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. An official website of the United States government. Lethal Injury (Cell Death) In many situations, the damage to a cell may be so severe that the cell cannot survive. Bookshelf Gushchina LV, Bhattacharya S, McElhanon KE, Choi JH, Manring H, Beck EX, Weisleder N. (2017). Interestingly, several methods for PIP2 micro-domain formation may allow for this to occur after plasma membrane injury. Thus, the signaling role of lipids affects membrane structure and how the wound is eventually resealed and remodeled, returning the plasma membrane to homeostasis. Similar to the changes in tension described above, the fluidity of the plasma membrane is also dynamic after injury. 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. 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). Sreetama SC, Chandra G, Van der Meulen JH, Ahmad MM, Suzuki P, Bhuvanendran S, Jaiswal JK (2018). For example, when inserted into a region abundant in phospholipids, cholesterol has a rigidifying effect; however, the opposite can be true with sphingolipids. Diz-Muoz A, Fletcher DA, & Weiner OD (2013). Yet to be fully understood is whether core membrane repair machinery exists in all cells, or whether evolutionary adaptation has resulted in multiple compensatory repair pathways that specialize in different tissues and cells within our body. McNeil AK, Rescher U, Gerke V, & McNeil PL (2006). Lipids also interact with plasma membrane localized proteins to regulate membrane tension and fluidity. Visualizing cytoplasmic flow during single-cell wound healing in Stentor coeruleus. Calcium also initiates lipid signaling after plasma membrane injury by activating phospholipases, such as phospholipase C (PLC). Do Heo W, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, & Meyer T (2006). Glycerol-3-phosphate is used to generate PA as well as PG through the intermediate phosphatidylglycerol phosphate (PGP). 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. One dead cell is not a big problem. Despite the many different types of tissue, there is a common repair program involved in tissue repair. 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. Cholesterol interacts with both phospholipids and sphingolipids, and its interactions with these lipids play a crucial role in determining the overall physical properties of the plasma membrane. Johnson JL, Erickson JW, & Cerione RA (2012). This Goldilocks principle applies to several aspects of lipid involvement in the repair process. Demonbreun AR, Quattrocelli M, Barefield DY, Allen MV, Swanson KE, & McNally EM (2016). Arun SN, Xie D, Howard AC, Zhong Q, Zhong X, McNeil PL, & Bollag WB (2013). Each of these pathways that facilitate repair through membrane remodeling also alter the local composition and distribution of plasma membrane lipids in healthy cells (van Meer, 1989) (Figure 2D). How does the cell membrane self heal? 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. Int J Mol Sci. 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 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). However, to successfully repair the cell also needs to restore the barrier function of the resealed membrane. From PA, cells generate DAG, or cytidine diphosphate-DAG (CDP-DAG), which serve as inputs into the phospholipid biosynthetic pathways (Figure 1A, ,B).B). and transmitted securely. It also holds the potential for new applications and therapeutic approaches for treating human disease. All of the above mechanisms for regulating the physical properties of the membrane play important roles in determining how a cell responds to plasma membrane injury and undergoes successful repair. Class Mammalia (breast): Bats, cats, whales, horses, humans. Thus, each of these lipids contributes significantly to the organization, structure, and function of the plasma membrane as a whole. Healing, Examples of self-repairing cells. Sezgin E, Levental I, Mayor S, & Eggeling C (2017). Repeated eccentric exercise in healthy subjects (i.e., stepping down for 20 min) is known to induce damage so severe that muscle fibers degenerate over the following days and weeks (91, 131, 199). By studying how the Trypanosoma cruzi parasite enters the cell, Andrews' laboratory discovered that an increase of intracellular calcium was triggering lysosomal . One model explaining membrane injury in dystrophin-deficient muscle fibers proposes that an initial injury causes a local influx of calcium and a local region of hypercontraction. However, ceramide formation also changes membrane dynamics by forming rigid microdomains and potentially by displacing cholesterol from lipid rafts (London, 2004). The antioxidant requirement for plasma membrane repair in skeletal muscle. When cells have DNA damage but fail to undergo apoptosis, they may be on the road to cancer. Abstract. Their localization and function in response to injury is controlled by the patterning of anionic lipids such as PS, which is present at the wound edge and is a known binding partner of annexins (Gerke, Creutz, & Moss, 2005). Analysis of Dysferlin Direct Interactions with Putative Repair Proteins Links Apoptotic Signaling to Ca. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). PI5K activity is itself driven by regulators of membrane repair including Rho GTPases (Gilmore & Burridge, 1996) and PLD (Roach et al., 2012). Lipids may serve as ligands for specific proteins, or act as a scaffold to bring cytosolic proteins to the plasma membrane. "Think of a . Endocytosis can also occur at sites of membrane invagination known as caveolae, and caveolae internalization has been implicated in membrane repair (Corrotte et al., 2013). Plasma membrane lipids help with successful repair by being part of the affected entity that also works to sense membrane injury, providing spatial and temporal cues to trigger signaling for downstream repair pathways, and ultimately being the benefactor of the successful wound repair response. 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. Changing the head group attached to the DAG backbone creates different phospholipid species, which include phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylserine (PS), phosphatidylinositol (PI), phosphatidylglycerol (PG), and PA (Oropeza, 2017) (Figure 1B). This results in the replacement of half of the body's adipocytes in 8 years. 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). 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). Structure and Composition of the Cell Membrane. The MG53 binding protein PTRF (cavin-1) binds cholesterol in response to membrane injury (Zhu et al., 2012). Would you like email updates of new search results? However, excessive force applied to the membrane can result in physical damage, such as the shear force applied on the endothelial cells by blood flow, on muscle cells during contraction, on lung alveolar cells during breathing, or by a blunt force trauma to any cell (Cong, Hubmayr, Li, & Zhao, 2017; Demonbreun & McNally, 2016; McNeil & Steinhardt, 2003). While the structural importance of plasma membrane cholesterol is well appreciated, it can also play a role in signaling. 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). For example, venomous snakes store precursor molecules to instantly synthesize a suite of toxins via enzyme-mediated cascades. Eukaryotic cells have been confronted throughout their evolution with potentially lethal plasma membrane injuries, including those caused by osmotic stress, by infection from bacterial toxins and parasites, and by mechanical and ischemic stress. Muscle fibers have a complex plasma membrane network with a repeating register of deep plasma membrane invaginations called the t-tubule network. 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. These same processes also work to dynamically control membrane fluidity by regulating the distribution of phospholipids, sphingolipids, and cholesterol in the membrane. 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. Phosphatidylinositol is found in many cell types and tissues, but is particularly abundant in the brain. Remorino A, De Beco S, Cayrac F, Di Federico F, Cornilleau G, Gautreau A, Coppey M (2017). Plasma membrane damage needs to be rapidly repaired to avoid cell death. 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. Of potential interest in this regard is the unconventional phospholipid lysobisphosphatidic acid (LBPA), which is found on endolysosomes. Because membrane tension limits the ability of cellular membranes to self-seal, cellular mechanisms that reduce membrane tension can promote membrane sealing. Definition. 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). Unable to load your collection due to an error, Unable to load your delegates due to an error, Spontaneous resealing of plasma membrane injuries in the nanometer range is opposed by the forces of the underlying membrane cytoskeleton. During the G1 stage, the cell prepares for division by increasing its mass. Gauthier NC, Masters TA, & Sheetz MP (2012). Copyright 2015 the American Physiological Society. Annexin A1 deficiency does not affect myofiber repair but delays regeneration of injured muscles. FOIA For example, when humans receive a cut, they must limit blood loss. Zhu H, Lin P. h., De G, Choi K. h., Takeshima H, Weisleder N, & Ma J (2012). doi: 10.3791/50848. The structural role of lipids described above illustrates how their ability to modify the biophysical properties of the plasma membrane is beneficial for resealing. MG53 (40) shows diffuse enrichment at injury sites within 2 s of membrane injury in a calcium-independent manner (150). Curr Biol. BMC Biol. Phosphatidic acid regulation of PIPKI is critical for actin cytoskeletal reorganization. The vast majority of biochemical assembly and break down processeseven by the most complex organismsoccur within cells. These structural changes to lipids are both necessary for repair and potentially pathogenic if left uncorrected (Sreetama et al., 2018). Rayens NT, Cook KJ, McKinley SA, Payne CK. Blauch LR, Gai Y, Khor JW, Sood P, Marshall WF, Tang SKY. Accumulation of GRAF1 at the repair site occurs 2 minutes after injury, supporting its potential role in membrane remodeling following resealing. Every cell has a fatty membrane that self-assembles when placed in water, then reassembles when a breach occurs. Muscle fibers are subject to huge variations in membrane tension, due to their contractile activity. government site. 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. Lysosome fusion is required for the process of repair (Reddy, Caler, & Andrews, 2001). 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). PMC These phospholipids are derived from glycerol-3-phosphate, itself a product of cellular metabolism that is enzymatically modified into phosphatidic acid (PA). As dysferlin may only be detected at injury sites with antibodies recognizing COOH-terminal epitopes, and not several antibodies to NH. Lipid domaindependent regulation of single-cell wound repair, Rho family GTPases bring a familiar ring to cell wound repair. This helps to remodel the newly repaired plasma membrane (Middel et al., 2016), but may also serve to potentiate tissue inflammation. These examples illustrate the far-reaching consequence of lipid movement on structural stability of the plasma membrane and its ability to successfully repair. Dysferlin regulates cell membrane repair by facilitating injury-triggered acid sphingomyelinase secretion, Demonbreun AR, & McNally EM (2016). Mitochondrial fragmentation and ROS signaling in wound response and repair. When a cell's DNA is damaged, it will typically detect the damage and try to repair it. 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. MG53 nucleates assembly of cell membrane repair machinery. If the damage is beyond repair, the cell will normally send itself into apoptosis, ensuring that it will not pass on its damaged DNA. Patients with muscular dystrophy are more susceptible to injury from eccentric stretch (216), with studies in mouse models suggesting susceptibility to injury can escalate with multiple insults (53). Kinetic disruption of lipid rafts is a mechanosensor for phospholipase D, Conversion of phosphatidylcholine to phosphatidylglycerol with phospholipase D and glycerol, Journal of the American Oil Chemists Society. cell, in biology, the basic membrane-bound unit that contains the fundamental molecules of life and of which all living things are composed. While reassembly of the cortical cytoskeleton in the minutes following injury is known to restore membrane tension (described in Section 3.3), membrane remodeling also contributes to increasing tension. Palmitate-mediated disruption of the endoplasmic reticulum decreases intracellular vesicle motility. (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). Verweij FJ, Revenu C, Arras G, Dingli F, Loew D, Pegtel DM, Zimmermann P (2019). Physico-chemical and biological considerations for membrane wound evolution and repair in animal cells. and transmitted securely. However, these repair activities can also be observed at the single-cell level. Yasuda S, Townsend D, Michele DE, Favre EG, Day SM, & Metzger JM (2005). 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). Promotion of plasma membrane repair by vitamin E. Idone V, Tam C, Goss JW, Toomre D, Pypaert M, & Andrews NW (2008). The primary plasma membrane sphingolipid in mammalian cells is sphingomyelin, which utilizes a ceramide backbone (Merrill Jr, 2008). The wounded cell can survive if a rapid repair respons Membrane Repair: Mechanisms and Pathophysiology Shed microvesicles containing streptolysin-O have been shown to also contain annexins A1 and A6 (219). 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. 2022 Aug 4;11:e80778. The nanoclusters appear to form specifically at the boundary of ordered raft domains and disordered domains where signaling lipids such as PIP3 and PIP2 are found. Why does our body heal itself? 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. Pollet H, Conrard L, Cloos A-S, & Tyteca D (2018). As lipids comprise the bulk of the plasma membrane, the acts of injury, resealing, and remodeling all directly impinge upon the plasma membrane lipids. Gurtner GC, Werner S, Barrandon Y, & Longaker MT (2008). 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. Phospholipids in particular show inter-leaflet heterogeneity. Before 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). 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 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). HHS Vulnerability Disclosure, Help The primary method for PIP2 formation in cells is by the activity of PI(4)P-5 kinase (PI5K) (Kolay, Basu, & Raghu, 2016). Other cells acquire specialized functions as they mature. Living systems must maintain a proper liquid balance, which is especially difficult in dry conditions. Membrane-stabilizing copolymers confer marked protection to dystrophic skeletal muscle in vivo, Molecular Therapy-Methods & Clinical Development. Phospholipids and sphingolipids are connected by the head group choline, found on both PC and sphingomyelin (SM). In contrast, Annexin 1, one of the earliest responders to plasma membrane injury (Leikina et al., 2015; McNeil, Rescher, Gerke, & McNeil, 2006), does not appear to be essential for plasma membrane repair (Leikina et al., 2015; McNeil et al., 2006). As discussed above, sphingolipids in the plasma membrane are an important regulator of plasma membrane repair. Bouter A, Gounou C, Brat R, Tan S, Gallois B, Granier T, Brisson AR. 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. 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). government site. 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. Tailored protection against plasmalemmal injury by annexins with different Ca2+ sensitivities, Sphingolipids and the formation of sterol-enriched ordered membrane domains, Plasma membrane repair is mediated by Ca2+-regulated exocytosis of lysosomes. 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). Structurally, the conical ceramide molecule results in negative membrane curvature associated with rapid nucleation of ESCRT complex proteins (Lee, Kai, Carlson, Groves, & Hurley, 2015). The plasma membrane has a unique lipid composition that helps distinguish its structural and functional properties from the other internal membrane-bound compartments. Alteration in this response inhibits the subsequent stages, tissue regeneration and remodeling, leading to increased tissue scarring. While PLC is able to cleave PC, the classic substrate of PLC is PIP2, which upon cleavage generates the membrane bound DAG and the cytosolic inositol trisphosphate (IP3) both of which are increased after injury (Lamb, Harper, McKinney, Rzigalinski, & Ellis, 1997; Vaughan et al., 2014). 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. The common eastern firefly produces light through a chemical reaction that energizes a molecule so it can release aphoton. Howard AC, McNeil AK, & McNeil PL (2011). Intriguingly, PA preferentially binds the Rho family member Rac1, resulting in nanocluster formation (Maxwell et al., 2018). These functions also require modulating the membrane area, such as through the processes of exocytosis and endocytosis or by changing the existing membrane architecture (Kozlov & Chernomordik, 2015; Nassoy & Lamaze, 2012). 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). Miyake K, McNeil PL, Suzuki K, Tsunoda R, & Sugai N (2001). the contents by NLM or the National Institutes of Health. Federal government websites often end in .gov or .mil. Plasma membrane lipids and proteins interact with the extracellular matrix (ECM) and the cortical actin network, both of which provide sources of tension that support the structure of the membrane. High force impact or stress can cause materials that comprise living systems to separate into two or more pieces (called fracturing) or to break or burst suddenly (called rupturing). Influx of calcium from the extracellular space, as well as locally increased oxidation, both trigger lipid signaling that is required for repair. Skalman LN, Holst MR, Larsson E, & Lundmark R (2018). While lipids are often ascribed a metabolic role as energy storage molecules, they also play important structural and signaling roles in the cell. Injury to the plasma membrane also changes the biochemical environment within the cell. Instead, distinct inter- and intra-leaflet heterogeneity exists. Thus, while increase in lipid mobility following plasma membrane injury is associated with successful repair, excessive lipid mobility leading to membrane instability is detrimental to the repair process. While no defined roles for PA after membrane injury are known, PA has been observed to rapidly appear at the wound edge (Vaughan et al., 2014), which fits with the fast (650 s) timescale of PA generation by PLD (Petersen et al., 2016). 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. 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. Below we describe the biochemical signaling role of lipids in facilitating plasma membrane repair. 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. Recombinant MG53 protein modulates therapeutic cell membrane repair in treatment of muscular dystrophy. Middel V, Zhou L, Takamiya M, Beil T, Shahid M, Roostalu U, Nienhaus GU (2016). Additionally, in contrast to PS, which recruits proteins directly involved in repair, DAG appears to recruit signaling proteins such as protein kinase C (PKC) (Vaughan et al., 2014; Zuzek, Fan, Spaeth, & Bittner, 2013). Bethesda, MD 20894, Web Policies The https:// ensures that you are connecting to the 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). To do so, they must control the movement of liquids across their boundaries. FRET biosensor allows spatiotemporal observation of shear stress-induced polar RhoGDI activation. This involves a series of distinct, but mutually dependent stages including inflammation, regeneration, and remodeling of the tissue (Gurtner, Werner, Barrandon, & Longaker, 2008). If the cell is damaged beyond repair, lysosomes can help it to self-destruct in a process called programmed . For example, PIP2 interacts with actin-associated proteins, resulting in a local strengthening of the plasma membrane-cytoskeleton interface. Clipboard, Search History, and several other advanced features are temporarily unavailable. Survival from bacterial pore-forming toxins utilizes both exocytic and endocytic responses. We know first-hand some of the characteristics that make mammals unique, like having hair, being able to sweat, and producing milk through mammary glands. 2015 Sep;45:2-9. doi: 10.1016/j.semcdb.2015.09.023. lipids) is one of the roles proposed for lysosome-mediated repair (Andrews et al., 2014; McNeil, 2002). This dissociation has the effect of allowing Rho GTPase translocation to the membrane where it can interact with signaling lipids. During the repair of sarcolemmal lesions, macrophages recognize exposed phosphatidylserine at the site of . Failure or delay in these processes, as in chronic inflammatory conditions and conditions of regenerative deficit would lead to aberrant tissue remodeling resulting in fibrotic or adipogenic replacement of the lost tissue. 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). This lipid binds ALIX and is capable of budding vesicles away from the cytosol (Matsuo et al., 2004). 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. It has since become evident that in addition to resealing, remodeling of the plasma membrane through vesicle fusion (exocytosis), vesicle internalization (endocytosis), and shedding (ectocytosis) also contribute to the repair process (reviewed in (Horn & Jaiswal, 2018)). 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.
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