Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos.
Mechanical deformations associated with embryonic morphogenetic movements have been suggested to actively participate in the signaling cascades regulating developmental gene expression. Here we develop an appropriate experimental approach to ascertain the existence and the physiological relevance of this phenomenon. By combining the use of magnetic tweezers with in vivo laser ablation, we locally control physiologically relevant deformations in wild-type Drosophila embryonic tissues. We demonstrate that the deformations caused by germ band extension upregulate Twist expression in the stomodeal primordium. We find that stomodeal compression triggers Src42A-dependent nuclear translocation of Armadillo/beta-catenin, which is required for Twist mechanical induction in the stomodeum. Finally, stomodeal-specific RNAi-mediated silencing of Twist during compression impairs the differentiation of midgut cells, resulting in larval lethality. These experiments show that mechanically induced Twist upregulation in stomodeal cells is necessary for subsequent midgut differentiation.
Desprat
Nicolas
N
Mechanics and Genetics of Embryonic and Tumoral Development Group, UMR168 CNRS, Institut Curie, 11 rue Pierre et Marie Curie, F-75005, Paris, France.
Supatto
Willy
W
Mechanics and Genetics of Embryonic and Tumoral Development Group, UMR168 CNRS, Institut Curie, 11 rue Pierre et Marie Curie, F-75005, Paris, France; Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS and INSERM U 696, 91128 Palaiseau, France.
Pouille
Philippe-Alexandre
PA
Mechanics and Genetics of Embryonic and Tumoral Development Group, UMR168 CNRS, Institut Curie, 11 rue Pierre et Marie Curie, F-75005, Paris, France.
Beaurepaire
Emmanuel
E
Laboratory for Optics and Biosciences, Ecole Polytechnique, CNRS and INSERM U 696, 91128 Palaiseau, France.
Farge
Emmanuel
E
Mechanics and Genetics of Embryonic and Tumoral Development Group, UMR168 CNRS, Institut Curie, 11 rue Pierre et Marie Curie, F-75005, Paris, France. Electronic address: efarge@curie.fr.
D021581:Active Transport, Cell Nucleus / Q000502:physiology; D000818:Animals; D051186:Armadillo Domain Proteins / Q000235:genetics / Q000378:metabolism; D002454:Cell Differentiation / Q000502:physiology*; D004064:Digestive System / Q000196:embryology / Q000378:metabolism; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000033:anatomy & histology* / Q000196:embryology* / Q000235:genetics / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000502:physiology; D054262:Gastrulation; D018507:Gene Expression Regulation, Developmental; D009024:Morphogenesis; D016392:Proto-Oncogene Proteins pp60(c-src) / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction / Q000502:physiology; D013314:Stress, Mechanical; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D051879:Twist-Related Protein 1 / Q000235:genetics / Q000378:metabolism*
C495305:ARM protein, Drosophila; D051186:Armadillo Domain Proteins; D029721:Drosophila Proteins; D014157:Transcription Factors; C497753:Twi protein, Drosophila; D051879:Twist-Related Protein 1; D016392:Proto-Oncogene Proteins pp60(c-src); C100382:Src42A protein, Drosophila