Lipid–protein interactions: Lessons learned from stress

• Published in: Biochimica et biophysica acta Vol. 1848; no. 9; pp. 1744 - 1756
• Main Authors: Battle, A.R., Ridone, P., Bavi, N., Nakayama, Y., Nikolaev, Y.A., Martinac, B.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.09.2015
• Subjects: Animals; Cell Membrane - chemistry; Cell Membrane - metabolism; Computer modeling; EPR; FRET/FLIM; Humans; Lipid Bilayers - chemistry; Lipid Bilayers - metabolism; Liposome; Mechanosensitive channel; Mechanotransduction, Cellular; Membrane Lipids - chemistry; Membrane Lipids - metabolism; Membrane Proteins - chemistry; Membrane Proteins - metabolism; Models, Molecular; Patch fluorometry; Protein Binding; Protein Structure, Tertiary; Patch fluorometry; Liposome; Mechanosensitive channel; FRET/FLIM; EPR; Computer modeling
• ISSN: 0005-2736; 0006-3002; 1879-2642
• DOI: 10.1016/j.bbamem.2015.04.012

Biological membranes are essential for normal function and regulation of cells, forming a physical barrier between extracellular and intracellular space and cellular compartments. These physical barriers are subject to mechanical stresses. As a consequence, nature has developed proteins that are able to transpose mechanical stimuli into meaningful intracellular signals. These proteins, termed Mechanosensitive (MS) proteins provide a variety of roles in response to these stimuli. In prokaryotes these proteins form transmembrane spanning channels that function as osmotically activated nanovalves to prevent cell lysis by hypoosmotic shock. In eukaryotes, the function of MS proteins is more diverse and includes physiological processes such as touch, pain and hearing. The transmembrane portion of these channels is influenced by the physical properties such as charge, shape, thickness and stiffness of the lipid bilayer surrounding it, as well as the bilayer pressure profile. In this review we provide an overview of the progress to date on advances in our understanding of the intimate biophysical and chemical interactions between the lipid bilayer and mechanosensitive membrane channels, focusing on current progress in both eukaryotic and prokaryotic systems. These advances are of importance due to the increasing evidence of the role the MS channels play in disease, such as xerocytosis, muscular dystrophy and cardiac hypertrophy. Moreover, insights gained from lipid–protein interactions of MS channels are likely relevant not only to this class of membrane proteins, but other bilayer embedded proteins as well. This article is part of a Special Issue entitled: Lipid–protein interactions. [Display omitted] •Mechanical force is major stimulus acting on membranes of living cells throughout evolution.•Mechanosensitive ion channels present a large class of molecular transducers of mechanical force.•Interactions between the cell membrane and force-gated channels are essential for their function.•“Force-from-lipids principle” is a main paradigm for the gating of mechanosensitive channels.•Lipid–protein interactions valid for force-gated channels may apply to other membrane proteins.