The expanding organelle lipidomes: current knowledge and challenges

Sarmento, Maria J.; Llorente, Alicia; Petan, Toni; Khnykin, Denis; Popa, Iuliana; Nikolac Perkovic, Matea; Konjevod, Marcela; Jaganjac, Morana

doi:10.1007/s00018-023-04889-3

Cited by 15 publications

(7 citation statements)

References 259 publications

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“…Lipids play vital roles in a variety of cellular structures and processes because they are indispensable elements of myelin, cellular membranes, and vesicles that enable intracellular trafficking. In addition, lipids are involved in metabolic processes for energy production and are implicated in inflammations and bone-related diseases . Largely, we are detecting membrane lipids, such as sphingomyelin (SM) and phosphatidylcholine (PC) lipids .…”

Section: Resultsmentioning

confidence: 99%

“…In addition, lipids are involved in metabolic processes for energy production and are implicated in inflammations and bone-related diseases. 77 Largely, we are detecting membrane lipids, such as sphingomyelin (SM) and phosphatidylcholine (PC) lipids. 78 Differences in lipid content may be a result of different cell types or cell shapes within these regions.…”

Section: Resultsmentioning

confidence: 99%

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Sample Preparation Method for MALDI Mass Spectrometry Imaging of Fresh-Frozen Spines

Bender,

Wang,

Zhai

et al. 2023

Anal. Chem.

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Technologies assessing the lipidomics, genomics, epigenomics, transcriptomics, and proteomics of tissue samples at single-cell resolution have deepened our understanding of physiology and pathophysiology at an unprecedented level of detail. However, the study of single-cell spatial metabolomics in undecalcified bones faces several significant challenges, such as the fragility of bone, which often requires decalcification or fixation leading to the degradation or removal of lipids and other molecules. As such, we describe a method for performing mass spectrometry imaging on undecalcified spine that is compatible with other spatial omics measurements. In brief, we use fresh-frozen rat spines and a system of carboxyl methylcellulose embedding, cryofilm, and polytetrafluoroethylene rollers to maintain tissue integrity while avoiding signal loss from variations in laser focus and artifacts from traditional tissue processing. This reveals various tissue types and lipidomic profiles of spinal regions at 10 μm spatial resolutions using matrix-assisted laser desorption/ionization mass spectrometry imaging. We expect this method to be adapted and applied to the analysis of the spinal cord, shedding light on the mechanistic aspects of cellular heterogeneity, development, and disease pathogenesis underlying different bone-related conditions and diseases. This study furthers the methodology for high spatial metabolomics of spines and adds to the collective efforts to achieve a holistic understanding of diseases via single-cell spatial multiomics.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Sample Preparation Method for MALDI Mass Spectrometry Imaging of Fresh-Frozen Spines

Bender,

Wang,

Zhai

et al. 2023

Anal. Chem.

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“…Mass spectrometry‐based lipidomics provides direct readout of lipid molecular species; however, isolating LDs with high purity is crucial for the characterization of the monolayer lipidome. Due to the large TG and CE content, LDs can be separated from other subcellular compartments using differential or density gradient centrifugation [51]. However, the presence of numerous LD contact sites with other organelles makes it challenging to address the LD monolayer composition alone.…”

Section: Ld Lipidome: Composition Of the Monolayermentioning

confidence: 99%

The lipid droplet lipidome

Wölk,

Fedorova

2024

FEBS Letters

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Lipid droplets (LDs) are intracellular organelles with a hydrophobic core formed by neutral lipids surrounded by a phospholipid monolayer harboring a variety of regulatory and enzymatically active proteins. Over the last few decades, our understanding of LD biology has evolved significantly. Nowadays, LDs are appreciated not just as passive energy storage units, but rather as active players in the regulation of lipid metabolism and quality control machineries. To fulfill their functions in controlling cellular metabolic states, LDs need to be highly dynamic and responsive organelles. A large body of evidence supports a dynamic nature of the LD proteome and its contact sites with other organelles. However, much less is known about the lipidome of LDs. Numerous examples clearly indicate the intrinsic link between LD lipids and proteins, calling for a deeper characterization of the LD lipidome in various physiological and pathological settings. Here, we reviewed the current state of knowledge in the field of the LD lipidome, providing a brief overview of the lipid classes and their molecular species present within the neutral core and phospholipid monolayer.

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“…Second, they create a dynamic molecular matrix that supports the vital functions of integral membrane proteins, thereby facilitating a wide range of biochemical processes, including neurotransmission, energy production, and immune response . Cell membranes exhibit a huge molecular heterogeneity of lipid compounds, as evident in the ever-evolving field of lipidomics, which aims to identify and quantify the molecular species of cellular lipids and their biological functions . Yet, it has been long recognized that the most abundant lipids found in mammalian cell membranes can be generally divided into three categories: glycerophospholipids (phosphatidylcholines in particular), sphingolipids, and cholesterol, which along with the nanoscopic layer of water directly hydrating the lipids, commonly referred to as biological water , define the structural scaffold of cellular membranes …”

Section: Introductionmentioning

confidence: 99%

“…5 Cell membranes exhibit a huge molecular heterogeneity of lipid compounds, as evident in the ever-evolving field of lipidomics, which aims to identify and quantify the molecular species of cellular lipids and their biological functions. 6 Yet, it has been long recognized that the most abundant lipids found in mammalian cell membranes can be generally divided into three categories: glycerophospholipids (phosphatidylcholines in particular), sphingolipids, and cholesterol, which along with the nanoscopic layer of water directly hydrating the lipids, commonly referred to as biological water, define the structural scaffold of cellular membranes. 7 The properties of biological water differ markedly from water in the bulk due to confinement effects and a perturbed interfacial H-bond donor/acceptor balance.…”

Section: ■ Introductionmentioning

confidence: 99%

Cholesterol Changes Interfacial Water Alignment in Model Cell Membranes

Orlikowska-Rzeznik,

Versluis,

Bakker

et al. 2024

J. Am. Chem. Soc.

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The nanoscopic layer of water that directly hydrates biological membranes plays a critical role in maintaining the cell structure, regulating biochemical processes, and managing intermolecular interactions at the membrane interface. Therefore, comprehending the membrane structure, including its hydration, is essential for understanding the chemistry of life. While cholesterol is a fundamental lipid molecule in mammalian cells, influencing both the structure and dynamics of cell membranes, its impact on the structure of interfacial water has remained unknown. We used surface-specific vibrational sum-frequency generation spectroscopy to study the effect of cholesterol on the structure and hydration of monolayers of the lipids 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC), 1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC), and egg sphingomyelin (SM). We found that for the unsaturated lipid DOPC, cholesterol intercalates in the membrane without significantly changing the orientation of the lipid tails and the orientation of the water molecules hydrating the headgroups of DOPC. In contrast, for the saturated lipids DPPC and SM, the addition of cholesterol leads to clearly enhanced packing and ordering of the hydrophobic tails. It is also observed that the orientation of the water hydrating the lipid headgroups is enhanced upon the addition of cholesterol. These results are important because the orientation of interfacial water molecules influences the cell membranes' dipole potential and the strength and specificity of interactions between cell membranes and peripheral proteins and other biomolecules. The lipid nature-dependent role of cholesterol in altering the arrangement of interfacial water molecules offers a fresh perspective on domain-selective cellular processes, such as protein binding.

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The expanding organelle lipidomes: current knowledge and challenges

Cited by 15 publications

References 259 publications

Sample Preparation Method for MALDI Mass Spectrometry Imaging of Fresh-Frozen Spines

Sample Preparation Method for MALDI Mass Spectrometry Imaging of Fresh-Frozen Spines

The lipid droplet lipidome

Cholesterol Changes Interfacial Water Alignment in Model Cell Membranes

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