DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila

Sotillos, Sol; Díaz-Meco, María Teresa; Caminero, Eva; Moscat, Jorge; Campuzano, Sonsoles

doi:10.1083/jcb.200311031

Title: DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila

Journal Article · 09 August 2004 · Journal of Cell Biology

DOI: https://doi.org/10.1083/jcb.200311031 · OSTI ID:1625133

Sotillos, Sol ^[1]; Díaz-Meco, María Teresa ^[1]; Caminero, Eva ^[1]; Moscat, Jorge ^[1]; Campuzano, Sonsoles ^[1]

Consejo Superior de Investigaciones Científicas, Madrid (Spain). Centro de Biología Molecular Severo Ochoa; Universidad Autonóma de Madrid, Cantoblanco, Madrid (Spain)

Both in Drosophila and vertebrate epithelial cells, the establishment of apicobasal polarity requires the apically localized, membrane-associated Par-3–Par-6–aPKC protein complex. In Drosophila, this complex colocalizes with the Crumbs–Stardust (Sdt)–Pals1-associated TJ protein (Patj) complex. Genetic and molecular analyses suggest a functional relationship between them. In this work we show, by overexpression of a kinase-dead Drosophila atypical PKC (DaPKC), the requirement for the kinase activity of DaPKC to maintain the position of apical determinants and to restrict the localization of basolateral ones. We demonstrate a novel physical interaction between the apical complexes, via direct binding of DaPKC to both Crb and Patj, and identify Crumbs as a phosphorylation target of DaPKC. This phosphorylation of Crumbs is functionally significant. Thus, a nonphosphorylatable Crumbs protein behaves in vivo as a dominant negative. Moreover, the phenotypic effect of overexpressing wild-type Crumbs is suppressed by reducing DaPKC activity. These results provide a mechanistic framework for the functional interaction between the Par-3–Par-6–aPKC and Crumbs–Sdt–Patj complexes based in the posttranslational modification of Crb by DaPKC.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Consejo Superior de Investigaciones Cientificas (CSIC), Madrid (Spain); Universidad Autonóma de Madrid, Cantoblanco, Madrid (Spain)

Sponsoring Organization:: Comunidad Autónoma de Madrid (CAM); Dirección General de Investigación Científica y Técnica; Fundación Ramón Areces

Grant/Contract Number:: 08.5/0030/2000; PB98-0682; BMC2002-00411; SAF1999-0053; 2FD97-1429; SAF2000-0175; 08.1/0060/2000

OSTI ID:: 1625133

Journal Information:: Journal of Cell Biology, Vol. 166, Issue 4; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (67)

Assembly of Epithelial Tight Junctions Is Negatively Regulated by Par6 Gao, Lin; Joberty, Gérard; Macara, Ian G. Current Biology, Vol. 12, Issue 3 https://doi.org/10.1016/S0960-9822(01)00663-7	journal	February 2002
The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions Woods, Daniel F.; Bryant, Peter J. Cell, Vol. 66, Issue 3 https://doi.org/10.1016/0092-8674(81)90009-X	journal	August 1991
An Atypical PKC Directly Associates and Colocalizes at the Epithelial Tight Junction with ASIP, a Mammalian Homologue of Caenorhabditis elegans Polarity Protein PAR-3 Izumi, Yasushi; Hirose, Tomonori; Tamai, Yoko Journal of Cell Biology, Vol. 143, Issue 1 https://doi.org/10.1083/jcb.143.1.95	journal	October 1998
Crumbs interacts with moesin and βHeavy-spectrin in the apical membrane skeleton of Drosophila Médina, Emmanuelle; Williams, Janice; Klipfell, Elizabeth Journal of Cell Biology, Vol. 158, Issue 5 https://doi.org/10.1083/jcb.200203080	journal	September 2002
Drosophila PAR-1 and 14-3-3 Inhibit Bazooka/PAR-3 to Establish Complementary Cortical Domains in Polarized Cells Benton, Richard; Johnston, Daniel St Cell, Vol. 115, Issue 6 https://doi.org/10.1016/S0092-8674(03)00938-3	journal	December 2003
Epithelial Cell Polarity and Cell Junctions in Drosophila Tepass, Ulrich; Tanentzapf, Guy; Ward, Robert Annual Review of Genetics, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.genet.35.102401.091415	journal	December 2001
Direct interaction of two polarity complexes implicated in epithelial tight junction assembly Hurd, Toby W.; Gao, Lin; Roh, Michael H. Nature Cell Biology, Vol. 5, Issue 2 https://doi.org/10.1038/ncb923	journal	January 2003
CRB3 Binds Directly to Par6 and Regulates the Morphogenesis of the Tight Junctions in Mammalian Epithelial Cells Lemmers, Céline; Michel, Didier; Lane-Guermonprez, Lydie Molecular Biology of the Cell, Vol. 15, Issue 3 https://doi.org/10.1091/mbc.e03-04-0235	journal	March 2004
Interaction of Par-6 and Crumbs complexes is essential for photoreceptor morphogenesis in Drosophila Nam, S. -C. Development, Vol. 130, Issue 18 https://doi.org/10.1242/dev.00648	journal	September 2003
armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. Müller, H. A.; Wieschaus, E. Journal of Cell Biology, Vol. 134, Issue 1 https://doi.org/10.1083/jcb.134.1.149	journal	July 1996
Discs Lost, a Novel Multi-PDZ Domain Protein, Establishes and Maintains Epithelial Polarity Bhat, Manzoor A.; Izaddoost, Shayan; Lu, Yue Cell, Vol. 96, Issue 6 https://doi.org/10.1016/S0092-8674(00)80593-0	journal	March 1999
aPKC kinase activity is required for the asymmetric differentiation of the premature junctional complex during epithelial cell polarization Suzuki, Atsushi; Ishiyama, Chikako; Hashiba, Katsutaka Journal of Cell Science, Vol. 115, Issue 18 https://doi.org/10.1242/jcs.00032	journal	September 2002
Atypical PKC Phosphorylates PAR-1 Kinases to Regulate Localization and Activity Hurov, Jonathan B.; Watkins, Janis L.; Piwnica-Worms, Helen Current Biology, Vol. 14, Issue 8 https://doi.org/10.1016/j.cub.2004.04.007	journal	April 2004
Drosophila Atypical Protein Kinase C Associates with Bazooka and Controls Polarity of Epithelia and Neuroblasts Wodarz, Andreas; Ramrath, Andreas; Grimm, Alexandra Journal of Cell Biology, Vol. 150, Issue 6 https://doi.org/10.1083/jcb.150.6.1361	journal	September 2000
Localization of apical epithelial determinants by the basolateral PDZ protein Scribble Bilder, David; Perrimon, Norbert Nature, Vol. 403, Issue 6770 https://doi.org/10.1038/35001108	journal	February 2000
Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia Rolls, Melissa M.; Albertson, Roger; Shih, Hsin-Pei Journal of Cell Biology, Vol. 163, Issue 5 https://doi.org/10.1083/jcb.200306079	journal	December 2003
DmPAR-6 directs epithelial polarity and asymmetric cell division of neuroblasts in Drosophila Petronczki, Mark; Knoblich, Juergen A. Nature Cell Biology, Vol. 3, Issue 1 https://doi.org/10.1038/35050550	journal	December 2000
The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl Betschinger, Jörg; Mechtler, Karl; Knoblich, Juergen A. Nature, Vol. 422, Issue 6929 https://doi.org/10.1038/nature01486	journal	March 2003
Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis Tanentzapf, Guy; Smith, Christian; McGlade, Jane Journal of Cell Biology, Vol. 151, Issue 4 https://doi.org/10.1083/jcb.151.4.891	journal	November 2000
Composition and Formation of Intercellular Junctions in Epithelial Cells Knust, E. Science, Vol. 298, Issue 5600 https://doi.org/10.1126/science.1072161	journal	December 2002
Integrated activity of PDZ protein complexes regulates epithelial polarity Bilder, David; Schober, Markus; Perrimon, Norbert Nature Cell Biology, Vol. 5, Issue 1 https://doi.org/10.1038/ncb897	journal	December 2002
Cooperative Regulation of Cell Polarity and Growth by Drosophila Tumor Suppressors Bilder, D. Science, Vol. 289, Issue 5476 https://doi.org/10.1126/science.289.5476.113	journal	July 2000
Visualization of Gene Expression in Living Adult Drosophila Calleja, M.; Moreno, E.; Pelaz, S. Science, Vol. 274, Issue 5285 https://doi.org/10.1126/science.274.5285.252	journal	October 1996
The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells Roh, Michael H.; Fan, Shuling; Liu, Chia-Jen Journal of Cell Science, Vol. 116, Issue 14 https://doi.org/10.1242/jcs.00500	journal	July 2003
Molecular cloning of lethal(2)giant larvae, a recessive oncogene of Drosophila melanogaster. Mechler, B. M.; McGinnis, W.; Gehring, W. J. The EMBO Journal, Vol. 4, Issue 6 https://doi.org/10.1002/j.1460-2075.1985.tb03816.x	journal	June 1985
Crumbs, a Component of the Apical Membrane, Is Required for Zonula Adherens Formation in Primary Epithelia ofDrosophila Tepass, Ulrich Developmental Biology, Vol. 177, Issue 1 https://doi.org/10.1006/dbio.1996.0157	journal	July 1996
Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization Tanentzapf, Guy; Tepass, Ulrich Nature Cell Biology, Vol. 5, Issue 1 https://doi.org/10.1038/ncb896	journal	December 2002
Drosophila Stardust interacts with Crumbs to control polarity of epithelia but not neuroblasts Hong, Yang; Stronach, Beth; Perrimon, Norbert Nature, Vol. 414, Issue 6864 https://doi.org/10.1038/414634a	journal	December 2001
Origins of Cell Polarity Drubin, David G.; Nelson, W. James Cell, Vol. 84, Issue 3 https://doi.org/10.1016/S0092-8674(00)81278-7	journal	February 1996
Zonula Adherens Formation in Caenorhabditis elegans Requires dlg-1, the Homologue of the Drosophila Gene discs large Bossinger, Olaf; Klebes, Ansgar; Segbert, Christoph Developmental Biology, Vol. 230, Issue 1 https://doi.org/10.1006/dbio.2000.0113	journal	February 2001
Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity Bachmann, André; Schneider, Martina; Theilenberg, Eva Nature, Vol. 414, Issue 6864 https://doi.org/10.1038/414638a	journal	December 2001
Composition and function of PDZ protein complexes during cell polarization Roh, Michael H.; Margolis, Ben American Journal of Physiology-Renal Physiology, Vol. 285, Issue 3 https://doi.org/10.1152/ajprenal.00086.2003	journal	September 2003
Loss of PALS1 Expression Leads to Tight Junction and Polarity Defects Straight, Samuel W.; Shin, Kunyoo; Fogg, Vanessa C. Molecular Biology of the Cell, Vol. 15, Issue 4 https://doi.org/10.1091/mbc.e03-08-0620	journal	April 2004
Control of spindle orientation in Drosophila by the Par-3-related PDZ-domain protein Bazooka Kuchinke, Ute; Grawe, Ferdi; Knust, Elisabeth Current Biology, Vol. 8, Issue 25 https://doi.org/10.1016/S0960-9822(98)00016-5	journal	December 1998
A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl Plant, Pamela J.; Fawcett, James P.; Lin, Dan C. C. Nature Cell Biology, Vol. 5, Issue 4 https://doi.org/10.1038/ncb948	journal	March 2003
The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost Roh, Michael H.; Makarova, Olga; Liu, Chia-Jen Journal of Cell Biology, Vol. 157, Issue 1 https://doi.org/10.1083/jcb.200109010	journal	April 2002
The interaction of p62 with RIP links the atypical PKCs to NF-kappa B activation Sanz, L. The EMBO Journal, Vol. 18, Issue 11 https://doi.org/10.1093/emboj/18.11.3044	journal	June 1999
The Drosophila Cell Survival Gene discs lost Encodes a Cytoplasmic Codanin-1-like Protein, Not a Homolog of Tight Junction PDZ Protein Patj Pielage, Jan; Stork, Tobias; Bunse, Ingrid Developmental Cell, Vol. 5, Issue 6 https://doi.org/10.1016/S1534-5807(03)00358-7	journal	December 2003
Genetic control of epithelial cell polarity: Lessons fromDrosophila M�ller, H. -Arno J. Developmental Dynamics, Vol. 218, Issue 1 https://doi.org/10.1002/(SICI)1097-0177(200005)218:1<52::AID-DVDY5>3.0.CO;2-L	journal	May 2000
Atypical Protein Kinase C Is Involved in the Evolutionarily Conserved Par Protein Complex and Plays a Critical Role in Establishing Epithelia-Specific Junctional Structures Suzuki, Atsushi; Yamanaka, Tomoyuki; Hirose, Tomonori Journal of Cell Biology, Vol. 152, Issue 6 https://doi.org/10.1083/jcb.152.6.1183	journal	March 2001
Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of drosophila Wodarz, Andreas; Hinz, Uwe; Engelbert, Martin Cell, Vol. 82, Issue 1 https://doi.org/10.1016/0092-8674(95)90053-5	journal	July 1995
Parsing the Polarity Code Macara, Ian G. Nature Reviews Molecular Cell Biology, Vol. 5, Issue 3 https://doi.org/10.1038/nrm1332	journal	March 2004
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Brand, A. H.; Perrimon, N. Development, Vol. 118, Issue 2 https://doi.org/10.1242/dev.118.2.401	journal	June 1993
The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions Grawe, F.; Wodarz, A.; Lee, B. Development, Vol. 122, Issue 3 https://doi.org/10.1242/dev.122.3.951	journal	March 1996
Involvement of ASIP/PAR-3 in the promotion of epithelial tight junction formation Hirose, Tomonori; Izumi, Yasushi; Nagashima, Yoji Journal of Cell Science, Vol. 115, Issue 12 https://doi.org/10.1242/jcs.115.12.2485	journal	June 2002
Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis Hortsch, M.; Patel, N. H.; Bieber, A. J. Development, Vol. 110, Issue 4 https://doi.org/10.1242/dev.110.4.1327	journal	December 1990
Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila Wodarz, A.; Hinz, U.; Engelbert, M. Trends in Genetics, Vol. 11, Issue 10, p. 387 https://doi.org/10.1016/s0168-9525(00)89127-1	journal	October 1995
Discs Lost, a Novel Multi-PDZ Domain Protein, Establishes and Maintains Epithelial Polarity Bhat, Manzoor A.; Izaddoost, Shayan; Lu, Yue Cell, Vol. 115, Issue 6 https://doi.org/10.1016/s0092-8674(03)00973-5	journal	December 2003
Molecular cloning of lethal(2)giant larvae, a recessive oncogene of Drosophila melanogaster. Mechler, B. M.; McGinnis, W.; Gehring, W. J. The EMBO Journal, Vol. 4, Issue 6 https://doi.org/10.1002/j.1460-2075.1985.tb03816.x	journal	June 1985
Protein kinase C ζ isoform is critical for mitogenic signal transduction Berra, Edurne; Diaz-Meco, Maria T.; Dominguez, Isabel Cell, Vol. 74, Issue 3 https://doi.org/10.1016/0092-8674(93)80056-k	journal	August 1993
Intercellular junctions and cellular polarity: the PAR–aPKC complex, a conserved core cassette playing fundamental roles in cell polarity Ohno, Shigeo Current Opinion in Cell Biology, Vol. 13, Issue 5 https://doi.org/10.1016/s0955-0674(00)00264-7	journal	October 2001
Positional cloning of heart and soul reveals multiple roles for PKCλ in zebrafish organogenesis Horne-Badovinac, Sally; Lin, Dan; Waldron, Steve Current Biology, Vol. 11, Issue 19 https://doi.org/10.1016/s0960-9822(01)00458-4	journal	October 2001
A conserved motif in Crumbs is required for E-cadherin localisation and zonula adherens formation in Drosophila Klebes, Ansgar; Knust, Elisabeth Current Biology, Vol. 10, Issue 2 https://doi.org/10.1016/s0960-9822(99)00277-8	journal	January 2000
Targeted Disruption of the ζPKC Gene Results in the Impairment of the NF-κB Pathway Leitges, Michael; Sanz, Laura; Martin, Pilar Molecular Cell, Vol. 8, Issue 4 https://doi.org/10.1016/s1097-2765(01)00361-6	journal	October 2001
Cell polarity: the PARty expands Doe, Chris Q. Nature Cell Biology, Vol. 3, Issue 1 https://doi.org/10.1038/35050684	journal	January 2001
Drosophila Stardust interacts with Crumbs to control polarity of epithelia but not neuroblasts Hong, Yang; Stronach, Beth; Perrimon, Norbert Nature, Vol. 414, Issue 6864 https://doi.org/10.1038/414634a	journal	December 2001
Drosophila Stardust is a partner of Crumbs in the control of epithelial cell polarity Bachmann, André; Schneider, Martina; Theilenberg, Eva Nature, Vol. 414, Issue 6864 https://doi.org/10.1038/414638a	journal	December 2001
The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl Betschinger, Jörg; Mechtler, Karl; Knoblich, Juergen A. Nature, Vol. 422, Issue 6929 https://doi.org/10.1038/nature01486	journal	March 2003
Parsing the Polarity Code Macara, Ian G. Nature Reviews Molecular Cell Biology, Vol. 5, Issue 3 https://doi.org/10.1038/nrm1332	journal	March 2004
Drosophila Atypical Protein Kinase C Associates with Bazooka and Controls Polarity of Epithelia and Neuroblasts Wodarz, Andreas; Ramrath, Andreas; Grimm, Alexandra Journal of Cell Biology, Vol. 150, Issue 6 https://doi.org/10.1083/jcb.150.6.1361	journal	September 2000
Atypical Protein Kinase C Is Involved in the Evolutionarily Conserved Par Protein Complex and Plays a Critical Role in Establishing Epithelia-Specific Junctional Structures Suzuki, Atsushi; Yamanaka, Tomoyuki; Hirose, Tomonori Journal of Cell Biology, Vol. 152, Issue 6 https://doi.org/10.1083/jcb.152.6.1183	journal	March 2001
Composition and Formation of Intercellular Junctions in Epithelial Cells Knust, E. Science, Vol. 298, Issue 5600 https://doi.org/10.1126/science.1072161	journal	December 2002
Epithelial Cell Polarity and Cell Junctions in Drosophila Tepass, Ulrich; Tanentzapf, Guy; Ward, Robert Annual Review of Genetics, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.genet.35.102401.091415	journal	December 2001
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes Brand, A. H.; Perrimon, N. Development, Vol. 118, Issue 2 https://doi.org/10.1242/dev.118.2.401	journal	June 1993
The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions Grawe, F.; Wodarz, A.; Lee, B. Development, Vol. 122, Issue 3 https://doi.org/10.1242/dev.122.3.951	journal	March 1996
The Crumbs3-Pals1 complex participates in the establishment of polarity in mammalian epithelial cells Roh, Michael H.; Fan, Shuling; Liu, Chia-Jen Journal of Cell Science, Vol. 116, Issue 14 https://doi.org/10.1242/jcs.00500	journal	July 2003
Involvement of ASIP/PAR-3 in the promotion of epithelial tight junction formation Hirose, Tomonori; Izumi, Yasushi; Nagashima, Yoji Journal of Cell Science, Vol. 115, Issue 12 https://doi.org/10.1242/jcs.115.12.2485	journal	June 2002

Cited By (87)

The Hippo pathway and apico–basal cell polarity Genevet, Alice; Tapon, Nicolas Biochemical Journal, Vol. 436, Issue 2 https://doi.org/10.1042/bj20110217	journal	May 2011
Coordinated protein sorting, targeting and distribution in polarized cells Mellman, Ira; Nelson, W. James Nature Reviews Molecular Cell Biology, Vol. 9, Issue 11 https://doi.org/10.1038/nrm2525	journal	November 2008
Atypical PKC contributes to poor prognosis through loss of apical-basal polarity and Cyclin E overexpression in ovarian cancer Eder, A. M.; Sui, X.; Rosen, D. G. Proceedings of the National Academy of Sciences, Vol. 102, Issue 35 https://doi.org/10.1073/pnas.0505641102	journal	August 2005
Using Drosophila melanogaster to map human cancer pathways Brumby, Anthony M.; Richardson, Helena E. Nature Reviews Cancer, Vol. 5, Issue 8 https://doi.org/10.1038/nrc1671	journal	July 2005
Crumbs3 Is Essential for Proper Epithelial Development and Viability Whiteman, Eileen L.; Fan, Shuling; Harder, Jennifer L. Molecular and Cellular Biology, Vol. 34, Issue 1 https://doi.org/10.1128/mcb.00999-13	journal	January 2014
Yorkie and JNK revert syncytial muscles into myoblasts during Org-1–dependent lineage reprogramming Schaub, Christoph; Rose, Marcel; Frasch, Manfred Journal of Cell Biology, Vol. 218, Issue 11 https://doi.org/10.1083/jcb.201905048	journal	October 2019
Polarization and Myelination in Myelinating Glia Masaki, Toshihiro ISRN Neurology, Vol. 2012 https://doi.org/10.5402/2012/769412	journal	December 2012
Multiple domains in the Crumbs Homolog 2a (Crb2a) protein are required for regulating rod photoreceptor size Hsu, Ya-Chu; Jensen, Abbie M. BMC Cell Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2121-11-60	journal	July 2010
A Polybasic Domain in aPKC Mediates Par-6-Dependent Control of Plasma Membrane Targeting and Kinase Activity Dong, Wei; Lu, Juan; Zhang, Xuejing https://doi.org/10.1101/588624	posted_content	January 2019
Expression and localization of the polarity protein CRB2 in adult mouse brain: a comparison with the CRB1rd8 mutant mouse model Dolón, Jorge F.; Paniagua, Antonio E.; Valle, Vicente Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30210-5	journal	August 2018
Towards understanding CRUMBS function in retinal dystrophies Richard, Mélisande; Roepman, Ronald; Aartsen, Wendy M. Human Molecular Genetics, Vol. 15, Issue suppl_2 https://doi.org/10.1093/hmg/ddl195	journal	October 2006
Nuclear fallout provides a new link between aPKC and polarized cell trafficking Calero-Cuenca, Francisco J.; Espinosa-Vázquez, José Manuel; Reina-Campos, Miguel BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0253-6	journal	April 2016
Epithelial cell polarity: what flies can teach us about cancer Bergstralh, Daniel T.; St Johnston, Daniel Essays in Biochemistry, Vol. 53 https://doi.org/10.1042/bse0530129	journal	August 2012
Mesenchymal–epithelial transition in development and reprogramming Pei, Duanqing; Shu, Xiaodong; Gassama-Diagne, Ama Nature Cell Biology, Vol. 21, Issue 1 https://doi.org/10.1038/s41556-018-0195-z	journal	January 2019
Polarity Protein Complex Scribble/Lgl/Dlg And Epithelial Cell Barriers Su, Wen-Hui; Mruk, Dolores D.; Wong, Elissa W. P. Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-1-4614-4711-5_7	book	January 2013
Epithelial cell polarity, stem cells and cancer Martin-Belmonte, Fernando; Perez-Moreno, Mirna Nature Reviews Cancer, Vol. 12, Issue 1 https://doi.org/10.1038/nrc3169	journal	December 2011
Trafficking through COPII Stabilises Cell Polarity and Drives Secretion during Drosophila Epidermal Differentiation Norum, Michaela; Tång, Erika; Chavoshi, Tina PLoS ONE, Vol. 5, Issue 5 https://doi.org/10.1371/journal.pone.0010802	journal	May 2010
Evolution and Cell Physiology. 4. Why invent yet another protein complex to build junctions in epithelial cells? Bivic, André Le American Journal of Physiology-Cell Physiology, Vol. 305, Issue 12 https://doi.org/10.1152/ajpcell.00272.2013	journal	December 2013
Domain-specific functions of Stardust in Drosophila embryonic development Koch, Leonie; Feicht, Sabine; Sun, Rui Royal Society Open Science, Vol. 3, Issue 11 https://doi.org/10.1098/rsos.160776	journal	November 2016
Apical transport of Crumbs maintains epithelial cell polarity Aguilar-Aragon, M.; Fletcher, G.; Thompson, B. J. bioRxiv https://doi.org/10.1101/592311	posted_content	January 2019
Disruption of Rab8a and Rab11a causes formation of basolateral microvilli in neonatal enteropathy Feng, Qiang; Bonder, Edward M.; Engevik, Amy C. Journal of Cell Science https://doi.org/10.1242/jcs.201897	journal	January 2017
Atypical protein kinase C induces cell transformation by disrupting Hippo/Yap signaling Archibald, Andrew; Al-Masri, Maia; Liew-Spilger, Alyson Molecular Biology of the Cell, Vol. 26, Issue 20 https://doi.org/10.1091/mbc.e15-05-0265	journal	October 2015
Drosophila Models of Cell Polarity and Cell Competition in Tumourigenesis Fahey-Lozano, Natasha; La Marca, John E.; Portela, Marta Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-3-030-23629-8_3	book	January 2019
The cytoskeleton and cancer Hall, Alan Cancer and Metastasis Reviews, Vol. 28, Issue 1-2 https://doi.org/10.1007/s10555-008-9166-3	journal	January 2009
The Crumbs3 Polarity Protein Margolis, Ben Cold Spring Harbor Perspectives in Biology, Vol. 10, Issue 3 https://doi.org/10.1101/cshperspect.a027961	journal	March 2017
α-Tocopherol promotes HaCaT keratinocyte wound repair through the regulation of polarity proteins leading to the polarized cell migration: α-Tocopherol Promotes HaCaT Keratinocyte Wound Repair Horikoshi, Yosuke; Kamizaki, Kouki; Hanaki, Takehiko BioFactors, Vol. 44, Issue 2 https://doi.org/10.1002/biof.1414	journal	February 2018
PAR3–PAR6–atypical PKC polarity complex proteins in neuronal polarization Hapak, Sophie M.; Rothlin, Carla V.; Ghosh, Sourav Cellular and Molecular Life Sciences, Vol. 75, Issue 15 https://doi.org/10.1007/s00018-018-2828-6	journal	April 2018
Rho-kinase planar polarisation at tissue boundaries depends on phospho-regulation of membrane residence time Sidor, Clara; Stevens, Tim J.; Jin, Li https://doi.org/10.1101/615062	posted_content	January 2019
The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila Chen, C. -L.; Gajewski, K. M.; Hamaratoglu, F. Proceedings of the National Academy of Sciences, Vol. 107, Issue 36 https://doi.org/10.1073/pnas.1004060107	journal	August 2010
Formation of a Bazooka–Stardust complex is essential for plasma membrane polarity in epithelia Krahn, Michael P.; Bückers, Johanna; Kastrup, Lars Journal of Cell Biology, Vol. 190, Issue 5 https://doi.org/10.1083/jcb.201006029	journal	September 2010
A conserved polybasic domain mediates plasma membrane targeting of Lgl and its regulation by hypoxia Dong, Wei; Zhang, Xuejing; Liu, Weijie The Journal of Cell Biology, Vol. 211, Issue 2 https://doi.org/10.1083/jcb.201503067	journal	October 2015
Tissue Polarity-Dependent Control of Mammary Epithelial Homeostasis and Cancer Development: an Epigenetic Perspective Lelièvre, Sophie A. Journal of Mammary Gland Biology and Neoplasia, Vol. 15, Issue 1 https://doi.org/10.1007/s10911-010-9168-y	journal	January 2010
Neural stem cell temporal patterning and brain tumour growth rely on oxidative phosphorylation van den Ameele, Jelle; Brand, Andrea H. eLife, Vol. 8 https://doi.org/10.7554/elife.47887	journal	September 2019
A dual role of the extracellular domain of Drosophila Crumbs for morphogenesis of the embryonic neuroectoderm Das, Shradha; Knust, Elisabeth Biology Open, Vol. 7, Issue 1 https://doi.org/10.1242/bio.031435	journal	January 2018
Casein kinase 1 family proteins promote Slimb-dependent Expanded degradation Fulford, Alexander D.; Holder, Maxine V.; Frith, David eLife, Vol. 8 https://doi.org/10.7554/elife.46592	journal	September 2019
Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module Humbert, P. O.; Grzeschik, N. A.; Brumby, A. M. Oncogene, Vol. 27, Issue 55 https://doi.org/10.1038/onc.2008.341	journal	November 2008
Localization and Function of Pals1-associated Tight Junction Protein in Drosophila Is Regulated by Two Distinct Apical Complexes Sen, Arnab; Sun, Rui; Krahn, Michael P. Journal of Biological Chemistry, Vol. 290, Issue 21 https://doi.org/10.1074/jbc.m114.629014	journal	May 2015
Organogenesis and tumorigenesis: Insight from the JAK/STAT pathway in the Drosophila eye Wang, Ying-Hsuan; Huang, Min-Lang Developmental Dynamics, Vol. 239, Issue 10 https://doi.org/10.1002/dvdy.22394	journal	August 2010
Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis Harris, Kathryn P.; Tepass, Ulrich Journal of Cell Biology, Vol. 183, Issue 6 https://doi.org/10.1083/jcb.200807020	journal	December 2008
A bidirectional antagonism between aPKC and Yurt regulates epithelial cell polarity Gamblin, Clémence L.; Hardy, Émilie J. -L.; Chartier, François J. -M. Journal of Cell Biology, Vol. 204, Issue 4 https://doi.org/10.1083/jcb.201308032	journal	February 2014
Atf3 links loss of epithelial polarity to defects in cell differentiation and cytoarchitecture Donohoe, Colin D.; Csordás, Gábor; Correia, Andreia PLOS Genetics, Vol. 14, Issue 3 https://doi.org/10.1371/journal.pgen.1007241	journal	March 2018
Novel Neuroprotective Function of Apical-Basal Polarity Gene Crumbs in Amyloid Beta 42 (Aβ42) Mediated Neurodegeneration Steffensmeier, Andrew M.; Tare, Meghana; Puli, Oorvashi Roy PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0078717	journal	November 2013
Oligomerization of the FERM-FA protein Yurt controls epithelial cell polarity Gamblin, Clémence L.; Parent-Prévost, Frédérique; Jacquet, Kévin Journal of Cell Biology, Vol. 217, Issue 11 https://doi.org/10.1083/jcb.201803099	journal	August 2018
The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila Harris, Tony J. C.; Peifer, Mark Journal of Cell Biology, Vol. 170, Issue 5 https://doi.org/10.1083/jcb.200505127	journal	August 2005
Enteropathogenic Escherichia coli (EPEC) Recruitment of PAR Polarity Protein Atypical PKCζ to Pedestals and Cell–Cell Contacts Precedes Disruption of Tight Junctions in Intestinal Epithelial Cells Tapia, Rocio; Kralicek, Sarah E.; Hecht, Gail A. International Journal of Molecular Sciences, Vol. 21, Issue 2 https://doi.org/10.3390/ijms21020527	journal	January 2020
Yorkie and JNK revert syncytial muscles into myoblasts during Org-1 dependent lineage reprogramming Schaub, Christoph; Rose, Marcel; Frasch, Manfred https://doi.org/10.1101/607820	posted_content	January 2019
A polybasic domain in aPKC mediates Par6-dependent control of membrane targeting and kinase activity Dong, Wei; Lu, Juan; Zhang, Xuejing Journal of Cell Biology, Vol. 219, Issue 7 https://doi.org/10.1083/jcb.201903031	journal	June 2020
The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila J. C., Harris, Tony; Mark, Peifer, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/fvst-yg23	text	January 2005
Neural stem cell temporal patterning and brain tumour growth rely on oxidative phosphorylation. Van Den Ameele, Jelle; Brand, Andrea Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.44301	text	January 2019
Casein kinase 1 family proteins promote Slimb-dependent Expanded degradation. Fulford, Alexander D.; Holder, Maxine V.; Frith, David The Francis Crick Institute https://doi.org/10.25418/crick.11637006.v1	text	January 2020
Rho-Kinase Planar Polarization at Tissue Boundaries Depends on Phospho-regulation of Membrane Residence Time Sidor, Clara; Stevens, Tim J.; Jin, Li Developmental Cell, Vol. 52, Issue 3 https://doi.org/10.1016/j.devcel.2019.12.003	journal	February 2020
Atf3 links loss of epithelial polarity to defects in cell differentiation and cytoarchitecture Donohoe, Colin D.; Csordas, Gabor; Correia, Andreia PLOS Genetics https://doi.org/10.1101/212969	posted_content	February 2018
Drosophila models of cell polarity and cell competition in tumourigenesis Fahey-Lozano, Natalia; La-Marca, John; Portela-Esteban, Marta La Trobe https://doi.org/10.26181/19305878.v3	other	January 2022
Tight junction and polarity interaction in the transporting epithelial phenotype Cereijido, Marcelino; Contreras, Rubén G.; Shoshani, Liora Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1778, Issue 3 https://doi.org/10.1016/j.bbamem.2007.09.001	journal	March 2008
aPKC Phosphorylation of Bazooka Defines the Apical/Lateral Border in Drosophila Epithelial Cells Morais-de-Sá, Eurico; Mirouse, Vincent; St Johnston, Daniel Cell, Vol. 141, Issue 3 https://doi.org/10.1016/j.cell.2010.02.040	journal	April 2010
Coordinated Control of Cell Adhesion, Polarity, and Cytoskeleton Underlies Hox-Induced Organogenesis in Drosophila Lovegrove, Bridget; Simões, Sergio; Rivas, María Luisa Current Biology, Vol. 16, Issue 22 https://doi.org/10.1016/j.cub.2006.09.029	journal	November 2006
KIBRA Suppresses Apical Exocytosis through Inhibition of aPKC Kinase Activity in Epithelial Cells Yoshihama, Yohei; Sasaki, Kazunori; Horikoshi, Yosuke Current Biology, Vol. 21, Issue 8 https://doi.org/10.1016/j.cub.2011.03.029	journal	April 2011
Lgl Regulates Notch Signaling via Endocytosis, Independently of the Apical aPKC-Par6-Baz Polarity Complex Parsons, Linda M.; Portela, Marta; Grzeschik, Nicola A. Current Biology, Vol. 24, Issue 18 https://doi.org/10.1016/j.cub.2014.07.075	journal	September 2014
Fragile X Protein Functions with Lgl and the PAR Complex in Flies and Mice Zarnescu, Daniela C.; Jin, Peng; Betschinger, Joerg Developmental Cell, Vol. 8, Issue 1 https://doi.org/10.1016/j.devcel.2004.10.020	journal	January 2005
aPKC Controls Microtubule Organization to Balance Adherens Junction Symmetry and Planar Polarity during Development Harris, Tony J. C.; Peifer, Mark Developmental Cell, Vol. 12, Issue 5 https://doi.org/10.1016/j.devcel.2007.02.011	journal	May 2007
The Tumor Suppressors Brat and Numb Regulate Transit-Amplifying Neuroblast Lineages in Drosophila Bowman, Sarah K.; Rolland, Vivien; Betschinger, Joerg Developmental Cell, Vol. 14, Issue 4 https://doi.org/10.1016/j.devcel.2008.03.004	journal	April 2008
Anisotropy of Crumbs and aPKC Drives Myosin Cable Assembly during Tube Formation Röper, Katja Developmental Cell, Vol. 23, Issue 5 https://doi.org/10.1016/j.devcel.2012.09.013	journal	November 2012
Rho-Kinase Planar Polarization at Tissue Boundaries Depends on Phospho-regulation of Membrane Residence Time Sidor, Clara; Stevens, Tim J.; Jin, Li Developmental Cell, Vol. 52, Issue 3 https://doi.org/10.1016/j.devcel.2019.12.003	journal	February 2020
The cytoskeletal motor proteins Dynein and MyoV direct apical transport of Crumbs Aguilar-Aragon, M.; Fletcher, G.; Thompson, B. J. Developmental Biology, Vol. 459, Issue 2 https://doi.org/10.1016/j.ydbio.2019.12.009	journal	March 2020
Epithelial cell polarity: a major gatekeeper against cancer? Royer, C.; Lu, X. Cell Death & Differentiation, Vol. 18, Issue 9 https://doi.org/10.1038/cdd.2011.60	journal	May 2011
The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila Harris, Tony J. C.; Peifer, Mark Journal of Cell Biology, Vol. 170, Issue 5 https://doi.org/10.1083/jcb.200505127	journal	August 2005
p32 is a novel mammalian Lgl binding protein that enhances the activity of protein kinase Cζ and regulates cell polarity Bialucha, Carl U.; Ferber, Emma C.; Pichaud, Franck The Journal of Cell Biology, Vol. 178, Issue 4 https://doi.org/10.1083/jcb.200612022	journal	August 2007
Formation of a Bazooka–Stardust complex is essential for plasma membrane polarity in epithelia Krahn, Michael P.; Bückers, Johanna; Kastrup, Lars Journal of Cell Biology, Vol. 190, Issue 5 https://doi.org/10.1083/jcb.201006029	journal	September 2010
Atypical protein kinase C induces cell transformation by disrupting Hippo/Yap signaling Archibald, Andrew; Al-Masri, Maia; Liew-Spilger, Alyson Molecular Biology of the Cell, Vol. 26, Issue 20 https://doi.org/10.1091/mbc.e15-05-0265	journal	October 2015
A Polybasic Domain in aPKC Mediates Par-6-Dependent Control of Plasma Membrane Targeting and Kinase Activity Dong, Wei; Lu, Juan; Zhang, Xuejing https://doi.org/10.1101/588624	posted_content	January 2019
Apical transport of Crumbs maintains epithelial cell polarity Aguilar-Aragon, M.; Fletcher, G.; Thompson, B. J. bioRxiv https://doi.org/10.1101/592311	posted_content	January 2019
Tight Junctions: A Barrier to the Initiation and Progression of Breast Cancer? Brennan, Kieran; Offiah, Gozie; McSherry, Elaine A. Journal of Biomedicine and Biotechnology, Vol. 2010 https://doi.org/10.1155/2010/460607	journal	January 2010
Multiple domains in the Crumbs Homolog 2a (Crb2a) protein are required for regulating rod photoreceptor size Hsu, Ya-Chu; Jensen, Abbie M. BMC Cell Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2121-11-60	journal	July 2010
Loss of the Drosophila cell polarity regulator Scribbled promotes epithelial tissue overgrowth and cooperation with oncogenic Ras-Raf through impaired Hippo pathway signaling Doggett, Karen; Grusche, Felix A.; Richardson, Helena E. BMC Developmental Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-213x-11-57	journal	January 2011
Nuclear fallout provides a new link between aPKC and polarized cell trafficking Calero-Cuenca, Francisco J.; Espinosa-Vázquez, José Manuel; Reina-Campos, Miguel BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0253-6	journal	April 2016
The BTB-zinc Finger Transcription Factor Abrupt Acts as an Epithelial Oncogene in Drosophila melanogaster through Maintaining a Progenitor-like Cell State Turkel, Nezaket; Sahota, Virender K.; Bolden, Jessica E. PLoS Genetics, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pgen.1003627	journal	July 2013
Functional Interactions between the erupted/tsg101 Growth Suppressor Gene and the DaPKC and rbf1 Genes in Drosophila Imaginal Disc Tumors Gilbert, M. Melissa; Robinson, Brian S.; Moberg, Kenneth H. PLoS ONE, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pone.0007039	journal	September 2009
A Modifier Screen for Bazooka/PAR-3 Interacting Genes in the Drosophila Embryo Epithelium Shao, Wei; Wu, Johnny; Chen, Jeyla PLoS ONE, Vol. 5, Issue 4 https://doi.org/10.1371/journal.pone.0009938	journal	April 2010
Genetic Interaction of Centrosomin and Bazooka in Apical Domain Regulation in Drosophila Photoreceptor Chen, Geng; Rogers, Alicia K.; League, Garrett P. PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016127	journal	January 2011
Protein Kinase C-Dependent Signaling Controls the Midgut Epithelial Barrier to Malaria Parasite Infection in Anopheline Mosquitoes Pakpour, Nazzy; Camp, Lauren; Smithers, Hannah M. PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0076535	journal	October 2013
Intrinsic regulation of enteroendocrine fate by Numb Sallé, Jérémy; Gervais, Louis; Boumard, Benjamin The EMBO Journal, Vol. 36, Issue 13 https://doi.org/10.15252/embj.201695622	journal	May 2017
Neural stem cell temporal patterning and brain tumour growth rely on oxidative phosphorylation. Van Den Ameele, Jelle; Brand, Andrea Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.44301	text	January 2019
Casein kinase 1 family proteins promote Slimb-dependent Expanded degradation. Fulford, Alexander D.; Holder, Maxine V.; Frith, David The Francis Crick Institute https://doi.org/10.25418/crick.11637006	text	January 2020
The Scribble Cell Polarity Module in the Regulation of Cell Signaling in Tissue Development and Tumorigenesis Stephens, Rebecca; Lim, Krystle; Portela-Esteban, Marta La Trobe https://doi.org/10.26181/19305938.v1	text	January 2022
Polarization and Myelination in Myelinating Glia Masaki, Toshihiro ISRN Neurology, Vol. 2012 https://doi.org/10.5402/2012/769412	journal	December 2012
Drosophila: A Model System That Allows in vivo Manipulation and Study of Epithelial Cell Polarity Leibfried, Andrea; Bellaiche, Yohanns Current Frontiers and Perspectives in Cell Biology https://doi.org/10.5772/37120	book	April 2012
Epithelial Cell Polarity Determinant CRB3 in Cancer Development Li, Pingping; Mao, Xiaona; Ren, Yu International Journal of Biological Sciences, Vol. 11, Issue 1 https://doi.org/10.7150/ijbs.10615	journal	January 2015

Similar Records

Structures of the human Pals1 PDZ domain with and without ligand suggest gated access of Crb to the PDZ peptide-binding groove

Journal Article · 2015 · Acta Crystallographica. Section D: Biological Crystallography · OSTI ID:22347722

Ivanova, Marina E.; Fletcher, Georgina C.; O’Reilly, Nicola; +2 more

Dynein Regulates Epithelial Polarity and the Apical Localization of stardust A mRNA

Journal Article · 2008 · PLoS Genetics · OSTI ID:1627268

Horne-Badovinac, Sally; Bilder, David

Behavior of tight-junction, adherens-junction and cell polarity proteins during HNF-4{alpha}-induced epithelial polarization

Journal Article · 2005 · Experimental Cell Research · OSTI ID:20717666

Satohisa, Seiro; Chiba, Hideki; Osanai, Makoto; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
cell biology
DaPKC
Crumbs
Drosophila
epithelial cell polarity
signal transduction

Title: DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila

Citation Formats

References (67)

Cited By (87)

Similar Records

Related Subjects