Specification and spatial arrangement of cells in the germline stem cell niche of the Drosophila ovary depend on the Maf transcription factor Traffic jam

Abstract

Germline stem cells in the Drosophila ovary are maintained by a somatic niche. The niche is structurally and functionally complex and contains four cell types, the escort, cap, and terminal filament cells and the newly identified transition cell. We find that the large Maf transcription factor Traffic jam (Tj) is essential for determining niche cell fates and architecture, enabling each niche in the ovary to support a normal complement of 2–3 germline stem cells. In particular, we focused on the question of how cap cells form. Cap cells express Tj and are considered the key component of a mature germline stem cell niche. We conclude that Tj controls the specification of cap cells, as the complete loss of Tj function caused the development of additional terminal filament cells at the expense of cap cells, and terminal filament cells developed cap cell characteristics when induced to express Tj. Further, we propose that Tj controls the morphogenetic behavior of cap cells as they adopted the shape and spatial organization of terminal filament cells but otherwise appeared to retain their fate when Tj expression was only partially reduced. Our data indicate that Tj contributes to the establishment of germline stem cells by promoting the cap cell fate, and controls the stem cell-carrying capacity of the niche by regulating niche architecture. Analysis of the interactions between Tj and the Notch (N) pathway indicates that Tj and N have distinct functions in the cap cell specification program. We propose that formation of cap cells depends on the combined activities of Tj and the N pathway, with Tj promoting the cap cell fate by blocking the terminal filament cell fate, and N supporting cap cells by preventing the escort cell fate and/or controlling the number of cap cell precursors.

The Bric-à-Brac transcription factors are necessary for formation of functional germline stem cell niches through control ofdppexpression in theDrosophila melanogasterovary

“…CCs have been shown to be essential for GSC establishment and maintenance (Panchal et al, 2017;Song et al, 2007;Ward et al, 2006;Xie and Spradling, 2000). Our results here show that Bab proteins are necessary in niche cells of the larval ovary for GSC establishment.…”

“…Each GSC niche is composed of several types of somatic cells: a Terminal Filament (TF), which is a stack of about 8 flattened cells, approximately 5 Cap Cells (CCs) present at the base of the TF (Gilboa, 2015), one triangularly-shaped transition cell connecting the TF and CCs (Panchal et al, 2017) and posterior to CCs, the anterior Escort Cells (ECs) ( Fig 1A) (Wang and Page-McCaw, 2018). Both CCs and anterior ECs, are in direct contact with GSCs.…”

“…Individualization of each TF is accomplished by the migration of apical somatic cells (Inner Sheath Cells) between TFs ( Fig 1A) (Cohen et al, 2002).The number of TFs that form in the larval ovary determines the number of GSC niches at the adult stage (Bartoletti et al, 2012;Green et al, 2011;Sarikaya et al, 2012). At the base of each newlyformed TF, the anterior-most Intermingled Cells (ICs-somatic cells intermingled with Primordial Germ Cells, PGCs) differentiate into CCs adopting a cuboidal shape clearly distinguishable from that of the flat TF cells (Fig 1A and Fig 1B and B', yellow and green brackets, respectively) (Panchal et al, 2017;Zhu and Xie, 2003). At this stage, the transition cell is already distinguishable (Fig 1A and 1B', green arrowhead) (Panchal et al, 2017).…”

“…At the base of each newlyformed TF, the anterior-most Intermingled Cells (ICs-somatic cells intermingled with Primordial Germ Cells, PGCs) differentiate into CCs adopting a cuboidal shape clearly distinguishable from that of the flat TF cells (Fig 1A and Fig 1B and B', yellow and green brackets, respectively) (Panchal et al, 2017;Zhu and Xie, 2003). At this stage, the transition cell is already distinguishable (Fig 1A and 1B', green arrowhead) (Panchal et al, 2017).…”

“…As for the engrailed/invected locus, induction of clones homozygous for a deletion encompassing both genes identified a cell autonomous function for these genes in the correct alignment of TF cells during TF formation (Bolívar et al, 2006). CC specification has been shown to require the combined action of Notch signaling and the large Maf transcription factor Traffic Jam (Tj) (Gancz et al, 2011;Hsu and Drummond-Barbosa, 2011;Panchal et al, 2017;Song et al, 2007;Yatsenko and Shcherbata, 2018).…”