Preferential adhesion mediated by Hibris and Roughest regulates morphogenesis and patterning in the Drosophila eye.
Cell adhesion is essential for morphogenesis; however, the mechanisms by which cell adhesion coordinates precisely regulated morphogenesis are poorly understood. Here we analyze the morphogenetic processes that organize the interommatidial precursor cells (IPCs) of the Drosophila pupal eye. We demonstrate that the Drosophila immunoglobulin superfamily members Hibris and Roughest are essential for IPC morphogenesis in the eye. The two loci are expressed in complementary cell types, and Hibris and Roughest proteins bind directly in vivo. Primary pigment cells employ Hibris to function as organizers in this process; IPCs minimize contacts with neighboring IPCs and utilize Roughest to maximize contacts with primaries. In addition, we provide evidence that interactions between Hibris and Roughest promote junction formation and that levels of Roughest in individual cells determine their capacity for competition. Our results demonstrate that preferential adhesion mediated by heterophilic interacting cell-adhesion molecules can create a precise pattern by minimizing surface free energy.
Bao
Sujin
S
Department of Molecular Biology and Pharmacology, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, Missouri 63110, USA.
Cagan
Ross
R
D000818:Animals; D015153:Blotting, Western / Q000379:methods; D019521:Body Patterning / Q000502:physiology*; D002448:Cell Adhesion / Q000502:physiology; D015816:Cell Adhesion Molecules, Neuronal / Q000235:genetics / Q000378:metabolism*; D002460:Cell Line; D004330:Drosophila; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004625:Embryo, Nonmammalian; D005123:Eye / Q000166:cytology / Q000196:embryology* / Q000378:metabolism*; D005136:Eye Proteins / Q000235:genetics / Q000378:metabolism*; D018507:Gene Expression Regulation, Developmental / Q000502:physiology; D005838:Genotype; D047468:Immunoprecipitation / Q000379:methods; D017403:In Situ Hybridization / Q000379:methods; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism*; D008954:Models, Biological; D009024:Morphogenesis / Q000502:physiology*; D012333:RNA, Messenger / Q000096:biosynthesis; D020133:Reverse Transcriptase Polymerase Chain Reaction / Q000379:methods; D013997:Time Factors; D014162:Transfection / Q000379:methods; D014170:Transformation, Genetic / Q000502:physiology
D015816:Cell Adhesion Molecules, Neuronal; D029721:Drosophila Proteins; D005136:Eye Proteins; D008565:Membrane Proteins; D012333:RNA, Messenger; C442230:hbs protein, Drosophila; C085209:rst protein, Drosophila