Membrane Fusion Induced by the Catalytic Activity of a Phospholipase C/Sphingomyelinase from <i>Listeria monocytogenes</i>

Montes, L. Ruth; Goñi, Félix M.; Johnston, Norah C.; Goldfine, Howard; Alonso, Alicia

doi:10.1021/bi0352522

Cited by 34 publications

(24 citation statements)

References 35 publications

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“…PlcB is secreted at acidic pH, which restricts its action to the lumen of L. monocytogenes-containing phagosomes (202). The dual enzymatic activity of PlcB as a PLase/SMase allows membrane fusion, which could be important for L. monocytogenes cell-to-cell spreading (203). Both the lecithinase and the SMase C activities of this enzyme are important for bacterial spread in cultured cells (189,204).…”

Section: Phospholipase Csmentioning

confidence: 99%

Bacterial Sphingomyelinases and Phospholipases as Virulence Factors

Flores-Dı́az

Monturiol-Gross

Naylor

et al. 2016

Microbiol Mol Biol Rev

163

130

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SUMMARYBacterial sphingomyelinases and phospholipases are a heterogeneous group of esterases which are usually surface associated or secreted by a wide variety of Gram-positive and Gram-negative bacteria. These enzymes hydrolyze sphingomyelin and glycerophospholipids, respectively, generating products identical to the ones produced by eukaryotic enzymes which play crucial roles in distinct physiological processes, including membrane dynamics, cellular signaling, migration, growth, and death. Several bacterial sphingomyelinases and phospholipases are essential for virulence of extracellular, facultative, or obligate intracellular pathogens, as these enzymes contribute to phagosomal escape or phagosomal maturation avoidance, favoring tissue colonization, infection establishment and progression, or immune response evasion. This work presents a classification proposal for bacterial sphingomyelinases and phospholipases that considers not only their enzymatic activities but also their structural aspects. An overview of the main physiopathological activities is provided for each enzyme type, as are examples in which inactivation of a sphingomyelinase- or a phospholipase-encoding gene impairs the virulence of a pathogen. The identification of sphingomyelinases and phospholipases important for bacterial pathogenesis and the development of inhibitors for these enzymes could generate candidate vaccines and therapeutic agents, which will diminish the impacts of the associated human and animal diseases.

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Section: Phospholipase Csmentioning

confidence: 99%

Bacterial Sphingomyelinases and Phospholipases as Virulence Factors

Flores-Dı́az

Monturiol-Gross

Naylor

et al. 2016

Microbiol Mol Biol Rev

163

130

View full text Add to dashboard Cite

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“…The escape of L. monocytogenes from vacuoles is also facilitated by a phosphatidylinositol-specific phospholipase C (PlcA) and a broad-range phospholipase C (PlcB) (238). Whereas Goldfine and colleagues showed that PlcA promotes phagosomal escape by activating the host PKCβ (239, 240), the involvement of PlcB in this process is attributed to a wide-spectrum activity again phospholipids and to an ability to mediate membrane fusion (241, 242). The interplay between LLO and the phospholipases C (PLCs) is not completely understood, but it is possible that these Listerial factors synergistically destabilize the membrane to promote optimal escape from the phagosome.…”

Section: Infection Of Macrophages By Cytosolic Bacteriamentioning

confidence: 99%

Strategies Used by Bacteria to Grow in Macrophages

Mitchell

Chen²,

Portnoy

2016

Microbiol Spectr

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Intracellular bacteria are often clinically relevant pathogens that infect virtually every cell type found in host organisms. However, myeloid cells, especially macrophages, constitute the primary cells targeted by most species of intracellular bacteria. Paradoxically, macrophages possess an extensive antimicrobial arsenal and are efficient at killing microbes. In addition to their ability to detect and signal the presence of pathogens, macrophages sequester and digest microorganisms using the phagolysosomal and autophagy pathways or, ultimately, eliminate themselves through the induction of programmed cell death. Consequently, intracellular bacteria influence numerous host processes and deploy sophisticated strategies to replicate within these host cells. Although most intracellular bacteria have a unique intracellular life cycle, these pathogens are broadly categorized into intravacuolar and cytosolic bacteria. Following phagocytosis, intravacuolar bacteria reside in the host endomembrane system and, to some extent, are protected from the host cytosolic innate immune defenses. However, the intravacuolar lifestyle requires the generation and maintenance of unique specialized bacteria-containing vacuoles and involves a complex network of host-pathogen interactions. Conversely, cytosolic bacteria escape the phagolysosomal pathway and thrive in the nutrient-rich cytosol despite the presence of host cell-autonomous defenses. The understanding of host-pathogen interactions involved in the pathogenesis of intracellular bacteria will continue to provide mechanistic insights into basic cellular processes and may lead to the discovery of novel therapeutics targeting infectious and inflammatory diseases.

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“…To overcome this problem, one can apply a technique that allows direct observation of mixing of the inner monolayer lipids (26). Naturally, this occurs only when a fusion process takes place, and thus detection of intervesicular mixing of inner monolayer lipids is diagnostic for vesiclevesicle fusion.…”

Section: Lipid Mixing Assaysmentioning

confidence: 99%

“…To our knowledge, studies in our laboratory were the first to describe model membrane fusion promoted by the catalytic activity of an enzyme, phospholipase C from Bacillus cereus (39). Later studies reported fusion induced by other phospholipases C and sphingomyelinases (16,26,40), and described intervesicular mixing of inner monolayer lipids as a novel marker for fusion (41). Montes et al (16) described the time-resolved process of aggregation, total lipid mixing, inner monolayer lipid mixing, and aqueous contents mixing, which started with increasing lag times after enzyme addition.…”

Section: Vesicle-vesicle Fusionmentioning

confidence: 99%

Histones Cause Aggregation and Fusion of Lipid Vesicles Containing Phosphatidylinositol-4-Phosphate

Lete

Sot

Gil

et al. 2015

Biophysical Journal

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In a previous article, we demonstrated that histones (H1 or histone octamers) interact with negatively charged bilayers and induce extensive aggregation of vesicles containing phosphatidylinositol-4-phosphate (PIP) and, to a lesser extent, vesicles containing phosphatidylinositol (PI). Here, we found that vesicles containing PIP, but not those containing PI, can undergo fusion induced by histones. Fusion was demonstrated through the observation of intervesicular mixing of total lipids and inner monolayer lipids, and by ultrastructural and confocal microscopy studies. Moreover, in both PI- and PIP-containing vesicles, histones caused permeabilization and release of vesicular aqueous contents, but the leakage mechanism was different (all-or-none for PI and graded release for PIP vesicles). These results indicate that histones could play a role in the remodeling of the nuclear envelope that takes place during the mitotic cycle.

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Membrane Fusion Induced by the Catalytic Activity of a Phospholipase C/Sphingomyelinase from Listeria monocytogenes

Cited by 34 publications

References 35 publications

Bacterial Sphingomyelinases and Phospholipases as Virulence Factors

Bacterial Sphingomyelinases and Phospholipases as Virulence Factors

Strategies Used by Bacteria to Grow in Macrophages

Histones Cause Aggregation and Fusion of Lipid Vesicles Containing Phosphatidylinositol-4-Phosphate

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