Middel V, Zhou L, Takamiya M, Beil T, Shahid M, Roostalu U, Nienhaus GU (2016). Self-repair: Our bodies are packages within packages. These roles of lipids in plasma membrane repair include both a structural role and a signaling role. 2023 Apr 4;122(7):1355-1363. doi: 10.1016/j.bpj.2023.03.001. Modular, cascade-like transcriptional program of regeneration in, R01 GM113602/GM/NIGMS NIH HHS/United States. (A) The plasma membrane is a fluid-mosaic of lipids, including glycerophospholipids, sphingolipids, and cholesterol, as well as plasma membrane-associated proteins. Such a role of CLIC/GEEC-mediated endocytosis in membrane remodeling is also supported by the observation that CLIC/GEEC is immediately activated in response to decreased membrane tension and has the capacity to turn over large amounts of plasma membrane (Thottacherry et al., 2018). During regeneration, sphingolipids such as sphingosine 1-phosphate (S1P) are known for their growth promoting effect on tissue resident stem cells (Calise et al., 2012; Nojima, Freeman, Gulbins, & Lentsch, 2015). 2021 Apr 2;19(1):63. doi: 10.1186/s12915-021-00970-0. When cells have DNA damage but fail to undergo apoptosis, they may be on the road to cancer. Das S, Yin T, Yang Q, Zhang J, Wu YI, & Yu J (2015). Each of these lipids contributes their own qualities that affect the structural and signaling characteristics of the plasma membrane (Nicolson, 2014). Viral infection controlled by a calcium-dependent lipid-binding module in ALIX. Disruption of the cell plasma membrane is a commonplace occurrence in many mechanically challenging, biological environments. Cebecauer M, Amaro M, Jurkiewicz P, Sarmento M. J. o., achl R, Cwiklik L, & Hof M (2018). Membrane damage: Damage to the cell membrane disturbs the state of cell electrolytes, e.g. Curr Biol. Please enable it to take advantage of the complete set of features! These observations on PIP2 kinetics line up remarkably well with the accumulation of F-actin at the injury site, which begins around 30 seconds after injury and extends for several minutes (Godin, Vergen, Prakash, Pagano, & Hubmayr, 2011; Horn et al., 2017). How the cell membrane maintains the integrity of the cell? PDF Membrane damage and repair - osuchildrensmusclegroup.org These phospholipids are derived from glycerol-3-phosphate, itself a product of cellular metabolism that is enzymatically modified into phosphatidic acid (PA). Before While being a mostly non-polar molecule, owing to its steroid backbone and hydrocarbon chain, cholesterol does possess a hydroxyl group opposite the hydrocarbon chain. The signaling lipid PS is interesting in this regard due to its localization to the wound edge after injury. This site needs JavaScript to work properly. Pollet H, Conrard L, Cloos A-S, & Tyteca D (2018). The mystery of membrane organization: composition, regulation and roles of lipid rafts. Thus, it is clear that there is a need to acknowledge the role of lipids as an active participant in the processes of both cell and tissue repair. doi: 10.1016/j.cub.2017.12.034. Trends Cell Biol. However, shear force on the membrane increases the kinetic energy required for lipid mixing (i.e. and transmitted securely. Transient and local lipid peroxidation may affect membrane stabilization as peroxidation of polyunsaturated fatty acids changes head group separation and acyl chain interdigitation, increasing their molecular volume and causing formation of distinct cholesterol domains in the membrane, which increases the membrane rigidity (Jacob & Mason, 2005; Mason, Walter, & Mason, 1997). While tension acts at the level of an entire membrane, the physical properties of the individual lipids and lipid domains dynamically guide the local changes required for adapting to the change in tension. The site is secure. This involves a series of distinct, but mutually dependent stages including inflammation, regeneration, and remodeling of the tissue (Gurtner, Werner, Barrandon, & Longaker, 2008). Following this, accumulation of Annexin 4 and Annexin 6 results in folding and inward contraction of the injured membrane, respectively (Boye et al., 2017). Roach AN, Wang Z, Wu P, Zhang F, Chan RB, Yonekubo Y, Du G (2012). It is unclear what role, if any, that IP3 may have in repair, but its role in calcium signaling and the fact that injured cells secrete IP3 for hours post-injury (Lamb et al., 1997) suggest a possible signaling role in repair that may extend beyond the process of membrane resealing, which needs further investigation. The .gov means its official. Furthermore, ASM activity at the injury site would locally produce ceramide from sphingomyelin. For example, PIP2 interacts with actin-associated proteins, resulting in a local strengthening of the plasma membrane-cytoskeleton interface. We use cookies to give you the best browsing experience. In. Federal government websites often end in .gov or .mil. Sphingolipids in liver injury, repair and regeneration, Development of Biomimetic Membrane Assemblies on Microspheres for High-Throughput and Multiplexable Studies, Caveolae as plasma membrane sensors, protectors and organizers. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. The https:// ensures that you are connecting to the HHS Vulnerability Disclosure, Help Another role identified for lysosomal fusion in membrane repair is the secretion of the lipid modifying enzyme acid sphingomyelinase (ASM) (Defour et al., 2014; Tam et al., 2010). Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Quantification of membrane tension after injury to fibroblasts demonstrated that a minimum tension force was reached by approximately 30 seconds post-injury, but tension was fully restored by 80 seconds post-injury (Togo et al., 2000). One such mechanism for this may be mediated by the protein MG53. ESCRT assembly for membrane shedding is activated by the calcium-dependent ALG-2 protein, which then recruits its interacting partner ALIX leading to subsequent recruitment of the remaining complex members (Scheffer et al., 2014). Epub 2008 Mar 3. This role of lipids extends further by way of regulating the response of proteins during the repair process as well as long-term gene expression-based adaptations required for the recovery of injured cells and tissues. (2009). By studying how the Trypanosoma cruzi parasite enters the cell, Andrews' laboratory discovered that an increase of intracellular calcium was triggering lysosomal . Early observations of cells undergoing plasma membrane repair identified that membrane bound vesicles are involved in the process of membrane resealing (Bi, Alderton, & Steinhardt, 1995). These enzymes initiate signaling through the generation of new lipid species, providing an added spatial, as well as a temporal component to lipid signaling, helping to more precisely coordinate the repair response. Further, PE and PC head groups can be cleaved and replaced with serine to produce PS (Oropeza, 2017). Disclaimer. Biosci Rep. 2023 Feb 27;43(2):BSR20220765. Schematic representation of the structural features of the protein families implicated in membrane repair. This is especially important for membrane signaling functions as the liquid-ordered domains often serve to aggregate membrane-associated proteins (Cebecauer et al., 2018). Acid sphingomyelinase activity triggers microparticle release from glial cells. While a common thread in lipid signaling is the modification of a target protein, either directly or indirectly, the numerous mechanisms lipids use to achieve this outcome allows for a great diversity of signaling. 1Childrens National Health System, Center for Genetic Medicine Research, 111 Michigan Avenue NW, Washington, DC 20010-2970 USA, 2Department of Genomics and Precision Medicine, George Washington University School of Medicine and Health Sciences, Washington, DC USA. Sinha B, Kster D, Ruez R, Gonnord P, Bastiani M, Abankwa D, Johannes L (2011). National Library of Medicine PLD-mediated activation of PI5K relies on the formation of PA, which itself is able to determine the spatial localization of PI5K as well as cause its activation (Roach et al., 2012). Here the sugar (oligosaccharide) moiety faces the extracellular space interacting with other cells and extracellular ligands required for processes such as signaling, cell adhesion or intercellular interactions. While PC exists in both the inner and outer leaflet of the plasma membrane, the charged phospholipids PE, PI, and PS are almost exclusively maintained within the inner leaflet (Nicolson, 2014; van Meer, 1989). While the structural importance of plasma membrane cholesterol is well appreciated, it can also play a role in signaling. Development of cell therapy and regenerative medicine using stem cells is expanding the medical industry and businesses as well as increasing the understanding of the nature of the cell itself. In contrast to PC, sphingomyelin forms a taller and narrower cylinder, which along with the configuration of its acyl chains, allowing this lipid to pack more tightly than phospholipids (Cebecauer et al., 2018). To do so, they must control the movement of liquids across their boundaries. At each of these levels the structural and signaling aspects of lipids are critical for the cell to mount an efficient response to plasma membrane injury. EVs are known to be generated in response to plasma membrane injury of single cells, and this is required for successful repair (Jimenez et al., 2014; Scheffer et al., 2014). Slabodnick M, Prevo B, Gross P, Sheung J, Marshall W. J Vis Exp. In this way, lipids play an important role in polarizing the cellular response to an injury. Would you like email updates of new search results? Defour A, Van der Meulen JH, Bhat R, Bigot A, Bashir R, Nagaraju K, & Jaiswal JK (2014). Survival from bacterial pore-forming toxins utilizes both exocytic and endocytic responses. Houang EM, Sham YY, Bates FS, & Metzger JM (2018). Individual lipids can serve as signaling molecules on their own or through binding proteins, and chemical changes to a single lipid can initiate change in local membrane composition. Cells defend themselves from viruses, bacteria with armor of protein Muscle fibers are subject to huge variations in membrane tension, due to their contractile activity. In this review, we have discussed how lipids working at the individual as well as at the population level facilitate the proper orchestration of the repair response. In addition to their structural role, and often as an extension of it, lipids also provide a signaling function that facilitates plasma membrane repair. In mammalian cells the majority of cellular cholesterol is found in the plasma membrane, where it can make up to 50% of lipid content (Van Meer, Voelker, & Feigenson, 2008). However, uninjured muscle cells from Limb Girdle Muscular Dystrophy 2B (LGMD2B) patients show increased membrane fluidity, which is associated with their poor membrane repair ability (Sreetama et al., 2018). Why Can Membranes Can Self Repair - BikeHike In the subsequent sections, we will discuss how this is achieved and utilized by the cell. 2022 Dec 14;10(12):3256. doi: 10.3390/biomedicines10123256. As a library, NLM provides access to scientific literature. F-actin accumulation is also responsible for providing support to the newly resealed membrane, restoring tension, and preventing subsequent injury. While initial loss of cortical actin aids in repair by allowing physical access for vesicles to fuse with the plasma membrane, the accumulation of F-actin at the injury site in the minutes following injury, is also required to provide structural support to the repairing/repaired membrane and prevent additional injury due to membrane fragility (Demonbreun et al., 2016; Horn et al., 2017; Jaiswal et al., 2014; McDade, Archambeau, & Michele, 2014; Miyake et al., 2001). 2015 Sep;45:2-9. doi: 10.1016/j.semcdb.2015.09.023. Membrane proteins also help locally shape and provide rigidity to the plasma membrane by interacting with specific lipids or lipid domains (Cebecauer et al., 2018). For example, lipid composition, distribution, and inter-lipid interactions actively control the rigidity and tension acting upon the plasma membrane, which in turn regulates cellular functions such as vesicle fusion, cell motility, and membrane resealing (Diz-Muoz, Fletcher, & Weiner, 2013; Gauthier, Fardin, Roca-Cusachs, & Sheetz, 2011; Togo, Krasieva, & Steinhardt, 2000). Translocation of existing lipid species to the site of injury provides a mechanism to recruit and activate protein machinery. Epub 2023 Mar 3. Caveolinopathies: from the biology of caveolin-3 to human diseases, Annexins: linking Ca 2+ signalling to membrane dynamics, Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-45-bisphosphate. This mechanism is particularly intriguing in light of the redox-sensitive nature of MG53. The plasma membrane is not a homogenous mixture of the different lipids described above (Figure 2A). Caveolae internalization repairs wounded cells and muscle fibers, Regulation of endocytosis, exocytosis, and shape by membrane tension, Paper presented at the Cold Spring Harbor symposia on quantitative biology. An organelle (think of it as a cell's internal organ) is a membrane bound structure found within a cell. Interphase has three stages: G1, S and G2. Cells respond to mechanical stress by rapid disassembly of caveolae. Stem cell extracellular vesicles: extended messages of regeneration, Annual review of pharmacology and toxicology. Dr. Norma Andrews overviews the mechanisms of cellular plasma membrane repair. Cell Calcium. These examples illustrate the far-reaching consequence of lipid movement on structural stability of the plasma membrane and its ability to successfully repair. calcium, which when constantly increased, induces apoptosis. Lysosome - Genome.gov The vast majority of biochemical assembly and break down processeseven by the most complex organismsoccur within cells.
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