×

zbMATH — the first resource for mathematics

Influence of magnesium sulfate on \(\mathrm{HCO}_3/\mathrm{Cl}\) transmembrane exchange rate in human erythrocytes. (English) Zbl 1343.92190
Summary: Magnesium sulfate (MgSO\(_{4}\)) is widely used in medicine but molecular mechanisms of its protection through influence on erythrocytes are not fully understood and are considerably controversial. Using scanning flow cytometry, in this work for the first time we observed experimentally (both in situ and in vitro) a significant increase of HCO\(_3^-\)/Cl\(^-\) transmembrane exchange rate of human erythrocytes in the presence of MgSO\(_4\) in blood. For a quantitative analysis of the obtained experimental data, we introduced and verified a molecular kinetic model, which describes activation of major anion exchanger Band 3 (or AE1) by its complexation with free intracellular Mg\(^{2+}\) (taking into account Mg\(^{2+}\) membrane transport and intracellular buffering). Fitting the model to our in vitro experimental data, we observed a good correspondence between theoretical and experimental kinetic curves that allowed us to evaluate the model parameters and to estimate for the first time the association constant of Mg\(^{2+}\) with Band 3 as \(K_B\sim 0.07\)mM, which is in agreement with known values of the apparent Mg\(^{2+}\) dissociation constant (from 0.01 to 0.1mM) that reflects experiments on enrichment of Mg\(^{2+}\) at the inner erythrocyte membrane (Gunther, 2007). Results of this work partly clarify the molecular mechanisms of MgSO\(_{4}\) action in human erythrocytes. The method developed allows one to estimate quantitatively a perspective of MgSO\(_{4}\) treatment for a patient. It should be particularly helpful in prenatal medicine for early detection of pathologies associated with the risk of fetal hypoxia.
MSC:
92C45 Kinetics in biochemical problems (pharmacokinetics, enzyme kinetics, etc.)
PDF BibTeX XML Cite
Full Text: DOI
References:
[1] Abad, C.; Teppa-Garran, A.; Proverbio, T.; Pinero, S.; Proverbio, F.; Marin, R., Effect of magnesium sulfate on the calcium-stimulated adenosine triphosphatase activity and lipid peroxidation of red blood cell membranes from preeclamptic women, Biochem. Pharmacol., 70, 1634-1641, (2005)
[2] Abad, C.; Carrasco, M. J.; Piñero, S.; Delgado, E.; Chiarello, D. I.; Teppa-Garrán, A.; Proverbio, T.; Proverbio, F.; Marín, R., Effect of magnesium sulfate on the osmotic fragility and lipid peroxidation of intact red blood cells from pregnant women with severe preeclampsia, Hypertens. Pregnancy, 29, 38-53, (2010)
[3] Achilles, W.; Cumme, G. A.; Hoppe, H., 2, 3-diphosphoglycerate: acid dissociation and complex formation with magnesium, potassium, and sodium, Acta Biol. Med. Ger., 29, 531-538, (1972)
[4] Antonov, S.; Johnson, J. W., Permeant ion regulation of N-methyl-daspartate receptor channel block by mg2, Proc. Natl. Acad. Sci. USA, 96, 14571-14576, (1999)
[5] Ariza, A. C.; Bobadillab, N.; Fernandez, C.; Munoz-Fuentes, R. M.; Larrea, F.; Halhali, A., Effects of magnesium sulfate on lipid peroxidation and blood pressure regulators in preeclampsia, Clin. Biochem., 38, 128-133, (2005)
[6] Bara, M.; Guiet-Bara, A.; Durlach, J., Regulation of sodium and potassium pathways by magnesium in cell membranes, Magnes. Res., 6, 167-177, (1993)
[7] Barbul, A.; Zipser, Y.; Nachles, A.; Korenstein, R., Deoxygenation and elevation of intracellular magnesium induce tyrosine phosphorylation of band 3 in human erythrocytes, FEBS Lett., 455, 87-91, (1999)
[8] Beydemir, S.; Ciftci, M.; Ozmen, I.; Okuroglu, M. E.B.; Ozdemir, H.; Kufrevioglu, O. I., Effects of some medical drugs on enzyme activities of carbonic anhydrase from human erythrocytes in vitro and from rat erythrocytes in vivo, Pharmacol. Res., 42, 187-191, (2000)
[9] Blitz, M.; Blitz, S.; Hughes, R.; Diner, B.; Beasley, R.; Knopp, J.; Rowe, B. H., Aerosolized magnesium sulfate for acute asthma: a systematic review, Chest, 128, 337-344, (2005)
[10] Bock, J. L.; Crull, G. B.; Wishnia, A.; Springer, C. S., 25mg NMR studies of magnesium binding to erythrocyte constituents, J. Inorg. Biochem., 44, 79-87, (1991)
[11] Brunati, A. M.; Bordin, L.; Clari, G.; Moret, V., The lyn-catalyzed tyr phosphorylation of the transmembrane band-3 protein of human erythrocytes, Eur. J. Biochem., 240, 394-399, (1996)
[12] Chanson, A.; Feillet-Coudray, C.; Gueux, E.; Coudray, C.; Rambeau, M.; Mazur, A.; Wolf, F. I.; Rayssiguier, Y., Evaluation of magnesium fluxes in rat erythrocytes using a stable isotope of magnesium, Front. Biosci., 10, 1720-1726, (2005)
[13] Chernyshev, A. V.; Tarasov, P. A.; Semianov, K. A.; Nekrasov, V. M.; Hoekstra, A. G.; Maltsev, V. P., Erythrocyte lysis in isotonic solution of ammonium chloride: theoretical modeling and experimental verification, J. Theor. Biol., 251, 93-107, (2008)
[14] Deering, S. H.; Stagg, A. R.; Spong, C. Y.; Abubakar, K.; Pezzullo, J. C.; Ghidini, A., Antenatal magnesium treatment and neonatal illness severity as measured by the score for neonatal acute physiology (SNAP), J. Matern. Fetal Neonatal. Med., 17, 151-155, (2005)
[15] Doyle, L. W.; Crowther, C. A.; Middleton, P.; Marret, S., Antenatal magnesium sulfate and neurologic outcome in preterm infants: a systematic review, Obstet. Gynecol., 113, 1327-1333, (2009)
[16] Duley, L.; Neilson, J. P., Magnesium sulphate and pre-eclampsia. trial needed to see whether it’s as valuable in pre-eclampsia as in eclampsia, Br. Med. J., 319, 3-4, (1999)
[17] Elimian, A.; Verma, R.; Ogburn, P.; Wiencek, V.; Spitzer, A.; Quirk, J. G., Magnesium sulfate and neonatal outcomes of preterm neonates, J. Matern. Fetal Neonatal. Med., 12, 118-122, (2002)
[18] Euser, A. G.; Cipolla, M. J., Magnesium sulfate for the treatment of eclampsia: a brief review, Stroke, 40, 1169-1175, (2009)
[19] Fawcett, W. J.; Haxby, E. J.; Male, D. A., Magnesium: physiology and pharmacology, Br. J. Anaesth., 83, 302-320, (1999)
[20] Ferru, E.; Giger, K.; Pantaleo, A.; Campanella, E.; Grey, J.; Ritchie, K.; Vono, R.; Turrini, F.; Low, P. S., Regulation of membrane-cytoskeletal interactions by tyrosine phosphorylation of erythrocyte band 3, Blood, 117, 5998-6006, (2011)
[21] Flatman, P. W., Mechanisms of magnesium transport, Annu. Rev. Physiol., 53, 259-271, (1991)
[22] Gill, P. E.; Murray, W., Algorithms for the solution of the nonlinear least-squares problem, SIAM J. Numer. Anal., 15, 977-992, (1978) · Zbl 0401.65042
[23] Grubbs, R. D., Intracellular magnesium and magnesium buffering, BioMetals, 15, 251-259, (2002)
[24] Gulczynska, E.; Gadzinowski, J.; Wilczynski, J.; Zylinska, L., Prenatal mgso4 treatment modifies the erythrocyte band 3 in preterm neonates, Pharmacol. Res., 53, 347-352, (2006)
[25] Gunther, T., Total and free mg^2+ contents in erythrocytes: a simple but still undisclosed cell model, Magnes Res, 20, 161-167, (2007)
[26] Gupta, R. K.; Benovic, J. L.; Rose, Z. B., The determination of the free magnesium level in the human red blood cell by 31P NMR, J. Biol. Chem., 253, 6172-6176, (1978)
[27] Guyton, A. C.; Hall, J. E., Textbook of medical physiology, (2006), Elsevier Saunders Philadelphia
[28] Harrison, M. L.; Isaacson, C. C.; Burg, D. L.; Geahlen, R. L.; Low, P. S., Phosphorylation of human erythrocyte band 3 by endogenous p72syk, J. Biol. Chem., 269, 955-959, (1994)
[29] Hoffmann, J. J.; van den Broek, N. M.; Curvers, J., Reference intervals of extended erythrocyte and reticulocyte parameters, Clin. Chem. Lab. Med., 50, 941-948, (2012)
[30] Idama, T. O.; Lindow, S. W., Magnesium sulphate: a review of clinical pharmacology applied to obstetrics, Br. J. Obstet. Gynaecol., 105, 260-268, (1998)
[31] Kummerow, D.; Hamann, J.; Browning, J. A.; Wilkins, R.; Ellory, J. C.; Bernhardt, I., Variations of intracellular ph in human erythrocytes via K^+(na^+)/H^+ exchange under low ionic strength conditions, J. Membr. Biol., 176, 207-216, (2000)
[32] Loer, S. A.; Scheeren, T. W.; Tarnow, J., How much oxygen does the human lung consume?, Anesthesiology, 86, 532-537, (1997)
[33] Maltsev, V. P., Scanning flow cytometry for individual particle analysis, Rev. Sci. Instrum., 71, 243-255, (2000)
[34] McLean, R. M., Magnesium and its therapeutic uses: a review, Am. J. Med., 96, 63-76, (1994)
[35] Merciris, P.; Hardy-Dessources, M. D.; Sauvage, M.; Giraud, F., Involvement of deoxygenation-induced increase in tyrosine kinase activity in sickle cell dehydration, Pflug. Arch., 436, 315-322, (1998)
[36] Michelet-Habchi, C.; Barberet, P.; Dutta, R.; Moretto, P.; Guiet-Bara, A.; Bara, M., Elemental maps in human allantochorial placental vessels cells. 2. mgcl_2 and mgso_4 effects, Magnes Res, 16, 171-175, (2003)
[37] Minetti, G.; Ciana, A.; Balduini, C., Differential sorting of tyrosine kinases and phosphotyrosine phosphatases acting on band 3 during vesiculation of human erythrocytes, Biochem. J., 377, 489-497, (2004)
[38] Minetti, G.; Seppi, C.; Ciana, A.; Balduini, C.; Low, P. S.; Brovelli, A., Characterization of the hypertonically induced tyrosine phosphorylation of erythrocyte band 3, Biochem. J., 335, 305-311, (1998)
[39] Mittendorf, R.; Roizen, N. J.; Pryde, P. G., The risks of extending the controversial use of tocolytic magnesium sulfate for the purpose of neuroprotection in preterm labor, J. Perinatol., 24, 465-466, (2004)
[40] Mittendorf, R.; Dambrosia, J.; Pryde, P. G.; Lee, K. S.; Gianopoulos, J. G.; Besinger, R. E.; Tomich, P. G., Association between the use of antenatal magnesium sulfate in preterm labor and adverse health outcomes in infants, Am. J. Obstet. Gynecol., 186, 1111-1118, (2002)
[41] Murata, Y.; Itakura, A.; Matsuzawa, K.; Okumura, A.; Wakai, K.; Mizutani, S., Possible antenatal and perinatal related factors in development of cystic periventricular leukomalacia, Brain Dev., 27, 17-21, (2005)
[42] Poole, J., Red cell antigens on band 3 and glycophorin A, Blood Rev., 14, 31-43, (2000)
[43] Puceat, M.; Roche, S.; Vassort, G., Src family tyrosine kinase regulates intracellular ph in cardiomyocytes, J. Cell Biol., 141, 1637-1646, (1998)
[44] Raftos, J. E.; Lew, V. L.; Flatman, P. W., Refinement and evaluation of a model of mg^2+ buffering in human red cells, Eur. J. Biochem., 263, 635-645, (1999)
[45] Shvalov, A. N.; Soini, J. T.; Chernyshev, A. V.; Tarasov, P. A.; Soini, E.; Maltsev, V. P., Light-scattering properties of individual erythrocytes, Appl. Opt., 38, 230-235, (1999)
[46] Strokotov, D. I.; Moskalensky, A. E.; Nekrasov, V. M.; Maltsev, V. P., Polarized light-scattering profile-advanced characterization of nonspherical particles with the scanning flow cytometry, Cytom. A, 79A, 570-579, (2011)
[47] Sugiyama, A.; Xue, Y.; Hagihara, A.; Saitoh, M.; Hashimoto, K., Characterization of magnesium sulfate as an antiarrhythmic agent, J. Cardiovasc. Pharmacol. Ther., 1, 243-254, (1996)
[48] Swaminathan, R., Magnesium metabolism and its disorders, Clin. Biochem. Rev., 24, 47-66, (2003)
[49] Swietach, P.; Tiffert, T.; Mauritz, J. M.A.; Seear, Rachel; Esposito, Alessandro; Kaminski, C. F.; Lew, V. L.; Vaughan-Jones, R. D., Hydrogen ion dynamics in human red blood cells, J. Physiol., 588, 4995-5014, (2010)
[50] Szemraj, J.; Sobolewska, B.; Gulczynska, E.; Wilczynski, J.; Zylinska, L., Magnesium sulfate effect on erythrocyte membranes of asphyxiated newborns, Clin. Biochem., 38, 457-464, (2005)
[51] Teti, D.; Venza, I.; Crupi, M.; Busa, M.; Loddo, S.; Romano, L., Anion transport in normal erythrocytes, sickle red cells, and ghosts in relation to hemoglobins and magnesium, Arch. Biochem. Biophys., 403, 149-154, (2002)
[52] Ulger, Z.; Ariogul, S.; Cankurtaran, M.; Halil, M.; Yavuz, B. B.; Orhan, B.; Kavas, G. O.; Aribal, P.; Canlar, S.; Dede, D. S.; Ozkayar, N.; Akyol, O., Intra-erythrocyte magnesium levels and their clinical implications in geriatric outpatients, J. Nutr. Health Aging, 14, 810-814, (2010)
[53] Vasseur, C.; Piau, J. P.; Bursaux, E., Cation dependence of the phosphorylation of specific residues in red cell membrane protein band 3, Biochim. Biophys. Acta, 899, 1-8, (1987)
[54] von Ruckmann, B.; Schubert, D., The complex of band 3 protein of the human erythrocyte membrane and glyceraldehyde-3-phosphate dehydrogenase: stoichiometry and competition by aldolase, Biochim. Biophys. Acta, 1559, 43-55, (2002)
[55] Weber, R. E.; Voelter, W., ‘novel’ factors that regulate oxygen binding in vertebrate hemoglobins, Micron, 35, 45-46, (2004)
[56] Weber, R. E.; Voelter, W.; Fago, A.; Echner, H.; Campanella, E.; Low, P. S., Modulation of red cell glycolysis: interactions between vertebrate hemoglobins and cytoplasmic domains of band 3 red cell membrane proteins, Am. J. Physiol. Regul. Integr. Comp. Physiol., 287, R454-R464, (2004)
[57] Wheeler, K. A., Computer software reviews, J. Am. Chem. Soc., 115, 3396, (1993), 3396
[58] Yeagle, P. L, The structure of biological membranes, (2005), CRC Press LLC USA
[59] Zhang, D.; Kiyatkin, A.; Bolin, J. T.; Low, P. S., Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3, Blood, 96, 2925-2933, (2000)
[60] Zipser, Y.; Kosower, N. S., Phosphotyrosine phosphatase associated with band 3 protein in the human erythrocyte membrane, Biochem. J., 314, 881-887, (1996)
[61] Zylinska, L.; Sobolewska, B.; Gulczynska, E.; Ochedalski, T.; Soszynski, M., Protein kinases activities in erythrocyte membranes of asphyxiated newborns, Clin. Biochem., 35, 93-98, (2002)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.