Biochimica et Biophysica Acta, 1023 (1990) 63-72 63
Elsevier
BBAMEM 74767
Membrane skeleton-bilayer interaction is not the major
determinant of membrane phospholipid asymmetry
in human erythrocytes *
S.R.P. Gudi, A. Kumar * *, V. Bhakuni, S.M. Gokhale and C.M. Gupta
Division of Membrane Biology, Central Drug Research Institute, Lucknow (India)
(Received 23 October 1989)
Key words: Phospholipid asymmetry; Membrane skeleton; Spectrin denaturation; (Human)
Transbilayer phospholipid distribution, membrane skeleton dissociation/association, and spectrin structure have been
analysed in human erythrocytes after subjecting them to heating at 50°C for 15 min. The membrane skeleton
dissociation/association was determined by measuring the Tris-induced dissociation of Triton-insoluble membrane
skeletons (Triton shells), the spectrin-actin extractability under low ionic conditions, and the binding of spectrin-actin
with normal erythrocyte membrane inside-out vesicles (IOVs). The spectrin structure was ascertained by measuring the
spectrin dimer-to-tetramer ratio as well as the spectrin tryptophan fluorescence. Both the Tris-induced Triton shell
dissociation and the spectrin-actin extractability under low ionic conditions were considerably reduced by the heat
treatment. Also, the binding of heated erythrocyte spectrin-actin to IOVs was significantly smaller than that observed
with the normal cell spectrin-actin. Further, the quantity of spectrin dimers was appreciably increased in beat-treated
erythrocytes as compared to the normal cells. This change in the spectrin dimer-to-tetramer ratio was accompanied by
marked changes in the spectrin tryptophan fluorescence. Inspite of these beat-induced alterations in structure and
hilayer interactions of the membrane skeleton, the inside-outside glycerophospholipid distribution remained virtually
unaffected in the heat-treated cells, as judged by employing bee venom and pancreatic phospholipase A 2, fluorescamine
and Merocyanine 540 as the external membrane probes. These results strongly indicate that membrane bilayer-skele-
ton interaction is not the major factor in determining the transbilayer phospholipid asymmetry in human erythrocyte
membrane.
Introduction
Human erythrocyte membrane is composite of two
structural units, viz. membrane skeleton (or cyto-
skeleton) and membrane bilayer. While the membrane
bilayer is comprised of lipids and integral membrane
* Communication No. 4063 from C.D.R.I., Lucknow, India.
* * Present address: Department of Pathology,Yale University, School
of Medicine, 310 Cedar Street, New Haven, CT 06510, U.S.A.
Abbreviations: RBC, red blood cells; PC, phosphatidylcholine; SM,
sphingomyelin; PE, phosphatidylethanolamine; PS, phosphatidyl-
serine; PMSF, phenylmethylsulfonyl fluoride; GSH, glutathione; ATP,
adenosine 5'-triphosphate; EDTA, ethylenediamine tetraacetic acid;
SDS, sodium dodecylsulfate; PBS, phosphate-bufferedsaline; Mc 540,
Merocyanine 540; IOVs, inside-out vesicles; ROVs, fight side-out
vesicles; TLC, thin-layer chromatography.
Correspondence: C.M. Gupta, Division of Membrane Biology, Central
Drug Research Institute, Lucknow 226 001, India.
proteins, membrane skeleton is a reticulate type of
structure formed from three major (spectrin, actin and
polypeptide 4.1) and several minor peripheral mem-
brane proteins and is associated with the cytoplasmic
face of the membrane bilayer through protein-protein
and protein-phospholipid interactions [1]. The mem-
brane bilayer-skeleton association controls not only the
membrane mechanical stability and deformability but
also the lateral mobility of the integral membrane pro-
teins [2]. Besides, this association has been considered
as the major factor in maintaining the asymmetric phos-
pholipid distribution across the erythrocyte membrane
bilayer [3].
Erythrocyte membrane phospholipids are asymmetri-
cally distributed in the two halves of the membrane
bilayer. The choline-containing phospholipids (PC and
SM) are present mainly in the outer monolayer, whereas
the aminophospholipids (PE and PS) are localized al-
most exclusively in the inner monolayer [4]. This typical
transbilayer phospholipid asymmetry is disturbed in
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