Tools to analyze the organization and formation of the germline cyst in zebrafish oogenesis

link之家

链接快照平台

输入网页链接，自动生成快照
标签化管理网页链接

Protocol for volume reconstruction in Imaris

1. From the Imaris homepage, open the working directory and import the labels in the Imaris Arena Tab.
2. Set the voxel size according to the raw image data.
- File>Image Preferences
3. In the Surpass Tree Item Menu, select the ‘Create New Surface’ tool from the Surpass Tree Item Menu.
4. In the Creation dialog box, uncheck the ‘Classify Surfaces’ and ‘Track Surface over time’ options.
5. Select ‘Absolute Intensity’ and select he area around the peak in the histogram to segment.
6. Set the desired color and transparency for the surface created in step 5 ( Fig. 2 A, right).
7. Repeat steps 3-6 for all surfaces of interest in the labeled image. Save the surface by exporting as ‘Scenes’.
8. Import the raw dataset in the Surpass workspace and the surfaces saved in step 7.
- File>Import Scenes
9. Add ‘Orthoslicer’ from the Surpass Tree Item Menu. Set the slice of choice.
10. Note: Uncheck ‘Volume’ in Surpass Tree Items to hide the raw dataset.
11. Go to the ‘3D Animation’ tab from the Surpass workspace menu.
12. Adjust the scene in the desired orientation.
13. Add the Animation option and the total number of frames.
14. Hit ‘Record’, and select the directory for saving the animation ( Fig. 2 B-G).

Deep learning-assisted instance segmentation

Sample preparation for live time-lapse imaging and immunostaining was previously described ( Elkouby and Mullins, 2017b ; Mytlis and Elkouby, 2021 ; Mytlis et al., 2022 ). Images were acquired on a Zeiss LSM 880 confocal microscope using a 40× lens. The acquisition setting was set between samples and experiments to: xy resolution=1104×1104 pixels, 12-bit, 2× sampling averaging, pixel dwell time=0.59 s, zoom=0.8×, pinhole adjusted to 1.1 μm of z thickness, increments between images in stacks 0.53 μm, laser power and gain set in an antibody-dependent manner to 7-11% and 400-650, respectively, and below saturation conditions.

Protocol for setting up the working environment

1. Install Anaconda environment manager ( https://www.anaconda.com/ ).
2. Create a virtual environment in Anaconda.
3. Install Jupyter Notebook.
4. Download the Jupyter notebooks for StarDist ( https://github.com/stardist/stardist.git ) and Cellpose ( https://github.com/MouseLand/cellpose.git ) from the respective GitHub repositories.
5. Launch the Anaconda Terminal.

Protocol for preparing the training dataset for StarDist

1. Open the images in Fiji. Using the crop tool, crop regions of 256×256 or 128×128.
2. Save the Crop regions in a directory named ‘Training Images’.
3. Open Training Images in Fiji and annotate all the structures of interest using Labkit ( Arzt et al., 2022 ) or TrakEM2 ( Cardona et al., 2012 ).
4. Export and save the labeled images in a directory named ‘Training Mask’.

Protocol for model training and predictions

1. From the Anaconda Terminal, activate the respective environment.
2. Launch Jupyter Notebook and browse to the Jupyter notebook downloaded earlier.
3. In the Notebook, enter the path to ‘Training Images’ and ‘Training Mask’ directories in the respective fields.
4. Enter the model name and the directory path in which to save it.
5. Train the model until the training curve plateaus.
6. Evaluate the quality of the model by looking at:
1. Inspection of loss function. The validation loss and training loss curves should converge at the end of training for successful model training. If the validation loss increases with the decrease of training loss, the model is overfitting and the training dataset should be increased.
2. ‘Intersection of Union (IOU)’. The closer to 1, the better the performance. (If IOU is less, the training dataset should be increased.)

Once the model is trained it can be further used to make predictions on unseen datasets.

7. Enter the path to unseen datasets in Jupyter Notebook ( Fig. 3 B). Choose the Custom Model.
8. Run the program to make predictions on the unseen dataset using the above created model ( Fig. 3 C).

Protocol for cell segmentation using Cellpose

1. Launch a new Jupyter browser in the Cellpose environment using the Anaconda environment manager.
2. Open a Cellpose notebook in the Jupyter notebook.
3. Provide the directory path for images to be predicted ( Fig. 3 B) and save results.
4. Choose the provided model.
5. Set do_3d=True for segmentation done using 3D image or set do_3d=False for 2D segmentation and stitching of labels.
6. Set the minimum diameter of cell in pixels, if do_3d=True in step 5.
7. Proceed to segmentation.

Protocol for features extraction from label images

1. Import the predicted label images into Fiji.
2. Set the voxel size to raw data voxel size from properties.
- Fiji>Image>Properties
3. Correct the labels for misidentification using the label editor from the MorphoLibJ plugin ( Legland et al., 2016 ).
4. Extract the features from the 3D label images using plugin ‘Analyze Regions 3D’ from MorphoLibJ ( Legland et al., 2016 ) ( Fig. 3 E).
5. Set the Glasbey colormap LUT on the predicted label image from LUT menu.
- Fiji>Image>Lookup Tables>Glasbey on Dark
6. Open 3D viewer from the Fiji Plugins menu.
- Fiji>Plugins>3D viewer
7. Select the filename from the drop-down menu in the import dialog box. Import as Volume.
8. Visualize the spatial arrangement of segmented structures in volume reconstruction.
9. Volume reconstruction can also be generated by importing the label images in to the Imaris Workspace followed by creating a surface using the ‘Surface Creation Tool’ ( Fig. 3 D).

Laser-induced ablation of cyst cell organelles

Ovary mounting and culture

Ovaries were isolated as described previously ( Elkouby and Mullins, 2017b ; Mytlis et al., 2022 ) ( Fig. 4 A1,2). A dissecting dish [made in-house by casting plastic Petri dishes with animal-proof nontoxic silicone for reusable dishes or 2-3% agarose in Hank's solution (0.137 M NaCl, 5.4 mM KCl, 0.25 mM Na ₂ HPO ₄ , 0.44 mM KH ₂ PO ₄ , 1.3 mM CaCl ₂ , 1.0 mM MgSO ₄ , 4.2 mM NaHCO ₃ ) for single-use dishes], micro-scissors and Forceps #5 (Sigma-Aldrich) were used for ovary dissection (for details, see Mytlis and Elkouby (2021) . Dissected ovaries were kept in a glass 9-well plate at 28°C until mounting.

In a glass-bottom dish (60 µ, ibidi), ∼150 µl of mounting solution was added (agarose layer 1) and left until it started to solidify. Ovaries were transferred carefully to the mounting solution (agarose layer 1) in the glass-bottom dish using forceps ( Fig. 4 A3). The ovaries were gently pushed to the bottom of the dish, avoiding curls, as described previously ( Elkouby and Mullins, 2017b ; Mytlis et al., 2022 ), and allowed to rest until the agar solidified ( Fig. 4 A3). Once the agar had solidified, more mounting solution was added (agarose layer 2) until it covered the solidified mounting solution containing the ovaries ( Fig. 4 A3), and then allowed to rest for the agar to solidify properly. An adequate volume (∼1.5 ml) of HL-15 medium (60% Hanks, 40% L-15, 1:100 GlutaMAX) was added to the cell culture dish ( Fig. 4 A3). Note that HL-15 should be stored at 4°C. L-15 (2× stock) was used without L-glutamine and Phenol Red. L-glutamine is not stable and should be added fresh from a stock (GlutaMAX 100×; Gibco, 35050-061; store at room temperature). Mounted ovaries were kept at 28°C until use. Agarose layers 1 and 2 were prepared by mixing 500 µl of Mounting Solution A (1% low-melt agarose in Hank's Solution; store at 4°C) with 500 µl of Mounting Solution B [490 µl of 2× L-15 (no L-glutamine, no Phenol Red) and 10 µl GlutaMax; equivalent to a 2× HL-15 solution; make fresh and keep at 28°C] to make a final solution of 0.5% low-melt agarose in 1× HL-15 (gelling temperature, 27.4°C).

Laser-induced ablation

Laser excisions were performed using a Leica TCS SP8 MP two-photon microscope with a 25× objective and equipped with an incubation chamber set to 28°C. The glass-bottom dish with the cultured ovaries was mounted on the microscope stage inside the incubator chamber. The region of interest (ROI) was located using a 25× objective. The desired zoomed view of the ROI was obtained using ‘Digital Zoom’ and ‘Capture a Live View’. and draw The ROI for ablation was drawn on the above acquired image using ‘ROI tools’. Once the ROI was marked, the imaging time parameters were set as follows: pre-ablation timelapse acquisition 60 s; laser stimulation of the ROI 60 s at laser power 2.0-8.0% out of a power source of ∼3 W; post-ablation timelapse acquisition 600 s. These steps were repeated for each ROI. Note that only one ablation per cyst should be performed to avoid cell and tissue damage. Ovaries (4-6 wpf) should be mounted in the cell culture dish towards the center, leaving enough space for the lens to move around.

Software

Fiji was used for the preprocessing of image datasets and post processing of labeled images. Anaconda, an open-source distribution of Python was used specifically to maintain a dedicated virtual environment with the desired versions of Python packages installed. Jupyter Notebook, a web-based interactive computational environment for creating and sharing documents, was used to run deep-learning algorithms. Cellpose ( Stringer et al., 2021 ) is an anatomical segmentation algorithm written in Python3. StarDist ( Weigert et al., 2020 ; Schmidt et al., 2018 ) is a deep learning based-algorithm for star-convex object detection for 2D and 3D images. Imaris is a commercial microscopy image analysis software.

Supplementary Material

Supplementary information

Click here for additional data file. ^{(1.7M, pdf)}

Acknowledgements

We thank A. Beckett, from the Biomedical EM unit at the University of Liverpool, for her help in processing our samples for SBF-SEM imaging. We also thank Z. Manevich, from the Faculty of Medicine Microscopy Core at the Hebrew University, and Y. Addadi, from the core facility at the Weizmann Institute, for their support of our multi-photon microscopy operation in our laser ablation experiments.

Footnotes

Author contributions

Conceptualization: V.K., Y.M.E.; Methodology: V.K., Y.M.E.; Validation: V.K.; Formal analysis: V.K.; Investigation: V.K., Y.M.E.; Resources: V.K.; Data curation: V.K.; Writing - original draft: V.K.; Writing - review & editing: V.K., Y.M.E.; Visualization: V.K.; Supervision: Y.M.E.; Funding acquisition: Y.M.E.

Funding

This work was supported by the Israel Science Foundation (3291/19 and 558/19 to Y.E.) and a Hebrew University of Jerusalem (HUJI) International PhD Talent Scholarship (V.K.). Open Access funding provided by Hebrew University of Jerusalem. Deposited in PMC for immediate release.

Data availability

All relevant data can be found within the article and its supplementary information .

References

Anderson, E. and Huebner, E. (1968). Development of the oocyte and its accessory cells of the polychaete, Diopatra cuprea (Bosc) . J. Morph. 126 , 163-198. 10.1002/jmor.1051260203 [ CrossRef ] [ Google Scholar ]
Anderson, R. A., Fulton, N., Cowan, G., Coutts, S. and Saunders, P. T. K. (2007). Conserved and divergent patterns of expression of DAZL, VASA and OCT4 in the germ cells of the human fetal ovary and testis . BMC Dev. Biol. 7 , 136. 10.1186/1471-213X-7-136 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Arzt, M., Deschamps, J., Schmied, C., Pietzsch, T., Schmidt, D., Tomancak, P., Haase, R. and Jug, F. (2022). LABKIT: labeling and segmentation toolkit for big image data . Front. Comput. Sci. 4 , 1-12. 10.3389/fcomp.2022.777728 [ CrossRef ] [ Google Scholar ]
Beer, R. L. and Draper, B. W. (2013a). Nanos3 maintains germline stem cells and expression of the conserved germline stem cell gene nanos2 in the zebrafish ovary . Dev. Biol. 374 , 308-318. 10.1016/j.ydbio.2012.12.003 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Behrndt, M., Salbreux, G., Campinho, P., Hauschild, R., Oswald, F., Roensch, J., Grill, S. W. and Heisenberg, C.-P. (2013). Forces driving epithelial spreading in zebrafish gastrulation . Science 338 , 257-260. 10.1126/science.1224143 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Berry, R. O. (1941). Chromosome behavior in the germ cells and development of the gonads in Sciara ocellaris . J. Morphol. 68 , 547-583. 10.1002/jmor.1050680307 [ CrossRef ] [ Google Scholar ]
Biliński, S. (1983). Differentiation of the oocyte and nurse cells in an apterygote insect (Campodea) . Tissue Cell 15 , 965-973. 10.1016/0040-8166(83)90061-7 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Bilinski, S. M. (1993). Structure of ovaries and oogenesis in entognathans (Apterygota) . Int. J. Insect Morphol. Embryol. 22 , 255-269. 10.1016/0020-7322(93)90014-R [ CrossRef ] [ Google Scholar ]
Blokhina, Y. P., Frees, M. A., Nguyen, A., Sharifi, M., Chu, D. B., Bispo, K., Olaya, I., Draper, B. W. and Burgess, S. M. (2021). Rad21l1 cohesin subunit is dispensable for spermatogenesis but not oogenesis in zebrafish . PLoS Genet. 17 , 1-22. 10.1371/journal.pgen.1009127 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Bogoch, Y., Jamieson-Lucy, A., Vejnar, C. E., Levy, K., Giraldez, A. J., Mullins, M. C. and Elkouby, Y. M. (2022). Stage specific transcriptomic analysis and database for zebrafish oogenesis . Front. Cell Dev. Biol. 10 , 1-13. 10.3389/fcell.2022.826892 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Borovina, A., Superina, S., Voskas, D. and Ciruna, B. (2010). Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia . Nat. Cell Biol. 12 , 407-412. 10.1038/ncb2042 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Brubacher, J. L. and Huebner, E. (2009). Development of polarized female germline cysts in the polychaete, ophryotrocha labronica . J. Morphol. 270 , 413-429. 10.1002/jmor.10687 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Büning, J. and Sohst, S. (1988). The flea ovary: ultrastructure and analysis of cell clusters . Tissue Cell 20 , 783-795. 10.1016/0040-8166(88)90023-7 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Burke, B. (2018). LINC complexes as regulators of meiosis . Curr. Opin. Cell Biol. 52 , 22-29. 10.1016/j.ceb.2018.01.005 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Cao, Z., Mao, X. and Luo, L. (2019). Germline stem cells drive ovary regeneration in zebrafish . Cell Rep. 26 , 1709-1717.e3. 10.1016/j.celrep.2019.01.061 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Cardona, A., Saalfeld, S., Schindelin, J., Arganda-Carreras, I., Preibisch, S., Longair, M., Tomancak, P., Hartenstein, V. and Douglas, R. J. (2012). TrakEM2 software for neural circuit reconstruction . PLoS ONE 7 , e38011. 10.1371/journal.pone.0038011 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Chu, L., Li, J., Liu, Y. and Cheng, C. H. K. (2015). Gonadotropin signaling in zebrafish ovary and testis development: Insights from gene knockout study . Mol. Endocrinol. 29 , 1743-1758. 10.1210/me.2015-1126 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Crowder, C. M., Lassiter, C. S. and Gorelick, D. A. (2018). Nuclear androgen receptor regulates testes organization and oocyte maturation in Zebrafish . Endocrinology 159 , 980-993. 10.1210/en.2017-00617 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Deis, R. and Elkouby, Y. M. (2022). Microtubules control Buc phase separation and Balbiani body condensation in zebrafish oocyte polarity . bioRxiv 10.1101/2022.03.11.484019 [ CrossRef ] [ Google Scholar ]
Diegmiller, R., Nunley, H., Shvartsman, S. Y. and Imran Alsous, J. (2022). Quantitative models for building and growing fated small cell networks . Interface Focus 12 , 8-12. 10.1098/rsfs.2021.0082 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Eastin, K. J., Huang, A. P. and Ferree, P. M. (2020). A novel pattern of germ cell divisions in the production of hymenopteran insect eggs . Biol. Lett. 16 , 20200137. 10.1098/rsbl.2020.0137 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Eggan, K., Jurga, S., Gosden, R., Min, I. M. and Wagers, A. J. (2006). Ovulated oocytes in adult mice derive from non-circulating germ cells . Nature 441 , 1109-1114. 10.1038/nature04929 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Elkouby, Y. M. and Mullins, M. C. (2017a). Coordination of cellular differentiation, polarity, mitosis and meiosis – New findings from early vertebrate oogenesis . Dev. Biol. 430 , 275-287. 10.1016/j.ydbio.2017.06.029 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Elkouby, Y. M. and Mullins, M. C. (2017b). Methods for the analysis of early oogenesis in zebrafish . Dev. Biol. 430 , 310-324. 10.1016/j.ydbio.2016.12.014 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Elkouby, Y. M., Jamieson-Lucy, A. and Mullins, M. C. (2016). Oocyte polarization is coupled to the chromosomal bouquet, a conserved polarized nuclear configuration in meiosis . PLoS Biol. 14 , e1002335. 10.1371/journal.pbio.1002335 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Escobar-Aguirre, M., Zhang, H., Jamieson-Lucy, A. and Mullins, M. C. (2017a). Microtubule-actin crosslinking factor 1 (Macf1) domain function in Balbiani body dissociation and nuclear positioning . PLoS Genet. 13 , 1-29. 10.1371/journal.pgen.1006983 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Escobar-Aguirre, M., Elkouby, Y. M. and Mullins, M. C. (2017b). Localization in oogenesis of maternal regulators of embryonic development . Adv. Exp. Med. Biol. 953 , 173-207. 10.1007/978-3-319-46095-6_5 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Farini, D. and De Felici, M. (2022). The beginning of meiosis in mammalian female germ cells: a never-ending story of intrinsic and extrinsic factors . Int. J. Mol. Sci. 23 , 12571. 10.3390/ijms232012571 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Gondos, B., Bhiraleus, P. and Hobel, C. J. (1971). Ultrastructural observations on germ cells in human fetal ovaries . Am. J. Obstet. Gynecol. 110 , 644-652. 10.1016/0002-9378(71)90245-6 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Greenbaum, M. P., Iwamori, N., Agno, J. E. and Matzuk, M. M. (2009). Mouse Tex14 is required for embryonic germ cell intercellular bridges but not female fertility 1 . Biol. Reprod. 80 , 449-457. 10.1095/biolreprod.108.070649 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Gutzeit, H. O. (1985). Oosome formation during in vitro oogenesis in Bradysia tritici (syn. Sciara ocellaris) . Wilhelm Roux's Arch. Dev. Biol. 194 , 404-410. 10.1007/BF00848553 [ CrossRef ] [ Google Scholar ]
Haglund, K., Nezis, I. P. and Stenmark, H. (2011). Structure and functions of stable intercellular bridges formed by incomplete cytokinesis during development . Commun. Integr. Biol. 4 , 1-9. 10.4161/cib.13550 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Hegner, R. W. and Russell, C. P. (1916). Differential mitoses in the germ-cell cycle of Dineutes Nigrior . Proc. Natl Acad. Sci. USA 2 , 356-360. 10.1073/pnas.2.7.356 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Hinnant, T. D., Merkle, J. A. and Ables, E. T. (2020). Coordinating proliferation, polarity, and cell fate in the drosophila female germline . Front. Cell Dev. Biol. 8 , 1-22. 10.3389/fcell.2020.00019 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Houwing, S., Kamminga, L. M., Berezikov, E., Cronembold, D., Girard, A., Van Den Elst, H., Filippov, D. V., Blaser, H., Raz, E., Moens, C. B.et al. (2007). A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish . Cell 129 , 69-82. 10.1016/j.cell.2007.03.026 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Houwing, S., Berezikov, E. and Ketting, R. F. (2008). Zili is required for germ cell differentiation and meiosis in zebrafish . EMBO J. 27 , 2702-2711. 10.1038/emboj.2008.204 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Hunter, N. (2017). Oocyte quality control: causes, mechanisms, and consequences . Cold Spring Harbor Symp. Quant. Biol. 82 , 235-247. 10.1101/sqb.2017.82.035394 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Jamieson-Lucy, A. H., Kobayashi, M., James Aykit, Y., Elkouby, Y. M., Escobar-Aguirre, M., Vejnar, C. E., Giraldez, A. J. and Mullins, M. C. (2022). A proteomics approach identifies novel resident zebrafish Balbiani body proteins Cirbpa and Cirbpb . Dev. Biol. 484 , 1-11. 10.1016/j.ydbio.2022.01.006 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Johnson, J., Canning, J., Kaneko, T., Pru, J. K. and Tilly, J. L. (2004). Erratum: corrigendum: Germline stem cells and follicular renewal in the postnatal mammalian ovary (Nature (2004) 428 (145-150)) . Nature 430 , 1062. 10.1038/nature02868 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kim, H. J., Liu, C. and Dernburg, A. F. (2022). How and why chromosomes interact with the cytoskeleton during meiosis . Genes 13 , 901. 10.3390/genes13050901 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kloc, M., Bilinski, S., Dougherty, M. T., Brey, E. M. and Etkin, L. D. (2004). Formation, architecture and polarity of female germline cyst in Xenopus . Dev. Biol. 266 , 43-61. 10.1016/j.ydbio.2003.10.002 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kobayashi, M., Jamieson-Lucy, A. and Mullins, M. C. (2021). Microinjection method for analyzing zebrafish early stage oocytes . Front. Cell Dev. Biol. 9 , 1-7. 10.3389/fcell.2021.753642 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Koch, E. A. and King, R. C. (1969). Further studies on the ring canal system of the ovarian cystocytes of Drosophila melanogaster . Z. Zellforsch. Mikroskopische Anat. 102 , 129-152. 10.1007/BF00336421 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kossack, M. E. and Draper, B. W. (2019). Genetic regulation of sex determination and maintenance in zebrafish (Danio rerio) . Curr. Top. Dev. Biol. 134 , 119-149. 10.1016/bs.ctdb.2019.02.004 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kubrakiewicz, J. (1997). Germ cells cluster organization in polytrophic ovaries of Neuroptera . Tissue Cell 29 , 221-228. 10.1016/S0040-8166(97)80022-5 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kubrakiewicz, J., Adamski, R. T. and Bilinski, S. M. (1991). Ultrastructural studies on accessory nuclei in developing oocytes of the crustacean, Siphonophanes grubei . Tissue Cell 23 , 903-907. 10.1016/0040-8166(91)90039-V [ PubMed ] [ CrossRef ] [ Google Scholar ]
Kumar, T. C. A. (1968). Oogenesis in Lorises; Loris tardigradus lydekkerianus and Nycticebus coucang . Proc. R. Soc. Lond. Ser. B Biol. Sci. 169 , 167-176. 10.1098/rspb.1968.0004 [ CrossRef ] [ Google Scholar ]
Kurilo, L. F. (1981). Oogenesis in antenatal development in man . Hum. Genet. 57 , 86-92. 10.1007/BF00271175 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Lee, W. (1985). An ultrastructural study on the ovariole, development in the oriental fruit fly. Bull. Inst. Academia Sinica 24 , 1-10. [ Google Scholar ]
Leerberg, D. M., Hopton, R. E. and Draper, B. W. (2019). Fibroblast growth factor receptors function redundantly during zebrafish embryonic development . Genetics 212 , 1301-1319. 10.1534/genetics.119.302345 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Legland, D., Arganda-Carreras, I. and Andrey, P. (2016). MorphoLibJ: Integrated library and plugins for mathematical morphology with ImageJ . Bioinformatics 32 , 3532-3534. 10.1093/bioinformatics/btw413 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Lei, L. and Spradling, A. C. (2013). Mouse primordial germ cells produce cysts that partially fragment prior to meiosis . Development (Camb.) 140 , 2075-2081. 10.1242/dev.093864 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Lei, L. and Spradling, A. C. (2016). Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells . Science 352 , 95-99. 10.1126/science.aad2156 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Lesch, B. J. and Page, D. C. (2012). Genetics of germ cell development . Nat. Rev. Genet. 13 , 781-794. 10.1038/nrg3294 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Leu, D. H. and Draper, B. W. (2010). The ziwi promoter drives germline-specific gene expression in zebrafish . Dev. Dyn. 239 , 2714-2721. 10.1002/dvdy.22404 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Li, J. and Ge, W. (2020). Zebrafish as a model for studying ovarian development: Recent advances from targeted gene knockout studies . Mol. Cell. Endocrinol. 507 , 110778. 10.1016/j.mce.2020.110778 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Liu, Y., Kossack, M. E., McFaul, M. E., Christensen, L. N., Siebert, S., Wyatt, S. R., Kamei, C. N., Horst, S., Arroyo, N., Drummond, I. A.et al. (2022). Single-cell transcriptome reveals insights into the development and function of the zebrafish ovary . eLife 11 , 1-39. 10.7554/eLife.76014 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Lu, K., Jensen, L., Lei, L. and Yamashita, Y. M. (2017). Stay connected: a germ cell strategy . Trends Genet. 33 , 971-978. 10.1016/j.tig.2017.09.001 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
MacLennan, M., Crichton, J. H., Playfoot, C. J. and Adams, I. R. (2015). Oocyte development, meiosis and aneuploidy . Semin. Cell Dev. Biol. 45 , 68-76. 10.1016/j.semcdb.2015.10.005 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Marec, F., Leutelt, J., Traut, W. and Wolf, K. W. (1993). Visualization of polyfusomes in gonads of a moth, Ephestia Kuehniella Z. (Lepidoptera: Pyralidae), by a microspreading technique and electron microscopy . Int. J. Insect Morphol. Embryol. 22 , 487-496. 10.1016/0020-7322(93)90035-Y [ CrossRef ] [ Google Scholar ]
Marlow, F. L. and Mullins, M. C. (2008). Bucky ball functions in Balbiani body assembly and animal-vegetal polarity in the oocyte and follicle cell layer in zebrafish . Dev. Biol. 321 , 40-50. 10.1016/j.ydbio.2008.05.557 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Martin, J., Woods, D. C. and Tilly, J. L. (2019). Implications and current limitations of oogenesis from female germline or oogonial stem cells in adult mammalian ovaries . Cells 8 , 93. 10.3390/cells8020093 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Matsuzaki, M. (1972). Oogenesis in adult net-spinning Caddisfly.pdf ’. Sci. Rep. Fukushima Univ. 22 , 27-40. [ Google Scholar ]
Matsuzaki, M. (1973). Oogenesis in the springtail, Tomocerus minutus Tullberg (Collembola: Tomoceridae) . Int. J. Insect Morphol. Embryol. 2 , 335-349. 10.1016/0020-7322(73)90023-8 [ CrossRef ] [ Google Scholar ]
Matuszewski, B. and Hoser, P. (1975). Gene amplification and its effect on the structure and function of the oocyte nucleus in the whirligig beetle Gyrinus natator (Gyrinidae, Coleoptera-Adephaga) . Experientia 31 , 431-433. 10.1007/BF02026360 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Mazurkiewicz, M. and Kubrakiewicz, J. (2005). Differentiation and diversification of follicular cells in polytrophic ovaries of crane flies (Diptera: Nematocera: Tipulomorpha and Trichoceridae) . Tissue Cell 37 , 367-377. 10.1016/j.tice.2005.06.001 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Mytlis, A. and Elkouby, Y. M. (2021). Live and time-lapse imaging of early oogenesis and meiotic chromosomal dynamics in cultured juvenile zebrafish ovaries . In Germline Development in the Zebrafish (ed. Dosch R.), pp. 137-155. Springer US. 10.1007/978-1-0716-0970-5_12 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Mytlis, A., Kumar, V., Qiu, T., Deis, R., Hart, N., Levy, K., Masek, M., Shawahny, A., Ahmad, A., Eitan, H.et al. (2022). Control of meiotic chromosomal bouquet and germ cell morphogenesis by the zygotene cilium . Science 376 , eabh3104. 10.1126/science.abh3104 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Mytlis, A., Levy, K. and Elkouby, Y. M. (2023). The many faces of the bouquet centrosome MTOC in meiosis and germ cell development . Curr. Opin. Cell Biol. 81 , 102158. 10.1016/j.ceb.2023.102158 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Nagaoka, S. I., Hassold, T. J. and Hunt, P. A. (2012). Human aneuploidy: mechanisms and new insights into an age-old problem . Nat. Rev. Genet. 13 , 493-504. 10.1038/nrg3245 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Nakamura, S., Kobayashi, K., Nishimura, T., Higashijima, S.-I. and Tanaka, M. (2010). Identification of germline stem cells in the ovary of the teleost medaka . Science 328 , 1561-1563. 10.1126/science.1185473 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Nashchekin, D., Busby, L., Jakobs, M., Squires, I. and St. Johnston, D. (2021). Symmetry breaking in the female germline cyst . Science 374 , 874-879. 10.1126/science.abj3125 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Niu, W. and Spradling, A. C. (2022). Mouse oocytes develop in cysts with the help of nurse cells . Cell 185 , 2576-2590.e12. 10.1016/j.cell.2022.05.001 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Novorol, C., Burkhardt, J., Wood, K. J., Iqbal, A., Roque, C., Coutts, N., Almeida, A. D., He, J., Wilkinson, C. J. and Harris, W. A. (2013). Microcephaly models in the developing zebrafish retinal neuroepithelium point to an underlying defect in metaphase progression . Open Biol. 3 , 130065. 10.1098/rsob.130065 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Pacchiarotti, J., Maki, C., Ramos, T., Marh, J., Howerton, K., Wong, J., Pham, J., Anorve, S., Chow, Y.-C. and Izadyar, F. (2010). Differentiation potential of germ line stem cells derived from the postnatal mouse ovary . Differentiation 79 , 159-170. 10.1016/j.diff.2010.01.001 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Parichy, D. M., Elizondo, M. R., Mills, M. G., Gordon, T. N. and Engeszer, R. E. (2009). Normal table of postembryonic zebrafish development: Staging by externally visible anatomy of the living fish . Dev. Dyn. 238 , 2975-3015. 10.1002/dvdy.22113 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Pauls, S., Geldmacher-Voss, B. and Campos-Ortega, J. A. (2001). A zebrafish histone variant H2A.F/Z and a transgenic H2A.F/Z:GFP fusion protein for in vivo studies of embryonic development . Dev. Genes Evol. 211 , 603-610. 10.1007/s00427-001-0196-x [ PubMed ] [ CrossRef ] [ Google Scholar ]
Qin, M., Zhang, Z., Song, W., Wong, Q. W.-L., Chen, W., Shirgaonkar, N. and Ge, W. (2018). Roles of figla/figla in juvenile ovary development and follicle formation during zebrafish gonadogenesis . Endocrinology 159 , 3699-3722. 10.1210/en.2018-00648 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Quinlan, M. E. (2016). Cytoplasmic streaming in the Drosophila oocyte . Annu. Rev. Cell Dev. Biol. 32 , 173-195. 10.1146/annurev-cellbio-111315-125416 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Ramamurty, P. S. (1967). The cytoplasmic inclusions of the trophocytes in the ovary of the scorpion fly Panorpa communis L. (Mecoptera: Panorpidae) . Proc. R. Entomol. Soc. Lond. A Gen. Entomol. 42 , 87-92. 10.1111/j.1365-3032.1967.tb01007.x [ CrossRef ] [ Google Scholar ]
Roovers, E. F., Kaaij, L. J. T., Redl, S., Bronkhorst, A. W., Wiebrands, K., de Jesus Domingues, A. M., Huang, H.-Y., Han, C.-T., Riemer, S., Dosch, R.et al. (2018). Tdrd6a regulates the aggregation of Buc into functional subcellular compartments that drive germ cell specification . Dev. Cell 46 , 285-301.e9. 10.1016/j.devcel.2018.07.009 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Rousset, A. (1978). La formation des cystes dans l'ovariole de chrysopa perla (L.) (neuroptera: Chrysopidae) . Int. J. Insect Morphol. Embryol. 7 , 45-57. 10.1016/S0020-7322(78)80014-2 [ CrossRef ] [ Google Scholar ]
Rubin, T., Macaisne, N. and Huynh, J.-R. (2020). Mixing and matching chromosomes during female meiosis . Cells 9 , 696. 10.3390/cells9030696 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Schmidt, U., Weigert, M., Broaddus, C. and Myers, G. (2018). Cell detection with star-convex polygons . Lecture Notes in Computer Science (including subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics) 11071 LNCS , 265-273. 10.1007/978-3-030-00934-2_30 [ CrossRef ] [ Google Scholar ]
Spałek-Wołczyńska, A., Klag, J., Bielecki, A. and Świątek, P. (2007). Oogenesis in four species of Piscicola (Hirudinea, Rhynchobdellida) . J. Morphol. 269 , 18-28. 10.1002/jmor.10568 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Stringer, C., Wang, T., Michaelos, M. and Pachitariu, M. (2021). Cellpose: a generalist algorithm for cellular segmentation . Nat. Methods 18 , 100-106. 10.1038/s41592-020-01018-x [ PubMed ] [ CrossRef ] [ Google Scholar ]
Świątek, P. and Urbisz, A. Z. (2019). Architecture and Life History of Female Germ-Line Cysts in Clitellate Annelids . In Evo-Devo: Non-model Species in Cell and Developmental Biology Results and Problems in Cell Differentiation (Tworzydlo W., Bilinski Szczepan M., eds), pp. 515-551. Springer. 10.1007/978-3-030-23459-1_21 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Świątek, P., Kubrakiewicz, J. and Klag, J. (2009). Formation of germ-line cysts with a central cytoplasmic core is accompanied by specific orientation of mitotic spindles and partitioning of existing intercellular bridges . Cell Tissue Res. 337 , 137-148. 10.1007/s00441-009-0788-8 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Świątek, P., de Wit, P., Jarosz, N., Chajec, Ł. and Urbisz, A. Z. (2018). Micromorphology of ovaries and oogenesis in Grania postclitellochaeta (Clitellata: Enchytraeidae) . Zoology 126 , 119-127. 10.1016/j.zool.2017.11.004 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Świątek, P., Pinder, A. and Gajda, Ł. (2020). Description of ovary organization and oogenesis in a phreodrilid clitellate . J. Morphol. 281 , 81-94. 10.1002/jmor.21081 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Tworzydło, W. and Kisiel, E. (2010). Structure of ovaries and oogenesis in Dermapterans. II. the nurse cells, nuage aggregates and sponge bodies . Folia Biol. 58 , 67-72. 10.3409/fb58_1-2.67-72 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Tworzydło, W., Biliński, S. M., Kočárek, P. and Haas, F. (2010). Ovaries and germline cysts and their evolution in Dermaptera (Insecta) . Arthropod. Struct. Dev. 39 , 360-368. 10.1016/j.asd.2010.05.004 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Tworzydlo, W., Kisiel, E., Jankowska, W., Witwicka, A. and Bilinski, S. M. (2016). Exclusion of dysfunctional mitochondria from Balbiani body during early oogenesis of Thermobia . Cell Tissue Res. 366 , 191-201. 10.1007/s00441-016-2414-x [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Urbisz, A. Z., Chajec, Ł., Brąszewska-Zalewska, A., Kubrakiewicz, J. and Świątek, P. (2017). Ovaries of the white worm (Enchytraeus albidus, Annelida, Clitellata) are composed of 16-celled meroistic germ-line cysts . Dev. Biol. 426 , 28-42. 10.1016/j.ydbio.2017.04.009 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Wang, S.-C., Ching, Y.-H., Krishnaraj, P., Chen, G.-Y., Radhakrishnan, A. S., Lee, H.-M., Tu, W.-C. and Lin, M.-D. (2020). Oogenesis of hematophagous midge Forcipomyia taiwana (Diptera: Ceratopogonidae) and nuage localization of Vasa in germline cells . Insects 11 , 106. 10.3390/insects11020106 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Webster, A. and Schuh, M. (2017). Mechanisms of aneuploidy in human eggs . Trends Cell Biol. 27 , 55-68. 10.1016/j.tcb.2016.09.002 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Webster, K. A., Schach, U., Ordaz, A., Steinfeld, J. S., Draper, B. W. and Siegfried, K. R. (2017). Dmrt1 is necessary for male sexual development in zebrafish . Dev. Biol. 422 , 33-46. 10.1016/j.ydbio.2016.12.008 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Weigert, M., Schmidt, U., Haase, R., Sugawara, K. and Myers, G. (2020). Star-convex polyhedra for 3D object detection and segmentation in microscopy . Proceedings - 2020 IEEE Winter Conference on Applications of Computer Vision, WACV 56 , 3655-3662. 10.1109/WACV45572.2020.9093435 [ CrossRef ] [ Google Scholar ]
White, Y. A. R., Woods, D. C., Takai, Y., Ishihara, O., Seki, H. and Tilly, J. L. (2012). Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women . Nat. Med. 18 , 413-421. 10.1038/nm.2669 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Yamauchi, H. and Yoshitake, N. (1982). Origin and differentiation of the oocyte - nurse cell complex in the germarium of the earwig, anisolabis Maritima borelli (Dermaptera : Labiduridae) . Int. J. Insect Morphol. Embryol. 11 , 293-305. 10.1016/0020-7322(82)90018-6 [ CrossRef ] [ Google Scholar ]
Yamauchi, H. and Yoshitake, N. (1984). Developmental stages of ovarian follicles of the silkworm, Bombyx mori L . J. Morphol. 179 , 21-31. 10.1002/jmor.1051790104 [ PubMed ] [ CrossRef ] [ Google Scholar ]
Yang, Y.-J., Wang, Y., Li, Z., Zhou, L. and Gui, J.-F. (2017). Sequential, divergent, and cooperative requirements of foxl2a and foxl2b in ovary development and maintenance of zebrafish . Genetics 205 , 1551-1572. 10.1534/genetics.116.199133 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Yu, G., Zhang, D., Liu, W., Wang, J., Liu, X., Zhou, C., Gui, J. and Xiao, W. (2018). Zebrafish androgen receptor is required for spermatogenesis and maintenance of ovarian function . Oncotarget 9 , 24320-24334. 10.18632/oncotarget.24407 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Zhang, Z., Zhu, B. and Ge, W. (2015). Genetic analysis of zebrafish gonadotropin (FSH and LH) functions by TALEN-mediated gene disruption . Mol. Endocrinol. 29 , 76-98. 10.1210/me.2014-1256 [ PMC free article ] [ PubMed ] [ CrossRef ] [ Google Scholar ]
Zou, K., Yuan, Z., Yang, Z., Luo, H., Sun, K., Zhou, L., Xiang, J., Shi, L., Yu, Q., Zhang, Y.et al. (2009). Production of offspring from a germline stem cell line derived from neonatal ovaries . Nat. Cell Biol. 11 , 631-636. 10.1038/ncb1869 [ PubMed ] [ CrossRef ] [ Google Scholar ]

Articles from Development (Cambridge, England) are provided here courtesy of Company of Biologists