Caveolae internalization repairs wounded cells and muscle fibers

Corrotte, Matthias; Almeida, Patrícia E. de; Tam, Christina; Castro-Gomes, Thiago; Fernandes, Maria Cecília; Millis, Bryan A.; Cortéz, Mauro; Miller, Heather; Song, Wenxia; Maugel, Timothy K.; Andrews, Norma W.

doi:10.7554/elife.00926

Cited by 138 publications

(212 citation statements)

References 63 publications

(118 reference statements)

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“…The application of hydrogen peroxide as the primary form of reactive oxygen species in mammals also induces very rapid calcium-dependent ASM release by lysosomal exocytosis, as detected by the exposure of lysosome-associated protein LAMP1 . The lysosomal origin of released ASM is also supported by the concomitant appearance of LAMP1 on the sarcolemma surface and the release of the lysosomal β-hexosaminidase in a wound repair study (Corrotte et al, 2013).…”

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confidence: 81%

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Secretory sphingomyelinase in health and disease

Kornhuber

Rhein

Müller

et al. 2015

Biological Chemistry

124

138

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Acid sphingomyelinase (ASM), a key enzyme in sphingolipid metabolism, hydrolyzes sphingomyelin to ceramide and phosphorylcholine. In mammals, the expression of a single gene, SMPD1, results in two forms of the enzyme that differ in several characteristics. Lysosomal ASM (L-ASM) is located within the lysosome, requires no additional Zn 2+ ions for activation and is glycosylated mainly with high-mannose oligosaccharides. By contrast, the secretory ASM (S-ASM) is located extracellularly, requires Zn 2+ ions for activation, has a complex glycosylation pattern and has a longer in vivo half-life. In this review, we summarize current knowledge regarding the physiology and pathophysiology of S-ASM, including its sources and distribution, molecular and cellular mechanisms of generation and regulation and relevant in vitro and in vivo studies. Polymorphisms or mutations of SMPD1 lead to decreased S-ASM activity, as detected in patients with Niemann-Pick disease B. Thus, lower serum/ plasma activities of S-ASM are trait markers. No genetic causes of increased S-ASM activity have been identified. Instead, elevated activity is the result of enhanced release (e.g., induced by lipopolysaccharide and cytokine stimulation) or increased enzyme activation (e.g., induced by oxidative stress). Increased S-ASM activity in serum or plasma is a state marker of a wide range of diseases. In particular, high S-ASM activity occurs in inflammation of the endothelium and liver. Several studies have demonstrated a correlation between S-ASM activity and mortality induced by severe inflammatory diseases. Serial measurements of S-ASM reveal prolonged activation and, therefore, the measurement of this enzyme may also provide information on past inflammatory processes. Thus, S-ASM may be both a promising clinical chemistry marker and a therapeutic target.

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confidence: 81%

“…In fact, ASM has recently emerged as a major regulator facilitating wound repair in eukaryotic cells, such as from pore-forming toxins (Tam et al, 2010;Corrotte et al, 2013). Plasmalemmal injury-triggered Ca 2+ influx induces the fusion of lysosomes with the plasma membrane and exocytosis of ASM.…”

mentioning

confidence: 99%

Secretory sphingomyelinase in health and disease

Kornhuber

Rhein

Müller

et al. 2015

Biological Chemistry

124

138

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“…Recently, endocytosis of caveolar clusters resembling rosettes has been implicated in the removal of plasma membrane wounds (Corrotte et al, 2013), suggesting that rosettes could represent a way to endocytose relatively big areas of the plasma membrane, which could help to regulate membrane integrity.…”

Section: The Actin Cytoskeleton Regulates the Organization Of Caveolamentioning

confidence: 99%

Caveolae – mechanosensitive membrane invaginations linked to actin filaments

Echarri

Pozo

2015

Journal of Cell Science

170

209

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An essential property of the plasma membrane of mammalian cells is its plasticity, which is required for sensing and transmitting of signals, and for accommodating the tensional changes imposed by its environment or its own biomechanics. Caveolae are unique invaginated membrane nanodomains that play a major role in organizing signaling, lipid homeostasis and adaptation to membrane tension. Caveolae are frequently associated with stress fibers, a major regulator of membrane tension and cell shape. In this Commentary, we discuss recent studies that have provided new insights into the function of caveolae and have shown that trafficking and organization of caveolae are tightly regulated by stress-fiber regulators, providing a functional link between caveolae and stress fibers. Furthermore, the tension in the plasma membrane determines the curvature of caveolae because they flatten at high tension and invaginate at low tension, thus providing a tension-buffering system. Caveolae also regulate multiple cellular pathways, including RhoA-driven actomyosin contractility and other mechanosensitive pathways, suggesting that caveolae could couple mechanotransduction pathways to actin-controlled changes in tension through their association with stress fibers. Therefore, we argue here that the association of caveolae with stress fibers could provide an important strategy for cells to deal with mechanical stress.

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“…It also remains to be tested whether lysosomal Ca 2+ release can serve as a more physiological trigger of membrane repair in vivo. Importantly, in addition to provide intracellular membranes, lysosomal exocytosis is also crucial for the release of lysosomal aSMases to mediate rapid endocytosis of damaged membranes, which in turn is essential for membrane repair ( 80 ).…”

Section: Releasable Lysosome Pool Although Lysosomes Can Undergo Camentioning

confidence: 99%

“…Secreted lysosomal contents may lead to various cellular responses, including altered cell mobility and cellular transformation ( 79 ). Secretion of lysosomal acid (a)SMase is essential for membrane repair ( 80 ).…”

Section: The Biological Implications Of Lysosomal Exocytosismentioning

confidence: 99%

Lysosomal exocytosis and lipid storage disorders

Samie

2014

Journal of Lipid Research

151

178

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respective smaller building-block molecules: amino acids, monosaccharides, free fatty acids, or nucleotides ( 1-4 ). Hence, since their discovery by Christian De Duve in 1955, lysosomes have been viewed as the cell's degradation center ( 3,5 ). Lysosomes, several hundreds of them in each mammalian cell, are heterogeneous in size (100-1,000 nm) and morphology, and collectively constitute ‫ف‬ 5% of the cell volume ( 6 ). Lysosomes are filled with more than 50 different types of hydrolases: sulphatases, phosphatases, lipases, proteases, carbohydrases, and glycosidases, which effectively catabolize proteins and complex lipids into their building-block molecules ( 1, 4 ). The functions of most lysosomal hydrolytic enzymes require an acidic lumen, which is established and maintained by the vacuolarATPase (V-ATPase)... proton pumps located on the perimeter limited membrane ( 6 ). To protect the perimeter membrane and its resident membrane proteins from degradation, the inner leafl et of the lysosomal membrane is coated with a polysaccharide layer called the glycocalyx ( 7 ).The biomaterials destined for degradation are delivered to lysosomes through endocytic/phagocytic and autophagic pathways ( Fig. 1 ). Endocytosis or phagocytosis of extracellular particles or plasma membrane proteins begins with the invagination of the plasma membrane to form endocytic vesicles, which then undergo a series of maturation processes to fi rst become early endosomes, and then late endosomes [excellently reviewed in ( 5 )] ( Fig. 1 ). In the late endosomes, the destined-to-be-degraded cargo is sorted into the intraluminal vesicles via the endosomal sorting complexes required for transport system ( 5 ). Intraluminal Abstract Lysosomes are acidic compartments in mammalian cells that are primarily responsible for the breakdown of endocytic and autophagic substrates such as membranes, proteins, and lipids into their basic building blocks. Lysosomal storage diseases (LSDs) are a group of metabolic disorders caused by genetic mutations in lysosomal hydrolases required for catabolic degradation, mutations in lysosomal membrane proteins important for catabolite export or membrane traffi cking, or mutations in nonlysosomal proteins indirectly affecting these lysosomal functions. A hallmark feature of LSDs is the primary and secondary excessive accumulation of undigested lipids in the lysosome, which causes lysosomal dysfunction and cell death, and subsequently pathological symptoms in various tissues and organs. There are more than 60 types of LSDs, but an effective therapeutic strategy is still lacking for most of them. Several recent in vitro and in vivo studies suggest that induction of lysosomal exocytosis could effectively reduce the accumulation of the storage materials. Meanwhile, the molecular machinery and regulatory mechanisms for lysosomal exocytosis are beginning to be revealed. In this paper, we fi rst discuss these recent developments with the focus on the functional interactions between lipid storage and lysosomal exocytosis. We th...

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Caveolae internalization repairs wounded cells and muscle fibers

Cited by 138 publications

References 63 publications

Secretory sphingomyelinase in health and disease

Secretory sphingomyelinase in health and disease

Caveolae – mechanosensitive membrane invaginations linked to actin filaments

Lysosomal exocytosis and lipid storage disorders

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