Skip to main content
Log in

The macronuclear envelope ofTetrahymena pyriformis GL in different physiological states

V. Nuclear pore complexes — A controlling system in protein biosynthesis?

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Summary

A simple formula is derived to calculate the nucleocytoplasmic RNA-Efflux per nuclear Pore complex per min (REP-rate) which is generally applicable both for “growing” and “stationary” eukaryotic cells. In actively growing cells this REP-rate is mainly dependent on the cytoplasmic RNA-pool, the number of RNA-transporting pores, and the growth constant of RNA. These parameters are determined in logarithmicTetrahymena pyriformis GL. In this organism, 45 molecules both of the larger ribosomal RNA (25s rRNA) and of the smaller (17s rRNA) are transported per pore per min from nucleus to cytoplasm. “Pulse-label” experiments with3H-uridine indicate that the 25s rRNA is obviously transferred more slowly to the cytoplasm than the 17s rRNA. We postulate a “gating hypothesis” on the regulation of the nucleocytoplasmic RNA-efflux by nuclear pore complexes. This gating hypothesis suggests that nucleopores are controlling points of secondary importance in the sequence of gene expression, and do not directly control the cytoplasmic protein synthesis in eukaryotic cells.

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

References

  1. Albanese, M.P. 1964. Passagio di nucleoli attraverso la membrana nucleare negli ovociti in accrescimento diPatella coerulea L.Experientia 20:550.

    PubMed  Google Scholar 

  2. Allen, E. R., Cave, M. D. 1968. Formation, transport and storage of ribonucleic acid containing structures in oocytes ofAcheta domesticus (Orthoptera).Z. Zellforsch. 92:477.

    PubMed  Google Scholar 

  3. Bal, A.K., Jubinville, F., Cousineau, G. H., Inoué, S. 1968. Origin and fate of annulate lamellae inArbacia punctuculata eggs.J. Ultrastruct. Res. 25:15.

    PubMed  Google Scholar 

  4. Beaulaton, J. 1968. Sur laction d'enzymes au niveau des pores nucléaires et d'autres structures de cellules secrétrice prothoraciques inclusés en épon.Z. Zellforsch. 89:453.

    PubMed  Google Scholar 

  5. Beermann, W. 1964. Control of differentiation at the chromosomal level.J. Exp. Zool. 157:49.

    PubMed  Google Scholar 

  6. Christenson, E. G. 1962. Different RNA fractions during cell growth and synchronous division in mass cultures ofTetrahymena pyriformis.Acta Physiol. Scand. 54:1.

    PubMed  Google Scholar 

  7. Christenson, E. G. 1969. Evidence of a synchronized RNA metabolism during cell growth and cell division in heat treated mass cultures ofTetrahymena pyriformis GL.Zschr. Biol. 116:143.

    Google Scholar 

  8. Clérot, J.C. 1968. Mise en évidence par cytochimie ultrastructurale de l'émission de protéines par le noyau d'auxocytes de batraciens.J. Microscopie 7:973.

    Google Scholar 

  9. Cole, M. B. 1969. Ultrastructural cytochemistry of granules associated with the nuclear pores of frog oocytes.J. Cell Biol. (abstract) 43:55.

    Google Scholar 

  10. Comes, P., Franke, W. W. 1970. Composition, structure and function of the Hela cell nuclear envelope.Z. Zelforsch. 107:240.

    Google Scholar 

  11. Darnell, J. E. 1968. Ribonucleic acids from animal cells.Bact. Rev. 32:262.

    PubMed  Google Scholar 

  12. DuPraw, E. J., Bahr, G. F. 1969. The dry mass of individual nuclear annuli.J. Cell Biol. 43:73.

    Google Scholar 

  13. Feldherr, C. M. 1962. The nuclear annuli as pathways for nucleocytoplasmic exchanges.J. Cell Biol. 14:65.

    PubMed  Google Scholar 

  14. Feldherr, C.M. 1965. The effect of the electron opaque pore material on exchange through the nuclear annuli.J. Cell Biol. 25:43.

    PubMed  Google Scholar 

  15. Franke, W. W. 1970. On the universality of nuclear pore complex structure.Z. Zellforsch. 105:405.

    PubMed  Google Scholar 

  16. Franke, W. W. 1970. Nuclear pore flow rate.Naturwissenschaften 57:44.

    Google Scholar 

  17. Franke, W. W., Falk, H. 1970. Appearence of nuclear pore complexes after Bernhard's staining procedure.Histochemie 24:266.

    Google Scholar 

  18. Franke, W. W., Kartenbeck, J., Deumling, B. 1971. Nuclear pore flow rate of ribonucleic acids in the mature rat hepatocyte.Experientia 27:372.

    PubMed  Google Scholar 

  19. Franke, W. W., Scheer, U. 1970. The ultrastructure of the nuclear envelope of amphibian oocytes: A reinvestigation. II. The immature oocyte and dynamic aspects.J. Ultrastruct. Res. 30:317.

    PubMed  Google Scholar 

  20. Gall, J. G. 1964. Electron microscopy of the nuclear envelope.In: Protoplasmatologia. V. F. Alfert, H. Bauer, and C. V. Harding, editors. p. 4. Springer-Verlag, Wien.

    Google Scholar 

  21. Georgiev, G. P. 1967. The nature and biosynthesis of nuclear ribonucleic acids.In: Progress in Nucleic Acid Research of Molecular Biology. J. N. Davidson and W. E. Cohn, editors. p. 259. Academic Press Inc., New York.

    Google Scholar 

  22. Georgiev, G. P. 1969. On the structural organization of operon and the regulation of RNA-synthesis in animal cells.J. Theoret. Biol. 25:473.

    Google Scholar 

  23. Georgiev, G. P. 1970. The hypothesis on the structural organization of operon and regulation of RNA synthesis in the animal cell.Molekularj. Biol. 4:17.

    Google Scholar 

  24. Girard, M., Penman, S., Darnell, J. E. 1964. The effect of actinomycin on ribosome formation in Hela cells.Proc. Nat. Acad. Sci. 51:205.

    PubMed  Google Scholar 

  25. Goldstein, L., Trescott, O. H. 1970. Characterization of RNA's that do and do not migrate between cytoplasm and nucleus.Proc. Nat. Acad. Sci. 67:1367.

    PubMed  Google Scholar 

  26. Gouranton, J. 1969. L'enveloppe nucléaire.Ann. Biol. 8, 7–8:385.

    Google Scholar 

  27. Gresson, R. A. R., Threadgold, L. T. 1962. Extrusion of nuclear material during oogenesis inBlatta orientalis. Quart..J. Micr. Sci. 103:141.

    Google Scholar 

  28. Harris, H. 1963. Rapidly labelled ribonucleic-acid in the cell nucleus.Nature 198:184.

    PubMed  Google Scholar 

  29. Harris, H. 1964. Breakdown of nuclear ribonucleic acid in the presence of actinomycin D.Nature 202:1301.

    PubMed  Google Scholar 

  30. Ischikawa, K., Kuroda, C., Ogata, K. 1970. Messenger ribonucleoprotein complexes released from rat liver nuclei by ATP. II. Chemical and metabolic properties of the protein moiety of messenger ribonucleoprotein complexes.Biochim. Biophys. Acta 213:505.

    PubMed  Google Scholar 

  31. Ischikawa, K., Kuroda, C., Ueki, M., Ogata, K. 1970. Messenger ribonucleoprotein complexes released from rat liver nuclei by ATP. I. Characterization of the RNA moiety of messenger ribonucleoprotein complexes.Biochim. Biophys. Acta 213:495.

    PubMed  Google Scholar 

  32. Ischikawa, K., Ueki, M., Nagai, K., Ogata, K. 1970. Incorporation of nuclear rapidly labeled RNA into polysomes in the reconstructed system of rat liver.Biochim. Biophys. Acta 213:542.

    PubMed  Google Scholar 

  33. Ito, S., Loewenstein, W. R. 1965. Permeability of a nuclear membrane: changes during normal development and changes induced by growth hormone.Science 150:909.

    PubMed  Google Scholar 

  34. Klein, R. L., Afzelius, B. A. 1966. Nuclear membrane hydrolysis of adenosine triphosphate.Nature 212:609.

    Google Scholar 

  35. Kumar, A. 1967. Patterns of ribosomal RNA synthesis inTetrahymena.J. Cell Biol. 35:74a.

    Google Scholar 

  36. Kumar, A. 1968. Kinetics of RNA synthesis inTetrahymena: Appearence of polysome-associated RNA and ribosomal subunits in the cytoplasm.J. Cell Biol. 39:76a.

    Google Scholar 

  37. Kumar, A. 1969. Studies on ribosomal RNA fromTetrahymena by zone velocity sedimentation in sucrose gradients and base ratio analysis.Biochim. Biophys. Acta 186:326.

    PubMed  Google Scholar 

  38. Kumar, A. 1970. Ribosome synthesis inTetrahymena.J. Cell Biol. 45:623.

    PubMed  Google Scholar 

  39. Lane, N. J. 1967. Spheroidal and ring nucleoli in amphibian oocytes. Patterns of uridine incorporation and fine structural features.J. Cell Biol. 35:421.

    PubMed  Google Scholar 

  40. Leick, V. 1969. Effect of actinomycin D and DL-p-fluorophenylalanine on ribosome formation inTetrahymena pyriformis.Europ. J. Biochem. 8:215.

    PubMed  Google Scholar 

  41. Leick, V. 1969. Formation of subribosomal particles in the macronuclei ofTetrahymena pyriformis.Europ. J. Biochem. 8:221.

    PubMed  Google Scholar 

  42. Leick, V., Andersen, S. B. 1970. Pools and turnover rates of nuclear ribosomal RNA inTetrahymena pyriformis.Europ. J. Biochem. 14:460.

    PubMed  Google Scholar 

  43. Leick, V., Engberg, J., Emmersen, J. 1970. Nascent subribosomal particles inTetrahymena pyriformis.Europ. J. Biochem. 13:238.

    PubMed  Google Scholar 

  44. Leick, V., Plesner, P. 1968. Formation of ribosomes inTetrahymena pyriformis.Biochim. Biophys. Acta 169:398.

    PubMed  Google Scholar 

  45. Leick, V., Plesner, P. 1968. Precursors of ribosomal subunits inTetrahymena pyriformis.Biochim. Biophys. Acta 169:409.

    PubMed  Google Scholar 

  46. Levy, H. B. 1963. Effect of actinomycin D on Hela cell nuclear RNA metabolism.Proc. Soc. Exp. Biol., N.Y. 113:886.

    Google Scholar 

  47. Loening, U. E. 1970. The mechanism of synthesis of ribosomal RNA.In: Organization and Control in Prokaryotic and Eukaryotic Cells. H. P. Charles and B. C. Knight, editors. p. 77. University Press, Cambridge.

    Google Scholar 

  48. Loewenstein, W. R. 1964. Permeability of the nuclear membrane as determined with electrical methods.In: Protoplasmatologia. V. F. Alfert, H. Bauer, and C. V. Harding, editors. p. 26. Springer-Verlag, Wien.

    Google Scholar 

  49. Loewenstein, W. R., Kanno, Y., Ito, S. 1966. Permeability of nuclear membranes.In: Biological Membranes: Recent Progress. E. M. Weyer, editor. p. 708.Ann. N.Y. Acad. Sci. 137:2.

  50. Maden, B. E. H. 1968. Ribosome formation in animal cells.Nature 219:685.

    Google Scholar 

  51. Maillet, P. L., Gouranton, J. 1965. Sur l'expulsion de l'acide ribonucléique nucléaire par les spermatids dePhilaenus spumarius L. (Homoptera, Cercopidae).Compt. Rend. Acad. Sci., Paris 261:1417.

    Google Scholar 

  52. Mentré, P. 1966. Etude des pores nucléaires sur des noyaux et des membranes nucléaires isolés.6th Int. Congr. Electr. Micr., Kyoto. R. Uyeda, editor. p. 2. Maruzen Ltd., Tokyo.

    Google Scholar 

  53. Mentré, P. 1969. Présence d'acide ribonucléique dans l'anneau osmiophile et le granule central des pores nucléaires.J. Microscopie 8:51.

    Google Scholar 

  54. Mepham, R. H., Lane, G. R. 1969. Nucleopores and polyribosome formation.Nature 221:288.

    Google Scholar 

  55. Merriam, R. W. 1962. Some dynamic aspects of the nuclear envelope.J. Cell Biol. 12:79.

    PubMed  Google Scholar 

  56. Mirsky, A. G. 1964. The nuclear membrane and nucleocytoplasmic interchange.In: Protoplasmatologia. V. F. Alfert, H. Bauer, and C. V. Harding, editors, p. 1. Springer-Verlag, Wien.

    Google Scholar 

  57. Mita, T. 1965. Effects of actinomycin D on the RNA-synthesis and the synchronous cell division ofTetrahymena pyriformis GL.Biochim. Biophys. Acta 103:182.

    PubMed  Google Scholar 

  58. Monneron, A., Bernhard, W. 1969. Fine structural organization of the interphase nucleus in some mammalian cells.J. Ultrastruct. Res. 27:266.

    PubMed  Google Scholar 

  59. Nórrevang, A. 1968. Electron microscopic morphology of oogenesis.Int. Rev. Cytol. 23:113.

    PubMed  Google Scholar 

  60. Perry, R. P. 1967. The nucleolus and the synthesis of ribosomes.Progr. Nucl. Acid Res. Mol. Biol. 6:219.

    Google Scholar 

  61. Pollister, A. W., Gettner, M., Ward, R. 1954. Nucleocytoplasmic interchange in oocytes.Science 120:789.

    Google Scholar 

  62. Scheer, U. 1970. Strukturen und Funktionen der Porenkomplexe in der Amphibieneizelle. Ph. D. Thesis, University Freiburg i. Br., West Germany.

    Google Scholar 

  63. Scherrer, K., Latham, H., Darnell, J. E. 1963. Demonstration of an unstable RNA and of precursor to ribosomal RNA in Hela cells.Proc. Nat. Acad. Sci. 49:240.

    PubMed  Google Scholar 

  64. Schjeide, O. A., Candless, M. C., Munn, R. 1965. Nuclear-cytoplasmic interactions.Nature 205:156.

    PubMed  Google Scholar 

  65. Sitte, P. 1971. Cellular morphology.In: Microbeam Irradiation and Cellular Morphology. E. Sidebottom and J. Hatfield editors. Plenum Publishing Co. Ltd., London. (In press)

    Google Scholar 

  66. Soeiro, R., Birnboim, H. C., Darnell, J. E. 1966. Rapidly labeled Hela cell nucleal RNA. II. Base composition and cellular localization of a heterogenous RNA fraction.J. Mol. Biol. 19:362.

    PubMed  Google Scholar 

  67. Speth, V., Wunderlich, F. 1970. The macronuclear envelope ofTetrahymena pyriformis GL in different physiological states. III. Appearence of freeze-etched nuclear pore complexes.J. Cell Biol. 47:772.

    PubMed  Google Scholar 

  68. Spirin, A. S., cited by McConkey, E. H. 1967. The fractionation of RNA's by sucrose gradient centrifugation.In: Methods in Enzymology, XII. A. L. Grossmann and K. Moldave, editors. p. 620. Academic Press Inc., New York.

    Google Scholar 

  69. Stevens, A. R. 1967. Machinery for exchange across the nuclear envelope.In: The Control of Nuclear Activity. L. Goldstein, editor. p. 189. Prentice-Hall International, London.

    Google Scholar 

  70. Stevens, B. J., André, J. 1969. The nuclear envelope.In: Handbook of Molecular Cytology. A. Lima-de-Faria, editor. p. 837. North Holland Publishing Co., Amsterdam-London.

    Google Scholar 

  71. Stevens, B., Swift, H. 1966. RNA transport from nucleus to cytoplasm inChironomus salivary glands.J. Cell Biol. 31:55.

    PubMed  Google Scholar 

  72. Takamoto, T. 1966. Ultrastructural transport mechanism of messenger ribonucleic acid in the young oocytes of amphibians.Nature 211:772.

    PubMed  Google Scholar 

  73. Tamaoki, T., Mueller, G. C. 1965. The effects of actinomycin D and puromycin on the formation of ribosomes in Hela cells.Biochim. Biophys. Acta 108:73.

    PubMed  Google Scholar 

  74. Ulrich, E. 1969. Etude des ultrastructures au cours de l'ovogenèse d'un poisson télésteen, le danio,Brachydanio rerio (Hamilton-Buchanan).J. Microscopie 8:447.

    Google Scholar 

  75. Verhey, C. A., Moyer, F. H. 1967. Fine structural changes during sea urchin oogenesis.J. Exp. Zool. 164:195.

    Google Scholar 

  76. Warner, J. R., Soeiro, R., Birnboim, H. C., Girard, M., Darnell, J. E. 1966. Ra labeled Hela cell nuclear RNA. I. Identification by zone sedimentation of a heterogenous fraction separate from ribosomal precursor RNA.J. Mol. Biol. 19:349.

    PubMed  Google Scholar 

  77. Wiener, J., Spiro, D., Loewenstein, W. R. 1965. Ultrastructure and permeability of nuclear membranes.J. Cell Biol. 27:107.

    PubMed  Google Scholar 

  78. Wunderlich, F. 1969. The macronuclear envelope ofTetrahymena pyriformis GL in different physiological states. I. Quantitative structural data.Exp. Cell Res. 56:369.

    PubMed  Google Scholar 

  79. Wunderlich, F. 1969. The macronuclear envelope ofTetrahymena pyriformis GL in different physiological states. II. Frequency of central granules in the pores.Z. Zellforsch. 101:581.

    PubMed  Google Scholar 

  80. Wunderlich, F. 1971. Zur Dynamik der Kernhülle. Struktur und Funktion der Kernhülle vonTetrahymena pyriformis GL in verschiedenen physiologischen Zuständen. Ph. D. Thesis, University Freiburg i. Br., West Germany.

    Google Scholar 

  81. Wunderlich, F., Franke, W. W. 1968. Structure of macronuclear envelopes ofTetrahymena pyriformis growing in the stationary phase.J. Cell Biol. 38:458.

    PubMed  Google Scholar 

  82. Wunderlich, F., Speth, V. 1971. The macronuclear envelope ofTetrahymena pyriformis GL in different physiological states. IV. Structural and functional aspects of nuclear pore complexes.J. Microscopie, in press, 1972.

  83. Yasuzumi, G., Kaye, G. I., Pappas, G. D., Yamamoto, H., Tsubo, I. 1961. Nuclear and cytoplasmic differentiation in developing sperm ofCambaroides japonicus.Z. Zellforsch. 53:141.

    PubMed  Google Scholar 

  84. Yasuzumi, G., Nakai, Y., Tsubo, J., Yasuda, M., Sugioka, T. 1967. The fine structure of nuclei as revealed by electron microscopy. IV. The intranuclear inclusion formation in Leydig cells of aging human testes.Exp. Cell Res. 45:261.

    PubMed  Google Scholar 

  85. Yasuzumi, G., Nakano, S., Matsuzak, W. 1962. Elektronenmikroskopische Untersuchungen über die Spermatogenese. IX. Über die Spermogenese der atypischen Spermatiden vonMelania libertina Gould.Z. Zellforsch. 57:495.

    PubMed  Google Scholar 

  86. Yasuzumi, G., Tsubo, J. 1966. The fine structure of nuclei as revealed by electron microscopy. III. Adenosine triphosphatase activity in the pores of nuclear envelope of mouse choroid plexus epithelial cells.Exp. Cell Res. 43:281.

    PubMed  Google Scholar 

  87. Zotikov, L., Barbarouk, L. 1970. Etude ultrastructurale des ribonucléoproteines nucléaires dans des cellules de la moelle osseuse du rat.7th Int. Congr. Microsc. Electr., Grenoble. (P. Favard, editor. p. 235.)Soc. Franc. Micr. Electr., Paris.

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wunderlich, F. The macronuclear envelope ofTetrahymena pyriformis GL in different physiological states. J. Membrain Biol. 7, 220–230 (1972). https://doi.org/10.1007/BF01867916

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01867916

Keywords

Navigation