Extracellular trap formation in kuruma shrimp (Marsupenaeus japonicus) hemocytes is coupled with c-type lysozyme

Koiwai, Keiichiro; Alenton, Rod Russel R.; Kondo, Hidehiro; Hirono, Ikuo

doi:10.1016/j.fsi.2016.03.039

Cited by 30 publications

(26 citation statements)

References 25 publications

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“…Catching of bacteria was also observed in the case of shrimp ETs released by M . japonicus [ 31 ] and L . vannamei [ 29 , 30 ], and the structures were further shown to kill Escherichia coli [ 29 , 30 ].…”

Section: Discussionmentioning

confidence: 99%

“…[ 28 ]. Furthermore, three groups reported of ETs being released by seawater invertebrates: shrimp Litopenaeus vannamei hemocytes [ 29 , 30 ] and shrimp Marsupenaeus japonicus [ 31 ], oyster Crassostrea gigas [ 32 ], shore crab Carcinus maenas , blue mussel Mytilus edulis but also by sea anemone Actinia equine [ 33 ]. Especially the data on A .…”

Section: Introductionmentioning

confidence: 99%

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Conservative Mechanisms of Extracellular Trap Formation by Annelida Eisenia andrei: Serine Protease Activity Requirement

2016

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Formation of extracellular traps (ETs) capturing and immobilizing pathogens is now a well-established defense mechanism added to the repertoire of vertebrate phagocytes. These ETs are composed of extracellular DNA (extDNA), histones and antimicrobial proteins. Formation of mouse and human ETs depends on enzymes (i) facilitating decondensation of chromatin by citrullination of histones, and (ii) serine proteases degrading histones. In invertebrates, initial reports revealed existence of ETs composed of extDNA and histones, and here we document for the first time that also coelomocytes, immunocompetent cells of an earthworm Eisenia andrei, cast ETs which successfully trap bacteria in a reactive oxygen species (ROS)-dependent and -independent manner. Importantly, the formation of ETs was observed not only when coelomocytes were studied ex vivo, but also in vivo, directly in the earthworm coelom. These ETs were composed of extDNA, heat shock proteins (HSP27) and H3 histones. Furthermore, the formation of E. andrei ETs depended on activity of serine proteases, including elastase-like activity. Moreover, ETs interconnected and hold together aggregating coelomocytes, a processes proceeding encapsulation. In conclusion, the study confirms ET formation by earthworms, and unravels mechanisms leading to ET formation and encapsulation in invertebrates.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Conservative Mechanisms of Extracellular Trap Formation by Annelida Eisenia andrei: Serine Protease Activity Requirement

2016

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“…Although 13 years has passed by since the discovery of ET structures, the number of reports on ETs in invertebrates is still limited. To date, it has been found that ETs are produced by the hemocytes of shrimps (Ng et al 2013 , 2015 ; Koiwai et al 2016 ), crab ( Carcinus maenas ) (Robb et al 2014 ), oyster ( Crassostrea gigas ) (Poirier et al 2014 ), gastropod slug species ( Arion lusitanicus and Limax maximus ), and snail ( Achatina fulica ) (Lange et al 2017 ). The latest reports indicate that the cells of simpler organisms, e.g., the social amoeba ( Dictyostelium discoideum ), also have an ability to release extracellular DNA with the formation of structures similar to NETs (Zhang et al 2016 ; Zhang and Soldati 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Earthworm coelomocyte extracellular traps: structural and functional similarities with neutrophil NETs

Homa

2018

Cell Tissue Res

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Invertebrate immunity is associated with natural mechanisms that include cellular and humoral elements, similar to those that play a role in vertebrate innate immune responses. Formation of extracellular traps (ETs) is a newly discovered mechanism to combat pathogens, operating not only in vertebrate leucocytes but also in invertebrate immune cells. The ET components include extracellular DNA (exDNA), antimicrobial proteins and histones. Formation of mammalian ETs depends on enzymes such as neutrophil elastase, myeloperoxidase, the citrullination of histones and protease activity. It was confirmed that coelomocytes—immunocompetent cells of the earthworm Eisenia andrei—are also able to release ETs in a protease-dependent manner, dependent or independent of the formation of reactive oxygen species and rearrangement of the cell cytoskeleton. Similar to vertebrate leukocytes (e.g., neutrophil), coelomocytes are responsible for many immune functions like phagocytosis, cytotoxicity and secretion of humoral factors. ETs formed by coelomocyte analogues to neutrophil ETs consist of exDNA, histone H3 and attached to these structures proteins, e.g., heat shock proteins HSP27. The latter fact confirms that mechanisms of ET release are conserved in evolution. The study on Annelida adds this animal group to the list of invertebrates capable of ET release, but most importantly provides insides into innate mechanisms of ET formation in lower animal taxa.

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“…In addition to vertebrates, recent studies have shown the ability of (aquatic) invertebrates including the blue mussel (Mytilus edulis), slug species (Arion lusitanicus and Limax maximus), snail (Achatina fulicato), and shore crab (Carcinus maenas) release chromatin-based ETs, termed invertebrate extracellular phagocyte traps (EPTs) [6,156]. Although the species discussed here are derived from different phyla, we decided to group them in this chapter, since studies on invertebrates have remained sparse and mostly limited to Arthropoda (crabs, shrimps) and Mollusca (mussel, snails, and slugs) [6,[91][92][93][94]156].…”

Section: Extracellular Traps In Invertebratesmentioning

confidence: 99%

“…The authors visualise ETs, 30 min after stimulation with PMA, LPS, and E. coli which were capable of entrapping and potentially killing E. coli [91]. An in vitro study showed that hemocytes from the kuruma shrimp (arthropod) release ETs upon challenge with LPS, which are able to entrap bacteria [156].…”

Section: Extracellular Traps In Invertebratesmentioning

confidence: 99%

Extracellular Traps: An Ancient Weapon of Multiple Kingdoms

Neumann

Brogden²,

Köckritz-Blickwede

2020

Biology

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The discovery, in 2004, of extracellular traps released by neutrophils has extended our understanding of the mode of action of various innate immune cells. This fascinating discovery demonstrated the extracellular trapping and killing of various pathogens by neutrophils. During the last decade, evidence has accumulated showing that extracellular traps play a crucial role in the defence mechanisms of various cell types present in vertebrates, invertebrates, and plants. The aim of this review is to summarise the relevant literature on the evolutionary history of extracellular traps used as a weapon in various kingdoms of life. Biology 2020, 9, 34 2 of 23On the basis of findings from several studies mostly performed with human and murine neutrophils, the following three different pathways that lead to the formation of ETs by innate immune cells have been identified: (1) Release of nuclear DNA by ETosis, a suicidal cell death associated with the rupture of the nuclear membrane prior to cell lysis [14,15]; (2) vesicular release of nuclear DNA by viable cells [16,17]; and (3) release of mitochondrial DNA [18,19]. However, the exact molecular mechanisms leading to one or the other phenotype of ET formation has still not been entirely clarified. A group of renowned scientists and experts on NETs has recently published an opinionated review on the subject due to the abundance of available data that has also led to some confusion in the NET/ET research community because of contradictory results and divergent scientific concepts, for example, the molecular pathways of ET formation or the origin of the DNA that forms the ET scaffold [20]. There is a strong consensus about the composition of ETs among the findings that NETs contain a high amount of granule proteins, for example, cell-type-specific proteases and other antibacterial molecules that are associated with DNA-histone complexes. However, it is still unclear how different triggers or pathways have led to phenotypical differences about the source of DNA or viability of the ET-releasing cell.Comparison of ET phenotypical differences between host species in relation to evolutionary aspects, especially by comparing data from phylogenetic groups, would help to understand the pathways of ET formation in more detail.

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Extracellular trap formation in kuruma shrimp (Marsupenaeus japonicus) hemocytes is coupled with c-type lysozyme

Cited by 30 publications

References 25 publications

Conservative Mechanisms of Extracellular Trap Formation by Annelida Eisenia andrei: Serine Protease Activity Requirement

Conservative Mechanisms of Extracellular Trap Formation by Annelida Eisenia andrei: Serine Protease Activity Requirement

Earthworm coelomocyte extracellular traps: structural and functional similarities with neutrophil NETs

Extracellular Traps: An Ancient Weapon of Multiple Kingdoms

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