Structural adaptations of proteins to different biological membranes

• Published in: Biochimica et biophysica acta Vol. 1828; no. 11; pp. 2592 - 2608
• Main Authors: Pogozheva, Irina D., Tristram-Nagle, Stephanie, Mosberg, Henry I., Lomize, Andrei L.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01-11-2013
• Subjects: Cell Membrane - metabolism; Hydrophobic thickness; Hyperthermophile; Lipid bilayer; Lipid Bilayers - metabolism; Membrane asymmetry; Membrane protein; Membrane Proteins - chemistry; Membrane Proteins - metabolism; Models, Molecular; Polarity profile; Protein Conformation; Scattering, Radiation; Lipid bilayer; Hyperthermophile; Membrane protein; Polarity profile; Hydrophobic thickness; Membrane asymmetry
• ISSN: 0005-2736; 0006-3002; 1879-2642
• DOI: 10.1016/j.bbamem.2013.06.023

To gain insight into adaptations of proteins to their membranes, intrinsic hydrophobic thicknesses, distributions of different chemical groups and profiles of hydrogen-bonding capacities (α and β) and the dipolarity/polarizability parameter (π*) were calculated for lipid-facing surfaces of 460 integral α-helical, β-barrel and peripheral proteins from eight types of biomembranes. For comparison, polarity profiles were also calculated for ten artificial lipid bilayers that have been previously studied by neutron and X-ray scattering. Estimated hydrophobic thicknesses are 30–31Å for proteins from endoplasmic reticulum, thylakoid, and various bacterial plasma membranes, but differ for proteins from outer bacterial, inner mitochondrial and eukaryotic plasma membranes (23.9, 28.6 and 33.5Å, respectively). Protein and lipid polarity parameters abruptly change in the lipid carbonyl zone that matches the calculated hydrophobic boundaries. Maxima of positively charged protein groups correspond to the location of lipid phosphates at 20–22Å distances from the membrane center. Locations of Tyr atoms coincide with hydrophobic boundaries, while distributions maxima of Trp rings are shifted by 3–4Å toward the membrane center. Distributions of Trp atoms indicate the presence of two 5–8Å-wide midpolar regions with intermediate π* values within the hydrocarbon core, whose size and symmetry depend on the lipid composition of membrane leaflets. Midpolar regions are especially asymmetric in outer bacterial membranes and cell membranes of mesophilic but not hyperthermophilic archaebacteria, indicating the larger width of the central nonpolar region in the later case. In artificial lipid bilayers, midpolar regions are observed up to the level of acyl chain double bonds.
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•We computed polarity profiles for 10 lipid bilayers and proteins from 8 biomembranes.•Calculated hydrophobic boundaries match locations of protein Tyr and lipid carbonyls.•Membranes with α-helical proteins are 4–9Å thicker than membranes with β-barrels.•Trp rings accumulate in 5–8Å-wide midpolar regions within the hydrocarbon core.•Asymmetry of midpolar regions correlates with lipid asymmetry of biomembranes.