Skip to main content

Advertisement

Log in

Molecular control of the female germline stem cell niche size in Drosophila

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Adult stem cells have a unique capacity to renew themselves and generate differentiated cells that are needed in the body. These cells are recruited and maintained by the surrounding microenvironment, known as the stem cell niche, during organ development. Thus, the stem cell niche is required for proper tissue homeostasis, and its dysregulation is associated with tumorigenesis and tissue degeneration. The identification of niche components and the mechanisms that regulate niche establishment and maintenance, however, are just beginning to be uncovered. Germline stem cells (GSCs) of the Drosophila ovary provide an excellent model for studying the stem cell niche in vivo because of their well-characterized cell biology and the availability of genetic tools. In this review, we introduce the ovarian GSC niche, and the key signaling pathways for niche precursor segregation, niche specification, and niche extracellular environment establishment and niche maintenance that are involved in regulating niche size during development and adulthood.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4(1–2):7–25 (PubMed PMID: 747780)

    CAS  PubMed  Google Scholar 

  2. Xie T, Spradling AC (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290(5490):328. https://doi.org/10.1126/science.290.5490.328

    Article  CAS  PubMed  Google Scholar 

  3. Tulina N, Matunis E (2001) Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294(5551):2546. https://doi.org/10.1126/science.1066700

    Article  CAS  PubMed  Google Scholar 

  4. Dubois L, Makki R, Meister M, Vincent A, Crozatier M (2007) Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446:325. https://doi.org/10.1038/nature05650. https://www.nature.com/articles/nature05650#supplementary-information

    Article  Google Scholar 

  5. Mandal L, Martinez-Agosto JA, Evans CJ, Hartenstein V, Banerjee U (2007) A hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature 446:320. https://doi.org/10.1038/nature05585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG et al (2002) A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417:660. https://doi.org/10.1038/nature754

    Article  CAS  PubMed  Google Scholar 

  7. Wong MD, Jin Z, Xie T (2005) Molecular mechanisms of germline stem cell regulation. Annu Rev Genet 39(1):173–195. https://doi.org/10.1146/annurev.genet.39.073003.105855

    Article  CAS  PubMed  Google Scholar 

  8. Zhang J, Li L (2008) Stem cell niche: microenvironment and beyond. J Biol Chem 283(15):9499–9503. https://doi.org/10.1074/jbc.R700043200 (PubMed PMID: 18272517)

    Article  CAS  PubMed  Google Scholar 

  9. Joshi PM, Riddle MR, Djabrayan NJV, Rothman JH (2010) Caenorhabditis elegans as a model for stem cell biology. Dev Dyn 239(5):1539–1554. https://doi.org/10.1002/dvdy.22296 (PubMed PMID: 20419785)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Losick Vicki P, Morris Lucy X, Fox Donald T, Spradling A (2011) Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev Cell 21(1):159–171. https://doi.org/10.1016/j.devcel.2011.06.018

    Article  CAS  PubMed  Google Scholar 

  11. Li L, Xie T (2005) Stem cell niche: structure and function. Annu Rev Cell Dev Biol 21(1):605–631. https://doi.org/10.1146/annurev.cellbio.21.012704.131525

    Article  CAS  PubMed  Google Scholar 

  12. König A, Yatsenko AS, Weiss M, Shcherbata HR (2011) Ecdysteroids affect Drosophila ovarian stem cell niche formation and early germline differentiation. EMBO J 30(8):1549–1562. https://doi.org/10.1038/emboj.2011.73 (Epub 03/18, PubMed PMID: 21423150)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bonfini A, Wilkin MB, Baron M (2015) Reversible regulation of stem cell niche size associated with dietary control of Notch signalling. BMC Dev Biol 15(1):8. https://doi.org/10.1186/s12861-015-0059-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hsu HJ, Drummond-Barbosa D (2011) Insulin signals control the competence of the Drosophila female germline stem cell niche to respond to Notch ligands. Dev Biol. 350(2):290–300. https://doi.org/10.1016/j.ydbio.2010.11.032 (PubMed PMID: 21145317)

    Article  CAS  PubMed  Google Scholar 

  15. Zhao R, Xuan Y, Li X, Xi R (2008) Age-related changes of germline stem cell activity, niche signaling activity and egg production in Drosophila. Aging Cell 7(3):344–354. https://doi.org/10.1111/j.1474-9726.2008.00379.x

    Article  CAS  PubMed  Google Scholar 

  16. Pan L, Chen S, Weng C, Call G, Zhu D, Tang H et al (2007) Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 1(4):458–469. https://doi.org/10.1016/j.stem.2007.09.010

    Article  CAS  PubMed  Google Scholar 

  17. McGovern M, Voutev R, Maciejowski J, Corsi AK, Hubbard EJ (2009) A “latent niche” mechanism for tumor initiation. Proc Natl Acad Sci USA 106(28):11617–11622. https://doi.org/10.1073/pnas.0903768106 (PubMed PMID: 19564624; PubMed Central PMCID: PMCPMC2710656)

    Article  PubMed  Google Scholar 

  18. Spradling AC (1993) Developmental genetics of oogenesis. In: Martinez-Arias B (ed) The development of Drosophila melanogaster, vol 1. Cold Spring Harbor Laboratory Press, New York, pp 1–70

    Google Scholar 

  19. Morris LX, Spradling AC (2011) Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138(11):2207. https://doi.org/10.1242/dev.065508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kirilly D, Wang S, Xie T (2011) Self-maintained escort cells form a germline stem cell differentiation niche. Development (Cambridge, England) 138(23):5087–5097. https://doi.org/10.1242/dev.067850 (PubMed PMID: 22031542)

    Article  CAS  Google Scholar 

  21. Chen S, Wang S, Xie T (2011) Restricting self-renewal signals within the stem cell niche: multiple levels of control. Curr Opin Genet Dev 21(6):684–689. https://doi.org/10.1016/j.gde.2011.07.008

    Article  CAS  PubMed  Google Scholar 

  22. Forbes AJ, Lin H, Ingham PW, Spradling AC (1996) hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122(4):1125

    CAS  PubMed  Google Scholar 

  23. Song X, Xie T (2002) DE-cadherin-mediated cell adhesion is essential for maintaining somatic stem cells in the Drosophila ovary. Proc Natl Acad Sci USA 99(23):14813–14818. https://doi.org/10.1073/pnas.232389399 (Epub 10/22, PubMed PMID: 12393817)

    Article  CAS  PubMed  Google Scholar 

  24. de Cuevas M, Spradling AC (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125(15):2781

    PubMed  Google Scholar 

  25. Dansereau DA, Lasko P (2008) The development of germline stem cells in Drosophila. Methods Mol Biol 450:3–26. https://doi.org/10.1007/978-1-60327-214-8_1 (PubMed PMID: 18370048; PubMed Central PMCID: PMCPMC2729445)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Williamson A, Lehmann R (1996) Germ cell development in Drosophila. Annu Rev Cell Dev Biol 12(1):365–391. https://doi.org/10.1146/annurev.cellbio.12.1.365

    Article  CAS  PubMed  Google Scholar 

  27. Lai C-M, Lin K-Y, Kao S-H, Chen Y-N, Huang F, Hsu H-J (2017) Hedgehog signaling establishes precursors for germline stem cell niches by regulating cell adhesion. J Cell Biol 216(5):1439. https://doi.org/10.1083/jcb.201610063

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chen Y, Struhl G (1996) Dual roles for patched in sequestering and transducing hedgehog. Cell 87(3):553–563. https://doi.org/10.1016/S0092-8674(00)81374-4

    Article  CAS  PubMed  Google Scholar 

  29. Cohen ED, Mariol M-C, Wallace RMH, Weyers J, Kamberov YG, Pradel J et al (2002) DWnt4 regulates cell movement and focal adhesion kinase during Drosophila ovarian morphogenesis. Dev Cell 2(4):437–448. https://doi.org/10.1016/S1534-5807(02)00142-9

    Article  CAS  PubMed  Google Scholar 

  30. Song X, Call GB, Kirilly D, Xie T (2007) Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development 134(6):1071. https://doi.org/10.1242/dev.003392

    Article  CAS  PubMed  Google Scholar 

  31. King RC, Aggarwal SK, Aggarwal U (1968) The development of the female Drosophila reproductive system. J Morphol 124(2):143–166. https://doi.org/10.1002/jmor.1051240203 (PubMed PMID: 5654408)

    Article  CAS  PubMed  Google Scholar 

  32. Li MA, Alls JD, Avancini RM, Koo K, Godt D (2003) The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol 5:994. https://doi.org/10.1038/ncb1058. https://www.nature.com/articles/ncb1058#supplementary-information

    Article  CAS  Google Scholar 

  33. Huangfu D, Anderson KV (2006) Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133(1):3–14. https://doi.org/10.1242/dev.02169 (PubMed PMID: 16339192)

    Article  CAS  PubMed  Google Scholar 

  34. Tseng C-Y, Su Y-H, Yang S-M, Lin K-Y, Lai C-M, Rastegari E et al (2018) Smad-independent BMP signaling in somatic cells limits the size of the germline stem cell pool. Stem Cell Rep 11(3):811–827. https://doi.org/10.1016/j.stemcr.2018.07.008 (PubMed PMID: 30122445)

    Article  CAS  Google Scholar 

  35. Gilboa L, Lehmann R (2006) Soma–germline interactions coordinate homeostasis and growth in the Drosophila gonad. Nature 443:97. https://doi.org/10.1038/nature05068. https://www.nature.com/articles/nature05068#supplementary-information

    Article  CAS  Google Scholar 

  36. Rutledge BJ, Zhang K, Bier E, Jan YN, Perrimon N (1992) The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev 6(8):1503–1517 (PubMed PMID: 1644292)

    Article  CAS  Google Scholar 

  37. Gancz D, Gilboa L (2013) Insulin and target of rapamycin signaling orchestrate the development of ovarian niche-stem cell units in Drosophila. Development 140(20):4145. https://doi.org/10.1242/dev.093773

    Article  CAS  PubMed  Google Scholar 

  38. Sarikaya DP, Extavour CG (2015) The Hippo pathway regulates homeostatic growth of stem cell niche precursors in the Drosophila ovary. PLoS Genet 11(2):e1004962. https://doi.org/10.1371/journal.pgen.1004962 (PubMed PMID: 25643260; PubMed Central PMCID: PMCPMC4333732)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cho Y, Lai C-M, Lin K-Y, Hsu H-J (2018) A targeted RNAi screen reveals Drosophila female-sterile genes that control the size of germline stem cell niche during development. G3 Genes Genomes Genet 8(7):2345. https://doi.org/10.1534/g3.118.200355

    Article  CAS  Google Scholar 

  40. Fiuza UM, Arias AM (2007) Cell and molecular biology of Notch. J Endocrinol 194(3):459–474. https://doi.org/10.1677/JOE-07-0242 (PubMed PMID: 17761886)

    Article  CAS  PubMed  Google Scholar 

  41. Yeh E, Dermer M, Commisso C, Zhou L, McGlade CJ, Boulianne GL (2001) Neuralized functions as an E3 ubiquitin ligase during Drosophila development. Curr Biol 11(21):1675–1679. https://doi.org/10.1016/S0960-9822(01)00527-9

    Article  CAS  PubMed  Google Scholar 

  42. Yatsenko AS, Shcherbata HR (2018) Stereotypical architecture of the stem cell niche is spatiotemporally established by miR-125-dependent coordination of Notch and steroid signaling. Development 145(3):dev159178. https://doi.org/10.1242/dev.159178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Diederich RJ, Matsuno K, Hing H, Artavanis-Tsakonas S (1994) Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signaling pathway. Development 120(3):473

    CAS  PubMed  Google Scholar 

  44. Wilkin MB, Baron M (2005) Endocytic regulation of Notch activation and down-regulation (review). Mol Membr Biol 22(4):279–289. https://doi.org/10.1080/09687860500129778 (PubMed PMID: 16154900)

    Article  CAS  PubMed  Google Scholar 

  45. Shimizu H, Wilkin Marian B, Woodcock Simon A, Bonfini A, Hung Y, Mazaleyrat S et al (2017) The Drosophila ZO-1 protein Polychaetoid suppresses Deltex-regulated Notch activity to modulate germline stem cell niche formation. Open Biol 7(4):160322. https://doi.org/10.1098/rsob.160322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Panchal T, Chen X, Alchits E, Oh Y, Poon J, Kouptsova J et al (2017) Specification and spatial arrangement of cells in the germline stem cell niche of the Drosophila ovary depend on the Maf transcription factor Traffic jam. PLoS Genet 13(5):e1006790. https://doi.org/10.1371/journal.pgen.1006790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Penalva LOF, Sánchez L (2003) RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev 67(3):343. https://doi.org/10.1128/MMBR.67.3.343-359.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sciabica KS, Hertel KJ (2006) The splicing regulators Tra and Tra2 are unusually potent activators of pre-mRNA splicing. Nucleic Acids Res 34(22):6612–6620. https://doi.org/10.1093/nar/gkl984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lund AH, van Lohuizen M (2004) Polycomb complexes and silencing mechanisms. Curr Opin Cell Biol 16(3):239–246. https://doi.org/10.1016/j.ceb.2004.03.010

    Article  CAS  PubMed  Google Scholar 

  50. Soldatov A, Nabirochkina E, Georgieva S, Belenkaja T, Georgiev P (1999) TAFII 40 protein is encoded by the e(y)1 gene: biological consequences of mutations. Mol Cell Biol 19(5):3769. https://doi.org/10.1128/MCB.19.5.3769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Shidlovskii YV, Krasnov AN, Nikolenko JV, Lebedeva LA, Kopantseva M, Ermolaeva MA et al (2005) A novel multidomain transcription coactivator SAYP can also repress transcription in heterochromatin. EMBO J 24(1):97. https://doi.org/10.1038/sj.emboj.7600508

    Article  CAS  PubMed  Google Scholar 

  52. van der Horst A, Lens SMA (2014) Cell division: control of the chromosomal passenger complex in time and space. Chromosoma 123(1):25–42. https://doi.org/10.1007/s00412-013-0437-6

    Article  CAS  PubMed  Google Scholar 

  53. Nakato H, Futch TA, Selleck SB (1995) The division abnormally delayed (dally) gene: a putative integral membrane proteoglycan required for cell division patterning during postembryonic development of the nervous system in Drosophila. Development 121(11):3687

    CAS  PubMed  Google Scholar 

  54. Iozzo RV, Schaefer L (2015) Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol 42:11–55. https://doi.org/10.1016/j.matbio.2015.02.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Matsuoka S, Hiromi Y, Asaoka M (2013) Egfr signaling controls the size of the stem cell precursor pool in the Drosophila ovary. Mech Dev 130(4):241–253. https://doi.org/10.1016/j.mod.2013.01.002

    Article  CAS  PubMed  Google Scholar 

  56. Hamaratoglu F, Affolter M, Pyrowolakis G (2014) Dpp/BMP signaling in flies: from molecules to biology. Semin Cell Dev Biol 32:128–136. https://doi.org/10.1016/j.semcdb.2014.04.036

    Article  CAS  PubMed  Google Scholar 

  57. Hafen E (2004) Cancer, type 2 diabetes, and ageing: news from flies and worms. Swiss Med Wkly 134(49–50):711–719. https://doi.org/10.4414/smw.2004.09885 (PubMed PMID: 15635489)

    Article  CAS  PubMed  Google Scholar 

  58. Hsu H-J, Drummond-Barbosa D (2009) Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proc Natl Acad Sci USA 106(4):1117–1121. https://doi.org/10.1073/pnas.0809144106 (Epub 01/09, PubMed PMID: 19136634)

    Article  PubMed  Google Scholar 

  59. Yang S-A, Wang W-D, Chen C-T, Tseng C-Y, Chen Y-N, Hsu H-J (2013) FOXO/Fringe is necessary for maintenance of the germline stem cell niche in response to insulin insufficiency. Dev Biol 382(1):124–135. https://doi.org/10.1016/j.ydbio.2013.07.018

    Article  CAS  PubMed  Google Scholar 

  60. Thomas JO (1999) Histone H1: location and role. Curr Opin Cell Biol 11(3):312–317. https://doi.org/10.1016/S0955-0674(99)80042-8

    Article  CAS  PubMed  Google Scholar 

  61. Yang Z, Sun J, Hu Y, Wang F, Wang X, Qiao H-H et al (2017) Histone H1 defect in escort cells triggers germline tumor in Drosophila ovary. Dev Biol 424(1):40–49. https://doi.org/10.1016/j.ydbio.2017.02.012

    Article  CAS  PubMed  Google Scholar 

  62. Eliazer S, Shalaby NA, Buszczak M (2011) Loss of lysine-specific demethylase 1 nonautonomously causes stem cell tumors in the Drosophila ovary. Proc Natl Acad Sci 108(17):7064. https://doi.org/10.1073/pnas.1015874108

    Article  PubMed  Google Scholar 

  63. Jin Z, Flynt Alex S, Lai Eric C (2013) Drosophila piwi mutants exhibit germline stem cell tumors that are sustained by elevated Dpp signaling. Curr Biol 23(15):1442–1448. https://doi.org/10.1016/j.cub.2013.06.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Wang X, Pan L, Wang S, Zhou J, McDowell W, Park J et al (2011) Histone H3K9 trimethylase Eggless controls germline stem cell maintenance and differentiation. PLoS Genet 7(12):e1002426. https://doi.org/10.1371/journal.pgen.1002426 (PubMed PMID: 22216012; PubMed Central PMCID: PMCPMC3245301)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Ma X, Wang S, Do T, Song X, Inaba M, Nishimoto Y et al (2014) Piwi is required in multiple cell types to control germline stem cell lineage development in the Drosophila ovary. PLoS One 9(3):e90267. https://doi.org/10.1371/journal.pone.0090267 (PubMed PMID: 24658126; PubMed Central PMCID: PMCPMC3962343)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yang F, Quan Z, Huang H, He M, Liu X, Cai T et al (2019) Ovaries absent links dLsd1 to HP1a for local H3K4 demethylation required for heterochromatic gene silencing. eLife 8:40806. https://doi.org/10.7554/elife.40806

    Article  Google Scholar 

  67. Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H, Dus M et al (2007) Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 21(18):2300–2311. https://doi.org/10.1101/gad.1564307 (PubMed PMID: 17875665; PubMed Central PMCID: PMCPMC1973144)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Lu X, Wontakal SN, Kavi H, Kim BJ, Guzzardo PM, Emelyanov AV et al (2013) Drosophila H1 regulates the genetic activity of heterochromatin by recruitment of Su(var)3–9. Science 340(6128):78. https://doi.org/10.1126/science.1234654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Ables ET, Drummond-Barbosa D (2010) The steroid hormone ecdysone functions with intrinsic chromatin remodeling factors to control female germline stem cells in Drosophila. Cell Stem Cell 7(5):581–592. https://doi.org/10.1016/j.stem.2010.10.001 (PubMed PMID: 21040900; PubMed Central PMCID: PMCPMC3292427)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Hayashi Y, Kobayashi S, Nakato H (2009) Drosophila glypicans regulate the germline stem cell niche. J Cell Biol 187(4):473–480. https://doi.org/10.1083/jcb.200904118 (PubMed PMID: 19948496)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Guo Z, Wang Z (2009) The glypican Dally is required in the niche for the maintenance of germline stem cells and short-range BMP signaling in the Drosophila ovary. Development 136(21):3627. https://doi.org/10.1242/dev.036939

    Article  CAS  PubMed  Google Scholar 

  72. Luo L, Wang H, Fan C, Liu S, Cai Y (2015) Wnt ligands regulate Tkv expression to constrain Dpp activity in the Drosophila ovarian stem cell niche. J Cell Biol 209(4):595. https://doi.org/10.1083/jcb.201409142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Krens SFG, Heisenberg C-P (2011) Chapter six—Cell sorting in development. In: Labouesse M (ed) Current topics in developmental biology, vol 95. Academic Press, Cambridge, pp 189–213

    Google Scholar 

  74. Sahut-Barnola I, Godt D, Laski FA, Couderc J-L (1995) Drosophila ovary morphogenesis: analysis of terminal filament formation and identification of a gene required for this process. Dev Biol 170(1):127–135. https://doi.org/10.1006/dbio.1995.1201

    Article  CAS  PubMed  Google Scholar 

  75. Godt D, Laski FA (1995) Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric a brac. Development 121(1):173

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Marcus Calkins for English editing.

Funding

The work was supported by the intramural funding from the Institute of Cellular and Organismic Biology, Academia Sinica, Taiwan and the Ministry of Science and Technology, Taiwan (107-2311-B-001-004-MY3).

Author information

Authors and Affiliations

Authors

Contributions

MB wrote the introduction, CML drew the germarium and larval ovary schemes, and HJH wrote the paper.

Corresponding author

Correspondence to Hwei-Jan Hsu.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hsu, HJ., Bahader, M. & Lai, CM. Molecular control of the female germline stem cell niche size in Drosophila. Cell. Mol. Life Sci. 76, 4309–4317 (2019). https://doi.org/10.1007/s00018-019-03223-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-019-03223-0

Keywords

Navigation