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      Flexibility of a Eukaryotic Lipidome – Insights from Yeast Lipidomics

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          Abstract

          Mass spectrometry-based shotgun lipidomics has enabled the quantitative and comprehensive assessment of cellular lipid compositions. The yeast Saccharomyces cerevisiae has proven to be a particularly valuable experimental system for studying lipid-related cellular processes. Here, by applying our shotgun lipidomics platform, we investigated the influence of a variety of commonly used growth conditions on the yeast lipidome, including glycerophospholipids, triglycerides, ergosterol as well as complex sphingolipids. This extensive dataset allowed for a quantitative description of the intrinsic flexibility of a eukaryotic lipidome, thereby providing new insights into the adjustments of lipid biosynthetic pathways. In addition, we established a baseline for future lipidomic experiments in yeast. Finally, flexibility of lipidomic features is proposed as a new parameter for the description of the physiological state of an organism.

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          Most cited references52

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          Getting started with yeast.

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            How lipids affect the activities of integral membrane proteins.

            The activities of integral membrane proteins are often affected by the structures of the lipid molecules that surround them in the membrane. One important parameter is the hydrophobic thickness of the lipid bilayer, defined by the lengths of the lipid fatty acyl chains. Membrane proteins are not rigid entities, and deform to ensure good hydrophobic matching to the surrounding lipid bilayer. The structure of the lipid headgroup region is likely to be important in defining the structures of those parts of a membrane protein that are located in the lipid headgroup region. A number of examples are given where the conformation of the headgroup-embedded region of a membrane protein changes during the reaction cycle of the protein; activities of such proteins might be expected to be particularly sensitive to lipid headgroup structure. Differences in hydrogen bonding potential and hydration between the headgroups of phosphatidycholines and phosphatidylethanolamines could be important factors in determining the effects of these lipids on protein activities, as well as any effects related to the tendency of the phosphatidylethanolamines to form a curved, hexagonal H(II) phase. Effects of lipid structure on protein aggregation and helix-helix interactions are also discussed, as well as the effects of charged lipids on ion concentrations close to the surface of the bilayer. Interpretations of lipid effects in terms of changes in protein volume, lipid free volume, and curvature frustration are also described. Finally, the role of non-annular, or 'co-factor' lipids, tightly bound to membrane proteins, is described.
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              Orm family proteins mediate sphingolipid homeostasis

              Despite the essential roles of sphingolipids as both structural components of membranes and critical signalling molecules, we have a limited understanding of how cells sense and regulate their levels. Here we reveal the function in sphingolipid metabolism of the ORM/ORMDL genes, a conserved gene family that includes ORMDL3, which has recently been identified as a potential risk factor for childhood asthma. Starting from an unbiased functional genomic approach, we identify Orm proteins as negative regulators of sphingolipid synthesis that form a conserved complex with serine palmitoyltransferase, the first and rate-limiting enzyme in sphingolipid production. We also define a regulatory pathway in which phosphorylation of Orm proteins relieves their inhibitory activity when sphingolipid production is disrupted. Changes in ORM gene expression or mutations to their phosphorylation sites cause dysregulation of sphingolipid metabolism. Our work identifies the Orm proteins as critical mediators of sphingolipid homeostasis and raises the possibility that sphingolipid misregulation contributes to the development of childhood asthma.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                18 April 2012
                : 7
                : 4
                : e35063
                Affiliations
                [1]Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
                Texas A&M University, United States of America
                Author notes

                Conceived and designed the experiments: CK MAS. Performed the experiments: CK MAS. Analyzed the data: CK MAS MJG FM KS. Contributed reagents/materials/analysis tools: AS FM. Wrote the paper: CK MAS KS.

                [¤]

                Current address: Heidelberg University Biochemistry Center, Heidelberg, Germany

                Article
                PONE-D-12-03565
                10.1371/journal.pone.0035063
                3329542
                22529973
                82b9aac9-feb4-4b39-b28e-c7ef751746da
                Klose et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 3 February 2012
                : 12 March 2012
                Page count
                Pages: 11
                Categories
                Research Article
                Biology
                Biochemistry
                Metabolism
                Biosynthesis
                Lipid Metabolism
                Metabolic Pathways
                Lipids
                Model Organisms
                Yeast and Fungal Models
                Saccharomyces Cerevisiae
                Molecular Cell Biology
                Cell Growth
                Membranes and Sorting
                Chemistry
                Analytical Chemistry
                Chemical Analysis
                Quantitative Analysis

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                Uncategorized

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