Abstract
Metal pollutants are a growing concern due to increased use in mining and other industrial processes. Moreover, the use of metals in daily life is becoming increasingly prevalent. Metals such as manganese (Mn), cobalt (Co), and nickel (Ni) are toxic in high amounts whereas lead (Pb) and cadmium (Cd) are acutely toxic at low µM concentrations. These metals are associated with system dysfunction in humans including cancer, neurodegenerative diseases, Alzheimer’s disease, Parkinson’s disease, and other cellular process’. One known but lesser studied target of these metals are lipids that are key membrane building blocks or serve signalling functions. It was shown that Mn, Co, Ni, Pb, and Cd cause rigidification of liposomes and increase the phase transition in membranes composed of both saturated or partly unsaturated phosphatidic acid (PA) and phosphatidylserine (PS). The selected metals showed differential effects that were more pronounced on saturated lipids. In addition, more rigidity was induced in the biologically relevant liquid-crystalline phase. Moreover, metal affinity, induced rigidification and liposome size increases also varied with the headgroup architecture, whereby the carboxyl group of PS appeared to play an important role. Thus, it can be inferred that Mn, Co, Ni, Cd, and Pb may have preferred binding coordination with the lipid headgroup, degree of acyl chain unsaturation, and membrane phase.
Similar content being viewed by others
References
Al Osman M, Yang F, Massey IY (2019) Exposure routes and health effects of heavy metals on children. Biometals 32(4):563–573. https://doi.org/10.1007/S10534-019-00193-5/METRICS
Allred AL (1961) Electronegativity values from thermochemical data. J Inorg Nucl Chem 17(3–4):215–221. https://doi.org/10.1016/0022-1902(61)80142-5
Alsop RJ, Maria Schober R, Rheinstädter MC (2016) Swelling of phospholipid membranes by divalent metal ions depends on the location of the ions in the bilayers. Soft Matter 12(32):6737–6748. https://doi.org/10.1039/C6SM00695G
Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8(C):115–118. https://doi.org/10.1016/0076-6879(66)08014-5
Ammendolia DA, Bement WM, Brumell JH (2021) Plasma membrane integrity: implications for health and disease. BMC Biol 19(1):1–29. https://doi.org/10.1186/S12915-021-00972-Y
Andruska KM, Racette BA (2015) Neuromythology of manganism. Curr Epidemiol Rep 2(2):143. https://doi.org/10.1007/S40471-015-0040-X
Balali-Mood M, Naseri K, Tahergorabi Z, Khazdair MR, Sadeghi M (2021) Toxic mechanisms of five heavy metals: mercury, lead, chromium, cadmium, and arsenic. Front Pharmacol 12:643972. https://doi.org/10.3389/FPHAR.2021.643972
Barceloux DG (1999a) Cobalt. J Toxicol Clin Toxicol 37(2):201–216. https://doi.org/10.1081/CLT-100102420
Barceloux DG (1999b) Nickel. J Toxicol Clin Toxicol 37(2):239–258. https://doi.org/10.1081/CLT-100102423
Battaglia V, Compagnone A, Bandino A, Bragadin M, Rossi CA, Zanetti F, Colombatto S, Grillo MA, Toninello A (2009) Cobalt induces oxidative stress in isolated liver mitochondria responsible for permeability transition and intrinsic apoptosis in hepatocyte primary cultures. Int J Biochem Cell Biol 41(3):586–594. https://doi.org/10.1016/J.BIOCEL.2008.07.012
Bazarkina EF, Pokrovski GS, Zotov AV, Hazemann JL (2010) Structure and stability of cadmium chloride complexes in hydrothermal fluids. Chem Geol 276(1–2):1–17. https://doi.org/10.1016/J.CHEMGEO.2010.03.006
Bevers EM, Williamson PL (2016) Getting to the outer leaflet: physiology of phosphatidylserine exposure at the plasma membrane. Physiol Rev 96(2):605–645. https://doi.org/10.1152/physrev.00020.2015
Binder H, Zschörnig O (2002) The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem Phys Lipid 115(1–2):39–61. https://doi.org/10.1016/S0009-3084(02)00005-1
Boettcher JM, Davis-Harrison RL, Clay MC, Nieuwkoop AJ, Ohkubo YZ, Tajkhorshid E, Morrissey JH, Rienstra CM (2011) Atomic view of calcium-induced clustering of phosphatidylserine in mixed lipid bilayers. Biochemistry 50(12):2264–2273. https://doi.org/10.1021/BI1013694/ASSET/IMAGES/LARGE/BI-2010-013694_0007.JPEG
Borsari M (2014) Cadmium: coordination chemistry. Encyclopedia of inorganic and bioinorganic chemistry. Wiley, pp 1–16. https://doi.org/10.1002/9781119951438.EIBC2261
Bridges CC, Zalups RK (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204(3):274–308. https://doi.org/10.1016/J.TAAP.2004.09.007
Casalino E, Calzaretti G, Sblano C, Landriscina C (2002) Molecular inhibitory mechanisms of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179(1–2):37–50. https://doi.org/10.1016/S0300-483X(02)00245-7
Chen RJ, Lee VR (2023) Cobalt toxicity. StatPearls. https://www.ncbi.nlm.nih.gov/books/NBK587403/
Costa M, Salnikow K, Sutherland JE, Broday L, Peng W, Zhang Q, Kluz T (2002) The role of oxidative stress in nickel and chromate genotoxicity. In: Vallyathan V, Shi X, Castranova V (eds) Oxygen/nitrogen radicals: cell injury and disease. Springer, Boston, MA, pp 265–275. https://doi.org/10.1007/978-1-4615-1087-1_30
Cotelle N, Trémolières E, Bernier JL, Catteau JP, Hénichart JP (1992) Redox chemistry of complexes of nickel(II) with some biologically important peptides in the presence of reduced oxygen species: an ESR study. J Inorg Biochem 46(1):7–15. https://doi.org/10.1016/0162-0134(92)80058-4
Czarnek K, Terpilowska S, Siwicki AK (2015) Selected aspects of the action of cobalt ions in the human body. Cent Eur J Immunol 40(2):236–242. https://doi.org/10.5114/CEJI.2015.52837
Daear W, Mundle R, Sule K, Prenner EJ (2021) The degree and position of phosphorylation determine the impact of toxic and trace metals on phosphoinositide containing model membranes. BBA Adv 1:100021. https://doi.org/10.1016/J.BBADVA.2021.100021
Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity, and carcinogenicity. Crit Rev Oncol Hematol 42(1):35–56. https://doi.org/10.1016/S1040-8428(01)00214-1
Devaux PF (1991) Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30(5):1163–1173
Dickey A, Faller R (2008) Examining the contributions of lipid shape and headgroup charge on bilayer behavior. Biophys J 95(6):2636–2646. https://doi.org/10.1529/biophysj.107.128074
Dorta DJ, Leite S, DeMarco KC, Prado IMR, Rodrigues T, Mingatto FE, Uyemura SA, Santos AC, Curti C (2003) A proposed sequence of events for cadmium-induced mitochondrial impairment. J Inorg Biochem 97(3):251–257. https://doi.org/10.1016/S0162-0134(03)00314-3
Engwa GA, Ferdinand PU, Nwalo FN, Unachukwu MN, Engwa GA, Ferdinand PU, Nwalo FN, Unachukwu MN (2019) Mechanism and health effects of heavy metal toxicity in humans. Poisoning in the modern world—new tricks for an old dog? IntechOpen, Croatia. https://doi.org/10.5772/INTECHOPEN.82511
Fadok VA, Henson PM (1998) Apoptosis: getting rid of the bodies. Curr Biol 8(19):R693–R695. https://doi.org/10.1016/S0960-9822(98)70438-5
Ferreira CMH, Pinto ISS, Soares EV, Soares HMVM (2015) (Un)suitability of the use of pH buffers in biological, biochemical and environmental studies and their interaction with metal ions—a review. RSC Adv 5(39):30989–31003. https://doi.org/10.1039/C4RA15453C
Finley JW, Davis CD (1999) Manganese deficiency and toxicity: are high or low dietary amounts of manganese cause for concern? BioFactors 10(1):15–24. https://doi.org/10.1002/BIOF.5520100102
Genchi G, Carocci A, Lauria G, Sinicropi MS, Catalano A (2020) Nickel: human health and environmental toxicology. Int J Environ Res Public Health 17(3):679. https://doi.org/10.3390/IJERPH17030679
Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol 1(1):1–6. https://doi.org/10.1186/1745-6673-1-22/TABLES/1
Harlos K, Eibl H, Pascher I, Sundell S (1984) Conformation and packing properties of phosphatidic acid: the crystal structure of monosodium dimyristoylphosphatidate. Chem Phys Lipid 34(2):115–126. https://doi.org/10.1016/0009-3084(84)90037-9
Hartwig A (1998) Carcinogenicity of metal compounds: possible role of DNA repair inhibition. Toxicol Lett 102–103:235–239. https://doi.org/10.1016/S0378-4274(98)00312-9
Hassanin M, Kerek E, Chiu M, Anikovskiy M, Prenner EJ (2016) Binding affinity of inorganic mercury and cadmium to biomimetic erythrocyte membranes. J Phys Chem B 120(50):12872–12882. https://doi.org/10.1021/acs.jpcb.6b10366
Huff J, Lunn RM, Waalkes MP, Tomatis L, Infante PF (2007) Cadmium-induced cancers in animals and in humans. Int J Occup Environ Health 13(2):202. https://doi.org/10.1179/OEH.2007.13.2.202
Ismael MA, Elyamine AM, Moussa MG, Cai M, Zhao X, Hu C (2019) Cadmium in plants: uptake, toxicity, and its interactions with selenium fertilizers. Metallomics 11(2):255–277. https://doi.org/10.1039/C8MT00247A
Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60. https://doi.org/10.2478/INTOX-2014-0009
Jezierska B, Witeska M (2006) The metal uptake and accumulation in fish living in polluted waters. Soil and water pollution monitoring, protection and remediation. Springer, Dordrecht, pp 107–114. https://doi.org/10.1007/978-1-4020-4728-2_6
Kaiser RD, London E (1998) Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth. Biochemistry 37(22):8180–8190. https://doi.org/10.1021/bi980064a
Kerek EM, Prenner EJ (2016) Inorganic cadmium affects the fluidity and size of phospholipid based liposomes. Biochim Biophys Acta BBA Biomembr 1858(12):3169–3181. https://doi.org/10.1016/J.BBAMEM.2016.10.005
Kim EJ, Herrera JE, Huggins D, Braam J, Koshowski S (2011) Effect of pH on the concentrations of lead and trace contaminants in drinking water: a combined batch, pipe loop and sentinel home study. Water Res 45(9):2763–2774. https://doi.org/10.1016/J.WATRES.2011.02.023
Kim HY, Huang BX, Spector AA (2014) Phosphatidylserine in the brain: metabolism and function. Prog Lipid Res. https://doi.org/10.1016/J.PLIPRES.2014.06.002
Kooijman EE, Burger KNJ (2009) Biophysics and function of phosphatidic acid: a molecular perspective. Biochim Biophys Acta Mol Cell Biol Lipids 1791(9):881–888. https://doi.org/10.1016/j.bbalip.2009.04.001
Kooijman EE, Tieleman DP, Testerink C, Munnik T, Rijkers DTS, Burger KNJ, De Kruijff B (2007) An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. J Biol Chem 282(15):11356–11364. https://doi.org/10.1074/jbc.M609737200
Kozak K, Antosiewicz DM (2023) Tobacco as an efficient metal accumulator. Biometals 36(2):351–370. https://doi.org/10.1007/S10534-022-00431-3
Küpper H, Andresen E (2016) Mechanisms of metal toxicity in plants. Metallomics 8(3):269–285. https://doi.org/10.1039/C5MT00244C
Lee YW, Broday L, Costa M (1998) Effects of nickel on DNA methyltransferase activity and genomic DNA methylation levels. Mutat Res 415(3):213–218. https://doi.org/10.1016/S1383-5718(98)00078-3
Lewis RNAH, McElhaney RN (2000) Calorimetric and spectroscopic studies of the thermotropic phase behavior of lipid bilayer model membranes composed of a homologous series of linear saturated phosphatidylserines. Biophys J 79(4):2043–2055. https://doi.org/10.1016/S0006-3495(00)76452-6
Leyssens L, Vinck B, Van Der Straeten C, Wuyts F, Maes L (2017) Cobalt toxicity in humans—a review of the potential sources and systemic health effects. Toxicology 387:43–56. https://doi.org/10.1016/J.TOX.2017.05.015
Mah V, Jalilehvand F (2012) Lead(II) complex formation with glutathione. Inorg Chem 51(11):6285–6298. https://doi.org/10.1021/IC300496T/SUPPL_FILE/IC300496T_SI_001.PDF
Mansour HM, Zografi G (2007) The relationship between water vapor absorption and desorption by phospholipids and bilayer phase transitions. J Pharm Sci 96(2):377–396. https://doi.org/10.1002/JPS.20810
Mao JS, Dong J, Graedel TE (2008) The multilevel cycle of anthropogenic lead: I. Methodology. Resour Conserv Recycl 52(8–9):1058–1064. https://doi.org/10.1016/J.RESCONREC.2008.04.004
Marquardt D, Geier B, Pabst G (2015) Asymmetric lipid membranes: towards more realistic model systems. Membranes 5(2):180–196. https://doi.org/10.3390/membranes5020180
Martinez-Finley EJ, Chakraborty S, Fretham SJB, Aschner M (2012) Cellular transport and homeostasis of essential and nonessential metals. Metallomics 4(7):593–605. https://doi.org/10.1039/C2MT00185C
Mattai J, Hauser H, Demel RA, Shipley GG (1989) Interactions of metal ions with phosphatidylserine bilayer membranes: effect of hydrocarbon chain unsaturation. Biochemistry 28(5):2322–2330. https://doi.org/10.1021/BI00431A051/ASSET/BI00431A051.FP.PNG_V03
McLaughlin AC (1982) Phosphorus-31 and carbon-13 nuclear magnetic resonance studies of divalent cation binding to phosphatidylserine membranes: use of cobalt as a paramagnetic probe. Biochemistry 21(20):4879–4885. https://doi.org/10.1021/BI00263A008/ASSET/BI00263A008.FP.PNG_V03
Miller AB (1996) Review of extant community-based epidemiologic studies on health effects of hazardous wastes. Toxicol Ind Health 12(2):225–233
Mondal Roy S, Sarkar M (2011) Membrane fusion induced by small molecules and ions. J Lipids 2011:1–14. https://doi.org/10.1155/2011/528784
Nickel, its adverse health effects & oxidative stress—PubMed. (n.d.). https://pubmed.ncbi.nlm.nih.gov/19106437/. Accessed 16 Jul 2023
Nowicka B (2022) Heavy metal-induced stress in eukaryotic algae—mechanisms of heavy metal toxicity and tolerance with particular emphasis on oxidative stress in exposed cells and the role of antioxidant response. Environ Sci Pollut Res 29(12):16860–16911. https://doi.org/10.1007/S11356-021-18419-W
Papavasiliou PS, Miller ST, Cotzias GC (1966) Role of liver in regulating distribution and excretion of manganese. Am J Physiol 211(1):211–216. https://doi.org/10.1152/AJPLEGACY.1966.211.1.211
Parasassi T, Krasnowska EK, Bagatolli L, Gratton E (1998) Laurdan and Prodan as polarity-sensitive fluorescent membrane probes. J Fluoresc 8(4):365–373
Payliss BJ, Hassanin M, Prenner EJ (2015) The structural and functional effects of Hg(II) and Cd(II) on lipid model systems and human erythrocytes: a review. Chem Phys Lipid 193:36–51. https://doi.org/10.1016/J.CHEMPHYSLIP.2015.09.009
Puskin JS, Coene MT (1980) Na+ and H+ dependent Mn2+ binding to phosphatidylserine vesicles as a test of the Gouy-Chapman-Stern theory. J Membr Biol 52(1):69–74. https://doi.org/10.1007/BF01869007
Ragsdale SW (2009) Nickel-based enzyme systems. J Biol Chem 284(28):18571–18575. https://doi.org/10.1074/JBC.R900020200
Roth J, Ponzoni S, Aschner M (2013) Manganese homeostasis and transport. Met Ions Life Sci 12:169. https://doi.org/10.1007/978-94-007-5561-1_6
Roux M, Neumann JM, Bloom M, Devaux PF (1988) 2H and 31P NMR study of pentalysine interaction with headgroup deuterated phosphatidylcholine and phosphatidylserine. Eur Biophys J 16(5):267–273. https://doi.org/10.1007/BF00254062/METRICS
Sanchez SA, Tricerri MA, Gunther G, Gratton E (2007) Laurdan generalized polarization: from cuvette to microscope. Modern research and educational topics in microscopy. FORMATEX, pp 1007–1014
Sánchez-Migallón MP, Aranda FJ, Gómez-Fernández JC (1996) The interaction of alpha-tocopherol with phosphatidylserine vesicles and calcium. Biochem Biophys Acta 1281(1):23–30. https://doi.org/10.1016/0005-2736(95)00300-2
Sigel A, Sigel H, Sigel RKO (eds) (2013) Interrelations between essential metal ions and human diseases, vol 13. Springer, Dordrecht
Simonsen LO, Harbak H, Bennekou P (2012) Cobalt metabolism and toxicology—a brief update. Sci Total Environ 432:210–215. https://doi.org/10.1016/J.SCITOTENV.2012.06.009
Singh N, Kumar A, Gupta VK, Sharma B (2018) Biochemical and molecular bases of lead-induced toxicity in mammalian systems and possible mitigations. Chem Res Toxicol 31(10):1009–1021. https://doi.org/10.1021/ACS.CHEMRESTOX.8B00193
Smith DW (1977) Ionic hydration enthalpies. J Chem Educ 54(9):540–542. https://doi.org/10.1021/ED054P540
Song X, Fiati Kenston SS, Kong L, Zhao J (2017) Molecular mechanisms of nickel induced neurotoxicity and chemoprevention. Toxicology 392:47–54. https://doi.org/10.1016/J.TOX.2017.10.006
Spiechowicz E, Glantz PO, Axell T, Grochowski P (1999) A long-term follow-up of allergy to nickel among fixed prostheses wearers. Eur J Prosthodont Restor Dentistry 7(2):41–44. https://europepmc.org/article/med/10865378
Sule K, Prenner EJ (2022) Lipid headgroup and side chain architecture determine manganese-induced dose dependent membrane rigidification and liposome size increase. Eur Biophys J 51(3):205–223. https://doi.org/10.1007/S00249-022-01589-X
Sule K, Umbsaar J, Prenner EJ (2020) Mechanisms of Co, Ni, and Mn toxicity: from exposure and homeostasis to their interactions with and impact on lipids and biomembranes. Biochim Biophys Acta Biomembr 1862(8):183250. https://doi.org/10.1016/J.BBAMEM.2020.183250
Sule K, Anikovskiy M, Prenner EJ (2023) Lipid structure determines the differential impact of single metal additions and binary mixtures of manganese, calcium and magnesium on membrane fluidity and liposome size. Int J Mol Sci 24(2):1066. https://doi.org/10.3390/IJMS24021066/S1
Tanguy E, Wang Q, Moine H, Vitale N (2019) Phosphatidic acid: from pleiotropic functions to neuronal pathology. Front Cell Neurosci 13:2. https://doi.org/10.3389/FNCEL.2019.00002/BIBTEX
Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Exp Suppl 101:133–164. https://doi.org/10.1007/978-3-7643-8340-4_6/COVER
Thévenod F (2009) Cadmium and cellular signaling cascades: to be or not to be? Toxicol Appl Pharmacol 238(3):221–239. https://doi.org/10.1016/J.TAAP.2009.01.013
Thévenod F, Lee WK (2013) Cadmium and cellular signaling cascades: interactions between cell death and survival pathways. Arch Toxicol 87(10):1743–1786. https://doi.org/10.1007/S00204-013-1110-9/FIGURES/1
Tilcock CPS, Cullis PR (1981) The polymorphic phase behavior of mixed phosphatidylserine-phosphatidylethanolamine model systems as detected by 31P-NMR. Effects of divalent cations and pH. Biochim Biophys Acta Biomembr 641(1):189–201. https://doi.org/10.1016/0005-2736(81)90583-6
van Dijck PWM, de Kruijff B, Verkleij AJ, van Deenen LLM, de Gier J (1978) Comparative studies on the effects of pH and Ca2+ on bilayers of various negatively charged phospholipids and their mixtures with phosphatidylcholine. Biochem Biophys Acta 512(1):84–96. https://doi.org/10.1016/0005-2736(78)90219-5
Van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112–124. https://doi.org/10.1038/nrm2330
Vernier PT, Ziegler MJ, Dimova R (2009) Calcium binding and head group dipole angle in phosphatidylserine-phosphatidylcholine bilayers. Langmuir 25(2):1020–1027. https://doi.org/10.1021/LA8025057/SUPPL_FILE/LA8025057_SI_002.MPG
Vest RS, Gonzales LJ, Permann SA, Spencer E, Hansen LD, Judd AM, Bell JD (2004) Divalent cations increase lipid order in erythrocytes and susceptibility to secretory phospholipase A2. Biophys J 86(4):2251–2260. https://doi.org/10.1016/S0006-3495(04)74283-6
Visual MINTEQ (n.d.) Visual MINTEQ—a free equilibrium speciation model. https://vminteq.lwr.kth.se/. Accessed 7 Aug 2023
Waalkes MP (2003) Cadmium carcinogenesis. Mutat Res 533(1–2):107–120. https://doi.org/10.1016/J.MRFMMM.2003.07.011
Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Prog Lipid Res 45(3):250–278. https://doi.org/10.1016/j.plipres.2006.01.005
Xiao CQ, Huang Q, Zhang Y, Zhang HQ, Lai L (2020) Binding thermodynamics of divalent metal ions to several biological buffers. Thermochim Acta 691:178721. https://doi.org/10.1016/J.TCA.2020.178721
Xu SC, He MD, Zhong M, Zhang YW, Wang Y, Yang L, Yang J, Yu ZP, Zhou Z (2010) Melatonin protects against nickel-induced neurotoxicity in vitro by reducing oxidative stress and maintaining mitochondrial function. J Pineal Res 49(1):86–94. https://doi.org/10.1111/J.1600-079X.2010.00770.X
Yamniuk AP, Vogel HJ (2009) Calcium- and magnesium-dependent interactions between calcium- and integrin-binding protein and the integrin αIIb cytoplasmic domain. Protein Sci 14(6):1429–1437. https://doi.org/10.1110/ps.041312805
Zilbermann I, Maimon E, Cohen H, Meyerstein D (2005) Redox chemistry of nickel complexes in aqueous solutions. Chem Rev 105(6):2609–2625. https://doi.org/10.1021/CR030717F/ASSET/IMAGES/LARGE/CR030717FF28.JPEG
Funding
This work is supported by an NSERC Discovery Grant to EJP.
Author information
Authors and Affiliations
Contributions
Data collection: TI, KS, AML. Funding: EJP. Drafting: TI, KS, AML. Figure preparation: TI, KS. Reviewing: TI, KS, EJP.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Issler, T., Sule, K., Lewrenz, AM. et al. Differential interactions of essential and toxic metal ions with biologically relevant phosphatidic acid and phosphatidylserine membranes. Biometals 37, 631–648 (2024). https://doi.org/10.1007/s10534-023-00576-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-023-00576-9