Frizzled signalling and cell polarisation in Drosophila and vertebrates

A key aspect of animal development is the appropriate polarisation of different cell types in the right place at the right time. Such polarisation is often precisely coordinated relative to the axes of a tissue or organ, but the mechanisms underlying this coordination are still poorly understood. Nevertheless, genetic analysis of animal development has revealed some of the pathways involved. For example, a non-canonical Frizzled signalling pathway has been found to coordinate cell polarity throughout the insect cuticle, and recent work has implicated an analogous pathway in coordinated polarisation of cells during vertebrate development. This review discusses recent findings regarding non-canonical Frizzled signalling and cell polarisation.

[1]  Peter J. Bryant,et al.  The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily , 1991, Cell.

[2]  J. Taylor,et al.  Van Gogh: a new Drosophila tissue polarity gene. , 1998, Genetics.

[3]  P. Adler,et al.  A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains , 1989, Nature.

[4]  Michael Kühl,et al.  Antagonistic regulation of convergent extension movements in Xenopus by Wnt/β-catenin and Wnt/Ca2+ signaling , 2001, Mechanisms of Development.

[5]  Yasuyuki Shima,et al.  Flamingo, a Seven-Pass Transmembrane Cadherin, Regulates Planar Cell Polarity under the Control of Frizzled , 1999, Cell.

[6]  J. Zhang,et al.  frizzled regulates mirror-symmetric pattern formation in the Drosophila eye. , 1995, Development.

[7]  H. Strutt,et al.  Polarity determination in the Drosophila eye. , 1999, Current opinion in genetics & development.

[8]  P. Adler,et al.  Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila , 1987, Nature.

[9]  N. Perrimon,et al.  The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the wingless signal. , 1994, Genes & development.

[10]  R. Moon,et al.  Wnt signaling and heterotrimeric G-proteins: strange bedfellows or a classic romance? , 2001, Biochemical and biophysical research communications.

[11]  H. Steinbeisser,et al.  Frizzled-7 signalling controls tissue separation during Xenopus gastrulation , 2001, Nature.

[12]  Robert Geisler,et al.  Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation , 2000, Nature.

[13]  H. Theisen,et al.  dishevelled is required during wingless signaling to establish both cell polarity and cell identity. , 1994, Development.

[14]  J. Villano,et al.  four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. , 1995, Development.

[15]  D. Tree,et al.  The balance between isoforms of the prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs. , 1999, Genes & development.

[16]  H. Steller,et al.  Positional information along the dorsal-ventral axis of the Drosophila eye: graded expression of the four-jointed gene. , 1996, Developmental biology.

[17]  R. Moon,et al.  Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos , 1995, Molecular and cellular biology.

[18]  Ajamete Kaykas,et al.  Zebrafish Prickle, a Modulator of Noncanonical Wnt/Fz Signaling, Regulates Gastrulation Movements , 2003, Current Biology.

[19]  C. Kimmel,et al.  Shaping the zebrafish notochord , 2003, Development.

[20]  J. Axelrod,et al.  Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. , 2001, Genes & development.

[21]  Lilianna Solnica-Krezel,et al.  Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements , 2002, Nature Cell Biology.

[22]  Yoichi Kato,et al.  Wnt/Frizzled Activation of Rho Regulates Vertebrate Gastrulation and Requires a Novel Formin Homology Protein Daam1 , 2001, Cell.

[23]  R. Moon,et al.  Dishevelled activates Ca2+ flux, PKC, and CamKII in vertebrate embryos , 2003, The Journal of cell biology.

[24]  N. Perrimon,et al.  Multiple roles for four-jointed in planar polarity and limb patterning. , 2000, Developmental biology.

[25]  M. Mlodzik,et al.  Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye. , 2000, Development.

[26]  R. Moon,et al.  Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling , 1997, Nature.

[27]  D. Strutt,et al.  The role of RhoA in tissue polarity and Frizzled signalling , 1997, Nature.

[28]  G. Rubin,et al.  Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. , 1998, Development.

[29]  Michael Kühl,et al.  Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis , 2002, Nature.

[30]  Scott E Fraser,et al.  Convergent extension: the molecular control of polarized cell movement during embryonic development. , 2002, Developmental Cell.

[31]  R. Moon,et al.  Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in aG-protein-dependent manner , 1999, Current Biology.

[32]  T. Mak,et al.  Polarization of Chemoattractant Receptor Signaling During Neutrophil Chemotaxis , 2022 .

[33]  P. Adler,et al.  Dishevelled is a component of the frizzled signaling pathway in Drosophila. , 1995, Development.

[34]  Suzanne Eaton,et al.  Planar cell polarization requires Widerborst, a B' regulatory subunit of protein phosphatase 2A. , 2002, Development.

[35]  L. Solnica-Krezel,et al.  Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity? , 2002, Trends in genetics : TIG.

[36]  P. Adler,et al.  Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells , 1993, The Journal of cell biology.

[37]  P. Adler,et al.  Tissue polarity points from cells that have higher Frizzled levels towards cells that have lower Frizzled levels , 1997, Current Biology.

[38]  T. Wolff,et al.  The Cadherins Fat and Dachsous Regulate Dorsal/Ventral Signaling in the Drosophila Eye , 2002, Current Biology.

[39]  J. A. Kaltschmidt,et al.  Planar polarity and actin dynamics in the epidermis of Drosophila , 2002, Nature Cell Biology.

[40]  N. Copeland,et al.  Identification of Vangl2 and Scrb1 as planar polarity genes in mammals , 2003, Nature.

[41]  P. Lawrence,et al.  Developmental Compartments and Planar Polarity in Drosophila , 2002, Current Biology.

[42]  I. Blitz,et al.  Involvement of the small GTPases XRhoA and XRnd1 in cell adhesion and head formation in early Xenopus development. , 1999, Development.

[43]  Marek Mlodzik,et al.  Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye , 1999, Nature.

[44]  M. Peifer,et al.  Wnt signaling: Moving in a new direction , 2000, Current Biology.

[45]  J. Axelrod,et al.  Coupling Planar Cell Polarity Signaling to Morphogenesis , 2002, TheScientificWorldJournal.

[46]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[47]  P. Adler,et al.  Planar signaling and morphogenesis in Drosophila. , 2002, Developmental cell.

[48]  M. Boutros,et al.  Dishevelled Activates JNK and Discriminates between JNK Pathways in Planar Polarity and wingless Signaling , 1998, Cell.

[49]  Kenneth R Chien,et al.  Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure , 2002, Development.

[50]  R. Moon,et al.  The Wnt/Ca2+ pathway: a new vertebrate Wnt signaling pathway takes shape. , 2000, Trends in genetics : TIG.

[51]  R. Moon,et al.  G Protein Signaling from Activated Rat Frizzled-1 to the β-Catenin-Lef-Tcf Pathway , 2001, Science.

[52]  Jin-Kwan Han,et al.  Xenopus Cdc42 regulates convergent extension movements during gastrulation through Wnt/Ca2+ signaling pathway. , 2002, Developmental biology.

[53]  D. Gubb,et al.  A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. , 1982, Journal of embryology and experimental morphology.

[54]  Ken W. Y. Cho,et al.  Dishevelled phosphorylation, subcellular localization and multimerization regulate its role in early embryogenesis , 2000, The EMBO journal.

[55]  R. Bastock,et al.  Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning , 2003, Development.

[56]  Marek Mlodzik,et al.  The planar polarity gene strabismus regulates convergent extension movements in Xenopus , 2002, The EMBO journal.

[57]  L. Luo,et al.  Drosophila Rho-Associated Kinase (Drok) Links Frizzled-Mediated Planar Cell Polarity Signaling to the Actin Cytoskeleton , 2001, Cell.

[58]  M. Scott,et al.  Prickle Mediates Feedback Amplification to Generate Asymmetric Planar Cell Polarity Signaling , 2002, Cell.

[59]  R. Carthew,et al.  Use of dsRNA-Mediated Genetic Interference to Demonstrate that frizzled and frizzled 2 Act in the Wingless Pathway , 1998, Cell.

[60]  P. Adler,et al.  The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. , 1996, Development.

[61]  J. Charlton,et al.  The domineering non-autonomy of frizzled and Van Gogh clones in the Drosophila wing is a consequence of a disruption in local signaling , 2000, Mechanisms of Development.

[62]  J. Charlton,et al.  The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. , 1999, Development.

[63]  D. Strutt,et al.  Asymmetric Localization of Frizzled and the Determination of Notch-Dependent Cell Fate in the Drosophila Eye , 2002, Current Biology.

[64]  R. Keller,et al.  The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. , 2002, Developmental biology.

[65]  M. Gessler,et al.  Fjx1, the murine homologue of the Drosophila four-jointed gene, codes for a putative secreted protein expressed in restricted domains of the developing and adult brain , 1999, Mechanisms of Development.

[66]  Jeremy Nathans,et al.  A new member of the frizzled family from Drosophila functions as a Wingless receptor , 1996, Nature.

[67]  J. Smith,et al.  Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. , 2000, Development.

[68]  P. Adler,et al.  A single frizzled protein has a dual function in tissue polarity. , 1994, Development.

[69]  W. Birchmeier,et al.  The ankyrin repeat protein Diversin recruits Casein kinase I (cid:1) to the (cid:2) -catenin degradation complex and acts in both canonical Wnt and Wnt/JNK signaling , 2002, Nature Reviews Molecular Cell Biology.

[70]  G. Struhl,et al.  Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye. , 1999, Development.

[71]  D. Gubb,et al.  Drosophila tissue polarity requires the cell-autonomous activity of the fuzzy gene, which encodes a novel transmembrane protein. , 1997, Development.

[72]  Julian Lewis,et al.  Planar cell polarity in the inner ear: how do hair cells acquire their oriented structure? , 2002, Journal of neurobiology.

[73]  Steve D. M. Brown,et al.  Mutation of Celsr1 Disrupts Planar Polarity of Inner Ear Hair Cells and Causes Severe Neural Tube Defects in the Mouse , 2003, Current Biology.

[74]  S. Sokol.  Analysis of Dishevelled signalling pathways during Xenopus development , 1996, Current Biology.

[75]  J. Klingensmith,et al.  The dishevelled protein is modified by wingless signaling in Drosophila. , 1995, Genes & development.

[76]  N. Ueno,et al.  The prickle-Related Gene in Vertebrates Is Essential for Gastrulation Cell Movements , 2003, Current Biology.

[77]  C. Goodman,et al.  Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. , 1995, Genes & development.

[78]  Ray Keller,et al.  Shaping the Vertebrate Body Plan by Polarized Embryonic Cell Movements , 2002, Science.

[79]  T. Uemura,et al.  Asymmetric colocalization of Flamingo, a seven-pass transmembrane cadherin, and Dishevelled in planar cell polarization , 2001, Current Biology.

[80]  S. Benzer,et al.  Rotation of photoreceptor clusters in the developing drosophila eye requires the nemo gene , 1994, Cell.

[81]  R. Moon,et al.  Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to mesoderm-inducing growth factors, may play a role in ventral mesodermal patterning during embryogenesis. , 1991, Development.

[82]  H. Steinbeisser,et al.  Xenopus frizzled 7 can act in canonical and non-canonical Wnt signaling pathways: implications on early patterning and morphogenesis , 2000, Mechanisms of Development.

[83]  A. McMahon,et al.  Differential transformation of mammary epithelial cells by Wnt genes , 1994, Molecular and cellular biology.

[84]  A. Copp,et al.  Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. , 2001, Human molecular genetics.

[85]  E. Nishida,et al.  JNK functions in the non‐canonical Wnt pathway to regulate convergent extension movements in vertebrates , 2002, EMBO reports.

[86]  M. Justice,et al.  Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail , 2001, Nature Genetics.

[87]  Tian Xu,et al.  Drosophila Atrophin Homolog Functions as a Transcriptional Corepressor in Multiple Developmental Processes , 2002, Cell.

[88]  David Strutt,et al.  Nonautonomous planar polarity patterning in Drosophila: dishevelled-independent functions of frizzled. , 2002, Developmental cell.

[89]  Jeffrey D. Axelrod,et al.  Regulation of Frizzled by Fat-like Cadherins during Planar Polarity Signaling in the Drosophila Compound Eye , 2002, Cell.

[90]  N. Perrimon,et al.  Differential Recruitment of Dishevelled Provides Signaling Specificity in the Planar Cell Polarity and Wingless Signaling Pathways in Drosophila, Planar Cell Polarity (pcp) Signaling Is Mediated by the Receptor Frizzled (fz) and Transduced by Dishevelled (dsh). Wingless (wg) Signaling Also Requires , 2022 .

[91]  S. Bray,et al.  Frizzled regulation of Notch signalling polarizes cell fate in the  Drosophila eye , 1999, Nature.

[92]  J. Wallingford,et al.  Regulation of convergent extension in Xenopus by Wnt5a and Frizzled-8 is independent of the canonical Wnt pathway. , 2001, The International journal of developmental biology.

[93]  E. Wieschaus,et al.  Wingless signaling in the Drosophila embryo: zygotic requirements and the role of the frizzled genes. , 1999, Development.

[94]  J. Rubin,et al.  Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea , 2003, Development.

[95]  P. Lawrence,et al.  Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. , 2002, Development.

[96]  M. Mlodzik,et al.  The atypical cadherin Flamingo links Frizzled and Notch signaling in planar polarity establishment in the Drosophila eye. , 2002, Developmental cell.

[97]  J Mao,et al.  Dishevelled Proteins Lead to Two Signaling Pathways , 1999, The Journal of Biological Chemistry.

[98]  N. Perrimon,et al.  The four-jointed gene is required in the Drosophila eye for ommatidial polarity specification , 1999, Current Biology.

[99]  D. Strutt.  Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. , 2001, Molecular cell.

[100]  S. Eaton,et al.  The ankyrin repeat protein Diego mediates Frizzled-dependent planar polarization. , 2001, Developmental cell.

[101]  J. Riou,et al.  Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. , 2000, Development.

[102]  Randall T. Moon,et al.  The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos , 2002, Nature Cell Biology.

[103]  R. Nusse,et al.  Mechanisms of Wnt signaling in development. , 1998, Annual review of cell and developmental biology.

[104]  Jeffrey D. Axelrod,et al.  Fidelity in planar cell polarity signalling , 2003, Nature.

[105]  R. Nusse,et al.  A mutational analysis of dishevelled in Drosophila defines novel domains in the dishevelled protein as well as novel suppressing alleles of axin. , 2002, Genetics.

[106]  Scott E. Fraser,et al.  Dishevelled controls cell polarity during Xenopus gastrulation , 2000, Nature.

[107]  S. Eaton.  Planar polarization of Drosophila and vertebrate epithelia. , 1997, Current opinion in cell biology.

[108]  J. Shih,et al.  Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. , 1993, Development.

[109]  J. Charlton,et al.  Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. , 1998, Development.

[110]  K. Matsumoto,et al.  Distinct Domains of Mouse Dishevelled Are Responsible for the c-Jun N-terminal Kinase/Stress-activated Protein Kinase Activation and the Axis Formation in Vertebrates* , 1999, The Journal of Biological Chemistry.

[111]  F. Marlow,et al.  Zebrafish Rho Kinase 2 Acts Downstream of Wnt11 to Mediate Cell Polarity and Effective Convergence and Extension Movements , 2002, Current Biology.

[112]  G. Golderer,et al.  Nitric oxide synthase is induced in sporulation of Physarum polycephalum. , 2001, Genes & development.

[113]  C. Heisenberg,et al.  The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation , 2003, Mechanisms of Development.

[114]  T. Wolff,et al.  Strabismus requires Flamingo and Prickle function to regulate tissue polarity in the Drosophila eye , 2003, Development.

[115]  B. Charroux,et al.  The tumor-suppressor and cell adhesion molecule Fat controls planar polarity via physical interactions with Atrophin, a transcriptional co-repressor , 2003, Development.

[116]  M. Deardorff,et al.  Frizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis. , 1998, Development.

[117]  E. Wilder,et al.  DWnt4 regulates cell movement and focal adhesion kinase during Drosophila ovarian morphogenesis. , 2002, Developmental cell.

[118]  J. Wallingford,et al.  Xenopus Dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. , 2001, Development.