Protoplasma

, Volume 113, Issue 1, pp 23–32

The cytomorphic system of anucleate non-mammalian erythrocytes

  • W. D. Cohen
Article

Summary

Cytomorphic structure was studied in erythrocytes ofBatrachoseps salamanders, a genus unique among non-mammalian vertebrates because most of the erythrocytes are anucleate. These anucleate erythrocytes are highly flattened, quite variable in size, and generally elliptical. All of them were found to contain marginal bands of microtubules (MBs), as observed in phase contrast and darkfield after Triton lysis. The MBs of larger cells typically twisted into figure-8 forms upon lysis. Whole mounts of the lysed anucleate cells consisted only of the MB plus a trans-MB network of material (TBM), as observed by electron microscopy. If lysis was carried out in the presence of 0.5 M KCl, all of the MBs circularized immediately and none were twisted. The network (TBM) was now missing, suggesting that it is needed for maintenance of MB ellipticity and plays a role in MB twisting. Small numbers of living anucleate erythrocytes were constricted in their mid-region, and others were pointed at one end. Correspondingly pointed MBs were observed after lysis, exhibiting a range of forms compatible with the mechanism proposed byEmmel (1924) in which the anucleate erythrocytes arise by amitotic division of nucleated ones.

The results show that these erythrocytes retain the typical nonmammalian cytomorphic system, and are thus unlike those of adult mammals. The network component (TBM) is present even though nuclei are absent, making it unlikely that it functions simply to position the nucleus. The observations are consistent with the hypothesis that the flattened, elliptical shape of non-mammalian vertebrate erythrocytes is generated by TBM tension applied across the faces of the MB “frame”, and that excessive tension induced by lysis (without KCl) produces MB twisting.

Keywords

Anucleate cells Cellular morphogenesis Erythrocyte, non-mammalian Marginal band Microtubules Batrachoseps 

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References

  1. Andrew, W., 1965: Comparative Hematology. New York, N.Y. Grune and Stratton.Google Scholar
  2. Barclay, N. E., 1966: Marginal bands in duck and camel erythrocytes. Anat. Rec.154, 313.Google Scholar
  3. Bertolini, B., Monaco, G., 1976: The microtubule marginal band of the newt erythrocyte. Observations on the isolated band. J. Ultrastruct. Res.54, 57–67.Google Scholar
  4. Blanchet, J. P., 1974: Chicken erythrocyte membranes: comparison of nuclear and plasma membranes from adults and embryos. Exp. Cell Res.84, 159–166.PubMedGoogle Scholar
  5. Cavanaugh, G. M., Ed., 1975: Formulae and Methods VI of the Marine Biological Laboratory Chemical Room. Woods Hole, Mass.: The Marine Biological Laboratory.Google Scholar
  6. Chan, L. L., 1977: Changes in the composition of plasma membrane proteins during differentiation of embryonic chick erythroid cell. P. N. A. S. USA74, 1062–1066.Google Scholar
  7. Cohen, W. D., 1978 a: Observations on the marginal band system of nucleated erythrocytes. J. Cell Biol.78, 260–273.PubMedGoogle Scholar
  8. —, 1978 b: Lability of the marginal band systemin vitro. J. Cell Biol.79, 309 a.Google Scholar
  9. —,Bartelt, D. C., Jaeger, R., Langford, G., Nemhauser, I., 1982: The cytoskeletal system of nucleated erythrocytes. I. Composition and function of major elements. J. Cell Biol.93, 828–838.PubMedGoogle Scholar
  10. —,Nemhauser, I., Jaeger, R. F., 1977: Rapid visualization of the marginal band system in blood cells of marine species. Biol. Bull.153, 420.Google Scholar
  11. — —,Cohen, M. F., 1978: Marginal bands ofHomarus americanus coelomocytes: disappearance associated with changes in cell morphology. Biol. Bull.155, 431–432.Google Scholar
  12. —,Terwilliger, N. B., 1979: Marginal bands in camel erythrocytes. J. Cell Sci.36, 97–107.PubMedGoogle Scholar
  13. Emmel, V. E., 1921: Hematological and respiratory conditions in the larval stages of the lungless amphibians. Anat. Rec.21, 56.Google Scholar
  14. —, 1924: Studies on the non-nucleated elements of the blood. Am. J. Anat.33, 347–391.Google Scholar
  15. Fairbanks, G., Steck, T. L., Wallach, D. F. H., 1971: Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry10(13), 2606–2617.PubMedGoogle Scholar
  16. Fischer, T. M., 1978: A comparison of the flow behavior of disc shaped versus elliptic red blood cells. Blood cells4, 453–461.Google Scholar
  17. Goniakowska-Witalinska, L., Witalinski, W., 1977: Occurrence of microtubules during erythropoiesis inLlama glama. J. Zool. (Lond.)181, 309–313.Google Scholar
  18. Hansen, V. K., Wingstrand, K. G., 1960: Further studies on the non-nucleated erythrocytes ofMaurolicus mulleri, and comparisons with the red blood cells of related fishes. Dana Rep. No.54, 1–15.Google Scholar
  19. Jackson, R. C., 1975: The exterior surface of the chicken erythrocyte. J. biol. Chem.250, 617–622.PubMedGoogle Scholar
  20. Kirkpatrick, F. H., 1976: Spectrin: current understanding of its physical, biochemical, and functional properties. Life Sci.19, 1–18.PubMedGoogle Scholar
  21. Lacelle, P. L., Evans, E. A., Hochmuth, R. M., 1977: Erythrocyte membrane elasticity, fragmentation, and lysis. Blood Cells3, 335–350.Google Scholar
  22. Lux, S. E., John, K. M., Karnovski, M. J., 1976: Irreversible deformation of the spectrin-actin lattice in irreversibly sickled cells. J. Clin. Invest.51, 1790–1797.Google Scholar
  23. Ralston, G. B., 1975: Proteins of the camel erythrocyte membrane. Biochim. biophys. Acta401, 83–94.PubMedGoogle Scholar
  24. Rebhun, L. I., Rosenbaum, J., Lefebre, P., Smith, G., 1974: Reversible restoration of the birefringence of cold-treated isolated mitotic apparatus of surf clam eggs with chick brain tubulin. Nature (Lond.)249, 113–115.Google Scholar
  25. Schmid-Schönbein, H., 1975: Erythrocyte rheology and the optimization of mass transport in the microcirculation. Blood cells1, 285–301.Google Scholar
  26. Stebbins, R. C., 1966: A Field Guide to Western Reptiles and Amphibians. Boston: Houghton Mifflin Co.Google Scholar
  27. Steck, T. L., 1974: The organization of proteins in the human red blood cell membrane. J. Cell Biol.62, 1–19.PubMedGoogle Scholar
  28. Tilney, L. G., Detmers, P., 1975: Actin in erythrocyte ghosts and its association with spectrin. J. Cell Biol.66. 508–520.PubMedGoogle Scholar
  29. Van Deurs, B., Behnke, O., 1965: The microtubule marginal band of mammalian red blood cells. Z. Anat. Entwickl.-Gesch.143, 43–47.Google Scholar
  30. Weisenberg, R. C., 1972: Microtubule formationin vitro in solutions containing low calcium concentrations. Science (Wash., D.C.)177, 1104–1105.Google Scholar
  31. Wingstrand, K. G., 1956: Non-nucleated erythrocytes in a teleostean fishMaurolicus mulleri. Z. Zellforsch.45, 195–200.PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1982

Authors and Affiliations

  • W. D. Cohen
    • 1
  1. 1.Department of Biological SciencesHunter CollegeNew YorkUSA

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