Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis

Harris, Kathryn P.; Tepass, Ulrich

doi:10.1083/jcb.200807020

Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis

Journal Article · Mon Dec 08 00:00:00 EST 2008 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.200807020· OSTI ID:1625152

Harris, Kathryn P. ^[1]; Tepass, Ulrich ^[2]

Univ. of Toronto, ON (Canada). Dept. of Cell and Systems Biology; DOE/OSTI
Univ. of Toronto, ON (Canada). Dept. of Cell and Systems Biology

Cell rearrangements require dynamic changes in cell–cell contacts to maintain tissue integrity. We investigated the function of Cdc42 in maintaining adherens junctions (AJs) and apical polarity in the Drosophila melanogaster neuroectodermal epithelium. About one third of cells exit the epithelium through ingression and become neuroblasts. Cdc42-compromised embryos lost AJs in the neuroectoderm during neuroblast ingression. In contrast, when neuroblast formation was suppressed, AJs were maintained despite the loss of Cdc42 function. Loss of Cdc42 function caused an increase in the endocytotic uptake of apical proteins, including apical polarity factors such as Crumbs, which are required for AJ stability. In addition, Cdc42 has a second function in regulating endocytotic trafficking, as it is required for the progression of apical cargo from the early to the late endosome. The Par complex acts as an effector for Cdc42 in controlling the endocytosis of apical proteins. This study reveals functional interactions between apical polarity proteins and endocytosis that are critical for stabilizing dynamic basolateral AJs.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Toronto, ON (Canada)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

OSTI ID:: 1625152

Journal Information:: Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 6 Vol. 183; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (74)

Expression profile of the cadherin family in the developingDrosophila brain Fung, Siaumin; Wang, Fay; Chase, Maretta The Journal of Comparative Neurology, Vol. 506, Issue 3 https://doi.org/10.1002/cne.21539	journal	January 2007
Mechanisms of early neurogenesis inDrosophila melanogaster Campos-Ortega, Jos� A. Journal of Neurobiology, Vol. 24, Issue 10 https://doi.org/10.1002/neu.480241005	journal	October 1993
The Development of Cellular Junctions in the Drosophila Embryo Tepass, Ulrich; Hartenstein, Volker Developmental Biology, Vol. 161, Issue 2 https://doi.org/10.1006/dbio.1994.1054	journal	February 1994
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
Functional Analysis of Cdc42 in Actin Filament Assembly, Epithelial Morphogenesis, and Cell Signaling during Drosophila Development Genova, Jennifer L.; Jong, Sena; Camp, J. Terese Developmental Biology, Vol. 221, Issue 1 https://doi.org/10.1006/dbio.2000.9671	journal	May 2000
crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia Tepass, Ulrich; Theres, Carin; Knust, Elisabeth Cell, Vol. 61, Issue 5 https://doi.org/10.1016/0092-8674(90)90189-L	journal	June 1990
Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor Rebay, Ilaria; Fehon, Richard G.; Artavanis-Tsakonas, Spyros Cell, Vol. 74, Issue 2 https://doi.org/10.1016/0092-8674(93)90423-N	journal	July 1993
Intrinsic activity of the lin-12 and Notch intracellular domains in vivo Struhl, Gary; Fitzgerald, Kevin; Greenwald, Iva Cell, Vol. 74, Issue 2 https://doi.org/10.1016/0092-8674(93)90424-O	journal	July 1993
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
Developmental Control of Endocytosis in Dendritic Cells by Cdc42 Garrett, Wendy S.; Chen, Li-Mei; Kroschewski, Ruth Cell, Vol. 102, Issue 3 https://doi.org/10.1016/S0092-8674(00)00038-6	journal	August 2000
Gradient Formation of the TGF-β Homolog Dpp Entchev, Eugeni V.; Schwabedissen, Anja; González-Gaitán, Marcos Cell, Vol. 103, Issue 6 https://doi.org/10.1016/S0092-8674(00)00200-2	journal	December 2000
Hrs Regulates Endosome Membrane Invagination and Tyrosine Kinase Receptor Signaling in Drosophila Lloyd, Thomas E.; Atkinson, Richard; Wu, Mark N. Cell, Vol. 108, Issue 2 https://doi.org/10.1016/S0092-8674(02)00611-6	journal	January 2002
Activated Cdc42 Sequesters c-Cbl and Prevents EGF Receptor Degradation Wu, Wen Jin; Tu, Shine; Cerione, Richard A. Cell, Vol. 114, Issue 6 https://doi.org/10.1016/S0092-8674(03)00688-3	journal	September 2003
Essential Roles of Drosophila RhoA in the Regulation of Neuroblast Proliferation and Dendritic but Not Axonal Morphogenesis Lee, Tzumin; Winter, Christopher; Marticke, Simone S. Neuron, Vol. 25, Issue 2 https://doi.org/10.1016/S0896-6273(00)80896-X	journal	February 2000
GPI-Anchored Proteins Are Delivered to Recycling Endosomes via a Distinct cdc42-Regulated, Clathrin-Independent Pinocytic Pathway Sabharanjak, Shefali; Sharma, Pranav; Parton, Robert G. Developmental Cell, Vol. 2, Issue 4 https://doi.org/10.1016/S1534-5807(02)00145-4	journal	April 2002
The challenges of abundance: epithelial junctions and small GTPase signalling Braga, Vania MM; Yap, Alpha S. Current Opinion in Cell Biology, Vol. 17, Issue 5 https://doi.org/10.1016/j.ceb.2005.08.012	journal	October 2005
ESCRT complexes and the biogenesis of multivesicular bodies Hurley, James H. Current Opinion in Cell Biology, Vol. 20, Issue 1 https://doi.org/10.1016/j.ceb.2007.12.002	journal	February 2008
A Rich1/Amot Complex Regulates the Cdc42 GTPase and Apical-Polarity Proteins in Epithelial Cells Wells, Clark D.; Fawcett, James P.; Traweger, Andreas Cell, Vol. 125, Issue 3 https://doi.org/10.1016/j.cell.2006.02.045	journal	May 2006
Closing the GAP between Polarity and Vesicle Transport Macara, Ian G.; Spang, Anne Cell, Vol. 125, Issue 3 https://doi.org/10.1016/j.cell.2006.04.011	journal	May 2006
RETRACTED: The Big Brain Aquaporin Is Required for Endosome Maturation and Notch Receptor Trafficking Kanwar, Ritu; Fortini, Mark E. Cell, Vol. 133, Issue 5 https://doi.org/10.1016/j.cell.2008.04.038	journal	May 2008
Trafficking through Rab11 Endosomes Is Required for Cellularization during Drosophila Embryogenesis Pelissier, Anne; Chauvin, Jean-Paul; Lecuit, Thomas Current Biology, Vol. 13, Issue 21 https://doi.org/10.1016/j.cub.2003.10.023	journal	October 2003
Par Proteins: Partners in Polarization Macara, Ian G. Current Biology, Vol. 14, Issue 4 https://doi.org/10.1016/j.cub.2004.01.048	journal	February 2004
Sequential Roles of Cdc42, Par-6, aPKC, and Lgl in the Establishment of Epithelial Polarity during Drosophila Embryogenesis Hutterer, Andrea; Betschinger, Joerg; Petronczki, Mark Developmental Cell, Vol. 6, Issue 6 https://doi.org/10.1016/j.devcel.2004.05.003	journal	June 2004
The PAR Proteins: Fundamental Players in Animal Cell Polarization Goldstein, Bob; Macara, Ian G. Developmental Cell, Vol. 13, Issue 5 https://doi.org/10.1016/j.devcel.2007.10.007	journal	November 2007
Cdc42: new roads to travel Cerione, R. Trends in Cell Biology, Vol. 14, Issue 3 https://doi.org/10.1016/j.tcb.2004.01.008	journal	March 2004
The ins and outs of E-cadherin trafficking Bryant, David M.; Stow, Jennifer L. Trends in Cell Biology, Vol. 14, Issue 8 https://doi.org/10.1016/j.tcb.2004.07.007	journal	August 2004
Disassembling adherens junctions: breaking up is hard to do D'Souza-Schorey, Crislyn Trends in Cell Biology, Vol. 15, Issue 1 https://doi.org/10.1016/j.tcb.2004.11.002	journal	January 2005
Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking Ridley, Anne J. Trends in Cell Biology, Vol. 16, Issue 10 https://doi.org/10.1016/j.tcb.2006.08.006	journal	October 2006
Selective Control of Basolateral Membrane Protein Polarity by Cdc42: Basolateral Membrane Polarity by Cdc42 Cohen, David; Müsch, Anne; Rodriguez-Boulan, Enrique Traffic, Vol. 2, Issue 8 https://doi.org/10.1034/j.1600-0854.2001.20805.x	journal	August 2001
Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases Feig, Larry A. Nature Cell Biology, Vol. 1, Issue 2 https://doi.org/10.1038/10018	journal	June 1999
Drosophila oocyte localization is mediated by differential cadherin-based adhesion Godt, Dorothea; Tepass, Ulrich Nature, Vol. 395, Issue 6700 https://doi.org/10.1038/26493	journal	September 1998
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
Rho-family GTPases in cadherin-mediated cell — cell adhesion Fukata, Masaki; Kaibuchi, Kozo Nature Reviews Molecular Cell Biology, Vol. 2, Issue 12 https://doi.org/10.1038/35103068	journal	December 2001
The role of RhoA in tissue polarity and Frizzled signalling Strutt, David I.; Weber, Ursula; Mlodzik, Marek Nature, Vol. 387, Issue 6630 https://doi.org/10.1038/387292a0	journal	May 1997
Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells Kroschewski, Ruth; Hall, Alan; Mellman, Ira Nature Cell Biology, Vol. 1, Issue 1 https://doi.org/10.1038/8977	journal	May 1999
Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis Pellikka, Milena; Tanentzapf, Guy; Pinto, Madalena Nature, Vol. 416, Issue 6877 https://doi.org/10.1038/nature721	journal	February 2002
Endocytic control of epithelial polarity and proliferation in Drosophila Lu, Han; Bilder, David Nature Cell Biology, Vol. 7, Issue 12 https://doi.org/10.1038/ncb1324	journal	October 2005
Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic Balklava, Zita; Pant, Saumya; Fares, Hanna Nature Cell Biology, Vol. 9, Issue 9 https://doi.org/10.1038/ncb1627	journal	August 2007
The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface Cappello, Silvia; Attardo, Alessio; Wu, Xunwei Nature Neuroscience, Vol. 9, Issue 9 https://doi.org/10.1038/nn1744	journal	August 2006
Regulation of cadherin-mediated adhesion in morphogenesis Gumbiner, Barry M. Nature Reviews Molecular Cell Biology, Vol. 6, Issue 8 https://doi.org/10.1038/nrm1699	journal	July 2005
Pathways of clathrin-independent endocytosis Mayor, Satyajit; Pagano, Richard E. Nature Reviews Molecular Cell Biology, Vol. 8, Issue 8 https://doi.org/10.1038/nrm2216	journal	August 2007
Cbl escapes Cdc42-mediated inhibition by downregulation of the adaptor molecule βPix Schmidt, M. H. H.; Husnjak, K.; Szymkiewicz, I. Oncogene, Vol. 25, Issue 21 https://doi.org/10.1038/sj.onc.1209329	journal	January 2006
Rab5a is a common component of the apical and basolateral endocytic machinery in polarized epithelial cells. Bucci, C.; Wandinger-Ness, A.; Lutcke, A. Proceedings of the National Academy of Sciences, Vol. 91, Issue 11 https://doi.org/10.1073/pnas.91.11.5061	journal	May 1994
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
Regulation of Cadherin Adhesive Activity Gumbiner, Barry M. Journal of Cell Biology, Vol. 148, Issue 3 https://doi.org/10.1083/jcb.148.3.399	journal	February 2000
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
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
Lava Lamp, a Novel Peripheral Golgi Protein, Is Required for Drosophila melanogaster Cellularization Sisson, John C.; Field, Christine; Ventura, Richard Journal of Cell Biology, Vol. 151, Issue 4 https://doi.org/10.1083/jcb.151.4.905	journal	November 2000
Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release Wucherpfennig, Tanja; Wilsch-Bräuninger, Michaela; González-Gaitán, Marcos Journal of Cell Biology, Vol. 161, Issue 3 https://doi.org/10.1083/jcb.200211087	journal	May 2003
Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1 Foletta, Victoria C.; Lim, Mei Ann; Soosairajah, Juliana Journal of Cell Biology, Vol. 162, Issue 6 https://doi.org/10.1083/jcb.200212060	journal	September 2003
DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila Sotillos, Sol; Díaz-Meco, María Teresa; Caminero, Eva The Journal of Cell Biology, Vol. 166, Issue 4 https://doi.org/10.1083/jcb.200311031	journal	August 2004
Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells Otani, Tetsuhisa; Ichii, Tetsuo; Aono, Shinya Journal of Cell Biology, Vol. 175, Issue 1 https://doi.org/10.1083/jcb.200605012	journal	October 2006
Rab11 in Recycling Endosomes Regulates the Sorting and Basolateral Transport of E-Cadherin Lock, John G.; Stow, Jennifer L. Molecular Biology of the Cell, Vol. 16, Issue 4 https://doi.org/10.1091/mbc.e04-10-0867	journal	April 2005
cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network Musch, A. The EMBO Journal, Vol. 20, Issue 9 https://doi.org/10.1093/emboj/20.9.2171	journal	May 2001
Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Uemura, T.; Oda, H.; Kraut, R. Genes & Development, Vol. 10, Issue 6 https://doi.org/10.1101/gad.10.6.659	journal	March 1996
shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Tepass, U.; Gruszynski-DeFeo, E.; Haag, T. A. Genes & Development, Vol. 10, Issue 6 https://doi.org/10.1101/gad.10.6.672	journal	March 1996
Cadherins in development: cell adhesion, sorting, and tissue morphogenesis Halbleib, J. M.; Nelson, W. J. Genes & Development, Vol. 20, Issue 23 https://doi.org/10.1101/gad.1486806	journal	December 2006
Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Lieber, T.; Kidd, S.; Alcamo, E. Genes & Development, Vol. 7, Issue 10 https://doi.org/10.1101/gad.7.10.1949	journal	October 1993
Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Luo, L.; Liao, Y. J.; Jan, L. Y. Genes & Development, Vol. 8, Issue 15 https://doi.org/10.1101/gad.8.15.1787	journal	August 1994
Role of Rho family GTPases in epithelial morphogenesis Van Aelst, L. Genes & Development, Vol. 16, Issue 9 https://doi.org/10.1101/gad.978802	journal	May 2002
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
Notch Signaling: Cell Fate Control and Signal Integration in Development Artavanis-Tsakonas, S. Science, Vol. 284, Issue 5415 https://doi.org/10.1126/science.284.5415.770	journal	April 1999
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
Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors Satoh, Akiko K.; O'Tousa, Joseph E.; Ozaki, Koichi Development, Vol. 132, Issue 7 https://doi.org/10.1242/dev.01704	journal	April 2005
Rho1 regulates Drosophila adherens junctions independently of p120ctn Fox, Donald T.; Homem, Catarina C. F.; Myster, Steven H. Development, Vol. 132, Issue 21 https://doi.org/10.1242/dev.02056	journal	November 2005
Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila Laplante, Caroline; Nilson, Laura A. Development, Vol. 133, Issue 16 https://doi.org/10.1242/dev.02492	journal	August 2006
Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis Bloor, James W.; Kiehart, Daniel P. Development, Vol. 129, Issue 13 https://doi.org/10.1242/dev.129.13.3173	journal	July 2002
Rab11 polarization of theDrosophilaoocyte: a novel link between membrane trafficking, microtubule organization, andoskarmRNA localization and translation Dollar, Gretchen; Struckhoff, Eric; Michaud, Jason Development, Vol. 129, Issue 2 https://doi.org/10.1242/dev.129.2.517	journal	January 2002
The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity Blankenship, J. Todd; Fuller, Margaret T.; Zallen, Jennifer A. Journal of Cell Science, Vol. 120, Issue 17 https://doi.org/10.1242/jcs.004770	journal	September 2007
Cdc42 acts downstream of Bazooka to regulate neuroblast polarity through Par-6–aPKC Atwood, Scott X.; Chabu, Chiswili; Penkert, Rhiannon R. Journal of Cell Science, Vol. 120, Issue 18 https://doi.org/10.1242/jcs.014902	journal	September 2007
Thirty-One Flavors of Drosophila Rab Proteins Zhang, Jun; Schulze, Karen L.; Hiesinger, P. Robin Genetics, Vol. 176, Issue 2 https://doi.org/10.1534/genetics.106.066761	journal	June 2007
Construction of Transgenic Drosophila by Using the Site-Specific Integrase From Phage C31 Groth, A. C. Genetics, Vol. 166, Issue 4 https://doi.org/10.1534/genetics.166.4.1775	journal	April 2004
The PAR Proteins: Fundamental Players in Animal Cell Polarization G., Macara, Ian; Bob, Goldstein, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/0q66-0q34	text	January 2007
Rho1 regulates Drosophila adherens junctions independently of p120ctn Mark, Peifer,; H., Myster, Steven; Eugene, Bain, E. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/vbmg-qz32	text	January 2005

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Rac1 controls epithelial tube length through the apical secretion and polarity pathways Sollier, Kévin; Gaudé, Helori-Mael; Chartier, François J. -M. Biology Open, Vol. 5, Issue 1 https://doi.org/10.1242/bio.015727	journal	December 2015
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
The Scribble module regulates retromer-dependent endocytic trafficking during epithelial polarization de Vreede, Geert; Schoenfeld, Joshua D.; Windler, Sarah L. Development, Vol. 141, Issue 14 https://doi.org/10.1242/dev.105403	journal	July 2014
The PAR proteins: from molecular circuits to dynamic self-stabilizing cell polarity Lang, Charles F.; Munro, Edwin Development, Vol. 144, Issue 19 https://doi.org/10.1242/dev.139063	journal	October 2017
Cdc42 defines apical identity and regulates epithelial morphogenesis by promoting apical recruitment of Par6-aPKC and Crumbs Nunes de Almeida, Francisca; Walther, Rhian F.; Pressé, Mary T. Development, Vol. 146, Issue 15 https://doi.org/10.1242/dev.175497	journal	August 2019
Regulation of Cdc42 and its effectors in epithelial morphogenesis Pichaud, Franck; Walther, Rhian F.; Nunes de Almeida, Francisca Journal of Cell Science, Vol. 132, Issue 10 https://doi.org/10.1242/jcs.217869	journal	May 2019
Cytocortex-dependent dynamics of Drosophila Crumbs controls junctional stability and tension during germ band retraction Bajur, Anna T.; Iyer, K. Venkatesan; Knust, Elisabeth Journal of Cell Science https://doi.org/10.1242/jcs.228338	journal	January 2019
ROP GTPase-Dependent Actin Microfilaments Promote PIN1 Polarization by Localized Inhibition of Clathrin-Dependent Endocytosis Nagawa, Shingo; Xu, Tongda; Lin, Deshu PLoS Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pbio.1001299	journal	April 2012
Morphological and functional aspects of progenitors perturbed in cortical malformations Bizzotto, Sara; Francis, Fiona Frontiers in Cellular Neuroscience, Vol. 9 https://doi.org/10.3389/fncel.2015.00030	journal	February 2015
Polarization and Myelination in Myelinating Glia Masaki, Toshihiro ISRN Neurology, Vol. 2012 https://doi.org/10.5402/2012/769412	journal	December 2012

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