Skip to main content
Log in

Electron microscope tomography of Balbiani Ring hnRNP substructure

  • Original Articles
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Three-dimensional (3-D) reconstructions, by electron microscope tomography, of selectively stained, contrast enhanced Balbiani Ring (BR) hnRNP granules reveal a complex spatial arrangement of RNA-rich domains. This particulate substructure was examined by volume rendering computer graphics. Modeling the arrangement of RNA-rich domains is made difficult by apparent structural flexibility and/or heterogeneity of composition. Formulation of a consensus 3-D arrangement of RNA-rich domains will require an expanded data base of reconstructed BR granules and the development of new image manipulation and analysis techniques. This study demonstrates the potential for ultra-structural cell biology of combining several new techniques: selective nucleic acid staining, electron spectroscopic imaging to enhance contrast, electron microscope tomography and volume rendering computer graphics.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

BR:

Balbiani Ring

EMT:

electron microscope tomography

ESI:

electron spectroscopic imaging

hnRNP:

heterogeneous nuclear ribonucleoprotein

OA-B:

osmium ammine-B

kb:

kilobases

References

  • Bazett-Jones DP, Locklear L, Rattner JB (1988) Electron spectroscopic imaging of DNA. J Ultrastruct Mol Struct Res 99:48–58

    Google Scholar 

  • Beermann W, Bahr GF (1954) The submicroscopic structure of the Balbiani Ring. Exp Cell Res 6:195–201

    Google Scholar 

  • Botella LM, Edström J-E (1991) The Balbiani Ring 6 induction in chironomus. Biol Cell 71:11–16

    Google Scholar 

  • Daneholt B (1982) Structural and functional analysis of Balbiani Ring genes in the salivary glands of Chironomus tentans. In: King R, Akai H (eds) Insect ultrastructure, vol 1. Plenum Publishing, New York, pp 382–401

    Google Scholar 

  • Hamming RW (1983) Digital filters. Prentice-Hall, Englewood Cliffs, NJ, p 257

    Google Scholar 

  • Ineichen H, Meyer B, Lezzi M (1983) Determination of the developmental stage of living fourth instar larvae of Chironomus tentans. Dev Biol 98:278–286

    Google Scholar 

  • Kim S-H, Moyer BA, Azan S, Brown GM, Olins AL, Allison DP (1989) Preparation and properties of the nitrido-bridged osmium (IV) binuclear complexes [OsIV 2N(NH3)10-nCln]Cl5-n (n=2,3). Inorg Chem 28:4648–4650

    Google Scholar 

  • Kirov N, Wurtz T, Daneholt B (1991) The complexity of 75S premessenger RNA in Balbiani ring granules studied by a new RNA band retardation assay. Nucleic Acids Res 19:3377–3382

    Google Scholar 

  • Lönnroth A, Alexciev K, Mehlin H, Wurtz T, Sköglund U, Daneholt B (1992) Demonstration of a 7-nm RNP fiber as a basic structural element in a premessenger RNP particle. Exp Cell Res 199:292–296

    Google Scholar 

  • Mehlin H, Lönnroth A, Sköglund U, Daneholt B (1988) Structure and transport of a specific premessenger RNP particle. Cell Biol Int Rep 12:729–736

    Google Scholar 

  • Mehlin H, Sköglund U, Daneholt B (1991) Transport of Balbiani Ring granules through nuclear pores in Chironomus tentans. Exp Cell Res 193:72–77

    Google Scholar 

  • Meyer B, Mahr R, Eppenberger M, Lezzi M (1983) The activity of Balbiani Rings 1 and 2 in salivary glands of Chironomus tentans larvae under different modes of development and polocarpine treatment. Dev Biol 98:265–277

    Google Scholar 

  • Olins AL, Olins DE, Franke WW (1980) Stereo-electron microscopy of nucleoli, Balbiani Rings and endoplasmic reticulum in chironomus salivary gland cells. Eur J Cell Biol 22:714–723

    Google Scholar 

  • Olins AL, Olins DE, Lezzi M (1982) Ultrastructural studies of chironomus salivary gland cells in different states of Balbiani Ring activity. Eur J Cell Biol 27:161–169

    Google Scholar 

  • Olins AL, Olins DE, Levy HA, Durfee RC, Margle SM, Tinnel EP Hingerty BE, Dover SD, Fuchs H (1984) Modeling Balbiani Ring gene transcription with electron microscope tomography. Eur J Cell Biol 35:129–142

    Google Scholar 

  • Olins AL, Olins DE, Levy HA, Durfee RC, Margle SM, Tinnel EP (1986) DNA compaction during intense transcription measured by electron microscope tomography. Eur J Cell Biol 40:105–110

    Google Scholar 

  • Olins AL, Moyer BA, Kim S-H, Allison DP (1989a) Synthesis of a more stable osmium ammine electron-dense DNA stain. J Histochem Cytochem 37:395–398

    Google Scholar 

  • Olins AL, Olins DE, Levy HA, Margle SM, Tinnel EP, Durfee RC (1989b) Tomography reconstruction from energy-filtered images of thick biological sections. J Microsc 154:257–265

    Google Scholar 

  • Olins AL, Olins DE, Bazett-Jones DP (1992) Balbiani ring hnRNP substructure visualized by selective staining and electron spectroscopic imaging. J Cell Biol 117:483–491

    Google Scholar 

  • Olins DE, Olins AL, Levy HA, Durfee RC, Margle SM, Tinnel EP, Dover SD (1983) Electron microscope tomography: transcription in three dimensions. Science 220:498–500

    Google Scholar 

  • Rattner JB, Bazett-Jones DP (1989) Kinetochore structure: electron spectroscopic imaging of the kinetochore. J Cell Biol 108:1209–1219

    Google Scholar 

  • Sköglund U, Daneholt B (1986) Electron microscope tomography. Trends Biochem Sci 11:499–503

    Google Scholar 

  • Sköglund U, Anderson K, Bjorkroth B, Lamb MM, Daneholt B (1983) Visualization of the formation and transport of a specific hnRNP particle. Cell 34:847–855

    Google Scholar 

  • Sköglund U, Anderson K, Strandberg B, Daneholt B (1986) Three-dimensional structure of a specific pre-messenger RNP established by electron microscope tomography. Nature 319:560–564

    Google Scholar 

  • Stevens BJ, Swift H (1966) RNA transport from nucleus to cytoplasm in chironomus salivary glands. J Cell Biol 31:55–77

    Google Scholar 

  • van Heel M, Frank J (1981) Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6:187–194

    Google Scholar 

  • Wurtz T, Lönnroth A, Ovchinnikov L, Sköglund U, Daneholt B (1990a) Isolation and initial characterization of a specific premessenger ribonucleoprotein particle. Proc Natl Acad Sci USA 87:831–835

    Google Scholar 

  • Wurtz T, Lönnroth A, Daneholt B (1990b) Higher order structure of Balbiani Ring premessenger RNP particles depends on certain RNAse A sensitive sites. J Mol Biol 215:93–101

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

by P.B. Moens

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olins, A.L., Olins, D.E., Levy, H.A. et al. Electron microscope tomography of Balbiani Ring hnRNP substructure. Chromosoma 102, 137–144 (1993). https://doi.org/10.1007/BF00356031

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00356031

Keywords

Navigation