Two-way traffic on the road to plasma membrane repair

Idone, Vincent; Tam, Christina; Andrews, Norma W.

doi:10.1016/j.tcb.2008.09.001

Cited by 126 publications

(138 citation statements)

References 71 publications

(101 reference statements)

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“…10,18 In addition, the biochemical destruction of pore-bearing membranes accompanied by simultaneous patching might be achieved by the fusion of lysosomes with the plasma membrane. 6 Our analysis confirmed that SLOperforated, recovering cells eliminate the pores by shedding them in the form of extracellular microparticles. We detected neither endocytosis nor exocytosis of internal membranes in the recovering cells.…”

Section: Discussionsupporting

confidence: 70%

“…1,2 As in particular, cells of the blood and the vascular systems are permanently exposed to potential deadly attacks by a variety of pore-forming (poly)peptides, it is not surprising that mechanisms repairing the damaged plasma membrane have evolved. [3][4][5][6] Biological effects occurring in the wake of membrane permeabilisation and its subsequent repair are multifaceted. Apart from the two obvious end points, complete recovery or death, recovering cells can newly acquire numerous (patho)physiological functions.…”

mentioning

confidence: 99%

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Intracellular Ca2+ operates a switch between repair and lysis of streptolysin O-perforated cells

et al. 2009

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Pore-forming (poly)peptides originating from invading pathogens cause plasma membrane damage in target cells, with consequences as diverse as proliferation or cell death. However, the factors that define the outcome remain unknown. We show that in cells maintaining an intracellular Ca 2 þ concentration [Ca 2 þ ] i below a critical threshold of 10 lM, repair mechanisms seal off 'hot spots' of Ca 2 þ entry and shed them in the form of microparticles, leading to [ Plasma membrane pores formed by cytotoxic proteins and peptides disrupt the permeability barrier in a target cell. Pathogens gain access and kill host cells by secreting pore-forming toxins, whereas the blood complement system utilises the pore-forming proteins of membrane attack complexes to eliminate both pathogens and the pathogen-invaded cells. 1,2 As in particular, cells of the blood and the vascular systems are permanently exposed to potential deadly attacks by a variety of pore-forming (poly)peptides, it is not surprising that mechanisms repairing the damaged plasma membrane have evolved. [3][4][5][6] Biological effects occurring in the wake of membrane permeabilisation and its subsequent repair are multifaceted. Apart from the two obvious end points, complete recovery or death, recovering cells can newly acquire numerous (patho)physiological functions. 3,7,8 A rise in intracellular Ca 2 þ concentration [Ca 2 þ ] i is critical for successful plasma membrane repair and cell recovery, 9,10 whereas an intracellular Ca 2 þ overload is held responsible for the death of pore-bearing cells. 11 In addition, Ca 2 þ influx, followed by transcriptional activation, is thought to induce a variety of biological responses associated with sublytic effects of pore-forming toxins. 3,4,7,8 Thus, it appears that the extent of [Ca 2 þ ] i elevation following pore formation determines the fate of a targeted cell. Consequently, Morgan et al. 11 suggested that in nucleated cells, an initial increase in [Ca 2 þ ] i stimulates the recovery processes, allowing the cell to withstand a limited complement attack. The recovery might be associated with cellular activation and the production of inflammatory modulators, which, in turn, amplify an ongoing inflammatory response. 3,11 The authors further hypothesised that a more severe membrane damage causes a sharp rise in [Ca 2 þ ] i , which overwhelms all recovery processes. 11 However, how [Ca 2 þ ] i determines cell fate, how the acquisition of novel functions is initiated and how the 'point of no return' is defined remain unknown.In this study, we have undertaken a simultaneous, real-time characterisation of [Ca 2 þ ] i and plasma membrane dynamics in living cells permeabilised with the bacterial pore-forming toxin streptolysin O (SLO). Our data show that the fate of SLOperforated cells is dependent on their ability to control the extent of a pore-induced elevation in [Ca 2 þ ] i . We detail Ca 2 þ -dependent mechanisms that elicit either repair or irreversible structural changes in the plasma membrane and show how intracellula...

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Section: Discussionsupporting

confidence: 70%

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confidence: 99%

Intracellular Ca2+ operates a switch between repair and lysis of streptolysin O-perforated cells

et al. 2009

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“…Cm recovers in this model, and by 24 hours post-infection the values are above control levels (Forero et al, 1999). Membrane donation by the macrophage plasma membrane upon phagocytosis requires recruitment of intracellular membranes from endosomes and lysosomes (Pitt et al, 1992;Desjardins et al, 1994a, Desjardins et al, 1994bBeron et al, 1995;Idone et al, 2008). The fusion of these membranes fulfils two purposes: extra membrane for the nascent PG, and early release of immune effectors as shown for TNF- (Murray et al, 2005(Murray et al, , 2005b.…”

Section: Macrophage Passive Membrane Propertiesmentioning

confidence: 83%

“…The majority of studies on the biogenesis and membrane composition of phagolysosomes have been made on the model of phagocytosis of latex beads by macrophages (Desjardins & Griffiths, 2003). These studies have shown highly regulated sequential acquisition into the phagosome of proteins from the plasma, endosomal and lysosomal membranes of the macrophage (Pitt et al, 1992;Desjardins et al, 1994aDesjardins et al, , 1994bDesjardins, 1995;Andrews, 1995;Beron et al, 1995;Idone et al, 2008). The compartment is thereby acidified, and with concentrated hydrolytic activity becomes a microbicidal environment.…”

Section: Parasitophorous Vacuole Membranementioning

confidence: 99%

Electrical Membrane Properties in the Model Leishmania-Macrophage

Camacho¹

2012

Patch Clamp Technique

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“…How host cell perforation by extracellular LLO has such diverse effects on target cells is not well understood. It is known that host cells can recover from perforation by moderate concentrations of pore-forming toxins (11,35,36). Fluxes of ions and small molecules subsequent to perforation elicit multiple signaling pathways that control cell repair and alert the immune system to cell damage and pathogen attack (37).…”

mentioning

confidence: 99%

The Pore-Forming Toxin Listeriolysin O Is Degraded by Neutrophil Metalloproteinase-8 and Fails To Mediate Listeria monocytogenes Intracellular Survival in Neutrophils

Arnett

Vadia

Nackerman

et al. 2014

The Journal of Immunology

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The pore-forming toxin listeriolysin O (LLO) is a major virulence factor secreted by the facultative intracellular pathogen Listeria monocytogenes. This toxin facilitates L. monocytogenes intracellular survival in macrophages and diverse nonphagocytic cells by disrupting the internalization vesicle, releasing the bacterium into its replicative niche, the cytosol. Neutrophils are innate immune cells that play an important role in the control of infections, yet it was unknown if LLO could confer a survival advantage to L. monocytogenes in neutrophils. We report that LLO can enhance the phagocytic efficiency of human neutrophils and is unable to protect L. monocytogenes from intracellular killing. To explain the absence of L. monocytogenes survival in neutrophils, we hypothesized that neutrophil degranulation leads to the release of LLO-neutralizing molecules in the forming phagosome. In support of this, L. monocytogenes is a potent inducer of neutrophil degranulation, since its virulence factors, such as LLO, facilitate granule exocytosis. Within the first few minutes of interaction with L. monocytogenes, granules can fuse with the plasma membrane at the bacterial interaction site before closure of the phagosome. Furthermore, granule products directly degrade LLO, irreversibly inhibiting its activity. The matrix metalloproteinase-8, stored in secondary granules, was identified as an endoprotease that degrades LLO, and blocking neutrophil proteases increased L. monocytogenes intracellular survival. In conclusion, we propose that LLO degradation by matrix metalloproteinase-8 during phagocytosis protects neutrophil membranes from perforation and contributes to maintaining L. monocytogenes in a bactericidal phagosome from which it cannot escape.

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Two-way traffic on the road to plasma membrane repair

Cited by 126 publications

References 71 publications

Intracellular Ca2+ operates a switch between repair and lysis of streptolysin O-perforated cells

Intracellular Ca2+ operates a switch between repair and lysis of streptolysin O-perforated cells

Electrical Membrane Properties in the Model Leishmania-Macrophage

The Pore-Forming Toxin Listeriolysin O Is Degraded by Neutrophil Metalloproteinase-8 and Fails To Mediate Listeria monocytogenes Intracellular Survival in Neutrophils

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