Advertisement

Cell Membranes pp 197-218 | Cite as

Regulation of Assembly of the Spectrin-Based Membrane Skeleton in Chicken Embryo Erythroid Cells

  • Randall T. Moon
  • Ingrid Blikstad
  • Elias Lazarides

Abstract

How newly synthesized proteins are routed to their proper locations and assembled into higher-order structures within the cell remains a challenge to cell biology. The magnitude of the problem is considerable, given that some newly synthesized proteins such as secreted immunoglobulins (Dulis, 1983) are destined for secretion from cells, others such as many glycoproteins (Fitting and Kabat, 1982; Polonoff et al., 1982) or hormone or neurotransmitter receptors (Jacobs et al., 1983; Merlie et al., 1982) become integrated into the plasma membrane, and the remaining proteins reside in intracellular vesicles, membranes, cytoskeletal structures, the nucleus, or the cytoplasm. As illustrated below, the selection of a protein’s destination can be made either cotranslationally or posttranslationally.

Keywords

Erythroid Cell Membrane Skeleton Nascent Chain Stabilization Hypothesis Cytoskeletal Fraction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agre, P., Gardner, K., and Bennett, V., 1983, Association between human erythrocyte calmodulin and the cytoplasmic surface of human erythrocyte membranes, J. Biol. Chem. 258: 6258–6265.PubMedGoogle Scholar
  2. Alper, S. L., Beam, K. G., and Greengard, P., 1980a, Hormonal control of Na+ K- cotransport in turkey erythrocytes. Multiple site phosphorylation of goblin, a high molecular weight protein of the plasma membrane, J. Biol. Chem. 255: 4864–4871.PubMedGoogle Scholar
  3. Alper, S. L., Palfrey, H. C., DeRiemer, S. A., and Greengard, P., 1980b, Hormonal control of protein phosphorylation in turkey erythrocytes. Phosphorylation by cAMP-dependent and Ca2 -dependent protein kinases of distinct sites in goblin, a high molecular weight protein of the plasma membrane, J. Biol. Chem. 255: 11029–11039.PubMedGoogle Scholar
  4. Anderson, J. M., 1979, Structural studies on human spectrin: Comparison of subunits and fragmentation of native spectrin, J. Biol. Chem. 254: 939–944.PubMedGoogle Scholar
  5. Anderson, R. A. and Lovrien, R. E., 1984, Glycophorin is linked by band 4.1 to the human erythrocyte membrane skeleton, Nature 307: 655–658.PubMedCrossRefGoogle Scholar
  6. Beam, K. G., Alper, S. L., Palade, G. E., and Greengard, P., 1979, Hormonally regulated phosphoprotein of turkey erythrocytes: Localization to plasma membrane, J. Cell Biol. 83: 1–15.PubMedCrossRefGoogle Scholar
  7. Bennett, V., 1982, The molecular basis for membrane-cytoskeleton association in human erythrocytes, J. Cell. Biochem. 18: 49–65.PubMedCrossRefGoogle Scholar
  8. Blikstad, I., and Lazarides, E., 1983a, Vimentin filaments are assembled from a soluble precursor in avian erythroid cells, J. Cell Biol. 96: 1803–1808.PubMedCrossRefGoogle Scholar
  9. Blikstad, I., and Lazarides, E., 1983b, Synthesis of spectrin in avian erythroid cells: Association of nascent polypeptide chains with the cytoskeleton, Proc. Natl. Acad. Sci. USA 80: 2637–2641.PubMedCrossRefGoogle Scholar
  10. Blikstad, I., Nelson, W. J., Moon, R. T., and Lazarides, E., 1983, Synthesis and assembly of spectrin during avian erythropoiesis: Stoichiometric assembly but unequal synthesis of a-and 13-spectrin, Cell 32: 1081–1091.PubMedCrossRefGoogle Scholar
  11. Braell, W. A., and Lodish, H. F., 1981, Biosynthesis of the erythrocyte anion transport protein, J. Biol. Chem. 256: 11337–11344.PubMedGoogle Scholar
  12. Braell, W. A., and Lodish, H. F., 1982, The erythroid anion transport protein is cotranslationally inserted into microsomes, Cell 28: 23–31.PubMedCrossRefGoogle Scholar
  13. Branton, D., Cohen, C. M., and Tyler, J., 1981, Interaction of cytoskeletal proteins on the human erythrocyte membrane, Cell 24: 24–32.PubMedCrossRefGoogle Scholar
  14. Burridge, K., Kelley, T., and Mangeat, P., 1982, Nonerythrocyte spectrins: Actin-membrane attachment proteins occurring in many cell types, J. Cell Biol. 95: 478–486.PubMedCrossRefGoogle Scholar
  15. Cervera, M., Dreyfuss, G., and Penman, S., 1981, Messenger RNA is translated when associated with the cytoskeletal framework in normal and VSV-infected HeLa cells, Cell 23: 113–120.PubMedCrossRefGoogle Scholar
  16. Chan, L.-N. L., Mahoney, K. A., Wacholtz, M., and Sha’afi, R. I., 1978, Asynchronous termination of plasma membrane protein synthesis in erythroid cells, Membrane Biochim. 2: 47–61.CrossRefGoogle Scholar
  17. Chang, H., Langer, P. J., and Lodish, H. F., 1976, Asynchronous synthesis of erythrocyte membrane proteins, Proc. Natl. Acad. Sci. USA 73: 3206–3210.PubMedCrossRefGoogle Scholar
  18. Cohen, C. M., 1983, The molecular organization of the red cell membrane skeleton, Semin. Hematol. 20: 141–158.PubMedGoogle Scholar
  19. DeRobertis, E. M., 1983, Nucleocytoplasmic segregation of proteins and RNAs, Cell 32: 1021–1025.CrossRefGoogle Scholar
  20. Dulis, B. H., 1983, Regulation of protein expression in differentiation by subunit assembly: Human membrane and secreted IgM, J. Biol. Chem. 258: 2181–2187.PubMedGoogle Scholar
  21. Fitting, T., and Kabat, D., 1982, Evidence for a glycoprotein “signal” involved in transport between subcellular organelles: Two membrane glycoproteins encoded by murine leukemia virus reach the cell surface at different rates, J. Biol. Chem. 257: 14011–14017.PubMedGoogle Scholar
  22. Fulton, A. B., and Wan, K. M., 1983, Many cytoskeletal proteins associate with the HeLa cytoskeleton during translation in vitro, Cell 32: 619–625.PubMedCrossRefGoogle Scholar
  23. Gard, D. L., and Lazarides, E., 1980, The synthesis and distribution of desmin and vimentin during myogenesis in vitro, Cell 19: 263–275.PubMedCrossRefGoogle Scholar
  24. Gasser, S. M., and Schatz, G., 1983, Import of proteins into mitochondria: In vitro studies on the biogenesis of the outer membrane, J. Biol. Chem. 258: 3427–3430.PubMedGoogle Scholar
  25. Glenney, J. R., Jr., Glenney, P., and Weber, K., 1982, F-actin-binding and cross-linking properties of porcine brain fodrin, a spectrin-related molecule, J. Biol. Chem. 257: 9781–9787.PubMedGoogle Scholar
  26. Goodman, S. R., and Shiffer, K., 1983, The spectrin membrane skeleton of normal and abnormal human erythrocytes: a review, Am. J. Physiol. 244: C121–C141.PubMedGoogle Scholar
  27. Goodman, S. R., Zagon, I. S., and Kulikowski, R. R., 1981, Identification of a spectrin-like protein in nonerythroid cells, Proc. Natl. Acad. Sci. USA 78: 7570–7574.PubMedCrossRefGoogle Scholar
  28. Granger, G. L., and Lazarides, E., 1979, Desmin and vimentin coexist at the periphery of the myofibril Z disc, Cell 18: 1053–1063.PubMedCrossRefGoogle Scholar
  29. Hargreaves, W. R., Giedd, K. N., Verkleij, A., and Branton, D., 1980, Reassociation of ankyrin with band 3 in erythrocyte membranes and in lipid vesicles, J. Biol. Chem. 255: 11965–11972.PubMedGoogle Scholar
  30. Hershko, A., 1983, Ubiquitin: Roles in protein modification and breakdown, Cell 34: 11–12.PubMedCrossRefGoogle Scholar
  31. Jackson, R. C., 1975, The exterior surface of the chicken erythrocyte, J. Biol. Chem. 250: 617–622.PubMedGoogle Scholar
  32. Jacobs, S., Frederick, F. C., Jr., and Cuatrecasas, P., 1983, Monensin blocks the maturation of receptors for insulin and somatomedin C: Identification of receptor precursors, Proc. Natl. Acad. Sci. USA 80: 1228–1231.PubMedCrossRefGoogle Scholar
  33. Jay, D. G., 1983, Characterization of the chicken erythrocyte anion exchange protein, J. Biol. Chem. 258: 9431–9436.PubMedGoogle Scholar
  34. Koch, P. A., Gardner, F. H., Gartrell, J. E., Jr., and Carter, J. R., Jr., 1975a, Biogenesis of erythrocyte membrane proteins: In vivo studies in anemic rabbits, Biochim. Biophys. Acta 389: 177–187.PubMedCrossRefGoogle Scholar
  35. Koch, P. A., Gartrell, J. E., Jr., Gardner, F. H., and Carter, J. R., Jr., 1975b, Biogenesis of erythrocyte membrane proteins: In vivo studies in anemic rabbits, Biochim. Biophys. Acta 389: 162–176.PubMedCrossRefGoogle Scholar
  36. Lazarides, E., and Nelson, W. J., 1983, Erythrocyte and brain forms of spectrin in cerebellum: Distinct membrane-cytoskeletal domains in neurons, Science 220: 1296–1297.CrossRefGoogle Scholar
  37. Lemieux, R., and Beaud, G., 1982, Expression of vaccinia virus early mRNA in Ehrlich ascites tumor cells, Eur. J. Biochem. 129: 273–279.PubMedCrossRefGoogle Scholar
  38. Lenk, R., Ransom, L., Kaufmann, Y., and Penman, S., 1977, A cytoskeletal structure with associated polyribosomes obtained from HeLa cells, Cell 10: 67–78.PubMedCrossRefGoogle Scholar
  39. Levine, J., and Willard, M., 1981, Fodrin: Axonally transported polypeptides associated with the internal periphery of many cells, J. Cell Biol. 90: 631–643.PubMedCrossRefGoogle Scholar
  40. Lodish, H. F., 1971, Alpha and beta globin messenger ribonucleic acid: Different amounts and rates of initiation of translation, J. Biol. Chem. 246: 7131–7138.PubMedGoogle Scholar
  41. Lodish, H. F., 1973, Biosynthesis of reticulocyte membrane proteins by membrane-free polyribosomes, Proc. Natl. Acad. Sci. USA 70: 1526–1530.PubMedCrossRefGoogle Scholar
  42. Lodish, H. F., and Small, B., 1975, Membrane proteins synthesized by rabbit reticulocytes, J. Cell Biol. 65: 51–64.PubMedCrossRefGoogle Scholar
  43. Lux, S. E., 1979, Spectrin—actin membrane skeleton of normal and abnormal red blood cells, Semin. Hematol. 16: 21–51.PubMedGoogle Scholar
  44. Marchesi, V. T., 1983, The red cell membrane skeleton: Recent progress, Blood 61:1–11. Mechler, B., 1981, Membrane-bound ribosomes of myeloma cells. VI. Initiation of immunoglobulin mRNA translation occurs on free ribosomes, J. Cell Biol. 88: 42–50.Google Scholar
  45. Merlie, J. P., Sebbane, R., Tzartos, S., and Lindstrom, J., 1982, Inhibition of glycosylation with tunicamycin blocks assembly of newly synthesized acetylcholine receptor subunits in muscle cells, J. Biol. Chem. 257: 2694–2701.PubMedGoogle Scholar
  46. Meyer, D. I., Krause, E., and Dobberstein, B., 1982, Secretory protein translocation across membranes—the role of the “docking protein,” Nature 297: 647–650.PubMedCrossRefGoogle Scholar
  47. Moon, R. T., and Lazarides, E., 1983a, Synthesis and post-translational assembly of intermediate filaments in avian erythroid cells: Vimentin assembly limits the rate of synemin assembly, Proc. Natl. Acad. Sci. USA 80: 5495–5499.PubMedCrossRefGoogle Scholar
  48. Moon, R. T., and Lazarides, E., 1983b, Canavanine inhibits vimentin assembly but not its synthesis in chicken embryo erythroid cells, J. Cell Biol. 97: 1309–1314.PubMedCrossRefGoogle Scholar
  49. Moon, R. T., and Lazarides, E., 1983c, {3-spectrin limits a-spectrin assembly on membranes following synthesis in a chicken erythroid cell lysate, Nature 305: 62–65.Google Scholar
  50. Moon, R. T., and Lazarides, E., 1984, Biogenesis of the avian erythroid membrane-skeleton: Receptor-mediated assembly and stabilization of ankyrin (globin) and spectrin, J. Cell Biol.,in press.Google Scholar
  51. Moon, R. T., Nicosia, R. F., Olsen, C., Hille, M. B., and Jeffery, W. R., 1983, The cytoskeletal framework of sea urchin eggs and embryos: Developmental changes in the association of messenger RNA, Develop. Biol. 95: 447–458.PubMedCrossRefGoogle Scholar
  52. Morrow, J. S., and Marchesi, V. T., 1981, Self assembly of spectrin oligomers in vitro: A basis for a dynamic cytoskeleton, J. Cell Biol. 88: 463–468.PubMedCrossRefGoogle Scholar
  53. Nelson, W. J., and Lazarides, E., 1983, Switching of subunit composition of muscle spectrin during myogenesis in vitro, Nature 304: 364–368.PubMedCrossRefGoogle Scholar
  54. Polonoff, E., Machida, C. A., and Kabat, D., 1982, Glycosylation and intracellular transport of membrane glycoproteins encoded by murine leukemia viruses: Inhibition by amino acid analogues and by tunicamycin, J. Biol. Chem. 257: 14023–14028.PubMedGoogle Scholar
  55. Repasky, E. A., Granger, B. L., and Lazarides, E., 1982, Widespread occurrence of avian spectrin in nonerythroid cells, Cell 29: 821–833.PubMedCrossRefGoogle Scholar
  56. Saborio, J. L., Pong, S. S., and Koch, D., 1974, Selective and reversible inhibition of initiation of protein synthesis in mammalian cells, J. Mol. Biol. 85: 195–211.PubMedCrossRefGoogle Scholar
  57. Schatz, G., and Butow, R. A., 1983, How are proteins imported into mitochondria? Cell 32: 316–318.PubMedCrossRefGoogle Scholar
  58. Tokuyasu, K. T., Schekman, R., and Singer, S. J., 1979, Domains of receptor mobility and endocytosis in the membranes of neonatal human erythrocytes and reticulocytes are deficient in spectrin, J. Cell Biol. 80: 481–486.PubMedCrossRefGoogle Scholar
  59. VanVenrooij, W. J., Sillekens, P. T. G., VanEekelen, C. A. G., and Reinders, R. J., 1981, On the association of RNA with the cytoskeleton in uninfected and adenovirus-infected human KB cells, Exp. Cell Res. 135: 79–91.CrossRefGoogle Scholar
  60. Walter, P., and Blobel, G., 1982, Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum, Nature 299: 691–698.PubMedCrossRefGoogle Scholar
  61. Weise, M. J., and Chan, L. L., 1978, Membrane protein synthesis in embryonic chick eyrthroid cells, J. Biol. Chem. 253: 1892–1897.PubMedGoogle Scholar
  62. Weise, M. J., and Ingram, V. M., 1976, Proteins and glycoproteins of membranes from developing chick red cells, J. Biol. Chem. 251: 6667–6673.PubMedGoogle Scholar
  63. Widmer, W., 1980, Assembly of proteins into membranes, Science 210: 861–868.CrossRefGoogle Scholar
  64. Woodruff, R. I., and Telfer, W. H., 1980, Electrophoresis of proteins in intracellular bridges, Nature 286: 84–86.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Randall T. Moon
    • 1
  • Ingrid Blikstad
    • 1
  • Elias Lazarides
    • 1
  1. 1.Division of BiologyCalifornia Institute of TechnologyPasadenaUSA

Personalised recommendations