Cell packing influences planar cell polarity signaling

Some epithelial cells display asymmetry along an axis orthogonal to the apical-basal axis, referred to as planar cell polarity (PCP). A Frizzled-mediated feedback loop coordinates PCP between neighboring cells, and the cadherin Fat transduces a global directional cue that orients PCP with respect to the tissue axes. The feedback loop can propagate polarity across clones of cells that lack the global directional signal, although this polarity propagation is error prone. Here, we show that, in the Drosophila wing, a combination of cell geometry and nonautonomous signaling at clone boundaries determines the correct or incorrect polarity propagation in clones that lack Fat mediated global directional information. Pattern elements, such as veins, and sporadic occurrences of irregular geometry are obstacles to polarity propagation. Hence, in the wild type, broad distribution of the global directional cue combines with a local feedback mechanism to overcome irregularities in cell packing geometry during PCP signaling.

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

[3]  D. Tree,et al.  A three-tiered mechanism for regulation of planar cell polarity. , 2002, Seminars in cell & developmental biology.

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

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

[6]  M. Jaiswal,et al.  Fat and Wingless signaling oppositely regulate epithelial cell-cell adhesion and distal wing development in Drosophila , 2006, Development.

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

[8]  A. Garcı́a-Bellido,et al.  Cell behaviour of Drosophila fat cadherin mutations in wing development , 2000, Mechanisms of Development.

[9]  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.

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

[11]  S. Blair,et al.  Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing , 2004, Development.

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

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

[14]  Peter A Lawrence,et al.  Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity , 2006, Development.

[15]  Peter A Lawrence,et al.  Cell interactions and planar polarity in the abdominal epidermis of Drosophila , 2004, Development.

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

[17]  M. Mlodzik,et al.  Planar cell polarization: an emerging model points in the right direction. , 2005, Annual review of cell and developmental biology.

[18]  N. Perrimon,et al.  Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. , 1992, Genetics.

[19]  C. Tomlin,et al.  Mathematical Modeling of Planar Cell Polarity to Understand Domineering Nonautonomy , 2005, Science.

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

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

[22]  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.

[23]  A. Garcı́a-Bellido,et al.  Cell cycling and patterned cell proliferation in the Drosophila wing during metamorphosis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[24]  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.

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

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

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

[28]  X. Morin,et al.  A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Eaton,et al.  Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. , 2005, Developmental cell.

[30]  S. Blair,et al.  The crossveinless gene encodes a new member of the Twisted gastrulation family of BMP-binding proteins which, with Short gastrulation, promotes BMP signaling in the crossveins of the Drosophila wing. , 2005, Developmental biology.

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

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

[33]  M. Simon Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression , 2004, Development.

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

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