Chromosome Research

, Volume 14, Issue 4, pp 465–475 | Cite as

Nuclear bodies in the Drosophila germinal vesicle



The germinal vesicle of the Drosophila oocyte is transcriptionally quiescent during the latter part of the first meiotic prophase. Concomitant with silencing of the genome, the nucleolus disappears at an early stage and the chromatin condenses into a compact mass called the karyosome. A prominent Cajal body (endobody) is present during most of prophase, attached to the karyosome. Components of the U7 small nuclear (sn) RNP reside in a separate body, the histone locus body, which is also attached to the karyosome. The histone locus body is no longer detectable with probes for the U7 snRNP after about stage 5 of oogenesis. Several other nuclear bodies of unknown nature can be detected by phase contrast, differential interference contrast, and electron microscopy.

Key words

Cajal body histone locus body karyosome scaRNA SMN snRNA U7 snRNP 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ambrosio L, Schedl P (1985) Two discrete modes of histone gene expression during oogenesis in Drosophila melanogaster. Dev Biol 111: 220–231.PubMedCrossRefGoogle Scholar
  2. Andrade LEC, Chan EKL, Raska I, Peebles CL, Roos G, Tan EM (1991) Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med 173: 1407–1419.PubMedCrossRefGoogle Scholar
  3. Batalova FM, Stepanova IS, Skovorodkin IN, Bogolyubov DS, Parfenov VN (2005) Identification and dynamics of Cajal bodies in relation to karyosphere formation in scorpionfly oocytes. Chromosoma 113: 428–439.PubMedCrossRefGoogle Scholar
  4. Bier K, Kunz W, Ribbert D (1967) Struktur und Funktion der Oocytenchromosomen und Nukleolen sowie der Extra-DNS während der Oogenese panoistischer und meroistischer Insekten. Chromosoma 23: 214–254.PubMedCrossRefGoogle Scholar
  5. Bier K, Kunz W, Ribbert D (1969) Insect oogenesis with and without lampbrush chromosomes. Chromosome Today 2: 107–115.Google Scholar
  6. Brahms H, Raymackers J, Union A, de Keyser F, Meheus L, Lührmann R (2000) The C-terminal RG dipeptide repeats of the spliceosomal Sm proteins D1 and D3 contain symmetrical dimethylarginines, which form a major B-cell epitope for anti-Sm autoantibodies. J Biol Chem 275: 17122–17129.PubMedCrossRefGoogle Scholar
  7. Brahms H, Meheus L, de Brabandere V, Fischer U, Lührmann R (2001) Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B′ and the Sm-like protein LSm4, and their interaction with the SMN protein. RNA 7: 1531–1542.PubMedCrossRefGoogle Scholar
  8. Carmo-Fonseca M (2002) New clues to the function of the Cajal body. EMBO Rep 3: 726–727.PubMedCrossRefGoogle Scholar
  9. Cave MD (1973) Synthesis and characterization of amplified DNA in oocytes of the house cricket Acheta domesticus (Orthoptera:Gryllidae). Chromosoma 42: 1–22.PubMedCrossRefGoogle Scholar
  10. Cioce M, Lamond A (2005) Cajal bodies: a long history of discovery. Annu Rev Cell Dev Biol 21: 105–131.PubMedCrossRefGoogle Scholar
  11. Darzacq X, Jády BE, Verheggen C, Kiss AM, Bertrand E, Kiss T (2002) Cajal body-specific small nuclear RNAs: a novel class of 2′-O-methylation and pseudouridylation guide RNAs. EMBO J 21: 2746–2756.PubMedCrossRefGoogle Scholar
  12. Dej KJ, Spradling AC (1999) The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis. Development 126: 293–303.PubMedGoogle Scholar
  13. Dominski Z, Marzluff WF (1999) Formation of the 3′ end of histone mRNA. Gene 239: 1–14.PubMedCrossRefGoogle Scholar
  14. Frey MR, Matera AG (1995) Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc Natl Acad Sci USA 92: 5915–5919.PubMedCrossRefGoogle Scholar
  15. Gall JG (2003) The centennial of the Cajal body. Nature Rev Mol Cell Biol 4: 975–980.CrossRefGoogle Scholar
  16. Gall JG, Tsvetkov A, Wu Z, Murphy C (1995) Is the sphere organelle/coiled body a universal nuclear component? Dev Genet 16: 25–35.PubMedCrossRefGoogle Scholar
  17. Gall JG, Bellini M, Wu Z, Murphy C (1999) Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) and transcriptosomes. Mol Biol Cell 10: 4385–4402.PubMedGoogle Scholar
  18. Gall JG, Wu Za, Murphy C, Gao H (2004) Structure in the amphibian germinal vesicle. Exp Cell Res 296: 28–34.PubMedCrossRefGoogle Scholar
  19. Gerbi SA, Borovjagin AV, Lange TS (2003) The nucleolus: a site of ribonucleoprotein maturation. Curr Opin Cell Biol 15: 318–325.PubMedCrossRefGoogle Scholar
  20. Ghabrial A, Schupbach T (1999) Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat Cell Biol 1: 354–357.PubMedCrossRefGoogle Scholar
  21. Ghabrial A, Ray RP, Schupbach T (1998) okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev 12: 2711–2723.PubMedGoogle Scholar
  22. Godfrey AC, Kupsco JM, Burch B et al. (2006) U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis. RNA 12: 396–409.PubMedCrossRefGoogle Scholar
  23. Grace TD (1962) Establishment of four strains of cells from insect tissues grown in vitro. Nature 195: 788–789.PubMedGoogle Scholar
  24. Gruzova MN, Parfenov VN (1993) Karyosphere in oogenesis and intranuclear morphogenesis. Int Rev Cytol 144: 1–52.PubMedCrossRefGoogle Scholar
  25. Ivanovska I, Khandan T, Ito T, Orr-Weaver TL (2005) A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Genes Dev 19: 2571–2582.PubMedCrossRefGoogle Scholar
  26. Jaglarz MK (2001) Nuclear bodies in the oocyte nucleus of ground beetles are enriched in snRNPs. Tissue Cell 33: 395–401.PubMedCrossRefGoogle Scholar
  27. Jörgensen M (1913) Zellenstudien I. Morphologische Beiträge zum Problem des Eiwachstums. Arch Zellforsch 10: 1–126.Google Scholar
  28. King RC (1970) Ovarian Development in Drosophila melanogaster. New York: Academic Press.Google Scholar
  29. Lerner EA, Lerner MR, Janeway CA, Steitz JA (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci USA 78: 2737–2741.PubMedCrossRefGoogle Scholar
  30. Lima-de-Faria A, Birnstiel ML, Jaworska H (1969) Amplification of ribosomal cistrons in heterochromatin of Acheta. Genetics 61(Suppl): 145–159.PubMedGoogle Scholar
  31. Liu Q, Dreyfuss G (1996) A novel nuclear structure containing the survival of motor neurons protein. EMBO J 15: 3555–3565.PubMedGoogle Scholar
  32. Liu J-L, Murphy C, Buszczak M, Clatterbuck S, Goodman R, Gall JG (2006) The Drosophila melanogaster Cajal body. J Cell Biol 172: 875–884.PubMedCrossRefGoogle Scholar
  33. Mahowald AP (1972) Ultrastructural observations on oogenesis in Drosophila. J Morphol 137: 29–48.PubMedCrossRefGoogle Scholar
  34. Mahowald AP, Strassheim JM (1970) Intercellular migration of centrioles in the germarium of Drosophila melanogaster. An electron microscopic study. J Cell Biol 45: 306–320.PubMedCrossRefGoogle Scholar
  35. Mahowald AP, Tiefert M (1970) Fine structural changes in the Drosophila oocyte nucleus during a short period of RNA synthesis. Wilhelm Roux’ Arch Entwicklungsmech Org 165: 8–25.CrossRefGoogle Scholar
  36. Mahowald AP, Caulton JH, Gehring WJ (1979) Ultrastructural studies of oocytes and embryos derived from females flies carrying the grandchildless mutation in Drosophila subobscura. Dev Biol 69: 118–132.PubMedCrossRefGoogle Scholar
  37. Marzluff WF (2005) Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr Opin Cell Biol 17: 274–280.PubMedCrossRefGoogle Scholar
  38. Matera AG (2003) Cajal bodies. Curr Biol 13: R503.PubMedCrossRefGoogle Scholar
  39. Matera AG, Frey MR (1998) Coiled bodies and gems: Janus or Gemini? Am J Hum Genet 63: 317–321.PubMedCrossRefGoogle Scholar
  40. McKim KS, Jang JK, Manheim EA (2002) Meiotic recombination and chromosome segregation in Drosophila females. Annu Rev Genet 36: 205–232.PubMedCrossRefGoogle Scholar
  41. Monneron A, Bernhard W (1969) Fine structural organization of the interphase nucleus in some mammalian cells. J Ultrastruct Res 27: 266–288.PubMedCrossRefGoogle Scholar
  42. Morgan GT (2002) Lampbrush chromosomes and associated bodies: new insights into principles of nuclear structure and function. Chromosome Res 10: 177–200.PubMedCrossRefGoogle Scholar
  43. Morin X, Daneman R, Zavortink M, Chia W (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc Natl Acad Sci USA 98: 15050–15055.PubMedCrossRefGoogle Scholar
  44. Olson M, Dundr M, Szebeni A (2000) The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol 10: 189–196.PubMedCrossRefGoogle Scholar
  45. Raska I, Andrade LEC, Ochs RL et al. (1991) Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp Cell Res 195: 27–37.PubMedCrossRefGoogle Scholar
  46. Reimer G, Pollard KM, Penning CA et al. (1987) Monoclonal autoantibody from a (New Zealand black × New Zealand white) F1 mouse and some human scleroderma sera target an Mr 34,000 nucleolar protein of the U3 RNP particle. Arthritis Rheum 30: 793–800.PubMedGoogle Scholar
  47. Reynolds ES (1967) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208–212.CrossRefGoogle Scholar
  48. Richard P, Darzacq X, Bertrand E, Jády BE, Verheggen C, Kiss T (2003) A common sequence motif determines the Cajal body-specific localisation of box H/ACA scaRNAs. EMBO J 22: 4283–4293.PubMedCrossRefGoogle Scholar
  49. Ruddell A, Jacobs-Lorena M (1985) Biphasic pattern of histone gene expression during Drosophila oogenesis. Proc Natl Acad Sci USA 82: 3316–3319.PubMedCrossRefGoogle Scholar
  50. Scheer U, Hock R (1999) Structure and function of the nucleolus. Curr Opin Cell Biol 11: 385–390.PubMedCrossRefGoogle Scholar
  51. Spradling AC (1993) Developmental Genetics of Oogenesis. In Bate M, Martinez-Arias A, eds., The Development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, pp. 1–70.Google Scholar
  52. Tsvetkov AG, Gruzova MN, Gall JG (1996) Spheres from cricket and damselfly oocytes contain factors for splicing of pre-mRNA and processing of pre-rRNA. Tsitologia 38: 311–318.Google Scholar
  53. Wallace RA, Jared DW, Dumont JN, Sega MW (1973) Protein incorporation by isolated amphibian oocytes: III. Optimum incubation conditions. J Exp Zool 184: 321–333.PubMedCrossRefGoogle Scholar
  54. Wu C-HH, Gall JG (1993) U7 small nuclear RNA in C snurposomes of the Xenopus germinal vesicle. Proc Natl Acad Sci USA 90: 6257–6259.PubMedCrossRefGoogle Scholar
  55. Zalokar M (1965) Etudes de la formation de l’acide ribonucléique et des protéines chez les insectes. Rev Suisse Zool 72: 241–261.PubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Ji-Long Liu
    • 1
  • Michael Buszczak
    • 1
  • Joseph G. Gall
    • 1
  1. 1.Department of EmbryologyCarnegie InstitutionBaltimoreUSA

Personalised recommendations