Lipid Composition of Multilamellar Bodies Secreted by Dictyostelium discoideum Reveals Their Amoebal Origin

Paquet, Valérie E.; Lessire, René; Domergue, Frédéric; Fouillen, Laëtitia; Filion, Geneviève; Sedighi, Ahmadreza; Charette, Steve J.

doi:10.1128/ec.00107-13

Cited by 29 publications

(59 citation statements)

References 33 publications

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“…For instance, the self-assembly of phosphatidylcholine (PC), cholesterol, and various cosurfactants resulted in an almost identical structure to those in the cryo-TEM images reported herein but coexisting with mainly individual multilamellar vesicles (28). Multilamellar bodies in biological systems have also exhibited structures almost identical to those reported herein, suggesting the possible utility of JDSs as models (29,30).…”

Section: Resultssupporting

confidence: 63%

Janus dendrimersomes coassembled from fluorinated, hydrogenated, and hybrid Janus dendrimers as models for cell fusion and fission

Xiao

Sherman

Wilner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

203

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A three-component system of Janus dendrimers (JDs) including hydrogenated, fluorinated, and hybrid hydrogenated-fluorinated JDs are reported to coassemble by film hydration at specific ratios into an unprecedented class of supramolecular Janus particles (JPs) denoted Janus dendrimersomes (JDSs). They consist of a dumbbellshaped structure composed of an onion-like hydrogenated vesicle and an onion-like fluorinated vesicle tethered together. The synthesis of dye-tagged analogs of each JD component enabled characterization of JDS architectures with confocal fluorescence microscopy. Additionally, a simple injection method was used to prepare submicron JDSs, which were imaged with cryogenic transmission electron microscopy (cryo-TEM). As reported previously, different ratios of the same three-component system yielded a variety of structures including homogenous onion-like vesicles, core-shell structures, and completely self-sorted hydrogenated and fluorinated vesicles. Taken together with the JDSs reported herein, a self-sorting pathway is revealed as a function of the relative concentration of the hybrid JD, which may serve to stabilize the interface between hydrogenated and fluorinated bilayers. The fission-like pathway suggests the possibility of fusion and fission processes in biological systems that do not require the assistance of proteins but instead may result from alterations in the ratios of membrane composition.Janus particles | onion-like vesicles | self-sorting | fusion mechanism J anus particles (JPs) are nanoscale or microscale objects that exhibit two-faced asymmetry, enabling the presentation of vastly different chemical or physical properties localized at distinct parts of the same structure. They have been prepared as unimolecular systems in the form of dendrimers, dendrimer-like polymers, heterografted polymers, and polyhedral oligomeric silsesquioxanes; as supramolecular assemblies from lipids, block copolymers, and terpolymers and other polymers; as liquid crystals; and as inorganic nanoparticles. JPs have gained increasing attention due to their application in a variety of fields including as emulsion stabilizers, facilitators for the development of novel liquid/liquid and liquid/air interfaces among other interfacial applications, optical nanoprobes, electronic inks, self-propelling beads, targeted stealth drug delivery systems, MRI contrast agents, and theranostics agents, among other biomedical applications (1).Asymmetric molecules such as phospholipids, block copolymers, and Janus dendrimers (JDs) can be thought of as the molecularlevel equivalent of JPs. Phospholipids are the major building block of the bilayers of biological membranes. Synthetic vesicles, which mimic biological membranes, have been prepared from phospholipids and are denoted liposomes. As the result of their instability due to oxidation, phospholipids must be coassembled with cholesterol and polyethylene glycol-conjugated phospholipids to form stable liposomes (2, 3). Furthermore, time-consuming fractionation and extrusio...

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Section: Resultssupporting

confidence: 63%

Janus dendrimersomes coassembled from fluorinated, hydrogenated, and hybrid Janus dendrimers as models for cell fusion and fission

Xiao

Sherman

Wilner

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

203

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“…Interestingly, since D. discoideum cells grown in liquid medium in the absence of bacteria produce virtually no MLB (Mercer and Shaffer, 1960; Hohl, 1965; Marchetti et al, 2004; Paquet et al, 2013), it was considered that these MLBs were undigested bacterial remains. However, new evidence has shown that MLB production by D. discoideum depends largely on the metabolism of the protozoa even if the presence of digestible bacteria is required to produce MLBs.…”

Section: Bacteria Packaging: a Protozoa-driven Processmentioning

confidence: 99%

Potential role of bacteria packaging by protozoa in the persistence and transmission of pathogenic bacteria

2014

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Many pathogenic bacteria live in close association with protozoa. These unicellular eukaryotic microorganisms are ubiquitous in various environments. A number of protozoa such as amoebae and ciliates ingest pathogenic bacteria, package them usually in membrane structures, and then release them into the environment. Packaged bacteria are more resistant to various stresses and are more apt to survive than free bacteria. New evidence indicates that protozoa and not bacteria control the packaging process. It is possible that packaging is more common than suspected and may play a major role in the persistence and transmission of pathogenic bacteria. To confirm the role of packaging in the propagation of infections, it is vital that the molecular mechanisms governing the packaging of bacteria by protozoa be identified as well as elements related to the ecology of this process in order to determine whether packaging acts as a Trojan Horse.

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“…Samples from C. jejuni-T. pyriformis and C. jejuni-A. castellanii cocultures were fixed for 3 h in 0.1 M sodium cacodylate buffer (pH 7.3) containing 2% glutaraldehyde and 0.3% osmium tetroxide, embedded in Epon resin, and ultrathin sectioned following standard electron microscopy protocols, as described previously (30). The samples were then examined using transmission electron microscopy (TEM) (JEOL 1230), at 80 kV.…”

Section: Methodsmentioning

confidence: 99%

“…After their internalization, some bacteria avoid digestion by protozoa and are packaged into multilamellar bodies (MLBs), which are formed by several concentric layers of lipid membranes and then excreted into the milieu. The production of MLBs is a protozoan-mediated process (30). Acanthamoeba spp.…”

mentioning

confidence: 99%

Packaging of Campylobacter jejuni into Multilamellar Bodies by the Ciliate Tetrahymena pyriformis

Trigui

Paquet

Charette

et al. 2016

Appl Environ Microbiol

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dCampylobacter jejuni is the leading cause of bacterial gastroenteritis worldwide. Transmission to humans occurs through consumption of contaminated food or water. The conditions affecting the persistence of C. jejuni in the environment are poorly understood. Some protozoa package and excrete bacteria into multilamellar bodies (MLBs). Packaged bacteria are protected from deleterious conditions, which increases their survival. We hypothesized that C. jejuni could be packaged under aerobic conditions by the amoeba Acanthamoeba castellanii or the ciliate Tetrahymena pyriformis, both of which are able to package other pathogenic bacteria. A. castellanii did not produce MLBs containing C. jejuni. In contrast, when incubated with T. pyriformis, C. jejuni was ingested, packaged in MLBs, and then expelled into the milieu. The viability of the bacteria inside MLBs was confirmed by microscopic analyses. The kinetics of C. jejuni culturability showed that packaging increased the survival of C. jejuni up to 60 h, in contrast to the strong survival defect seen in ciliate-free culture. This study suggests that T. pyriformis may increase the risk of persistence of C. jejuni in the environment and its possible transmission between different reservoirs in food and potable water through packaging. Campylobacter jejuni is a leading cause of human gastroenteritis worldwide and a major public health problem (1-3). Severe symptoms of C. jejuni infection include high fever, watery to bloody diarrhea, nausea, and vomiting (4). In severe cases, C. jejuni is associated with serious postinfectious complications, such as Guillain-Barré syndrome (5, 6).Despite causing a serious disease in humans, C. jejuni is usually viewed as commensal in chickens (7) and livestock animals such as cattle (8) and pigs (9). Once these animals are colonized with Campylobacter spp., they excrete large numbers of the microorganisms in their feces and commonly contaminate different aquatic habitats, such as surface waters close to farming activities, agricultural runoff, wastewater effluent, sewage, and marine environments (10). Numerous epidemiological studies have demonstrated that water is not only a significant reservoir of C. jejuni but also an important factor for the spread of C. jejuni in farms, throughout flocks, and in slaughterhouses (11-15).C. jejuni requires a microaerobic environment (80% N 2 , 10% CO 2 , 5% H 2 , and 5% O 2 ) (16) and a narrow range of temperatures (37 to 43°C) for optimal growth (17). Because of the constraints imposed by its sensitivity to oxygen, C. jejuni is considered less able to tolerate environmental stress than other foodborne pathogens (18). Once outside the host, however, the interaction of C. jejuni with other microorganisms could help it survive high concentrations of oxygen and other environmental stresses.Since the study by Snelling et al. (19), in which Campylobacter and protozoa were isolated from the same broiler drinking water systems, the potential interactions between these microorganisms have been investigate...

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Lipid Composition of Multilamellar Bodies Secreted by Dictyostelium discoideum Reveals Their Amoebal Origin

Cited by 29 publications

References 33 publications

Janus dendrimersomes coassembled from fluorinated, hydrogenated, and hybrid Janus dendrimers as models for cell fusion and fission

Janus dendrimersomes coassembled from fluorinated, hydrogenated, and hybrid Janus dendrimers as models for cell fusion and fission

Potential role of bacteria packaging by protozoa in the persistence and transmission of pathogenic bacteria

Packaging of Campylobacter jejuni into Multilamellar Bodies by the Ciliate Tetrahymena pyriformis

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