Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation.
Tubulogenesis is an essential component of organ development, yet the underlying cellular mechanisms are poorly understood. We analyze here the formation of the Drosophila melanogaster cardiac lumen that arises from the migration and subsequent coalescence of bilateral rows of cardioblasts. Our study of cell behavior using three-dimensional and time-lapse imaging and the distribution of cell polarity markers reveals a new mechanism of tubulogenesis in which repulsion of prepatterned luminal domains with basal membrane properties and cell shape remodeling constitute the main driving forces. Furthermore, we identify a genetic pathway in which roundabout, slit, held out wings, and dystroglycan control cardiac lumen formation by establishing nonadherent luminal membranes and regulating cell shape changes. From these data we propose a model for D. melanogaster cardiac lumen formation, which differs, both at a cellular and molecular level, from current models of epithelial tubulogenesis. We suggest that this new example of tube formation may be helpful in studying vertebrate heart tube formation and primary vasculogenesis.
Medioni
Caroline
C
Institut de Biologie du Développement de Marseille-Luminy, Centre National de la Recherche Scientifique UMR 6216, Université de la Méditerranée, 13288 Marseille, Cedex 9, France.
Astier
Martine
M
Zmojdzian
Monika
M
Jagla
Krzysztof
K
Sémériva
Michel
M
D000818:Animals; D002448:Cell Adhesion / Q000235:genetics; D002454:Cell Differentiation / Q000235:genetics*; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism / Q000648:ultrastructure; D002465:Cell Movement / Q000235:genetics; D016764:Cell Polarity / Q000235:genetics; D048430:Cell Shape / Q000235:genetics; D029721:Drosophila Proteins / Q000235:genetics; D004331:Drosophila melanogaster / Q000196:embryology*; D049030:Dystroglycans / Q000235:genetics; D042783:Endothelial Cells / Q000166:cytology / Q000378:metabolism; D004847:Epithelial Cells / Q000166:cytology / Q000378:metabolism; D018507:Gene Expression Regulation, Developmental / Q000235:genetics*; D006321:Heart / Q000196:embryology*; D018919:Neovascularization, Physiologic / Q000235:genetics*; D009419:Nerve Tissue Proteins / Q000235:genetics; D009687:Nuclear Proteins / Q000235:genetics; D038081:Organogenesis / Q000235:genetics*; D016601:RNA-Binding Proteins / Q000235:genetics; D011971:Receptors, Immunologic / Q000235:genetics; D015398:Signal Transduction / Q000235:genetics; D013234:Stem Cells / Q000166:cytology / Q000378:metabolism; D000097905:Roundabout Proteins
D029721:Drosophila Proteins; D049030:Dystroglycans; D009419:Nerve Tissue Proteins; D009687:Nuclear Proteins; D016601:RNA-Binding Proteins; D011971:Receptors, Immunologic; D000097905:Roundabout Proteins; C106296:how protein, Drosophila; C066819:sli protein, Drosophila