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Cajal bodies in insects. II. Molecular composition of cajal bodies in oocytes of house cricket. Relationship between cajal bodies and interchromatin granule clusters

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Abstract

Cajal bodies (CB) in the oocytes of the house cricket Acheta domesticus are large nuclear organelles of regular spherical form and complex inner structure. They are composed of a fibrillar coilin-containing matrix and a central cavity with a prominent fibrogranular body inside. The latter we identified as the “internal” inter-chromatin granule cluster (IGC). Transcription coactivators CBP/p300 and TATA-binding protein (TBP) were localized in the CB matrix. RNA polymerase II was not revealed in CB both under normal conditions and after oocyte treatment with actinomycin D. A small number of free IGCs were detected in the nucleoplasm of Acheta domesticus oocytes. In oocytes treated with actinomycin D the number of free IGCs in the nucleoplasm significantly increased, fibrillar and granular components of IGCs segregated, and the fibrillar zones of IGCs accumulated RNA polymerase II and CBP/p300 proteins.

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Abbreviations

IGC:

interchromatin granule cluster

snRNPs:

small nuclear RNPs

Pol II:

RNA polymerase II

CB:

Cajal body

CBP:

CREB-binding protein

CTD:

C-terminal domain of large subunit of RNA polymerase II

DAPI:

4′,6-diamidino-2-phenylindol

DRB:

5,6-dichloro-1-β-D-ribofuranosylbensimidazole

mAb:

monoclonal antibody

TBP:

TATA-box binding protein

References

  1. Aizenshtadt, T.B., Cytology of the Oogenesis, Moscow: Nauka, 1984.

    Google Scholar 

  2. Alexandrova, O.A., The intranuclear bodies and karyosphere capsule formation in oocytes of the darkling beetle Tentyria nomas taurica, Tsitologiia, 1992, Vol. 34, no. 6, pp. 30–37.

    Google Scholar 

  3. Alexandrova, O.A., Bogolyubov, D.S., and Gruzova, M.N., The karyosphere and intranuclear bodies in the oocyte nuclei of the beetle Tenebrio molitor (Coleoptera, Polyphaga), Tsitologiia, 1995, Vol. 37 no. 12, pp. 1142–1150.

    Google Scholar 

  4. Andrade, L.E.C., Chan, E.K.L., Raška, I., et al., Human antibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin, J. Exp. Med., 1991, Vol. 173, pp. 1407–1419.

    Article  PubMed  CAS  Google Scholar 

  5. Batalova, F.M., Bogolyubov, D.S., and Parfenov, V.N., Karyosphere and extrachromosomal nuclear bodies in oocytes of the scorpionfly, Panorpa communis, Tsitologiia, 2005b, Vol. 47, no. 10, pp. 847–859.

    PubMed  CAS  Google Scholar 

  6. Batalova, F.M., Stepanova, I.S., and Bogolyubov, D.S., Cajal bodies in nuclei of oocytes from the scorpion fly Panorpa communis, Tsitologiia, 2000, Vol. 42, no. 11, pp. 1037–1047.

    PubMed  CAS  Google Scholar 

  7. Batalova, F.M., Stepanova, I.S., Skovorodkin, I.N., et al., Identification and dynamics of Cajal bodies in relation to karyosphere formation in scorpionfly oocytes, Chromosoma, 2005a, Vol. 113. pp. 428–439.

    Article  PubMed  CAS  Google Scholar 

  8. Batalova, F.M. and Tsvetkov, A.G., Nuclear structures from Panorpa communis (Mecoptera) oocytes, Tsitologiia, 1998, Vol. 40, no. 10, pp. 826–834.

    Google Scholar 

  9. Bellini, M. and Gall, J.G., Coilin can form a complex with the U7 small nuclear ribonucleoprotein, Mol. Biol. Cell, 1998, Vol. 9, pp. 2987–3001.

    PubMed  CAS  Google Scholar 

  10. Bellini, M. and Gall, J.G., Coilin shuttles between the nucleus and cytoplasm in Xenopus oocytes, Mol. Biol. Cell, 1999, Vol. 10, pp. 3425–3434.

    PubMed  CAS  Google Scholar 

  11. Bernhard, W., A new staining procedure for electron microscopical cytology. J. Ultrastruct. Res., 1969, Vol. 27, pp. 250–265.

    Article  PubMed  CAS  Google Scholar 

  12. Berry, S.J., RNA synthesis and storage during insect oogenesis. In: Developmental Biology. A comprehensive synthesis, New York, London: Plenum Press, 1985, pp. 351–384.

    Google Scholar 

  13. Bier, K., Kuntz, W. und Ribbert, D., Struktur und Funktion der Oocytenchromosomen und Nukleolen sowie der Extra-DNS während der Oogenese panoistischer und meroistischer Insekten, Chromosoma, 1967, Vol. 23, pp. 214–254.

    Article  PubMed  CAS  Google Scholar 

  14. Biliński, S.M., Filogeneza owadów a struktura i ultrastruktura ich jajników, Przegląd Zool., 1998, Vol. 42, pp. 35–51.

    Google Scholar 

  15. Biliński, S.M. and Kloc, M., Accessory nuclei revisited: the translocation of snRNPs from the germinal vesicle to the periphery of the future embryo, Chromosoma, 2002, Vol. 111, pp. 62–68.

    Article  PubMed  CAS  Google Scholar 

  16. Bogolyubov, D.S., Cajal bodies in insect oocytes. I. Identification and immunocytochemical characteristics of Cajal bodies in vitellogenic oocytes of the yellow mealworm beetle, Tenebrio molitor, Tsitilogiia, 2003, Vol. 45, no. 11, pp. 1083–1093.

    Google Scholar 

  17. Bogolyubov, D.S., Alexandrova, O.A., and Tsvetkov, A.G., The oocyte nucleus in the mealworm Tenebrio molitor (Coleoptera, Polyphaga). Ultrastructural, cytochemical and autoradiographical studies, Tsitologiia, 1997, Vol. 39, no. 8, pp. 643–650.

    Google Scholar 

  18. Bogolyubov, D., Alexandrova, O., Tsvetkov, A., and Parfenov, V., An immunoelectron study of karyosphere and nuclear bodies in oocytes of mealworm beetle, Tenebrio molitor (Coleoptera: Polyphaga). Chromosoma, 2000, Vol. 109, pp. 415–425.

    PubMed  CAS  Google Scholar 

  19. Bogolyubov, D. and Parfenov, V., Immunogold localization of RNA polymerase II and pre-mRNA splicing factors in Tenebrio molitor oocyte nuclei with special emphasis on karyosphere development, Tissue and Cell, 2001, Vol. 33, pp. 549–561.

    Article  PubMed  CAS  Google Scholar 

  20. Bogolyubov, D. and Parfenov, V., Do nuclear bodies in oocytes of Tenebrio molitor (Coleoptera: Polyphaga, Tenebrionidae) contain two forms of RNA polymerase II? Tissue and Cell, 2004, Vol. 36, pp. 13–17.

    Article  PubMed  CAS  Google Scholar 

  21. Brasch, K. and Ochs, R.L., Nuclear bodies (NBs): a newly “rediscovered” organelle, Exp. Cell Res., 1992, Vol. 202, pp. 211–223.

    Article  PubMed  CAS  Google Scholar 

  22. Bregman, D.B., Du, L., van der Zee, S., and Warren, S.L., Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains, J. Cell Biol., 1995, Vol. 129, pp. 287–298.

    Article  PubMed  CAS  Google Scholar 

  23. Büning, J., The ovary of Ectognatha, the insects s.str. In.: The Insect Ovary: Ultrastructure, Previtellogenic Growth and Evolution. London: Chapman and Hall, 1994, pp. 31–400.

    Google Scholar 

  24. Callan, H.G., Gall, J.G., and Murphy, C., Histone genes are located at the sphere loci of Xenopus lampbrush chromosomes, Chromosoma, 1991, Vol. 101, pp. 245–251.

    Article  PubMed  CAS  Google Scholar 

  25. Carmo-Fonseca, M., New clues to the function of the Cajal body, EMBO Reports, 2002, Vol. 3, pp. 726–727.

    Article  PubMed  CAS  Google Scholar 

  26. Cave, M.D., Morphological manifestation of ribosomal DNA amplification during insect oogenesis. In: Insect Ultrastructure, New York, London: Plenum Press, 1982, Vol. 1, pp. 86–117.

    Google Scholar 

  27. Cerami, B.A., Reich, E., Ward, D.C., and Goldberg, I.H., The interaction of actynomycin with DNA: requirement for the 2-amino group of purines, Proc. Natl. Acad. Sci. USA, 1967, Vol. 57, pp. 1036–1042.

    Article  PubMed  CAS  Google Scholar 

  28. Cioce, M. and Lamond, A.I., Cajal bodies: a long history of discovery, Annu. Rev. Cell. Dev. Biol., 2005, Vol. 21, pp. 105–131.

    Article  PubMed  CAS  Google Scholar 

  29. Darzacq, X., Jády, B.E., Verheggen, C., et al., Cajal body-specific small nuclear RNAs: a novel class of 2′-O-methylation and pseudouridylation guide RNAs, EMBO J., 2002, Vol. 21, pp. 2746–2756.

    Article  PubMed  CAS  Google Scholar 

  30. Dominski, Z. and Marzluff, W.F., Formation of the 3′ end of histone mRNA, Gene, 1999, Vol. 239, pp. 1–14.

    Article  PubMed  CAS  Google Scholar 

  31. Doyle, O., Corden, J.L., Murphy, C., and Gall, J.G., The distribution of RNA polymerase II largest subunit (RPB1) in the Xenopus germinal vesicle, J. Struct. Biol., 2002, Vol. 140, pp. 154–166.

    Article  PubMed  CAS  Google Scholar 

  32. Du, L. and Warren, S.L., A functional interaction between the carboxy-terminal domain of RNA polymerase II and pre-mRNA splicing, J. Cell Biol., 1997, Vol. 136, pp. 5–18.

    Article  PubMed  CAS  Google Scholar 

  33. Dundr, M. and Misteli, T., Functional architecture in the cell nucleus, Biochem. J., 2001, Vol. 356, pp. 297–310.

    Article  PubMed  CAS  Google Scholar 

  34. Filek, K., Jarek, E., and Biliński, S.M., Cajal bodies (coiled bodies) in the nuclei of the house cricket (Acheta domesticus) oocytes, Folia Histochem. Cytobiol., 2002, Vol. 40, pp. 221–222.

    PubMed  CAS  Google Scholar 

  35. Frey, M.R. and Matera, A.G., Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells, Proc. Natl. Acad. Sci. USA, 1995, Vol. 92, pp. 5915–5919.

    Article  PubMed  CAS  Google Scholar 

  36. Fu, X.-D. and Maniatis, T., Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus, Nature, 1990, Vol. 343, pp. 437–441.

    Article  PubMed  CAS  Google Scholar 

  37. Gaginskaya, E.R., Problem of classification of oogenesis, Ontogenesis, 1975, Vol. 6, no. 6, pp. 539–545.

    Google Scholar 

  38. Gall, J.G., Cajal bodies: the first 100 years, Annu. Rev. Cell. Dev. Biol., 2000, Vol. 16, pp. 273–300.

    Article  PubMed  CAS  Google Scholar 

  39. Gall, J.G., A role of Cajal bodies in assembly of the nuclear transcription machinery, FEBS Lett., 2001, Vol. 498, pp. 164–167.

    Article  PubMed  CAS  Google Scholar 

  40. Gall, J.G., The centennial of the Cajal body, Nat. Rev. Mol. Cell Biol., 2003, Vol. 4, pp. 975–980.

    Article  PubMed  CAS  Google Scholar 

  41. Gall, J.G., Bellini, M., Wu, Z., and Murphy, C., Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) and transcriptosomes, Mol. Biol. Cell, 1999, Vol. 10, pp. 4385–4402.

    PubMed  CAS  Google Scholar 

  42. Gall, J.G. and Callan, H.G., The sphere organelle contains small nuclear ribonucleoproteins, Proc. Natl. Acad. Sci. USA, 1989, Vol. 86, pp. 6635–6639.

    Article  PubMed  CAS  Google Scholar 

  43. Gall, J.G., Tsvetkov, A., Wu, Z., and Murphy, C., Is the sphere organelle/coiled body a universal nuclear component? Dev. Genet., 1995, Vol. 16, pp. 25–35.

    Article  PubMed  CAS  Google Scholar 

  44. Gall, J.G., Wu, Z., Murphy, C., and Gao, H., Structure in the amphibian germinal vesicle, Exp. Cell Res., 2004, Vol. 296, pp. 28–34.

    Article  PubMed  CAS  Google Scholar 

  45. Gao, L., Frey, M.R., and Matera, A.G., Human genes encoding U3 snRNA associate with coiled bodies in interphase cells and are clustered on chromosome 17p11.2 in a complex inverted repeat structure, Nucleic Acids Res., 1997, Vol. 25, pp. 4740–4747.

    Article  PubMed  CAS  Google Scholar 

  46. Grande, M.A., van der Kraan, I., de Jong, L., and van Driel, R., Nuclear distribution of transcription factors in relation to sites of transcription and RNA polymerase II, J. Cell Sci., 1997, Vol. 110, pp. 1781–1791.

    PubMed  CAS  Google Scholar 

  47. Greenblatt, J., RNA polymerase II holoenzyme and transcriptional regulation. Curr. Opin. Cell Biol., 1997, Vol. 9, pp. 310–319.

    Article  PubMed  CAS  Google Scholar 

  48. Gruzova, M.N., Functional morphology of nuclear structures in different oogenesis types. Usp. Sovr. Genet., 1971, Vol. 3, pp. 206–212.

    Google Scholar 

  49. Gruzova, M.N., The nucleus during oogenesis with special reference to extrachromosomal structures, In: Oocyte growth and maturation, New York: Plenum Press, 1988, pp. 77–163.

    Google Scholar 

  50. Gruzova, M.N., Tsvetkov, A.G., Pochukalina, G.N., and Parfenov, V.N., Karyosphere formation in oogenesis of some insects and amphibians, Tsitologiia, 1995, Vol. 37, no. 8, pp. 744–769.

    PubMed  CAS  Google Scholar 

  51. Gruzova, M.N. and Parfenov, V.N., Karyosphere in oogenesis and intranuclear morphogenesis, Int. Rev. Cytol., 1993, Vol. 144, pp. 1–52.

    PubMed  CAS  Google Scholar 

  52. Halkka, L. and Halkka, O., RNA and protein in nucleolar structures of dragonfly oocytes, Science, 1968, Vol. 162, pp. 803–805.

    Article  PubMed  CAS  Google Scholar 

  53. Handwerger, K.E. and Gall, J.G., Subnuclear organelles: new insights into form and function, Trends Cell Biol., 2006, Vol. 16, pp. 19–26.

    Article  PubMed  CAS  Google Scholar 

  54. Handwerger, K.E., Murphy, C., and Gall, J.G., Steady-state dynamics of Cajal body components in the Xenopus germinal vesicle, J. Cell Biol., 2003, Vol. 160, pp. 495–504.

    Article  PubMed  CAS  Google Scholar 

  55. Hulsebos, T., Hackstein, J. and Henning, W., Lampbrush loopspecific protein of Drosophila hydei, Proc. Natl. Acad. Sci. USA, 1984, Vol. 16, pp. 9415–9429.

    Google Scholar 

  56. Jacobs, E.Y., Frey, M.R., Wu, W., et al., Coiled bodies preferentially associate with U4, U11, and U12 small nuclear RNA genes in interphase HeLa cells but not with U6 and U7 genes. Mol. Biol. Cell, 1999, Vol. 10, pp. 1653–1663.

    PubMed  CAS  Google Scholar 

  57. Jády, B.E., Darzacq, X., Tucker, K.E., et al., Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm, EMBO J., 2003, Vol. 22, pp. 1878–1888.

    Article  PubMed  Google Scholar 

  58. Jaglarz, M.K., Nuclear bodies in the oocyte nucleus of ground beetles are enriched in snRNPs, Tissue and Cell, 2001, Vol. 33, pp. 395–401.

    Article  PubMed  CAS  Google Scholar 

  59. Jaglarz, M.K., Biliński, S.M., and Kloc, M., Assembly and breakdown of Cajal bodies in accessory nuclei of Hymenoptera, Differentiation, 2005, Vol. 73, pp. 99–108.

    Article  PubMed  CAS  Google Scholar 

  60. Jaworska, H. and Lima-de-Faria, A., Amplification of ribosomal DNA in Acheta. VI. Ultrastructure of two types of nucleolar components associated with ribosomal DNA, Hereditas, 1973, Vol. 74, pp. 309–327.

    Google Scholar 

  61. Johnson, C., Primorac, D., McKinstry, M., et al., Tracking COL1A1 RNA in osteogenesis imperfecta: splice-defective transcripts initiate transport from the gene but are retained within the SC35 domain, J. Cell Biol., 2000, Vol. 150, pp. 417–432.

    Article  PubMed  CAS  Google Scholar 

  62. Jordan, P., Cunha, C., and Carmo-Fonseca, M., The cdk7-cyclin H-MAT1 complex associated with TFIIH is localized in coiled bodies, Mol. Biol. Cell, 1997, Vol. 8, pp. 1207–1217.

    PubMed  CAS  Google Scholar 

  63. Jörgensen, M., Zellenstudien. I., Morphologische Beiträge zum Problem des Eiwachstums, Arch. Zellforsch., 1913, Vol. 10, pp. 1–126.

    Google Scholar 

  64. Kim, E., Du, L., Bregman, D.B., and Warren, S.L., Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA, J. Cell Biol., 1997, Vol. 136, pp. 19–28.

    Article  PubMed  CAS  Google Scholar 

  65. King, R.C. and Büning, J., The origin and functioning of insect oocytes and nurse cells, In.: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Oxford: Pergamon Press, 1985, Vol. 1, pp. 37–82.

    Google Scholar 

  66. Krainer, A., Pre-mRNA splicing by complementation with purified human U1, U2, U4/U6 and U5 snRNPs, Nucleic Acids Res., 1988, Vol. 16, pp. 9415–9429.

    Article  PubMed  CAS  Google Scholar 

  67. Kunz, W., Lampenbürstenchromosomen und multiple Nukleolen bei Orthopteren, Chromosoma, 1967, Vol. 21, pp. 446–462.

    Article  PubMed  CAS  Google Scholar 

  68. Lamond, A.I. and Earnshow, W.C., Structure and function in the nucleus, Science, 1998, Vol. 280, pp. 547–553.

    Article  PubMed  CAS  Google Scholar 

  69. Lamond, A.I. and Spector, D.L., Nuclear speckles: a model for nuclear organelles, Nat. Rev. Mol. Cell Biol., 2003, Vol. 4, pp. 605–612.

    Article  PubMed  CAS  Google Scholar 

  70. Leung, A.K.L., Andersen, J.S., Mann, M. and Lamond, A.I., Bioinformatic analysis of the nucleolus, Biochem J., 2003, Vol. 376, pp. 553–569.

    Article  PubMed  CAS  Google Scholar 

  71. Malatesta, M., Zancanaro, C., Martin, T.E., et al., Is the coiled body involved in nucleolar functions? Exp. Cell Res., 1994, Vol. 211, pp. 415–419.

    Article  PubMed  CAS  Google Scholar 

  72. Matera, A.G., Nuclear bodies: multifaceted subdomains of the interchromatin space, Trends Cell Biol., 1999, Vol. 9, pp. 302–309.

    Article  PubMed  CAS  Google Scholar 

  73. Melčák, I., Melčáková, Š., Kopský, V., et al., Prespliceosomal assembly on microinjected precursor mRNA takes place in nuclear speckles, Mol. Biol. Cell. 2001, Vol. 12, pp. 393–406.

    PubMed  Google Scholar 

  74. Methods in developmental biology, Moscow: Nauka, 1974.

  75. Mintz, P.J., Patterson, S.D., Neuwald, A.F., et al., Purification and biochemical characterization of interchromatin granule clusters, EMBO J., 1999, Vol. 18, pp. 4308–4320.

    Article  PubMed  CAS  Google Scholar 

  76. Miralles, F., Öfverstedt, L.-G., Sabri, N., et al., Electron tomography reveals posttranscriptional binding of pre-mRNPs to specific fibers in the nucleoplasm, J. Cell Biol., 2000, Vol. 148, pp. 271–282.

    Article  PubMed  CAS  Google Scholar 

  77. Misteli, T., Cell biology of transcription and pre-mRNA splicing: nuclear architecture meets nuclear function, J. Cell Sci., 2000, Vol. 113, pp. 1841–1849.

    PubMed  CAS  Google Scholar 

  78. Misteli, T., Protein dynamics: implications for nuclear architecture and gene expression, Science, 2001, Vol. 291, pp. 843–847.

    Article  PubMed  CAS  Google Scholar 

  79. Misteli, T. and Spector, D.L., The cellular organization of gene expression, Curr. Opin. Cell Biol., 1998, Vol. 10, pp. 323–331.

    Article  PubMed  CAS  Google Scholar 

  80. Misteli, T. and Spector, D.L., RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo, Mol. Cell. 1999, Vol. 3, pp. 697–705.

    Article  PubMed  CAS  Google Scholar 

  81. Molenaar, C., Abdulle, A., Gena, A., et al., Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells, J. Cell Biol., 2004, Vol. 165, pp. 191–202.

    Article  PubMed  CAS  Google Scholar 

  82. Monneron, A. and Bernhard, W., Fine structural organization of the interphase nucleus in some mammalian cells, J. Ultrastruct. Res. 1969, Vol. 27, pp. 266–288.

    Article  PubMed  CAS  Google Scholar 

  83. Morgan, G.T., Doyle, O., Murphy, C., and Gall, J.G., RNA polymerase II in Cajal bodies of amphibian oocytes, J. Struct. Biol., 2000, Vol. 129, pp. 258–268.

    Article  PubMed  CAS  Google Scholar 

  84. Murphy C., Wang Z., Roeger R.G. and Gall J.G., RNA polymerase III in Cajal bodies and lampbrush chromosomes of the Xenopus oocyte nucleus, Mol. Biol. Cell, 2002, Vol. 13, pp. 3466–3476.

    Article  PubMed  CAS  Google Scholar 

  85. Ogg, S.C. and Lamond, A.I., Cajal bodies and coilin—moving towards function, J. Cell Biol., 2002, Vol. 159, pp. 17–21.

    Article  PubMed  CAS  Google Scholar 

  86. Parfenov, V.N., Davis, D.S., Pochukalina, G.N., et al., Dynamics of distribution of splicing components relative to the transcriptional state of human oocytes from antral follicles, J. Cell Biochem., 1998, Vol. 69, pp. 72–80.

    Article  PubMed  CAS  Google Scholar 

  87. Parfenov, V.N., Pochukalina, G.N., Davis, D.S., et al., Nuclear distribution of Oct-4 transcription factor in transcriptionally active and inactive mouse oocytes and its relation to RNA polymerase II and splicing factors, J. Cell Biochem, 2003, Vol. 89, pp. 720–732.

    Article  PubMed  CAS  Google Scholar 

  88. Perry, R.P. and Kelley, D.E., Inhibition of RNA synthesis by actynomycin D: characteristic doze—response of different RNA species, J. Cell Physiol., 1970, Vol. 76, pp. 127–139.

    Article  PubMed  CAS  Google Scholar 

  89. Raška, I., Andrade, L.E.C., Ochs, R.L., et al., Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies, Exp. Cell Res., 1991, Vol. 195, pp. 27–37.

    Article  PubMed  Google Scholar 

  90. Raška, I., Dundr, M., and Koberna, K., Structure-function subcompartments of the mammalian cell nucleus as revealed by the electron microscopic affinity cytochemistry, Cell Biol. Int. Rep., 1992, Vol. 16, pp. 771–789.

    PubMed  Google Scholar 

  91. Raven, C.P., Oogenesis. The storage of developmental information, New York, Oxford, London: Pergamon Press, 1961.

    Google Scholar 

  92. Reimer, G., Pollard, K., Pennig, C., Ochs, R., et al., 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, 1987, Vol. 30, pp. 793–800.

    Article  PubMed  CAS  Google Scholar 

  93. Sacco-Bubulya, P. and Spector, D.L., Disassembly of interchromatin granule clusters alters the coordination of transcription and pre-mRNA splicing, J. Cell Biol., 2002, Vol. 156, pp. 425–436.

    Article  PubMed  CAS  Google Scholar 

  94. Schul, W., van Driel, R., and de Jong, L., Coiled bodies and U2 snRNA genes adjacent to coiled bodies are enriched in factors required for snRNA transcription, Mol. Biol. Cell, 1998, Vol. 9, pp. 1025–1036.

    PubMed  CAS  Google Scholar 

  95. Sehgal, P.B., Darnell, J.E., Jr., and Tamm, I., The inhibition by DRB (5,6-dichloro-1-β-D-ribofuranosylbenzimidazole) of hnRNA and mRNA production in HeLa cells, Cell, 1976, Vol. 9, pp. 473–480.

    Article  PubMed  CAS  Google Scholar 

  96. Seshachar, B.R. and Bagga, S., A cytochemical study of oogenesis in dragonfly Pantala flavescens (Fabricius), Growth, 1963, Vol. 27, pp. 225–246.

    Google Scholar 

  97. Shikama, N., Lyon, J., and La Thangue, N., The p300/CBP family: integrating signals with transcription factors and chromatin, Trends Cell Biol. 1997, Vol. 7, pp. 230–236.

    Article  CAS  Google Scholar 

  98. Shopland, L.S., Johnson, C.V., and Lawrence, J.B., Evidence that all SC-35 domains contain mRNAs and that transcripts can be structurally constrained within these domains, J. Struct. Biol., 2002, Vol. 140, pp. 131–139.

    Article  PubMed  CAS  Google Scholar 

  99. Sobell, H.M., Actinomycin and DNA transcription, Proc. Natl. Acad. Sci. USA, 1985, Vol. 82, pp. 5328–5331.

    Article  PubMed  CAS  Google Scholar 

  100. Spector, D.L., Macromolecular domains within the cell nucleus, Annu. Rev. Cell Biol. USA, 1993, Vol. 9, pp. 265–315.

    Article  CAS  Google Scholar 

  101. Spector, D.L., Nuclear domains, J. Cell Sci., 2001, Vol. 114, pp. 2891–2893.

    PubMed  CAS  Google Scholar 

  102. Spector, D.L., Fu, X.-D., and Maniatis, T., Associations between distinct pre-mRNA splicing components and the cell nucleus, EMBO J., 1991, Vol. 10, pp. 3467–3481.

    PubMed  CAS  Google Scholar 

  103. Shtein, G.I., Laser scanning confocal microscopy, St.-Petersburg, 2004.

  104. Stepanova, I.S., Bogolyubov, D.S., Skovorodkin, I.N., and Parfenov, V.N., Cajal bodies and interchromatin granule clusters in cricket oocytes: composition, dynamics and interactions, Cell Biol. Int., 2006, in press.

  105. Štys, P. and Biliński, S., Ovariole types and the phylogeny of hexapods, Biol. Rev, 1990, Vol. 65, pp. 401–429.

    Google Scholar 

  106. Świątek, P. and Jaglarz, M.K., SnRNPs are present in the karyosome capsule in the weevil germinal vesicle, Tissue and Cell, 2004, Vol. 36, pp. 253–262.

    Article  PubMed  CAS  Google Scholar 

  107. Telfer, W.H., Development and physiology of the oocyte-nurse syncytium, Adv. Insect Physiol., 1975, Vol. 2, pp. 223–320.

    Article  Google Scholar 

  108. Thompson, C.M., Koleske, A.J., Chao, D.M., and Young, R.A., A multisubunit complex associated with the RNA polymerase II CTD and TATA-binding protein in yeast, Cell, 1993, Vol. 73, pp. 1361–1375.

    Article  PubMed  CAS  Google Scholar 

  109. Thompson, N.E., Steinberg, T.H., Aronson, D.B., and Burgess, R.R., Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II, J. Biol. Chem., 1989, Vol. 264, pp. 11511–11520.

    PubMed  CAS  Google Scholar 

  110. Tsvetkov, A., Alexandrova, O., Bogolyubov, D., and Gruzova, M., Nuclear bodies from cricket and meal-worm oocytes contain splicing factors of pre-mRNA, Eur. J. Entomol., 1997, Vol. 94, pp. 393–407.

    CAS  Google Scholar 

  111. Tsvetkov, A.G., Gruzova, M.N., and Gall, J., Spheres from the oocyte nuclei of the house cricket and the damselfly contain pre-mRNA splicing and pre-rRNA processing factors, Tsitologiia, 1996, Vol. 38, no. 3, pp. 311–318.

    PubMed  CAS  Google Scholar 

  112. Verheggen, C., Lafontaine, D.L.J., Samarsky, D., et al., Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments, EMBO J., 2002, Vol. 21, pp. 2736–2745.

    Article  PubMed  CAS  Google Scholar 

  113. von Mikecz, A., Zhang, S., Montminy, M., et al., CREB-binding protein (CBP)/p300 and RNA polymerase II colocalize in transcriptionally active domains in the nucleus, J. Cell Biol., 2000, Vol. 150, pp. 265–274.

    Article  Google Scholar 

  114. Wu, C.-H. and Gall, J.G., U7 small nuclear RNA in C snurposomes of the Xenopus germinal vesicle, Proc. Natl. Acad. Sci. USA, 1993, Vol. 90, pp. 6257–6259.

    Article  PubMed  CAS  Google Scholar 

  115. Wu, C.-H., Murphy, C., and Gall, J.G., The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes, RNA, 1996, Vol. 2, pp. 811–823.

    PubMed  CAS  Google Scholar 

  116. Wu, Z., Murphy, C., Callan, H.G., and Gall, J.G., Small nuclear ribonucleoproteins and heterogeneous nuclear ribonucleoproteins in the amphibian germinal vesicle: loops, spheres and snurposomes, J. Cell Biol., 1991, Vol. 113, pp. 465–483.

    Article  PubMed  CAS  Google Scholar 

  117. Yu, Y.T., Shu, M.D., and Steitz, J.A., Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing, EMBO J., 1998, Vol. 17, pp. 5783–5795.

    Article  PubMed  CAS  Google Scholar 

  118. Zandomeni, R., Zandomeni, M.C., Shugar, D., and Weinmann, R., Casein kinase type II is involved in the inhibition by 5,6-Dichloro-1-β-D-ribofuranosylbenz-imidazole of specific RNA polymerase II transcription, J. Biol. Chem., 1986, Vol. 261, pp. 3414–3419.

    PubMed  CAS  Google Scholar 

  119. Żelazowska, M. and Jaglarz, M.K., Oogenesis in phthirapterans (Insecta: Phthiraptera). I. Morphological and histochemical characterization of the oocyte nucleus and its inclusions, Arthr. Struct. Dev., 2004, Vol. 33, pp. 161–172.

    Article  Google Scholar 

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Original Russian Text © I.S. Stepanova, D.S. Bogolyubov, V.N. Parfenov, 2007, published in Tsitologiya, Vol. 49, No. 1, 2007, pp. 5–20.

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Stepanova, I.S., Bogolyubov, D.S. & Parfenov, V.N. Cajal bodies in insects. II. Molecular composition of cajal bodies in oocytes of house cricket. Relationship between cajal bodies and interchromatin granule clusters. Cell Tiss. Biol. 1, 14–29 (2007). https://doi.org/10.1134/S1990519X07010038

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