Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1983 Apr 1;96(4):1047–1055. doi: 10.1083/jcb.96.4.1047

Quantitative analysis of modulations in numerical and lateral distribution of intramembrane particles during the cell cycle of neuroblastoma cells

PMCID: PMC2112319  PMID: 6833390

Abstract

Modulations in the internal structure of the plasma membrane during the cell cycle of mouse C1300 neuroblastoma cells (clone Neuro-2A) have been studied by freeze-fracture electron microscopy. Both the numerical and lateral distributions of the intramembrane particles (IMP) of the P face of the medium-exposed plasma membrane were determined as a function of the IMP diameter. The lateral IMP-distribution was quantified by a differential density distribution analysis, that could distinguish between random, aggregated, and dispersed distributions of IMP-subpopulations at various levels of spatial organization. Nonrandom lateral IMP-distribution was considered to indicate significant directional constraints on the lateral mobility of the represented molecules. The analysis demonstrated that the density, the size distribution, and the lateral distribution of the IMP are modulated during the cell cycle, such that characteristic structural and dynamic membrane properties can be attributed to the various cell cycle phases (M, G1, S, and G2). The results are interpreted in terms of asynchronous assembly of different membrane components and dynamic reorganizations within the plasma membrane during the cell cycle. Furthermore, they provide a structural manifestation of earlier observed changes in the dynamic properties of membrane proteins and lipids, and functional membrane transport properties in these neuroblastoma cells.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Bluemink J. G., Tertoolen L. G., Ververgaert P. H., Verkleij A. J. Freeze-fracture electron microscopy of preexisting and nascent cell membrane in cleaving eggs of Xenopus laevis. Biochim Biophys Acta. 1976 Aug 4;443(1):143–155. doi: 10.1016/0005-2736(76)90498-3. [DOI] [PubMed] [Google Scholar]
  2. Boonstra J., Mummery C. L., Tertoolen L. G., Van Der Saag P. T., De Laat S. W. Cation transport and growth regulation in neuroblastoma cells. Modulations of K+ transport and electrical membrane properties during the cell cycle. J Cell Physiol. 1981 Apr;107(1):75–83. doi: 10.1002/jcp.1041070110. [DOI] [PubMed] [Google Scholar]
  3. Borochov H., Shinitzky M. Vertical displacement of membrane proteins mediated by changes in microviscosity. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4526–4530. doi: 10.1073/pnas.73.12.4526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Edelman G. M. Surface modulation in cell recognition and cell growth. Science. 1976 Apr 16;192(4236):218–226. doi: 10.1126/science.769162. [DOI] [PubMed] [Google Scholar]
  5. Garrido J. Ultrastructural labeling of cell surface lectin receptors during the cell cycle. Exp Cell Res. 1975 Aug;94(1):159–175. doi: 10.1016/0014-4827(75)90543-1. [DOI] [PubMed] [Google Scholar]
  6. Ito K., Sato T., Yura T. Synthesis and assembly of the membrane proteins in E. coli. Cell. 1977 Jul;11(3):551–559. doi: 10.1016/0092-8674(77)90073-3. [DOI] [PubMed] [Google Scholar]
  7. Knutton S. Structural changes in the plasma membrane of synchronized P815Y mastocytoma cells. Exp Cell Res. 1976 Oct 1;102(1):109–116. doi: 10.1016/0014-4827(76)90305-0. [DOI] [PubMed] [Google Scholar]
  8. Mummery C. L., Boonstra J., Van Der Saag P. T., de Laat S. W. Modulation of functional and optimal (Na+-K+)ATPase activity during the cell cycle of neuroblastoma cells. J Cell Physiol. 1981 Apr;107(1):1–9. doi: 10.1002/jcp.1041070102. [DOI] [PubMed] [Google Scholar]
  9. Mummery C. L., Boonstra J., van der Saag P. T., de Laat S. W. Modulations of Na+ transport during the cell cycle of neuroblastoma cells. J Cell Physiol. 1982 Jul;112(1):27–34. doi: 10.1002/jcp.1041120106. [DOI] [PubMed] [Google Scholar]
  10. Nicolson G. L. Trans-membrane control of the receptors on normal and tumor cells. II. Surface changes associated with transformation and malignancy. Biochim Biophys Acta. 1976 Apr 30;458(1):1–72. doi: 10.1016/0304-419x(76)90014-7. [DOI] [PubMed] [Google Scholar]
  11. Nicolson G. L. Transmembrane control of the receptors on normal and tumor cells. I. Cytoplasmic influence over surface components. Biochim Biophys Acta. 1976 Apr 13;457(1):57–108. doi: 10.1016/0304-4157(76)90014-9. [DOI] [PubMed] [Google Scholar]
  12. Scott R. E., Carter R. L., Kidwell W. R. Structural changes in memebranes of synchronized cells demonstrated by freeze-cleavage. Nature. 1971 Oct 13;233(5320):219–220. [PubMed] [Google Scholar]
  13. Singer S. J., Nicolson G. L. The fluid mosaic model of the structure of cell membranes. Science. 1972 Feb 18;175(4023):720–731. doi: 10.1126/science.175.4023.720. [DOI] [PubMed] [Google Scholar]
  14. Torpier G., Montagnier L., Biquard J. M., Vigier P. A structural change of the plasma membrane induced by oncogenic viruses: quantitative studies with the freeze-fracture technique. Proc Natl Acad Sci U S A. 1975 May;72(5):1695–1698. doi: 10.1073/pnas.72.5.1695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. de Laat S. W., Tertoolen L. G., Bluemink J. G. Quantitative analysis of the numerical and lateral distribution of intramembrane particles in freeze-fractured biological membranes. Eur J Cell Biol. 1981 Feb;23(2):273–279. [PubMed] [Google Scholar]
  16. de Laat S. W., van der Saag P. T., Elson E. L., Schlessinger J. Lateral diffusion of membrane lipids and proteins during the cell cycle of neuroblastoma cells. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1526–1528. doi: 10.1073/pnas.77.3.1526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. de Laat S. W., van der Saag P. T., Shinitzky M. Microviscosity modulation during the cell cycle of neuroblastoma cells. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4458–4461. doi: 10.1073/pnas.74.10.4458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. de Laat S. W., van der Saag P. T. The plasma membrane as a regulatory site in growth and differentiation of neuroblastoma cells. Int Rev Cytol. 1982;74:1–54. doi: 10.1016/s0074-7696(08)61168-7. [DOI] [PubMed] [Google Scholar]
  19. van Zoelen E. J., van der Saag P. T., de Laat S. W. Family tree analysis of a transformed cell line and the transition probability model for the cell cycle. Exp Cell Res. 1981 Feb;131(2):395–406. doi: 10.1016/0014-4827(81)90243-3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES