Advertisement

Biophysical Reviews

, Volume 11, Issue 3, pp 483–490 | Cite as

Competing for the same space: protons and alkali ions at the interface of phospholipid bilayers

  • Evelyne DeplazesEmail author
  • Jacqueline White
  • Christopher Murphy
  • Charles G Cranfield
  • Alvaro GarciaEmail author
Review

Abstract

Maintaining gradients of solvated protons and alkali metal ions such as Na+ and K+ across membranes is critical for cellular function. Over the last few decades, both the interactions of protons and alkali metal ions with phospholipid membranes have been studied extensively and the reported interactions of these ions with phospholipid headgroups are very similar, yet few studies have investigated the potential interdependence between proton and alkali metal ion binding at the water–lipid interface. In this short review, we discuss the similarities between the proton–membrane and alkali ion–membrane interactions. Such interactions include cation attraction to the phosphate and carbonyl oxygens of the phospholipid headgroups that form strong lipid–ion and lipid–ion–water complexes. We also propose potential mechanisms that may modulate the affinities of these cationic species to the water–phospholipid interfacial oxygen moieties. This review aims to highlight the potential interdependence between protons and alkali metal ions at the membrane surface and encourage a more nuanced understanding of the complex nature of these biologically relevant processes.

Keywords

Protons Hydronium ions Alkali ions Ion lipid interactions Membranes Lipid bilayers 

Notes

Acknowledgements

The authors wish to acknowledge Adj Prof Bruce Cornell (UTS), Associate Prof Ron Clarke (University of Sydney), Dr Stephen Holt (Australian Nuclear Science and Technology Organisation) and Dr Paul Duckworth (eDAQ Pty Ltd) for valuable discussions on these topics.

Compliance with ethical standards

Funding

ED and AG are supported by the UTS Chancellor’s Postdoctoral Research Fellowship scheme.

Conflicts of interest

Evelyne Deplazes declares that she has no conflict of interest. Jacqueline White declares that she has no conflict of interest. Christopher Murphy declares that he has no conflict of interest. Charles G Cranfield declares that he has no conflict of interest. Alvaro Garcia declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Ädelroth P, Brzezinski P (2004) Surface-mediated proton-transfer reactions in membrane-bound proteins. BBA-Bioenergetics 1655:102–115.  https://doi.org/10.1016/j.bbabio.2003.10.018 CrossRefGoogle Scholar
  2. Agmon N et al (2016) Protons and hydroxide ions in aqueous systems. Chem Rev 116:7642–7672.  https://doi.org/10.1021/acs.chemrev.5b00736 CrossRefGoogle Scholar
  3. Akutsu H, Seelig J (1981) Interaction of metal ions with phosphatidylcholine bilayer membranes. Biochemistry 20:7366–7373CrossRefGoogle Scholar
  4. Alexiev U, Mollaaghababa R, Scherrer P, Khorana HG, Heyn MP (1995) Rapid long-range proton diffusion along the surface of the purple membrane and delayed proton transfer into the bulk. Proc Natl Acad Sci U S A 92:372–376CrossRefGoogle Scholar
  5. Amdursky N, Lin Y, Aho N, Groenhof G (2019) Exploring fast proton transfer events associated with lateral proton diffusion on the surface of membranes. Proc Natl Acad Sci U S A 116:2443.  https://doi.org/10.1073/pnas.1812351116 CrossRefGoogle Scholar
  6. Antonenko YN, Pohl P (2008) Microinjection in combination with microfluorimetry to study proton diffusion along phospholipid membranes. Eur Biophys J 37:865–870.  https://doi.org/10.1007/s00249-008-0295-y CrossRefGoogle Scholar
  7. Binder H, Zschornig O (2002) The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem Phys Lipids 115:39–61CrossRefGoogle Scholar
  8. Böckmann RA, Hac A, Heimburg T, Grubmüller H (2003) Effect of sodium chloride on a lipid bilayer. Biophys J 85:1647–1655.  https://doi.org/10.1016/S0006-3495(03)74594-9 CrossRefGoogle Scholar
  9. Boström M, Kunz W, Ninham BW (2005) Hofmeister effects in surface tension of aqueous electrolyte solution. Langmuir 21:2619–2623.  https://doi.org/10.1021/la047437v CrossRefGoogle Scholar
  10. Brändén M, Sandén T, Brzezinski P, Widengren J (2006) Localized proton microcircuits at the biological membrane-water interface. Proc Natl Acad Sci U S A 103:19766–19770.  https://doi.org/10.1073/pnas.0605909103 CrossRefGoogle Scholar
  11. Brown MF, Seelig J (1977) Ion-induced changes in head group conformation of lecithin bilayers. Nature 269:721–723.  https://doi.org/10.1038/269721a0 CrossRefGoogle Scholar
  12. Catte A et al (2016) Molecular electrometer and binding of cations to phospholipid bilayers. Phys Chem Chem Phys 18:32560–32569.  https://doi.org/10.1039/C6CP04883H CrossRefGoogle Scholar
  13. Cherepanov DA, Junge W, Mulkidjanian AY (2004) Proton transfer dynamics at the membrane/water interface: dependence on the fixed and mobile pH buffers, on the size and form of membrane particles, and on the interfacial potential barrier. Biophys J 86:665–680.  https://doi.org/10.1016/s0006-3495(04)74146-6 CrossRefGoogle Scholar
  14. Clarke RJ, Lupfert C (1999) Influence of anions and cations on the dipole potential of phosphatidylcholine vesicles: a basis for the Hofmeister effect. Biophys J 76:2614–2624.  https://doi.org/10.1016/s0006-3495(99)77414-x CrossRefGoogle Scholar
  15. Collins KD (1995) Sticky ions in biological systems. Proc Natl Acad Sci U S A 92:5553.  https://doi.org/10.1073/pnas.92.12.5553 CrossRefGoogle Scholar
  16. Cordomí A, Edholm O, Perez JJ (2008) Effect of ions on a dipalmitoyl phosphatidylcholine bilayer. A molecular dynamics simulation study. J Phys Chem B 112:1397–1408.  https://doi.org/10.1021/jp073897w CrossRefGoogle Scholar
  17. Cordomí A, Edholm O, Perez JJ (2009) Effect of force field parameters on sodium and potassium ion binding to dipalmitoyl phosphatidylcholine bilayers. J Chem Theory Comput 5:2125–2134.  https://doi.org/10.1021/ct9000763 CrossRefGoogle Scholar
  18. Cornell BA, Separovic F (1983) Membrane thickness and acyl chain length. Biochim Biophys Acta 733:189–193CrossRefGoogle Scholar
  19. Cranfield CG et al (2016) Evidence of the key role of H3O+ in phospholipid membrane morphology. Langmuir 32:10725–10734.  https://doi.org/10.1021/acs.langmuir.6b01988 CrossRefGoogle Scholar
  20. Cunningham BA, Shimotake JE, Tamura-Lis W, Mastran T, Kwok WM, Kauffman JW, Lis LJ (1986) The influence of ion species on phosphatidylcholine bilayer structure and packing. Chem Phys Lipids 39:135–143CrossRefGoogle Scholar
  21. Cunningham BA, Gelerinter E, Lis LJ (1988) Monovalent ion-phosphatidylcholine interactions: an electron paramagnetic resonance study. Chem Phys Lipids 46:205–211CrossRefGoogle Scholar
  22. Deplazes E, Poger D, Cornell B, Cranfield CG (2017) The effect of hydronium ions on the structure of phospholipid membranes. Phys Chem Chem Phys 20:357–366.  https://doi.org/10.1039/c7cp06776c CrossRefGoogle Scholar
  23. Deplazes E, Poger D, Cornell B, Cranfield CG (2018) The effect of H(3)O(+) on the membrane morphology and hydrogen bonding of a phospholipid bilayer. Biophys Rev 10:1371–1376.  https://doi.org/10.1007/s12551-018-0454-z CrossRefGoogle Scholar
  24. Gabriel B, Teissie J (1996) Proton long-range migration along protein monolayers and its consequences on membrane coupling. Proc Natl Acad Sci U S A 93:14521–14525CrossRefGoogle Scholar
  25. Gabriel B, Prats M, Teissié J (1994) Proton lateral conduction along a lipid monolayer spread on a physiological subphase. BBA-Bioenergetics 1186:172–176.  https://doi.org/10.1016/0005-2728(94)90176-7 CrossRefGoogle Scholar
  26. Gambu I, Roux B (1997) Interaction of K+ with a phospholipid bilayer: a molecular dynamics study. J Phys Chem B 101:6066–6072.  https://doi.org/10.1021/jp9640134 CrossRefGoogle Scholar
  27. Garcia A, Zou H, Hossain KR, Xu QH, Buda A, Clarke RJ (2019) Polar interactions play an important role in the energetics of the main phase transition of phosphatidylcholine membranes. ACS Omega 4:518–527.  https://doi.org/10.1021/acsomega.8b03102 CrossRefGoogle Scholar
  28. Garcia-Manyes S, Oncins G, Sanz F (2005) Effect of ion-binding and chemical phospholipid structure on the nanomechanics of lipid bilayers studied by force spectroscopy. Biophys J 89:1812–1826.  https://doi.org/10.1529/biophysj.105.064030 CrossRefGoogle Scholar
  29. Garcia-Manyes S, Oncins G, Sanz F (2006) Effect of pH and ionic strength on phospholipid nanomechanics and on deposition process onto hydrophilic surfaces measured by AFM. Electrochim Acta 51:5029–5036.  https://doi.org/10.1016/j.electacta.2006.03.062 CrossRefGoogle Scholar
  30. Gottlieb MH, Eanes ED (1972) Influence of electrolytes on the thicknesses of the phospholipid bilayers of lamellar lecithin mesophases. Biophys J 12:1533–1548CrossRefGoogle Scholar
  31. Gurtovenko AA, Vattulainen I (2008) Effect of NaCl and KCl on phosphatidylcholine and phosphatidylethanolamine lipid membranes: insight from atomic-scale simulations for understanding salt-induced effects in the plasma membrane. J Phys Chem B 112:1953–1962.  https://doi.org/10.1021/jp0750708 CrossRefGoogle Scholar
  32. Gutman M, Nachliel E (1990) The dynamic aspects of proton transfer processes. BBA-Bioenergetics 1015:391–414.  https://doi.org/10.1016/0005-2728(90)90073-D CrossRefGoogle Scholar
  33. Heberle J (2000) Proton transfer reactions across bacteriorhodopsin and along the membrane. BBA-Bioenergetics 1458:135–147.  https://doi.org/10.1016/S0005-2728(00)00064-5 CrossRefGoogle Scholar
  34. Heberle J, Dencher NA (1992) Surface-bound optical probes monitor protein translocation and surface potential changes during the bacteriorhodopsin photocycle. Proc Natl Acad Sci U S A 89:5996.  https://doi.org/10.1073/pnas.89.13.5996 CrossRefGoogle Scholar
  35. Heberle J, Riesle J, Thiedemann G, Oesterhelt D, Dencher NA (1994) Proton migration along the membrane surface and retarded surface to bulk transfer. Nature 370:379–382.  https://doi.org/10.1038/370379a0 CrossRefGoogle Scholar
  36. Javanainen M, Melcrová A, Magarkar A, Jurkiewicz P, Hof M, Jungwirth P, Martinez-Seara H (2017) Two cations, two mechanisms: interactions of sodium and calcium with zwitterionic lipid membranes. Chem Commun 53:5380–5383.  https://doi.org/10.1039/C7CC02208E CrossRefGoogle Scholar
  37. Jones MR, Jackson JB (1989) Proton release by the quinol oxidase site of the cytochrome b/c1 complex following single turnover flash excitation of intact cells of Rhodobacter capsulatus. Biochim Biophys Acta Biomembr 975:34–43.  https://doi.org/10.1016/S0005-2728(89)80198-7 CrossRefGoogle Scholar
  38. Junge W, McLaughlin S (1987) The role of fixed and mobile buffers in the kinetics of proton movement. Biochim Biophys Acta 890:1–5CrossRefGoogle Scholar
  39. Jurkiewicz P, Cwiklik L, Vojtiskova A, Jungwirth P, Hof M (2012) Structure, dynamics, and hydration of POPC/POPS bilayers suspended in NaCl, KCl, and CsCl solutions. Biochim Biophys Acta 1818:609–616.  https://doi.org/10.1016/j.bbamem.2011.11.033 CrossRefGoogle Scholar
  40. Kagawa R, Hirano Y, Taiji M, Yasuoka K, Yasui M (2013) Dynamic interactions of cations, water and lipids and influence on membrane fluidity. J Membr Sci 435:130–136.  https://doi.org/10.1016/j.memsci.2013.02.006 CrossRefGoogle Scholar
  41. Klasczyk B, Knecht V (2011) Validating affinities for ion–lipid association from simulation against experiment. J Phys Chem A 115:10587–10595.  https://doi.org/10.1021/jp202928u CrossRefGoogle Scholar
  42. Koynova R, Caffrey M (1998) Phases and phase transitions of the phosphatidylcholines. BBA Biomembranes 1376:91–145.  https://doi.org/10.1016/S0304-4157(98)00006-9 Google Scholar
  43. Lee SJ, Song Y, Baker NA (2008) Molecular dynamics simulations of asymmetric NaCl and KCl solutions separated by phosphatidylcholine bilayers: potential drops and structural changes induced by strong Na+-lipid interactions and finite size effects. Biophys J 94:3565–3576.  https://doi.org/10.1529/biophysj.107.116335 CrossRefGoogle Scholar
  44. Leontidis E (2017) Investigations of the Hofmeister series and other specific ion effects using lipid model systems. Adv Colloid Interf Sci 243:8–22.  https://doi.org/10.1016/j.cis.2017.04.001 CrossRefGoogle Scholar
  45. Mao Y, Du Y, Cang X, Wang J, Chen Z, Yang H, Jiang H (2013) Binding competition to the POPG lipid bilayer of Ca2+, Mg2+, Na+, and K+ in different ion mixtures and biological implication. J Phys Chem B 117:850–858.  https://doi.org/10.1021/jp310163z CrossRefGoogle Scholar
  46. Medvedev ES, Stuchebrukhov AA (2011) Proton diffusion along biological membranes. J Phys Condens Matter 23:234103.  https://doi.org/10.1088/0953-8984/23/23/234103 CrossRefGoogle Scholar
  47. Melcr J, Martinez-Seara H, Nencini R, Kolafa J, Jungwirth P, Ollila OHS (2018) Accurate binding of sodium and calcium to a POPC bilayer by effective inclusion of electronic polarization. J Phys Chem B 122:4546–4557.  https://doi.org/10.1021/acs.jpcb.7b12510 CrossRefGoogle Scholar
  48. Mukhopadhyay P, Monticelli L, Tieleman DP (2004) Molecular dynamics simulation of a palmitoyl-oleoyl phosphatidylserine bilayer with Na+ counterions and NaCl. Biophys J 86:1601–1609.  https://doi.org/10.1016/s0006-3495(04)74227-7 CrossRefGoogle Scholar
  49. Mulkidjanian AY, Cherepanov DA (2006) Probing biological interfaces by tracing proton passage across them. Photochem Photobiol Sci 5:577–587.  https://doi.org/10.1039/b516443e CrossRefGoogle Scholar
  50. Mulkidjanian AY, Heberle J, Cherepanov DA (2006) Protons @ interfaces: implications for biological energy conversion. Biochim Biophys Acta 1757:913–930.  https://doi.org/10.1016/j.bbabio.2006.02.015 CrossRefGoogle Scholar
  51. Nachliel E, Gutman M (1996) Quantitative evaluation of the dynamics of proton transfer from photoactivated bacteriorhodopsin to the bulk. FEBS Lett 393:221–225CrossRefGoogle Scholar
  52. Nachliel E, Gutman M, Kiryati S, Dencher NA (1996) Protonation dynamics of the extracellular and cytoplasmic surface of bacteriorhodopsin in the purple membrane. Proc Natl Acad Sci U S A 93:10747.  https://doi.org/10.1073/pnas.93.20.10747 CrossRefGoogle Scholar
  53. Nguyen TH, Zhang C, Weichselbaum E, Knyazev DG, Pohl P, Carloni P (2018) Interfacial water molecules at biological membranes: structural features and role for lateral proton diffusion. PLoS One 13:e0193454.  https://doi.org/10.1371/journal.pone.0193454 CrossRefGoogle Scholar
  54. Ojemyr LN, Lee HJ, Gennis RB, Brzezinski P (2010) Functional interactions between membrane-bound transporters and membranes. Proc Natl Acad Sci U S A 107:15763–15767.  https://doi.org/10.1073/pnas.1006109107 CrossRefGoogle Scholar
  55. Pabst G, Hodzic A, Strancar J, Danner S, Rappolt M, Laggner P (2007) Rigidification of neutral lipid bilayers in the presence of salts. Biophys J 93:2688–2696.  https://doi.org/10.1529/biophysj.107.112615 CrossRefGoogle Scholar
  56. Pandit SA, Bostick D, Berkowitz ML (2003) Molecular dynamics simulation of a dipalmitoylphosphatidylcholine bilayer with NaCl. Biophys J 84:3743–3750.  https://doi.org/10.1016/S0006-3495(03)75102-9 CrossRefGoogle Scholar
  57. Petelska AD, Figaszewski ZA (2002) Effect of pH on the interfacial tension of bilayer lipid membrane formed from phosphatidylcholine or phosphatidylserine. BBA Biomembranes 1561:135–146.  https://doi.org/10.1016/S0005-2736(01)00463-1 CrossRefGoogle Scholar
  58. Petrache HI, Tristram-Nagle S, Harries D, Kucerka N, Nagle JF, Parsegian VA (2006) Swelling of phospholipids by monovalent salt. J Lipid Res 47:302–309.  https://doi.org/10.1194/jlr.M500401-JLR200 CrossRefGoogle Scholar
  59. Piantanida L, Bolt HL, Rozatian N, Cobb SL, Voitchovsky K (2017) Ions modulate stress-induced nanotexture in supported fluid lipid bilayers. Biophys J 113:426–439.  https://doi.org/10.1016/j.bpj.2017.05.049 CrossRefGoogle Scholar
  60. Reif MM, Kallies C, Knecht V (2017) Effect of sodium and chloride binding on a lecithin bilayer. A molecular dynamics study. Membranes 7.  https://doi.org/10.3390/membranes7010005
  61. Sandén T, Salomonsson L, Brzezinski P, Widengren J (2010) Surface-coupled proton exchange of a membrane-bound proton acceptor. Proc Natl Acad Sci U S A 107:4129–4134.  https://doi.org/10.1073/pnas.0908671107 CrossRefGoogle Scholar
  62. Scherrer P, Alexiev U, Marti T, Khorana HG, Heyn MP (1994) Covalently bound pH-indicator dyes at selected extracellular or cytoplasmic sites in bacteriorhodopsin. 1. Proton migration along the surface of bacteriorhodopsin micelles and its delayed transfer from surface to bulk. Biochemistry 33:13684–13692.  https://doi.org/10.1021/bi00250a019 CrossRefGoogle Scholar
  63. Serowy S, Saparov SM, Antonenko YN, Kozlovsky W, Hagen V, Pohl P (2003) Structural proton diffusion along lipid bilayers. Biophys J 84:1031–1037.  https://doi.org/10.1016/S0006-3495(03)74919-4 CrossRefGoogle Scholar
  64. Smondyrev AM, Voth GA (2002) Molecular dynamics simulation of proton transport through the influenza A virus M2 channel. Biophys J 83:1987–1996.  https://doi.org/10.1016/s0006-3495(02)73960-x CrossRefGoogle Scholar
  65. Springer A, Hagen V, Cherepanov DA, Antonenko YN, Pohl P (2011) Protons migrate along interfacial water without significant contributions from jumps between ionizable groups on the membrane surface. Proc Natl Acad Sci U S A 108:14461–14466.  https://doi.org/10.1073/pnas.1107476108 CrossRefGoogle Scholar
  66. Tocanne J-F, Teissié J (1990) Ionization of phospholipids and phospholipid-supported interfacial lateral diffusion of protons in membrane model systems. BBA Biomembranes 1031:111–142.  https://doi.org/10.1016/0304-4157(90)90005-W Google Scholar
  67. Vácha R, Buch V, Milet A, Devlin JP, Jungwirth P (2007) Autoionization at the surface of neat water: is the top layer pH neutral, basic, or acidic? Phys Chem Chem Phys 9:4736–4747.  https://doi.org/10.1039/B704491G CrossRefGoogle Scholar
  68. Vácha R et al (2009) Effects of alkali cations and halide anions on the DOPC lipid membrane. J Phys Chem A 113:7235–7243.  https://doi.org/10.1021/jp809974e CrossRefGoogle Scholar
  69. Vácha R et al (2010) Mechanism of interaction of monovalent ions with phosphatidylcholine lipid membranes. J Phys Chem B 114:9504–9509.  https://doi.org/10.1021/jp102389k CrossRefGoogle Scholar
  70. Vorobyov I, Olson TE, Kim JH, Koeppe RE 2nd, Andersen OS, Allen TW (2014) Ion-induced defect permeation of lipid membranes. Biophys J 106:586–597.  https://doi.org/10.1016/j.bpj.2013.12.027 CrossRefGoogle Scholar
  71. Weichselbaum E et al (2017) Origin of proton affinity to membrane/water interfaces. Sci Rep 7:4553.  https://doi.org/10.1038/s41598-017-04675-9 CrossRefGoogle Scholar
  72. Wolf MG, Grubmuller H, Groenhof G (2014) Anomalous surface diffusion of protons on lipid membranes. Biophys J 107:76–87.  https://doi.org/10.1016/j.bpj.2014.04.062 CrossRefGoogle Scholar
  73. Yamashita T, Voth GA (2010) Properties of hydrated excess protons near phospholipid bilayers. J Phys Chem B 114:592–603.  https://doi.org/10.1021/jp908768c CrossRefGoogle Scholar
  74. Zhang C, Knyazev DG, Vereshaga YA, Ippoliti E, Nguyen TH, Carloni P, Pohl P (2012) Water at hydrophobic interfaces delays proton surface-to-bulk transfer and provides a pathway for lateral proton diffusion. Proc Natl Acad Sci U S A 109:9744–9749.  https://doi.org/10.1073/pnas.1121227109 CrossRefGoogle Scholar
  75. Zhou Y, Raphael RM (2007) Solution pH alters mechanical and electrical properties of phosphatidylcholine membranes: relation between interfacial electrostatics, intramembrane potential, and bending elasticity. Biophys J 92:2451–2462.  https://doi.org/10.1529/biophysj.106.096362 CrossRefGoogle Scholar
  76. Zimmermann R, Küttner D, Renner L, Kaufmann M, Werner C (2012) Fluidity modulation of phospholipid bilayers by electrolyte ions: insights from fluorescence microscopy and microslit electrokinetic experiments. J Phys Chem A 116:6519–6525.  https://doi.org/10.1021/jp212364q CrossRefGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of Technology SydneyUltimoAustralia
  2. 2.School of Pharmacy and Biomedical SciencesCurtin UniversityPerthAustralia

Personalised recommendations