Specificity of Drosophila Cytonemes for Distinct Signaling Pathways

Signaling protein receptors are segregated into different cell protrusions in Drosophila cells. Cytonemes are types of filopodia in the Drosophila wing imaginal disc that are proposed to serve as conduits in which morphogen signaling proteins move between producing and target cells. We investigated the specificity of cytonemes that are made by target cells. Cells in wing discs made cytonemes that responded specifically to Decapentaplegic (Dpp) and cells in eye discs made cytonemes that responded specifically to Spitz (the Drosophila epidermal growth factor protein). Tracheal cells had at least two types: one made in response to Branchless (a Drosophila fibroblast growth factor protein, Bnl), to which they segregate the Bnl receptor, and another to which they segregate the Dpp receptor. We conclude that cells can make several types of cytonemes, each of which responds specifically to a signaling pathway by means of the selective presence of a particular signaling protein receptor that has been localized to that cytoneme.

[1]  D. Haydon,et al.  An Introduction to the Principles of Surface Chemistry , 1973 .

[2]  Chonnettia Jones,et al.  Cell-cycle regulation and cell-type specification in the developing Drosophila compound eye. , 2004, Seminars in cell & developmental biology.

[3]  S. Kain,et al.  Optimized codon usage and chromophore mutations provide enhanced sensitivity with the green fluorescent protein. , 1996, Nucleic acids research.

[4]  T. Kornberg,et al.  Cytonemes Cellular Processes that Project to the Principal Signaling Center in Drosophila Imaginal Discs , 1999, Cell.

[5]  J. B. Duffy,et al.  Bipartite Inhibition of Drosophila Epidermal Growth Factor Receptor by the Extracellular and Transmembrane Domains of Kekkon1 , 2004, Genetics.

[6]  T. Kornberg,et al.  Regulation of Drosophila matrix metalloprotease Mmp2 is essential for wing imaginal disc:trachea association and air sac tubulogenesis. , 2009, Developmental biology.

[7]  N. Perrimon,et al.  Small wing PLCgamma is required for ER retention of cleaved Spitz during eye development in Drosophila. , 2004, Developmental cell.

[8]  K. Moses,et al.  Genetics of epithelial polarity and pattern in the Drosophila retina , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[9]  M. Affolter,et al.  An absolute requirement for both the type II and type I receptors, punt and thick veins, for Dpp signaling in vivo , 1995, Cell.

[10]  B. Shilo,et al.  Secreted Spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. , 1995, Genes & development.

[11]  Jean-Yves Roignant,et al.  Pattern formation in the Drosophila eye disc. , 2009, The International journal of developmental biology.

[12]  T. Kornberg,et al.  Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic , 2005, Nature.

[13]  Makoto Sato,et al.  FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system. , 2002, Developmental cell.

[14]  Arjun Guha,et al.  Understanding morphogen gradients: a problem of dispersion and containment. , 2007, Current opinion in genetics & development.

[15]  Mark Miodownik,et al.  Dynamic filopodia transmit intermittent Delta-Notch signaling to drive pattern refinement during lateral inhibition. , 2010, Developmental cell.

[16]  Justin P. Kumar,et al.  EGF Receptor and Notch Signaling Act Upstream of Eyeless/Pax6 to Control Eye Specification , 2001, Cell.

[17]  J. Stockman,et al.  Noncanonical TGFβ Signaling Contributes to Aortic Aneurysm Progression in Marfan Syndrome Mice , 2012 .

[18]  M. Freeman,et al.  Reiterative Use of the EGF Receptor Triggers Differentiation of All Cell Types in the Drosophila Eye , 1996, Cell.