Abstract
We have studied changes in the structural parameters of 1,2-dimyristoyl-sn-3-phosphocholine (DMPC) unilamellar vesicles at a concentration series 0–30 mM of divalent metal cations Ca2+, Mg2+, and Co2+ by means of small-angle neutron scattering (SANS). The membrane structural parameters (thickness and area per lipid) were obtained at different concentrations of cations in the gel and fluid phases of membrane. Both Ca2+ and Mg2+ ions at the concentrations of 0–1 mM increase the membrane thickness by 1.9 Å and 2.9 Å in the fluid and gel phase, respectively. In the concentration range of 1–30 mM, either a weak tendency to a thickness decrease of ~ 1 Å is observed, or the thickness does not change at all. In the case of Co2+ ions, all changes are extremely weak. We advocate a model of electrostatic interactions for these systems that encompasses the formation of ion bridges between lipid headgroups. Using the Langmuir adsorption isotherm we estimate the fraction of Ca2+ ions bound to the DMPC membrane. The developed model is of an interest to the future studies of membrane interactions with various charged peptides, such as those from the amyloid-β family.
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REFERENCES
G. Pabst, N. Kučerka, M.-P. Nieh, M. C. Rheinstädter, and J. Katsaras, Chem. Phys. Lipids 163, 460 (2010). https://doi.org/10.1016/j.chemphyslip.2010.03.010
B. Alberts, A. Johnson, J. Lewis, D. Morgan, M. Raff, K. Roberts, and P. Walter, Molecular Biology of the Cell (Garland Science, New York, 2015).
P. Lo Nostro and B. W. Ninham, Chem. Rev. 112, 2286 (2012). https://doi.org/10.1021/cr200271j
S. A. Tatulian, Eur. J. Biochem. 170, 413 (1987). https://doi.org/10.1111/j.1432-1033.1987.tb13715.x
N. Kučerka, E. Papp-Szabo, M.-P. Nieh, T. A. Harroun, S. R. Schooling, J. Pencer, E. A. Nicholson, T. J. Beveridge, and J. Katsaras, J. Phys. Chem. B 112, 8057 (2008). https://doi.org/10.1021/jp8027963
J. A. Beto, Clin. Nutr. Res. 4, 1 (2015). https://doi.org/10.7762/cnr.2015.4.1.1
U. Gröber, J. Schmidt, and K. Kisters, Nutrients 7, 8199 (2015). https://doi.org/10.3390/nu7095388
G. Bánfalvi, Heavy metals, trace elements and their cellular effects, in Cellular Effects of Heavy Metals, Ed. by G. Bánfalvi (Springer, Amsterdam, Netherlands, 2011), p. 3. https://doi.org/10.1007/978-94-007-0428-2_1
H. I. Petrache, T. Zemb, L. Belloni, and V. A. Parsegian, Proc. Natl. Acad. Sci. U. S. A. 103, 7982 (2006). https://doi.org/10.1073/pnas.0509967103
L. J. Lis, W. T. Lis, V. A. Parsegian, and R. P. Rand, Biochemistry 20, 1771 (1981). https://doi.org/10.1021/bi00510a010
C. G. Sinn, M. Antonietti, and R. Dimova, Colloids Surf., A 282, 410 (2006). https://doi.org/10.1016/j.colsurfa.2005.10.014
A. Lee, Biochim. Biophys. Acta 1666, 62 (2004). https://doi.org/10.1016/j.bbamem.2004.05.012
N. Kučerka, M.-P. Nieh, J. Pencer, J. N. Sachs, and J. Katsaras, Gen. Physiol. Biophys. 28, 117 (2009). https://doi.org/10.4149/gpb_2009_02_117
D. Uhríková, N. Kučerka, J. Teixeira, V. Gordeliy, and P. Balgavý, Chem. Phys. Lipids 155, 80 (2008). https://doi.org/10.1016/j.chemphyslip.2008.07.010
N. Kučerka, J. Pencer, J. N. Sachs, J. F. Nagle, and J. Katsaras, Langmuir 23, 1292 (2007). https://doi.org/10.1021/la062455t
A. I. Kuklin, D. V. Soloviev, A. V. Rogachev, P. K. Utrobin, Y. S. Kovalev, M. Balasoiu, O. I. Ivankov, A. P. Sirotin, T. N. Murugova, T. B. Petukhova, Y. E. Gorshkova, R. V. Erhan, S. A. Kutuzov, A. G. Soloviev, and V. I. Gordelii, J. Phys.: Conf. Ser. 291, 7 (2011). https://doi.org/10.1088/1742-6596/291/1/012013
A. I. Kuklin, A. D. Rogov, Y. E. Gorshkova, P. K. Utrobin, Y. S. Kovalev, A. V. Rogachev, O. I. Ivankov, S. A. Kutuzov, D. V. Soloviov, and V. I. Gordeliy, Phys. Part. Nucl. Lett. 8, 119 (2011). https://doi.org/10.1134/S1547477111020075
A. G. Soloviev, T. M. Solovjeva, O. I. Ivankov, D. V. Soloviov, A. V. Rogachev, and A. I. Kuklin, J. Phys.: Conf. Ser. 848, 7 (2017). https://doi.org/10.1088/1742-6596/848/1/012020
L. A. Feigin and D. I. Svergun, Structure Analysis by Small-Angle X-Ray and Neutron Scattering (Springer, New York, 1987). https://doi.org/10.1007/978-1-4757-6624-0
M. A. Kiselev, D. Lombarde, A. M. Kiselev, P. Lezi, and V. L. Aksenov, Poverkhn.: Rentgenovskie, Sinkhrotronnye Neitr. Issled., No. 11, 24 (2003).
N. Kučerka, M. A. Kiselev, and P. Balgavý, Eur. Biophys. J. 33, 328 (2004). https://doi.org/10.1007/s00249-003-0349-0
G. Fournet, Small-Angle Scattering of X-Rays (Wiley, New York, 1955).
SasView (2020). Sas View for Small Angle Scattering Analysis. https://www.sasview.org/. Cited May 25, 2020.
Yu. E. Gorshkova, PhD. Dissertation in Mathematics and Physics (Joint Inst. Nucl. Res., Dubna, 2017).
J. F. Nagle and S. Tristram-Nagle, Biochim. Biophys. Acta 1469, 159 (2000). https://doi.org/10.1016/S0304-4157(00)00016-2
J. F. Nagle and D. A. Wilkinson, Biophys. J. 23, 159 (1978). https://doi.org/10.1016/S0006-3495(78)85441-1
N. Kučerka, S. Tristram-Nagle, and J. F. Nagle, J. Membr. Biol. 208, 193 (2005). https://doi.org/10.1007/s00232-005-7006-8
N. Kučerka, E. Dushanov, K. T. Kholmurodov, J. Katsaras, and D. Uhríková, Langmuir 33, 3134 (2017). https://doi.org/10.1021/acs.langmuir.6b03228
J. Seelig, Cell Biol. Int. Rep. 14, 353 (1990). https://doi.org/10.1016/0309-1651(90)91204-H
Y. Izumitani, J. Colloid Interface Sci. 166, 143 (1994). https://doi.org/10.1006/jcis.1994.1281
D. Huster, G. Paasche, U. Dietrich, O. Zschörnig, T. Gutberlet, K. Gawrisch, and K. Arnold, Biophys. J. 77, 879 (1999). https://doi.org/10.1016/S0006-3495(99)76939-0
R. Zidovetzki, A. W. Atiya, and H. De Boeck, Membr. Biochem. 8, 177 (1989). https://doi.org/10.3109/09687688909025830
H. Binder and O. Zschörnig, Chem. Phys. Lipids 115, 39 (2002). https://doi.org/10.1016/S0009-3084(02)00005-1
C. T. M. Le, A. Houri, N. Balage, B. J. Smith, and A. Mechler, Front. Mater. 5, 1 (2019). https://doi.org/10.3389/fmats.2018.00080
S. De Kanti, N. Kanwa, V. Ahamed, and A. Chakraborty, Phys. Chem. Chem. Phys. 20, 14796 (2018). https://doi.org/10.1039/c8cp01774c
J. Yang, C. Calero, M. Bonomi, and J. Marti, J. Chem. Theory Comput. 11, 4495 (2015). https://doi.org/10.1021/acs.jctc.5b00540
M. Javanainen, A. Melcrová, A. Magarkar, Z. P. Jurkiewic, M. Hof, P. Jungwirth, and H. Martinez-Seara, Chem. Commun. 53, 5380 (2017). https://doi.org/10.1039/c7cc02208e
C. Scomparin, S. Lecuyer, M. Ferreira, T. Charitat, and B. Tinland, Eur. Phys. J. E 28, 211 (2009). https://doi.org/10.1140/epje/i2008-10407-3
H. A. Stern and S. E. Feller, J. Chem. Phys. 118, 3401 (2003). https://doi.org/10.1063/1.1537244
J. M. Moore, Physical Chemistry, 4th ed. (Prentice-Hall, Englewood Cliffs, NJ, 1972).
K. Satoh, Biochim. Biophys. Acta 1239, 239 (1995). https://doi.org/10.1016/0005-2736(95)00154-U
C. Altenbach and J. Seelig, Biochemistry 23, 3913 (1984). https://doi.org/10.1021/bi00312a019
E. Chibowski and A. Szcześ, Adsorption 22, 755 (2016). https://doi.org/10.1007/s10450-016-9767-z
A. McLaughlin, C. Grathwohl, and S. McLaughlin, Biochim. Biophys. Acta 513, 338 (1978). https://doi.org/10.1016/0005-2736(78)90203-1
J. Umbsaar, E. Kerek, and E. J. Prenner, Chem. Phys. Lipids 210, 28 (2018). https://doi.org/10.1016/j.chemphyslip.2017.11.016
E. Eriksson, Principles and Applications of Hydrochemistry (Springer, Amsterdam, 1985). https://doi.org/10.1007/978-94-009-4836-5
F. David, V. Vokhmin, and G. Ionova, J. Mol. Liq. 90, 45 (2001). https://doi.org/10.1016/S0167-7322(01)00106-4
Y. Marcus, J. Chem. Soc., Faraday Trans. 87, 2995 (1991). https://doi.org/10.1039/FT9918702995
H. Ohtaki and T. Radnai, Chem. Rev. 93, 1157 (1993). https://doi.org/10.1021/cr00019a014
H. Ohtaki and H. Yamatera, Structure and Dynamics of Solutions (Elsevier, Oxford, 1992).
I. Bertini, C. Luchinat, G. Parigi, and E. Ravera, NMR of Paramagnetic Molecules: Applications to Metallobiomolecules and Models, 2nd ed. (Elsevier, Amsterdam, 2016).
R. Crichton, Biological Inorganic Chemistry: A New Introduction to Molecular Structure and Function, 3rd ed. (Elsevier, Amsterdam, 2018).
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This study was supported by the Russian Science Foundation (grant no. 19-72-20 186).
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Kurakin, S.A., Ermakova, E.V., Ivankov, A.I. et al. The Effect of Divalent Ions on the Structure of Bilayers in the Dimyristoylphosphatidylcholine Vesicles. J. Surf. Investig. 15, 211–220 (2021). https://doi.org/10.1134/S1027451021020075
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DOI: https://doi.org/10.1134/S1027451021020075