Traffic jam regulates the function of the ovarian germline stem cell progeny differentiation niche during pre-adult stage in Drosophila

doi:10.1038/s41598-019-45317-6

. 2019 Jul 12;9(1):10124.

doi: 10.1038/s41598-019-45317-6.

Traffic jam regulates the function of the ovarian germline stem cell progeny differentiation niche during pre-adult stage in Drosophila

Mengjie Li¹, Xiaolong Hu¹, Shu Zhang², Margaret S Ho³, Geng Wu⁴, Lei Zhang^{5

6}

Affiliations

¹ State Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, The Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University, Shanghai, 200240, China.
² School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China.
³ School of Life Science and Technology, Shanghai Tech University, Shanghai, 201210, China.
⁴ State Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, The Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University, Shanghai, 200240, China. geng.wu@sjtu.edu.cn.
⁵ State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Innovation Center for Cell Signaling Network, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai, 200031, China. rayzhang@sibcb.ac.cn.
⁶ School of Life Science and Technology, Shanghai Tech University, Shanghai, 201210, China. rayzhang@sibcb.ac.cn.

PMID: 31300663
PMCID: PMC6626045
DOI: 10.1038/s41598-019-45317-6

Traffic jam regulates the function of the ovarian germline stem cell progeny differentiation niche during pre-adult stage in Drosophila

Mengjie Li et al. Sci Rep. 2019.

. 2019 Jul 12;9(1):10124.

doi: 10.1038/s41598-019-45317-6.

Authors

Mengjie Li¹, Xiaolong Hu¹, Shu Zhang², Margaret S Ho³, Geng Wu⁴, Lei Zhang^{5

6}

Affiliations

¹ State Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, The Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University, Shanghai, 200240, China.
² School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China.
³ School of Life Science and Technology, Shanghai Tech University, Shanghai, 201210, China.
⁴ State Key Laboratory of Microbial Metabolism, School of Life Sciences & Biotechnology, The Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University, Shanghai, 200240, China. geng.wu@sjtu.edu.cn.
⁵ State Key Laboratory of Cell Biology, CAS Center for Excellence in Molecular Cell Science, Innovation Center for Cell Signaling Network, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai, 200031, China. rayzhang@sibcb.ac.cn.
⁶ School of Life Science and Technology, Shanghai Tech University, Shanghai, 201210, China. rayzhang@sibcb.ac.cn.

PMID: 31300663
PMCID: PMC6626045
DOI: 10.1038/s41598-019-45317-6

Abstract

Stem cell self-renewal and the daughter cell differentiation are tightly regulated by the respective niches, which produce extrinsic cues to support the proper development. In Drosophila ovary, Dpp is secreted from germline stem cell (GSC) niche and activates the BMP signaling in GSCs for their self-renewal. Escort cells (ECs) in differentiation niche restrict Dpp outside the GSC niche and extend protrusions to help with proper differentiation of the GSC daughter cells. Here we provide evidence that loss of large Maf transcriptional factor Traffic jam (Tj) blocks GSC progeny differentiation. Spatio-temporal specific knockdown experiments indicate that Tj is required in pre-adult EC lineage for germline differentiation control. Further molecular and genetic analyses suggest that the defective germline differentiation caused by tj-depletion is partly attributed to the elevated dpp in the differentiation niche. Moreover, our study reveals that tj-depletion induces ectopic En expression outside the GSC niche, which contributes to the upregulated dpp expression in ECs as well as GSC progeny differentiation defect. Alternatively, loss of EC protrusions and decreased EC number elicited by tj-depletion may also partially contribute to the germline differentiation defect. Collectively, our findings suggest that Tj in ECs regulates germline differentiation by controlling the differentiation niche characteristics.

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Conflict of interest statement

The authors declare no competing interests.

Figures

**Figure 1**
Tj is required for proper GSC progeny differentiation. **(a–d’)** Gonads are stained for α-spectrin (red), to mark spectrosomes and fusomes, Vasa (green), to mark germline, and Zfh-1 (blue), to mark somatic cells. **(a-b’)** White pre-pupal (WPP) gonads are examined. The control group **(a,a’)** contains branched fusomes, as indicated by white arrow. tj mutant gonad **(b,b’)** lacks branched fusome-containing-germline cyst. White dashed lines indicate TF stacks. **(c–d’)** Early pupal (EP) gonads are examined. The control group **(c,c’)** displays well-organized primordial ovarioles. White arrows indicate branched fusome-containing differentiating cysts. The tj mutant **(d,d’)** displays few differentiating germline cysts. White arrowheads indicate round fusome-containing germ cells. Yellow dash lines indicate TFs and white broken ovals indicate CpCs. **(e,f)** Germaria from newly eclosed flies (<1-day old) are stained for α-spectrin (red), to mark spectrosomes and fusomes, Vasa (green), to mark germline. The control group **(e)** shows normal number of CB. The *C587* > *tj RNAi-1* **(f)** group displays excess UGCs. **(g,h)** Mosaic germaria with MARCM clones are stained for α-spectrin (red), to mark spectrosomes and fusomes, GFP (green), to mark the clone cells positively. Germaria from newly eclosed flies (<1-day old) are examined. The control group (with *FRT40A* clone) **(g)** exhibits normal in germline differentiation. The tj mutant group (with tj^PL3, *FRT40A* clone) **(h)** exhibits more spectrosome-containing cells. **(i)** Graph shows the UGC number in germaria of indicated genotypes. Error bars are shown as Means ± S.D. of each genotype. Scale bar for (**a–d’**) is shown in each panel. Scale bar for (**e–h**) is shown in panel (e). Anterior is up in (**a–d**) and left in (**e–h**).

**Figure 2**
GSC progeny differentiation defects due to tj KD predominantly arise in EC lineage during pre-adult stage. **(a–d)** Germaria from *C587*^ts > *tj RNAi-1* flies are stained for α-spectrin (red), to mark spectrosomes and fusomes, Vasa (green), to mark germline. *C587*^ts-driven other tj RNAi lines present similar phenotype. **(a,b)** Germaria from newly eclosed flies (<1-day old), which are raised at 18 °C up to LL3 **(a)** or EP stage (b) and then maintained at 29 °C till eclosion, display UGC accumulation. **(c,d**) Germaria from 10-day-old females, which are raised at 18 °C up to eclosion and then shifted to 29 °C **(c)** or still maintained at 18 °C (d), present normal procedure of germline differentiation. (**e,f**) Graph shows the UGC number in germaria of indicated genotypes. Error bars are shown as Means ± S.D. of each genotype. Scale bar is shown in panel (a). Anterior is always to the left.

**Figure 3**
Loss of Tj in ECs results in expanded BMP signaling. **(a–c,k** & m) Germaria are stained for pMad (green), to indicate the BMP pathway activity, α-spectrin (red), to mark spectrosomes and fusomes. In germaria from newly eclosed flies (<1-day old), the control group **(a)** displays dense pMad staining in GSCs. The *C587* > *tj RNAi-1* **(b)** and *C587* > *tj RNAi-2* **(c)** groups display excess UGCs negative for pMad. **(d–f, l & n)** Germaria are stained for α-spectrin (red) to mark spectrosomes and fusomes. The *bamP-GFP/+* (green) is introduced to indicate the transcriptional activity of *bam*. In germaria from newly eclosed flies (<1-day old), the control group **(d)** displays the absence of *bamP-GFP* in GSCs but upregulation in CBs. The *C587* > *tj RNAi-1* **(e)** and *C587* > *tj RNAi-2* **(f)** groups display *bamP-GFP-*positive UGCs. **(g–i’)** Germaria from newly eclosed flies (<1-day old) are stained for α-spectrin (red), to mark spectrosomes and fusomes. The *dad-lacZ*/+ is introduced to indicate BMP pathway activity (marked by β-gal, green). The control group **(g,g’)** presents high level of *dad-lacZ* activity in GSCs and intermediate CBs. The *C587* > *tj RNAi-1* **(h,h’)** and *C587* > *tj RNAi-2* **(i,i’)** groups present *dad-lacZ*-positive UGCs outside the GSC niche. **(j)** Graph shows the percentage of germaria that contain the indicated number of *dad-lacZ*-positive germ cells for each genotype. **(k,l)** *C587*^ts > *UAS-dpp* flies are maintained at 18 °C up to eclosion and then shifted to 29 °C for 2–3 days before dissection. The germaria are full of pMad-positive UGCs **(k)** and *bamP-GFP-*negative UGCs **(l)**. **(m,n)** Germaria from newly eclosed flies (<1-day old) of *C587*^ts > *UAS-dpp*, which are maintained at 18 °C up to EP stage and then maintained at 25 °C till eclosion, exhibit excess pMad-negative UGCs **(m)** and *bamP-GFP*-positive UGCs **(n)**. Scale bar is shown in panel (a). Anterior is always to the left.

**Figure 4**
Ectopic *dpp* partly contributes to the germline differentiation defect in *C587*-mediated tj KD germaria. **(a)** Result of qRT-PCR shows that the *dpp* mRNA is increased by 1.53 ± 0.06 fold in tj > *tj RNAi-1* ovaries and 2.66 ± 0.14 fold in that of tj > *tj RNAi-2*. Data are shown as Means ± S.D. of three independent experiments. (**b–d’)** Germaria from newly eclosed flies (<1-day old) are stained for Vasa (red), to mark germline. The *dpp2.0-lacZ*/+ is introduced to indicate *dpp* transcription activity (marked by β-gal, green). DAPI is blue. Yellow dashed lines indicate TFs. White broken ovals indicate CpC clusters. The control group **(b,b’)** exhibits β-gal staining only in cap cells. The *C587* > *tj RNAi-1* **(c,c’)** and *C587* > *tj RNAi-2* **(d,d’)** groups show ectopic *dpp2.0-lacZ* activity in some ECs, as indicated by white arrows. **(e–n)** Germaria from newly eclosed flies (<1-day old) are stained for α-spectrin (red), to mark spectrosomes and fusomes, Vasa (green) to mark germline. The *C587* > *tj RNAi-1* group **(e)** exhibits excess UGCs. The *C587* > *tj RNAi-1; dppe90*/+ **(f)**, *C587* > *tj RNAi-1; dpp*^hr4/+ **(g)**, *C587* > *tj RNAi-1* + *dpp RNAi-1* **(h)** and *C587* > *tj RNAi-1* + *dpp RNAi-2* **(i)** groups exhibit reduced UGC accumulation. **(j–n)** The *C587* > *tj RNAi-2* **(j)** group exhibits excess UGCs. The *C587* > *tj RNAi-2; dpp*^e90/+ **(k)**, *C587* > *tj RNAi-2; dpp*^hr4/+ **(l)**, *C587* > *tj RNAi-2* + *dpp RNAi-1* **(m)** and *C587* > *tj RNAi-2* + *dpp RNAi-2* **(n)** groups exhibit reduced UGC accumulation. **(o,p)** Graphs show the percentage of germaria that contain the indicated number of UGC for each genotype. Scale bar is shown in panel (b). Anterior is always to the left.

**Figure 5**
Engrailed misregulation partly contributes to the germline differentiation defect in tj KD ECs. (**a–c’**) Germaria from newly eclosed flies (<1-day old) are stained for Vasa (green), to mark germline, En (red), to mark TF and CpCs. Yellow dashed lines indicate TFs and white broken ovals indicate CpC clusters. The control group (a,**a’)** displays specific En expression in TF and CpCs. The *C587* > *tj RNAi-1* **(b,b’)** and *C587* > *tj RNAi-2* **(c,c’)** group show ectopic En staining in some ECs, as indicated by white arrowheads. (d–k) Germaria from newly eclosed flies (<1-day old) are stained for α-spectrin (red), to mark spectrosomes and fusomes, Vasa (green), to mark germline. The *C587* > *tj RNAi-1; en*⁴/+ **(d)**, *C587* > *tj RNAi-1; en*⁷/+ **(e)**, *C587* > *tj RNAi-1* + *en RNAi-1* **(f)** and *C587* > *tj RNAi-1* + *en RNAi-2* **(g)** groups exhibit a reduced UGCs accumulation, compared with Fig. 4e. The *C587* > *tj RNAi-2; en*⁴/+ **(h)**, *C587* > *tj RNAi-2; en*⁷/+ **(i)**, *C587* > *tj RNAi-2* + *en RNAi-1* **(j)** and *C587* > *tj RNAi-2* + *en RNAi-2* **(k)** groups exhibit a reduced UGCs accumulation, compared with Fig. 4j. (l, m) Graphs show the percentage of germaria that contain the indicated number of UGC for each genotype. Scale bar is shown in panel (a). Anterior is always to the left.

**Figure 6**
Tj represses *dpp* expression in ECs partially through En. **(a–f’**) Germaria from newly eclosed flies (<1-day old) are stained for Vasa (red) to mark germline. The *dpp2.0-lacZ*/+ is introduced to indicate *dpp* transcription activity (marked by β-gal, green). DAPI is blue. White broken ovals indicate CpC clusters. The *C587* > *tj RNAi-1; en*⁴/+ **(a,a’)**, *C587* > *tj RNAi-1* + *en RNAi-1* **(b,b’)** and *C587* > *tj RNAi-1* + *en RNAi-2* **(c,c’)** groups exhibit relieved expression of *dpp2.0-lacZ* in ECs, compared with Fig. 4(c,c’). The *C587* > *tj RNAi-2; en*⁴/+ **(d,d’)**, *C587* > *tj RNAi-2* + *en RNAi-1* **(e,e’)** and *C587* > *tj RNAi-2* + *en RNAi-2* **(f,f’)** groups exhibit relieved expression of *dpp2.0-lacZ* in ECs, compared with Fig. 4(d,d’). **(g,h)** Graphs show the percentage of germaria that contain a given number of EC with ectopic *dpp2.0-lacZ* expression of indicated genotypes.

**Figure 7**
En acts upstream of Dpp. **(a–f’)** Germaria from newly eclosed flies (<1-day old) are stained for Vasa (green), to mark germline, En (red) to mark TF and CpCs. Yellow dashed lines indicate TFs and white broken ovals indicate CpC clusters. The *C587* > *tj RNAi-1; dpp*^e90/+ **(a,a’)**, *C587* > *tj RNAi-1; dpp*^hr4/+ **(b,b’)**, *C587* > *tj RNAi-1* + *dpp RNAi-1* **(c,c’)***, C587* > *tj RNAi-2; dpp*^e90/+ **(d,d’)**, *C587* > *tj RNAi-2; dpp*^hr4/+ **(e,e’)** and *C587* > *tj RNAi-2* + *dpp RNAi-1* **(f,f’)** groups exhibit ectopic En expression in ECs, as indicated by white arrowheads. **(g,h)** Graphs show the percentage of germaria containing ectopic En expression in ECs of indicated genotypes. Scale bar is shown in panel (a). Anterior is always to the left.

**Figure 8**
Tj controls EC protrusions independent of En. **(a–l)** Germaria from newly born (<1-day old) females are stained for α-spectrin (red) to mark spectrosomes and fusomes. *C587-*driven *UAS-mCD8-GFP* (green) visualizes the EC protrusions. **(a–f)** The *hs-bam*/+ is introduced. (**a–c**) Ovaries from females without heat shock treatment are examined. The control group **(a)** displays normal protrusions extended by ECs. White arrows indicate the EC protrusions separating developing germline cysts. The *C587* > *tj RNAi-1* + *hs-bam*/+ **(b)** and *C587* > *tj RNAi-2* + *hs-bam*/+ **(c)** groups exhibit abnormal EC morphology as well as UGCs accumulation. White arrowheads indicate the absence of EC protrusions. **(d–f)** Ovaries from females with heat shock treatment during pupal stage are examined. The control group **(d)** exhibits branched fusome-containing germline closed to niche cells. White arrows indicate the protrusions extended by ECs. The *C587* > *tj RNAi-1* + *hs-bam*/+ **(e)** or *C587* > *tj RNAi-2* + *hs-bam*/+ **(f)** groups exhibit no UGCs in the germaria. White arrowheads indicate the absence of EC protrusions. The *C587* > *tj RNAi-1* **(g)**, *C587* > *tj RNAi-1* + *en RNAi-1* **(h)**, *C587* > *tj RNAi-1* + *en RNAi-2* **(i)**, *C587* > *tj RNAi-2* **(j)**, *C587* > *tj RNAi-2* + *en RNAi-1* **(k)** and *C587* > *tj RNAi-2* + *en RNAi-2* **(l)** groups display abnormal EC protrusions. White arrows indicate the absence of EC protrusions. **(m,n)** The graph shows the percentage of germaria that contain EC with abnormal protrusions of indicated genotypes. Scale bar is showed in panel (a). Anterior is always to the left.

**Figure 9**
Tj regulates EC number independent of En. **(a–c,e–h)** Germaria from newly born (<1-day old) females are stained for α-spectrin (red), to mark spectrosomes and fusomes. The *PZ1444*/+ is introduced to indicate ECs and CpC (marked by β-gal, green). White broken ovals indicate CpC clusters. The control group **(a)** exhibits a normal EC number. The *C587* > *tj RNAi-1* **(b)** or *C587* > *tj RNAi-2* **(c)** groups exhibit a reduction of EC number. **(d)** Graph shows the ECs number in germaria of indicated genotypes. Error bars are shown as Means ± S.D. of each genotype. The *C587* > *tj RNAi-1* + *en RNAi-1* **(e)** and *C587* > *tj RNAi-1* + *en RNAi-2* **(f)** groups show a similar EC number to *C587* > *tj RNAi-1* **(b)**. The *C587* > *tj RNAi-2* + *en RNAi-1* **(g)** *and C587* > *tj RNAi-2* + *en RNAi-2* **(h)** groups show a similar EC number to *C587* > *tj RNAi-2* **(c)**. **(i,j)** Graphs show the ECs number in germaria of indicated genotypes. Error bars are shown as Means ± S.D. of each genotype. Scale bar is showed in panel (a). Anterior is always to the left.

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References

1. Lin H, Spradling AC. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol. 1993;159:140–152. doi: 10.1006/dbio.1993.1228. - DOI - PubMed
1. Kirilly D, Xie T. The Drosophila ovary: an active stem cell community. Cell Res. 2007;17:15–25. doi: 10.1038/sj.cr.7310123. - DOI - PubMed
1. Liu Z, et al. Coordinated niche-associated signals promote germline homeostasis in the Drosophila ovary. J Cell Biol. 2015;211:469–484. doi: 10.1083/jcb.201503033. - DOI - PMC - PubMed
1. Chen D, McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol. 2003;13:1786–1791. doi: 10.1016/j.cub.2003.09.033. - DOI - PubMed
1. Chen D, McKearin DM. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 2003;130:1159–1170. doi: 10.1242/dev.00325. - DOI - PubMed

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[1] Lin H, Spradling AC. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol. 1993;159:140–152. doi: 10.1006/dbio.1993.1228. - DOI - PubMed

[2] Lin H, Spradling AC. Germline stem cell division and egg chamber development in transplanted Drosophila germaria. Dev Biol. 1993;159:140–152. doi: 10.1006/dbio.1993.1228. - DOI - PubMed

[3] Kirilly D, Xie T. The Drosophila ovary: an active stem cell community. Cell Res. 2007;17:15–25. doi: 10.1038/sj.cr.7310123. - DOI - PubMed

[4] Kirilly D, Xie T. The Drosophila ovary: an active stem cell community. Cell Res. 2007;17:15–25. doi: 10.1038/sj.cr.7310123. - DOI - PubMed

[5] Liu Z, et al. Coordinated niche-associated signals promote germline homeostasis in the Drosophila ovary. J Cell Biol. 2015;211:469–484. doi: 10.1083/jcb.201503033. - DOI - PMC - PubMed

[6] Liu Z, et al. Coordinated niche-associated signals promote germline homeostasis in the Drosophila ovary. J Cell Biol. 2015;211:469–484. doi: 10.1083/jcb.201503033. - DOI - PMC - PubMed

[7] Chen D, McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol. 2003;13:1786–1791. doi: 10.1016/j.cub.2003.09.033. - DOI - PubMed

[8] Chen D, McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol. 2003;13:1786–1791. doi: 10.1016/j.cub.2003.09.033. - DOI - PubMed

[9] Chen D, McKearin DM. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 2003;130:1159–1170. doi: 10.1242/dev.00325. - DOI - PubMed

[10] Chen D, McKearin DM. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 2003;130:1159–1170. doi: 10.1242/dev.00325. - DOI - PubMed

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Traffic jam regulates the function of the ovarian germline stem cell progeny differentiation niche during pre-adult stage in Drosophila

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Traffic jam regulates the function of the ovarian germline stem cell progeny differentiation niche during pre-adult stage in Drosophila

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