Home LiteratureArticle Details
PMID: 3279051 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Relation between the organization of spectrin and of membrane lipids in lymphocytes.

The Journal of cell biology ·Vol. 106 ·No. 3 ·1988-03-00 ·Pages 697-703

Del Buono BJ, Williamson PL, Schlegel RA

Abstract

In lymphocytes, the cytoskeletal protein spectrin exhibits two organizational states. Because the plasma membrane lipids of lymphocytes also display two organizational states, it was asked whether there is a relation between the organization of spectrin and of membrane lipids. When mouse thymocytes were stained with merocyanine 540 (MC540), a fluorescent lipophilic probe that binds preferentially to loosely packed, disorganized lipid bilayers, some cells fluoresced brightly and some only dimly or not at all. When the same population was stained for spectrin by indirect immunofluorescence, the spectrin in some cells was uniformly distributed, while in others it was concentrated in a unipolar aggregate. Techniques enriching for mature thymocytes selected for cells displaying low MC540 fluorescence and aggregated spectrin, the same characteristics found in peripheral blood lymphocytes. Flow cytometric sorting of thymocytes based on MC540 phenotype simultaneously sorted them by spectrin phenotype. Finally, treatment with agents that alter the distribution of spectrin caused mature lymphocytes to display high MC540 fluorescence and uniform spectrin. Thus, a relation exists between the organizational states of spectrin and of membrane lipids in lymphocytes: aggregated spectrin is found in cells with tightly organized membrane lipids, uniform spectrin in those with loosely organized lipids. Spectrin may thus be involved in modulating membrane lipid organization in lymphocytes as it is in erythrocytes. Since loosely organized lipids may promote adhesion of blood cells to reticuloendothelial cells, spectrin may thereby be involved in transducing an internally generated adhesion signal to the lymphocyte surface.

MeSH Terms
Animals Cell Adhesion Cell Separation Cells, Cultured Diterpenes Flow Cytometry Fluorescent Antibody Technique Humans Lymphocytes/analysis,physiology,ultrastructure Membrane Lipids/analysis,physiology Mice Spectrin/analysis,physiology T-Lymphocytes/analysis,physiology,ultrastructure Terpenes/pharmacology Tetradecanoylphorbol Acetate/pharmacology Tetrathionic Acid/pharmacology Thymus Gland/cytology
Chemicals
Diterpenes Membrane Lipids Terpenes Spectrin mezerein Tetrathionic Acid Tetradecanoylphorbol Acetate
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Del Buono B J
Department of Molecular and Cell Biology, Pennsylvania State University, University Park 16802.
Williamson P L
Schlegel R A
References (41)
41 references, click to expand
  1. Cytoskeletal influence on merocyanine 540 receptors in the plasma membrane of erythroleukemic cells.
    Biochim Biophys Acta. 1982 Feb 10;720(1):106-10 PMID: 6949612
  2. Enucleation eliminates a differentiation-specific surface marker from normal and leukemic murine erythroid cells.
    Exp Cell Res. 1982 Jun;139(2):321-8 PMID: 6953013
  3. The human erythrocyte membrane skeleton may be an ionic gel. II. Numerical analyses of cell shapes and shape transformations.
    Eur Biophys J. 1986;13(4):219-33 PMID: 3709420
  4. Spectrin-phospholipid interaction. A monolayer study.
    Biochim Biophys Acta. 1980 Dec 2;603(1):52-62 PMID: 7448187
  5. Interaction of cytoskeletal proteins on the human erythrocyte membrane.
    Cell. 1981 Apr;24(1):24-32 PMID: 6453651
  6. Fatty acids in phospholipids isolated from human red cells.
    Lipids. 1966 Nov;1(6):391-8 PMID: 17805646
  7. Identification of immunoreactive forms of human erythrocyte band 3 in nonerythroid cells.
    Eur J Cell Biol. 1984 May;34(1):144-50 PMID: 6203749
  8. Platelets contain proteins immunologically related to red cell spectrin and protein 4.1.
    Blood. 1985 Jan;65(1):52-9 PMID: 3880645
  9. Thymocyte subpopulations: an experimental review, including flow cytometric cross-correlations between the major murine thymocyte markers.
    Thymus. 1983 Sep;5(5-6):245-95 PMID: 6362104
  10. A lymphoma plasma membrane-associated protein with ankyrin-like properties.
    J Cell Biol. 1986 Jun;102(6):2115-24 PMID: 2940251
  11. Immunofluorescent patterns of spectrin in lymphocyte cell lines.
    J Immunol. 1986 Jan;136(1):246-53 PMID: 3510004
  12. A T-lymphoma transmembrane glycoprotein (gp180) is linked to the cytoskeletal protein, fodrin.
    J Cell Biol. 1985 Aug;101(2):477-87 PMID: 3874872
  13. Brain spectrin, a membrane-associated protein related in structure and function to erythrocyte spectrin.
    Nature. 1982 Sep 9;299(5879):126-31 PMID: 7110333
  14. The functional capabilities of cells leaving the thymus.
    J Immunol. 1984 Jan;132(1):25-30 PMID: 6197445
  15. Widespread occurrence of avian spectrin in nonerythroid cells.
    Cell. 1982 Jul;29(3):821-33 PMID: 6758951
  16. Fodrin is the general spectrin-like protein found in most cells whereas spectrin and the TW protein have a restricted distribution.
    Cell. 1983 Sep;34(2):503-12 PMID: 6352052
  17. Maintenance of membrane phospholipid asymmetry. Lipid-cytoskeletal interactions or lipid pump?
    FEBS Lett. 1987 Jul 27;219(2):316-20 PMID: 3609296
  18. Spectrin immunofluorescence distinguishes a population of naturally capped lymphocytes in situ.
    J Cell Biol. 1984 Jul;99(1 Pt 1):350-5 PMID: 6376522
  19. Ankyrin is fatty acid acylated in erythrocytes.
    Proc Natl Acad Sci U S A. 1986 Jan;83(2):318-22 PMID: 2934741
  20. Involvement of spectrin in cell-surface receptor capping in lymphocytes.
    Proc Natl Acad Sci U S A. 1983 Mar;80(6):1626-30 PMID: 6572928
  21. The spectrin membrane skeleton of normal and abnormal human erythrocytes: a review.
    Am J Physiol. 1983 Mar;244(3):C121-41 PMID: 6338732
  22. Membrane phospholipid asymmetry as a factor in erythrocyte-endothelial cell interactions.
    J Cell Physiol. 1985 May;123(2):215-8 PMID: 3980587
  23. F-actin-binding and cross-linking properties of porcine brain fodrin, a spectrin-related molecule.
    J Biol Chem. 1982 Aug 25;257(16):9781-7 PMID: 7107591
  24. Disruption of phospholipid asymmetry in erythrocyte vesicles deficient in spectrin.
    Cell Biol Int Rep. 1985 Jul;9(7):597-606 PMID: 2411434
  25. Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages.
    Proc Natl Acad Sci U S A. 1986 May;83(10):3311-5 PMID: 3458184
  26. Involvement of spectrin in the maintenance of phase-state asymmetry in the erythrocyte membrane.
    Cell. 1982 Oct;30(3):725-33 PMID: 7139713
  27. The human erythrocyte membrane skeleton may be an ionic gel. I. Membrane mechanochemical properties.
    Eur Biophys J. 1986;13(4):203-18 PMID: 3709419
  28. Spectrin as a stabilizer of the phospholipid asymmetry in the human erythrocyte membrane.
    Biochim Biophys Acta. 1978 May 4;509(1):21-32 PMID: 647006
  29. Nonerythrocyte spectrins: actin-membrane attachment proteins occurring in many cell types.
    J Cell Biol. 1982 Nov;95(2 Pt 1):478-86 PMID: 6183274
  30. Merocyanine 540, a fluorescent probe sensitive to lipid packing.
    Biochim Biophys Acta. 1983 Jul 27;732(2):387-93 PMID: 6871207
  31. Separation of mouse thymocytes into two subpopulations by the use of peanut agglutinin.
    Cell Immunol. 1976 Jul;25(1):129-34 PMID: 9202
  32. Lipid asymmetry in membranes.
    Annu Rev Biochem. 1979;48:47-71 PMID: 382989
  33. Lectin-induced rearrangement of an immature hematopoietic cell surface marker.
    J Cell Physiol. 1982 Mar;110(3):245-8 PMID: 6896334
  34. Capping and the cytoskeleton.
    Int Rev Cytol. 1984;87:195-224 PMID: 6325363
  35. Asymmetric lateral mobility of phospholipids in the human erythrocyte membrane.
    Proc Natl Acad Sci U S A. 1986 Sep;83(18):6863-7 PMID: 3462734
  36. Membrane phospholipid organization as a determinant of blood cell-reticuloendothelial cell interactions.
    J Cell Physiol. 1987 Aug;132(2):381-4 PMID: 3305527
  37. Alteration of red cell membrane organization in sickle cell anaemia.
    Br J Haematol. 1986 Aug;63(4):761-73 PMID: 3730297
  38. Alterations in plasma membrane lipid organization during lymphocyte differentiation.
    J Cell Physiol. 1986 Mar;126(3):379-88 PMID: 2419347
  39. Binding of merocyanine 540 to normal and leukemic erythroid cells.
    Cell. 1980 Jun;20(2):321-8 PMID: 6156006
  40. Heterogeneity in the fluidity of intact erythrocyte membrane and its homogenization upon hemolysis.
    Biochim Biophys Acta. 1976 Mar 5;426(2):218-31 PMID: 1252507
  41. Characteristics of the immunocompetent cells in the mouse thymus: cell population changes during cortisone-induced atrophy and subsequent regeneration.
    Cell Immunol. 1970 Nov;1(5):545-60 PMID: 4399790
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1988-03-00
Pages
697-703
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2115087
Subset
IM
Grants
NCI NIH HHS · CA28921 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com