward & R. Fehon: Epithelial cell polarity and cell junctions in Drosophila. Annu Rev Genet, 35, 747-84 (2001). (Pubitemid 34032991)
75. Lecuit, T.: Junctions and vesicular trafficking during Drosophila cellularization. J Cell Sci, 117, 3427-33 (2004). (Pubitemid 39206383)
76. Nam, S. C. & K. W. Choi: Domain-specific early and late function of Dpatj in Drosophila photoreceptor cells. Dev Dyn, 235, 1501-7 (2006).
77. Hutterer, A., J. Betschinger, M. Petronczki & J. A. Knoblich: Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev Cell, 6, 845-54 (2004). (Pubitemid 38745418)
78. Li, Z., L. Wang, T. S. Hays & Y. Cai: Dynein-mediated apical localization of crumbs transcripts is required for Crumbs activity in epithelial polarity. J Cell Biol, 180, 31-8 (2008).
79. Horne-Badovinac, S. & D. Bilder: Dynein Regulates Epithelial Polarity and the Apical Localization of stardust A mRNA. PLoS Genet, 4, e8 (2008).
80. Grawe, F., A. Wodarz, B. Lee, E. Knust & H. Skaer: The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development, 122, 951-9 (1996). (Pubitemid 26095999)
81. Margolis, B. & J. P. Borg: Apicobasal polarity complexes. J Cell Sci, 118, 5157-9 (2005). (Pubitemid 41819579)
82. Bilder, D., M. Schober & N. Perrimon: Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat Cell Biol, 5, 53-8 (2003). (Pubitemid 36054329)
83. Assemat, E., E. Bazellieres, E. Pallesi-Pocachard, A. Le Bivic & D. Massey-Harroche: Polarity complex proteins. Biochim Biophys Acta (2007).
84. Malicki, J.: Harnessing the power of forward genetics- analysis of neuronal diversity and patterning in the zebrafish retina. Trends Neurosci, 23, 531-41 (2000).
85. Mehalow, A. K., S. Kameya, R. S. Smith, N. L. Hawes, J. M. Denegre, J. A. Young, L. Bechtold, N. B. Haider, U. Tepass, J. R. Heckenlively, B. Chang, J. K. Naggert & P. M. Nishina: CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Hum Mol Genet, 12, 2179-89 (2003). (Pubitemid 37098988)
86. Chalmers, A. D., M. Pambos, J. Mason, S. Lang, C. Wylie & N. Papalopulu: aPKC, Crumbs3 and Lgl2 control apicobasal polarity in early vertebrate development. Development, 132, 977-86 (2005). (Pubitemid 40484932)
87. Fleming, T. P. & M. J. Hay: Tissue-specific control of expression of the tight junction polypeptide ZO-1 in the mouse early embryo. Development, 113, 295-304 (1991).
88. Sheth, B., B. Moran, J. M. Anderson & T. P. Fleming: Post-translational control of occludin membrane assembly in mouse trophectoderm: a mechanism to regulate timing of tight junction biogenesis and blastocyst formation. Development, 127, 831-40 (2000). (Pubitemid 30129029)
89. Lee, J. D., N. F. Silva-Gagliardi, U. Tepass, C. J. McGlade & K. V. Anderson: The FERM protein Epb4.1l5 is required for organization of the neural plate and for the epithelial-mesenchymal transition at the primitive streak of the mouse embryo. Development, 134, 2007-16 (2007). (Pubitemid 46979788)
90. Jensen, A. M. & M. Westerfield: Zebrafish mosaic eyes is a novel FERM protein required for retinal lamination and retinal pigmented epithelial tight junction formation. Curr Biol, 14, 711-7 (2004). (Pubitemid 38503609)
91. Wang, Q., X. W. Chen & B. Margolis: PALS1 regulates E-cadherin trafficking in mammalian epithelial cells. Mol Biol Cell, 18, 874-85 (2007). (Pubitemid 46399493)
92. van Rossum, A. G., W. M. Aartsen, J. Meuleman, J. Klooster, A. Malysheva, I. Versteeg, J. P. Arsanto, A. Le Bivic & J. Wijnholds: Pals1/Mpp5 is required for correct localization of Crb1 at the subapical region in polarized Muller glia cells. Hum Mol Genet, 15, 2659-72 (2006). (Pubitemid 44400393)
93. Afonso, C. & D. Henrique: PAR3 acts as a molecular organizer to define the apical domain of chick neuroepithelial cells. J Cell Sci, 119, 4293-304 (2006). (Pubitemid 44774036)
94. Pellikka, M., G. Tanentzapf, M. Pinto, C. Smith, C. J. McGlade, D. F. Ready & U. Tepass: Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature, 416, 143-9 (2002). (Pubitemid 34246466)
95. Izaddoost, S., S. C. Nam, M. A. Bhat, H. J. Bellen & K. W. Choi: Drosophila Crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature, 416, 178-83 (2002).
96. Johnson, K., F. Grawe, N. Grzeschik & E. Knust: Drosophila crumbs is required to inhibit light-induced photoreceptor degeneration. Curr Biol, 12, 1675-80 (2002). (Pubitemid 35161922)
97. Hong, Y., L. Ackerman, L. Y. Jan & Y. N. Jan: Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc Natl Acad Sci U S A, 100, 12712-7 (2003). (Pubitemid 37339964)
98. Richard, M., F. Grawe & E. Knust: DPATJ plays a role in retinal morphogenesis and protects against lightdependent degeneration of photoreceptor cells in the Drosophila eye. Dev Dyn, 235, 895-907 (2006).
99. Tepass, U. & K. P. Harris: Adherens junctions in Drosophila retinal morphogenesis. Trends Cell Biol, 17, 26-35 (2007). (Pubitemid 46027588)
100. Berger, S., N. A. Bulgakova, F. Grawe, K. Johnson & E. Knust: Unraveling the genetic complexity of Drosophila stardust during photoreceptor morphogenesis and prevention of light-induced degeneration. Genetics, 176, 2189-200 (2007). (Pubitemid 47360652)
101. Richard, M., R. Roepman, W. M. Aartsen, A. G. van Rossum, A. I. den Hollander, E. Knust, J. Wijnholds & F. P. Cremers: Towards understanding CRUMBS function in retinal dystrophies. Hum Mol Genet, 15 Spec No 2, R235-43 (2006). (Pubitemid 44446799)
102. Schneeberger, D. & T. Raabe: Mbt, a Drosophila PAK protein, combines with Cdc42 to regulate photoreceptor cell morphogenesis. Development, 130, 427-37 (2003). (Pubitemid 36236120)
103. Karagiosis, S. A. & D. F. Ready: Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development, 131, 725-32 (2004). (Pubitemid 38263189)
104. Malicki, J., S. C. Neuhauss, A. F. Schier, L. Solnica-Krezel, D. L. Stemple, D. Y. Stainier, S. Abdelilah, F. Zwartkruis, Z. Rangini & W. Driever: Mutations affecting development of the zebrafish retina. Development, 123, 263-73 (1996). (Pubitemid 27056753)
105. Malicki, J. & W. Driever: oko meduzy mutations affect neuronal patterning in the zebrafish retina and reveal cell-cell interactions of the retinal neuroepithelial sheet. Development, 126, 1235-46 (1999). (Pubitemid 29182119)
106. Wei, X. & J. Malicki: nagie oko, encoding a MAGUK-family protein, is essential for cellular patterning of the retina. Nat Genet, 31, 150-7 (2002).
107. Wei, X., J. Zou, M. Takechi, S. Kawamura & L. Li: Nok plays an essential role in maintaining the integrity of the outer nuclear layer in the zebrafish retina. Exp Eye Res, 83, 31-44 (2006). (Pubitemid 43783234)
108. den Hollander, A. I., J. R. Heckenlively, L. I. van den Born, Y. J. de Kok, S. D. van der Velde-Visser, U. Kellner, B. Jurklies, M. J. van Schooneveld, A. Blankenagel, K. Rohrschneider, B. Wissinger, J. R. Cruysberg, A. F. Deutman, H. G. Brunner, E. Apfelstedt-Sylla, C. B. Hoyng & F. P. Cremers: Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene. Am J Hum Genet, 69, 198-203 (2001). (Pubitemid 32614031)
109. den Hollander, A. I., J. Davis, S. D. van der Velde-Visser, M. N. Zonneveld, C. O. Pierrottet, R. K. Koenekoop, U. Kellner, L. I. van den Born, J. R. Heckenlively, C. B. Hoyng, P. A. Handford, R. Roepman & F. P. Cremers: CRB1 mutation spectrum in inherited retinal dystrophies. Hum Mutat, 24, 355-69 (2004). (Pubitemid 39473661)
110. Lotery, A. J., S. G. Jacobson, G. A. Fishman, R. G. Weleber, A. B. Fulton, P. Namperumalsamy, E. Heon, A. V. Levin, S. Grover, J. R. Rosenow, K. K. Kopp, V. C. Sheffield & E. M. Stone: Mutations in the CRB1 gene cause Leber congenital amaurosis. Arch Ophthalmol, 119, 415-20 (2001). (Pubitemid 32207264)
111. Lotery, A. J., A. Malik, S. A. Shami, M. Sindhi, B. Chohan, C. Maqbool, P. A. Moore, M. J. Denton & E. M. Stone: CRB1 mutations may result in retinitis pigmentosa without para-arteriolar RPE preservation. Ophthalmic Genet, 22, 163-9 (2001). (Pubitemid 34248303)
112. Jacobson, S. G., A. V. Cideciyan, T. S. Aleman, M. J. Pianta, A. Sumaroka, S. B. Schwartz, E. E. Smilko, A. H. Milam, V. C. Sheffield & E. M. Stone: Crumbs homolog 1 (CRB1) mutations result in a thick human retina with abnormal lamination. Hum Mol Genet, 12, 1073-8 (2003). (Pubitemid 36553527)
113. McKay, G. J., S. Clarke, J. A. Davis, D. A. Simpson & G. Silvestri: Pigmented paravenous chorioretinal atrophy is associated with a mutation within the crumbs homolog 1 (CRB1) gene. Invest Ophthalmol Vis Sci, 46, 322-8 (2005). (Pubitemid 40041215)
114. van de Pavert, S. A., A. S. Sanz, W. M. Aartsen, R. M. Vos, I. Versteeg, S. C. Beck, J. Klooster, M. W. Seeliger & J. Wijnholds: Crb1 is a determinant of retinal apical Muller glia cell features. Glia, 55, 1486-97 (2007). (Pubitemid 47461163)
115. Stohr, H., L. L. Molday, R. S. Molday, B. H. Weber, B. Biedermann, A. Reichenbach & F. Kramer: Membraneassociated guanylate kinase proteins MPP4 and MPP5 associate with Veli3 at distinct intercellular junctions of the neurosensory retina. J Comp Neurol, 481, 31-41 (2005). (Pubitemid 39578768)
116. Kantardzhieva, A., S. Alexeeva, I. Versteeg & J. Wijnholds: MPP3 is recruited to the MPP5 protein scaffold at the retinal outer limiting membrane. Febs J, 273, 1152-65 (2006). (Pubitemid 43345036)
117. Aartsen, W. M., A. Kantardzhieva, J. Klooster, A. G. van Rossum, S. A. van de Pavert, I. Versteeg, B. N. Cardozo, F. Tonagel, S. C. Beck, N. Tanimoto, M. W. Seeliger & J. Wijnholds: Mpp4 recruits Psd95 and Veli3 towards the photoreceptor synapse. Hum Mol Genet, 15, 1291-302 (2006).
118. Stohr, H. & B. H. Weber: Cloning and characterization of the human retina-specific gene MPP4, a novel member of the p55 subfamily of MAGUK proteins. Genomics, 74, 377-84 (2001).
119. Conte, I., M. Lestingi, A. den Hollander, M. G. Miano, G. Alfano, D. Circolo, M. Pugliese, F. Testa, F. Simonelli, E. Rinaldi, M. Baiget, S. Banfi & A. Ciccodicola: Characterization of MPP4, a gene highly expressed in photoreceptor cells, and mutation analysis in retinitis pigmentosa. Gene, 297, 33-8 (2002). (Pubitemid 35217777)
120. Stohr, H., J. Stojic & B. H. Weber: Cellular localization of the MPP4 protein in the mammalian retina. Invest Ophthalmol Vis Sci, 44, 5067-74 (2003). (Pubitemid 37475372)
121. Yang, J., B. Pawlyk, X. H. Wen, M. Adamian, M. Soloviev, N. Michaud, Y. Zhao, M. A. Sandberg, C. L. Makino & T. Li: Mpp4 is required for proper localization of plasma membrane calcium ATPases and maintenance of calcium homeostasis at the rod photoreceptor synaptic terminals. Hum Mol Genet, 16, 1017-29 (2007). (Pubitemid 47071652)
122. Fan, S., T. W. Hurd, C. J. Liu, S. W. Straight, T. Weimbs, E. A. Hurd, S. E. Domino & B. Margolis: Polarity proteins control ciliogenesis via kinesin motor interactions. Curr Biol, 14, 1451-61 (2004). (Pubitemid 39123742)
123. Olsen, O., L. Funke, J. F. Long, M. Fukata, T. Kazuta, J. C. Trinidad, K. A. Moore, H. Misawa, P. A. Welling, A. L. Burlingame, M. Zhang & D. S. Bredt: Renal defects associated with improper polarization of the CRB and DLG polarity complexes in MALS-3 knockout mice. J Cell Biol, 179, 151-64 (2007). (Pubitemid 47606691)
124. Grasset, E., J. Bernabeu & M. Pinto: Epithelial properties of human colonic carcinoma cell line Caco-2: effect of secretagogues. Am J Physiol, 248, C410-8 (1985). (Pubitemid 15018347)
125. Wice, B. M., G. Trugnan, M. Pinto, M. Rousset, G. Chevalier, E. Dussaulx, B. Lacroix & A. Zweibaum: The intracellular accumulation of UDP-N-acetylhexosamines is concomitant with the inability of human colon cancer cells to differentiate. J Biol Chem, 260, 139-46 (1985). (Pubitemid 15165293)
126. Le Bivic, A., A. Quaroni, B. Nichols & E. Rodriguez-Boulan: Biogenetic pathways of plasma membrane proteins in Caco-2, a human intestinal epithelial cell line. J Cell Biol, 111, 1351-61 (1990).
127. Matter, K., M. Brauchbar, K. Bucher & H. P. Hauri: Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2). Cell, 60, 429-37 (1990).
128. O'Brien, L. E., M. M. Zegers & K. E. Mostov: Opinion: Building epithelial architecture: insights from three-dimensional culture models. Nat Rev Mol Cell Biol, 3, 531-7 (2002). (Pubitemid 34733434)
129. Saaf, A. M., J. M. Halbleib, X. Chen, S. T. Yuen, S. Y. Leung, W. J. Nelson & P. O. Brown: Parallels between global transcriptional programs of polarizing Caco-2 intestinal epithelial cells in vitro and gene expression programs in normal colon and colon cancer. Mol Biol Cell, 18, 4245-60 (2007). (Pubitemid 350060156)
130. Sfakianos, J., A. Togawa, S. Maday, M. Hull, M. Pypaert, L. Cantley, D. Toomre & I. Mellman: Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. J Cell Biol, 179, 1133-40 (2007). (Pubitemid 350277733)
131. Gao, L., G. Joberty & I. G. Macara: Assembly of epithelial tight junctions is negatively regulated by Par6. Curr Biol, 12, 221-5 (2002). (Pubitemid 34122378)
132. Straight, S. W., K. Shin, V. C. Fogg, S. Fan, C. J. Liu, M. Roh & B. Margolis: Loss of PALS1 expression leads to tight junction and polarity defects. Mol Biol Cell, 15, 1981-90 (2004). (Pubitemid 38401844)
133. Shin, K., S. Straight & B. Margolis: PATJ regulates tight junction formation and polarity in mammalian epithelial cells. J Cell Biol, 168, 705-11 (2005). (Pubitemid 40328155)
134. Michel, D., J. P. Arsanto, D. Massey-Harroche, C. Beclin, J. Wijnholds & A. Le Bivic: PATJ connects and stabilizes apical and lateral components of tight junctions in human intestinal cells. J Cell Sci, 118, 4049-57 (2005). (Pubitemid 41410286)
135. Hurd, T. W., L. Gao, M. H. Roh, I. G. Macara & B. Margolis: Direct interaction of two polarity complexes implicated in epithelial tight junction assembly. Nat Cell Biol, 5, 137-42 (2003). (Pubitemid 36210848)
136. Chishti, A. H., A. C. Kim, S. M. Marfatia, M. Lutchman, M. Hanspal, H. Jindal, S. C. Liu, P. S. Low, G. A. Rouleau, N. Mohandas, J. A. Chasis, J. G. Conboy, P. Gascard, Y. Takakuwa, S. C. Huang, E. J. Benz, Jr., A. Bretscher, R. G. Fehon, J. F. Gusella, V. Ramesh, F. Solomon, V. T. Marchesi, S. Tsukita, S. Tsukita, K. B. Hoover & et al.: The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem Sci, 23, 281-2 (1998). (Pubitemid 28461889)
137. Hurd, T. W., S. Fan, C. J. Liu, H. K. Kweon, K. Hakansson & B. Margolis: Phosphorylation-dependent binding of 14-3-3 to the polarity protein Par3 regulates cell polarity in mammalian epithelia. Curr Biol, 13, 2082-90 (2003). (Pubitemid 37502525)
138. Etienne-Manneville, S., J. B. Manneville, S. Nicholls, M. A. Ferenczi & A. Hall: Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J Cell Biol, 170, 895-901 (2005). (Pubitemid 41306289)
139. Grindstaff, K. K., C. Yeaman, N. Anandasabapathy, S. C. Hsu, E. Rodriguez-Boulan, R. H. Scheller & W. J. Nelson: Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell, 93, 731-40 (1998). (Pubitemid 28257580)
140. Yeaman, C., K. K. Grindstaff & W. J. Nelson: Mechanism of recruiting Sec6/8 (exocyst) complex to the apical junctional complex during polarization of epithelial cells. J Cell Sci, 117, 559-70 (2004). (Pubitemid 38240197)
141. Hsu, S. C., C. D. Hazuka, D. L. Foletti & R. H. Scheller: Targeting vesicles to specific sites on the plasma membrane: the role of the sec6/8 complex. Trends Cell Biol, 9, 150-3 (1999). (Pubitemid 29161441)
142. Lu, H. & D. Bilder: Endocytic control of epithelial polarity and proliferation in Drosophila. Nat Cell Biol, 7, 1232-9 (2005).
143. Garami, A., F. J. Zwartkruis, T. Nobukuni, M. Joaquin, M. Roccio, H. Stocker, S. C. Kozma, E. Hafen, J. L. Bos & G. Thomas: Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol Cell, 11, 1457-66 (2003). (Pubitemid 36776533)
144. Inoki, K., Y. Li, T. Xu & K. L. Guan: Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev, 17, 1829-34 (2003). (Pubitemid 36944560)
145. Saucedo, L. J., X. Gao, D. A. Chiarelli, L. Li, D. Pan & B. A. Edgar: Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat Cell Biol, 5, 566-71 (2003). (Pubitemid 36781092)
146. Katajisto, P., T. Vallenius, K. Vaahtomeri, N. Ekman, L. Udd, M. Tiainen & T. P. Makela: The LKB1 tumor suppressor kinase in human disease. Biochim Biophys Acta, 1775, 63-75 (2007). (Pubitemid 44889272)
147. Krapivinsky, G., I. Medina, L. Krapivinsky, S. Gapon & D. E. Clapham: SynGAP-MUPP1-CaMKII synaptic complexes regulate p38 MAP kinase activity and NMDA receptor-dependent synaptic AMPA receptor potentiation. Neuron, 43, 563-74 (2004). (Pubitemid 39094682)
148. Kimber, W. A., L. Trinkle-Mulcahy, P. C. Cheung, M. Deak, L. J. Marsden, A. Kieloch, S. Watt, R. T. Javier, A. Gray, C. P. Downes, J. M. Lucocq & D. R. Alessi: Evidence that the tandem-pleckstrin-homology-domaincontaining protein TAPP1 interacts with Ptd (3, 4)P2 and the multi-PDZ-domain-containing protein MUPP1 in vivo. Biochem J, 361, 525-36 (2002). (Pubitemid 34177822)
149. Dakoji, S., S. Tomita, S. Karimzadegan, R. A. Nicoll & D. S. Bredt: Interaction of transmembrane AMPA receptor regulatory proteins with multiple membrane associated guanylate kinases. Neuropharmacology, 45, 849-56 (2003). (Pubitemid 38340369)
150. Griffon, N., F. Jeanneteau, F. Prieur, J. Diaz & P. Sokoloff: CLIC6, a member of the intracellular chloride channel family, interacts with dopamine D (2)-like receptors. Brain Res Mol Brain Res, 117, 47-57 (2003). (Pubitemid 37123109)
151. Barritt, D. S., M. T. Pearn, A. H. Zisch, S. S. Lee, R. T. Javier, E. B. Pasquale & W. B. Stallcup: The multi-PDZ domain protein MUPP1 is a cytoplasmic ligand for the membrane-spanning proteoglycan NG2. J Cell Biochem, 79, 213-24 (2000).
152. Jeansonne, B., Q. Lu, D. A. Goodenough & Y. H. Chen: Claudin-8 interacts with multi-PDZ domain protein 1 (MUPP1) and reduces paracellular conductance in epithelial cells. Cell Mol Biol (Noisy-le-grand), 49, 13-21 (2003).
153. Mancini, A., A. Koch, M. Stefan, H. Niemann & T. Tamura: The direct association of the multiple PDZ domain containing proteins (MUPP-1) with the human c-Kit Cterminus is regulated by tyrosine kinase activity. FEBS Lett, 482, 54-8 (2000).
154. Coyne, C. B., T. Voelker, S. L. Pichla & J. M. Bergelson: The coxsackievirus and adenovirus receptor interacts with the multi-PDZ domain protein-1 (MUPP-1) within the tight junction. J Biol Chem, 279, 48079-84 (2004). (Pubitemid 39540961)