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Cytoskeletal polarity in mammalian lymphocytes in situ

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Summary

The distribution of vimentin and spectrin in lymphocytes within murine lymphoid tissues was studied by means of immunofluorescence. A polarized submembranous aggregate of intermediate filaments was observed to be characteristic of lymphocytes within the medulla of the thymus as well as in lymphocytes within specific areas of spleen and lymph-node. This aggregate was determined to be in close association with a similarly polarized aggregate of spectrin. Lymphocytes of both B and T surface phenotype comprise the population of cells that are naturally polarized in terms of these cytoskeletal proteins. Lymphocytes with such a naturally polarized cytoskeleton are not observed in the spleen until approximately 5 days after birth, but are observed in the thymus by day 19 of gestation. Incubating lymphocytes with cytochalasin D, but not colchicine, caused a rapid dispersal of the spectrin aggregate without altering the polar accumulation of intermediate filaments. When splenic B-cells were allowed to form uropods as a result of ligand binding, the uropod (as well as surface receptor “cap”) was positioned above the region containing the polar aggregate of spectrin and vimentin. The possible physiological significance of naturally occurring cytoskeletal polarity in lymphocytes is discussed.

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References

  • Asch BB, Asch H (1986) Cell surface and cytoskeletal components as markers of differentiation and neoplastic progression in mammary epithelium. In: Ip C, Medina D, Kidwek W, Hepner G, Andersen E (eds) Cell and Molecular Biology of Experimental Mammary Cancer, Plenum Press New York (In press)

    Google Scholar 

  • Bennett V (1985) The membrane skeleton of human erythrocytes and its implication for more complex cells. Annu Rev Biochem 54:273–304

    Google Scholar 

  • Bourguignon LYW, Bourguignon G (1981) Immunocytochemical localization of intermediate filament proteins during lymphocyte capping. Cell Biol Int Rep 5:783–789

    Google Scholar 

  • Cohen CM (1983) The molecular organization of the red cell membrane cytoskeleton. Semin Hematol 20:141–158

    Google Scholar 

  • Dellagi K, Brouet J-C (1982) Redistribution of intermediate filaments during capping of lymphocyte surface proteins. Nature (Lond) 298:284–286

    Google Scholar 

  • Franke WW, Schmid E, Osborn M, Weber K (1978) Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc Natl Acad Sci USA 75:5034–5038

    Google Scholar 

  • Geiger B, Rosen D, Berke G (1982) Spatial relationships of microtubule-organizing centers and the contact area of cytotoxic T lymphocytes and target cells. J Cell Biol 95:137–143

    Google Scholar 

  • Geiger B (1983) Membrane-cytoskeleton interaction. Biochim Biophys Acta 737:305–341

    Google Scholar 

  • Goldman RD (1971) The role of three cytoplasmic fibers in BHK-21 cell motility. I. Microtubules and the effects of colchicine. J Cell Biol 51:752–762

    Google Scholar 

  • Granger BL, Repasky EA, Lazarides E (1982) Synemin and vimentin are components of intermediate filaments in avian erythrocytes. J Cell Biol 92:299–312

    Google Scholar 

  • Granger BL, Lazarides E (1984) Membrane skeletal protein 4.1 of avian erythrocytes is composed of multiple variants that exhibit tissue-specific expression. Cell 37:595–607

    Google Scholar 

  • Hainfeld JF, Steck TL (1977) The sub-membrane reticulum of the human erythrocyte: A scanning electron microscope study. J Supramol Struct 6:301–311

    Google Scholar 

  • Hirokawa N, Cheney RE, Willard M (1983) Location of the fodrinspectrin-TW260/240 family in the mouse intestinal brush border. Cell 32:953–965

    Google Scholar 

  • Kupfer A, Dennert G (1984) Reorientation of the microtubuleorganizing center and the Golgi apparatus in cloned cytotoxic lymphocytes triggered by binding to lysable target cells. J Immunol 133:2762–2766

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond) 277:680–685

    Google Scholar 

  • Lazarides E (1984) Assembly and morphogenesis of the avian erythrocyte cytoskeleton. In: Borisy GG, Cleveland DW, Murphy DB (eds) Molecular Biology of the Cytoskeleton, pp 131–150, Cold Spring Harbor, New York

    Google Scholar 

  • Lazarides E, Granger BL (1982) Preparation and assay of the intermediate filament proteins desmin and vimentin. Methods Enzymol 85:488–508

    Google Scholar 

  • Langley RC, Cohen CM (1984) atSpectrin binds to intermediate filaments. J Cell Biol 99(4. Pt. 2): 303a (Abstr)

  • Levine J, Willard M (1983) Redistribution of fodrin (a component of the cortical cytoplasm) accompanying capping of cell surface molecules. Proc Natl Acad Sci USA 80:191–195

    Google Scholar 

  • Mangeat PH, Burridge K (1984) Immunoprecipitation of nonerythrocyte spectrin within live cells following microinjection of specific antibodies: relation to cytoskeletal structures. J Cell Biol 98:1363–1377

    Google Scholar 

  • Marchesi VT (1985) Stabilizing infrastructure of cell membranes. Annu Rev Cell Biol 1:531–561

    Google Scholar 

  • Nelson WJ, Colaco CALS, Lazarides E (1983) Involvement of spectrin in cell-surface receptor capping in lymphocytes. Proc Natl Acad Sci USA 80:1626–1630

    Google Scholar 

  • Nicholson GL, Marchesi VT, Singer SJ (1971) The localization of spectrin on the inner surface of human red blood cell membranes by ferritin-conjugated antibodies. J Cell Biol 51:265–272

    Google Scholar 

  • Pauly JL, Bankert RB, Repasky EA (1986) Immunofluorescence patterns of spectrin in lymphocyte cell lines. J Immunol 136:246–252

    Google Scholar 

  • Repasky EA, Granger BL, Lazarides E (1982) Widespread occurrence of avian spectrin in nonerythroid cells. Cell 29:821–833

    Google Scholar 

  • Repasky EA, Symer D, Bankert RB (1984) Spectrin immunofluorescence distinguishes a population of naturally capped lymphocytes in situ. J Cell Biol 99:350–355

    Google Scholar 

  • Rothenberg E, Lugo JP (1985) Differentiation and cell division in the mammalian thymus. Dev Biol 112:1–17

    Google Scholar 

  • Sommer JR (1977) To cationize glass. J Cell Biol 75(2 Pt. 2):745a (Abstr)

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some application. Proc Natl Acad Sci USA 76:4350–5354

    CAS  PubMed  Google Scholar 

  • Unanue ER, Perkins WD, Karnovsky MJ (1972) Ligand induced movement of lymphocyte membrane macromolecules. I. Analysis by immunofluorescence and ultrastructural radiography. J Exp Med 136:885–906

    Google Scholar 

  • Zucker-Franklin D, Liebes LF, Sibler R (1979) Differences in the behavior of the membrane and membrane-associated filamentous structures in normal and chronic lymphocytic leukemia (CLL) lymphocytes. J Immunol 122:97–107

    Google Scholar 

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Lee, J.K., Repasky, E.A. Cytoskeletal polarity in mammalian lymphocytes in situ. Cell Tissue Res. 247, 195–202 (1987). https://doi.org/10.1007/BF00216562

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