Phospholipid subclass specific alterations in the passive ion permeability of membrane bilayers: Separation of enthalpic and entropic contributions to transbilayer ion flux

Youchun Zeng, Xianlin Han, Richard W. Gross

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

Alterations in phospholipid class, subclass, and individual molecular species contribute to the diversity of biologic membranes, but their effects on membrane passive ion permeability have not been systematically studied. Herein, we developed a simple and efficient fluorescence technique based upon the loss of valinomycin-inducible membrane potential to characterize the passive flux of ions across phospholipid bilayers. Detailed kinetic characterization of ion flux across membrane bilayers composed of discrete chemical entities demonstrated that the class, subclass, and individual molecular species of each phospholipid have substantive effects on membrane passive ion permeability properties. Increasing the degree of unsaturation in either the sn-1 or sn-2 aliphatic chains in phosphatidyicholine markedly enhanced transmembrane ion flux, with over 10-fold differences in the first- order rate constant manifested in molecular species containing four double bonds in comparison to those possessing three double bonds (e.g., k(app) = 0.0014 min-1 for 1-octadec-9'-enoyl-2-octadec-9',12'-z-sn-glycero-3- phosphocholine (18:1-18:2 phosphatidylcholine) while k(app) = 0.021 min-1 for 1,2-dioctadec-9',12'-dienoyl-sn-glycero-3- phosphocholine (18:2-18:2 phosphatidylcholine)). Moreover, although the apparent first-order rate constants for transmembrane ion flux in vesicles composed of phosphatidylcholine or plasmanylcholine containing palmitate at the sn-1 position and arachidonate at the sn-2 position were similar (k(app) = 0.04 min-1 at 22 C for both), the k(app) for corresponding vesicles composed of plasmenylcholine was 20-fold less (k(app) = 0.002 min-1 at 22 C). Examination of the temperature dependence of passive membrane ion permeability demonstrated that altered ion flux across membranes composed of choline glycerophospholipids was primarily due to entropic effects without substantial changes in the activation energy for ion translocation. For example, E(a) = 19.7 ± 0.5 and 20.7 ± 0.6 kcal-mol-1 for l-hexadecanoyl- 2-eicosa-5',8',11',14'tetraenoyl-sn-glycero-3-phosphocholine (16:0-20:4 phosphatidylcholine) and 1-O-(Z)-hexadec-1'-enyl-2-eicosa-5',8',11',14'- tetraenoyl-sn-glycero-3-phosphocholine (16:0-20:4 plasmenylcholine), respectively, while their difference in the entropies of activation (AS) was 4.3 ± 0.5 cal·mol-1·K-1. Collectively, these results identify substantial differences in the membrane passive ion permeability properties of phospholipid classes, subclasses, and molecular species present in biologic membranes of eukaryotic cells and identify entropic alterations as an important contributor to these differences.

Original languageEnglish (US)
Pages (from-to)2346-2355
Number of pages10
JournalBiochemistry
Volume37
Issue number8
DOIs
StatePublished - Feb 24 1998
Externally publishedYes

ASJC Scopus subject areas

  • Biochemistry

Fingerprint Dive into the research topics of 'Phospholipid subclass specific alterations in the passive ion permeability of membrane bilayers: Separation of enthalpic and entropic contributions to transbilayer ion flux'. Together they form a unique fingerprint.

Cite this