Abstract
Drosophila oogenesis is a fascinating phenomenon. The coordinated action of many cellular processes produces a fully mature egg containing a maternal dowry that both directs and supports development of the embryo. The ovary is one of the best studied organs of Drosophila, and much of our knowledge of oogenesis is contained in several monographs (1–4) and recent reviews (5–8). This chapter describes some of the most important cellular processes of oogenesis, and provides detailed methods for their identification and immunocytological analysis.
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References
King, R.C. (1970) Ovarian Development in Drosophila melanogaster. Academic, New York.
Mahowald, A.P. and Kambysellis, M.P. (1980) Oogenesis, in The Genetics and Biology of Drosophila (Ashburner, M. and Wright, T.R.F., eds.), Academic, New York, Vol. 2d, pp. 141–225.
Spradling, A. (1993) Developmental genetics of oogenesis, in The Development of Drosophila melanogaster (Bate, M. and Martinez-Arias, A., eds.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, Vol. 1, pp. 1–70.
Matova, N. and Cooley, L. (2001) Comparative aspects of animal oogenesis. Dev. Biol. 231, 291–320.
de Cuevas, M., Lilly, M. A., and Spradling, A. C. (1997) Germline cyst formation in Drosophila. Annu.Rev. Genet. 31, 405–428.
Navarro, C., Lehmann, R., and Morris, J. (2001) Setting one sister above the rest. Curr. Biol. 11, R162–R165.
Riechmann, V. and Ephrussi, A. (2001) Axis formation during Drosophila oogenesis. Curr. Opin. Gen. Dev. 11, 374–383.
Endow, S. A. and Komma, D. J. (1997) Spindle dynamics during meiosis in Drosophila oocytes. J. Cell Biol. 137, 1321–1336.
Illmensee, K. and Mahowald, A.P. (1974) Transplantation of posterior polar plasm in Drosophila: induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA 71, 1016–1020.
Howard, K., Jaglarz, M., Zhang, N., Shah, J., and Warrior, R. (1993) Migration of Drosophila germ cells: analysis using enhancer trap lines. Development (Suppl.) 213–218.
Warrior, R. (1994) Primordial germ cell migration and the assembly of Drosophila embryonic gonad. Dev. Biol. 166, 180–194.
Babcock, B. M. (1971) Oviduct development in Drosophila. II. Metamorphic events in normal and ovariectomized females. Wilhelm Roux. Arch. 167, 24–63.
van Eeden, F. and St. Johnston, D. (1999) The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev. 9, 396–404.
Robinson, D. N., Cant, K., and Cooley, L. (1994) Morphogenesis of the Drosophila ovarian ring canals. Development 120, 2015–2025.
King, R. C. (1957) Oogenesis in adult Drosophila melanogaster. II. Stage distribution as a function of age. Growth 21, 95–102.
Cummings, M. R. and King, R. C. (1969) The cytology of the vitellogenic stages of oogenesis in Drosophila melanogaster I. General staging characteristics. J. Morphol. 128, 427–442.
Gelti-Douka, H., Gingeras, T. R., and Kambysellis, M. P. (1974) Yolk proteins in Drosophila: identification and site of synthesis. J. Exp. Zool. 187, 167–172.
DiMario, P. J. and Mahowald, A. P. (1986) The effects of pH and weak bases on the in vitro endocytosis of vitellogenin by oocytes of Drosophila melanogaster. Cell Tissue Res. 246, 103–108.
Brennan, M.D., Weiner, A. J., Goralski, T. J., and Mahowald, A. P. (1982) The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev. Biol. 89, 225–236.
Margaritis, L., Kafatos, F., and Petri, W. (1980) The eggshell of Drosophila melanogaster: I. Fine structure of the layers and regions of the wild-type egg-shell. J. Cell Sci. 43, 1–35.
Dobens, L. L. and Raftery, L. A. (2000) Integration of epithelial patterning and morphogenesis in Drosophila ovarian follicle cells. Dev. Dynam. 218, 80–93.
Chao, S. and Nagoshi, R. (1999) Induction of apoptosis in the germline and follicle cell layers of Drosophila egg chambers. Mech. Dev. 88, 159–172.
Bownes, M. and Blair, M. (1986) The effects of a sugar diet and hormones on the expression of the Drosophila yolk-protein genes. J. Insect Physiol. 32, 493–501.
Chen, P. S., Stumm-Zollinger, E., Aigaki, T., Balmer, J., Bienz, M., and Bohlen, P. (1988) A male accessory gland peptide that regulates reproductive behaviour of female D. melanogaster. Cell 54, 291–298.
Soller, M., Bownes, M., and Kubli, E. (1997) Mating and sex peptide stimulate the accumulation of yolk in oocytes of Drosophila melanogaster. Eur. Biochem, J. 243, 732–738.
Riddiford, L. M. and Ashburner, M. (1991) Effects of juvenile hormones mimics on larval development and metamorphosis of Drosophila melanogaster. Gen. Comp. Endocrinol. 82, 172–183.
Soller, M., Bownes, M., and Kubli, E. (1999) Control of oocyte maturation in sexually mature Drosophila females. Dev. Biol. 208, 337–351.
Buszczak, M. B. M., Freeman, M. R., Carlson, J. R., Bender, M., Cooley, L., and Segraves, W. A. (1999) Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development 126, 4581–4589.
Carney, G. E. and Bender, M. (2000) The Drosophila ecdysone receptor (EcR) gene is required maternally for normal oogenesis. Genetics 154, 1203–1211.
Böhni, R., Riesgo-Escovar, J., Oldham, S., et al. (1999) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS114. Cell 97, 865–875.
Drummond-Barbosa, D. and Spradling, A. C. (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev. Biol. 231, 265–278.
Wieschaus, E. and Szabad, J. (1979) The development and function of the female germ line in Drosophila melanogaster: a cell lineage study. Dev. Biol. 68, 29–46.
Lin, H. and Spradling, A. C. (1993) Germline stem-cell division and egg chamber development in transplanted Drosophila germaria. Dev. Biol. 159, 140–152.
Lin, H. and Spradling, A. C. (1997) A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124, 2463–2476.
Deng, W. and 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, 79–94.
de Cuevas, M. and Spradling, A. C. (1998) Morphogenesis of the Drosophila fusome and its implications for the oocyte specification. Development 125, 2781–2789.
Storto, P. D. and King, R. C. (1989) The role of polyfusomes in generating branched chains of cystocytes during Drosophila oogenesis. Dev. Genet. 10, 70–86.
McGrail, M., Gepner, J., Silvanovich, A., Ludmann, S., Serr, M., and Hays, T. S. (1995) Regulation of cytoplasmic dynein function in vivo by the Drosophila Glued Complex. J. Cell Biol. 131, 411–425.
McGrail, M. and Hays, T. S. (1997) The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124, 2409–2419.
Cha, B.-J., Koppetsch, B. S., and Theurkauf, W. E. (2001) In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106, 35–46.
Theurkauf, W. E., Alberts, M., Jan, Y. N., and Jongens, T. A. (1993) A central role for microtubules in the differentiation of Drosophila oocytes. Development 118, 1169–1180.
Grieder, N. C., de Cuevas, M., and Spradling, A. C. (2000) The fusome organizes the microtubule network during oocyte differentiation in Drosophila. Development 127, 4253–4264.
Bolivar, J., Huynh, J. R., Lopez-Schier, H., Gonzales, C., St. Johnston, D., and Gonzales-Reyes, A. (2001) Centrosome migration into the Drosophila oocyte is dependent of BicD, egl and the organisation of the microtubule cytoskeleton. Development 128, 1889–1909.
Carpenter, A. T. C. (1994) Egalitarian and the choice of the cell fates in Drosophila melanogaster oogenesis. Ciba Found. Symp. 182, 223–246.
Huynh, J. R. and St. Johnston, D. (2000) The role of BicD, egl, orb and the microtubules in the restriction of meiosis to the Drosophila oocyte. Development 127, 2785–2794.
Ghabrial, A. and Schüpbach, T. (1999) Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nature Cell Biol. 1, 354–357.
Cox, D. N., Lu, B., Sun, T. S., Williams, L. T., and Jan, Y. N. (2001) Drosophila par-1 is required for oocyte differentiation and microtubule organization. Curr. Biol. 11, 75–87.
Huynh, J. R., Shulman, J., Benton, R., and St. Johnston, D. (2001) PAR-1 is required for the maintenance of oocyte fate in Drosophila. Development 128, 1201–1209.
Pare, C. and Suter, B. (2000) Subcellular localization of Bic-D: GFP is linked to an asymmetric oocyte nucleus. J. Cell Sci. 113, 2119–2127.
Clegg, N. J., Findley, S. D., Mahowald, A. P., and Ruohola-Baker, H. (2001) Maelstrom is required to position the MTOC in stage 2–6 Drosophila oocytes. Dev. Genes Evol. 211, 44–48.
Huynh, J. R., Petronczki, M., Knoblich, J., and St. Johnston, D. (2001) Bazooka and PAR-6 are required with PAR-1 for the maintenance of oocyte fate in Drosophila. Curr. Biol. 11, 901–906.
Margolis, J. and Spradling, A. C. (1995) Identification and behaviour of epithelial stem cells in Drosophila ovary. Development 121, 3797–3807.
Forbes, A., Lin, H., Ingham, P., and Spradling, A. C. (1996) Hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122, 1125–1135.
Gonzales-Reyes, A. and St. Johnstone, D. (1998) The Drosophila AP axis is polarized by the cadherin-mediated positioning of the oocyte. Development 125, 3635–3644.
Tanentzapf, G., Smith, C., McGlade, J., and Tepass, U. (2000) Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis. J. Cell Biol. 151, 891–904.
Godt, D. and Tepass, U. (1998) Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387–391.
Gonzales-Reyes, A. and St. Johnstone, D. (1998) Patterning of the follicle cell epithelium along the anterior-posterior axis during Drosophila development. Development 125, 2837–2846.
Gonzales-Reyes, A., Elliott, H., and St. Johnstone, D. (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654–658.
Roth, S., Neuman-Silberberg, F. S., Barcelo, G., and Schüpbach, T. (1995) cornichon and the EGF receptor signalling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967–978.
Nilson, L. A. and Schüpbach, T. (1999) EGF receptor signalling in Drosophila oogenesis. Curr. Topics Dev. Biol. 44, 203–243.
van Buskirk, C. and Schüpbach, T. (1999) Versatility in signalling: multiple responses to EGF receptor activation during Drosophila oogenesis. Trends Cell Biol. 9, 1–4.
Stevens, L. (1998) Twin peaks: Spitz and Argos star in patterning of the Drosophila egg. Cell 95, 291–294.
Edwards, K., Demsky, M., Montague, R., Weymouth, N., and Kiehart, D. (1997) GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 191, 103–117.
Li, K. and Kaufman, T.C. (1996) The homeotic target gene centrosomin encodes an essential centrosomal component. Cell 85, 585–596.
Swan, A., Nguyen, T., and Suter, B. (1999) Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning. Nature Cell Biol. 1, 444–449.
Shulman, J. M., Benton, R., and St. Johnston, D. (2000) The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377–388.
Jankovics, F., Sinka, R., and Erdélyi, M. (2001) An interaction type of genetic screen reveals a role of the Rab11 gene in oskar mRNA localization in the developing Drosophila melanogaster oocyte. Genetics 158, 1177–1188.
Baum, B., Li, W., and Perrimon, N. (2000) A cyclase-associated protein regulates actin and cell polarity during Drosophila oogenesis and in yeast. Curr. Biol. 10, 964–973.
Pokrywka, N. J. and Stephenson, E. C. (1995) Microtubules are a general component of mRNA localization systems in Drosophila oocytes. Dev. Biol. 167, 363–370.
Clark, I., Jan, L. Y., and Jan, Y. N. (1997) Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in Drosophila oocyte, epithelium, neuron and muscle. Development 124, 461–470.
Lasko, P. (1999) RNA sorting in Drosophila oocytes and embryos. FASEB J. 13, 421–433.
Hays, T. and Karess, R. (2000) Swallowing dynein: a missing link in RNA localization? Nature Cell Biol. 2, E60–E62.
Mahajan-Miklos, S. and Cooley, L. (1994) Intercellular cytoplasm transport during Drosophila oogenesis. Dev. Biol. 165, 336–351.
Robinson, D. N. and Cooley, L. (1997) Drosophila Kelch is an oligomeric ring canal actin organizer. J. Cell Biol. 138, 799–810.
Robinson, D. N., Smith-Leiker, T. A., Sokol, N. S., Hudson, A. M., and Cooley, L. (1997) Formation of the Drosophila ovarian ring canal inner rim depends on cheerio. Genetics 145, 1063–1072
Sokol, N. S. and Cooley, L. (1999) Drosophila Filamin encoded by the cheerio locus is a component of the ovarian ring canals. Curr. Biol. 9, 1221–1230
Field, C. M. and Alberts, B. M. (1995) Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165–178
Minestrini, G., Máthé, E., and Glover, D. M. (2002) Mutations that disrupt the sub-cellular localisation of the Pavarotti kinesin-like protein lead to defects in the tubulin and actin cytoskeleton during Drosophila oogenesis. J. Cell Sci. 115, 725–736.
Koch, E. A. and King, R. C. (1966) The origin and early differentiation of the egg chamber of Drosophila melanogaster. J. Morphol. 119, 283–304.
Bohrmann, J. and Biber, K. (1994) Cytoskeleton-dependent transport of cyto-plasmic particles in previtellogenic to midvitellogenic ovarian follicles of Drosophila: time lapse analysis using video-enhanced contrast microscopy. J. Cell Sci. 107, 849–858.
Cooley, L., Verheyen, E., and Ayers, K. (1992) The chickadee gene encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69, 173–184.
Gutzeit, H. (1990) The microfilament pattern in the somatic follicle cells of mid-vitellogenic ovarian follicles of Drosophila. Eur. J. Cell Biol. 53, 349–356.
Nokkala, S. and Puro, J. (1976) Cytological evidence for a chromocenter in Drosophila melanogaster oocytes. Hereditas 83, 265–268.
Puro, J. and Nokkala, S. (1977) Meiotic segregation of chromosomes in Drosophila melanogaster oocytes. A cytological approach. Chromosoma 63, 273–286.
Neuman-Silberberg, F. S. and Schüpbach, T. (1993) The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell 75, 165–174.
Máthé, E., Bates, H., Huikeshoven, H., Deák, P., Glover, D. M., and Cotterill, S. (2000) Importin-α3 is required at multiple stages of Drosophila development and has a stage specific role in the completion of oogenesis. Dev. Biol. 223, 307–322.
Theurkauf, W.E. and Hawley, R.S. (1992) Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J. Cell Biol. 116, 1167–1180.
Walczak, C. E., Vernos, I., Mitchison, T. J., Karsenti, E., and Heald, R. A. (1998). A model for the proposed roles of different microtubule-based motor proteins in establishing spindle bipolarity. Curr. Biol. 8, 903–913.
Walczak, C. E. (2001) Ran hits the ground running. Nature Cell Biol. 3, E69–E71.
Cullen, C. F. and Ohkura, H. (2001) Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nature Cell Biol. 3, 637–642.
Afshar, K., Barton, N. R., Hawley, R. S., and Goldstein, L. S. (1995) DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell 81, 129–138.
Sonnenblick, B. P. (1950) The early embryology of Drosophila melanogaster, in Biology of Drosophila (Demerec, M., ed.), Wiley, New York, pp. 62–167.
Puro, J. (1991) Differential mechanisms governing segregation of a univalent in oocytes and spermatocytes of Drosophila melanogaster. Chromosoma 100, 305–314.
Endow, S. A. and Komma, D. J. (1997) Spindle dynamics during meiosis in Drosophila oocytes. J. Cell Biol. 137, 1321–1336.
Endow, S. A. and Komma, D. J. (1998) Assembly and dynamics of an anstral: astral spindle: the meiosis II spindle in Drosophila oocytes. J. Cell Sci. 111, 2487–2495.
Riparbelli, M. G. and Callaini, G. (1996) Meiotic spindle organization in fertilized Drosophila oocyte: presence of centrosomal components in the meiotic apparatus. J. Cell Sci. 109, 911–918.
Wakefield, J. G., Bonaccorsi, S., and Gatti, M. (2001) The Drosophila protein Asp is involved in microtubule organization during spindle formation and cytokinesis. J. Cell Biol. 153, 637–648.
Máthé, E., Boros, I., Jósvay, K., et al. (1998) The Tomaj mutant alleles of αTubulin67C reveal a requirement for the encoded maternal specific tubulin isoform in the sperm aster, the cleavage spindle apparatus and neurogenesis during embryonic development in Drosophila. J. Cell Sci. 111, 887–896.
Huettner, A.F. (1924) Maturation and fertilization of Drosophila melanogaster. J. Morphol. 37, 385–423.
Rabinowitz, M. (1941) Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J. Morphol. 69, 1–49.
Orr-Weaver, T. L. (1995) Meiosis in Drosophila: seeing is believing. Proc. Natl. Acad. Sci. USA 92, 10,443–10,449.
Rieder, C. L. and Cole, R. (1999) Chromatid cohesion during mitosis: lessons from meiosis. J. Cell Sci. 112, 2607–2613.
Moore, D. P., Page, A. W., Tang, T. T., Kerrebrock, A. W., and Orr-Weaver, T. (1998) The cohesion protein MEI-S332 localizes to condensed meiotic and mitotic centromeres until sister chromatids separate. J. Cell Biol. 140, 1003–1012.
Lopez, J. M., Karpen, G. H., and Orr-Weaver (2000) Sister-chromatids cohesion via MEI-S332 and kinetochore assembly are separable functions of the Drosophila centromere. Curr. Biol. 10, 997–1000.
Robb, J. A. (1969) Maintenance of imaginal discs of Drosophila melanogaster in chemically defined media. J. Cell Biol. 41, 876–885.
Mahowald, A. P., Goralski, T. J., and Caulton, J. H. (1983). In vitro activation of Drosophila eggs. Dev. Biol. 98, 437–445.
Page, A. W. and Orr-Weaver, T. L. (1997) Activation of the meiotic divisions in Drosophila oocytes. Dev. Biol. 183, 195–207.
Tavosanis, G., Llamazares, S., Goulielmos, G., and Gonzalez, C. (1997) Essential role for γ-tubulin in the acentriolar female meiotic spindle of Drosophila. EMBO. J. 16, 1809–1819.
Szabad, J. (1998) Genetic requirement of epidermal and female germline cells in Drosophila in the light of clonal analysis. Int. J. Dev. Biol. 42, 257–262.
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Máthé, E. (2004). Immunocytological Analysis of Oogenesis. In: Henderson, D.S. (eds) Drosophila Cytogenetics Protocols. Methods in Molecular Biology, vol 247. Humana Press. https://doi.org/10.1385/1-59259-665-7:89
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