Hedgehog signaling establishes precursors for germline stem cell niches by regulating cell adhesion

Lai, Chun-Ming; Lin, Kun-Yang; Kao, Shih-Han; Chen, Yi-Ning; Huang, Fu; Hsu, Hwei-Jan

doi:10.1083/jcb.201610063

Cited by 35 publications

(71 citation statements)

References 59 publications

(80 reference statements)

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“…For example, cut-Gal4 labeled SH cells at LL3 gave rise to the epithelial sheath that surrounds each ovariole in the adult (Figure 3C, S3C) (Irizarry and Stathopoulos, 2015). As described previously, hh-Gal4 marked the TF continuously from the larva to the adult ( Figure 3C, S3C) (Lai et al, 2017). A CG3625-Gal4 line predominantly labeled CCs at LL3 ( Figure 3C, S3C, S4B) and their progeny gave rise to adult CCs and rarely ECs, which are thought to be IC descendants, suggesting common ancestry of both cell types (Song et al, 2007).…”

Section: Connecting Precursors To Adult Cell Types By Lineage Tracingsupporting

confidence: 71%

“…In contrast, assignment of somatic cell clusters to specific cell types was more difficult as many genes are expressed by several cell clusters. Nonetheless, we were able to assign SH fate based on stumps and ths expression (Irizarry and Stathopoulos, 2015), TF and CC fates on the basis of high hh expression in both (Lai et al, 2017) and alternate enrichment for en in TFs (Forbes et al, 1996) and tj in CC (Li et al, 2003) ( Figure 2B, S2CI-M).…”

Section: The Cell Types Of the Developing Ovarymentioning

confidence: 92%

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A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

Slaidina¹,

Banisch²,

Gupta³

et al. 2019

Preprint

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Addressing the complexity of organogenesis at a system-wide level requires a complete understanding of adult cell types, their origin and precursor relationships. The Drosophila ovary has been a model to study how coordinated stem cell units, germline and somatic follicle stem cells, maintain and renew an organ. However, lack of cell-type specific tools have limited our ability to study the origin of individual cell types and stem cell units. Here, we use a single cell RNA sequencing approach to uncover all known cell types of the developing ovary, reveal transcriptional signatures, and identify cell type specific markers for lineage tracing. Our study identifies a novel cell type corresponding to the elusive follicle stem cell precursors and predicts sub-types of known cell types. Altogether, we reveal a previously unanticipated complexity of the developing ovary, and provide a comprehensive resource for the systematic analysis of ovary morphogenesis.

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Section: Connecting Precursors To Adult Cell Types By Lineage Tracingsupporting

confidence: 71%

Section: The Cell Types Of the Developing Ovarymentioning

confidence: 92%

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

Slaidina¹,

Banisch²,

Gupta³

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…In addition to genes that regulate basic cellular processes, the core module is enriched for the 425 core components of the Hh signalling cascade, namely patched (ptc), smoothened (smo) and 426 costa (cos) (Lee et al, 2016). However, we find that the loss of Hh ligand, which is expressed in 427 the TF cells in the developing larval ovary (Lai et al, 2017), does not significantly affect either 428 ovariole number or egg laying. Though surprising, ligand-independent activation of Hedgehog 429 signalling has been observed before.…”

mentioning

confidence: 79%

Topology-driven protein-protein interaction network analysis detects genetic sub-networks regulating reproductive capacity

Kumar

Blondel

Extavour

2019

Preprint

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10Understanding the genetic regulation of organ structure is a fundamental problem in 11 developmental biology. Here, we use egg-producing structures of insect ovaries, called 12 ovarioles, to deduce systems-level gene regulatory relationships from quantitative functional 13 genetic analysis. We previously showed that Hippo signalling, a conserved regulator of animal 14 organ size, regulates ovariole number in Drosophila melanogaster. To comprehensively 15 determine how Hippo signalling interacts with other pathways in this regulation, we screened all 16 known signalling pathway genes, and identified Hpo-dependent and Hpo-independent signalling 17 requirements. Network analysis of known protein-protein interactions among screen results 18 identified independent gene regulatory modules regulating one or both of ovariole number and 19 egg laying. These modules predict involvement of previously uncharacterised genes with higher 20 accuracy than the original candidate screen. This shows that network analysis combining 21 functional genetic and large-scale interaction data can predict function of novel genes regulating 22 development. 23 24

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“…Ovarioles are established during larval development by the differentiation of intermingled cells into either terminal filament cells or basal stalk cells. These cell fate specifications are controlled by hippo (Sarikaya and Extavour, 2015) and hedgehog signaling (Lai et al, 2017), and the process by which the cells coalesce into rudimentary ovarioles requires cell migration, intercalation (Godt and Laski, 1995;Li et al, 2003), and actomyosin contractility (Vlachos et al, 2015). Interestingly, several of these processes are influenced by pH dynamics in other contexts.…”

Section: Discussionmentioning

confidence: 99%

Drosophila anion exchanger 2 is required for proper ovary development and oogenesis

Benitez¹,

Tatapudy²,

Barber³

et al. 2018

Preprint

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Understanding how cell fate decisions are regulated is a central question in stem cell biology. Recent studies have demonstrated that intracellular pH (pHi) dynamics contribute to this process. Indeed, the pHi of cells within a tissue is not simply a consequence of chemical reactions in the cytoplasm and other cellular activity, but is actively maintained at a specific setpoint in each cell type. We found previously that the pHi of cells in the follicle stem cell (FSC) lineage in the Drosophila ovary increases progressively during differentiation from an average of 6.8 in the FSCs, to 7.0 in newly produced daughter cells, to 7.3 in more differentiated cells. Two major regulators of pHi in this lineage are Drosophila sodium-proton exchanger 2 (dNhe2) and a previously uncharacterized gene, CG8177, that is homologous to mammalian anion exchanger 2 (AE2). Based on this homology, we named the gene ae2. Here, we generated null alleles of ae2 and found that homozygous mutant flies are viable but have severe defects in ovary development and adult oogenesis. Specifically, we find that ae2 null flies have smaller ovaries, reduced fertility, and impaired follicle formation. In addition, we find that the follicle formation defect can be suppressed by a decrease in dNhe2 copy number and enhanced by the overexpression of dNhe2, suggesting that this phenotype is due to the dysregulation of pHi. These findings support the emerging idea that pHi dynamics regulate cell fate decisions and our studies provide new genetic tools to investigate the mechanisms by which this occurs.

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Hedgehog signaling establishes precursors for germline stem cell niches by regulating cell adhesion

Cited by 35 publications

References 59 publications

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

A single cell atlas of the developingDrosophilaovary identifies follicle stem cell progenitors

Topology-driven protein-protein interaction network analysis detects genetic sub-networks regulating reproductive capacity

Drosophila anion exchanger 2 is required for proper ovary development and oogenesis

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