The Journal of Membrane Biology

, Volume 64, Issue 1–2, pp 11–21 | Cite as

Membrane transport during erythroid differentiation

  • Portia B. Gordon
  • Meryl S. Rubin
Articles

Summary

Transport, unidirectional flux, of a monosaccharide, a nucleoside and three amino acids, all of which enter cells by independent, discrete carriers, was compared at three stages of erythroid maturation, the normal (anucleate) mouse erythrocyte, and in differentiated and undifferentiated Friend erythroleukemia cells. We found specific transport alterations during this developmental program. Transport of 3-O-methylglucose increased with each successive developmental stage. Aminoisobutyrate transport was maintained during Friend cell differentiation, but fell slightly in erythrocytes. Leucine, lysine and uridine transport began to fall two days after dimethylsulfoxide exposure, and diminished further in red cells. These studies of transport are not directly comparable to uptake studies reported by others.

Median cell volume and thus surface area decreased more during differentiation than amino acid transport declined, so flux, transport past a unit area of membrane, actually increased. Monosaccharide flux also increased. Only uridine transport fell in parallel to surface area. Perhaps sites for nutrient transport required for energy production are preferentially maintained.

Key words

Friend cells membrane transport erythroid differentiation 

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References

  1. 1.
    Arndt-Jovin, D.J., Ostertag, W., Eisen, H., Klimek, F., Jovin, T.M. 1976. Studies of cellular differentiation by automatic cell separation. Two model systems: Friend virus-transformed cells and Hydra attenuata.J. Histochem. Cytochem. 24:332–347PubMedGoogle Scholar
  2. 2.
    Berlin, R.D. 1973. Temperature dependence of nucleoside membrane transport in rabbit alveolar macrophages and polymorphonuclear leukocytes.J. Biol. Chem. 248:4724–4730PubMedGoogle Scholar
  3. 3.
    Berlin, R.D., Oliver, J.M. 1975. Membrane transport of purine and pyrimidine bases and nucleosides in animal cells.Int. Rev. Cytol. 42:287–336PubMedGoogle Scholar
  4. 4.
    Brown, J., Klotz, K. 1980. Appearance of blebs on the surface of differentiating Friend erythroleukemia cells.Cell Differ. 9:239–246PubMedGoogle Scholar
  5. 5.
    Cabantchik, Z., Ginsburg, H. 1977. Transport of uridine in human red blood cells. Demonstration of a simple carrier-mediated process.J. Gen. Physiol. 69:75–96PubMedGoogle Scholar
  6. 6.
    Christensen, H.N. 1969. Some special kinetic problems of transport.In: Advances in Enzymology, F.F. Nord, editor. Vol. 32, pp. 1–36. Interscience Publishers, New YorkGoogle Scholar
  7. 7.
    Christensen, H.N. 1972. On the meaning of effects of substrate structure on biological transport.J. Bioenerg. 4:31–61Google Scholar
  8. 8.
    Christensen, H.N. 1973. On the development of amino acid transport systems.Fed. Proc. 32:19–28PubMedGoogle Scholar
  9. 9.
    Christensen, H.N. 1973. Recognition sites for material transport and information transfer.In: Current Topics in Membranes and Transport. F. Bonner and A. Kleinzeller, editors. Vol. 6, p. 277–278. Academic Press, New YorkGoogle Scholar
  10. 10.
    Christensen, H.N., de Cespedes, C., Handlogten, M., Ronquist, G. 1974. Modified transport substrates as probes for intramembrane gradients.Biochem. Biophys. Acta 227:355–379Google Scholar
  11. 11.
    Conscience, J.F., Miller, R.A., Henry, J., Ruddle, F.H. 1977. Acetylcholinesterase, carbonic anhydrase, and catalase activity in Friend erythroleukemic cells, non-erythroid cell lines and their somatic hybrids.Exp. Cell Res. 105:401–412PubMedGoogle Scholar
  12. 12.
    Czech, M.P. 1976. Regulation of thed-glucose transport system in isolated fat cells.Mol. Cell. Biochem. 11:51–61PubMedGoogle Scholar
  13. 13.
    Dube, S.K., Gaedich, G., Kluge, N., Weiman, B.J., Nelderis, H., Steinheider, G., Grozier, T., Beckmann, H., Ostertag, W. 1974. Hemoglobin-synthesizing mouse and human erythroleukemic cell lines as model systems for the study of differentiation and control of gene expression.In: Differentiation and Control of Malignancies of Tumor Cells. W. Nakahara, T. Ono, T. Sugimura, and H. Sugano, editors. pp. 103–135. University Park Press, Baltimore Md.Google Scholar
  14. 14.
    Freund, J. 1962. Mathematical Statistics. p. 266. Prentice-Hall, Trenton (New Jersey)Google Scholar
  15. 15.
    Friend, C., Scher, W. 1975. Stimulation by dimethyl sulfoxide of erythroid differentiation and hemoglobin synthesis on murine virus-induced leukemic cells.Ann. N.Y. Acad. Sci. 243:155–163PubMedGoogle Scholar
  16. 16.
    Friend, C., Scher, W., Holland, J.G., Sato, T. 1971. Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: Stimulation of erythroid differentiation by dimethyl sulfoxide.Proc. Natl. Acad. Sci. (USA) 68:378–382Google Scholar
  17. 17.
    Friend, C., Scher, W., Preisler, H. 1974. Hemoglobin biosynthesis in murine virus-induced leukemic cells in vitro.Ann. N.Y. Acad. Sci. 241:582–588PubMedGoogle Scholar
  18. 18.
    Gazitt, Y. 1979. Early decrease of 2-deoxyglucose and α-aminoisobutyric acid transport are among the first events in differentiating synchronized murine erythroleukemia cells.J. Cell. Physiol. 99:407–416PubMedGoogle Scholar
  19. 19.
    Gazitt, Y., Deitch, A., Marks, P.A., Rifkind, R.A. 1978. Cell volume changes in relation to the cell cycle of differentiating erythroleukemic cells.Exp. Cell Res. 117:413–420PubMedGoogle Scholar
  20. 20.
    Germinario, R., Kleiman, L., Peters, S., Oliveira, M. 1977. Decreased deoxy-d-glucose transport in Friend cells during exposure to inducers of erythroid differentiation.Exp. Cell Res. 110:375–385PubMedGoogle Scholar
  21. 21.
    Goodwin, F., Shafritz, D., Weissbach, H. 1969. In vitro polypeptide synthesis in brain.Arch. Biochem. 130:183–190PubMedGoogle Scholar
  22. 22.
    Guidotti, G., Borghetti, A., Gazzola, G. 1978. The regulation of amino acid transport in animal cells.Biochim. Biophys. Acta 515:329–366PubMedGoogle Scholar
  23. 23.
    Hankin, B.L., Stein, W.D. 1972. On the temperature dependence of initial velocities of glucose transport in the human red blood cell.Biochim. Biophys. Acta 288:127–136PubMedGoogle Scholar
  24. 24.
    Harrison, P.R. 1976. Analysis of erythropoiesis at the molecular level.Nature 262:353–356PubMedGoogle Scholar
  25. 25.
    Heichal, O., Ish-Shalom, D., Koren, R., Stein, W. 1979. The kinetic dissection of transport from metabolic trapping during substrate uptake by intact cells. Uridine uptake by quiescent and serum-activated Nil 8 hamster cells and their murine sarcoma virus-transformed counterparts.Biochim. Biophys. Acta 551:169–186PubMedGoogle Scholar
  26. 26.
    Hempling, H.G., Wise, W.C. 1975. Maturation of membrane function: The permeability of the rat erythroblastic leukemic cell to water and to non-electrolytes.J. Cell. Physiol. 85:195–207PubMedGoogle Scholar
  27. 27.
    Ikawa, Y., Furusawa, M., Sugano, H. 1973. Erythrocyte-membrane specific antigens in Friend virus-induced leukemia cells.In: Unifying Concepts of Leukemia Bibliotheca Hematologia. R.M. Dutcher and L. Chieco-Biachi, editors. Vol. 39, pp. 955–967. Karger, BaselGoogle Scholar
  28. 28.
    Jacquez, J.A. 1975. One-way fluxes of alpha-aminoisobutyric acid in Ehrlich ascites tumor cells. Trans effects and effects of sodium and potassium.J. Gen. Physiol. 65:57–83PubMedGoogle Scholar
  29. 29.
    Kabat, D., Sherton, C., Evans, L., Bigley, R., Koler, R. 1975. Synthesis of erythrocyte-specific proteins in cultured Friend leukemia cells. Cell5:331–338PubMedGoogle Scholar
  30. 30.
    Lieb, W.R., Stein, W.D. 1975. Testing and characterizing the simple carrier.Biochim. Biophys. Acta 373:178–196Google Scholar
  31. 31.
    Loritz, F., Bernstein, A., Miller, R. 1977. Early and late volume changes during erythroid differentiation of cultured Friend leukemic cells.J. Cell. Physiol. 90:423–438PubMedGoogle Scholar
  32. 32.
    Mager, D., Bernstein, A. 1978. Early transport changes during erythroid differentiation of Friend leukemic cells.J. Cell. Physiol. 94:275–286PubMedGoogle Scholar
  33. 33.
    Mager, D., Bernstein, A. 1978. The program of Friend cell erythroid differentiation: Early changes in Na+/K+ ATPase function.J. Supramol. Struct. 8:431–438PubMedGoogle Scholar
  34. 34.
    Marks, P.A., Rifkind, R.A. 1978. Erythroleukemic differentiation.Annu. Rev. Biochem. 47:419–448PubMedGoogle Scholar
  35. 35.
    Nishioka, Y., Silverstein, S. 1978. Alterations in the protein synthetic apparatus of Friend erythroleukemia cells during their erythroid differentiation.J. Cell. Physiol. 95:323–332PubMedGoogle Scholar
  36. 36.
    Orkin, S.H., Harosi, F.I., Leder, P. 1975. Differentiation in erythroleukemic cells and their somatic hybrids.Proc. Natl. Acad. Sci. USA 72:98–102PubMedGoogle Scholar
  37. 37.
    Oxender, D.L. 1974. Membrane transport proteins.In: Biomembranes. L. Manson, editor. Vol. 5, p. 25. Plenum Press, New YorkGoogle Scholar
  38. 38.
    Patterson, M.S., Greene, R.C. 1965. Measurement of low energy beta-emitters in aqueous solution by liquid scintillation counting of emulsions.Anal. Chem. 37:854–857PubMedGoogle Scholar
  39. 39.
    Plagemann, P.G.W., Richey, D.P. 1974. Transport of nucleosides, nucleic acid bases choline and glucose.Biochim. Biophys. Acta 344:263–305PubMedGoogle Scholar
  40. 40.
    Renner, E., Plagemann, P.G.W., Bernlohr, R. 1972. Permeation of glucose by simple and facilitated diffusion by Novikoff rat hepatoma cells in suspension culture and its relationship to glucose metabolism.J. Biol. Chem. 247:5765–5776PubMedGoogle Scholar
  41. 41.
    Riggs, T.R., Christensen, H.N., Palantine, I.M. 1952. Concentrating activity of reticulocytes for glycine.J. Biol. Chem. 194:53–55PubMedGoogle Scholar
  42. 42.
    Riggs, T., Walker, L. 1963. Some relation between active transport of free amino acids into cells and their incorporation into protein.J. Biol. Chem. 238:2663–2668PubMedGoogle Scholar
  43. 43.
    Rubin, C.S. 1978. Effects of cyclic AMP on growth of differentiating and undifferentiated Friend erythroleukemic cells.J. Cell. Physiol. 94:57–68PubMedGoogle Scholar
  44. 44.
    Schafer, J.A. 1977. A reassessment of decreased amino acid accumulation by Ehrlich ascites tumor cells in the presence of metabolic inhibitors.J. Gen Physiol. 69:681–704PubMedGoogle Scholar
  45. 45.
    Segel, I. 1975. Enzyme Kinetics: Behavior and analysis of rapid equilibrium and steady state enzyme systems. John Wiley and Sons, Inc., New YorkGoogle Scholar
  46. 46.
    Sherton, C.C., Kabat, D. 1976. Changes in RNA and protein metabolism preceeding onset of hemoglobin synthesis in cultured Friend leukemia cells.Devel. Biol. 48:118–131Google Scholar
  47. 47.
    Terada, M., Fujiki, H., Marks, P.A., Sugimura, T. 1979. Induction of erythroid differentiation of murine erythroleukemia cells by nicotinamide and related compounds.Proc. Natl. Acad. Sci. USA 76:6411–6414PubMedGoogle Scholar
  48. 48.
    Tramacere, M., Borghetti, A., Guidotti, G. 1977. Serum-mediated regulation of amino acid transport in cultured chick embryo fibroblasts.J. Cell. Physiol. 93:425–434PubMedGoogle Scholar
  49. 49.
    Tsiftsoglou, A., Sartorelli, A. 1978. Membrane alterations occurring during dimethylsulfoxide (DMSO)-induced differentiation of Friend erythroleukemia cells.J. Cell Biol. 79:CD 108Google Scholar
  50. 50.
    Wilson, G., Fox, C.F. 1971. Biogenesis of microbial transport systems: Evidence for coupled incorporation of newly synthesized lipids and proteins into membrane.J. Mol. Biol. 55:49–60PubMedGoogle Scholar
  51. 51.
    Winter, C.G., Christensen, H.N. 1965. Contrasts in neutral amino acid transport by rabbit erythrocytes and reticulocytes.J. Biol. Chem. 240:3594–3600PubMedGoogle Scholar
  52. 52.
    Wise, W.C. 1974. Transport changes during cellular maturation.Fed. Proc. 33:1393Google Scholar
  53. 54.
    Wisnieski, B.J., Parkes, J.G., Huang, Y.O., Fox, C.F. 1974. Physical and physiological evidence for two phase transitions in cytoplasmic membranes of animal cells.Proc. Natl. Acad. Sci. USA 71:4381–4385PubMedGoogle Scholar
  54. 55.
    Wong, P.T.S., Kasket, E.R., Wilson, T.H. 1970. Energy coupling in the lactose transport system ofEscherichia coli.Proc. Natl. Acad. Sci. USA 65:63–69PubMedGoogle Scholar
  55. 56.
    Wong, P.T.S., Wilson, T.H. 1970. Counterflow of galactosides inEscherichia coli.Biochim. Biophys. Acta 196:336–350PubMedGoogle Scholar
  56. 57.
    Zylka, J.M., Plagemann, P.G.W. 1975. Purine and pyrimidine transport by cultured Novikoff cells.J. Biol. Chem. 250:5756–5767Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1982

Authors and Affiliations

  • Portia B. Gordon
    • 1
  • Meryl S. Rubin
    • 1
  1. 1.Departments of Molecular Pharmacology, Medicine and BiochemistryAlbert Einstein College of MedicineBronx

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