Exocytic fusion reduces membrane tension, and vesicle-vesicle fusion events provide a patch as a replacement for the membrane barrier missing at the disruption site. Plasma membrane repair relies on the coordinated activity of repair machinery, which carries out vesicle fusion to the membrane, membrane shedding, and polymerization of F-actin at the site of repair (Horn & Jaiswal, 2018). Mechanochemical feedback control of dynamin independent endocytosis modulates membrane tension in adherent cells, Long-term Potentiation of Wound-induced Exocytosis and Plasma Membrane Repair Is Dependant on cAMP-response Element-mediated Transcription via a Protein Kinase C-and p38 MAPK-dependent Pathway. Annexins are a class of calcium-sensitive proteins that rapidly accumulate at the site of a membrane injury (Potez et al., 2011). EHD2 localization at caveolae results from its affinity for phosphatidylinositol 4,5-bisphosphate (PIP2), which is enriched around the caveolae boundary (Parton & Del Pozo, 2013; Simone, Caplan, & Naslavsky, 2013). Stem cell extracellular vesicles: extended messages of regeneration, Annual review of pharmacology and toxicology. We use cookies to give you the best browsing experience. They consist of a variety of lipid mediators derived from the omega-3 essential fatty acids, eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), and include lipoxins, resolvins and protectins. We here review what is known about the cellular and molecular mechanisms of membrane repair, with particular emphasis on the relevance of repair as it relates to disease pathologies. The most abundant component of the cells plasma membrane is the lipids. Phosphatidylinositol is found in many cell types and tissues, but is particularly abundant in the brain. government site. A single cell is often a complete organism in itself, such as a bacterium or yeast. Calcium can activate proteins directly, and ultimately is the initiator of many downstream repair pathways. Scheffer LL, Sreetama SC, Sharma N, Medikayala S, Brown KJ, Defour A, & Jaiswal JK (2014). While much attention has been paid to the involvement of proteins in the membrane repair pathway, the role of lipids in facilitating plasma membrane repair remains poorly studied. Spaeth C, Fan J, Spaeth E, Robison T, Wilcott R, & Bittner G (2012). Cambridge (MA): Harvard Stem Cell Institute; 2008. Limiting the spread of lipid hydroperoxides may also explain the beneficial effect of vitamin E treatment on plasma membrane repair (Howard, McNeil, & McNeil, 2011; Labazi et al., 2015). Similar inter-leaflet heterogeneity exists among sphingolipids, with the glycosphingolipids maintained exclusively in the outer leaflet. Therefore, injury-triggered protein-lipid interactions that result in modified lipids generates signaling that allows for changes in activity and localization of plasma membrane repair machinery. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). When a crack moves from the scallops stiff material to the less stiff one, the latter reduces the force at the tip of the crack, thereby stopping it from spreadingfarther. As described above, damage to the plasma membrane transiently increases the mobility of individual lipids. As discussed above, sphingolipids in the plasma membrane are an important regulator of plasma membrane repair. Just like cells have membranes to hold everything in, these mini-organs are also bound in a double layer of phospholipids to insulate their little compartments within the larger cells. One signaling function of lipids is the recruitment of peripheral membrane proteins to the plasma membrane. Injury to the plasma membrane also changes the biochemical environment within the cell. This allows for the movement and patterning of lipids into signaling domains, changing the spatial arrangement of proteins that selectively interact with a particular lipid species. Epub 2008 Oct 9. While lipids are often ascribed a metabolic role as energy storage molecules, they also play important structural and signaling roles in the cell. 2022 Dec 1;11(1):38. doi: 10.1186/s13619-022-00141-8. They break down excess or worn-out cell parts. McDade JR, Archambeau A, & Michele DE (2014). Weisleder N, Takizawa N, Lin P, Wang X, Cao C, Zhang Y, Chen P-J (2012). Palmitate-mediated disruption of the endoplasmic reticulum decreases intracellular vesicle motility. Accessibility What's found inside a cell. Sheng R, Chen Y, Gee HY, Stec E, Melowic HR, Blatner NR, Fujiwara TK (2012). "Think of a . Newer pharmacological approaches for antioxidant neuroprotection in traumatic brain injury. Membrane tension: A challenging but universal physical parameter in cell biology, Paper presented at the Seminars in cell & developmental biology. (C) Plasma membrane is dynamic and individual lipids have the capacity to move laterally within a leaflet (shown in pink) and between the leaflets (shown in blue). Front Cell Dev Biol. Thus, DAG acts as a scaffold that initiates and coordinates downstream signaling pathways within a tight spatial and temporal window rather than as a marker of membrane injury for fast-acting structural proteins. In. Instead, distinct inter- and intra-leaflet heterogeneity exists. For example, membrane shedding is a known mechanism of plasma membrane repair, which functions to limit the lateral expansion of the wound area (Andrews, Almeida, & Corrotte, 2014; Horn & Jaiswal, 2018). For plasma membrane repair to occur successfully, the cell must possess a means to sense that injury has occurred, coordinate the change in activity and localization of repair machinery, and ultimately close the wounded area. The calcium influx, Survival from bacterial pore-forming toxins, Survival from bacterial pore-forming toxins utilizes both exocytic and endocytic responses. These membrane invaginations require the presence of caveolin proteins, loss of which can result in poor membrane repair and muscular dystrophy (Gazzerro, Sotgia, Bruno, Lisanti, & Minetti, 2010; Minetti et al., 1998). Das S, Yin T, Yang Q, Zhang J, Wu YI, & Yu J (2015). This is due to their lack of integration into the membrane under normal lipid packing conditions. The spatial arrangement of lipids at the plasma membrane is not only important for GTPase recruitment, but also for their activity. Unlike Annexin 5 that forms a lattice structure at the wound edge (Bouter et al., 2011), Annexins A4 and A6 work together to mediate constriction of the wounded edges of the plasma membrane, aiding in the closure of the wound (Boye et al., 2017). Rather than these roles being separated from each other, they overlap significantly such that one can easily be an extension of the other. Wound closure is mediated in part by the interactions of the cortical actin cytoskeleton with the plasma membrane. Cell damage (also known as cell injury) is a variety of changes of stress that a cell suffers due to external as well as internal environmental changes. Each month, well bring you a selection of compelling updates to this ever-growing library of biological strategies and innovations. Clipboard, Search History, and several other advanced features are temporarily unavailable. The wounded cell can survive if a rapid repair response is mounted that restores boundary integrity. Subsequent insult(s) of eccentric stretch result in a more severe wound and global hypercontraction, producing fiber retraction within the muscle bundle (53). The product of PC metabolism by PLD is the signaling lipid PA (Cazzolli, Shemon, Fang, & Hughes, 2006). In bacterial and plant cells, a cell wall is attached to the plasma membrane on its outside surface. The radiation could prevent the DNA from replicating correctly. Arp2/3-mediated F-actin formation controls regulated exocytosis in vivo. cell, in biology, the basic membrane-bound unit that contains the fundamental molecules of life and of which all living things are composed. Unable to load your collection due to an error, Unable to load your delegates due to an error, Examples of self-repairing cells. Lipids also interact with plasma membrane localized proteins to regulate membrane tension and fluidity. By direct imaging of skeletal myofibers during the course of repair from a focal injury, exposure of PS on the injured myofiber surface was found to attract macrophages to the injury site. These examples illustrate the far-reaching consequence of lipid movement on structural stability of the plasma membrane and its ability to successfully repair. Plasma membrane damage needs to be rapidly repaired to avoid cell death. Bacterial pore-forming, What might membrane injury to muscle fibers look like? The antioxidant requirement for plasma membrane repair in skeletal muscle. Marg A, Schoewel V, Timmel T, Schulze A, Shah C, Daumke O, & Spuler S (2012). These phospholipids are derived from glycerol-3-phosphate, itself a product of cellular metabolism that is enzymatically modified into phosphatidic acid (PA). Epub 2012 Jul 9. Acid sphingomyelinase activity triggers microparticle release from glial cells. Alteration in this response inhibits the subsequent stages, tissue regeneration and remodeling, leading to increased tissue scarring. PA is itself generated primarily from glycerol-3-phosphate, which is a product of glycolysis. Small GTPases, such as Rho family members, associate with biological membranes via lipid modifications (ten Klooster & Hordijk, 2007); however, selectivity for the plasma membrane is regulated through the polybasic domain comprised of a cluster of positively charged amino acids (Do Heo et al., 2006; Maxwell, Zhou, & Hancock, 2018). The plasma membrane has a unique lipid composition that helps distinguish its structural and functional properties from the other internal membrane-bound compartments. The physical and molecular mechanisms by which a cell can heal membrane ruptures and rebuild damaged or missing cellular structures remain poorly understood. Accumulation of GRAF1 at the repair site occurs 2 minutes after injury, supporting its potential role in membrane remodeling following resealing. lipids) is one of the roles proposed for lysosome-mediated repair (Andrews et al., 2014; McNeil, 2002). This signaling function may occur due to the activity of the repair protein EHD2, which accumulates at the site of membrane injury and is thought to play a role in shaping membrane dynamics (Daumke et al., 2007; Demonbreun et al., 2016; Marg et al., 2012). Copyright 2015 the American Physiological Society. With larger injuries, the opposing force of membrane tension exceeds the resealing forces of lipid disorder at the edges of the disruption, negating the driving forces of spontaneous membrane resealing. 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). Calcium-activated exocytosis reduces membrane tension and promotes spontaneous repair driven by lipid disorder for injuries hundreds of nanometers in diameter. Jaiswal JK, Lauritzen SP, Scheffer L, Sakaguchi M, Bunkenborg J, Simon SM, Nylandsted J (2014). Semin Cell Dev Biol. Intriguingly, PA preferentially binds the Rho family member Rac1, resulting in nanocluster formation (Maxwell et al., 2018). 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. Translocation of existing lipid species to the site of injury provides a mechanism to recruit and activate protein machinery. Federal government websites often end in .gov or .mil. Demonbreun AR, Quattrocelli M, Barefield DY, Allen MV, Swanson KE, & McNally EM (2016). This occurs primarily through the direct interaction of PIP2 with actin-binding proteins, and change in PIP2 distribution has been shown to precede actin build-up at the plasma membrane (Nebl, Oh, & Luna, 2000; Senju & Lappalainen, 2019; Tran, Masedunskas, Weigert, & Ten Hagen, 2015). Dystrophic heart failure blocked by membrane sealant poloxamer, Cytosolic proteins can exploit membrane localization to trigger functional assembly, Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement, Phosphatidic acid signaling regulation of Ras superfamily of small guanosine triphosphatases, Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids. This phenomenon may be explained by the kinetic energy imparted on the membrane lipids by mechanical disruption, which can result in lipid mixing without relying on membrane tension (Petersen, Chung, Nayebosadri, & Hansen, 2016). Zhu H, Lin P. h., De G, Choi K. h., Takeshima H, Weisleder N, & Ma J (2012). Matsuo H, Chevallier J, Mayran N, Le Blanc I, Ferguson C, Faur J, Sadoul R (2004). The radiation could damage the cell's DNA, but the DNA repairs itself. FOIA Influx of calcium, increase in oxidation, and change in tension on the plasma membrane due to injury all trigger changes in lipid structure and behavior to initiate signaling. The chemical structure of the cell membrane makes it remarkably flexible, the ideal boundary for rapidly growing and dividing cells. Many organisms and tissues display the ability to heal and regenerate as needed for normal physiology and as a result of pathogenesis. PIP2 accumulation was observed as early as 4 seconds in mouse myofibers; however, it continued to accumulate even 1 minute post-injury suggesting a role in the later stages of repair (Demonbreun et al., 2016). Copolymers such as poloxamer 188 avoid this potential issue by only stabilizing the plasma membrane once lipid packing density is sufficiently reduced, such as after an injury. MG53 (40) shows diffuse enrichment at injury sites within 2 s of membrane injury in a calcium-independent manner (150). While PLD is also activated by calcium, recent findings have provided insight into the role of mechanical stress on initiating lipid signaling regulated by PLD (Petersen et al., 2016). EHD2 is a mechanotransducer connecting caveolae dynamics with gene transcription. Membrane lipids: where they are and how they behave. 2023 Feb 28;24(5):4647. doi: 10.3390/ijms24054647. Sood P, Lin A, Yan C, McGillivary R, Diaz U, Makushok T, Nadkarni AV, Tang SKY, Marshall WF. doi: 10.3791/50848. Further, PA is implicated in processes critical to the success of membrane repair such as vesicle fusion with the plasma membrane and GTPase signaling (Cazzolli et al., 2006; Zhang & Du, 2009). Thus, caveolae may serve a signaling function during membrane repair (see Section 4). 2008 Dec 31. This results in the replacement of half of the body's adipocytes in 8 years. The physical and molecular mechanisms by which a cell can heal membrane ruptures and rebuild damaged or missing cellular structures remain poorly understood. Blood cells called platelets release clotting factors to stop the bleeding; white blood cells rid the area of foreign materials and release molecules to coordinate healing; cells called fibroblasts start rebuilding using proteins called collagen; new blood vessels form; and skin cells called keratinocytes create the newsurface. Abstract. Survival from bacterial pore-forming toxins utilizes both exocytic and endocytic responses. These structural changes to lipids are both necessary for repair and potentially pathogenic if left uncorrected (Sreetama et al., 2018). Scattered throughout the bloodstream are lens-shaped structures that serve to plug thewound. Sealing of transected neurites of rat B104 cells requires a diacylglycerol PKC-dependent pathway and a PKA-dependent pathway, Sezgin, Levental, Mayor, & Eggeling, 2017, Gauthier, Fardin, Roca-Cusachs, & Sheetz, 2011, Miyake, McNeil, Suzuki, Tsunoda, & Sugai, 2001, Skalman, Holst, Larsson, & Lundmark, 2018, Gazzerro, Sotgia, Bruno, Lisanti, & Minetti, 2010, Petersen, Chung, Nayebosadri, & Hansen, 2016, Lee, Kai, Carlson, Groves, & Hurley, 2015, Campelo, Fabrikant, McMahon, & Kozlov, 2010, Lamb, Harper, McKinney, Rzigalinski, & Ellis, 1997, Ligeti, Dagher, Hernandez, Koleske, & Settleman, 2004, Tran, Masedunskas, Weigert, & Ten Hagen, 2015, Godin, Vergen, Prakash, Pagano, & Hubmayr, 2011, Gurtner, Werner, Barrandon, & Longaker, 2008, Taverna, Nanney, Pollins, Sindona, & Caprioli, 2011, Nojima, Freeman, Gulbins, & Lentsch, 2015. Copyright 2017, American Association for the Advancement of Science. Disclaimer. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. Cazzolli R, Shemon AN, Fang MQ, & Hughes WE (2006). Bomal E, Grandgeorge P, Yeo RJ, Candau N, Reis PM, Frauenrath H. Nat Commun. Similarly, peak PIP2 accumulation at the injury site occurred 45 seconds post-injury in Xenopus oocytes (Vaughan et al., 2014). Within a single leaflet, lateral heterogeneity is found in the form of lipid microdomains, such as the cholesterol and sphingolipid-rich domains that serve as signaling platforms to accumulate plasma membrane-associated proteins. Physico-chemical and biological considerations for membrane wound evolution and repair in animal cells. Dysferlin-mediated phosphatidylserine sorting engages macrophages in sarcolemma repair. Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, & Perez F (2014). Ceramide microdomains formed by the activity of extracellular acid sphingomyelinase near the site of injury could appear on the extracellular leaflet (resulting in endocytosis) or the inner leaflet either by selective flipping across the membrane bilayer (Pollet et al., 2018) or through diffusion of sphingomyelinase through the wounded area to act on inner leaflet sphingomyelin found proximal to the wound edge. Using these dating methods, it was inferred that fat cells (adipocytes) replace at a rate of 86% per year (BNID 103455). In addition to their structural role in shaping the physical properties of the plasma membrane, lipids also play an important signaling role in maintaining plasma membrane integrity. Rac1, a Rho family GTPase required for repair (Verboon & Parkhurst, 2015), forms nanoclusters at sites enriched in PA and PIP3, whose roles in regulating Rac1 appear to be non-overlapping (Maxwell et al., 2018). Gazzerro E, Sotgia F, Bruno C, Lisanti MP, & Minetti C (2010). For example, when humans receive a cut, they must limit blood loss. Cell wounding activates phospholipase D in primary mouse keratinocytes. Recombinant MG53 protein modulates therapeutic cell membrane repair in treatment of muscular dystrophy. Not only is the composition and organization of the plasma membrane in constant flux, the membrane itself also must interact with forces being applied to it from all directions. What might membrane injury to muscle fibers look like? (2017). We have briefly discussed how such an integral role of lipids in plasma membrane repair also extends into tissue-level repair and restoration of organ function. Membrane repair is a conserved physiologic process in multiple tissues Organ Type of mechanical force Principal cells stressed Cell wounding Bacterial pore-forming toxins oligomerize and insert in the plasma membrane of target cells forming a diffusible pore. See this image and copyright information in PMC. Calcium has been identified as the key trigger to activate an effective membrane repair response that utilizes exocytosis and endocytosis to repair a membrane tear, or remove a membrane pore. Mechanistic principles underlying regulation of the actin cytoskeleton by phosphoinositides, Regulation of actin dynamics by PI (4, 5) P2 in cell migration and endocytosis, Pro-resolving lipid mediators are leads for resolution physiology. We will highlight how lipids respond to injury and facilitate repair both at the level of individual molecules and at the bulk level by collectively altering the plasma membrane form and function. HHS Vulnerability Disclosure, Help Diz-Muoz A, Fletcher DA, & Weiner OD (2013). Int J Mol Sci. Of potential interest in this regard is the unconventional phospholipid lysobisphosphatidic acid (LBPA), which is found on endolysosomes. PA is then used to create other phospholipids including PI, PC, PS, and PE, through the use of the DAG backbone. The radiation could damage the DNA so badly that the cell dies. 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. This is achieved in part through the activity of lipid modifying enzymes, such as phospholipases, which are activated by the changing biochemical environment after injury. McNeil AK, Rescher U, Gerke V, & McNeil PL (2006). Bethesda, MD 20894, Web Policies Would you like email updates of new search results? Dr. Norma Andrews overviews the mechanisms of cellular plasma membrane repair. Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E, Clementi E. (2009).
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