The asymmetric arrangement of phospholipids in the human erythrocyte membrane

Gordesky, Stanley E.; Marinetti, G.V.

doi:10.1016/0006-291x(73)91509-x

Cited by 330 publications

(125 citation statements)

References 7 publications

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“…From these results they concluded that at least two thirds of the lecithin is localized in the outer monolayer, whereas phosphatidylserine and phosphatidylethanolamine are largely confined to the membrane interior of the human erythrocyte. A similar conclusion regarding the non-random distribution of phospholipids was reached by Bretscher [12] and also by Gordeski and Marinetti [13]. In these latter studies the observation was mainly based on indirect evidence obtained by labelling the cell with relatively non-permeant reagents.…”

supporting

confidence: 72%

Preferential incorporation of fatty acids at the inside of human erythrocyte membranes

Renooij

Golde

Zwaal

et al. 1974

Biochimica et Biophysica Acta (BBA) - Biomembranes

100

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Summary1. Phospholipase A2 isolated from Naja naja venom was used as a tool to discriminate between the outer and inner lipid monolayer of the membranes of human erythrocytes.2. Incubation of human erythorcytes with radioactive fatty acids resulted in the formation of labelled lecithin in the membrane. The label was found predominantly in that pool of lecithin which is localized in the inner monolayer of the membrane.3. Lecithins isolated from the total erythrocyte membrane and from the inner monolayer of the membrane possess identical fatty acid patterns and identical positional distributions of their fatty acyl constituents.Circulating red blood cells should be capable of incorporating fatty acids into their phospholipids since variations in the diet can induce alterations in the fatty acid pattern of the phospholipids within a much shorter period than the average lifespan of the erythrocyte [1,2], Two mechanisms have been described to play a major role in the renewal of the phospholipids of the erythrocyte membrane: (1) an exchange of phospholipids between serum lipoproteins and the red cell membrane [3--5] and (2) the incorporation of fatty acids into lysophospholipids which are either formed in the membrane or supplied by the surrounding serum [6,7]. Shohet [8,9] proposed the existence of two compartments of lecithin in the erythrocyte membrane: one of these is thought to be in equilibrium with lecithin from

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supporting

confidence: 72%

Preferential incorporation of fatty acids at the inside of human erythrocyte membranes

Renooij

Golde

Zwaal

et al. 1974

Biochimica et Biophysica Acta (BBA) - Biomembranes

100

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“…These observations were essentially confirmed by Gordeski and Marinetti [8] using the non-penetrating probe 2,4,6-trinitrobenzene sulphonate, and very recently by Whiteley and Berg [9] upon amidination of the outer and inner surfaces of the red cell membrane.…”

Section: Introductionsupporting

confidence: 57%

Organization of phospholipids in human red cell membranes as detected by the action of various purified phospholipases

Zwaal

Roelofsen

Comfurius

et al. 1975

Biochimica et Biophysica Acta (BBA) - Biomembranes

351

119

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SUMMARY1. The action of eight purified phospholipases on intact human erythrocytes has been investigated. Four enzymes, e.g. phospholipases A2 from pancreas and Crotalus adamanteus, phospholipase C from Bacillus cereus, and phospholipase D from cabbage produce neither haemolysis nor hydrolysis of phospholipids in intact cells. On the other hand, both phospholipases A2 from bee venom and Naja naja cause a non-haemolytic breakdown of more than 50 ~ of the lecithin, while sphingomyelinase C from Staphylococcus aureus is able to produce a non-lytic degradation of more than 80 ~o of the sphingomyelin.2. Phospholipase C from Clostridium welchii appeared to be the only lipolytic enzyme tested, which produces haemolysis of human erythrocytes. Evidence is presented that the unique properties of the enzyme itself, rather than possible contaminations in the purified preparation, are responsible for the observed haemolytic effect.3. With non-sealed ghosts, all phospholipases produce essentially complete breakdown of those phospholipids which can be considered as proper substrates for the enzymes involved.4. Due to its absolute requirement for Ca 2 ÷, pancreatic phospholipase A2 can be trapped inside resealed ghosts in the presence of EDTA, without producing phospholipid breakdown during the resealing procedure. Subsequent addition of Ca 2 ÷ stimulates phospholipase A z activity at the inside of the resealed cell, eventually leading to lysis. Before lysis occurs, however, 25 ~o of the lecithin, half of the phosphatidylethanolamine and some 65 ~ of the phosphatidylserine can be hydrolysed. This observation is explained in relation to an asymmetric phospholipid distribution in red cell membranes.Phospholipases used: phospholipase A2 (phosphatide acyl-hydrolyse, EC 3.1.1.4) from pig pancreas, bee venom, Naja naja, and Crotalus adamanteus, respectively. Phospholipase C (phosphatidylcholine cholinephosphohydrolase, EC 3.1.4.3) from Bacillus cereus and Clostridium welchii. Sphingomyelinase C (sphingomyelin cholinephosphohydrolase) from Staphylococcus aureus. Phospholipase D (phosphatidylcholine phosphatidohydrolase, EC 3.1.4.4) from Savoy cabbage. 84 5. It is concluded that the ability of the various phospholipases to attack the red cell membrane is dependent upon: (i) substrate specificity of the phospholipases, (ii) sidedness of the phospholipids when only one side of the membrane is exposed to phospholipase action, and (iii) compression state of the membranous lipid layer. The latter point is dealt with in more detail in the accompanying paper (Demel, R.

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“…In a monolayer containing a total lipid extract of B. subtilis it was found that both phosphatidylethanolamine and lysyl phosphatidylglycerol were incompletely trinitrophenylated ( Table I). The above data obtained with the monolayer technique may offer an explanation for the incomplete labelling of phosphatidylethanolamine [8,11] and phosphatidylserine [3,5] in some natural membranes. A high surface pressure as well as a negative surface charge clearly inhibit the reaction and it is obvious that both parameters become more effective as more amino phospholipids are converted into the trinitrophenyl derivatives.…”

Section: Resultsmentioning

confidence: 73%

A monolayer study of the reaction of trinitrobenzene sulphonic acid with amino phospholipids

Bishop

Bevers

Meer

et al. 1979

Biochimica et Biophysica Acta (BBA) - Biomembranes

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SummaryThe reaction of trinitrobenzene sulphonic acid with amino phospholipids, and in particular phosphatidylethanolamine has been studied by the monolayer technique. Injection of trinitrobenzene sulphonic acid under a monolayer of amino phospholipid results in an increase in surface pressure. The rate and extent of the pressure change is greatly affected by the initial surface pressure, the fatty acid composition of the lipid, and the presence of other non-reactive lipids, especially negatively charged phospholipids.The extent of the reaction was measured with 32P-labelled phospholipids isolated from Bacillus subtilis. Only about 80% of the phosphatidylethanolamine in the monolayer could be converted to its trinitrophenyl derivative. In the presence of negatively charged phospholipids such as cardiolipin or phosphatidylglycerol, a further 20% decrease in the trinitrophenylation of phosphatidylethanolamine was found. The pressure increase occurring during trinitrophenylation could also be correlated with the extent of the reaction by comparison of the force-area curves of pure phosphatidylethanolamine, its trinitrophenyl derivative and mixtures of both compounds.The data may offer an explanation for the observation that incomplete labelling of amino phospholipids frequently occurs in natural membranes and furthermore indicate that the use of chemical labelling techniques in the study of lipid asymmetry in biological membranes must be approached with great caution.

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The asymmetric arrangement of phospholipids in the human erythrocyte membrane

Cited by 330 publications

References 7 publications

Preferential incorporation of fatty acids at the inside of human erythrocyte membranes

Preferential incorporation of fatty acids at the inside of human erythrocyte membranes

Organization of phospholipids in human red cell membranes as detected by the action of various purified phospholipases

A monolayer study of the reaction of trinitrobenzene sulphonic acid with amino phospholipids

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