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. 1986 Apr 1;102(4):1157–1163. doi: 10.1083/jcb.102.4.1157

Assembly of protein 4.1 during chicken erythroid differentiation

PMCID: PMC2114178  PMID: 3958041

Abstract

Protein 4.1 is a peripheral membrane protein that strengthens the actin- spectrin based membrane skeleton of the red blood cell and also serves to attach this structure to the plasma membrane. In avian erythrocytes it exists as a family of closely related polypeptides that are differentially expressed during erythropoiesis. We have analyzed the synthesis and assembly onto the membrane skeleton of protein 4.1 and in this paper we show that its assembly is extremely rapid and highly efficient since greater than 95% of the molecules synthesized are assembled in less than 1 min. The remaining minor fraction of unassembled protein 4.1 differs kinetically and is either degraded or assembled with slower kinetics. All protein 4.1 variants exhibit a similar kinetic behavior irrespective of the stage of erythroid differentiation. Thus, the amount and the variants ratio of protein 4.1 assembled are determined largely at the transcriptional or at the translational level and not posttranslationally. During erythroid terminal differentiation the molar amounts of protein 4.1 and spectrin assembled change. In postmitotic cells, as compared with proliferative cells, far more protein 4.1 than spectrin is assembled onto the membrane-skeleton. This modulation may permit the assembly of an initially flexible membrane skeleton in mitotic erythroid cells. As cells become postmitotic and undergo the final steps of maturation the membrane skeleton may be gradually stabilized by the assembly of protein 4.1.

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Selected References

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

  1. Anderson R. A., Lovrien R. E. Glycophorin is linked by band 4.1 protein to the human erythrocyte membrane skeleton. Nature. 1984 Feb 16;307(5952):655–658. doi: 10.1038/307655a0. [DOI] [PubMed] [Google Scholar]
  2. Bennett V. The membrane skeleton of human erythrocytes and its implications for more complex cells. Annu Rev Biochem. 1985;54:273–304. doi: 10.1146/annurev.bi.54.070185.001421. [DOI] [PubMed] [Google Scholar]
  3. Blanchet J. P. Chicken erythrocyte membranes: comparison of nuclear and plasma membranes from adults and embryos. Exp Cell Res. 1974 Mar 15;84(1):159–166. doi: 10.1016/0014-4827(74)90392-9. [DOI] [PubMed] [Google Scholar]
  4. Blikstad I., Lazarides E. Synthesis of spectrin in avian erythroid cells: association of nascent polypeptide chains with the cytoskeleton. Proc Natl Acad Sci U S A. 1983 May;80(9):2637–2641. doi: 10.1073/pnas.80.9.2637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blikstad I., Nelson W. J., Moon R. T., Lazarides E. Synthesis and assembly of spectrin during avian erythropoiesis: stoichiometric assembly but unequal synthesis of alpha and beta spectrin. Cell. 1983 Apr;32(4):1081–1091. doi: 10.1016/0092-8674(83)90292-1. [DOI] [PubMed] [Google Scholar]
  6. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  7. Branton D., Cohen C. M., Tyler J. Interaction of cytoskeletal proteins on the human erythrocyte membrane. Cell. 1981 Apr;24(1):24–32. doi: 10.1016/0092-8674(81)90497-9. [DOI] [PubMed] [Google Scholar]
  8. Bruns G. A., Ingram V. M. The erythroid cells and haemoglobins of the chick embryo. Philos Trans R Soc Lond B Biol Sci. 1973 Oct 25;266(877):225–305. doi: 10.1098/rstb.1973.0050. [DOI] [PubMed] [Google Scholar]
  9. Chan L. L. Changes in the composition of plasma membrane proteins during differentiation of embryonic chick erythroid cell. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1062–1066. doi: 10.1073/pnas.74.3.1062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cohen C. M., Foley S. F. The role of band 4.1 in the association of actin with erythrocyte membranes. Biochim Biophys Acta. 1982 Jun 28;688(3):691–701. doi: 10.1016/0005-2736(82)90281-4. [DOI] [PubMed] [Google Scholar]
  11. Cohen C. M., Korsgren C. Band 4.1 causes spectrin-actin gels to become thixiotropic. Biochem Biophys Res Commun. 1980 Dec 31;97(4):1429–1435. doi: 10.1016/s0006-291x(80)80025-8. [DOI] [PubMed] [Google Scholar]
  12. Fowler V., Taylor D. L. Spectrin plus band 4.1 cross-link actin. Regulation by micromolar calcium. J Cell Biol. 1980 May;85(2):361–376. doi: 10.1083/jcb.85.2.361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Granger B. L., Lazarides E. Appearance of new variants of membrane skeletal protein 4.1 during terminal differentiation of avian erythroid and lenticular cells. Nature. 1985 Jan 17;313(5999):238–241. doi: 10.1038/313238a0. [DOI] [PubMed] [Google Scholar]
  14. Granger B. L., Lazarides E. Membrane skeletal protein 4.1 of avian erythrocytes is composed of multiple variants that exhibit tissue-specific expression. Cell. 1984 Jun;37(2):595–607. doi: 10.1016/0092-8674(84)90390-8. [DOI] [PubMed] [Google Scholar]
  15. Granger B. L., Repasky E. A., Lazarides E. Synemin and vimentin are components of intermediate filaments in avian erythrocytes. J Cell Biol. 1982 Feb;92(2):299–312. doi: 10.1083/jcb.92.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jackson R. C. The exterior surface of the chicken erythrocyte. J Biol Chem. 1975 Jan 25;250(2):617–622. [PubMed] [Google Scholar]
  17. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  18. Lazarides E., Moon R. T. Assembly and topogenesis of the spectrin-based membrane skeleton in erythroid development. Cell. 1984 Jun;37(2):354–356. doi: 10.1016/0092-8674(84)90364-7. [DOI] [PubMed] [Google Scholar]
  19. Mahoney K. A., Hyer B. J., Chan L. N. Separation of primitive and definitive erythroid cells of the chick embryo. Dev Biol. 1977 Apr;56(2):412–416. doi: 10.1016/0012-1606(77)90280-9. [DOI] [PubMed] [Google Scholar]
  20. Moon R. T., Lazarides E. Biogenesis of the avian erythroid membrane skeleton: receptor-mediated assembly and stabilization of ankyrin (goblin) and spectrin. J Cell Biol. 1984 May;98(5):1899–1904. doi: 10.1083/jcb.98.5.1899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nelson W. J., Lazarides E. Expression of the beta subunit of spectrin in nonerythroid cells. Proc Natl Acad Sci U S A. 1983 Jan;80(2):363–367. doi: 10.1073/pnas.80.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nelson W. J., Lazarides E. Goblin (ankyrin) in striated muscle: identification of the potential membrane receptor for erythroid spectrin in muscle cells. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3292–3296. doi: 10.1073/pnas.81.11.3292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pasternack G. R., Anderson R. A., Leto T. L., Marchesi V. T. Interactions between protein 4.1 and band 3. An alternative binding site for an element of the membrane skeleton. J Biol Chem. 1985 Mar 25;260(6):3676–3683. [PubMed] [Google Scholar]
  24. Repasky E. A., Granger B. L., Lazarides E. Widespread occurrence of avian spectrin in nonerythroid cells. Cell. 1982 Jul;29(3):821–833. doi: 10.1016/0092-8674(82)90444-5. [DOI] [PubMed] [Google Scholar]
  25. Sato S. B., Ohnishi S. Interaction of a peripheral protein of the erythrocyte membrane, band 4.1, with phosphatidylserine-containing liposomes and erythrocyte inside-out vesicles. Eur J Biochem. 1983 Jan 17;130(1):19–25. doi: 10.1111/j.1432-1033.1983.tb07111.x. [DOI] [PubMed] [Google Scholar]
  26. Shiffer K. A., Goodman S. R. Protein 4.1: its association with the human erythrocyte membrane. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4404–4408. doi: 10.1073/pnas.81.14.4404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Staufenbiel M., Deppert W. Intermediate filament systems are collapsed onto the nuclear surface after isolation of nuclei from tissue culture cells. Exp Cell Res. 1982 Mar;138(1):207–214. doi: 10.1016/0014-4827(82)90107-0. [DOI] [PubMed] [Google Scholar]
  28. Ungewickell E., Bennett P. M., Calvert R., Ohanian V., Gratzer W. B. In vitro formation of a complex between cytoskeletal proteins of the human erythrocyte. Nature. 1979 Aug 30;280(5725):811–814. doi: 10.1038/280811a0. [DOI] [PubMed] [Google Scholar]
  29. Weise M. J., Ingram V. M. Proteins and glycoproteins of membranes from developing chick red cells. J Biol Chem. 1976 Nov 10;251(21):6667–6673. [PubMed] [Google Scholar]
  30. Woods C. M., Lazarides E. Degradation of unassembled alpha- and beta-spectrin by distinct intracellular pathways: regulation of spectrin topogenesis by beta-spectrin degradation. Cell. 1985 Apr;40(4):959–969. doi: 10.1016/0092-8674(85)90356-3. [DOI] [PubMed] [Google Scholar]

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