Sarcolemmal repair is a slow process and includes EHD2, Effect of oxidative stress on membrane structure: small-angle X-ray diffraction analysis. 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). Modeling membrane shaping by proteins: Focus on EHD2 and NBAR domains. Idone V, Tam C, Goss JW, Toomre D, Pypaert M, Andrews NW. Liquids, mostly water, make up 70 to 90% of all living systems, and the loss of even a small percentage can mean the difference between life and death. Similarly, peak PIP2 accumulation at the injury site occurred 45 seconds post-injury in Xenopus oocytes (Vaughan et al., 2014). Calcium also initiates lipid signaling after plasma membrane injury by activating phospholipases, such as phospholipase C (PLC). Togo T, Krasieva TB, & Steinhardt RA (2000). 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). Lethal Injury (Cell Death) In many situations, the damage to a cell may be so severe that the cell cannot survive. It also holds the potential for new applications and therapeutic approaches for treating human disease. Cell membrane disruption initially stimulates repair responses in the wounded cell itself, as described in this chapter, but other cells can subsequently respond to membrane disruption to "help" repair the membrane of the injured cell. 8600 Rockville Pike 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. As muscle fibers have strong interfiber connections, muscle injuries may manifest both as shearing of the membrane from increased membrane tension and strain, as well as ripping of plasma membrane regions from fiber retraction or hypercontraction. Cells (whether entire unicellular organisms or parts of multicellular living systems) grow, metabolize nutrients (that is, chemically transform them), produce proteins and enzymes, replicate, and move. 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. When the plasma membrane of eukaryotic cells is mechanically injured, Ca 2+ influx triggers a rapid repair process that involves exocytosis (Reddy et al., 2001; McNeil, 2002; McNeil et al., 2003).Although the precise repair mechanism is still unknown, current hypotheses propose that resealing is directly mediated by the delivery of intracellular membrane to the cell surface. Miyake K, McNeil PL, Suzuki K, Tsunoda R, & Sugai N (2001). Tools. Leikina E, Defour A, Melikov K, Van der Meulen JH, Nagaraju K, Bhuvanendran S, Jaiswal JK (2015). National Library of Medicine The goal of signaling during plasma membrane repair is to generate a polarized response such that the repair machinery can be spatially and temporally localized and activated at the repair site. These observations suggest that lipids are not bystanders during the repair process, but are instead actively involved in organizing the playing field on which repair machinery operates. Necrosis is a progressive failure of essential metabolic and structural cell components usually in the cytoplasm. 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). Modular, cascade-like transcriptional program of regeneration in, R01 GM113602/GM/NIGMS NIH HHS/United States. Bethesda, MD 20894, Web Policies Thus, each of these lipids contributes significantly to the organization, structure, and function of the plasma membrane as a whole. government site. F-actin accumulation is also responsible for providing support to the newly resealed membrane, restoring tension, and preventing subsequent injury. One such mechanism is addition of more membrane via vesicle fusion (Fig 1B ). Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Phospholipids in particular show inter-leaflet heterogeneity. The plasma membrane separates the extracellular environment from the cell interior, where biochemical reactions necessary for life occur. However, to successfully repair the cell also needs to restore the barrier function of the resealed membrane. In a similar manner, PS signaling may be involved in the early recruitment of other membrane repair proteins such as dysferlin (McDade et al., 2014; Middel et al., 2016) and MG53 (Cai et al., 2009). These phospholipids are derived from glycerol-3-phosphate, itself a product of cellular metabolism that is enzymatically modified into phosphatidic acid (PA). Lipids may serve as ligands for specific proteins, or act as a scaffold to bring cytosolic proteins to the plasma membrane. Compared with cytosolic antioxidants, which can be detrimental to repair (Spaeth et al., 2012), vitamin E is membrane-localized and could therefore allow for the local buildup of oxidized lipids at the site of injury while preventing the global spread of lipid oxidation. These lipids also exist at the boundary of lipid-ordered domains, such as lipid rafts, indicating that GTPases are targeted to these regions where protein accumulation at the membrane is common (Moissoglu et al., 2014), increasing their relative signaling capacity. official website and that any information you provide is encrypted A surprise arrived when heart muscle cells were analyzed. Spatiotemporal dynamics of actin remodeling and endomembrane trafficking in alveolar epithelial type I cell wound healing. Promotion of plasma membrane repair by vitamin E. Idone V, Tam C, Goss JW, Toomre D, Pypaert M, & Andrews NW (2008). While PA mediates targeting to the membrane, Rac1 activity depends on PIP3, suggesting multiple roles for signaling lipids in GTPase activity after repair. sharing sensitive information, make sure youre on a federal The radiation could damage the cell's DNA, but the DNA repairs itself. Remorino A, De Beco S, Cayrac F, Di Federico F, Cornilleau G, Gautreau A, Coppey M (2017). Local oxidation at the site of membrane injury activates MG53 oligomerization (Cai et al., 2009), which may locally increase membrane rigidity. Plasma Membrane Repair: Norma Andrews - iBiology C-terminal di-arginine motif of Cdc42 protein is essential for binding to phosphatidylinositol 4, 5-bisphosphate-containing membranes and inducing cellular transformation, Plasma membraneCortical cytoskeleton interactions: A cell biology approach with biophysical considerations, Control of diverse subcellular processes by a single multi-functional lipid phosphatidylinositol 4, 5-bisphosphate [PI (4, 5) P2], The structural role of cholesterol in cell membranes: from condensed bilayers to lipid rafts. These structural changes to lipids are both necessary for repair and potentially pathogenic if left uncorrected (Sreetama et al., 2018). 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). Lipids contribute to cellular physiology at both an individual and population level. Similar benefits have been attributed to membrane stabilizing copolymers such as poloxamer 188, that improved repair after physiological mechanical injury (Plataki, Lee, Rasmussen, & Hubmayr, 2011), and injury to dystrophic cells (Houang et al., 2015; Yasuda et al., 2005). Membrane stabilization by modified steroid offers a potential therapy for muscular dystrophy due to dysferlin deficit, Transverse distribution of plasma membrane bilayer cholesterol: Picking sides. Copyright 2017, American Association for the Advancement of Science. Further, the addition of new membrane by increased calcium-triggered exocytosis also decreases membrane tension and is required for plasma membrane repair (Togo et al., 2000). As discussed above, sphingolipids in the plasma membrane are an important regulator of plasma membrane repair. PTRF Anchors MG53 to Cell Injury Site for Initiation of Membrane Repair. There also exists lateral heterogeneity of lipid composition within each leaflet, which is demonstrated by the formation of lipid microdomains, such as the sphingomyelin and cholesterol-rich domains that exist interspersed among the phospholipids throughout the plasma membrane (Cebecauer et al., 2018; Sezgin, Levental, Mayor, & Eggeling, 2017) (Figure 2B). 2015 Sep;45:2-9. doi: 10.1016/j.semcdb.2015.09.023. Abrams ST, Wang L, Yong J, Yu Q, Du M, Alhamdi Y, Cheng Z, Dart C, Lane S, Yu W, Toh CH, Wang G. Biomedicines. In this case, cholesterol actually increases the fluidity among these lipids, which prevents them from forming a gel-like phase that is incompatible with the overall fluid nature of the plasma membrane (Krause & Regen, 2014). The reduction in membrane tension is likely due directly to the addition of phospholipids to reduced lipid packing, as well as due in part to the cytoskeletal remodeling associated with vesicular transport at the plasma membrane. What is Mitosis? | Let's Talk Science Membrane tension: A challenging but universal physical parameter in cell biology, Paper presented at the Seminars in cell & developmental biology. Additional structural changes the plasma membrane must adopt for repair include molding the shape of the membrane to limit wound expansion as well as pulling in the membrane edges to close the wound. These examples of organizational heterogeneity, along with the differences among the lipids that comprise the plasma membrane confer a variety of structural and signaling properties to the plasma membrane and allow the plasma membrane to mount and sustain localized signaling despite being fully interconnected and fluid. The radiation could prevent the DNA from replicating correctly. Stem cell therapy in pain medicine - PMC - National Center for 2017 Jul 11;114(28):7283-7288. doi: 10.1073/pnas.1705059114. (D) The lipid make-up of the plasma membrane constantly changes. Plasma membrane integrity in health and disease: significance and MG53 (40) shows diffuse enrichment at injury sites within 2 s of membrane injury in a calcium-independent manner (150). By studying how the Trypanosoma cruzi parasite enters the cell, Andrews' laboratory discovered that an increase of intracellular calcium was triggering lysosomal . Regulation of actin binding proteins by PIP2 occurs in part through electrostatic interactions (Senju et al., 2017), suggesting that clusters of PIP2 molecules may be necessary to achieve build-up of F-actin itself. Endocytosis also occurs in response to plasma membrane injury and has been described as a mechanism for membrane resealing (Idone et al., 2008). Accessibility (B) Phospholipid biosynthesis depends on multiple inputs from metabolism (glycerol-3-phosphate) and extracellular import (choline and ethanolamine). . 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. Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E, Clementi E. (2009). HHS Vulnerability Disclosure, Help In fact, cells are able to perform hundreds, even thousands, of chemical transformations at the same time under life-friendly conditions (ambient temperature and pressure in an aqueous environment). Due to the differences in the three-dimensional conformations of membrane lipids, a change in their distribution changes the lipid packing density in a given lipid domain. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Here we will discuss the current knowledge of how lipids facilitate plasma membrane repair by regulating membrane structure and signaling to coordinate the repair response, and will briefly note how lipid involvement extends beyond plasma membrane repair to the tissue repair response. Phospholipid biosynthetic pathways require the addition of different head groups to the DAG backbone. Andrews NW, Almeida PE, & Corrotte M (2014). 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. While it is unclear whether caveolae can provide structural assistance to the damaged membrane in the context of a large membrane injury (as opposed to sub-injury threshold stress, (Sinha et al., 2011)), caveolae may still provide a signaling function during the repair process. Lipid domaindependent regulation of single-cell wound repair, Rho family GTPases bring a familiar ring to cell wound repair. Simone LC, Caplan S, & Naslavsky N (2013). Enzymes that generate lipid signaling after plasma membrane injury (in red) include the phospholipases C and D (PLC and PLD), phosphatidyloinositol kinases (PI5K and PI3K), and sphingomyelinase (SMase). In either case, the outward budding of the membrane produced by these ceramide-rich microdomains is thought to assist in microvesicle shedding. What happens when cell membrane is damaged? - Studybuff Thus, the signaling role of lipids affects membrane structure and how the wound is eventually resealed and remodeled, returning the plasma membrane to homeostasis. Analysis of Dysferlin Direct Interactions with Putative Repair Proteins Links Apoptotic Signaling to Ca. While small injuries to the plasma membrane (on the nanometer scale) can be spontaneously resealed due to the line tension imposed by plasma membrane lipids alone (McNeil & Terasaki, 2001), larger membrane injuries (on the micron scale) require a series of coordinated mechanisms to undergo repair. 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). As structural components of the plasma membrane, lipids are responsible for contributing to membrane tension, rigidity, and overall shape. 2023 Feb 28;24(5):4647. doi: 10.3390/ijms24054647. Interestingly, as a result of caveolae flattening, EHD2 dissociates from the plasma membrane and translocates to the nucleus where it alters gene transcription (Torrino et al., 2018). This dissociation has the effect of allowing Rho GTPase translocation to the membrane where it can interact with signaling lipids. and transmitted securely. Please enable it to take advantage of the complete set of features! Without adequate remodeling, the plasma membrane protein and lipid composition would change dramatically, particularly after repeat injuries, and no longer function as in its pre-injury state. This causes the exposure of the membrane hydrophobic core and allows proteins to interact with cholesterol. Repair of injured plasma membrane by rapid Ca The spatial arrangement of lipids at the plasma membrane is not only important for GTPase recruitment, but also for their activity. An organelle (think of it as a cell's internal organ) is a membrane bound structure found within a cell. 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). Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. (2017). A different model for plasma membrane repair began to emerge when mammalian cells injured mechanically or by SLO pores were found to undergo massive endocytosis, after Ca 2+ -triggered exocytosis of lysosomes ( Figure 1 C). official website and that any information you provide is encrypted These remodeling events actively promote plasma membrane repair; however, they also act as extensions of the repair response and may continue long after successful resealing in order to restore the plasma membrane to its pre-injury state. SM utilizes the ceramide (Cer) backbone and can be used to generate the signaling lipid sphingosine-1-phosphate (S1P). PIP2 dynamics after plasma membrane injury support a role for PIP2 in actin assembly during repair as its accumulation near the site of injury is generally delayed. Nakamura M, Hui J, Stjepi V, Parkhurst SM. Horn A, Van der Meulen JH, Defour A, Hogarth M, Sreetama SC, Reed A, Jaiswal JK. For example, when inserted into a region abundant in phospholipids, cholesterol has a rigidifying effect; however, the opposite can be true with sphingolipids. Self-repairing cells: How single cells heal membrane ruptures and Among these lipids, PC is the most abundant in the plasma membrane and is formed by adding choline to the DAG backbone. This allows local and functional diversity between the two leaflets as well as various parts of the single contiguous plasma membrane (Figure 2B). Survival from bacterial pore-forming toxins utilizes both exocytic and endocytic responses. Collectively, these changes enable lipids to initiate/regulate local signaling allowing precise spatial and temporal control over downstream plasma membrane repair pathways. McNeil AK, Rescher U, Gerke V, & McNeil PL (2006). Failure of injured cells to repair results in cell death and activates a tissue repair response. One signaling function of lipids is the recruitment of peripheral membrane proteins to the plasma membrane. This results in the replacement of half of the body's adipocytes in 8 years. Torrino S, Shen W-W, Blouin CM, Mani SK, de Lesegno CV, Bost P, Chambon V (2018). Bethesda, MD 20894, Web Policies What is membrane remodeling? - Studybuff Spiders turn liquid into a strong, stretchy fiber by squeezing it through a small space that helps protein molecules to connect with eachother. 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. These same processes also work to dynamically control membrane fluidity by regulating the distribution of phospholipids, sphingolipids, and cholesterol in the membrane. These mediators promote wound resolution by acting upon the immune and endothelial cells and help to control the duration and nature of the immune and phagocytic cell infiltration at the injury site (Serhan, 2014). Clipboard, Search History, and several other advanced features are temporarily unavailable. Gurtner GC, Werner S, Barrandon Y, & Longaker MT (2008). Calcium entry after plasma membrane injury is required for repair. While membrane stabilization at the time of injury appears to improve membrane repair, a chronically rigid plasma membrane may inhibit the beneficial effects of transient lipid mobility after injury. Boye TL, Maeda K, Pezeshkian W, Snder SL, Haeger SC, Gerke V, Nylandsted J. 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. Prior to increase in shear force, PLD associates with lipid rafts, physically segregated from its activator PIP2 and its substrate PC (Petersen et al., 2016). Class Mammalia (breast): Bats, cats, whales, horses, humans. Being the most abundant component of the plasma membrane, lipids are also essential player in the process of plasma membrane repair; however, much of the research committed to identifying the mechanisms of plasma membrane repair has focused on the proteins associated with plasma membrane repair (Cooper & McNeil, 2015). Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. FOIA Plasma membrane repair in health and disease. In order to balance any decrease in membrane tension, such as that caused by exocytosis, cells routinely utilize endocytosis, which reduces the membrane area and results in increased tension (Dai & Sheetz, 1995). See this image and copyright information in PMC. Further, the complexity of signaling afforded by lipids allows the cell to coordinate a highly organized response to injury across space and time (Figure 1B). Evidence suggests these pores are removed both by endosomal degradative pathways (123, 164, 280) and exosomal shedding (14, 118, 136). While initial depolymerization of the local F-actin network is thought to assist with vesicle fusion and membrane shedding, delayed accumulation of F-actin may facilitate repair either by working in coordination with myosin to pull the wounded membrane edges toward each other or by providing a barrier and stabilizing function for the newly formed membrane. This form of membrane remodeling maintains lipid homeostasis and plasma membrane functionality. Federal government websites often end in .gov or .mil. This may allow these lipids and proteins to interact with new partners that were unavailable due to spatial segregation prior to injury. Lipids also react to the changing biochemical environment to become signaling molecules that determine the spatiotemporal dynamics of protein activation (Eyster, 2007) (Figure 1B). Jimenez AJ, Maiuri P, Lafaurie-Janvore J, Divoux S, Piel M, & Perez F (2014). PS) in the inner leaflet, causes the plasma membrane to attain an overall outward curvature. For example, PIP2 interacts with actin-associated proteins, resulting in a local strengthening of the plasma membrane-cytoskeleton interface. For example, a scallop prevents structural failure from fracture because its shell is comprised of two materials of varying stiffness. Instead, distinct inter- and intra-leaflet heterogeneity exists. The plasma membrane consists of a lipid bilayer that is semipermeable. Epub 2017 Jun 26. Muscle fibers have a, Schematic representation of the structural, Schematic representation of the structural features of the protein families implicated in membrane, A cartoon depicting the potential role of dysferlin-mediated vesicle fusion in membrane repair., MeSH Use of lipidomics during epidermal wound repair identified that several of the plasma membrane lipids discussed above are enriched during wound repair. increased lipid fluidity described in Section 3) and allows for the membrane associated PLD to diffuse outward from lipid rafts and interact with PIP2 in order to metabolize PC. Transient change in lipid mobility can have many effects on plasma membrane function related to both structure and signaling, and deciphering which of these are beneficial for repair requires further studies. Lipids act as signaling molecules through their ability to directly bind or otherwise alter the activity or localization of target proteins (Figure 2B, ,C).C). Sezgin E, Levental I, Mayor S, & Eggeling C (2017). The poor repair of these patient cells can be mirrored in healthy cells by increasing their membrane lipid mobility through the removal of cholesterol or by addition of a glucocorticoid (prednisone) (Heier et al., 2013; Sreetama et al., 2018). Hall ED, Wang JA, Miller DM, Cebak JE, & Hill RL (2018). Palmitate-mediated disruption of the endoplasmic reticulum decreases intracellular vesicle motility. Roach AN, Wang Z, Wu P, Zhang F, Chan RB, Yonekubo Y, Du G (2012). Inclusion in an NLM database does not imply endorsement of, or agreement with, Why Can Membranes Can Self Repair - BikeHike Role of LBPA and Alix in multivesicular liposome formation and endosome organization, Rac1 nanoscale organization on the plasma membrane is driven by lipid binding specificity encoded in the membrane anchor. The basement membrane plays an important role in cellular functions, including those involved in healing, by controlling the binding of growth factors and their local concentrations between cell layers. Minetti C, Sotgia F, Bruno C, Scartezzini P, Broda P, Bado M, Donati MA (1998). In response to increased stress on the plasma membrane, caveolae have been proposed to act as mechanosensors, buffering membrane tension in response to mechanical stress (Cheng et al., 2015; Sinha et al., 2011). Once membrane tension is restored, the poloxamer compound is forced out of the outer membrane leaflet (Houang, Sham, Bates, & Metzger, 2018). PA is then used to create other phospholipids including PI, PC, PS, and PE, through the use of the DAG backbone. Int J Mol Sci. One of the roles of lipid mobility may be to allow for the movement of individual lipids to form microdomains near the site of injury, which has been shown to be important for repair (Vaughan et al., 2014), perhaps by facilitating lipid-mediated signaling. In bacterial and plant cells, a cell wall is attached to the plasma membrane on its outside surface. Rayens NT, Cook KJ, McKinley SA, Payne CK. 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. Self-repair: Our bodies are packages within packages. McDade JR, Archambeau A, & Michele DE (2014). calcium, which when constantly increased, induces apoptosis. In the case of lipid mobility, this principle is exemplified by the observation that decreasing the excessive lipid mobility in LGMD2B patient cells using a membrane permeant modified glucocorticoid improves repair (Sreetama et al., 2018). Tam C, Idone V, Devlin C, Fernandes MC, Flannery A, He X, Andrews NW (2010). Calcium-activated exocytosis reduces membrane tension and promotes spontaneous repair driven by lipid disorder for injuries hundreds of nanometers in diameter. Each of these provides another mechanism for generating specific membrane lipids acutely in parallel to biosynthetic inputs. 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. Living systems must maintain a proper liquid balance, which is especially difficult in dry conditions. These observations align well with the observed kinetics of membrane resealing, which suggests that plasma membrane wounds can be resealed within 30 seconds; however, restoration of membrane tension shortly afterward is required for successful membrane remodeling and completion of the repair process. Membrane Repair: Mechanisms and Pathophysiology - PubMed In addition to allowing for the lateral translocation of membrane lipids, injury-triggered increase in membrane fluidity also results in reduced lipid packing. (B) The plasma membrane is not a homogenous mixture of proteins and lipids (as in A). This homeostatic process of vesicle fusion that maintains the plasma membrane at rest also enables plasma membrane repair through regulated fusion of vesicles triggered by calcium influx following plasma membrane injury (Horn & Jaiswal, 2018; McNeil & Steinhardt, 2003). The publisher's final edited version of this article is available at, Lipids, plasma membrane, membrane injury, tissue repair. Learn whats new on AskNature by signing up for our e-newsletter. At the population level, the composition of lipids in a membrane can result in formation of signaling platforms that can change the properties of an entire membrane, enabling the cell to finely tune tension, shape, and rigidity. Curr Biol. How quickly do different cells in the body replace themselves? Very large plasma membrane disruptions (micron diameter) require membrane patching. Coping with the inevitable: how cells repair a torn surface membrane Bacterial pore-forming, What might membrane injury to muscle fibers look like? Cell membrane repair repurposes mechanisms from various cellular functions, including vesicle trafficking, exocytosis, and endocytosis, to mend the broken membrane.
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