title: Regulation of Gonad Morphogenesis in Drosophila melanogaster by BTB Family Transcription Factors.
abstract: During embryogenesis, primordial germ cells (PGCs) and somatic gonadal precursor cells (SGPs) migrate and coalesce to form the early gonad. A failure of the PGCs and SGPs to form a gonad with the proper architecture not only affects germ cell development, but can also lead to infertility. Therefore, it is critical to identify the molecular mechanisms that function within both the PGCs and SGPs to promote gonad morphogenesis. We have characterized the phenotypes of two genes, longitudinals lacking (lola) and ribbon (rib), that are required for the coalescence and compaction of the embryonic gonad in Drosophila melanogaster. rib and lola are expressed in the SGPs of the developing gonad, and genetic interaction analysis suggests these proteins cooperate to regulate gonad development. Both genes encode proteins with DNA binding motifs and a conserved protein-protein interaction domain, known as the Broad complex, Tramtrack, Bric-à-brac (BTB) domain. Through molecular modeling and yeast-two hybrid studies, we demonstrate that Rib and Lola homo- and heterodimerize via their BTB domains. In addition, analysis of the colocalization of Rib and Lola with marks of transcriptional activation and repression on polytene chromosomes reveals that Rib and Lola colocalize with both repressive and activating marks and with each other. While previous studies have identified Rib and Lola targets in other tissues, we find that Rib and Lola are likely to function via different downstream targets in the gonad. These results suggest that Rib and Lola act as dual-function transcription factors to cooperatively regulate embryonic gonad morphogenesis.
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Diane
authors.initials: D
authors.lastname: Silva
authors.affiliation: Department of Chemistry and Biochemistry, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Kenneth W
authors.initials: KW
authors.lastname: Olsen
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Magdalena N
authors.initials: MN
authors.lastname: Bednarz
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Andrew
authors.initials: A
authors.lastname: Droste
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Christopher P
authors.initials: CP
authors.lastname: Lenkeit
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Edwin
authors.initials: E
authors.lastname: Chaharbakhshi
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Emily R
authors.initials: ER
authors.lastname: Temple-Wood
authors.affiliation: Department of Biology, Loyola University Chicago, Chicago, IL, United States of America.
authors.forename: Jennifer C
authors.initials: JC
authors.lastname: Jemc
mesh_terms: D000818:Animals; D003598:Cytoskeletal Proteins / Q000235:genetics / Q000378:metabolism*; D019281:Dimerization; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster / Q000378:metabolism*; D005854:Germ Cells / Q000166:cytology / Q000378:metabolism; D006066:Gonads / Q000166:cytology / Q000196:embryology*; D007150:Immunohistochemistry; D008565:Membrane Proteins / Q000378:metabolism; D008648:Mesoderm / Q000378:metabolism / Q000473:pathology; D008856:Microscopy, Fluorescence; D009024:Morphogenesis; D009154:Mutation; D020033:Protein Isoforms / Q000235:genetics / Q000378:metabolism; D012469:Salivary Glands / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*; D020798:Two-Hybrid System Techniques
chemical_list: D003598:Cytoskeletal Proteins; D029721:Drosophila Proteins; D008565:Membrane Proteins; D020033:Protein Isoforms; D014157:Transcription Factors; C064360:crb protein, Drosophila; C121765:lola protein, Drosophila; C115864:rib protein, Drosophila