XB-ART-50716
Semin Cell Dev Biol
2015 Jun 01;42:78-85. doi: 10.1016/j.semcdb.2015.05.002.
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Spatial and temporal aspects of Wnt signaling and planar cell polarity during vertebrate embryonic development.
Sokol SY
.
Abstract
Wnt signaling pathways act at multiple locations and developmental stages to specify cell fate and polarity in vertebrate embryos. A long-standing question is how the same molecular machinery can be reused to produce different outcomes. The canonical Wnt/β-catenin branch modulates target gene transcription to specify cell fates along the dorsoventral and anteroposterior embryonic axes. By contrast, the Wnt/planar cell polarity (PCP) branch is responsible for cell polarization along main body axes, which coordinates morphogenetic cell behaviors during gastrulation and neurulation. Whereas both cell fate and cell polarity are modulated by spatially- and temporally-restricted Wnt activity, the downstream signaling mechanisms are very diverse. This review highlights recent progress in the understanding of Wnt-dependent molecular events leading to the establishment of PCP and linking it to early morphogenetic processes.
PubMed ID: 25986055
PMC ID: PMC4562884
Article link: Semin Cell Dev Biol
Grant support: [+]
R01 GM096959 NIGMS NIH HHS , R21 HD078874 NICHD NIH HHS , R56 NS040972 NINDS NIH HHS , R01 NS040972 NINDS NIH HHS
Species referenced: Xenopus
Genes referenced: ankrd6 axin1 ctnnb1 daam1 dvl1 fuz fzd1 gsk3b intu lrp5 lrp6 prickle1 rab11a rhoa rock1 ror2 tcf7 tcf7l1 tjp1 vangl2 wnt1
Article Images: [+] show captions
Fig. 1. Two major Wnt pathway branches.The canonical Wnt/-catenin pathway antagonizes the -catenin destruction complex, consisting of Axin, GSK3 and APC to promote target gene transcription. By contrast,the Wnt/PCP pathway is thought to involve Frizzled/Dishevelled signaling to locally activate RhoA, ROCK and Myosin II and, at the same time, precludes the recruitment ofVangl2/Prickle to the same membrane subdomain. Roles of the vertebrate PCP proteins Fuzzy, Inturned and Diversin in PCP are unclear. Besides the mutually antagonisticinteractions inside the cell, PCP is coordinated by the positive feedback between the Frizzled/Dishevelled complex and the Vangl2/Prickle complex across the cell junction.Two neighboring epithelial cells are shown. | |
Fig. 2. Anteroposterior and mediolateral PCP in the Xenopus neural plate.En face views of the Xenopus neural plate shown for stage 14–16 embryos. Left, immunostaining for Vangl2 and ZO1 reveals anterior accumulation of Vangl2 in neural midline cells (arrows). Inset shows whole embryo view with indicated anteroposterior (A-P) and mediolateral (M-L) axes. Right, the middle area of the neural plate exhibits mediolateral planar polarity of the cells mosaically expressing GFP-Rab11 (green) and RFP-Diversin (red puncta) that are enriched at medial domains of cells in the lateral neural plate. Arrows mark cell polarization towards the midline (dotted line). | |
Fig. 3. Regulation of morphogenetic behaviors by Wnt/PCP signaling. The Wnt/PCP pathway modulates actomyosin dynamics and vesicular trafficking to control mediolateral and radial cell intercalations, apical constriction, collective and individual cell migration and oriented cell division. Together, these cell behaviors ensure proper vertebrate neural tube closure. |
References [+] :
Acebron,
Mitotic wnt signaling promotes protein stabilization and regulates cell size.
2014, Pubmed
Acebron, Mitotic wnt signaling promotes protein stabilization and regulates cell size. 2014, Pubmed
Adler, The frizzled/stan pathway and planar cell polarity in the Drosophila wing. 2012, Pubmed
Aigouy, Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. 2010, Pubmed
Andre, The Wnt coreceptor Ryk regulates Wnt/planar cell polarity by modulating the degradation of the core planar cell polarity component Vangl2. 2012, Pubmed
Andre, Wnt5a and Wnt11 regulate mammalian anterior-posterior axis elongation. 2015, Pubmed
Antic, Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. 2010, Pubmed , Xenbase
Azzolin, YAP/TAZ incorporation in the β-catenin destruction complex orchestrates the Wnt response. 2014, Pubmed
Bastock, Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. 2003, Pubmed
Borovina, Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. 2010, Pubmed
Buckley, Mirror-symmetric microtubule assembly and cell interactions drive lumen formation in the zebrafish neural rod. 2013, Pubmed
Burnside, Analysis of morphogenetic movements in the neural plate of the newt Taricha torosa. 1968, Pubmed
Carreira-Barbosa, Flamingo regulates epiboly and convergence/extension movements through cell cohesive and signalling functions during zebrafish gastrulation. 2009, Pubmed
Carvallo, Non-canonical Wnt signaling induces ubiquitination and degradation of Syndecan4. 2010, Pubmed , Xenbase
Cervantes, Wnt5a is essential for intestinal elongation in mice. 2009, Pubmed
Cha, The roles of maternal Vangl2 and aPKC in Xenopus oocyte and embryo patterning. 2011, Pubmed , Xenbase
Chae, The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. 1999, Pubmed
Chen, Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. 2008, Pubmed
Cirone, A role for planar cell polarity signaling in angiogenesis. 2008, Pubmed
Ciruna, Planar cell polarity signalling couples cell division and morphogenesis during neurulation. 2006, Pubmed
Classen, Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. 2005, Pubmed
Clevers, Wnt/β-catenin signaling and disease. 2012, Pubmed
Collier, Drosophila tissue polarity requires the cell-autonomous activity of the fuzzy gene, which encodes a novel transmembrane protein. 1997, Pubmed
Deblandre, A two-step mechanism generates the spacing pattern of the ciliated cells in the skin of Xenopus embryos. 1999, Pubmed , Xenbase
Devenport, Mitotic internalization of planar cell polarity proteins preserves tissue polarity. 2011, Pubmed
Devenport, The cell biology of planar cell polarity. 2014, Pubmed
Devenport, Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. 2008, Pubmed
Donoughe, dachsous and frizzled contribute separately to planar polarity in the Drosophila ventral epidermis. 2011, Pubmed
Drysdale, Cell Migration and Induction in the Development of the Surface Ectodermal Pattern of the Xenopus laevis Tadpole: (Xenopus/ciliated cell/hatching gland/cement gland/ectodermal differentiation). 1992, Pubmed , Xenbase
Elul, Monopolar protrusive activity: a new morphogenic cell behavior in the neural plate dependent on vertical interactions with the mesoderm in Xenopus. 2000, Pubmed , Xenbase
Feiguin, The ankyrin repeat protein Diego mediates Frizzled-dependent planar polarization. 2001, Pubmed
Funayama, Embryonic axis induction by the armadillo repeat domain of beta-catenin: evidence for intracellular signaling. 1995, Pubmed , Xenbase
Gao, Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. 2011, Pubmed
Gerhart, Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. 1989, Pubmed , Xenbase
Glasco, The mouse Wnt/PCP protein Vangl2 is necessary for migration of facial branchiomotor neurons, and functions independently of Dishevelled. 2012, Pubmed
Goldstein, Wnt signals can function as positional cues in establishing cell polarity. 2006, Pubmed
Gong, Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. 2004, Pubmed
González-Sancho, Functional consequences of Wnt-induced dishevelled 2 phosphorylation in canonical and noncanonical Wnt signaling. 2013, Pubmed
Goodrich, Principles of planar polarity in animal development. 2011, Pubmed
Gray, Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. 2011, Pubmed
Gray, The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. 2009, Pubmed , Xenbase
Grumolato, Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. 2010, Pubmed
Gubb, A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. 1982, Pubmed
Gubb, The balance between isoforms of the prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs. 1999, Pubmed
Guo, A novel GTP-binding protein-adaptor protein complex responsible for export of Vangl2 from the trans Golgi network. 2013, Pubmed
Habas, Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. 2001, Pubmed , Xenbase
Habib, A localized Wnt signal orients asymmetric stem cell division in vitro. 2013, Pubmed
Harland, Formation and function of Spemann's organizer. 1997, Pubmed
Hashimoto, Planar polarization of node cells determines the rotational axis of node cilia. 2010, Pubmed
Heasman, Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. 1994, Pubmed , Xenbase
Heisenberg, Forces in tissue morphogenesis and patterning. 2013, Pubmed
Heisenberg, Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. 2000, Pubmed
Hikasa, The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. 2002, Pubmed , Xenbase
Hikasa, Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. 2010, Pubmed , Xenbase
Hikasa, Wnt signaling in vertebrate axis specification. 2013, Pubmed , Xenbase
Iioka, Wnt signalling regulates paxillin ubiquitination essential for mesodermal cell motility. 2007, Pubmed , Xenbase
Itoh, GEF-H1 functions in apical constriction and cell intercalations and is essential for vertebrate neural tube closure. 2014, Pubmed , Xenbase
Itoh, Specific modulation of ectodermal cell fates in Xenopus embryos by glycogen synthase kinase. 1995, Pubmed , Xenbase
Itoh, Graded amounts of Xenopus dishevelled specify discrete anteroposterior cell fates in prospective ectoderm. 1997, Pubmed , Xenbase
Jenny, Prickle and Strabismus form a functional complex to generate a correct axis during planar cell polarity signaling. 2003, Pubmed , Xenbase
Jenny, Diego and Prickle regulate Frizzled planar cell polarity signalling by competing for Dishevelled binding. 2005, Pubmed
Jessen, Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. 2002, Pubmed
Jiang, Ascidian prickle regulates both mediolateral and anterior-posterior cell polarity of notochord cells. 2005, Pubmed
Keller, Shaping the vertebrate body plan by polarized embryonic cell movements. 2002, Pubmed
Keller, The cellular basis of epiboly: an SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis. 1980, Pubmed , Xenbase
Kiecker, A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. 2001, Pubmed , Xenbase
Lake, Strabismus regulates asymmetric cell divisions and cell fate determination in the mouse brain. 2009, Pubmed
Larabell, Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in beta-catenin that are modulated by the Wnt signaling pathway. 1997, Pubmed , Xenbase
Lawrence, Planar cell polarity: one or two pathways? 2007, Pubmed
Lee, Endocytosis is required for efficient apical constriction during Xenopus gastrulation. 2010, Pubmed , Xenbase
Li, Sfrp5 coordinates foregut specification and morphogenesis by antagonizing both canonical and noncanonical Wnt11 signaling. 2008, Pubmed , Xenbase
Li, Gpr125 modulates Dishevelled distribution and planar cell polarity signaling. 2013, Pubmed
Lin, Wnt5b-Ryk pathway provides directional signals to regulate gastrulation movement. 2010, Pubmed
Liu, Null and hypomorph Prickle1 alleles in mice phenocopy human Robinow syndrome and disrupt signaling downstream of Wnt5a. 2014, Pubmed
Lu, The Drosophila planar polarity proteins inturned and multiple wing hairs interact physically and function together. 2010, Pubmed
Löfberg, Apical surface topography of invaginating and noninvaginating cells. A scanning-transmission study of amphibian neurulae. 1974, Pubmed
Ma, Fidelity in planar cell polarity signalling. 2003, Pubmed
MacDonald, Wnt/beta-catenin signaling: components, mechanisms, and diseases. 2009, Pubmed , Xenbase
Macheda, The Wnt receptor Ryk plays a role in mammalian planar cell polarity signaling. 2012, Pubmed
Mahaffey, Cofilin and Vangl2 cooperate in the initiation of planar cell polarity in the mouse embryo. 2013, Pubmed
Martin, Apical constriction: themes and variations on a cellular mechanism driving morphogenesis. 2014, Pubmed
Matakatsu, Separating planar cell polarity and Hippo pathway activities of the protocadherins Fat and Dachsous. 2012, Pubmed
Matis, Microtubules provide directional information for core PCP function. 2014, Pubmed
Matis, Regulation of PCP by the Fat signaling pathway. 2013, Pubmed
McGreevy, Shroom3 functions downstream of planar cell polarity to regulate myosin II distribution and cellular organization during neural tube closure. 2015, Pubmed
Mikels, Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. 2006, Pubmed
Miller, Pronephric tubulogenesis requires Daam1-mediated planar cell polarity signaling. 2011, Pubmed , Xenbase
Miller, Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation. 1999, Pubmed , Xenbase
Mirkovic, Rearrangements between differentiating hair cells coordinate planar polarity and the establishment of mirror symmetry in lateral-line neuromasts. 2012, Pubmed
Mitchell, The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. 2009, Pubmed , Xenbase
Mitchell, A positive feedback mechanism governs the polarity and motion of motile cilia. 2007, Pubmed , Xenbase
Montcouquiol, Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. 2003, Pubmed
Mottola, A novel function for the Rab5 effector Rabenosyn-5 in planar cell polarity. 2010, Pubmed
Narimatsu, Regulation of planar cell polarity by Smurf ubiquitin ligases. 2009, Pubmed
Newman-Smith, Reciprocal and dynamic polarization of planar cell polarity core components and myosin. 2015, Pubmed
Niehrs, The complex world of WNT receptor signalling. 2012, Pubmed
Nishimura, Planar cell polarity links axes of spatial dynamics in neural-tube closure. 2012, Pubmed
Nishita, Filopodia formation mediated by receptor tyrosine kinase Ror2 is required for Wnt5a-induced cell migration. 2006, Pubmed
Olofsson, Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity. 2014, Pubmed
Ooi, Genome-wide RNAi screen identifies novel host proteins required for alphavirus entry. 2013, Pubmed
Ossipova, Role of Rab11 in planar cell polarity and apical constriction during vertebrate neural tube closure. 2014, Pubmed , Xenbase
Ossipova, Planar polarization of Vangl2 in the vertebrate neural plate is controlled by Wnt and Myosin II signaling. 2015, Pubmed , Xenbase
Ossipova, Vangl2 cooperates with Rab11 and Myosin V to regulate apical constriction during vertebrate gastrulation. 2015, Pubmed , Xenbase
Ossipova, The involvement of PCP proteins in radial cell intercalations during Xenopus embryonic development. 2015, Pubmed , Xenbase
Park, The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. 1996, Pubmed
Park, Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. 2006, Pubmed , Xenbase
Petersen, Wnt signaling and the polarity of the primary body axis. 2009, Pubmed
Qian, Wnt5a functions in planar cell polarity regulation in mice. 2007, Pubmed , Xenbase
Sawa, Control of cell polarity and asymmetric division in C. elegans. 2012, Pubmed
Sawyer, Apical constriction: a cell shape change that can drive morphogenesis. 2010, Pubmed , Xenbase
Schlesinger, Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. 1999, Pubmed
Schneider, beta-Catenin asymmetries after all animal/vegetal- oriented cell divisions in Platynereis dumerilii embryos mediate binary cell-fate specification. 2007, Pubmed
Schneider, Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. 1996, Pubmed , Xenbase
Schroeder, Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy. 1970, Pubmed , Xenbase
Semenov, SnapShot: Noncanonical Wnt Signaling Pathways. 2007, Pubmed
Sepich, Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements. 2011, Pubmed
Shafer, Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. 2011, Pubmed
Shimada, Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. 2006, Pubmed
Shindo, PCP and septins compartmentalize cortical actomyosin to direct collective cell movement. 2014, Pubmed , Xenbase
Simons, Planar cell polarity signaling: from fly development to human disease. 2008, Pubmed
Smith, Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. 1991, Pubmed , Xenbase
Sokol, Wnt signaling and dorso-ventral axis specification in vertebrates. 1999, Pubmed
Sokol, Injected Wnt RNA induces a complete body axis in Xenopus embryos. 1991, Pubmed , Xenbase
Sokol, Analysis of Dishevelled signalling pathways during Xenopus development. 1996, Pubmed , Xenbase
Sokol, Dorsalizing and neuralizing properties of Xdsh, a maternally expressed Xenopus homolog of dishevelled. 1995, Pubmed , Xenbase
Song, Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. 2010, Pubmed
Strutt, Planar polarity genes in the Drosophila wing regulate the localisation of the FH3-domain protein Multiple Wing Hairs to control the site of hair production. 2008, Pubmed
Strutt, Dynamics of core planar polarity protein turnover and stable assembly into discrete membrane subdomains. 2011, Pubmed
Strutt, A Cul-3-BTB ubiquitylation pathway regulates junctional levels and asymmetry of core planar polarity proteins. 2013, Pubmed
Sugioka, Wnt regulates spindle asymmetry to generate asymmetric nuclear β-catenin in C. elegans. 2011, Pubmed
Ségalen, The Fz-Dsh planar cell polarity pathway induces oriented cell division via Mud/NuMA in Drosophila and zebrafish. 2010, Pubmed
Tao, Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos. 2005, Pubmed , Xenbase
Taylor, Van Gogh: a new Drosophila tissue polarity gene. 1998, Pubmed
Tissir, Shaping the nervous system: role of the core planar cell polarity genes. 2013, Pubmed
Tree, Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. 2002, Pubmed
Usui, Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. 1999, Pubmed
Walck-Shannon, Cell intercalation from top to bottom. 2014, Pubmed
Wallingford, Convergent extension: the molecular control of polarized cell movement during embryonic development. 2002, Pubmed , Xenbase
Wallingford, Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. 2011, Pubmed , Xenbase
Walston, Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. 2004, Pubmed
Wang, Tissue/planar cell polarity in vertebrates: new insights and new questions. 2007, Pubmed
Winter, Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. 2001, Pubmed
Witze, Wnt5a control of cell polarity and directional movement by polarized redistribution of adhesion receptors. 2008, Pubmed
Wolda, Overlapping expression of Xwnt-3A and Xwnt-1 in neural tissue of Xenopus laevis embryos. 1993, Pubmed , Xenbase
Wolff, Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. 1998, Pubmed
Wu, The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. 2008, Pubmed
Wu, Wg and Wnt4 provide long-range directional input to planar cell polarity orientation in Drosophila. 2013, Pubmed
Yamada, Ror2 is required for midgut elongation during mouse development. 2010, Pubmed
Yamamoto, Wnt5a modulates glycogen synthase kinase 3 to induce phosphorylation of receptor tyrosine kinase Ror2. 2007, Pubmed
Yan, Rho1 has multiple functions in Drosophila wing planar polarity. 2009, Pubmed
Yan, The multiple-wing-hairs gene encodes a novel GBD-FH3 domain-containing protein that functions both prior to and after wing hair initiation. 2008, Pubmed
Yanagawa, The dishevelled protein is modified by wingless signaling in Drosophila. 1995, Pubmed
Yates, The PCP genes Celsr1 and Vangl2 are required for normal lung branching morphogenesis. 2010, Pubmed
Yates, The planar cell polarity gene Vangl2 is required for mammalian kidney-branching morphogenesis and glomerular maturation. 2010, Pubmed
Yin, Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. 2008, Pubmed
Zallen, Planar polarity and tissue morphogenesis. 2007, Pubmed
Zallen, Patterned gene expression directs bipolar planar polarity in Drosophila. 2004, Pubmed
Zhang, Expression of Wnt signaling components during Xenopus pronephros development. 2011, Pubmed , Xenbase
Zilber, The PCP effector Fuzzy controls cilial assembly and signaling by recruiting Rab8 and Dishevelled to the primary cilium. 2013, Pubmed