Skip to main content

Fusome as a Cell-Cell Communication Channel of Drosophila Ovarian Cyst

  • Chapter
Book cover Cell-Cell Channels

Abstract

In most animal species, female and male gametes are produced within clusters of germ cells which share a common cytoplasm through cell-cell channels. In Drosophila ovaries, these cells synchronise their divisions and specialise one cell of the cluster as the future egg. Both processes are organised by a germline-specific organelle of communication called the fusome. Until recently, the fusome has remained largely mysterious despite a hundred years of research on its composition, formation and functions. Novel results have now suggested several molecular mechanisms to explain how the fusome synchronises the divisions by controlling cell-cycle regulators and how it determines and polarises the future egg by organising the microtubule cytoskeleton. Importantly, a structure similar to the fusome has been identified during Xenopus oogenesis, suggesting that it is widely conserved from invertebrates to vertebrates, and that it thus serves an essential function.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Pepling ME, de Cuevas M, Spradling AC. Germline cysts: A conserved phase of germ cell development. Trends Cell Biol 1999; 9:257–262.

    Article  PubMed  CAS  Google Scholar 

  2. Giardina A. Origine dell’oocite e delle cellule nutrici nel Dytiscus. Int Mschr Anat Physiol 1901; 18:417–484.

    Google Scholar 

  3. Grieder N, De Cuevas M, Spradling A. The fusome organizes the microtubules network during oocyte differentiation in Drosophila. Development 2000; 127:4253–4264.

    PubMed  CAS  Google Scholar 

  4. Braun RE, Behringer RR, Peschon JJ et al. Genetically haploid spermatids are phenotypically diploid. Nature 1989; 337:373–376.

    Article  PubMed  CAS  Google Scholar 

  5. Hime G, Brill J, Fuller M. Assembly of ring canals in the male germ line from structural components of the contractile ring. J Cell Sci 1996; 109:2779–2788.

    PubMed  CAS  Google Scholar 

  6. Telfer W. Development and physiology of the oocyte-nurse cell syncytium. Adv Insect Physiol 1975; 11:223–319.

    Article  Google Scholar 

  7. Buning J. The Insect Ovary: Ultrastructure, previtellogenic growth and evolution. New-York: Chapman and Hall, 1994.

    Google Scholar 

  8. Kloc M, Bilinski S, Dougherty MT et al. Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol 2004; 266:43–61.

    Article  PubMed  CAS  Google Scholar 

  9. de Cuevas M, Lee JL, Spradling AC. α-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 1996; 124:3959–3968.

    Google Scholar 

  10. Yue L, Spradling A. hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev 1992; 6:2443–2454.

    Article  PubMed  CAS  Google Scholar 

  11. Cooley L. Drosophila ring canal growth requires Src and Tec kinases. Cell 1998; 93:913–915.

    Article  PubMed  CAS  Google Scholar 

  12. Hudson AM, Cooley L. Understanding the function of actin-binding proteins through genetic analysis of Drosophila oogenesis. Annu Rev Genet 2002; 36:455–488.

    Article  PubMed  CAS  Google Scholar 

  13. Spradling A, Drummond-Barbosa D, Kai T. Stem cells find their niche. Nature 2001; 414:98–104.

    Article  PubMed  CAS  Google Scholar 

  14. de Cuevas M, Lilly MA, Spradling AC. Germline cyst formation in Drosophila. Annu Rev Genet 1997; 31:405–428.

    Article  PubMed  Google Scholar 

  15. Huynh JR, St Johnston D. The origin of asymmetry: Early polarisation of the Drosophila germline cyst and oocyte. Curr Biol 2004; 14:R438–449.

    Article  PubMed  CAS  Google Scholar 

  16. Spradling A. Developmental genetics of oogenesis. In: Bate M, Martinez-Arias A, eds. The Development of Drosophila melanogaster. New-York: Cold Spring Harbor Laboratory Press, 1993:1–70.

    Google Scholar 

  17. Gonzalez-Reyes A. Stem cells, niches and cadherins: A view from Drosophila. J Cell Sci 2003; 116:949–954.

    Article  PubMed  CAS  Google Scholar 

  18. Platner G. Die Karyokinese bie den Lepidopteran als Grundlage fur eine Theorie der Zellteilung. Int Mschr Anat Physiol 1886; 3:341–398.

    Google Scholar 

  19. Koch E, King R. The origin and early differentiation of the egg chamber of Drosophila. J Morph 1966; 119:283–304.

    Article  PubMed  CAS  Google Scholar 

  20. Mahowald AP. The formation of ring canals by cell furrows in Drosophila. Z Zellforsch Mikrosk Anat 1971; 118:162–167.

    Article  PubMed  CAS  Google Scholar 

  21. Mahowald AP. Ultrastructural observations on oogenesis in Drosophila. J Morphol 1972; 137:29–48.

    Article  PubMed  CAS  Google Scholar 

  22. de Cuevas M, Spradling AC. Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 1998; 125:2781–2789.

    PubMed  Google Scholar 

  23. Lin H, Spradling A. Fusome asymmetry and oocyte determination in Drosophila. Dev Genet 1995; 16:6–12.

    Article  PubMed  CAS  Google Scholar 

  24. Lin H, Yue L, Spradling A. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 1994; 120:947–956.

    PubMed  CAS  Google Scholar 

  25. Zaccai M, Lipshitz H. Role of Adducin-like (hu-li tai shao) mRNA and protein localization in regulating cytoskeletal structure and function during Drosophila oogenesis and early embryogenesis. Dev Genet 1996; 19:249–257.

    Article  PubMed  CAS  Google Scholar 

  26. Snapp EL, Iida T, Frescas D et al. The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. Mol Biol Cell 2004; 15:4512–4521.

    Article  PubMed  CAS  Google Scholar 

  27. Lin H, Spradling A. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997; 124:2463–2476.

    PubMed  CAS  Google Scholar 

  28. Xie TAS. A niche maintaining germline stem cells in the Drosophila ovary. Science 2000; 290:328–330.

    Article  PubMed  CAS  Google Scholar 

  29. Deng W, 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; 189:79–94.

    Article  PubMed  CAS  Google Scholar 

  30. Lin H, Spradling AC. Fusome asymmetry and oocyte determination in Drosophila. Dev Gen 1995; 16:6–12.

    Article  CAS  Google Scholar 

  31. McGrail M, Hays TS. The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 1997; 124:2409–2419.

    PubMed  CAS  Google Scholar 

  32. Storto PD, King RC. The role of polyfusomes in generating branched chains of cystocytes during Drosophila oogenesis. Dev Genet 1989; 10:70–86.

    Article  PubMed  CAS  Google Scholar 

  33. Huynh JR, Petronczki M, Knoblich JA et al. Bazooka and PAR-6 are required with PAR-1 for the maintenance of oocyte fate in Drosophila. Curr Biol 2001; 11:901–906.

    Article  PubMed  CAS  Google Scholar 

  34. Bolivar J, Huynh JR, Lopez-Schier H et al. Centrosome migration into the Drosophila oocyte is independent of BicD and egl, and of the organisation of the microtubule cytoskeleton. Development 2001; 128:1889–1897.

    PubMed  CAS  Google Scholar 

  35. Liu Z, Xie T, Steward R. Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation. Development 1999; 126:4477–4488.

    PubMed  CAS  Google Scholar 

  36. Mathe E, Inoue YH, Palframan W et al. Orbit/Mast, the CLASP orthologue of Drosophila, is required for asymmetric stem cell and cystocyte divisions and development of the polarised microtubule network that interconnects oocyte and nurse cells during oogenesis. Development 2003; 130:901–915.

    Article  PubMed  CAS  Google Scholar 

  37. Riparbelli MG, Massarelli C, Robbins LG et al. The abnormal spindle protein is required for germ cell mitosis and oocyte differentiation during Drosophila oogenesis. Exp Cell Res 2004; 298:96–106.

    Article  PubMed  CAS  Google Scholar 

  38. Cox RT, Spradling AC. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 2003; 130:1579–1590.

    Article  PubMed  CAS  Google Scholar 

  39. Hirschler J. Gesetzmassigkeiten in den Ei-Nahrzellenverbanden. Zool Jb Abt Allg Zool Physiol 1945; 61:141–236.

    Google Scholar 

  40. Straight AF, Field CM. Microtubules, membranes and cytokinesis. Curr Biol 2000; 10:R760–770.

    Article  PubMed  CAS  Google Scholar 

  41. Bennett V, Baines AJ. Spectrin and ankyrin-based pathways: Metazoan inventions for integrating cells into tissues. Physiol Rev 2001; 81:1353–1392.

    PubMed  CAS  Google Scholar 

  42. Devarajan P, Stabach PR, Mann AS et al. Identification of a small cytoplasmic ankyrin (AnkG119) in the kidney and muscle that binds beta I sigma spectrin and associates with the Golgi apparatus. J Cell Biol 1996; 133:819–830.

    Article  PubMed  CAS  Google Scholar 

  43. McCartney BM, Fehon RG. Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J Cell Biol 1996; 133:843–852.

    Article  PubMed  CAS  Google Scholar 

  44. Djagaeva I, Doronkin S, Beckendorf SK. Src64 is involved in fusome development and karyosome formation during Drosophila oogenesis. Dev Biol 2005.

    Google Scholar 

  45. McKearin D, Ohlstein B. A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 1995; 121:2937–2947.

    PubMed  CAS  Google Scholar 

  46. McKearin D, Spradling A. bag-of-marbles: A Drosophila gene required to initiate both male and female gametogenesis. Genes Dev 1990; 4:2242–2251.

    Article  PubMed  CAS  Google Scholar 

  47. Lavoie CA, Ohlstein B, McKearin DM. Localization and function of Bam protein require the benign gonial cell neoplasm gene product. Dev Biol 1999; 212:405–413.

    Article  PubMed  CAS  Google Scholar 

  48. Leon A, McKearin D. Identification of TER94, an AAA ATPase protein, as a Bam-dependent component of the Drosophila fusome. Mol Biol Cell 1999; 10:3825–3834.

    PubMed  CAS  Google Scholar 

  49. Benton R, Palacios IM, St Johnston D. Drosophila 14-3-3/PAR-5 is an essential mediator of PAR-1 function in axis formation. Dev Cell 2002; 3:659–671.

    Article  PubMed  CAS  Google Scholar 

  50. Cox DN, Lu B, Sun T et al. Drosophila par-1 is required for oocyte differentiation and microtubule organization. Curr Biol 2001; 11:75–87.

    Article  PubMed  CAS  Google Scholar 

  51. Huynh JR, Shulman JM, Benton R et al. PAR-1 is required for the maintenance of oocyte fate in Drosophila. Development 2001; 128:1201–1209.

    PubMed  CAS  Google Scholar 

  52. Martin SG, St Johnston D. A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 2003; 421:379–384.

    Article  PubMed  CAS  Google Scholar 

  53. Ohlmeyer JT, Schupbach T. Encore facilitates SCF-Ubiquitin-proteasome-dependent proteolysis during Drosophila oogenesis. Development 2003; 130:6339–6349.

    Article  PubMed  CAS  Google Scholar 

  54. Roper K, Brown NH. A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr Biol 2004; 14:99–110.

    PubMed  CAS  Google Scholar 

  55. Lilly MA, de Cuevas M, Spradling AC. Cyclin A associates with the fusome during germline cyst formation in the Drosophila ovary. Dev Biol 2000; 218:53–63.

    Article  PubMed  CAS  Google Scholar 

  56. Hawkins N, Thorpe J, Schupbach T. Encore, a gene required for the regulation of germ line mitosis and oocyte differentiation during Drosophila oogenesis. Development 1996; 122:281–290.

    PubMed  CAS  Google Scholar 

  57. Lilly M, Spradling A. The Drosophila endocyde is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev 1996; 10:2514–2526.

    Article  PubMed  CAS  Google Scholar 

  58. Carpenter A. Electron microscopy of meiosis in Drosophila melanogaster females. I Structure, arrengement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 1975; 51:157–182.

    Article  PubMed  CAS  Google Scholar 

  59. Carpenter A. Egalitarian and the choice of cell fates in Drosophila melanogaster oogenesis. Ciba Found Symp 1994; 182:223–246,(246–254).

    PubMed  CAS  Google Scholar 

  60. Theurkauf WE. Microtubules and cytoplasm organisation during Drosophila oogenesis. Dev Biol 1994; 165:352–360.

    Article  PubMed  CAS  Google Scholar 

  61. Storto P, King R. The role of polyfusomes in generating branched chains of cystocytes during Drosophila oogenesis. Dev Genet 1989; 10:70–86.

    Article  PubMed  CAS  Google Scholar 

  62. Lambert JD, Nagy LM. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 2002; 420:682–686.

    Article  PubMed  CAS  Google Scholar 

  63. Theurkauf W, Alberts M, Jan Y et al. A central role for microtubules in the differentiation of Drosophila oocytes. Development 1993; 118:1169–1180.

    PubMed  CAS  Google Scholar 

  64. Koch E, Spitzer R. Multiple effects of colchicine on oogenesis in Drosophila; induced sterility and switch of potencial oocyte to nurse-cell developmental pathway. Cell Tissue Res 1983; 228:21–32.

    Article  PubMed  CAS  Google Scholar 

  65. Mach JM, Lehmann R. An Egalitarian-BicaudalD complex is essential for oocyte specification and axis determination in Drosophila. Genes Dev 1997; 11:423–435.

    Article  PubMed  CAS  Google Scholar 

  66. Navarro C, Puthalakath H, Adams JM et al. Egalitarian binds dynein light chain to establish oocyte polarity and maintain oocyte fate. Nat Cell Biol 2004; 6:427–435.

    Article  PubMed  CAS  Google Scholar 

  67. Ran B, Bopp R, Suter B. Null alleles reveal novel requirements for Bic-D during Drosophila oogenesis and zygotic development. Development 1994; 120:1233–1242.

    PubMed  CAS  Google Scholar 

  68. Huynh JR, St Johnston D. The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte. Development 2000; 127:2785–2794.

    PubMed  CAS  Google Scholar 

  69. Paré C, Suter B. Subcellular localization of Bic-D:GFP is linked to an asymmetric oocyte nucleus. J Cell Sci 2000; 113:2119–2127.

    PubMed  Google Scholar 

  70. Pellettieri J, Seydoux G. Anterior-posterior polarity in C. elegans and Drosophila-PARallels and differences. Science 2002; 298:1946–1950.

    Article  PubMed  CAS  Google Scholar 

  71. Ohno S. Intercellular junctions and cellular polarity: The PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol 2001; 13:641–648.

    Article  PubMed  CAS  Google Scholar 

  72. Kai T, Williams D, Spradling AC. The expression profile of purified Drosophila germline stem cells. Dev Biol 2005.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Huynh, JR. (2006). Fusome as a Cell-Cell Communication Channel of Drosophila Ovarian Cyst. In: Cell-Cell Channels. Springer, New York, NY. https://doi.org/10.1007/978-0-387-46957-7_16

Download citation

Publish with us

Policies and ethics