Randomly organized lipids and marginally stable proteins: A coupling of weak interactions to optimize membrane signaling

Anne M. Rice, Ryan Mahling, Michael E. Fealey, Anika Rannikko, Katie Dunleavy, Troy Hendrickson, K. Jean Lohese, Spencer Kruggel, Hillary Heiling, Daniel Harren, R. Bryan Sutton, John Pastor, Anne Hinderliter

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Eukaryotic lipids in a bilayer are dominated by weak cooperative interactions. These interactions impart highly dynamic and pliable properties to the membrane. C2 domain-containing proteins in the membrane also interact weakly and cooperatively giving rise to a high degree of conformational plasticity. We propose that this feature of weak energetics and plasticity shared by lipids and C2 domain-containing proteins enhance a cell's ability to transduce information across the membrane. We explored this hypothesis using information theory to assess the information storage capacity of model and mast cell membranes, as well as differential scanning calorimetry, carboxyfluorescein release assays, and tryptophan fluorescence to assess protein and membrane stability. The distribution of lipids in mast cell membranes encoded 5.6-5.8 bits of information. More information resided in the acyl chains than the head groups and in the inner leaflet of the plasma membrane than the outer leaflet. When the lipid composition and information content of model membranes were varied, the associated C2 domains underwent large changes in stability and denaturation profile. The C2 domain-containing proteins are therefore acutely sensitive to the composition and information content of their associated lipids. Together, these findings suggest that the maximum flow of signaling information through the membrane and into the cell is optimized by the cooperation of near-random distributions of membrane lipids and proteins. This article is part of a Special Issue entitled: Interfacially Active Peptides and Proteins. Guest Editors: William C. Wimley and Kalina Hristova.

Original languageEnglish (US)
Pages (from-to)2331-2340
Number of pages10
JournalBiochimica et Biophysica Acta - Biomembranes
Volume1838
Issue number9
DOIs
StatePublished - Sep 2014

Keywords

  • C2 domain
  • Disorder
  • Information theory
  • Membrane domain
  • Signaling

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