Calcium entry after plasma membrane injury is required for repair. In addition to their structural role, and often as an extension of it, lipids also provide a signaling function that facilitates plasma membrane repair. Blauch LR, Gai Y, Khor JW, Sood P, Marshall WF, Tang SKY. It also holds the potential for new applications and therapeutic approaches for treating human disease. Plasma membrane repair in health and disease. The wounded cell can survive if a rapid repair response is mounted that restores boundary integrity. Intriguingly, PA preferentially binds the Rho family member Rac1, resulting in nanocluster formation (Maxwell et al., 2018). 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). and transmitted securely. Sezgin E, Levental I, Mayor S, & Eggeling C (2017). and transmitted securely. The Biomimicry Institute empowers people to create nature-inspired solutions for a healthy planet. 2021 The Biomimicry Institute. 'Resealing' is the emergency response required for cell . Spaeth C, Fan J, Spaeth E, Robison T, Wilcott R, & Bittner G (2012). Pollet H, Conrard L, Cloos A-S, & Tyteca D (2018). Lipids may serve as ligands for specific proteins, or act as a scaffold to bring cytosolic proteins to the plasma membrane. The fluidity of the membrane is determined in part by its composition, with cholesterol and sphingolipid-rich regions being less fluid than those areas comprised primarily of phospholipids. Constitutive fusion of biosynthetic vesicles is a major mechanism for delivery of new lipids and proteins, which helps to build and maintain the plasma membrane. Cebecauer M, Amaro M, Jurkiewicz P, Sarmento M. J. o., achl R, Cwiklik L, & Hof M (2018). Inflammatory exudates provide insights into the regulation of the first stage of wound repair inflammation. In the subsequent sections, we will discuss how this is achieved and utilized by the cell. 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. Lipid-soluble molecules and some small molecules can permeate the membrane, but the lipid bilayer effectively repels the many large . (2017). Role of calcium-sensor proteins in cell membrane repair. However, these repair activities can also be observed at the single-cell level. Living systems do this using structures or waterproof materials to prevent or slow liquid movement. F-actin accumulation is also responsible for providing support to the newly resealed membrane, restoring tension, and preventing subsequent injury. The plasma membrane itself forms the barrier responsible for the hydrostatic pressure experienced by the cell, while the cortical actin cytoskeleton, focal adhesions, and extracellular matrix regulate the structural tension (Burridge & Guilluy, 2016; Gauthier et al., 2012). Similar inter-leaflet heterogeneity exists among sphingolipids, with the glycosphingolipids maintained exclusively in the outer leaflet. Marmots maintain strong bones during hibernation by building up without breakingdown. Calcium-activated exocytosis reduces membrane tension and promotes spontaneous repair driven by lipid disorder for injuries hundreds of nanometers in diameter. Gazzerro E, Sotgia F, Bruno C, Lisanti MP, & Minetti C (2010). Thus, electrostatic interaction with signaling lipids helps to facilitate GTPase localization, which is a critical feature that determines the efficiency and magnitude of the downstream response (Das et al., 2015; Yogurtcu & Johnson, 2018). Stem cell extracellular vesicles: extended messages of regeneration, Annual review of pharmacology and toxicology. As she describes, a lesion is followed by a Ca2+-dependent movement of vesicles to the plasma membrane. 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. 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). Plasma membrane lipids are routinely interconverted as a means to maintain lipid homeostasis and for lipid-mediated signaling. Furthermore, ASM activity at the injury site would locally produce ceramide from sphingomyelin. 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). Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Unauthorized use of these marks is strictly prohibited. Int J Mol Sci. In addition to regulating the patterning and activity of Rho family GTPases, lipids also have a more direct role in regulating F-actin association with the plasma membrane. 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). An organelle (think of it as a cell's internal organ) is a membrane bound structure found within a cell. 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). Yasuda S, Townsend D, Michele DE, Favre EG, Day SM, & Metzger JM (2005). The plasma membrane is not a homogenous mixture of the different lipids described above (Figure 2A). The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Many of the sphingolipids also contain a glycosidically bound carbohydrate moiety causing formation of the glycosphingolipids. Healing, Examples of self-repairing cells. However, all cells are susceptible to plasma membrane damage, which results in the mixture of the intracellular fluid and extracellular milieu and can result in death if the damage is not rapidly repaired. However, lipid signaling also helps to coordinate downstream repair pathways that result in the membrane trafficking and cytoskeletal reorganization required for repair. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Slabodnick M, Prevo B, Gross P, Sheung J, Marshall W. J Vis Exp. Sterols, or steroid alcohols, are a third type of plasma membrane lipid, with cholesterol being the predominant form found in mammalian cells. Imagine a polymer wrapper that would heal when ripped during use, but would eventually decompose when placed in a compost heap. (Biomimicry Guild unpublished report). Bethesda, MD 20894, Web Policies Senju Y, Kalimeri M, Koskela EV, Somerharju P, Zhao H, Vattulainen I, & Lappalainen P (2017). 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. 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. Lipids also interact with plasma membrane localized proteins to regulate membrane tension and fluidity. Lipid domaindependent regulation of single-cell wound repair, Rho family GTPases bring a familiar ring to cell wound repair. Modeling membrane shaping by proteins: Focus on EHD2 and NBAR domains. 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. The .gov means its official. The wounded cell can survive if a rapid repair respons Membrane Repair: Mechanisms and Pathophysiology A cartoon depicting the potential role of dysferlin-mediated vesicle fusion in membrane repair. (D) The lipid make-up of the plasma membrane constantly changes. Bouter A, Gounou C, Brat R, Tan S, Gallois B, Granier T, Brisson AR. Bi G-Q, Alderton JM, & Steinhardt RA (1995). Careers. The physical and molecular mechanisms by which a cell can heal membrane ruptures and rebuild damaged or missing cellular structures remain poorly understood. 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. Visualizing cytoplasmic flow during single-cell wound healing in Stentor coeruleus. and transmitted securely. Zhu H, Lin P. h., De G, Choi K. h., Takeshima H, Weisleder N, & Ma J (2012). Lee I-H, Kai H, Carlson L-A, Groves JT, & Hurley JH (2015). Phospholipid signalling through phospholipase D and phosphatidic acid. Spatial arrangement of lipids is also known to regulate Rho family GTPase activity (see Section 4.3). Self-repair: Our bodies are packages within packages. VBP15, a novel antiinflammatory and membranestabilizer, improves muscular dystrophy without side effects, Cellular mechanisms and signals that coordinate plasma membrane repair. 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). In. Healing of a punctured, The regeneration and reorganization of the oral apparatus (green) of, Wound healing studies in model cells such as. Ligeti E, Dagher M-C, Hernandez SE, Koleske AJ, & Settleman J (2004). PTRF presumably contributes to the translocation of MG53 to the injury-site, where MG53 is also able to bind PS and become activated in an oxidation-dependent manner (Cai et al., 2009). The signaling lipid PS is interesting in this regard due to its localization to the wound edge after injury. The observation, that endocytosis may not be required for resealing through the removal of pore-forming toxins but instead acts as a mechanosensor to buffer membrane tension, may also explain how endocytosis participates in the repair of mechanical damage, where no membrane-spanning pores need to be removed. Nakamura M, Hui J, Stjepi V, Parkhurst SM. National Library of Medicine Examples of self-repairing cells. The primary method for PIP2 formation in cells is by the activity of PI(4)P-5 kinase (PI5K) (Kolay, Basu, & Raghu, 2016). Thus, caveolae may serve a signaling function during membrane repair (see Section 4). sharing sensitive information, make sure youre on a federal The calcium influx of a membrane injury activates vesicular exocytosis and homo- and heterotypic fusion of cytoplasmic vesicles. Epub 2012 Jul 9. Cell before mitosis showing the location of the centrioles, microtubules, nuclear membrane, nucleolus, and DNA (Let's Talk Science using an image by Aldona via iStockphoto). Epub 2017 Jun 26. 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)). official website and that any information you provide is encrypted Please enable it to take advantage of the complete set of features! Structure and Composition of the Cell Membrane. J.K.J. 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. 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). The https:// ensures that you are connecting to the Influx of calcium from the extracellular space, as well as locally increased oxidation, both trigger lipid signaling that is required for repair. Do Heo W, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, & Meyer T (2006). Calcium can activate proteins directly, and ultimately is the initiator of many downstream repair pathways. Careers, Unable to load your collection due to an error. Hall ED, Wang JA, Miller DM, Cebak JE, & Hill RL (2018). In mammalian cells, lipids formed upon the phosphate and glycerol (e.g. Houang EM, Sham YY, Bates FS, & Metzger JM (2018). 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. 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. The organization of lipids within the membrane also affects the structure of underlying cortical cytoskeleton. Membrane tension: A challenging but universal physical parameter in cell biology, Paper presented at the Seminars in cell & developmental biology.
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