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ORIGINAL ARTICLE

Magnesium Research (1989) 2, 4, 243-247


A qualitative theory of the screening-binding effects of magnesium salts on epithelial cell membranes: a new hypothesis


M. Bara1, A. Guiet-Bara2, J. Durlach3

1Laboratory of Biology of Reproduction, University P. M. Curie, 7 Quai Saint-Bernard, 75252 Paris Cedex 05; 2Laboratory of Biology of Reproduction, University P. M. Curie, 7 Quai Saint-Bernard, 75252 Paris Cedex 05; 3CHU Cochin Port-Royal, 27 Rue du Faubourg Saint-Jacques, 75674 Paris Cedex 14, France


Summary: A theoretical explanation is given of the screening-binding effects of various magnesium salts on the ionic permeability of epithelial amniotic cell membranes. It is suggested that the 'screening process' induces an increase in the electrical membrane resistance and in membrane stability which is a unique action at low concentration. At high concentration, the binding process induces a reduction or an increase in these parameters as a function of the magnesium salt present. The different effects are due to changes in the distribution and in the repartition of the fixed charges on the cell membrane.

Key words: Binding, magnesium, membrane, screening.

Introduction

There are two categories of electrostatic interactions between cations and negatively charged surfaces 1,2. In the first category, there is the usual type of electrostatic binding where the cations complex to anionic surface moities and are not mobile. In the second category of associations, often referred to as 'screening', the cations remain mobile, most likely fully hydrated and unbound, being held loosely by hydrogen bonds in a diffuse layer close to the surface 3. The two types of interactions together can explain the effects of cations on the stability of the membrane.

In studies on ionic permeability through the human isolated amniotic membrane, it has been shown 1,4 that different magnesium salts have different effects on the membrane stability, as follows (Table):

Table. The magnesium salts employed.

Magnesium salt
hydrated Name

MgSO4.7H2O Magnesium sulphate heptahydrate
Mg(Cl2.6H2O Magnesium chloride hexahydrate
Mg (NO3)2.2H2O Magnesium nitrate dihydrate
Mg (CH3COO)2.4H2O    Magnesium acetate tetrahydrate
Mg (C3H3O3)2.3H2O Magnesium lactate trihydrate
Mg(HC6H5O7).5H2O Magnesium citrate pentahydrate

1. The salts MgCl.6H2O, Mg(CH3OO)2.4H2O, and magnesium citrate increase the stability at low concentrations, then decrease it at higher concentrations on both sides of the amnion.

2. The effects of the salts of MgSO4 and Mg(NO3)2.2H2O are independent of concentration. They increase the stability on the maternal side and decrease it on the fetal side.

3. The salt of magnesium lactate increases the stability on the maternal side, whatever the concentration; it increases the stability on the fetal side at low concentrations, and it decreases it at high concentrations.

We now propose a theory to explain the effects of the addition of magnesium salts on the surface polar groups, which are responsible for the exchange through the isolated human amnion.

Hypothesis

This new theory concerns the 'screening' and binding effects.

The 'screening effect' (Figure 1)


Figure 1.

The term 'screening' is used to show the existence of ions at a distance of a few angstroms from the membrane surface in the aqueous diffuse layer and to distinguish this effect from the phenomenon of the specific adsorption 5 . In this case, the distance membrane polar groups (positive and negative), whatever their location and distribution, are masked by the hydration shell around the cations and that this reduces considerably the repulsive or attractive forces between the divalent cations and the surface charges, but there are now H-bond interactions 3. The external sites on the membrane are not accessible to the ions present in the medium and the electrical resistance of the membrane increases; thus the 'screening process' induces an increase of the membrane stability.

The binding effect (Figures 2-5)

In the binding processes, the cations have lost their hydration shell and the interactions between cations and surface polar groups are direct and possible. These interactions are a function of the location and the distribution of the surface binding sites. In this work, we have analysed different situations depending to the location of the external sites, which are illustrated in Figs 2-5.

In Fig. 2 it can be seen that:

1. the divalent cations are near the surface sites and there are attractive forces between cations and negative surface sites (L-) and repulsive forces between cations and positive surface sites (L+);

2. the divalent cations are drawn towards two negative sites (L-) with formation of strong covalent bonds between cation (Mg2+) and sites; and

3. there is formation of neutral complexes of the type [L-Mg-L]0 (zero charged magnesium complexes)--the number of accessible sites is reduced, the electrical membrane resistance increases and the membrane stability is increased.


Figure 2.

Figure 3 shows that:

(1) the divalent cations are again near the surface sites and there are attractive forces between cations and negative surface sites (L-), and repulsive forces between cations and positive surface sites (L+);

(2) the divalent cations are drawn towards one negative side (L-) with formation of a strong covalent bond and repulsion with the positive surface sites (L+); and

(3) there is neutralization of a negative surface site by one positive divalent cation charge. There is formation of positive complexes of the type [Mg-L]+ (singly charged magnesium complexes). A positive surface site is established instead of a negative surface charge. A repulsion with regard to an adjacent positive site results, the binding surface sites is weakened, and the intersite distance is increased (b>a) -- the electrical membrane resistance is reduced and the membrane stability is decreased.


Figure 3.

Figure 4 shows that:

1. the divalent cations are again near the surface sites and there are attractive forces between cations and negative surface sites (L-), and repulsive forces between cations and positive surface sites (L+);

2. the divalent cations are drawn towards one negative site (L-) with formation of a strong covalent bond and repulsion of the positive surface sites; and

3. there is neutralization of a negative surface site by one positive divalent cation charge. There is formation of positive complexes of the type [Mg-L]+ singly charged magnesium complexes. A positive surface site is established instead of a negative surface charge. A repulsion with regard to adjacent positive sites is induced, the bindings between surface sites are weakened, and the intersite distance is increased (b>a and b'<a); as a result the electrical membrane resistance is reduced and the membrane stability is decreased.


Figure 4.

Figure 5 shows that:

1. the divalent cations are again near the surface sites and there are attractive forces between cations and negative surface sites (L-), and repulsive forces between cations and positive surface sites (L+);

2. in this case, some (divalent cations are drawn towards two negative sites (L-) with formation of strong covalent bonds, some other divalent cations are drawn towards one negative site (L-) and repel the adjacent positive site (L+), and some repel two adjacent positive sites; and

3. there are three possible situations:

The result of the cases described in Fig. 5 may be either a decrease (left) or an increase (middle and right) in the membrane stability.

The distribution and the location of the surface sites will determine the binding process which may be of two different forms:

(1) an increase in the membrane stability (Figs 2, and 5 middle and right);

(2) a decrease of the membrane stability (Figs 3, 4 and 5 left).


Figure 5.

Implications

The results obtained with various magnesium salts on the ionic permeability of the human amnion 1,4, may be explained by the above theoretical considerations.

Maternal side

At low concentrations, all magnesium salts decrease the electrical conductance and the ionic fluxes. This action may be described as a 'screening effect' (Fig. 1): the hydration shell is present, the salts are highly hydrated and the external sites are masked. The electrical membrane resistance increases 1,4.

At high concentrations, it has been shown that there are two effects as a function of the magnesium salt present.

(a) A 'screening effect' (concerning, ie MgSO4, Mg lactate, Mg(NO3)2) has been described because of a decrease in the electrical conductance or the ionic fluxes 1,4 . In this case, the hydration shell is still present, but in the preceding hypothesis the interaction may be more complex: a decrease in the electrical conductance and in the ionic fluxes may be observed in a binding saturation (Figs 2 and 5, middle and right). This explanation may be applicable to the action of these magnesium salts at high concentration.

(b) A binding effect (concerning, ie, MgCl2, Mg acetate, Mg citrate) has been described, because of an increase in the electrical conductance and the ionic fluxes 1,4. These observations correspond to the situation described in Figs 3, 4 and 5 (left).

Fetal side

At low concentrations, the electrical conductance and the ionic fluxes are decreased by all the magnesium salts studied except MgSO4 and Mg(NO3)2 1,4. In general, there is a 'screening effect' (Fig. 1). However, with MgSO4, and Mg nitrate the hydration shell is immediately lost, in favour of a strong attraction between these salts and the external surface sites of the fetal face. This effect may be related to the lipid composition of the fetal membrane 3,6.

At high concentrations, the electrical conductance and the ionic fluxes are increased by all magnesium salts. This corresponds to the binding effect described in Figs 3, 4 and 5 (left).

Discussion

It has often been suggested that fixed electrical charges in the cell membrane are related to the ionic mechanism and electrical activity of the cell. Thus, fixed charges have been implicated in hypotheses related to the ionic transport across the membrane 7,8.

Our results 1,4 have been analysed in terms of changes in surface potential by 'screening' of counter-ions in the external solution which form a diffuse double layer at the surface, or by the binding of cations to the fixed charges on the cell membranes. If the negative charge density on the membrane is high, the diffuse double layer theory predicts that the addition of even a low concentration of divalent cations to one side of the membrane will reduce the negative surface potential on that side by a 'screening process'. The increase in the negative surface potential would be the result of a binding process. The magnesium salts interact with the surface charges of the epithelial amniotic cell by 'screening' and binding processes. The 'screening process' induces an increase in tile electrical resistance and the membrane stability.

The new hypothesis shows that the binding process induces either a decrease or an increase in the electrical resistance and the membrane stability. The induction of these two processes is generally due to the concentration of the magnesium salts . In a binding process, the increase or decrease in the membrane stability is a function of the distribution and the location of the external sites. These two parameters are not fixed in the membrane and are conditioned by the external medium. The magnesium salts affect the packing of the phospholipids in a membrane and can lead to membrane alterations, such as morphological changes or site distribution changes. One might hypothesize that the disturbance due to the insertion of a few molecules between the lipid layers affects the membrane sufficiently to change its binding characteristics 9.

Conclusion

The various effects of magnesium salts on the membrane stability may be explained with this hypothesis, which shows the important role of the anion. Indeed, with a common cation (Mg2+), different effects may be obtained after anion change. Tile surface charges react differently and/or selectivity with the membrane, and its stability may be increased or decreased. Furthermore, at high salt concentrations, the hydration shell may disappear and a direct binding process may result as a function of the distribution, repartition of fixed charges, and anions present: the membrane stability may increase or decrease.

References:

1. Bara, M., Guiet-Bara, A. & Durlach, J. (1988): Analysis of magnesium membraneous effects: binding and screening. Magnesium Res. 1, 29-33.

2. Puskin, J.S.. (1977): Divalent cation binding to phospholipids: an EPR study. J. Memb. Biol. 35, 39-55.

3. Theophanides, T., Angiboust, J.F., Anastassopoulou, J. & Manfait, M. (1990): Possible role of water structure in magnesium biological Systems. Magnesium Res. (in press).

4. Bara, M., Guiet-Bara, A. & Durlach, J. (1988): Modification of human amniotic membrane stability after addition of magnesium salts.. Magnesium Res. 1, 23-28.

5. Kass, R.S. & Krafte, D.S. (1987): Negative surface charge density near heart calcium channels. J. Geit. Physiol. 89, 629-644.

6. Bara, M. (1982): Electron transport through human epithelial amniotic membrane in vitro. Comparative study with artificial membranes (bilayer and millipore filters). Bioelectr. Bioenerg. 9, 517-525.

7. Teorell, T. (1935): An attempt to formulate a quantitative theory of membrane permeability. Proc. Soc. Exp.Biol. Med. 33, 282-285.

8. Ling, G.N. (1952): The role of phosphorus in the maintenance of the resting potential and selective accumulation in frog muscle cells. In Phosphorus metabolism, ed W.D. McElroy & B. Glass, vol. 2. Baltimore: Johns Hopkins Press.

9. Zachowski, A. & Durand, P. (1988): Biphasic nature of the binding of cationic amphipaths with artificial and biological membranes. Biochem. Biophys. Acta 937, 411-416.


All articles by Dr. Durlach are copyrighted, and permission is granted to Web users only to make single hard copies for personal use. Additional reprints should be obtained from the originating journals. Excerpts may be used by the media with attribution to Dr. Durlach.


This page was first uploaded to The Magnesium Web Site on April 29, 1996



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