Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Apr 1;110(4):883–894. doi: 10.1083/jcb.110.4.883

Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components

PMCID: PMC2116066  PMID: 2324201

Abstract

Nuclear pore complexes (NPCs) prepared from Xenopus laevis oocyte nuclear envelopes were studied in "intact" form (i.e., unexposed to detergent) and after detergent treatment by a combination of conventional transmission electron microscopy (CTEM) and quantitative scanning transmission electron microscopy (STEM). In correlation- averaged CTEM pictures of negatively stained intact NPCs and of distinct NPC components (i.e., "rings," "spoke" complexes, and "plug- spoke" complexes), several fine structural features arranged with octagonal symmetry about a central axis could reproducibly be identified. STEM micrographs of unstained/freeze-dried intact NPCs as well as of their components yielded comparable but less distinct features. Mass determination by STEM revealed the following molecular masses: intact NPC with plug, 124 +/- 11 MD; intact NPC without plug, 112 +/- 11 MD; heavy ring, 32 +/- 5 MD; light ring, 21 +/- 4 MD; plug- spoke complex, 66 +/- 8 MD; and spoke complex, 52 +/- 3 MD. Based on these combined CTEM and STEM data, a three-dimensional model of the NPC exhibiting eightfold centrosymmetry about an axis perpendicular to the plane of the nuclear envelope but asymmetric along this axis is proposed. This structural polarity of the NPC across the nuclear envelope is in accord with its well-documented functional polarity facilitating mediated nucleocytoplasmic exchange of molecules and particles.

Full Text

The Full Text of this article is available as a PDF (3.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abelson H. T., Smith G. H. Nuclear pores: the pore-annulus relationship in thin section. J Ultrastruct Res. 1970 Mar;30(5):558–588. doi: 10.1016/s0022-5320(70)90052-3. [DOI] [PubMed] [Google Scholar]
  2. Aebi U., Cohn J., Buhle L., Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature. 1986 Oct 9;323(6088):560–564. doi: 10.1038/323560a0. [DOI] [PubMed] [Google Scholar]
  3. Akey C. W., Goldfarb D. S. Protein import through the nuclear pore complex is a multistep process. J Cell Biol. 1989 Sep;109(3):971–982. doi: 10.1083/jcb.109.3.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Akey C. W. Interactions and structure of the nuclear pore complex revealed by cryo-electron microscopy. J Cell Biol. 1989 Sep;109(3):955–970. doi: 10.1083/jcb.109.3.955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blobel G. Gene gating: a hypothesis. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8527–8529. doi: 10.1073/pnas.82.24.8527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bonner W. M. Protein migration into nuclei. I. Frog oocyte nuclei in vivo accumulate microinjected histones, allow entry to small proteins, and exclude large proteins. J Cell Biol. 1975 Feb;64(2):421–430. doi: 10.1083/jcb.64.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bonner W. M. Protein migration into nuclei. II. Frog oocyte nuclei accumulate a class of microinjected oocyte nuclear proteins and exclude a class of microinjected oocyte cytoplasmic proteins. J Cell Biol. 1975 Feb;64(2):431–437. doi: 10.1083/jcb.64.2.431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buhle E. L., Jr, Aebi U., Smith P. R. Correlation of surface topography of metal-shadowed specimens with their negatively stained reconstructions. Ultramicroscopy. 1985;16(3-4):436–450. doi: 10.1016/0304-3991(85)90110-x. [DOI] [PubMed] [Google Scholar]
  9. Buhle E. L., Jr, Knox B. E., Serpersu E., Aebi U. The structure of the Ca2+ ATPase as revealed by electron microscopy and image processing of ordered arrays. J Ultrastruct Res. 1983 Nov;85(2):186–203. doi: 10.1016/s0022-5320(83)90106-5. [DOI] [PubMed] [Google Scholar]
  10. De Robertis E. M., Longthorne R. F., Gurdon J. B. Intracellular migration of nuclear proteins in Xenopus oocytes. Nature. 1978 Mar 16;272(5650):254–256. doi: 10.1038/272254a0. [DOI] [PubMed] [Google Scholar]
  11. Dingwall C., Laskey R. A. Protein import into the cell nucleus. Annu Rev Cell Biol. 1986;2:367–390. doi: 10.1146/annurev.cb.02.110186.002055. [DOI] [PubMed] [Google Scholar]
  12. Dingwall C., Sharnick S. V., Laskey R. A. A polypeptide domain that specifies migration of nucleoplasmin into the nucleus. Cell. 1982 Sep;30(2):449–458. doi: 10.1016/0092-8674(82)90242-2. [DOI] [PubMed] [Google Scholar]
  13. Dworetzky S. I., Feldherr C. M. Translocation of RNA-coated gold particles through the nuclear pores of oocytes. J Cell Biol. 1988 Mar;106(3):575–584. doi: 10.1083/jcb.106.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dwyer N., Blobel G. A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei. J Cell Biol. 1976 Sep;70(3):581–591. doi: 10.1083/jcb.70.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Engel A., Baumeister W., Saxton W. O. Mass mapping of a protein complex with the scanning transmission electron microscope. Proc Natl Acad Sci U S A. 1982 Jul;79(13):4050–4054. doi: 10.1073/pnas.79.13.4050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Engel A., Meyer J. Preparation of unstained protein structures for mass determination by electron scattering. J Ultrastruct Res. 1980 Aug;72(2):212–222. doi: 10.1016/s0022-5320(80)90059-3. [DOI] [PubMed] [Google Scholar]
  17. Engel A. Molecular weight determination by scanning transmission electron microscopy. Ultramicroscopy. 1978;3(3):273–281. doi: 10.1016/s0304-3991(78)80037-0. [DOI] [PubMed] [Google Scholar]
  18. Engel A., Reichelt R. Processing of quantitative scanning transmission electron micrographs. Scanning Microsc Suppl. 1988;2:285–293. [PubMed] [Google Scholar]
  19. Feldherr C. M., Kallenbach E., Schultz N. Movement of a karyophilic protein through the nuclear pores of oocytes. J Cell Biol. 1984 Dec;99(6):2216–2222. doi: 10.1083/jcb.99.6.2216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Feldherr C. M. The uptake of endogenous proteins by oocyte nuclei. Exp Cell Res. 1975 Jul;93(2):411–419. doi: 10.1016/0014-4827(75)90467-x. [DOI] [PubMed] [Google Scholar]
  21. Franke W. W., Scheer U., Krohne G., Jarasch E. D. The nuclear envelope and the architecture of the nuclear periphery. J Cell Biol. 1981 Dec;91(3 Pt 2):39s–50s. doi: 10.1083/jcb.91.3.39s. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Franke W. W., Scheer U. The ultrastructure of the nuclear envelope of amphibian oocytes: a reinvestigation. I. The mature oocyte. J Ultrastruct Res. 1970 Feb;30(3):288–316. doi: 10.1016/s0022-5320(70)80064-8. [DOI] [PubMed] [Google Scholar]
  23. Franke W. W. Structure, biochemistry, and functions of the nuclear envelope. Int Rev Cytol. 1974;Suppl 4:71–236. [PubMed] [Google Scholar]
  24. Gall J. G. Octagonal nuclear pores. J Cell Biol. 1967 Feb;32(2):391–399. doi: 10.1083/jcb.32.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gerace L., Burke B. Functional organization of the nuclear envelope. Annu Rev Cell Biol. 1988;4:335–374. doi: 10.1146/annurev.cb.04.110188.002003. [DOI] [PubMed] [Google Scholar]
  26. Harris J. R. Some electron microscopic studies on intact nuclear 'ghosts' and nuclear membrane fragments. Philos Trans R Soc Lond B Biol Sci. 1974 Jul 25;268(891):109–117. doi: 10.1098/rstb.1974.0019. [DOI] [PubMed] [Google Scholar]
  27. Harris J. R. The biochemistry and ultrastructure of the nuclear envelope. Biochim Biophys Acta. 1978 Apr 10;515(1):55–104. doi: 10.1016/0304-4157(78)90008-4. [DOI] [PubMed] [Google Scholar]
  28. Hoeijmakers J. H., Schel J. H., Wanka F. Structure of the nuclear pore complex in mammalian cells. Two annular components. Exp Cell Res. 1974 Jul;87(1):195–206. doi: 10.1016/0014-4827(74)90542-4. [DOI] [PubMed] [Google Scholar]
  29. Kartenbeck J., Zentgraf H., Scheer U., Franke W. W. The nuclear envelope in freeze-etching. Ergeb Anat Entwicklungsgesch. 1971;45(1):3–55. doi: 10.1007/978-3-662-10390-6. [DOI] [PubMed] [Google Scholar]
  30. Krohne G., Franke W. W., Scheer U. The major polypeptides of the nuclear pore complex. Exp Cell Res. 1978 Oct 1;116(1):85–102. doi: 10.1016/0014-4827(78)90067-8. [DOI] [PubMed] [Google Scholar]
  31. Leapman R. D., Ornberg R. L. Quantitative electron energy loss spectroscopy in biology. Ultramicroscopy. 1988;24(2-3):251–268. doi: 10.1016/0304-3991(88)90314-2. [DOI] [PubMed] [Google Scholar]
  32. Maul G. G. The nuclear and the cytoplasmic pore complex: structure, dynamics, distribution, and evolution. Int Rev Cytol Suppl. 1977;(6):75–186. [PubMed] [Google Scholar]
  33. Newport J. W., Forbes D. J. The nucleus: structure, function, and dynamics. Annu Rev Biochem. 1987;56:535–565. doi: 10.1146/annurev.bi.56.070187.002535. [DOI] [PubMed] [Google Scholar]
  34. Paine P. L., Moore L. C., Horowitz S. B. Nuclear envelope permeability. Nature. 1975 Mar 13;254(5496):109–114. doi: 10.1038/254109a0. [DOI] [PubMed] [Google Scholar]
  35. Unwin P. N., Milligan R. A. A large particle associated with the perimeter of the nuclear pore complex. J Cell Biol. 1982 Apr;93(1):63–75. doi: 10.1083/jcb.93.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Unwin P. N. Three-dimensional model of membrane-bound ribosomes obtained by electron microscopy. Nature. 1977 Sep 8;269(5624):118–122. doi: 10.1038/269118a0. [DOI] [PubMed] [Google Scholar]
  37. Wrigley N. G. The lattice spacing of crystalline catalase as an internal standard of length in electron microscopy. J Ultrastruct Res. 1968 Sep;24(5):454–464. doi: 10.1016/s0022-5320(68)80048-6. [DOI] [PubMed] [Google Scholar]
  38. Zimmer F. J., Dreyer C., Hausen P. The function of the nuclear envelope in nuclear protein accumulation. J Cell Biol. 1988 May;106(5):1435–1444. doi: 10.1083/jcb.106.5.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES