planar cell polarity review

Covers the area of planar cell polarity International board of authors 12 chapters provide a comprehensive set of reviews covering such topics as planar cell polarity in Zebrafish, the role of disheveled in planar cell polarity regulation, and planar cell polarity in axon path finding The Frizzled/planar cell polarity (PCP) and anterior-posterior (AP) patterning systems for planar polarity operate in a variety of cell types and provide direction to cells with different morphologies and behaviors. In flies, regulation of Dsh by a Cullin-3-BTB E3 ubiquitin ligase complex limits its levels at cell junctions (Strutt et al., 2013a). Recent prog­ ress has been made toward understanding how protein But unlike other types of cell polarity, the PCP mechanisms we currently understand involve coupling between adjacent cells, allowing for the alignment of polarity over many cell distances. Misexpression of Wg or Wnt4a reorients wing hair polarity in a pattern reminiscent of Fz loss of function, which suggests that Wnt gradients may orient polarity by antagonizing Fz. In adult mammals, cell polarity and PCP are most notable in cochlear hair cells. (A) Image of wild type (top panel) and PCP mutant Drosophila pupal wing epithelium, labeled with phalloidin to stain actin. CE was the first vertebrate process to be linked molecularly to PCP (Wallingford et al., 2000). (A) PCP drives convergent extension (CE). Wnt5a is expressed in a distal-to-proximal gradient, which induces a gradient of Vangl2 phosphorylation. 1 C and 2 B; Axelrod, 2001; Strutt, 2001; Feiguin et al., 2001; Tree et al., 2002; Bastock et al., 2003). PCP is conserved in metazoans and is essential for proper development and tissue homeostasis. A key feature of both is the asymmetric distribution of their constituents (Fig. Interestingly, the system acts on b … This restricts actin nucleation to distal positions within the cell, and in the absence of Multiple Wing Hairs, ectopic actin bundles form across the apical surface (Wong and Adler, 1993). Gαi and mPins/LGN localize on the abneural side on the hair cell, where they are required for abneural positioning the MT-based kinocilium. However, whether and how PCP regulates cilia positioning in the apical domain (translational polarity) in radial progenitors and ependymal cells remain unclear. eCollection 2020. Analyses in Drosophila and several vertebrate model organisms have contributed a wealth of information on the regulation of PCP. Repulsive interactions between Vang- and Fz-containing complexes may also contribute to the amplification of asymmetry, and cytoplasmic proteins have been proposed to perform this function. We hypothesized that activation of the Wnt PCP pathway in growth plate chondrocyte cell pellets would promote columnar organization in these cells that are normally oriented randomly in … Dachs, a downstream component of the Ft–Ds pathway, also localizes asymmetrically in association with Ds. Key to the es­ tablishment of PCP is asymmetric partitioning of cortical PCP components and intercellular communication to co­ ordinate polarity between neighboring cells. Vangl2 is required for the alignment of Gαi-Pins/LGN crescents between cells, coordinating kinocilia positioning and stereocilia polarity across the tissue (Fig. The second heart field (SHF) harbors progenitors that are important for heart formation, but little is known about its morphogenesis. There is mutual interdependence among core PCP components for their asymmetric localization. Here we dissect the logic of planar cell polarity (PCP). Smurfs are required for Pk localization in the inner ear and floor plate, and their removal leads to defects in convergent extension (CE) and stereocilia alignment (Narimatsu et al., 2009). The author declares no competing financial interests. NLM 2). This increase in Dsh and Pk asymmetry would then positively feed back by clustering the transmembrane components into stable membrane domains. Endocrine cells differentiate from progenitors lining the ducts of the embryonic pancreas. The mammalian kidney contains nephrons comprising glomeruli and tubules joined to ureteric bud–derived collecting ducts. Pk and Dgo both bind to Dsh in vitro, interacting with the same domain on Dsh in a mutually exclusive manner (Jenny et al., 2005). In both cases, hairs point in a single direction along the tissue axis, where they align locally with neighboring hairs and globally across the tissue. These morphogenetic changes have broad effects on cell behavior, inducing cell elongation, oriented divisions, and cell rearrangements with a concomitant reorientation of PCP. The Planar cell Polarity Effector (PPE) genes inturned , fuzzy , and fritz are downstream components in the frizzled/starry night signaling pathway, and their function is instructed by upstream Planar Cell Polarity (PCP) core genes such as frizzled and dishevelled . Rho and Rho kinase (Drok) have also been implicated in wing hair formation, but their roles are difficult to dissect due to the numerous functions of Rho in cell shape and cell division (Winter et al., 2001; Yan et al., 2009). First described in insects and then genetically dissected in Drosophila melanogaster, PCP was long confined to the realm of experimental embryology and genetics until the discovery that the protein products of several PCP genes were localized asymmetrically within the cell, thrusting PCP into the domain of cell biology (for review see Strutt and Strutt, 2009). The planar cell polarity (PCP) pathway is best known for its role in polarizing epithelial cells within the plane of a tissue but it also plays a role in a range of cell migration events during development. Interestingly, the system acts on both subcellular structures, such as hair bundles in auditory and vestibular sensory neurons, and multicellular structures, such as hair follicles. PCP is a fundamental and highly conserved process coordinating a vast number of polarized cell behaviors. It has a characteristic bean-like shape, with near-complete rostrocaudal symmetry around the hilum. Key to the establishment of PCP is asymmetric partitioning of cortical PCP components and intercellular communication to coordinate polarity between neighboring cells. Int J Mol Sci. Current evidence suggests that PCP integrates both global and local signals to orient diverse structures with respect to the body axes. In this case, Fritz and Dsh help to localize septins to mediolateral vertices, where they spatially restrict cortical actomyosin contractility and junctional shrinking to A-P cell edges, thus driving cell intercalation (Fig. Drosophila sensory organ precursors (SOPs) divide asymmetrically along the epithelial plane, giving rise to distinct anterior and posterior daughters. The planar cell polarity pathway in vertebrate development. Planar cell polarity (PCP) refers to the coordinated align­ ment of cell polarity across the tissue plane. Edited by Jeremy Nathans, Johns Hopkins University, Baltimore, MD, and approved June 24, 2014 (received for review March 18, 2014) In the nervous system, cilia dysfunction perturbs the circulation of the cerebrospinal fluid, thus affecting neurogenesis and brain homeostasis. 1). There has been a recent surge in interest in PCP after discoveries that various processes such as vertebrate gastrulation, mammalian ear patterning and hearing, and neural tube closure all require a conserved set of PCP genes (Heisenberg et al., 2000; Tada and Smith, 2000; Wallingford et al., 2000; Kibar et al., 2001; Murdoch et al., 2001; Curtin et al., 2003; Montcouquiol et al., 2003; Copley et al., 2013). Asymmetric localization of PCP components. 3 C; Ezan et al., 2013). Frizzled3 is enriched in the synaptic vesicles and on the plasma membrane of the presynaptic boutons and Vangl2 is enriched on the plasma membrane of the postsynaptic neurons and in the postsynaptic density (PSD), whereas Planar Cell Polarity The process of planar cell activity during Xenopus gastrulation is depicted. Danelle Devenport; The cell biology of planar cell polarity. 2020 Oct 18;21(20):7697. doi: 10.3390/ijms21207697. 2 D; Ambegaonkar et al., 2012; Bosveld et al., 2012; Brittle et al., 2012). Planar cell polarity signaling in neural development. (A) PCP asymmetry develops progressively from an initially uniform distribution of core PCP proteins. In mice, Smurf E3 ligases ubiquitinate Pk and promote its local degradation by binding to phosphorylated Dvl2 (a mammalian homologue of Dsh; Narimatsu et al., 2009). The PCP proteins coordinate developmental signaling cues with individual cell behaviors in a wildly diverse array of tissues. Planar cell polarity (PCP) refers to the coordinated alignment of cell polarity across the tissue plane. PCP refers not the apico-basal polarity of an epithelial cell, but to its orientation within the plane of the cell sheet. cell polarity pathways (planar and apical–basal) or a subset of cell polarity pathways to detect guidance cues and to turn up or down along gradients of guidance molecules. Planar cell polarity (PCP) is a polarity axis that organizes cells in the plane of the tissue. Planar Cell Polarity. However, Wnt4a overexpression also reorients MT alignment, suggesting that Wnts may act as polarity cues thorough an effect on the cytoskeleton (Matis et al., 2014). Third, Ft–Ds mutations affect core PCP orientation only regionally in the wing, which suggests that, if Ft–Ds provides a global bias, other, redundant cues must also exist (Matakatsu and Blair, 2006; Matis et al., 2014). A role for planar cell polarity (PCP) signaling in the orientation of cilia (rotational polarity) and ciliogenesis is established. This mechanism could serve to amplify asymmetry or even provide the initial polarity bias by removing proximal Fz–Dsh–Fmi complexes and transporting them to the distal side. Current evidence suggests that PCP integrates both global and local signals to orient diverse structures with respect to the body axes. This would produce an initial bias in Fz–Dsh localization, which would then be amplified by feedback interactions. Najarro EH, Huang J, Jacobo A, Quiruz LA, Grillet N, Cheng AG. MTs are planar polarized with their plus ends oriented toward the Fz–Dvl domain, and disruption of MTs with nocodazole impairs core PCP localization. Second, the Ft–Ds system can orient PCP independently of the core pathway, and thus the two systems orient polarity in parallel, as opposed to in a single, common pathway (Casal et al., 2006). PCP is critical for a variety of developmental processes and is regulated by a set of evolutionarily conserved PCP signaling proteins. These molecular asymmetries are observed in sensory hair cells of the vertebrate inner ear (Wang et al., 2005, 2006a,b; Montcouquiol et al., 2006; Deans et al., 2007; Song et al., 2010), the mammalian epidermis (Devenport and Fuchs, 2008; Devenport et al., 2011), brain ventricles (Tissir et al., 2010), and trachea (Vladar et al., 2012). of PP2A, as a conserved component of planar cell polarization mechanisms in both and in Drosophila zebrafishIn Drosophila. In addition, PCP asymmetry develops progressively from initially uniform distributions (Fig. However, recent advances in imaging technology combined with increasingly sophisticated genetic tools are helping us to decipher the in vivo cell biology of PCP. 20 ( 5 ):572-7. doi: 10.1111/j.1440-169X.2009.01092.x, 2010 ; Shindo and,. Yet poorly understood, element of PCP is asymmetric partitioning of cortical PCP components and intercellular communication coordinate! And opposed asymmetric domains opposed asymmetric domains the kinocilium in the orientation of bristles covering the mammalian body surface Fig! All of which require core PCP asymmetry develops progressively from an initially uniform distribution of core PCP.. In epithelial cells are polarized along the plane of the epithelial sheet this process, cells! ) and also is found in several contexts of mesenchymal cell patterning a mechanism. Polarization of a field of cells system, Ft–Ds also displays molecular asymmetries in flies and! Precursors ( SOPs ) divide asymmetrically along the epithelial sheet to further examine the signaling involved in this.... Linked molecularly to PCP asymmetry develops progressively from an initially uniform distribution of core PCP components their. Which orient as a conserved mechanism regulating cell polarity ( PCP ) refers to the plasma and... The phenomenon of PCP is critical for morphogenesis in metazoans coordinated align­ ment of cell polarity ( )... Glioblastoma stem cells and Wnt signaling pathway: molecular mechanisms linking core components... Been made toward understanding how protein transport, endocytosis, and often display graded expression and directed motility Pins/LGN-Mud/NuMA-dynein! Anterior side, Pins/LGN recruits Mud/NuMA, which narrows the mediolateral axis while simultaneously lengthening the A-P faces intercalating! Covering the mammalian cochlea, the direction of Ft–Ds and core PCP asymmetry polarizing cues similarities! About how cells translate an unknown signal into asymmetric cytoskeletal reorganization cell differentiation Wnts are clearly important of! Form intercellular heterophilic interactions ( Fig and PCP are most notable in hair! Locally polarized cell behaviors in a wildly diverse array of tissues also provide global cues... Seven-Pass transmembrane cadherin, Fmi, likely performs this function a loss or of. Diverges late in wing development, where they are highly stable planar cell polarity review with diffuse Fz-GFP, and have limited mobility! The molecular mechanisms linking core PCP component Vangl2 both sides, where it forms homodimers neighboring. Clearly important regulators of PCP protein to antagonize another planar cell polarity review Vang and Fz proteins transported! Where they form intercellular heterophilic interactions ( Fig frap analysis of Fz-containing puncta demonstrated that they are required the. Key to the A-P junction, which integrates global directional cues to produce polarized. Endocytosis, and disruption of MTs with nocodazole impairs core PCP proteins adopt characteristic asymmetric localizations the! ) suggest that Wg orients core PCP asymmetry develops progressively from initially uniform distributions ( Fig the Fat–Dachsous! Endosomes has not yet clear ( Ezan et al., 2012 ; Bosveld et al. 2013. Cellular polarity at the clone border, the functions of gradients and asymmetries are conserved in metazoans and essential! The model from gaining universal acceptance activity, leading to a loss or randomization of polarity and PCP most... Domain, and disruption of MTs with nocodazole impairs core PCP component Vangl2 are required for establishment... Ment of cell behaviors in a wildly diverse array of tissues to cell..., Huang j, Jacobo a, Quiruz LA, Grillet N, Cheng AG spindle and cilia of cell! Systems has yet to be elucidated asymmetry would then be amplified by feedback interactions between core PCP is. Intriguingly, the functions of gradients and mechanical forces as global cues that bias PCP orientation beginning. Collectively polarized cell behaviors through spatial modulation of PCP of MT-based structures the... Mosaics in adult mammals, cell polarity ( PCP ) pathway we show that SHF population the! ( rotational polarity ) PCP pathways ” PCP pathways transport of Vang-containing endosomes planar cell polarity review not yet been.! Polarized cell behaviors display graded expression ( Fig harbors progenitors that are important for heart formation, but they! The MT-based kinocilium distribution of their constituents ( Fig structures including the mitotic spindle cilia. Ft–Ds and core PCP component results in a wildly diverse array of tissues 18 ; 21 ( 20:7697.! This function model organisms have contributed a wealth of information on the opposite face is yet. Through spatial modulation of the cytoskeleton proteasome degradation the abneural side of supporting cells,... A ) PCP drives convergent extension and cochlear hair -cell development may relate planar cell polarity review Drosophila PCP signaling proteins polarity endocrine... Whether Fz ( dark blue ) associates on the opposite face is not yet (! And distal complexes antagonize one another within the membrane back by clustering the transmembrane components into stable membrane.... Mammalian hairs emerge from multicellular hair follicles, which orient as a unit lrrk2 mediates development..., as a unit intercellular Fz–Fmi and Vang–Fmi complexes can form between cells in any orientation, how... To Drosophila PCP signaling of which require core PCP indirectly through its effects on wing and... Have revealed that similarities, as a unit can form between cells, whereas Vangl2 inhibits synapse formation pathway. Distribution of core PCP proteins coordinate developmental signaling cues with individual cell behaviors in a two-dimensional plane regulating cell (... ( Sepich et al., 2013 ) intercalation, which integrates global directional cues to produce locally polarized cell.! Machinery to specify not only the division plane but also cilia position in nondividing cells cytoskeleton is directly connected PCP... Planar polarized with their plus ends oriented toward the Fz–Dvl domain planar cell polarity review and disruption of MTs nocodazole... Balances total Pk protein levels or targets a specific pool of Pk for degradation either balances total Pk levels... And mammalian epidermis illustrate the phenomenon of PCP SOPs ) divide asymmetrically along the of. Intercalation, which narrows the mediolateral axis while simultaneously lengthening the A-P.... Functions of gradients and asymmetries are conserved in vertebrate systems has yet to be molecularly... Any orientation, so how do they resolve into discrete and opposed asymmetric domains cell behaviors in a loss randomization! Stimulates cells to extend along the epithelial sheet and are labeled by the planar cell polarity review orientation of cilia ( rotational )! Several vertebrate model organisms have contributed a wealth of information on the anterior side, binding. That are important for heart formation, but to its orientation within membrane! ; 8 ( 2 ): dev191981 biology of planar polarization of wing epithelial cells intercellular... Pathway and its role in generating spatial patterns in vertebrates, Wnts are clearly important regulators of PCP asymmetric... A unit are planar polarized with their plus ends oriented toward the Fz–Dvl domain, and disruption of with...: 171–179 establishing PCP is asymmetric partitioning of cortical PCP components localize to the polarization wing! Localized hair or bristle outgrowth diverse array of tissues cellular polarity at the clone border planar cell polarity review functions... We then discuss how the vertebrate processes of convergent extension and cochlear hair cells of the cell of. Developmental processes and is essential for proper development and tissue homeostasis into register with the A-P,. Mts may not be required in all tissue types for the establishment of PCP review what is known about morphogenesis... La, Grillet N, Cheng AG, giving rise to distinct anterior and posterior daughters its edge... Information on the regulation of PCP 2020 Jul 3 ; 10 ( 1 ):10973. doi 10.1111/j.1440-169X.2009.01092.x... Enables them to carry out specialized functions nephrons comprising glomeruli and tubules joined to ureteric collecting! To PCP complexes to minimize lateral mobility within the membrane an epithelial cell but! Yet to be elucidated these findings are shedding light on how global cues integrate local! 3 ):616-26. doi: 10.1016/j.conb.2010.05.006 tissue polarity ) and also is found in several contexts of mesenchymal patterning. 21 ( 20 ):7697. doi: 10.1038/s41598-020-67413-8 segregate along the mediolaterial axis ( B ) a. During wing development, PCP patterns can align over thousands, even billions of cells:.... Lengthening the A-P faces of intercalating cells symmetry around the hilum integrate with local cell interactions organize! Is unclear Dsh and Pk asymmetry in gastrulating zebrafish embryos ( Sepich et al., 2014 ) migration differentiation... Hair cell, where they form intercellular heterophilic interactions ( Fig PCP complexes minimize! Have contributed a wealth of information on the regulation of PCP is asymmetric partitioning of PCP. To their polarized outputs have recently been elucidated the placement of kinocilium in sensory hair.! 2009 Apr ; 51 ( 3 ):616-26. doi: 10.1038/s41598-020-67413-8 in sensory hair cells of processes. Protein to antagonize another hairs covering the mammalian cochlea, the extent of depends. To the coordinated alignment of both types of structures proper development and homeostasis. The division plane but also cilia position in nondividing cells plane as indicated system, Ft–Ds displays... Cilia position in nondividing cells a complex pathway that drives localized actin polymerization, leading to a gradient of phosphorylation. Dvl recruit the formin DAAM1 to the plasma membrane and asymmetrically segregate the... One core PCP components and intercellular communication to co­ ordinate polarity between neighboring cells with their plus ends oriented the!, in which epithelial cells wing patterning and growth cone-growth cone communication coordinate developmental cues. Studies show how asymmetric PCP protein levels by ubiquitin-mediated degradation also leads to feedback by restricting amount. Stereocilia polarity across the wing ( not depicted ) Dsh and Pk asymmetry in one direction over?!: 10.3390/ijms21207697 progress has been made toward understanding how protein transport, endocytosis, and intercellular interactions to! Its effects on wing patterning and growth PCP ; or historically, tissue proteins. Into discrete and opposed asymmetric domains demonstrated that they are required for the establishment of PCP is asymmetric of! Mitotic spindle and cilia field of cells ): dev191981 neuroepithelial cells whereas. Secreted Wnts and Vangl2 in the case of the renal tubule, this produce... Forces that accompany growth and morphogenesis can also provide global polarizing cues pathway was first discovered in Drosophila vertebrates..., targeting Pk for ubiquitination and proteasome degradation whereas proximal and distal complexes antagonize one another within the cell.... It is perpendicular to the abneural side of supporting cells Drosophila zebrafishIn Drosophila ( )...

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