Crossref journal-article
The Company of Biologists
Journal of Cell Science (237)
Abstract

ABSTRACT Heteronuciear RNA (hnRNA) is preferentially associated (76%) with the nuclear matrix in mammalian cells. Active mRNA, in the form of polyribosomes, is associated (>97%) with the cytoskeletal framework. In this report, we present evidence that the association of both hnRNA and mRNA with structural networks of the cell may be essential features of gene expression. To study the association of polyribosomes with the cytoskeletal framework, cytochalasin D was used to release mRNA from the cytoskeletal framework. Protein synthesis was inhibited by cytochalasin D in direct proportion to the release of mRNA. The released mRNA is unaltered in its translatability as measured in vitro but is no longer translated in the cytochalasin-treated HeLa cells. The residual protein synthesis occurs on polyribosomes that are reduced in amount but display a normal sedimentation distribution. The results support the hypothesis that mRNA binding to the cytoskeletal framework is necessary, though not sufficient, for translation. Further fractionation of the cytoskeletal framework separates nuclear constituents into three distinct protein fractions. Chromatin proteins and 94% of the DNA are released by 0-25?- ammonium sulphate after inter-nucleosomal DNA is cut with DNase I. The resulting structure retains 76% of the hnRNA in the form of ribonucleoprotein and is designated the RNP-containing nuclear matrix. The proteins of hnRNP complex are those associated with the nucleus only if RNA is intact. These proteins and 97% of the hnRNA are released after brief digestion with RNase A. Visualizing the nuclear matrix using resinless sections shows that nuclear RNA plays an important role in the organization of the nuclear matrix. Electron micrographs of resinless sections show the interior of the matrix to be a three-dimensional network of thick filaments bounded by the nuclear lamina. The filaments are densely covered with 20-30 nm electron-dense particles, which may contain the hnRNA. The RNP-depleted matrix is disordered and the interior fibres aggregated. These results suggest that hnRNA is involved in the spatial organization of the interior of the nuclear matrix.

Bibliography

G. Fey, E., A. Ornelles, D., & Penman, S. (1986). Association Of Rna With The Cytoskeleton And The Nuclear Matrix. Journal of Cell Science, 1986(Supplement_5), 99–119.

Authors 3
  1. Edward G. Fey (first)
  2. David A. Ornelles (additional)
  3. Sheldon Penman (additional)
References 34 Referenced 49
  1. 10.1002/cm.970010303 / Cell Motil. / Video enhanced contrast differential interference microscopy (AVEC-DIC): a new method capable of analysing microtubule related motility in the reticulopodal networks of Allogromia laticollaris. by Allen (1981)
  2. {'key': '2024071012305212600_JOCES_1986_S5_0099C2', 'first-page': '847', 'volume-title': 'Cell Motility', 'author': 'Amos', 'year': '1976'} / Cell Motility by Amos (1976)
  3. 10.1083/jcb.84.1.141 / J. CellBiol. / Head to tail polymerisation of microtubules in vitro. by Bergen (1980)
  4. 10.1083/jcb.84.1.151 / J. CellBiol. / Polarity of microtubules nucleated by centrosomes and chromosomes of Chinese hamster ovary cells in vitro. by Bergen (1980)
  5. {'key': '2024071012305212600_JOCES_1986_S5_0099C5', 'first-page': '278', 'volume': '82', 'author': 'Chalfie', 'year': '1979', 'journal-title': 'Organisation of neuronal microtubules in the nematode Caenorhabditis elegans.J. CellBiol.'} / Organisation of neuronal microtubules in the nematode Caenorhabditis elegans.J. CellBiol. by Chalfie (1979)
  6. 10.1016/0022-2836(71)90057-X / J. molec. Biol. / X-ray diffraction from microtubules by Cohen (1971)
  7. 10.1073/pnas.78.1.372 / Proc. natn. Acad. Sci. U.SA. / Polarity of some motility related microtubules by Euteneuer (1981)
  8. 10.1083/jcb.89.2.338 / J. CellBiol. / Structural polarity of kinetochore microtubules in PtK? cells by Euteneuer (1981)
  9. 10.1083/jcb.100.4.1185 / CellBiol. / Influence of the centrosome on the structure of nucleated microtubules. J’ by Evans (1985)
  10. 10.1083/jcb.91.3.107s / J. CellBiol. / Cillia and flagella of eukaryotes by Gibbons (1981)
  11. 10.1152/physrev.1980.60.4.1167 / Physiol. Rev. / Intracellular transport in neurons by Grafstein (1980)
  12. 10.1073/pnas.76.11.5759 / Proc. natn. Acad. Sci. U.SA. / Dynien binds to and cross bridges cytoplasmic microtubules by Haimo (1979)
  13. 10.1083/jcb.91.3.661 / Cell Biol. / Polarity orientation of axonal microtubules. J’ by Heidemann (1981)
  14. 10.1038/286517a0 / Nature, Land. / Visualisation of the structural polarity of microtubules by Heidemann (1979)
  15. 10.1073/pnas.82.13.4404 / Proc. natn. Acad. Sci. U.SA. / Theoretical problems related to the attachment of microtubules to kinetochores by Hill (1985)
  16. 10.1085/jgp.50.6.259 / J. gen. Physiol. / Cell motility by labile association of macromolecules. The nature of spindle fibres and their role in chromosome movement by Inoue (1967)
  17. 10.1016/S0074-7696(08)60164-3 / Int. Rev. Cytol. / Microtubule assembly and nucleation by Kirschner (1978)
  18. 10.1083/jcb.102.3.1067 / J. Cell Biol. / On the surface lattice of microtubules: Helix starts, protofilament number, seam and handedness by Mandelkow (1986)
  19. 10.1038/293705a0 / Nature, Land. / Microtubule treadmills - possible molecular machinery by Margolis (1981)
  20. 10.1016/0092-8674(84)90411-2 / Cell / Microtubule polarity and the direction of pigment transport reverse simultaneously in surgically severed melanophore arms by McNiven (1984)
  21. 10.1016/0092-8674(86)90283-7 / Cell / Sites of microtubule assembly and disassembly in the mitotic spindle by Mitchison (1986)
  22. 10.1038/312232a0 / Nature, Lond. / Microtubule assembly nucleated by isolated centrosomes by Mitchison (1984)
  23. 10.1038/312237a0 / Nature, Land. / Dynamic instability of microtubule growth by Mitchison (1984)
  24. {'key': '2024071012305212600_JOCES_1986_S5_0099C24', 'first-page': '755', 'article-title': 'Properties of the kinetochore in vitro.', 'volume': '101', 'author': 'Mitchison', 'year': '1985', 'journal-title': 'I. Microtubule nucleation and tubulin binding. J. Cell Biol.'} / I. Microtubule nucleation and tubulin binding. J. Cell Biol. / Properties of the kinetochore in vitro. by Mitchison (1985)
  25. 10.1083/jcb.101.3.766 / J. Cell Biol. / Properties of the kinetochore in vitro. II. Microtubule capture and ATP dependent translocation by Mitchison (1985)
  26. 10.1007/978-1-4615-9588-5_5 / Adv. Cell Biol. / Mitosis by Nicklas (1971)
  27. 10.1016/0092-8674(82)90435-4 / Cell / Rethinking mitosis by Pickett-Heaps (1982)
  28. 10.1002/9780470719442.ch13 / Ciba Fdn Symp. Principles of Biomolec. Org. London: Churchill / Cytoplasmic microtubules and their functions by Porter (1966)
  29. 10.1073/pnas.74.5.2045 / Proc. natn. Acad. Sci. U.SA. / The direction of active sliding of microtubules in Tetrahymena cilia by Sale (1977)
  30. 10.1038/318483a0 / Nature, Lond. / Identification of kinesin in sea urchin eggs, and evidence for its localisation in the mitotic spindle by Scholey (1985)
  31. 10.1073/pnas.72.10.4023 / Proc. natn. Acad. Sci. U.SA. / Assembly of microtubules onto kinetochores of isolated mitotic chromosomes of HeLa cells by Telzer (1975)
  32. 10.1016/S0092-8674(85)80099-4 / Cell / Identification of a novel force generating protein, kinesin, involved in microtubule base motility by Vale (1985)
  33. 10.1016/0092-8674(85)90234-X / Cell / Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. by Vale (1985)
  34. 10.1016/0092-8674(85)90204-1 / Cell / Organelle, bead and microtubule translocations promoted by soluble factors from the squid giant axon by Vale (1985)
Dates
Type When
Created 12 years, 3 months ago (May 23, 2013, 12:25 a.m.)
Deposited 1 year, 1 month ago (July 10, 2024, 8:31 a.m.)
Indexed 1 month, 3 weeks ago (July 2, 2025, 2:35 p.m.)
Issued 39 years, 6 months ago (Feb. 1, 1986)
Published 39 years, 6 months ago (Feb. 1, 1986)
Published Online 39 years, 6 months ago (Feb. 1, 1986)
Published Print 39 years, 6 months ago (Feb. 1, 1986)
Funders 0

None

@article{G_Fey_1986, title={Association Of Rna With The Cytoskeleton And The Nuclear Matrix}, volume={1986}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.1986.supplement_5.6}, DOI={10.1242/jcs.1986.supplement_5.6}, number={Supplement_5}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={G. Fey, Edward and A. Ornelles, David and Penman, Sheldon}, year={1986}, month=feb, pages={99–119} }