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Basic aspects of ovarian development in Drosophila melanogaster

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Abstract

Modern views of the development and structural organization of the female reproductive system in Drosophila melanogaster are reviewed. Special emphasis is placed on the generation and development of follicles in the germarium and the interactions of germline and somatic cells in the egg chamber. Detailed consideration is given to the main events that ensure and regulate the transport of mRNA, proteins, and organelles from nurse cells to the oocyte in the germarium and at later stages of egg chamber development.

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References

  1. Mahowald, A.P., Assembly of the Drosophila Germ Plasm, Int. Rev. Cytol., 2001, vol. 203, pp. 187–213.

    Article  PubMed  CAS  Google Scholar 

  2. Williamson, A. and Lehmann, R., Germ Cell Development in Drosophila, Annu. Rev. Cell. Dev. Biol., 1996, vol. 12, pp. 365–391.

    Article  PubMed  CAS  Google Scholar 

  3. Santos, A.C. and Lehmann, R., Germ Cell Specification and Migration in Drosophila and beyond, Curr. Biol., 2004, vol. 14, no. 14, pp. 578–589.

    Article  CAS  Google Scholar 

  4. Coffman, C.R., Cell Migration and Programmed Cell Death of Drosophila Germ Cells, Ann. N.Y. Acad. Sci., 2003, vol. 995, pp. 117–126.

    PubMed  CAS  Google Scholar 

  5. Brower, D.L., Smith, R.J., and Wilcox, M., Differentiation within the Gonads of Drosophila Revealed by Immunofluorescence, J. Embryol. Exp. Morphol., 1981, vol. 63, pp. 233–242.

    PubMed  CAS  Google Scholar 

  6. Lasko, P.F. and Ashburner, M., Posterior Localization of VASA Protein Correlates with, but Is not Sufficient for, Pole Cell Development, Genes Dev., 1990, vol. 4, no. 6, pp. 905–921.

    Article  PubMed  CAS  Google Scholar 

  7. Godt, D. and Laski, F.A., Mechanisms of Cell Rearrangement and Cell Recruitment in Drosophila Ovary Morphogenesis and the Requirement of bric a brac, Development, 1995, vol. 121, no. 1, pp. 173–187.

    PubMed  CAS  Google Scholar 

  8. Spradling, A.C., Developmental Genetics of Oogenesis, in The Development of Drosophila melanogaster, Cold Spring Harbor Lab., 1993, pp. 1–70.

  9. Estrada, B., Casares, F., and Sanchez-Herrero, E., Development of the Genitalia in Drosophila melanogaster, Differentiation, 2003, vol. 71, no. 6, pp. 299–310.

    Article  PubMed  CAS  Google Scholar 

  10. Chen, E.H. and Baker, B.S., Compartmental Organization of the Drosophila Genital Imaginal Discs, Development, 1997, vol. 124, no. 1, pp. 205–218.

    PubMed  CAS  Google Scholar 

  11. Miller, A., The Internal Anatomy and Histology of the Imago of Drosophila melanogaster, in Biology of Drosophila, New York: Wiley, 1950, pp. 420–534.

    Google Scholar 

  12. Demerec, M., Biology of Drosophila, New York: Wiley, 1950.

    Google Scholar 

  13. Bloch Qazi, M.C., Heifetz, Y., and Wolfner, M.F., The Developments between Gametogenesis and Fertilization: Ovulation and Female Sperm Storage in Drosophila melanogaster, Dev. Biol., 2003, vol. 256, no. 2, pp. 195–211.

    Article  PubMed  CAS  Google Scholar 

  14. Fowler, G.L., Eroshevich, K.E., and Zimmering, S., Distribution of Sperm in the Storage Organs of the Drosophila melanogaster Female at Various Levels of Insemination, Mol. Gen. Genet., 1968, vol. 101, pp. 120–122.

    Article  PubMed  CAS  Google Scholar 

  15. Horne-Badovinac, S. and Bilder, D., Mass Transit: Epithelial Morphogenesis in the Drosophila Egg Chamber, Dev. Dyn., 2005, vol. 232, no. 3, pp. 559–574.

    Article  PubMed  CAS  Google Scholar 

  16. King, R.C., Ovarian Development in Drosophila melanogaster, New York: Academic, 1970.

    Google Scholar 

  17. Forbes, A.J., Lin, H., Ingham, P.W., et al., Hedgehog Is Required for the Proliferation and Specification of Ovarian Somatic Cells Prior to Egg Chamber Formation in Drosophila, Development, 1996, vol. 122, no. 4, pp. 1125–1135.

    PubMed  CAS  Google Scholar 

  18. Spradling, A.C., de Cuevas, M., Drummond-Barbosa, D., et al., The Drosophila Germarium: Stem Cells, Germ Line Cysts, and Oocytes, Cold Spring Harbor Symp. Quant. Biol., 1997, vol. 62, pp. 25–34.

    PubMed  CAS  Google Scholar 

  19. Xie, T. and Spradling, A.C., A Niche Maintaining Germ Line Stem Cells in the Drosophila Ovary, Science, 2000, vol. 290, no. 5490, pp. 328–330.

    Article  PubMed  CAS  Google Scholar 

  20. Chen, J., Godt, D., Gunsalus, K., et al., Cofilin/ADF Is Required for Cell Motility during Drosophila Ovary Development and Oogenesis, Nat. Cell Biol., 2001, vol. 3, no. 2, pp. 204–209.

    Article  PubMed  CAS  Google Scholar 

  21. Spradling, A., Drummond-Barbosa, D., and Kai, T., Stem Cells Find Their Niche, Nature, 2001, vol. 414, no. 6859, pp. 98–104.

    Article  PubMed  CAS  Google Scholar 

  22. Cox, D.N., Chao, A., Baker, J., et al., A Novel Class of Evolutionarily Conserved Genes Defined by piwi Are Essential for Stem Cell Self-Renewal, Genes Dev., 1998, vol. 12, no. 23, pp. 3715–3727.

    PubMed  CAS  Google Scholar 

  23. Cox, D.N., Chao, A., and Lin, H., piwi Encodes a Nucleoplasmic Factor Whose Activity Modulates the Number and Division Rate of Germline Stem Cells, Development, 2000, vol. 127, no. 3, pp. 503–514.

    PubMed  CAS  Google Scholar 

  24. King, F.J. and Lin, H., Somatic Signaling Mediated by fs(1)Yb Is Essential for Germline Stem Cell Maintenance during Drosophila Oogenesis, Development, 1999, vol. 126, no. 9, pp. 1833–1844.

    PubMed  CAS  Google Scholar 

  25. King, F.J., Szakmary, A., Cox, D.N., et al., Yb Modulates the Divisions of both Germline and Somatic Stem Cells through piwi- and hh-Mediated Mechanisms in the Drosophila Ovary, Mol. Cell, 2001, vol. 7, no. 3, pp. 497–508.

    Article  PubMed  CAS  Google Scholar 

  26. Xie, T. and Spradling, A.C., decapentaplegic Is Essential for the Maintenance and Division of Germline Stem Cells in the Drosophila Ovary, Cell, 1998, vol. 94, no. 2, pp. 251–260.

    Article  PubMed  CAS  Google Scholar 

  27. Zhang, Y. and Kalderon, D., Hedgehog Acts as a Somatic Stem Cell Factor in the Drosophila Ovary, Nature, 2001, vol. 410, no. 6828, pp. 599–604.

    Article  PubMed  CAS  Google Scholar 

  28. Song, X. and Xie, T., Wingless Signaling Regulates the Maintenance of Ovarian Somatic Stem Cells in Drosophila, Development, 2003, vol. 130, no. 14, pp. 3259–3268.

    Article  PubMed  CAS  Google Scholar 

  29. de Cuevas, M. and Spradling, A.C., Morphogenesis of the Drosophila Fusome and Its Implications for Oocyte Specification, Development, 1998, vol. 125, no. 15, pp. 2781–2789.

    PubMed  Google Scholar 

  30. Lin, H. and Spradling, A.C., Germline Stem Cell Division and Egg Chamber Development in Transplanted Drosophila Germaria, Dev. Biol., 1993, vol. 159, no. 1, pp. 140–152.

    Article  PubMed  CAS  Google Scholar 

  31. Lin, H. and Spradling, A.C., A Novel Group of Pumilio Mutations Affects the Asymmetric Division of Germline Stem Cells in the Drosophila Ovary, Development, 1997, vol. 124, no. 12, pp. 2463–2476.

    PubMed  CAS  Google Scholar 

  32. Lin, H., Yue, L., and Spradling, A.C., The Drosophila Fusome, a Germline-Specific Organelle, Contains Membrane Skeletal Proteins and Functions in Cyst Formation, Development, 1994, vol. 120, no. 4, pp. 947–956.

    PubMed  CAS  Google Scholar 

  33. Deng, W. and Lin, H., 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., 1997, vol. 189, no. 1, pp. 79–94.

    Article  PubMed  CAS  Google Scholar 

  34. Lilly, M.A., de Cuevas, M., and Spradling, A.C., Cyclin A Associates with the Fusome during Germline Cyst Formation in the Drosophila Ovary, Dev. Biol., 2000, vol. 218, no. 1, pp. 53–63.

    Article  PubMed  CAS  Google Scholar 

  35. Lilly, M.A. and Spradling, A.C., The Drosophila Endocycle Is Controlled by Cyclin E and Lacks a Checkpoint Ensuring S-Phase Completion, Genes Dev., 1996, vol. 10, no. 19, pp. 2514–2526.

    Article  PubMed  CAS  Google Scholar 

  36. Morris, J.Z., Hong, A., Lilly, M.A., et al., twin, a CCR4 Homolog, Regulates Cyclin Poly(A) Tail Length to Permit Drosophila Oogenesis, Development, 2005, vol. 132, no. 6, pp. 1165–1174.

    Article  PubMed  CAS  Google Scholar 

  37. Mata, J., Curado, S., Ephrussi, A., et al., Tribbles Coordinates Mitosis and Morphogenesis in Drosophila by Regulating String/C DC25 Proteolysis, Cell, 2000, vol. 101, no. 5, pp. 511–522.

    Article  PubMed  CAS  Google Scholar 

  38. de Cuevas, M., Lee, J.K., and Spradling, A.C., α-Spectrin is Required for Germline Cell Division and Differentiation in the Drosophila Ovary, Development, 1996, vol. 122, no. 12, pp. 3959–3968.

    PubMed  Google Scholar 

  39. McKearin, D. and Ohlstein, B., A Role for the Drosophila Bag-of-Marbles Protein in the Differentiation of Cystoblasts from Germline Stem Cells, Development, 1995, vol. 121, no. 9, pp. 2937–2947.

    PubMed  CAS  Google Scholar 

  40. McKearin, D., The Drosophila Fusome, Organelle Biogenesis and Germ Cell Differentiation: If You Build It, BioEssays, 1997, vol. 19, no. 2, pp. 147–152.

    Article  PubMed  CAS  Google Scholar 

  41. Grieder, N.C., de Cuevas, M., and Spradling, A.C., The Fusome Organizes the Microtubule Network during Oocyte Differentiation in Drosophila, Development, 2000, vol. 127, no. 19, pp. 4253–4264.

    PubMed  CAS  Google Scholar 

  42. de Cuevas, M., Lilly, M.A., and Spradling, A.C., Germline Cyst Formation in Drosophila, Ann. Rev. Genet., 1997, vol. 31, pp. 405–428.

    Article  PubMed  Google Scholar 

  43. Gilbert, L.I., Iatrou, K., and Gill, S., Comprehensive Molecular Insect Science, Elsevier, 2005.

  44. Theurkauf, W.E., Alberts, B.M., Jan, Y.N., et al., A Central Role for Microtubules in the Differentiation of Drosophila Oocytes, Development, 1993, vol. 118, no. 4, pp. 1169–1180.

    PubMed  CAS  Google Scholar 

  45. Suter, B., Romberg, L.M., and Steward, R., Bicaudal-D, a Drosophila Gene Involved in Developmental Asymmetry: Localized Transcript Accumulation in Ovaries and Sequence Similarity to Myosin Heavy Chain Tail Domains, Genes Dev., 1989, vol. 3, no. 12A, pp. 1957–1968.

    Article  PubMed  CAS  Google Scholar 

  46. Ephrussi, A., Dickinson, L.K., and Lehmann, R., Oskar Organizes the Germ Plasm and Directs Localization of the Posterior Determinant Nanos, Cell, 1991, vol. 66, no. 1, pp. 37–50.

    Article  PubMed  CAS  Google Scholar 

  47. Lantz, V., Chang, J.S., Horabin, J.I., et al., The Drosophila Orb RNA-Binding Protein Is Required for the Formation of the Egg Chamber and Establishment of Polarity, Genes Dev., 1994, vol. 8, no. 5, pp. 598–613.

    Article  PubMed  CAS  Google Scholar 

  48. Yue, L. and Spradling, A.C., hu-li tai shao, a Gene Required for Ring Canal Formation during Drosophila Oogenesis, Encodes a Homolog of Adducin, Genes Dev., 1992, vol. 6, no. 12B, pp. 2443–2454.

    Article  PubMed  CAS  Google Scholar 

  49. Mahowald, A.P. and Strassheim, J.M., Intercellular Migration of Centrioles in the Germarium of Drosophila melanogaster: An Electron Microscopic Study, J. Cell Biol., 1970, vol. 45, no. 2, pp. 306–320.

    Article  PubMed  CAS  Google Scholar 

  50. Cox, R.T. and Spradling, A.C., A Balbiani Body and the Fusome Mediate Mitochondrial Inheritance during Drosophila Oogenesis, Development, 2003, vol. 130, no. 8, pp. 1579–1590.

    Article  PubMed  CAS  Google Scholar 

  51. Carpenter, A.T., Synaptonemal Complex and Recombination Nodules in Wild-Type Drosophila melanogaster Females, Genetics, 1979, vol. 92, no. 2, pp. 511–541.

    PubMed  CAS  Google Scholar 

  52. Carpenter, A.T., Egalitarian and the Choice of Cell Fates in Drosophila melanogaster Oogenesis, Ciba Found. Symp., 1994, vol. 182, pp. 223–246.

    Article  PubMed  CAS  Google Scholar 

  53. Margolis, J. and Spradling, A., Identification and Behavior of Epithelial Stem Cells in the Drosophila Ovary, Development, 1995, vol. 121, no. 11, pp. 3797–3807.

    PubMed  CAS  Google Scholar 

  54. Carpenter, A.T., EM Autoradiographic Evidence That DNA Synthesis Occurs at Recombination Nodules during Meiosis in Drosophila melanogaster Females, Chromosoma, 1981, vol. 83, no. 1, pp. 59–80.

    Article  PubMed  CAS  Google Scholar 

  55. Tworoger, M., Larkin, M.K., Bryant, Z., et al., Mosaic Analysis in the Drosophila Ovary Reveals a Common Hedgehog-Inducible Precursor Stage for Stalk and Polar Cells, Genetics, 1999, vol. 151, no. 2, pp. 739–748.

    PubMed  CAS  Google Scholar 

  56. Grammont, M. and Irvine, K.D., Organizer Activity of the Polar Cells during Drosophila Oogenesis, Development, 2002, vol. 129, no. 22, pp. 5131–5140.

    PubMed  CAS  Google Scholar 

  57. Torres, I.L., Lopez-Schier, H., and St Johnston, D., A Notch/Delta-Dependent Relay Mechanism Establishes Anterior-Posterior Polarity in Drosophila, Dev. Cell, 2003, vol. 5, no. 4, pp. 547–558.

    Article  PubMed  CAS  Google Scholar 

  58. Bai, J. and Montell, D., Eyes Absent, a Key Repressor of Polar Cell Fate during Drosophila Oogenesis, Development, 2002, vol. 129, no. 23, pp. 5377–5388.

    Article  PubMed  CAS  Google Scholar 

  59. Grammont, M. and Irvine, K.D., fringe and notch Specify Polar Cell Fate during Drosophila Oogenesis, Development, 2001, vol. 128, no. 12, pp. 2243–2253.

    PubMed  CAS  Google Scholar 

  60. Lopez-Schier, H. and St. Johnston, D., Delta Signaling from the Germ Line Controls the Proliferation and Differentiation of the Somatic Follicle Cells during Drosophila Oogenesis, Genes Dev., 2001, vol. 15, no. 11, pp. 1393–1405.

    Article  PubMed  CAS  Google Scholar 

  61. Bruckner, K., Perez, L., Clausen, H., et al., Glycosyltransferase Activity of Fringe Modulates Notch-Delta Interactions, Nature, 2000, vol. 406, no. 6794, pp. 411–415.

    Article  PubMed  CAS  Google Scholar 

  62. Moloney, D.J., Panin, V.M., Johnston, S.H., et al., Fringe Is a Glycosyltransferase That Modifies Notch, Nature, 2000, vol. 406, no. 6794, pp. 369–375.

    Article  PubMed  CAS  Google Scholar 

  63. Cummings, C.A. and Cronmiller, C., The daughterless Gene Functions together with Notch and Delta in the Control of Ovarian Follicle Development in Drosophila, Development, 1994, vol. 120, no. 2, pp. 381–394.

    PubMed  CAS  Google Scholar 

  64. Grammont, M., Dastugue, B., and Couderc, J.L., The Drosophila toucan (toc) Gene Is Required in Germline Cells for the Somatic Cell Patterning during Oogenesis, Development, 1997, vol. 124, no. 24, pp. 4917–4926.

    PubMed  CAS  Google Scholar 

  65. McCaffrey, R., St. Johnston, D., and Gonzalez-Reyes, A., A Novel Mutant Phenotype Implicates dicephalic in Cyst Formation in the Drosophila Ovary, Dev. Dyn., 2006, vol. 235, no. 4, pp. 908–917.

    Article  PubMed  CAS  Google Scholar 

  66. Gonzalez-Reyes, A. and St. Johnston, D., Role of Oocyte Position in Establishment of Anterior-Posterior Polarity in Drosophila, Science, 1994, vol. 266, no. 5185, pp. 639–642.

    Article  PubMed  CAS  Google Scholar 

  67. Gonzalez-Reyes, A. Elliott, H., and St. Johnston, D., Oocyte Determination and the Origin of Polarity in Drosophila: The Role of the Spindle Genes, Development, 1997, vol. 124, no. 24, pp. 4927–4937.

    PubMed  CAS  Google Scholar 

  68. Hawkins, N.C., Thorpe, J., and Schupbach, T., Encore, a Gene Required for the Regulation of Germ Line Mitosis and Oocyte Differentiation during Drosophila Oogenesis, Development, 1996, vol. 122, no. 1, pp. 281–290.

    PubMed  CAS  Google Scholar 

  69. Robinson, D.N., Cant, K., and Cooley, L., Morphogenesis of Drosophila Ovarian Ring Canals, Development, 1994, vol. 120, no. 7, pp. 2015–2025.

    PubMed  CAS  Google Scholar 

  70. King, R.C., Rubinson, A.C., and Smith, R.F., Oogenesis in Adult Drosophila melanogaster, Growth, 1956, vol. 20, no. 2, pp. 121–157.

    PubMed  CAS  Google Scholar 

  71. Cummings, M.R. and King, R.C., The Cytology of the Vitellogenic Stages of Oogenesis in Drosophila melanogaster: I. General Staging Characteristics, J. Morphol., 1969, vol. 128, pp. 427–442.

    Article  Google Scholar 

  72. Margaritis, L.H., The Eggshell of Drosophila melanogaster: New Staging Characteristics and Fine Structural Analysis of Choriogenesis, Can. J. Zool., 1986, vol. 64, pp. 2152–2175.

    Google Scholar 

  73. Wieschaus, E. and Szabad, J., The Development and Function of the Female Germ Line in Drosophila melanogaster: A Cell Lineage Study, Dev. Biol., 1979, vol. 68, no. 1, pp. 29–46.

    Article  PubMed  CAS  Google Scholar 

  74. Middleton, C.A., Nongthomba, U., Parry, K., et al., Neuromuscular Organization and Aminergic Modulation of Contractions in the Drosophila Ovary, BMC Biol., 2006, vol. 4, p. 17.

    Article  PubMed  CAS  Google Scholar 

  75. Calvi, B.R., Lilly, M.A., and Spradling, A.C., Cell Cycle Control of Chorion Gene Amplification, Genes Dev., 1998, vol. 12, no. 5, pp. 734–744.

    PubMed  CAS  Google Scholar 

  76. Deng, W.M., Althauser, C., and Ruohola-Baker, H., Notch-Delta Signaling Induces a Transition from Mitotic Cell Cycle to Endocycle in Drosophila Follicle Cells, Development, 2001, vol. 128, no. 23, pp. 4737–4746.

    PubMed  CAS  Google Scholar 

  77. Montell, D.J., Rorth, P., and Spradling, A.C., slow border cells, a Locus Required for a Developmentally Regulated Cell Migration during Oogenesis, Encodes Drosophila C/EBP, Cell, 1992, vol. 71, no. 1, pp. 51–62.

    Article  PubMed  CAS  Google Scholar 

  78. Duchek, P. and Rorth, P., Guidance of Cell Migration by EGF Receptor Signaling during Drosophila Oogenesis, Science, 2001, vol. 291, no. 5501, pp. 131–133.

    Article  PubMed  CAS  Google Scholar 

  79. Duchek, P., Somogyi, K., Jekely, G., et al., Guidance of Cell Migration by the Drosophila PDGF/VEGF Receptor, Cell, 2001, vol. 107, no. 1, pp. 17–26.

    Article  PubMed  CAS  Google Scholar 

  80. Harrison, D.A., McCoon, P.E., Binari, R., et al., Drosophila Unpaired Encodes a Secreted Protein That Activates the JAK Signaling Pathway, Genes Dev., 1998, vol. 12, no. 20, pp. 3252–3263.

    PubMed  CAS  Google Scholar 

  81. Silver, D.L. and Montell, D.J., Paracrine Signaling through the JAK/STAT Pathway Activates Invasive Behavior of Ovarian Epithelial Cells in Drosophila, Cell, 2001, vol. 107, no. 7, pp. 831–841.

    Article  PubMed  CAS  Google Scholar 

  82. Bai, J., Uehara, Y., and Montell, D.J., Regulation of Invasive Cell Behavior by Taiman, a Drosophila Protein Related to AIB1, a Steroid Receptor Coactivator Amplified in Breast Cancer, Cell, 2000, vol. 103, no. 7, pp. 1047–1058.

    Article  PubMed  CAS  Google Scholar 

  83. Montell, D.J., Border-Cell Migration: The Race Is on, Nat. Rev. Mol. Cell Biol., 2003, vol. 4, no. 1, pp. 13–24.

    Article  PubMed  CAS  Google Scholar 

  84. Swan, A. and Suter, B., Role of Bicaudal-D in Patterning the Drosophila Egg Chamber in Mid-Oogenesis, Development, 1996, vol. 122, no. 11, pp. 3577–3586.

    PubMed  CAS  Google Scholar 

  85. Roth, S., Neuman-Silberberg, F.S., Barcelo, G., et al., Cornichon and the EGF Receptor Signaling Process Are Necessary for both Anterior-Posterior and Dorsal-Ventral Pattern Formation in Drosophila, Cell, 1995, vol. 81, no. 6, pp. 967–978.

    Article  PubMed  CAS  Google Scholar 

  86. Edwards, K.A. and Kiehart, D.P., Drosophila Nonmuscle Myosin II Has Multiple Essential Roles in Imaginal Disc and Egg Chamber Morphogenesis, Development, 1996, vol. 122, no. 5, pp. 1499–1511.

    PubMed  CAS  Google Scholar 

  87. Twombly, V., Blackman, R.K., Jin, H., et al., The TGF-β Signaling Pathway Is Essential for Drosophila Oogenesis, Development, 1996, vol. 122, no. 5, pp. 1555–1565.

    PubMed  CAS  Google Scholar 

  88. Wang, X., Bo, J., Bridges, T., et al., Analysis of Cell Migration Using Whole-Genome Expression Profiling of Migratory Cells in the Drosophila Ovary, Dev. Cell, 2006, vol. 10, no. 4, pp. 483–495.

    Article  PubMed  CAS  Google Scholar 

  89. Margaritis, L.H., Kafatos, F.C., and Petri, W.H., The Eggshell of Drosophila melanogaster: I. Fine Structure of the Layers and Regions of the Wild-Type Eggshell, J. Cell Sci., 1980, vol. 43, pp. 1–35.

    PubMed  CAS  Google Scholar 

  90. Chao, S. and Nagoshi, R.N., Induction of Apoptosis in the Germline and Follicle Layer of Drosophila Egg Chambers, Mech. Dev., 1999, vol. 88, no. 2, pp. 159–172.

    Article  PubMed  CAS  Google Scholar 

  91. Ambrosio, L. and Schedl, P., Two Discrete Modes of Histone Gene Expression during Oogenesis in Drosophila melanogaster, Dev. Biol., 1985, vol. 111, no. 1, pp. 220–231.

    Article  PubMed  CAS  Google Scholar 

  92. Duncan, J.E. and Warrior, R., The Cytoplasmic Dynein and Kinesin Motors Have Interdependent Roles in Patterning the Drosophila Oocyte, Curr. Biol., 2002, vol. 12, no. 23, pp. 1982–1991.

    Article  PubMed  CAS  Google Scholar 

  93. Januschke, J., Gervais, L., Dass, S., et al., Polar Transport in the Drosophila Oocyte Requires Dynein and Kinesin I Cooperation, Curr. Biol., 2002, vol. 12, no. 23, pp. 1971–1981.

    Article  PubMed  CAS  Google Scholar 

  94. Koch, E.A. and Spitzer, R.H., Multiple Effects of Colchicine on Oogenesis in Drosophila: Induced Sterility and Switch of Potential Oocyte to Nurse-Cell Developmental Pathway, Cell Tissue Res., 1983, vol. 228, no. 1, pp. 21–32.

    Article  PubMed  CAS  Google Scholar 

  95. Guild, G.M., Connelly, P.S., Shaw, M.K., et al., Actin Filament Cables in Drosophila Nurse Cells Are Composed of Modules That Slide Passively Past One Another during Dumping, J. Cell Biol., 1997, vol. 138, no. 4, pp. 783–797.

    Article  PubMed  CAS  Google Scholar 

  96. Gutzeit, H.O., The Role of Microfilaments in Cytoplasmic Streaming in Drosophila Follicles, J. Cell Sci., 1986, vol. 80, pp. 159–169.

    PubMed  CAS  Google Scholar 

  97. Cooley, L., Verheyen, E., and Ayers, K., chickadee Encodes a Profilin Required for Intercellular Cytoplasm Transport during Drosophila Oogenesis, Cell, 1992, vol. 69, no. 1, pp. 173–184.

    Article  PubMed  CAS  Google Scholar 

  98. Mahajan-Miklos, S. and Cooley, L., The Villin-Like Protein Encoded by the Drosophila quail Gene Is Required for Actin Bundle Assembly during Oogenesis, Cell, 1994, vol. 78, no. 2, pp. 291–301.

    Article  PubMed  CAS  Google Scholar 

  99. Paterson, J. and O’Hare, K., Structure and Transcription of the singed Locus of Drosophila melanogaster, Genetics, 1991, vol. 129, no. 4, pp. 1073–1084.

    PubMed  CAS  Google Scholar 

  100. Cant, K., Knowles, B.A., Mooseker, M.S., et al., Drosophila singed, a Fascin Homolog, Is Required for Actin Bundle Formation during Oogenesis and Bristle Extension, J. Cell Biol., 1994, vol. 125, no. 2, pp. 369–380.

    Article  PubMed  CAS  Google Scholar 

  101. Verheyen, E.M. and Cooley, L., Profilin Mutations Disrupt Multiple Actin-Dependent Processes during Drosophila Development, Development, 1994, vol. 120, no. 4, pp. 717–728.

    PubMed  CAS  Google Scholar 

  102. Bryan, J., Edwards, R., Matsudaira, P., et al., Fascin, an Echinoid Actin-Bundling Protein, Is a Homolog of the Drosophila singed Gene Product, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, no. 19, pp. 9115–9119.

    Article  PubMed  CAS  Google Scholar 

  103. Granok, H., Leibovitch, B.A., Shaffer, C.D., et al., Chromatin: Ga-ga over GAGA Factor, Curr. Biol., 1995, vol. 5, no. 3, pp. 238–241.

    Article  PubMed  CAS  Google Scholar 

  104. Wilkins, R.C. and Lis, J.T., Dynamics of Potentiation and Activation: GAGA Factor and Its Role in Heat Shock Gene Regulation, Nucleic Acids Res., 1997, vol. 25, no. 20, pp. 3963–3968.

    Article  PubMed  CAS  Google Scholar 

  105. Chung, Y.T. and Keller, E.B., Regulatory Elements Mediating Transcription from the Drosophila melanogaster Actin 5C Proximal Promoter, Mol. Cell Biol., 1990, vol. 10, no. 1, pp. 206–216.

    PubMed  CAS  Google Scholar 

  106. O’Brien, T., Wilkins, R.C., Giardina, C., et al., Distribution of GAGA Protein on Drosophila Genes in vivo, Genes Dev., 1995, vol. 9, no. 9, pp. 1098–1110.

    Article  PubMed  CAS  Google Scholar 

  107. van Steensel, B., Delrow, J., and Bussemaker, H.J., Genome-Wide Analysis of Drosophila GAGA Factor Target Genes Reveals Context-Dependent DNA Binding, Proc. Natl. Acad. Sci. USA, 2003, vol. 100, no. 5, pp. 2580–2585.

    Article  PubMed  CAS  Google Scholar 

  108. Satterfield, T.F., Jackson, S.M., and Pallanck, L.J., A Drosophila Homolog of the Polyglutamine Disease Gene SCA2 is a Dosage-Sensitive Regulator of Actin Filament Formation, Genetics, 2002, vol. 162, no. 4, pp. 1687–1702.

    PubMed  CAS  Google Scholar 

  109. McNeil, G.P., Smith, F., and Galioto, R., The Drosophila RNA-Binding Protein LARK is Required for the Organization of the Actin Cytoskeleton and Hu-Li tai shao Localization during Oogenesis, Genesis, 2004, vol. 40, no. 2, pp. 90–100.

    Article  PubMed  CAS  Google Scholar 

  110. Robinson, D.N. and Cooley, L., Stable Intercellular Bridges in Development: The Cytoskeleton Lining the Tunnel, Trends Cell Biol., 1996, vol. 6, no. 12, pp. 474–479.

    Article  PubMed  CAS  Google Scholar 

  111. Tilney, L.G., Tilney, M.S., and Guild, G.M., Formation of Actin Filament Bundles in the Ring Canals of Developing Drosophila Follicles, J. Cell Biol., 1996, vol. 133, no. 1, pp. 61–74.

    Article  PubMed  CAS  Google Scholar 

  112. Kramerov, A.A., Mikhaleva, E.A., Rozovsky, Ya.M., et al., Insect Mucin-Type Glycoprotein: Immunodetection of the O-Glycosylated Epitope in Drosophila melanogaster Cells and Tissues, Insect Biochem. Mol. Biol., 1997, vol. 27, no. 6, pp. 513–521.

    Article  PubMed  CAS  Google Scholar 

  113. Field, C.M. and Alberts, B.M., Anillin, a Contractile Ring Protein That Cycles from the Nucleus to the Cell Cortex, J. Cell Biol., 1995, vol. 131, no. 1, pp. 165–178.

    Article  PubMed  CAS  Google Scholar 

  114. Sokol, N.S. and Cooley, L., Drosophila Filamin Encoded by the cheerio Locus Is a Component of Ovarian Ring Canals, Curr. Biol., 1999, vol. 9, no. 21, pp. 1221–1230.

    Article  PubMed  CAS  Google Scholar 

  115. Dodson, G.S., Guarnieri, D.J., and Simon, M.A., Src64 Is Required for Ovarian Ring Canal Morphogenesis during Drosophila Oogenesis, Development, 1998, vol. 125, no. 15, pp. 2883–2892.

    PubMed  CAS  Google Scholar 

  116. Roulier, E.M., Panzer, S., and Beckendorf, S.K., The Tec29 Tyrosine Kinase Is Required during Drosophila Embryogenesis and Interacts with Src64 in Ring Canal Development, Mol. Cell, 1998, vol. 1, no. 6, pp. 819–829.

    Article  PubMed  CAS  Google Scholar 

  117. King, R.C., Cassidy, J.D., and Roussett, A., The Formation of Clones of Interconnected Cells during Oogenesis in Insects, Insect Ultrastruct., 1982, vol. 1, pp. 3–31.

    Google Scholar 

  118. Dobens, L.L. and Raftery, L.A., Integration of Epithelial Patterning and Morphogenesis in Drosophila Ovarian Follicle Cells, Dev. Dyn., 2000, vol. 218, no. 1, pp. 80–93.

    Article  PubMed  CAS  Google Scholar 

  119. Cavaliere, V., Donati, A., Hsouna, A., et al., dAkt Kinase Controls Follicle Cell Size during Drosophila Oogenesis, Dev. Dyn., 2005, vol. 232, no. 3, pp. 845–854.

    Article  PubMed  CAS  Google Scholar 

  120. Ogienko, A.A., Karagodin, D.A., Pavlova, N.V., et al., Molecular Genetic Characteristic of Hypomorphic Mutation of Trithorax-like (trlen82) Gene, Analysis of Its Influence on Drosophila melanogaster Oogenesis, Ontogenez, 2007 (in press).

  121. Gondos, B., Intercellular Bridges and Mammalian Germ Cell Differentiation, Differentiation, 1973, vol. 1, pp. 177–182.

    Article  Google Scholar 

  122. Pepling, M.E. and Spradling, A.C., Female Mouse Germ Cells Form Synchronously Dividing Cysts, Development, 1998, vol. 125, no. 17, pp. 3323–3328.

    PubMed  CAS  Google Scholar 

  123. Pepling, M.E., de Cuevas, M., and Spradling, A.C., Germline Cysts: A Conserved Phase of Germ Cell Development?, Trends Cell Biol., 1999, vol. 9, no. 7, pp. 257–262.

    Article  PubMed  CAS  Google Scholar 

  124. Braun, R.E., Behringer, R.R., Peschon, J.J., et al., Genetically Haploid Spermatids Are Phenotypically Diploid, Nature, 1989, vol. 337, no. 6205, pp. 373–376.

    Article  PubMed  CAS  Google Scholar 

  125. Matova, N. and Cooley, L., Comparative Aspects of Animal Oogenesis, Dev. Biol., 2001, vol. 231, no. 2, pp. 291–320.

    Article  PubMed  CAS  Google Scholar 

  126. Jenuth, J.P., Peterson, A.C., Fu, K., et al., Random Genetic Drift in the Female Germline Explains the Rapid Segregation of Mammalian Mitochondrial DNA, Nat. Genet., 1996, vol. 14, no. 2, pp. 146–151.

    Article  PubMed  CAS  Google Scholar 

  127. Weakley, B.S., Light and Electron Microscopy of Developing Germ Cells and Follicle Cells in the Ovary of the Golden Hamster: Twenty-Four Hours before Birth to Eight Days Post Partum, J. Anat., 1967, vol. 101, no. 3, pp. 435–459.

    PubMed  CAS  Google Scholar 

  128. Gondos, B., The Ultrastructure of Granulose Cells in the Newborn Rabbit Ovary, Anat. Rec., 1969, vol. 165, no. 1, pp. 67–77.

    Article  PubMed  CAS  Google Scholar 

  129. Kurilo, L.F., Oogenesis in Antenatal Development in Man, Hum. Genet., 1981, vol. 57, no. 1, pp. 86–92.

    Article  PubMed  CAS  Google Scholar 

  130. Selman, K., Robin, A.W., Sarka, A., et al., Stages of Oocyte Development in the Zebrafish, Brachydanio rerio, J. Morphol., 1993, vol. 218, pp. 203–224.

    Article  Google Scholar 

  131. Dumont, J.N., Oogenesis in Xenopus laevis (Daudin): I. Stages of Oocyte Development in Laboratory Maintained Animals, J. Morphol., 1972, vol. 136, no. 2, pp. 153–179.

    Article  PubMed  CAS  Google Scholar 

  132. Dumont, J.N. and Brummett, A.R., Oogenesis in Xenopus laevis (Daudin): V. Relationships between Developing Oocytes and Their Investing Follicular Tissues, J. Morphol., 1978, vol. 155, no. 1, pp. 73–97.

    Article  PubMed  CAS  Google Scholar 

  133. Neaves, W.B., Intercellular Bridges between Follicle Cells and Oocyte in the Lizard, Anolis carolinensis, Anat. Rec., 1971, vol. 170, no. 3, pp. 285–301.

    Article  PubMed  CAS  Google Scholar 

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  1. Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    A. A. Ogienko, S. A. Fedorova & E. M. Baricheva

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Original Russian Text © A.A. Ogienko, S.A. Fedorova, E.M. Baricheva, 2007, published in Genetika, 2007, Vol. 43, No. 10, pp. 1341–1357.

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Ogienko, A.A., Fedorova, S.A. & Baricheva, E.M. Basic aspects of ovarian development in Drosophila melanogaster . Russ J Genet 43, 1120–1134 (2007). https://doi.org/10.1134/S1022795407100055

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