Abstract
The interaction of phosphatidylserine (PS) synthase from Escherichia coli with lipid membranes was studied with a recently developed variant of the surface plasmon resonance technique, referred to as coupled plasmon-waveguide resonance spectroscopy. The features of the new technique are increased sensitivity and spectral resolution, and a unique ability to directly measure the structural anisotropy of lipid and proteolipid films. Solid-supported lipid bilayers with the following compositions were used: 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC); POPC-1-palmitoyl-2-oleoyl-sn-glycero-3-phosphate (POPA) (80:20, mol/mol); POPC-POPA (60:40, mol/mol); and POPC-1-palmitoyl-2-oleoyl-sn-glycero-3-[phospho-rac-(1-glycerol)] (POPG) (75:25, mol/mol). Addition of either POPA or POPG to a POPC bilayer causes a considerable increase of both the bilayer thickness and its optical anisotropy. PS synthase exhibits a biphasic interaction with the bilayers. The first phase, occurring at low protein concentrations, involves both electrostatic and hydrophobic interactions, although it is dominated by the latter, and the enzyme causes a local decrease of the ordering of the lipid molecules. The second phase, occurring at high protein concentrations, is predominantly controlled by electrostatic interactions, and results in a cooperative binding of the enzyme to the membrane surface. Addition of the anionic lipids to a POPC bilayer causes a 5- to 15-fold decrease in the protein concentration at which the first binding phase occurs. The results reported herein lend experimental support to a previously suggested mechanism for the regulation of the polar head group composition in E. coli membranes.
MeSH Terms
Anisotropy
CDPdiacylglycerol-Serine O-Phosphatidyltransferase/chemistry,metabolism
Escherichia coli/enzymology
Kinetics
Lipid Bilayers/chemistry,metabolism
Phosphatidic Acids/chemistry,metabolism
Phosphatidylcholines/chemistry,metabolism
Phosphatidylglycerols/chemistry,metabolism
Substrate Specificity
Surface Plasmon Resonance/methods
Chemicals
1-palmitoyl-2-oleoyl-glycero-3-phosphatidic acid
Lipid Bilayers
Phosphatidic Acids
Phosphatidylcholines
Phosphatidylglycerols
1-palmitoyl-2-oleoylglycero-3-phosphoglycerol
CDPdiacylglycerol-Serine O-Phosphatidyltransferase
1-palmitoyl-2-oleoylphosphatidylcholine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Salamon Z
Department of Biochemistry, University of Arizona, Tucson, Arizona 85721, USA.
Lindblom G
Rilfors L
Linde K
Tollin G
References (31)
31 references, click to expand
-
Ribosomal-associated phosphatidylserine synthetase from Escherichia coli: purification by substrate-specific elution from phosphocellulose using cytidine 5'-diphospho-1,2-diacyl-sn-glycerol.
Biochemistry. 1976 Nov 30;15(24):5212-8
PMID: 187212
-
Reconstitution of cell membrane structure in vitro and its transformation into an excitable system.
Nature. 1962 Jun 9;194:979-80
PMID: 14476933
-
Phosphatidic acid accumulation in the membranes of Escherichia coli mutants defective in CDP-diglyceride synthetase.
J Biol Chem. 1980 Feb 25;255(4):1623-9
PMID: 6243645
-
The temperature dependence of molecular order and the influence of cholesterol in Acholeplasma laidlawii membranes.
Biochim Biophys Acta. 1980 Apr 24;597(3):477-91
PMID: 6892886
-
Escherichia coli membrane vesicles with elevated phosphatidic acid levels. A detergent-free system for in vitro phospholipid synthesis.
Biochim Biophys Acta. 1984 Dec 6;796(3):373-83
PMID: 6391555
-
Substrate-induced membrane association of phosphatidylserine synthase from Escherichia coli.
J Bacteriol. 1986 Mar;165(3):805-12
PMID: 3005238
-
Amphitropic proteins: a new class of membrane proteins.
Trends Biochem Sci. 1988 Mar;13(3):79-83
PMID: 3245067
-
Biosynthesis and function of phospholipids in Escherichia coli.
J Biol Chem. 1990 Jan 25;265(3):1235-8
PMID: 2404013
-
Sequence and inactivation of the pss gene of Escherichia coli. Phosphatidylethanolamine may not be essential for cell viability.
J Biol Chem. 1991 Mar 15;266(8):5323-32
PMID: 2002065
-
Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective.
Q Rev Biophys. 1991 Aug;24(3):293-397
PMID: 1749824
-
Combined influence of cholesterol and synthetic amphiphillic peptides upon bilayer thickness in model membranes.
Biophys J. 1992 May;61(5):1176-83
PMID: 1600079
-
Metabolic regulations and biological functions of phospholipids in Escherichia coli.
Prog Lipid Res. 1992;31(3):245-99
PMID: 1287667
-
Regulation and phase equilibria of membrane lipids from Bacillus megaterium and Acholeplasma laidlawii strain A containing methyl-branched acyl chains.
Biochemistry. 1994 May 24;33(20):6110-20
PMID: 8193124
-
Conformational changes in rhodopsin probed by surface plasmon resonance spectroscopy.
Biochemistry. 1994 Nov 22;33(46):13706-11
PMID: 7947780
-
Assembly and molecular organization of self-assembled lipid bilayers on solid substrates monitored by surface plasmon resonance spectroscopy.
Biochim Biophys Acta. 1994 Nov 2;1195(2):267-75
PMID: 7947920
-
Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures.
J Biol Chem. 1996 Mar 22;271(12):6801-9
PMID: 8636103
-
New aspects on membrane lipid regulation in Acholeplasma laidlawii A and phase equilibria of monoacyldiglucosyldiacylglycerol.
Biochemistry. 1996 Aug 27;35(34):11119-30
PMID: 8780516
-
Surface plasmon resonance spectroscopy studies of membrane proteins: transducin binding and activation by rhodopsin monitored in thin membrane films.
Biophys J. 1996 Jul;71(1):283-94
PMID: 8804611
-
A regulatory mechanism for the balanced synthesis of membrane phospholipid species in Escherichia coli.
Biosci Biotechnol Biochem. 1996 Jan;60(1):111-6
PMID: 8824831
-
Molecular basis for membrane phospholipid diversity: why are there so many lipids?
Annu Rev Biochem. 1997;66:199-232
PMID: 9242906
-
Surface plasmon resonance spectroscopy as a tool for investigating the biochemical and biophysical properties of membrane protein systems. I: Theoretical principles.
Biochim Biophys Acta. 1997 Sep 8;1331(2):117-29
PMID: 9325438
-
Surface plasmon resonance spectroscopy as a tool for investigating the biochemical and biophysical properties of membrane protein systems. II: Applications to biological systems.
Biochim Biophys Acta. 1997 Sep 8;1331(2):131-52
PMID: 9325439
-
Phosphatidylserine synthase from bacteria.
Biochim Biophys Acta. 1997 Sep 4;1348(1-2):214-27
PMID: 9370336
-
Coupled plasmon-waveguide resonators: a new spectroscopic tool for probing proteolipid film structure and properties.
Biophys J. 1997 Nov;73(5):2791-7
PMID: 9370473
-
Phosphatidylethanolamine mediates insertion of the catalytic domain of leader peptidase in membranes.
FEBS Lett. 1998 Jul 10;431(1):75-9
PMID: 9684869
-
Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine.
J Bacteriol. 1998 Aug;180(16):4252-7
PMID: 9696776
-
Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease.
EMBO J. 1998 Sep 15;17(18):5255-64
PMID: 9736605
-
Coupled plasmon-waveguide resonance spectroscopy studies of the cytochrome b6f/plastocyanin system in supported lipid bilayer membranes.
Biophys J. 1998 Oct;75(4):1874-85
PMID: 9746528
-
Reconstituted phosphatidylserine synthase from Escherichia coli is activated by anionic phospholipids and micelle-forming amphiphiles.
Biochim Biophys Acta. 1999 May 18;1438(2):281-94
PMID: 10320811
-
Plasmon resonance spectroscopy: probing molecular interactions within membranes.
Trends Biochem Sci. 1999 Jun;24(6):213-9
PMID: 10366845
-
Phosphatidylserine synthase from Escherichia coli. The role of Triton X-100 in catalysis.
J Biol Chem. 1979 Sep 10;254(17):8391-7
PMID: 224052