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The Vast Utility of Drosophila Oogenesis

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Drosophila Oogenesis

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2626))

Abstract

In this chapter, we highlight examples of the diverse array of developmental, cellular, and biochemical insights that can be gained by using Drosophila melanogaster oogenesis as a model tissue. We begin with an overview of ovary development and adult oogenesis. Then we summarize how the adult Drosophila ovary continues to advance our understanding of stem cells, cell cycle, cell migration, cytoplasmic streaming, nurse cell dumping, and cell death. We also review emerging areas of study, including the roles of lipid droplets, ribosomes, and nuclear actin in egg development. Finally, we conclude by discussing the growing conservation of processes and signaling pathways that regulate oogenesis and female reproduction from flies to humans.

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References

  1. Cooley L (1995) Oogenesis: variations on a theme. Dev Genet 16(1):1–5. https://doi.org/10.1002/dvg.1020160103

    Article  CAS  Google Scholar 

  2. Elis S, Desmarchais A, Cardona E, Fouchecourt S, Dalbies-Tran R, Nguyen T, Thermes V, Maillard V, Papillier P, Uzbekova S, Bobe J, Couderc JL, Monget P (2018) Genes involved in Drosophila melanogaster ovarian function are highly conserved throughout evolution. Genome Biol Evol 10(10):2629–2642. https://doi.org/10.1093/gbe/evy158

    Article  CAS  Google Scholar 

  3. Doherty CA, Amargant F, Shvartsman SY, Duncan FE, Gavis ER (2022) Bidirectional communication in oogenesis: a dynamic conversation in mice and Drosophila. Trends Cell Biol 32(4):311–323. https://doi.org/10.1016/j.tcb.2021.11.005

    Article  CAS  Google Scholar 

  4. Santos AC, Lehmann R (2004) Germ cell specification and migration in Drosophila and beyond. Curr Biol 14(14):R578–R589. https://doi.org/10.1016/j.cub.2004.07.018

    Article  CAS  Google Scholar 

  5. Ephrussi A, Lehmann R (1992) Induction of germ cell formation by Oskar. Nature 358(6385):387–392

    Article  CAS  Google Scholar 

  6. Jemc JC (2011) Somatic gonadal cells: the supporting cast for the germline. Genesis 49(10):753–775. https://doi.org/10.1002/dvg.20784

    Article  CAS  Google Scholar 

  7. King RC, Aggarwal SK, Aggarwal U (1968) The development of the female Drosophila reproductive system. J Morphol 124(2):143–165. https://doi.org/10.1002/jmor.1051240203

    Article  CAS  Google Scholar 

  8. Boyle M, DiNardo S (1995) Specification, migration and assembly of the somatic cells of the Drosophila gonad. Development 121(6):1815–1825. https://doi.org/10.1242/dev.121.6.1815

    Article  CAS  Google Scholar 

  9. Saitou M, Yamaji M (2012) Primordial germ cells in mice. Cold Spring Harb Perspect Biol 4(11). https://doi.org/10.1101/cshperspect.a008375

  10. Zhang H, Risal S, Gorre N, Busayavalasa K, Li X, Shen Y, Bosbach B, Brännström M, Liu K (2014) Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr Biol 24(21):2501–2508. https://doi.org/10.1016/j.cub.2014.09.023

    Article  CAS  Google Scholar 

  11. Gilboa L (2015) Organizing stem cell units in the Drosophila ovary. Curr Opin Genet Dev 32:31–36. https://doi.org/10.1016/j.gde.2015.01.005

    Article  CAS  Google Scholar 

  12. Slaidina M, Banisch TU, Gupta S, Lehmann R (2020) A single-cell atlas of the developing Drosophila ovary identifies follicle stem cell progenitors. Genes Dev 34(3–4):239–249

    Article  CAS  Google Scholar 

  13. Xie T, Spradling AC (2000) A niche maintaining germ line stem cells in the Drosophila ovary. Science 290(5490):328–330. https://doi.org/10.1126/science.290.5490.328

    Article  CAS  Google Scholar 

  14. 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(11):994–1000. https://doi.org/10.1038/ncb1058

    Article  CAS  Google Scholar 

  15. Gilboa L, Forbes A, Tazuke SI, Fuller MT, Lehmann R (2003) Germ line stem cell differentiation in Drosophila requires gap junctions and proceeds via an intermediate state. Development 130(26):6625–6634. https://doi.org/10.1242/dev.00853

    Article  CAS  Google Scholar 

  16. Reilein A, Kogan HV, Misner R, Park KS, Kalderon D (2021) Adult stem cells and niche cells segregate gradually from common precursors that build the adult Drosophila ovary during pupal development. elife 10:e69749. C69741 – elife 62021;69710:e69749. https://doi.org/10.7554/eLife.69749

    Article  CAS  Google Scholar 

  17. Allen AK, Spradling AC (2008) The Sf1-related nuclear hormone receptor Hr39 regulates Drosophila female reproductive tract development and function. Development 135(2):311–321. https://doi.org/10.1242/dev.015156

    Article  CAS  Google Scholar 

  18. Wolfner MF (2011) Precious essences: female secretions promote sperm storage in Drosophila. PLoS Biol 9(11):e1001191. https://doi.org/10.1371/journal.pbio.1001191

    Article  CAS  Google Scholar 

  19. Schnakenberg SL, Siegal ML, Bloch Qazi MC (2012) Oh, the places they’ll go: female sperm storage and sperm precedence in Drosophila melanogaster. Spermatogenesis 2(3):224–235. https://doi.org/10.4161/spmg.21655

    Article  Google Scholar 

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

    Google Scholar 

  21. de Cuevas M (2015) Drosophila oogenesis. In: eLS, pp 1–7. https://doi.org/10.1002/9780470015902.a0001502.pub2

    Chapter  Google Scholar 

  22. Deng W, Lin H (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol 189(1):79–94. https://doi.org/10.1006/dbio.1997.8669

    Article  CAS  Google Scholar 

  23. Yue L, Spradling AC (1992) hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev 6(12b):2443–2454. https://doi.org/10.1101/gad.6.12b.2443

    Article  CAS  Google Scholar 

  24. Robinson DN, Cant K, Cooley L (1994) Morphogenesis of Drosophila ovarian ring canals. Development 120(7):2015–2025. https://doi.org/10.1242/dev.120.7.2015

    Article  CAS  Google Scholar 

  25. Hinnant TD, Merkle JA, Ables ET (2020) Coordinating proliferation, polarity, and cell fate in the drosophila female germline. Front Cell Dev Biol 8. https://doi.org/10.3389/fcell.2020.00019

  26. Lighthouse DV, Buszczak M, Spradling AC (2008) New components of the Drosophila fusome suggest it plays novel roles in signaling and transport. Dev Biol 317(1):59–71. https://doi.org/10.1016/j.ydbio.2008.02.009

    Article  CAS  Google Scholar 

  27. Röper K, Brown NH (2004) A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr Biol 14(2):99–110. https://doi.org/10.1016/j.cub.2003.12.056

    Article  CAS  Google Scholar 

  28. Snapp EL, Iida T, Frescas D, Lippincott-Schwartz J, Lilly MA (2004) The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. Mol Biol Cell 15(10):4512–4521. https://doi.org/10.1091/mbc.e04-06-0475

    Article  CAS  Google Scholar 

  29. Huynh J-R, St Johnston D (2004) The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 14(11):R438–R449. https://doi.org/10.1016/j.cub.2004.05.040

    Article  CAS  Google Scholar 

  30. Bastock R, St Johnston D (2008) Drosophila oogenesis. Curr Biol 18(23):R1082–R1087. https://doi.org/10.1016/j.cub.2008.09.011

    Article  CAS  Google Scholar 

  31. Margolis J, Spradling A (1995) Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121(11):3797–3807. https://doi.org/10.1242/dev.121.11.3797

    Article  CAS  Google Scholar 

  32. Nystul T, Spradling A (2007) An epithelial niche in the Drosophila ovary undergoes long-range stem cell replacement. Cell Stem Cell 1(3):277–285. https://doi.org/10.1016/j.stem.2007.07.009

    Article  CAS  Google Scholar 

  33. Nystul T, Spradling A (2010) Regulation of epithelial stem cell replacement and follicle formation in the Drosophila ovary. Genetics 184(2):503–515. https://doi.org/10.1534/genetics.109.109538

    Article  CAS  Google Scholar 

  34. Rust K, Byrnes LE, Yu KS, Park JS, Sneddon JB, Tward AD, Nystul TG (2020) A single-cell atlas and lineage analysis of the adult Drosophila ovary. Nat Commun 11(1):5628. https://doi.org/10.1038/s41467-020-19361-0

    Article  CAS  Google Scholar 

  35. Grammont M, Irvine KD (2002) Organizer activity of the polar cells during Drosophilaoogenesis. Development 129(22):5131–5140. https://doi.org/10.1242/dev.129.22.5131

    Article  CAS  Google Scholar 

  36. Wu X, Tanwar PS, Raftery LA (2008) Drosophila follicle cells: morphogenesis in an eggshell. Semin Cell Dev Biol 19(3):271–282. https://doi.org/10.1016/j.semcdb.2008.01.004

    Article  CAS  Google Scholar 

  37. Horne-Badovinac S (2014) The Drosophila egg chamber-a new spin on how tissues elongate. Integr Comp Biol 54(4):667–676. https://doi.org/10.1093/icb/icu067

    Article  CAS  Google Scholar 

  38. Montell DJ (2003) Border-cell migration: the race is on. Nat Rev Mol Cell Biol 4(1):13–24. https://doi.org/10.1038/nrm1006

    Article  CAS  Google Scholar 

  39. Montell DJ, Yoon WH, Starz-Gaiano M (2012) Group choreography: mechanisms orchestrating the collective movement of border cells. Nat Rev Mol Cell Biol 13(10):631–645. https://doi.org/10.1038/nrm3433

    Article  CAS  Google Scholar 

  40. Saadin A, Starz-Gaiano M (2016) Circuitous genetic regulation governs a straightforward cell migration. Trends Genet 32(10):660–673. https://doi.org/10.1016/j.tig.2016.08.001

    Article  CAS  Google Scholar 

  41. Horne-Badovinac S (2020) The Drosophila micropyle as a system to study how epithelia build complex extracellular structures. Philos Trans R Soc Lond Ser B Biol Sci 375(1809):20190561. https://doi.org/10.1098/rstb.2019.0561

    Article  CAS  Google Scholar 

  42. Buszczak M, Cooley L (2000) Eggs to die for: cell death during drosophila oogenesis. Cell Death Differ 7(11):1071–1074. https://doi.org/10.1038/sj.cdd.4400755

    Article  CAS  Google Scholar 

  43. Lebo DPV, McCall K (2021) Murder on the ovarian express: a tale of non-autonomous cell death in the Drosophila ovary. Cell 10(6). https://doi.org/10.3390/cells10061454

  44. Berg CA (2005) The Drosophila shell game: patterning genes and morphological change. Trends Genet 21(6):346–355. https://doi.org/10.1016/j.tig.2005.04.010

    Article  CAS  Google Scholar 

  45. Gattazzo F, Urciuolo A, Bonaldo P (2014) Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim Biophys Acta Gen Subj 1840(8):2506–2519. https://doi.org/10.1016/j.bbagen.2014.01.010

    Article  CAS  Google Scholar 

  46. Kahney EW, Snedeker JC, Chen X (2019) Regulation of Drosophila germline stem cells. Curr Opin Cell Biol 60:27–35. https://doi.org/10.1016/j.ceb.2019.03.008

    Article  CAS  Google Scholar 

  47. Losick VP, Morris LX, Fox DT, 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  Google Scholar 

  48. Sahai-Hernandez P, Castanieto A, Nystul TG (2012) Drosophila models of epithelial stem cells and their niches. Wiley Interdiscip Rev Dev Biol 1(3):447–457. https://doi.org/10.1002/wdev.36

    Article  CAS  Google Scholar 

  49. Rust K, Nystul T (2020) Signal transduction in the early Drosophila follicle stem cell lineage. Curr Opin Insect Sci 37:39–48. https://doi.org/10.1016/j.cois.2019.11.005

    Article  Google Scholar 

  50. Laws KM, Drummond-Barbosa D (2015) Genetic mosaic analysis of stem cell lineages in the Drosophila ovary. Methods Mol Biol 1328:57–72. https://doi.org/10.1007/978-1-4939-2851-4_4

    Article  CAS  Google Scholar 

  51. McLaughlin JM, Bratu DP (2015) Drosophila melanogaster oogenesis: an overview. Methods Mol Biol 1328:1–20. https://doi.org/10.1007/978-1-4939-2851-4_1

    Article  CAS  Google Scholar 

  52. Eliazer S, Buszczak M (2011) Finding a niche: studies from the Drosophila ovary. Stem Cell Res Ther 2(6):45. https://doi.org/10.1186/scrt86

    Article  Google Scholar 

  53. Kirilly D, Xie T (2007) The Drosophila ovary: an active stem cell community. Cell Res 17(1):15–25. https://doi.org/10.1038/sj.cr.7310123

    Article  CAS  Google Scholar 

  54. 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):2207–2215. https://doi.org/10.1242/dev.065508

    Article  CAS  Google Scholar 

  55. 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 99(23):14813–14818. https://doi.org/10.1073/pnas.232389399

    Article  CAS  Google Scholar 

  56. Song X, Zhu C-H, Doan C, Xie T (2002) Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296(5574):1855–1857. https://doi.org/10.1126/science.1069871

    Article  CAS  Google Scholar 

  57. Xie T, Spradling AC (1998) Decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94(2):251–260. https://doi.org/10.1016/S0092-8674(00)81424-5

    Article  CAS  Google Scholar 

  58. Wharton KA, Thomsen GH, Gelbart WM (1991) Drosophila 60A gene, another transforming growth factor beta family member, is closely related to human bone morphogenetic proteins. Proc Natl Acad Sci U S A 88(20):9214–9218. https://doi.org/10.1073/pnas.88.20.9214

    Article  CAS  Google Scholar 

  59. Chen D, McKearin D (2003) Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol 13(20):1786–1791. https://doi.org/10.1016/j.cub.2003.09.033

    Article  CAS  Google Scholar 

  60. Chen D, McKearin DM (2003) A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130(6):1159–1170. https://doi.org/10.1242/dev.00325

    Article  CAS  Google Scholar 

  61. Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, Xie T (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131(6):1353–1364. https://doi.org/10.1242/dev.01026

    Article  CAS  Google Scholar 

  62. McKearin D, Ohlstein B (1995) A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121(9):2937–2947. https://doi.org/10.1242/dev.121.9.2937

    Article  CAS  Google Scholar 

  63. McKearin DM, Spradling AC (1990) bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev 4(12B):2242–2251. https://doi.org/10.1101/gad.4.12b.2242

    Article  CAS  Google Scholar 

  64. Ohlstein B, Lavoie CA, Vef O, Gateff E, McKearin DM (2000) The Drosophila cystoblast differentiation factor, benign gonial cell neoplasm, is related to DExH-box proteins and interacts genetically with bag-of-marbles. Genetics 155(4):1809–1819. https://doi.org/10.1093/genetics/155.4.1809

    Article  CAS  Google Scholar 

  65. Díaz-Torres A, Rosales-Nieves AE, Pearson JR, Santa-Cruz Mateos C, Marín-Menguiano M, Marshall OJ, Brand AH, González-Reyes A (2021) Stem cell niche organization in the Drosophila ovary requires the ECM component Perlecan. Curr Biol 31(8):1744–1753.e1745. https://doi.org/10.1016/j.cub.2021.01.071

    Article  CAS  Google Scholar 

  66. Wilcockson SG, Sutcliffe C, Ashe HL (2017) Control of signaling molecule range during developmental patterning. Cell Mol Life Sci 74(11):1937–1956. https://doi.org/10.1007/s00018-016-2433-5

    Article  CAS  Google Scholar 

  67. 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 Drosophilaovary. Development 136(21):3627–3635. https://doi.org/10.1242/dev.036939

    Article  CAS  Google Scholar 

  68. Liu M, Lim TM, Cai Y (2010) The Drosophila female germline stem cell lineage acts to spatially restrict DPP function within the niche. Sci Signal 3(132):ra57. https://doi.org/10.1126/scisignal.2000740

    Article  CAS  Google Scholar 

  69. Wang L, Li Z, Cai Y (2008) The JAK/STAT pathway positively regulates DPP signaling in the Drosophila germline stem cell niche. J Cell Biol 180(4):721–728. https://doi.org/10.1083/jcb.200711022

    Article  CAS  Google Scholar 

  70. Decotto E, Spradling AC (2005) The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev Cell 9(4):501–510. https://doi.org/10.1016/j.devcel.2005.08.012

    Article  CAS  Google Scholar 

  71. Lopez-Onieva L, Fernandez-Minan A, Gonzalez-Reyes A (2008) Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary. Development 135(3):533–540. https://doi.org/10.1242/dev.016121

    Article  CAS  Google Scholar 

  72. Gilboa L, Lehmann R (2006) Soma-germline interactions coordinate homeostasis and growth in the Drosophila gonad. Nature 443(7107):97–100. https://doi.org/10.1038/nature05068

    Article  CAS  Google Scholar 

  73. Maimon I, Popliker M, Gilboa L (2014) Without children is required for Stat-mediated zfh1 transcription and for germline stem cell differentiation. Development 141(13):2602–2610. https://doi.org/10.1242/dev.109611

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  75. Antel M, Inaba M (2020) Modulation of cell–cell interactions in Drosophila oocyte development. Cell 9(2):274

    Article  CAS  Google Scholar 

  76. Liu Z, Zhong G, Chai PC, Luo L, Liu S, Yang Y, Baeg G-H, Cai Y (2015) Coordinated niche-associated signals promote germline homeostasis in the Drosophila ovary. J Cell Biol 211(2):469–484. https://doi.org/10.1083/jcb.201503033

    Article  CAS  Google Scholar 

  77. Ting X (2013) Control of germline stem cell self-renewal and differentiation in the Drosophila ovary: concerted actions of niche signals and intrinsic factors. WIREs Dev Biol 2(2):261–273. https://doi.org/10.1002/wdev.60

    Article  CAS  Google Scholar 

  78. Duan T, Green N, Tootle TL, Geyer PK (2020) Nuclear architecture as an intrinsic regulator of Drosophila female germline stem cell maintenance. Curr Opin Insect Sci 37:30–38. https://doi.org/10.1016/j.cois.2019.11.007

    Article  Google Scholar 

  79. Burke B, Stewart CL (2013) The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 14(1):13–24. https://doi.org/10.1038/nrm3488

    Article  CAS  Google Scholar 

  80. Vahabikashi A, Adam SA, Medalia O, Goldman RD (2022) Nuclear lamins: structure and function in mechanobiology. APL Bioeng 6(1):011503. https://doi.org/10.1063/5.0082656

    Article  CAS  Google Scholar 

  81. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC, Pinter J, Pajerowski JD, Spinler KR, Shin JW, Tewari M, Rehfeldt F, Speicher DW, Discher DE (2013) Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341(6149):1240104. https://doi.org/10.1126/science.1240104

    Article  CAS  Google Scholar 

  82. Segura-Totten M, Wilson KL (2004) BAF: roles in chromatin, nuclear structure and retrovirus integration. Trends Cell Biol 14(5):261–266. https://doi.org/10.1016/j.tcb.2004.03.004

    Article  CAS  Google Scholar 

  83. Sears RM, Roux KJ (2020) Diverse cellular functions of barrier-to-autointegration factor and its roles in disease. J Cell Sci 133(16). https://doi.org/10.1242/jcs.246546

  84. Barton LJ, Duan T, Ke W, Luttinger A, Lovander KE, Soshnev AA, Geyer PK (2018) Nuclear lamina dysfunction triggers a germline stem cell checkpoint. Nat Commun 9(1):3960. https://doi.org/10.1038/s41467-018-06277-z

    Article  CAS  Google Scholar 

  85. Barton Lacy J, Pinto Belinda S, Wallrath Lori L, Geyer Pamela K (2013) The Drosophila nuclear lamina protein otefin is required for germline stem cell survival. Dev Cell 25(6):645–654. https://doi.org/10.1016/j.devcel.2013.05.023

    Article  CAS  Google Scholar 

  86. Duan T, Kitzman SC, Geyer PK (2020) Survival of Drosophila germline stem cells requires the chromatin-binding protein barrier-to-autointegration factor. Development 147(9). https://doi.org/10.1242/dev.186171

  87. Duan T, Cupp R, Geyer PK (2021) Drosophila female germline stem cells undergo mitosis without nuclear breakdown. Curr Biol 31(7):1450–1462. e1453. https://doi.org/10.1016/j.cub.2021.01.033

    Article  CAS  Google Scholar 

  88. Tatli M, Medalia O (2018) Insight into the functional organization of nuclear lamins in health and disease. Curr Opin Cell Biol 54:72–79. https://doi.org/10.1016/j.ceb.2018.05.001

    Article  CAS  Google Scholar 

  89. Shin JY, Worman HJ (2022) Molecular pathology of laminopathies. Annu Rev Pathol 17:159–180. https://doi.org/10.1146/annurev-pathol-042220-034240

    Article  CAS  Google Scholar 

  90. Bosco G, Orr-Weaver TL (2002) The cell cycle during oogenesis and early embryogenesis in Drosophila. In: Advances in developmental biology and biochemistry, vol 12. Elsevier, pp 107–154. https://doi.org/10.1016/S1569-1799(02)12026-0

    Chapter  Google Scholar 

  91. Smith PA, King RC (1968) Genetic control of synaptonemal complexes in Drosophila melanogaster. Genetics 60(2):335–351. https://doi.org/10.1093/genetics/60.2.335

    Article  CAS  Google Scholar 

  92. Von Stetina JR, Orr-Weaver TL (2011) Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol 3(10):a005553. https://doi.org/10.1101/cshperspect.a005553

    Article  CAS  Google Scholar 

  93. Mahowald AP, Goralski TJ, Caulton JH (1983) In vitro activation of Drosophila eggs. Dev Biol 98(2):437–445. https://doi.org/10.1016/0012-1606(83)90373-1

    Article  CAS  Google Scholar 

  94. Lilly MA, Spradling AC (1996) The Drosophila endocycle is controlled by cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev 10(19):2514–2526. https://doi.org/10.1101/gad.10.19.2514

    Article  CAS  Google Scholar 

  95. Klusza S, Deng WM (2011) At the crossroads of differentiation and proliferation: precise control of cell-cycle changes by multiple signaling pathways in Drosophila follicle cells. BioEssays 33(2):124–134. https://doi.org/10.1002/bies.201000089

    Article  CAS  Google Scholar 

  96. Lopez-Schier H, St Johnston D (2001) Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev 15(11):1393–1405. https://doi.org/10.1101/gad.200901

    Article  CAS  Google Scholar 

  97. Deng WM, Althauser C, Ruohola-Baker H (2001) Notch-Delta signaling induces a transition from mitotic cell cycle to endocycle in Drosophila follicle cells. Development 128(23):4737–4746. https://doi.org/10.1242/dev.128.23.4737

    Article  CAS  Google Scholar 

  98. Sun J, Smith L, Armento A, Deng WM (2008) Regulation of the endocycle/gene amplification switch by Notch and ecdysone signaling. J Cell Biol 182(5):885–896. https://doi.org/10.1083/jcb.200802084

    Article  CAS  Google Scholar 

  99. Calvi BR, Lilly MA, Spradling AC (1998) Cell cycle control of chorion gene amplification. Genes Dev 12(5):734–744. https://doi.org/10.1101/gad.12.5.734

    Article  CAS  Google Scholar 

  100. Sun J, Deng WM (2007) Hindsight mediates the role of notch in suppressing hedgehog signaling and cell proliferation. Dev Cell 12(3):431–442. https://doi.org/10.1016/j.devcel.2007.02.003

    Article  CAS  Google Scholar 

  101. Sun J, Deng WM (2005) Notch-dependent downregulation of the homeodomain gene cut is required for the mitotic cycle/endocycle switch and cell differentiation in Drosophila follicle cells. Development 132(19):4299–4308. https://doi.org/10.1242/dev.02015

    Article  CAS  Google Scholar 

  102. Edgar BA, Zielke N, Gutierrez C (2014) Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat Rev Mol Cell Biol 15(3):197–210. https://doi.org/10.1038/nrm3756

    Article  CAS  Google Scholar 

  103. Lee HO, Davidson JM, Duronio RJ (2009) Endoreplication: polyploidy with purpose. Genes Dev 23(21):2461–2477. https://doi.org/10.1101/gad.1829209

    Article  CAS  Google Scholar 

  104. Cross JC (2005) How to make a placenta: mechanisms of trophoblast cell differentiation in mice--a review. Placenta 26(Suppl A):S3–S9. https://doi.org/10.1016/j.placenta.2005.01.015

    Article  CAS  Google Scholar 

  105. Rossant J, Cross JC (2001) Placental development: lessons from mouse mutants. Nat Rev Genet 2(7):538–548. https://doi.org/10.1038/35080570

    Article  CAS  Google Scholar 

  106. Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20:180–193. https://doi.org/10.1152/physiol.00001.2005

    Article  CAS  Google Scholar 

  107. Lazzerini Denchi E, Celli G, de Lange T (2006) Hepatocytes with extensive telomere deprotection and fusion remain viable and regenerate liver mass through endoreduplication. Genes Dev 20(19):2648–2653. https://doi.org/10.1101/gad.1453606

    Article  CAS  Google Scholar 

  108. Fox DT, Duronio RJ (2013) Endoreplication and polyploidy: insights into development and disease. Development 140(1):3–12. https://doi.org/10.1242/dev.080531

    Article  CAS  Google Scholar 

  109. Claycomb JM, Benasutti M, Bosco G, Fenger DD, Orr-Weaver TL (2004) Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev Cell 6(1):145–155. https://doi.org/10.1016/s1534-5807(03)00398-8

    Article  CAS  Google Scholar 

  110. Claycomb JM, Orr-Weaver TL (2005) Developmental gene amplification: insights into DNA replication and gene expression. Trends Genet 21(3):149–162. https://doi.org/10.1016/j.tig.2005.01.009

    Article  CAS  Google Scholar 

  111. Kim JC, Nordman J, Xie F, Kashevsky H, Eng T, Li S, MacAlpine DM, Orr-Weaver TL (2011) Integrative analysis of gene amplification in Drosophila follicle cells: parameters of origin activation and repression. Genes Dev 25(13):1384–1398. https://doi.org/10.1101/gad.2043111

    Article  CAS  Google Scholar 

  112. Nordman J, Orr-Weaver TL (2012) Regulation of DNA replication during development. Development 139(3):455–464. https://doi.org/10.1242/dev.061838

    Article  CAS  Google Scholar 

  113. Shoshani O, Brunner SF, Yaeger R, Ly P, Nechemia-Arbely Y, Kim DH, Fang R, Castillon GA, Yu M, Li JSZ, Sun Y, Ellisman MH, Ren B, Campbell PJ, Cleveland DW (2021) Chromothripsis drives the evolution of gene amplification in cancer. Nature 591(7848):137–141. https://doi.org/10.1038/s41586-020-03064-z

    Article  CAS  Google Scholar 

  114. Matsui A, Ihara T, Suda H, Mikami H, Semba K (2013) Gene amplification: mechanisms and involvement in cancer. Biomol Concepts 4(6):567–582. https://doi.org/10.1515/bmc-2013-0026

    Article  CAS  Google Scholar 

  115. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10(7):445–457. https://doi.org/10.1038/nrm2720

    Article  CAS  Google Scholar 

  116. Ilina O, Friedl P (2009) Mechanisms of collective cell migration at a glance. J Cell Sci 122(Pt 18):3203–3208. https://doi.org/10.1242/jcs.036525

    Article  CAS  Google Scholar 

  117. De Pascalis C, Etienne-Manneville S (2017) Single and collective cell migration: the mechanics of adhesions. Mol Biol Cell 28(14):1833–1846. https://doi.org/10.1091/mbc.E17-03-0134

    Article  Google Scholar 

  118. Mayor R, Etienne-Manneville S (2016) The front and rear of collective cell migration. Nat Rev Mol Cell Biol 17(2):97–109. https://doi.org/10.1038/nrm.2015.14

    Article  CAS  Google Scholar 

  119. Aguilar-Cuenca R, Juanes-Garcia A, Vicente-Manzanares M (2014) Myosin II in mechanotransduction: master and commander of cell migration, morphogenesis, and cancer. Cell Mol Life Sci 71(3):479–492. https://doi.org/10.1007/s00018-013-1439-5

    Article  CAS  Google Scholar 

  120. Gasparski AN, Ozarkar S, Beningo KA (2017) Transient mechanical strain promotes the maturation of invadopodia and enhances cancer cell invasion in vitro. J Cell Sci 130(11):1965–1978. https://doi.org/10.1242/jcs.199760

    Article  CAS  Google Scholar 

  121. Eble JA, Niland S (2019) The extracellular matrix in tumor progression and metastasis. Clin Exp Metastasis 36(3):171–198. https://doi.org/10.1007/s10585-019-09966-1

    Article  CAS  Google Scholar 

  122. Cetera M, Ramirez-San Juan GR, Oakes PW, Lewellyn L, Fairchild MJ, Tanentzapf G, Gardel ML, Horne-Badovinac S (2014) Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation. Nat Commun 5(1):5511. https://doi.org/10.1038/ncomms6511

    Article  CAS  Google Scholar 

  123. Haigo SL, Bilder D (2011) Global tissue revolutions in a morphogenetic movement controlling elongation. Science 331(6020):1071–1074. https://doi.org/10.1126/science.1199424

    Article  CAS  Google Scholar 

  124. Gutzeit HO (1991) Organization and in vitro activity of microfilament bundles associated with the basement membrane of Drosophila follicles. Acta Histochem Suppl 41:201–210

    CAS  Google Scholar 

  125. Gutzeit HO (1990) The microfilament pattern in the somatic follicle cells of mid-vitellogenic ovarian follicles of Drosophila. Eur J Cell Biol 53(2):349–356

    CAS  Google Scholar 

  126. Gutzeit HO, Eberhardt W, Gratwohl E (1991) Laminin and basement membrane-associated microfilaments in wild-type and mutant Drosophila ovarian follicles. J Cell Sci 100(Pt 4):781–788. https://doi.org/10.1242/jcs.100.4.781

    Article  Google Scholar 

  127. Sherrard KM, Cetera M, Horne-Badovinac S (2021) DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila. elife 10. https://doi.org/10.7554/eLife.72881

  128. Bateman J, Reddy RS, Saito H, Van Vactor D (2001) The receptor tyrosine phosphatase Dlar and integrins organize actin filaments in the Drosophila follicular epithelium. Curr Biol 11(17):1317–1327. https://doi.org/10.1016/s0960-9822(01)00420-1

    Article  CAS  Google Scholar 

  129. Delon I, Brown NH (2009) The integrin adhesion complex changes its composition and function during morphogenesis of an epithelium. J Cell Sci 122(Pt 23):4363–4374. https://doi.org/10.1242/jcs.055996

    Article  CAS  Google Scholar 

  130. Bianco A, Poukkula M, Cliffe A, Mathieu J, Luque CM, Fulga TA, Rorth P (2007) Two distinct modes of guidance signalling during collective migration of border cells. Nature 448(7151):362–365. https://doi.org/10.1038/nature05965

    Article  CAS  Google Scholar 

  131. Poukkula M, Cliffe A, Changede R, Rorth P (2011) Cell behaviors regulated by guidance cues in collective migration of border cells. J Cell Biol 192(3):513–524. https://doi.org/10.1083/jcb.201010003

    Article  CAS  Google Scholar 

  132. Dai W, Guo X, Cao Y, Mondo JA, Campanale JP, Montell BJ, Burrous H, Streichan S, Gov N, Rappel WJ, Montell DJ (2020) Tissue topography steers migrating Drosophila border cells. Science 370(6519):987–990. https://doi.org/10.1126/science.aaz4741

    Article  CAS  Google Scholar 

  133. Aranjuez G, Burtscher A, Sawant K, Majumder P, McDonald JA (2016) Dynamic myosin activation promotes collective morphology and migration by locally balancing oppositional forces from surrounding tissue. Mol Biol Cell 27(12):1898–1910. https://doi.org/10.1091/mbc.E15-10-0744

    Article  CAS  Google Scholar 

  134. Majumder P, Aranjuez G, Amick J, McDonald JA (2012) Par-1 controls myosin-II activity through myosin phosphatase to regulate border cell migration. Curr Biol 22(5):363–372. https://doi.org/10.1016/j.cub.2012.01.037

    Article  CAS  Google Scholar 

  135. Lamb MC, Kaluarachchi CP, Lansakara TI, Mellentine SQ, Lan Y, Tivanski AV, Tootle TL (2021) Fascin limits Myosin activity within Drosophila border cells to control substrate stiffness and promote migration. elife 10:e69836. C69831 – elife 62021;69810:e69836. https://doi.org/10.7554/eLife.69836

    Article  CAS  Google Scholar 

  136. Fox EF, Lamb MC, Mellentine SQ, Tootle TL (2020) Prostaglandins regulate invasive, collective border cell migration. Mol Biol Cell 31(15):1584–1594. https://doi.org/10.1091/mbc.E19-10-0578

    Article  CAS  Google Scholar 

  137. Prasad M, Montell DJ (2007) Cellular and molecular mechanisms of border cell migration analyzed using time-lapse live-cell imaging. Dev Cell 12(6):997–1005. https://doi.org/10.1016/j.devcel.2007.03.021

    Article  CAS  Google Scholar 

  138. Prasad M, Wang X, He L, Montell DJ (2011) Border cell migration: a model system for live imaging and genetic analysis of collective cell movement. Methods Mol Biol 769:277–286. https://doi.org/10.1007/978-1-61779-207-6_19

    Article  CAS  Google Scholar 

  139. Sapir A, Schweitzer R, Shilo BZ (1998) Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis. Development 125(2):191–200. https://doi.org/10.1242/dev.125.2.191

    Article  CAS  Google Scholar 

  140. Peri F, Bokel C, Roth S (1999) Local Gurken signaling and dynamic MAPK activation during Drosophila oogenesis. Mech Dev 81(1–2):75–88. https://doi.org/10.1016/s0925-4773(98)00228-7

    Article  CAS  Google Scholar 

  141. Wasserman JD, Freeman M (1998) An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95(3):355–364. https://doi.org/10.1016/s0092-8674(00)81767-5

    Article  CAS  Google Scholar 

  142. Neuman-Silberberg FS, Schupbach T (1994) Dorsoventral axis formation in Drosophila depends on the correct dosage of the gene gurken. Development 120(9):2457–2463. https://doi.org/10.1242/dev.120.9.2457

    Article  CAS  Google Scholar 

  143. Dequier E, Souid S, Pal M, Maroy P, Lepesant JA, Yanicostas C (2001) Top-DER- and Dpp-dependent requirements for the Drosophila fos/kayak gene in follicular epithelium morphogenesis. Mech Dev 106(1–2):47–60. https://doi.org/10.1016/s0925-4773(01)00418-x

    Article  CAS  Google Scholar 

  144. Peri F, Roth S (2000) Combined activities of Gurken and decapentaplegic specify dorsal chorion structures of the Drosophila egg. Development 127(4):841–850. https://doi.org/10.1242/dev.127.4.841

    Article  CAS  Google Scholar 

  145. Queenan AM, Ghabrial A, Schupbach T (1997) Ectopic activation of torpedo/Egfr, a Drosophila receptor tyrosine kinase, dorsalizes both the eggshell and the embryo. Development 124(19):3871–3880. https://doi.org/10.1242/dev.124.19.3871

    Article  CAS  Google Scholar 

  146. Deng WM, Bownes M (1997) Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis. Development 124(22):4639–4647. https://doi.org/10.1242/dev.124.22.4639

    Article  CAS  Google Scholar 

  147. Twombly V, Blackman RK, Jin H, Graff JM, Padgett RW, Gelbart WM (1996) The TGF-beta signaling pathway is essential for Drosophila oogenesis. Development 122(5):1555–1565. https://doi.org/10.1242/dev.122.5.1555

    Article  CAS  Google Scholar 

  148. Dorman JB, James KE, Fraser SE, Kiehart DP, Berg CA (2004) bullwinkle is required for epithelial morphogenesis during Drosophila oogenesis. Dev Biol 267(2):320–341. https://doi.org/10.1016/j.ydbio.2003.10.020

    Article  CAS  Google Scholar 

  149. Ward EJ, Berg CA (2005) Juxtaposition between two cell types is necessary for dorsal appendage tube formation. Mech Dev 122(2):241–255. https://doi.org/10.1016/j.mod.2004.10.006

    Article  CAS  Google Scholar 

  150. Tran DH, Berg CA (2003) bullwinkle and shark regulate dorsal-appendage morphogenesis in Drosophila oogenesis. Development 130(25):6273–6282. https://doi.org/10.1242/dev.00854

    Article  CAS  Google Scholar 

  151. Cartwright JH, Piro O, Tuval I (2009) Fluid dynamics in developmental biology: moving fluids that shape ontogeny. HFSP J 3(2):77–93. https://doi.org/10.2976/1.3043738

    Article  Google Scholar 

  152. Quinlan ME (2016) Cytoplasmic streaming in the Drosophila oocyte. Annu Rev Cell Dev Biol 32:173–195. https://doi.org/10.1146/annurev-cellbio-111315-125416

    Article  CAS  Google Scholar 

  153. Gutzeit H, Koppa R (1982) Time-lapse film analysis of cytoplasmic streaming during late oogenesis of Drosophila. Development 67(1):101–111. https://doi.org/10.1242/dev.67.1.101

    Article  Google Scholar 

  154. Quinlan ME (2013) Direct interaction between two actin nucleators is required in Drosophila oogenesis. Development 140(21):4417–4425. https://doi.org/10.1242/dev.097337

    Article  CAS  Google Scholar 

  155. Serbus LR, Cha BJ, Theurkauf WE, Saxton WM (2005) Dynein and the actin cytoskeleton control kinesin-driven cytoplasmic streaming in Drosophila oocytes. Development 132(16):3743–3752. https://doi.org/10.1242/dev.01956

    Article  CAS  Google Scholar 

  156. Gutzeit HO (1986) The role of microfilaments in cytoplasmic streaming in Drosophila follicles. J Cell Sci 80:159–169. https://doi.org/10.1242/jcs.80.1.159

    Article  CAS  Google Scholar 

  157. Palacios IM, St Johnston D (2002) Kinesin light chain-independent function of the Kinesin heavy chain in cytoplasmic streaming and posterior localisation in the Drosophila oocyte. Development 129(23):5473–5485. https://doi.org/10.1242/dev.00119

    Article  CAS  Google Scholar 

  158. Dahlgaard K, Raposo AA, Niccoli T, St Johnston D (2007) Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev Cell 13(4):539–553. https://doi.org/10.1016/j.devcel.2007.09.003

    Article  CAS  Google Scholar 

  159. Becalska AN, Gavis ER (2009) Lighting up mRNA localization in Drosophila oogenesis. Development 136(15):2493–2503. https://doi.org/10.1242/dev.032391

    Article  CAS  Google Scholar 

  160. Kugler JM, Lasko P (2009) Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly (Austin) 3(1):15–28. https://doi.org/10.4161/fly.3.1.7751

    Article  CAS  Google Scholar 

  161. Lei L, Spradling AC (2016) Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science 352(6281):95–99. https://doi.org/10.1126/science.aad2156

    Article  CAS  Google Scholar 

  162. Niu W, Spradling AC (2022) Mouse oocytes develop in cysts with the help of nurse cells. Cell 185:2576. https://doi.org/10.1016/j.cell.2022.05.001

    Article  CAS  Google Scholar 

  163. Guild GM, Connelly PS, Shaw MK, Tilney LG (1997) Actin filament cables in Drosophila nurse cells are composed of modules that slide passively past one another during dumping. J Cell Biol 138(4):783–797. https://doi.org/10.1083/jcb.138.4.783

    Article  CAS  Google Scholar 

  164. Huelsmann S, Ylänne J, Brown Nicholas H (2013) Filopodia-like actin cables position nuclei in association with perinuclear actin in Drosophila nurse cells. Dev Cell 26(6):604–615. https://doi.org/10.1016/j.devcel.2013.08.014

    Article  CAS  Google Scholar 

  165. Wheatley S, Kulkarni S, Karess R (1995) Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121(6):1937–1946

    Article  CAS  Google Scholar 

  166. Imran Alsous J, Romeo N, Jackson JA, Mason FM, Dunkel J, Martin AC (2021) Dynamics of hydraulic and contractile wave-mediated fluid transport during Drosophila oogenesis. Proc Natl Acad Sci U S A 118(10). https://doi.org/10.1073/pnas.2019749118

  167. Cooley L, Verheyen E, Ayers K (1992) chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69(1):173–184. https://doi.org/10.1016/0092-8674(92)90128-y

    Article  CAS  Google Scholar 

  168. Cant K, Knowles BA, Mooseker MS, Cooley L (1994) Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J Cell Biol 125(2):369–380. https://doi.org/10.1083/jcb.125.2.369

    Article  CAS  Google Scholar 

  169. Gates J, Nowotarski SH, Yin H, Mahaffey JP, Bridges T, Herrera C, Homem CC, Janody F, Montell DJ, Peifer M (2009) Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev Biol 333(1):90–107. https://doi.org/10.1016/j.ydbio.2009.06.030

    Article  CAS  Google Scholar 

  170. Tootle TL (2013) Genetic insights into the in vivo functions of prostaglandin signaling. Int J Biochem Cell Biol 45(8):1629–1632. https://doi.org/10.1016/j.biocel.2013.05.008

    Article  CAS  Google Scholar 

  171. Tootle TL, Spradling AC (2008) Drosophila Pxt: a cyclooxygenase-like facilitator of follicle maturation. Development 135(5):839–847. https://doi.org/10.1242/dev.017590

    Article  CAS  Google Scholar 

  172. Groen CM, Spracklen AJ, Fagan TN, Tootle TL (2012) Drosophila Fascin is a novel downstream target of prostaglandin signaling during actin remodeling. Mol Biol Cell 23(23):4567–4578. https://doi.org/10.1091/mbc.E12-05-0417

    Article  CAS  Google Scholar 

  173. Spracklen AJ, Kelpsch DJ, Chen X, Spracklen CN, Tootle TL (2014) Prostaglandins temporally regulate cytoplasmic actin bundle formation during Drosophila oogenesis. Mol Biol Cell 25(3):397–411. https://doi.org/10.1091/mbc.E13-07-0366

    Article  CAS  Google Scholar 

  174. Spracklen AJ, Lamb MC, Groen CM, Tootle TL (2019) Pharmaco-genetic screen to uncover actin regulators targeted by prostaglandins during Drosophila oogenesis. G3 (Bethesda) 9(11):3555–3565. https://doi.org/10.1534/g3.119.400704

    Article  CAS  Google Scholar 

  175. Hamm DC, Harrison MM (2018) Regulatory principles governing the maternal-to-zygotic transition: insights from Drosophila melanogaster. Open Biol 8(12):180183. https://doi.org/10.1098/rsob.180183

    Article  CAS  Google Scholar 

  176. Welte MA (2015) As the fat flies: the dynamic lipid droplets of Drosophila embryos. Biochim Biophys Acta 1851(9):1156–1185. https://doi.org/10.1016/j.bbalip.2015.04.002

    Article  CAS  Google Scholar 

  177. Brusentsev EY, Mokrousova VI, Igonina TN, Rozhkova IN, Amstislavsky SY (2019) Role of lipid droplets in the development of oocytes and preimplantation embryos in mammals. Russ J Dev Biol 50(5):230–237. https://doi.org/10.1134/S1062360419050102

    Article  CAS  Google Scholar 

  178. Dunning KR, Russell DL, Robker RL (2014) Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation. Reproduction 148(1):R15–R27. https://doi.org/10.1530/REP-13-0251

    Article  CAS  Google Scholar 

  179. Ami D, Mereghetti P, Natalello A, Doglia SM, Zanoni M, Redi CA, Monti M (2011) FTIR spectral signatures of mouse antral oocytes: molecular markers of oocyte maturation and developmental competence. Biochim Biophys Acta 1813(6):1220–1229. https://doi.org/10.1016/j.bbamcr.2011.03.009

    Article  CAS  Google Scholar 

  180. Cardozo E, Pavone ME, Hirshfeld-Cytron JE (2011) Metabolic syndrome and oocyte quality. Trends Endocrinol Metab 22(3):103–109. https://doi.org/10.1016/j.tem.2010.12.002

    Article  CAS  Google Scholar 

  181. Jungheim ES, Schoeller EL, Marquard KL, Louden ED, Schaffer JE, Moley KH (2010) Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 151(8):4039–4046. https://doi.org/10.1210/en.2010-0098

    Article  CAS  Google Scholar 

  182. Marei WFA, Smits A, Mohey-Elsaeed O, Pintelon I, Ginneberge D, Bols PEJ, Moerloose K, Leroy J (2020) Differential effects of high fat diet-induced obesity on oocyte mitochondrial functions in inbred and outbred mice. Sci Rep 10(1):9806. https://doi.org/10.1038/s41598-020-66702-6

    Article  CAS  Google Scholar 

  183. Prates EG, Nunes JT, Pereira RM (2014) A role of lipid metabolism during cumulus-oocyte complex maturation: impact of lipid modulators to improve embryo production. Mediat Inflamm 2014:692067. https://doi.org/10.1155/2014/692067

    Article  CAS  Google Scholar 

  184. Khajeh M, Rahbarghazi R, Nouri M, Darabi M (2017) Potential role of polyunsaturated fatty acids, with particular regard to the signaling pathways of arachidonic acid and its derivatives in the process of maturation of the oocytes: contemporary review. Biomed Pharmacother 94:458–467. https://doi.org/10.1016/j.biopha.2017.07.140

    Article  CAS  Google Scholar 

  185. Cermelli S, Guo Y, Gross SP, Welte MA (2006) The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr Biol 16(18):1783–1795. https://doi.org/10.1016/j.cub.2006.07.062

    Article  CAS  Google Scholar 

  186. Li Z, Thiel K, Thul Peter J, Beller M, Kühnlein Ronald P, Welte Michael A (2012) Lipid droplets control the maternal histone supply of Drosophila embryos. Curr Biol 22(22):2104–2113. https://doi.org/10.1016/j.cub.2012.09.018

    Article  CAS  Google Scholar 

  187. Li Z, Johnson Matthew R, Ke Z, Chen L, Welte Michael A (2014) Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development. Curr Biol 24(13):1485–1491. https://doi.org/10.1016/j.cub.2014.05.022

    Article  CAS  Google Scholar 

  188. Johnson MR, Stephenson RA, Ghaemmaghami S, Welte MA (2018) Developmentally regulated H2Av buffering via dynamic sequestration to lipid droplets in Drosophila embryos. elife 7:e36021. C36021 – elife 32018;36027:e36021. https://doi.org/10.7554/eLife.36021

    Article  Google Scholar 

  189. Sieber MH, Spradling AC (2015) Steroid signaling establishes a female metabolic state and regulates SREBP to control oocyte lipid accumulation. Curr Biol 25(8):993–1004. https://doi.org/10.1016/j.cub.2015.02.019

    Article  CAS  Google Scholar 

  190. Parra-Peralbo E, Culi J (2011) Drosophila lipophorin receptors mediate the uptake of neutral lipids in oocytes and imaginal disc cells by an endocytosis-independent mechanism. PLoS Genet 7(2):e1001297. https://doi.org/10.1371/journal.pgen.1001297

    Article  CAS  Google Scholar 

  191. Rodriguez-Vazquez M, Vaquero D, Parra-Peralbo E, Mejia-Morales JE, Culi J (2015) Drosophila lipophorin receptors recruit the lipoprotein LTP to the plasma membrane to mediate lipid uptake. PLoS Genet 11(6):e1005356. https://doi.org/10.1371/journal.pgen.1005356

    Article  CAS  Google Scholar 

  192. Buszczak M, Lu X, Segraves WA, Chang TY, Cooley L (2002) Mutations in the midway gene disrupt a Drosophila acyl coenzyme a: diacylglycerol acyltransferase. Genetics 160(4):1511–1518. https://doi.org/10.1093/genetics/160.4.1511

    Article  CAS  Google Scholar 

  193. Pompeia C, Lima T, Curi R (2003) Arachidonic acid cytotoxicity: can arachidonic acid be a physiological mediator of cell death? Cell Biochem Funct 21(2):97–104. https://doi.org/10.1002/cbf.1012

    Article  CAS  Google Scholar 

  194. Zhang N, Wang L, Luo G, Tang X, Ma L, Zheng Y, Liu S, Price C, Jiang Z (2019) Arachidonic acid regulation of intracellular signaling pathways and target gene expression in bovine ovarian granulosa cells. Animals (Basel) 9(6). https://doi.org/10.3390/ani9060374

  195. Giedt MS, Thomalla JM, Johnson MR, Lai ZW, Tootle TL, Welte MA (2022) Adipose triglyceride lipase promotes prostaglandin-dependent actin remodeling by regulating substrate release from lipid droplets. bioRxiv:2021.2008.2002.454724. https://doi.org/10.1101/2021.08.02.454724

  196. Drummond-Barbosa D, Spradling AC (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol 231(1):265–278. https://doi.org/10.1006/dbio.2000.0135

    Article  CAS  Google Scholar 

  197. Hou YC, Chittaranjan S, Barbosa SG, McCall K, Gorski SM (2008) Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis. J Cell Biol 182(6):1127–1139. https://doi.org/10.1083/jcb.200712091

    Article  Google Scholar 

  198. Nezis IP, Lamark T, Velentzas AD, Rusten TE, Bjorkoy G, Johansen T, Papassideri IS, Stravopodis DJ, Margaritis LH, Stenmark H, Brech A (2009) Cell death during Drosophila melanogaster early oogenesis is mediated through autophagy. Autophagy 5(3):298–302. https://doi.org/10.4161/auto.5.3.7454

    Article  CAS  Google Scholar 

  199. Besse F, Pret AM (2003) Apoptosis-mediated cell death within the ovarian polar cell lineage of Drosophila melanogaster. Development 130(5):1017–1027. https://doi.org/10.1242/dev.00313

    Article  CAS  Google Scholar 

  200. Khammari A, Agnes F, Gandille P, Pret AM (2011) Physiological apoptosis of polar cells during Drosophila oogenesis is mediated by Hid-dependent regulation of Diap1. Cell Death Differ 18(5):793–805. https://doi.org/10.1038/cdd.2010.141

    Article  CAS  Google Scholar 

  201. Borensztejn A, Mascaro A, Wharton KA (2018) JAK/STAT signaling prevents excessive apoptosis to ensure maintenance of the interfollicular stalk critical for Drosophila oogenesis. Dev Biol 438(1):1–9. https://doi.org/10.1016/j.ydbio.2018.03.018

    Article  CAS  Google Scholar 

  202. Pritchett TL, McCall K (2012) Role of the insulin/Tor signaling network in starvation-induced programmed cell death in Drosophila oogenesis. Cell Death Differ 19(6):1069–1079. https://doi.org/10.1038/cdd.2011.200

    Article  CAS  Google Scholar 

  203. Chao S, Nagoshi RN (1999) Induction of apoptosis in the germline and follicle layer of Drosophila egg chambers. Mech Dev 88(2):159–172. https://doi.org/10.1016/s0925-4773(99)00183-5

    Article  CAS  Google Scholar 

  204. Timmons AK, Mondragon AA, Schenkel CE, Yalonetskaya A, Taylor JD, Moynihan KE, Etchegaray JI, Meehan TL, McCall K (2016) Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary. Proc Natl Acad Sci U S A 113(9):E1246–E1255. https://doi.org/10.1073/pnas.1522830113

    Article  CAS  Google Scholar 

  205. Yalonetskaya A, Mondragon AA, Hintze ZJ, Holmes S, McCall K (2020) Nuclear degradation dynamics in a nonapoptotic programmed cell death. Cell Death Differ 27(2):711–724. https://doi.org/10.1038/s41418-019-0382-x

    Article  CAS  Google Scholar 

  206. Mondragon AA, Yalonetskaya A, Ortega AJ, Zhang Y, Naranjo O, Elguero J, Chung WS, McCall K (2019) Lysosomal machinery drives extracellular acidification to direct non-apoptotic cell death. Cell Rep 27(1):11–19 e13. https://doi.org/10.1016/j.celrep.2019.03.034

    Article  CAS  Google Scholar 

  207. Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS (2006) Autophagy is required for the degeneration of the ovarian follicular epithelium in higher Diptera. Autophagy 2(4):297–298. https://doi.org/10.4161/auto.2858

    Article  CAS  Google Scholar 

  208. Nezis IP, Stravopodis DJ, Margaritis LH, Papassideri IS (2006) Programmed cell death of follicular epithelium during the late developmental stages of oogenesis in the fruit flies Bactrocera oleae and Ceratitis capitata (Diptera, Tephritidae) is mediated by autophagy. Develop Growth Differ 48(3):189–198. https://doi.org/10.1111/j.1440-169X.2006.00856.x

    Article  Google Scholar 

  209. Buszczak M, Signer RA, Morrison SJ (2014) Cellular differences in protein synthesis regulate tissue homeostasis. Cell 159(2):242–251. https://doi.org/10.1016/j.cell.2014.09.016

    Article  CAS  Google Scholar 

  210. Zhang Q, Shalaby NA, Buszczak M (2014) Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science 343(6168):298–301. https://doi.org/10.1126/science.1246384

    Article  CAS  Google Scholar 

  211. Sanchez CG, Teixeira FK, Czech B, Preall JB, Zamparini AL, Seifert JR, Malone CD, Hannon GJ, Lehmann R (2016) Regulation of ribosome biogenesis and protein synthesis controls germline stem cell differentiation. Cell Stem Cell 18(2):276–290. https://doi.org/10.1016/j.stem.2015.11.004

    Article  CAS  Google Scholar 

  212. Martin ET, Blatt P, Nguyen E, Lahr R, Selvam S, Yoon HAM, Pocchiari T, Emtenani S, Siekhaus DE, Berman A, Fuchs G, Rangan P (2022) A translation control module coordinates germline stem cell differentiation with ribosome biogenesis during drosophila oogenesis. Dev Cell 57(7):883–900 e810. https://doi.org/10.1016/j.devcel.2022.03.005

    Article  CAS  Google Scholar 

  213. Kong J, Han H, Bergalet J, Bouvrette LPB, Hernandez G, Moon NS, Vali H, Lecuyer E, Lasko P (2019) A ribosomal protein S5 isoform is essential for oogenesis and interacts with distinct RNAs in Drosophila melanogaster. Sci Rep 9(1):13779. https://doi.org/10.1038/s41598-019-50357-z

    Article  CAS  Google Scholar 

  214. Jang S, Lee J, Mathews J, Ruess H, Williford AO, Rangan P, Betran E, Buszczak M (2021) The Drosophila ribosome protein S5 paralog RpS5b promotes germ cell and follicle cell differentiation during oogenesis. Development 148(19). https://doi.org/10.1242/dev.199511

  215. Hopes T, Norris K, Agapiou M, McCarthy CGP, Lewis PA, O’Connell MJ, Fontana J, Aspden JL (2022) Ribosome heterogeneity in Drosophila melanogaster gonads through paralog-switching. Nucleic Acids Res 50(4):2240–2257. https://doi.org/10.1093/nar/gkab606

    Article  CAS  Google Scholar 

  216. Green NM, Kimble GC, Talbot DE, Tootle TL (2021) Nuclear actin. In: eLS. Wiley, pp 958–967. https://doi.org/10.1002/9780470015902.a0028471

    Chapter  Google Scholar 

  217. Kelpsch DJ, Tootle TL (2018) Nuclear actin: from discovery to function. Anat Rec (Hoboken) 301(12):1999–2013. https://doi.org/10.1002/ar.23959

    Article  CAS  Google Scholar 

  218. Misu S, Takebayashi M, Miyamoto K (2017) Nuclear actin in development and transcriptional reprogramming. Front Genet 8:27. https://doi.org/10.3389/fgene.2017.00027

    Article  CAS  Google Scholar 

  219. Klages-Mundt NL, Kumar A, Zhang Y, Kapoor P, Shen X (2018) The nature of actin-family proteins in chromatin-modifying complexes. Front Genet 9:398. https://doi.org/10.3389/fgene.2018.00398

    Article  CAS  Google Scholar 

  220. Spracklen AJ, Fagan TN, Lovander KE, Tootle TL (2014) The pros and cons of common actin labeling tools for visualizing actin dynamics during Drosophila oogenesis. Dev Biol 393(2):209–226. https://doi.org/10.1016/j.ydbio.2014.06.022

    Article  CAS  Google Scholar 

  221. Wineland DM, Kelpsch DJ, Tootle TL (2018) Multiple pools of nuclear actin. Anat Rec (Hoboken) 301(12):2014–2036. https://doi.org/10.1002/ar.23964

    Article  CAS  Google Scholar 

  222. Kelpsch DJ, Groen CM, Fagan TN, Sudhir S, Tootle TL (2016) Fascin regulates nuclear actin during Drosophila oogenesis. Mol Biol Cell 27(19):2965–2979. https://doi.org/10.1091/mbc.E15-09-0634

    Article  CAS  Google Scholar 

  223. Sokolova M, Moore HM, Prajapati B, Dopie J, Meriläinen L, Honkanen M, Matos RC, Poukkula M, Hietakangas V, Vartiainen MK (2018) Nuclear actin is required for transcription during Drosophila oogenesis. iScience 9:63–70. https://doi.org/10.1016/j.isci.2018.10.010

    Article  CAS  Google Scholar 

  224. Hudson AM, Mannix KM, Gerdes JA, Kottemann MC, Cooley L (2019) Targeted substrate degradation by Kelch controls the actin cytoskeleton during ring canal expansion. Development 146(1). https://doi.org/10.1242/dev.169219

  225. Mannix KM, Starble RM, Kaufman RS, Cooley L (2019) Proximity labeling reveals novel interactomes in live Drosophila tissue. Development 146(14). https://doi.org/10.1242/dev.176644

  226. Zhang B, Zhang Y, Liu J-L (2021) Highly effective proximate labeling in drosophila. G3 Genes|Genomes|Genetics 11(5). https://doi.org/10.1093/g3journal/jkab077

  227. Liu J-L (2016) The cytoophidium and its kind: filamentation and compartmentation of metabolic enzymes. Annu Rev Cell Dev Biol 32(1):349–372. https://doi.org/10.1146/annurev-cellbio-111315-124907

    Article  CAS  Google Scholar 

  228. Liu JL (2010) Intracellular compartmentation of CTP synthase in Drosophila. J Genet Genomics 37(5):281–296. https://doi.org/10.1016/S1673-8527(09)60046-1

    Article  CAS  Google Scholar 

  229. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK (1997) Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91(2):197–208. https://doi.org/10.1016/s0092-8674(00)80402-x

    Article  CAS  Google Scholar 

  230. Langenbach R, Loftin C, Lee C, Tiano H (1999) Cyclooxygenase knockout mice: models for elucidating isoform-specific functions. Biochem Pharmacol 58(8):1237–1246. https://doi.org/10.1016/s0006-2952(99)00158-6

    Article  CAS  Google Scholar 

  231. Takahashi T, Morrow JD, Wang H, Dey SK (2006) Cyclooxygenase-2-derived prostaglandin E(2) directs oocyte maturation by differentially influencing multiple signaling pathways. J Biol Chem 281(48):37117–37129. https://doi.org/10.1074/jbc.M608202200

    Article  CAS  Google Scholar 

  232. Pall M, Friden BE, Brannstrom M (2001) Induction of delayed follicular rupture in the human by the selective COX-2 inhibitor rofecoxib: a randomized double-blind study. Hum Reprod 16(7):1323–1328. https://doi.org/10.1093/humrep/16.7.1323

    Article  CAS  Google Scholar 

  233. Droujinine IA, Perrimon N (2016) Interorgan communication pathways in physiology: focus on Drosophila. Annu Rev Genet 50:539–570. https://doi.org/10.1146/annurev-genet-121415-122024

    Article  CAS  Google Scholar 

  234. Armstrong AR (2020) Drosophila melanogaster as a model for nutrient regulation of ovarian function. Reproduction 159(2):R69–R82. https://doi.org/10.1530/REP-18-0593

    Article  CAS  Google Scholar 

  235. Barth JM, Szabad J, Hafen E, Kohler K (2011) Autophagy in Drosophila ovaries is induced by starvation and is required for oogenesis. Cell Death Differ 18(6):915–924. https://doi.org/10.1038/cdd.2010.157

    Article  CAS  Google Scholar 

  236. LaFever L, Drummond-Barbosa D (2005) Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309(5737):1071–1073. https://doi.org/10.1126/science.1111410

    Article  CAS  Google Scholar 

  237. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 12(15):1293–1300. https://doi.org/10.1016/s0960-9822(02)01043-6

    Article  CAS  Google Scholar 

  238. Armstrong AR, Drummond-Barbosa D (2018) Insulin signaling acts in adult adipocytes via GSK-3beta and independently of FOXO to control Drosophila female germline stem cell numbers. Dev Biol 440(1):31–39. https://doi.org/10.1016/j.ydbio.2018.04.028

    Article  CAS  Google Scholar 

  239. Armstrong AR, Laws KM, Drummond-Barbosa D (2014) Adipocyte amino acid sensing controls adult germline stem cell number via the amino acid response pathway and independently of Target of Rapamycin signaling in Drosophila. Development 141(23):4479–4488. https://doi.org/10.1242/dev.116467

    Article  CAS  Google Scholar 

  240. Matsuoka S, Armstrong AR, Sampson LL, Laws KM, Drummond-Barbosa D (2017) Adipocyte metabolic pathways regulated by diet control the female germline stem cell lineage in Drosophila melanogaster. Genetics 206(2):953–971. https://doi.org/10.1534/genetics.117.201921

    Article  CAS  Google Scholar 

  241. Weaver LN, Drummond-Barbosa D (2019) The nuclear receptor seven up functions in adipocytes and oenocytes to control distinct steps of Drosophila oogenesis. Dev Biol 456(2):179–189. https://doi.org/10.1016/j.ydbio.2019.08.015

    Article  CAS  Google Scholar 

  242. Weaver LN, Drummond-Barbosa D (2021) Hormone receptor 4 is required in muscles and distinct ovarian cell types to regulate specific steps of Drosophila oogenesis. Development 148(5). https://doi.org/10.1242/dev.198663

  243. Espey LL, Richards JS (2006) Chapter 11 – Ovulation. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction, 3rd edn. Academic Press, St Louis, pp 425–474. https://doi.org/10.1016/B978-012515400-0/50016-6

    Chapter  Google Scholar 

  244. Duffy DM, Ko C, Jo M, Brannstrom M, Curry TE Jr (2019) Ovulation: parallels with inflammatory processes. Endocr Rev 40(2):369–416. https://doi.org/10.1210/er.2018-00075

    Article  Google Scholar 

  245. Fan H-Y, Liu Z, Mullany LK, Richards JS (2012) Consequences of RAS and MAPK activation in the ovary: the good, the bad and the ugly. Mol Cell Endocrinol 356(1):74–79. https://doi.org/10.1016/j.mce.2011.12.005

    Article  CAS  Google Scholar 

  246. Robker RL, Hennebold JD, Russell DL (2018) Coordination of ovulation and oocyte maturation: a good egg at the right time. Endocrinology 159(9):3209–3218. https://doi.org/10.1210/en.2018-00485

    Article  CAS  Google Scholar 

  247. Li W, Young JF, Sun J (2018) NADPH oxidase-generated reactive oxygen species in mature follicles are essential for Drosophila ovulation. Proc Natl Acad Sci 115(30):7765–7770. https://doi.org/10.1073/pnas.1800115115

    Article  CAS  Google Scholar 

  248. Deady LD, Shen W, Mosure SA, Spradling AC, Sun J (2015) Matrix metalloproteinase 2 is required for ovulation and corpus luteum formation in Drosophila. PLoS Genet 11(2):e1004989

    Article  Google Scholar 

  249. Knapp E, Sun J (2017) Steroid signaling in mature follicles is important for Drosophila ovulation. Proc Natl Acad Sci U S A 114(4):699–704. https://doi.org/10.1073/pnas.1614383114

    Article  CAS  Google Scholar 

  250. Deady LD, Sun J (2015) A follicle rupture assay reveals an essential role for follicular adrenergic signaling in Drosophila ovulation. PLoS Genet 11(10):e1005604

    Article  Google Scholar 

  251. Jiang K, Zhang J, Huang Y, Wang Y, Xiao S, Hadden MK, Woodruff TK, Sun J (2021) A platform utilizing Drosophila ovulation for nonhormonal contraceptive screening. Proc Natl Acad Sci U S A 118(28). https://doi.org/10.1073/pnas.2026403118

  252. Tootle TL, Hoffmann DS, Allen AK, Spracklen AJ, Groen CM, Kelpsch DJ (2019) Research and teaching: mini-course-based undergraduate research experience: impact on student understanding of STEM research and interest in STEM programs. J Coll Sci Teach. 48(6)

    Google Scholar 

  253. Cortes JA, Swanson CI (2023) Using Drosophila oogenesis in the classroom to increase student participation in biomedical research. In: Tootle TL, Giedt MS (eds) Drosophila oogenesis. Methods in molecular biology. Springer Nature, New York

    Google Scholar 

  254. Ruiz-Whalen DM, P. Aichele CP, Dywon ER et al (2023) Drosophila oogenesis. Methods in Molecular Biology. Springer Nature, New York

    Google Scholar 

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Acknowledgments

We thank the Tootle lab for helpful discussions and careful review of the manuscript. The following sources provided funding for this project: National Institutes of Health R35 GM144057 (T.L.T.) and National Science Foundation MCB 2017797 (T.L.T.). M.S.G. is supported by NIH T32 CA078586 Free Radical and Radiation Biology, University of Iowa.

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Giedt, M.S., Tootle, T.L. (2023). The Vast Utility of Drosophila Oogenesis. In: Giedt, M.S., Tootle, T.L. (eds) Drosophila Oogenesis. Methods in Molecular Biology, vol 2626. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2970-3_1

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