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

Development

Volumn 136, Issue 5, 2009, Pages 739-747

  Kadam, Snehalata ^a   McMahon, Amy ^a   Tzou, Phoebe ^a   Stathopoulos, Angelike ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cell migration and differentiation; Drosophila; FGF signaling; Ligand receptor interactions

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; LIGAND; PROTEIN BRANCHLESS; PROTEIN PYRAMUS; PROTEIN THISBE; TRANSCRIPTION FACTOR GAL4; UNCLASSIFIED DRUG; BRANCHLESS PROTEIN, DROSOPHILA; BREATHLESS PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HEARTLESS PROTEIN, DROSOPHILA; PROTEIN TYROSINE KINASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTION; CELL SPREADING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE INSERTION; GENE LOCATION; GENE SEQUENCE; MESODERM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; THISBE; VERTEBRATA;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; LIGANDS; MESODERM; MODELS, BIOLOGICAL; MUTATION; PROTEIN-TYROSINE KINASES; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 65549142248     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.027904     Document Type: Article

References (41)

1. Ahmad, S. M. and Baker, B. S. (2002). Sex-specific deployment of FGF signaling in Drosophila recruits mesodermal cells into the male genital imaginal disc. Cell 109, 651-661.
2. Beiman, M., Shilo, B. Z. and Volk, T. (1996). Heartless, a Drosophila FGF receptor homolog, is essential for cell migration and establishment of several mesodermal lineages. Genes Dev. 10, 2993-3002.
3. Birnbaum, D., Popovici, C. and Roubin, R. (2005). A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Dev. Dyn. 232, 247-255.
4. Carmena, A., Gisselbrecht, S., Harrison, J., Jimenez, F. and Michelson, A. M. (1998). Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev. 12, 3910-3922.
5. Chen, L. and Deng, C. X. (2005). Roles of FGF signaling in skeletal development and human genetic diseases. Front. Biosci. 10, 1961-1976.
6. Coumoul, X. and Deng, C. X. (2003). Roles of FGF receptors in mammalian development and congenital diseases. Birth Defects Res. C Embryo Today 69, 286-304.
7. Dossenbach, C., Rock, S. and Affolter, M. (2001). Specificity of FGF signaling in cell migration in Drosophila. Development 128, 4563-4572.
8. Eswarakumar, V. P., Lax, I. and Schlessinger, J. (2005). Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16, 139-149.
9. Frasch, M. (1995). Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 374, 464-467.
10. Frasch, M. (1999). Intersecting signalling and transcriptional pathways in Drosophila heart specification. Semin. Cell Dev. Biol. 10, 61-71.
11. Gabay, L., Seger, R. and Shilo, B. Z. (1997). MAP kinase in situ activation atlas during Drosophila embryogenesis. Development 124, 3535-3541.
12. Gisselbrecht, S., Skeath, J. B., Doe, C. Q. and Michelson, A. M. (1996). heartless encodes a fibroblast growth factor receptor (DFR1/ DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo. Genes Dev. 10, 3003-3017.
13. Gryzik, T. and Muller, H. A. (2004). FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl and are required for mesoderm migration in the Drosophila gastrula. Curr. Biol. 14, 659-667.
14. Huang, P. and Stern, M. J. (2005). FGF signaling in flies and worms: more and more relevant to vertebrate biology. Cytokine Growth Factor Rev. 16, 151-158.
15. Ishimoto, H., Takahashi, K., Ueda, R. and Tanimura, T. (2005). G-protein gamma subunit 1 is required for sugar reception in Drosophila. EMBO J. 24, 3259-3265.
16. Kosman, D., Mizutani, C. M., Lemons, D., Cox, W. G., McGinnis, W. and Bier, E. (2004). Multiplex detection of RNA expression in Drosophila embryos. Science 305, 846.
17. Lehmann, R. and Tautz, D. (1994). In situ hybridization to RNA. Methods Cell Biol. 44, 575-598.
18. Leptin, M. and Grunewald, B. (1990). Cell shape changes during gastrulation in Drosophila. Development 110, 73-84.
19. Mariani, F. V., Ahn, C. P. and Martin, G. R. (2008). Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 453, 401-405.
20. McMahon, A., Supatto, W., Fraser, S. E. and Stathopoulos, A. (2008). Dynamic analyses of Drosophila gastrulation provide insights into collective cell migration. Science 322, 1546-1550.
21. Michelson, A. M., Gisselbrecht, S., Zhou, Y., Baek, K. H. and Buff, E. M. (1998). Dual functions of the heartless fibroblast growth factor receptor in development of the Drosophila embryonic mesoderm. Dev. Genet. 22, 212-229.
22. Ornitz, D. M. (2005). FGF signaling in the developing endochondral skeleton. Cytokine Growth Factor Rev. 16, 205-213.
23. Ornitz, D. M. and Itoh, N. (2001). Fibroblast growth factors. Genome Biol. 2, reviews3005.1-3005.12.
24. Ornitz, D. M., Xu, J., Colvin, J. S., McEwen, D. G., MacArthur, C. A., Coulier, F., Gao, G. and Goldfarb, M. (1996). Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271, 15292-15297.
25. Preston, C. R., Sved, J. A. and Engels, W. R. (1996). Flanking duplications and deletions associated with P-induced male recombination in Drosophila. Genetics 144, 1623-1638.
26. Rentzsch, F., Fritzenwanker, J. H., Scholz, C. B. and Technau, U. (2008). FGF signalling controls formation of the apical sensory organ in the cnidarian Nematostella vectensis. Development 135, 1761-1769.
27. Rottinger, E., Saudemont, A., Duboc, V., Besnardeau, L., McClay, D. and Lepage, T. (2008). FGF signals guide migration of mesenchymal cells, control skeletal morphogenesis and regulate gastrulation during sea urchin development. Development 135, 353-365.
28. San Martin, B. and Bate, M. (2001). Hindgut visceral mesoderm requires an ectodermal template for normal development in Drosophila. Development 128, 233-242.
29. Sato, M. and Kornberg, T. B. (2002). FGF is an essential mitogen and chemoattractant for the air sacs of the drosophila tracheal system. Dev. Cell 3, 195-207.
30. Shishido, E., Ono, N., Kojima, T. and Saigo, K. (1997). Requirements of DFR1/Heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. Development 124, 2119-2128.
31. Spralding, A. C. and Rubin, G. M. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
32. Stathopoulos, A., Tam, B., Ronshaugen, M., Frasch, M. and Levine, M. (2004). pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. Genes Dev. 18, 687-699.
33. Sutherland, D., Samakovlis, C. and Krasnow, M. A. (1996). branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87, 1091-1101.
34. Szebenyi, G. and Fallon, J. F. (1999). Fibroblast growth factors as multifunctional signaling factors. Int. Rev. Cytol. 185, 45-106.
35. Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L. et al. (2004). A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287.
36. Thisse, B. and Thisse, C. (2005). Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev. Biol. 287, 390-402.
37. Wilkie, A. O. (2005). Bad bones, absent smell, selfish testes: the pleiotropic consequences of human FGF receptor mutations. Cytokine Growth Factor Rev. 16, 187-203.
38. Wilson, R., Vogelsang, E. and Leptin, M. (2005). FGF signalling and the mechanism of mesoderm spreading in Drosophila embryos. Development 132, 491-501.
39. Xiao, H., Hrdlicka, L. A. and Nambu, J. R. (1996). Alternate functions of the single-minded and rhomboid genes in development of the Drosophila ventral neuroectoderm. Mech. Dev. 58, 65-74.
40. Yang, X., Dormann, D., Munsterberg, A. E. and Weijer, C. J. (2002). Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev. Cell 3, 425-437.
41. Zhang, X., Ibrahimi, O. A., Olsen, S. K., Umemori, H., Mohammadi, M. and Ornitz, D. M. (2006). Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15694-15700.