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FGF ligands in Drosophila have distinct activities required to support cell migration and differentiation

Kadam, Snehalata and McMahon, Amy and Tzou, Phoebe and Stathopoulos, Angelike (2009) FGF ligands in Drosophila have distinct activities required to support cell migration and differentiation. Development, 136 (5). pp. 739-747. ISSN 0950-1991. PMCID PMC2685942. http://resolver.caltech.edu/CaltechAUTHORS:KADdev09

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[img] PDF (Fig. S1. pyr and ths ectopic expression in the mesoderm results in ectopic dpERK activation) - Supplemental Material
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[img] PDF (Fig. S2. Ectopic expression of pyr and ths does not support tracheal branching) - Supplemental Material
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[img] PDF (Fig. S3. pyr and ths expression domains suggest that both ligands influence dorsal mesoderm specification) - Supplemental Material
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[img] PDF (Fig. S4. Quantitative PCR analyses of ectopic pyr and ths expression demonstrates that the levels of ectopic expression supported by the respective transgenes are similar) - Supplemental Material
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[img] PDF (Fig. S5. Clumping phenotypes) - Supplemental Material
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[img] PDF (Fig. S6. Multilayer formation at the dorsal mesoderm) - Supplemental Material
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Abstract

Fibroblast growth factor (FGF) signaling controls a vast array of biological processes including cell differentiation and migration, wound healing and malignancy. In vertebrates, FGF signaling is complex, with over 100 predicted FGF ligand-receptor combinations. Drosophila melanogaster presents a simpler model system in which to study FGF signaling, with only three ligands and two FGF receptors (FGFRs) identified. Here we analyze the specificity of FGFR [Heartless (Htl) and Breathless (Btl)] activation by each of the FGF ligands [Pyramus (Pyr), Thisbe (Ths) and Branchless (Bnl)] in Drosophila. We confirm that both Pyr and Ths can activate Htl, and that only Bnl can activate Btl. To examine the role of each ligand in supporting activation of the Htl FGFR, we utilize genetic approaches that focus on the earliest stages of embryonic development. When pyr and ths are equivalently expressed using the Gal4 system, these ligands support qualitatively different FGFR signaling responses. Both Pyr and Ths function in a non-autonomous fashion to support mesoderm spreading during gastrulation, but Pyr exhibits a longer functional range. pyr and ths single mutants exhibit defects in mesoderm spreading during gastrulation, yet only pyr mutants exhibit severe defects in dorsal mesoderm specification. We demonstrate that the Drosophila FGFs have different activities and that cell migration and differentiation have different ligand requirements. Furthermore, these FGF ligands are not regulated solely by differential expression, but the sequences of these linked genes have evolved to serve different functions. We contend that inherent properties of FGF ligands make them suitable to support specific FGF-dependent processes, and that FGF ligands are not always interchangeable.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1242/dev.027904DOIArticle
http://dev.biologists.org/cgi/content/abstract/136/5/739PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2685942/PubMed CentralArticle
ORCID:
AuthorORCID
Stathopoulos, Angelike0000-0001-6597-2036
Additional Information:© The Company of Biologists Ltd 2009. Accepted 30 December 2008. We thank S. Crews, M. Frasch, E. Giniger, M. Krasnow, M. Levine, A. Michelson, the Bloomington Stock Center, and Harvard Exelixis Distribution Center for providing antibodies and fly stocks; Manfred Frasch and the Stathopoulos laboratory members, especially Sarah Payne, for discussions and comments on the manuscript; Leslie Dunipace for conducting the inverse PCR experiments; Smadar Ben-Tabou de-Leon for advice on the qPCR experiments; and Jagan Srinivasan for help with graphical representations. This work was supported by grants to A.S. from the NIH (R01 GM078542), the Searle Scholars Program, and the March of Dimes (Basil O'Conner Starter Scholar Award, 5-FY06-12). Deposited in PMC for release after 12 months. Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/136/5/739/DC1
Funders:
Funding AgencyGrant Number
NIHR01 GM078542
Searle Scholars ProgramUNSPECIFIED
March of Dimes5-FY06-12
Subject Keywords:Cell migration and differentiation, Drosophila, FGF signaling, Ligand-receptor interactions
Issue or Number:5
PubMed Central ID:PMC2685942
Record Number:CaltechAUTHORS:KADdev09
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:KADdev09
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:13327
Collection:CaltechAUTHORS
Deposited By: Archive Administrator
Deposited On:09 Feb 2009 19:12
Last Modified:24 Apr 2017 18:20

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