The DNA fibers of shrimp hemocyte extracellular traps are essential for the clearance of Escherichia coli

Ng, Tze Hann; Wu, Miao Hsien; Chang, Sheng Hsiung; Aoki, Takashi; Wang, Han Ching

doi:10.1016/j.dci.2014.10.011

Cited by 27 publications

(26 citation statements)

References 30 publications

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“…Neither the granular haemocytes nor the prohaemocytes of this animal display ETotic activity (Robb et al, 2014). Crucially, in vitro immunocytochemical studies have confirmed that externalised chromatin becomes decorated with histone H2A (Robb et al, 2014;Ng et al, 2015) with, in shrimp, the trapped E. coli permeabilised and killed on the chromatin fibres (Ng et al, 2015). Pretreatment of the chromatin nets with DNAse dismantles net structure (Robb et al, 2014) and, if added before bacterial challenge, digestion of the chromatin traps reduces the number of the bacteria caught and killed (Ng et al, 2015).…”

Section: Role In Microbial Trapping and Encapsulationmentioning

confidence: 76%

“…Crucially, in vitro immunocytochemical studies have confirmed that externalised chromatin becomes decorated with histone H2A (Robb et al, 2014;Ng et al, 2015) with, in shrimp, the trapped E. coli permeabilised and killed on the chromatin fibres (Ng et al, 2015). Pretreatment of the chromatin nets with DNAse dismantles net structure (Robb et al, 2014) and, if added before bacterial challenge, digestion of the chromatin traps reduces the number of the bacteria caught and killed (Ng et al, 2015). As yet, the co-localisation of penaeidin or other conventional AMPs on the chromatin mesh structures has not been demonstrated for either shrimp or crab, although ROS and hypercitrullinated histones would almost certainly contribute to killing on the nets.…”

Section: Role In Microbial Trapping and Encapsulationmentioning

confidence: 79%

“…1) and shrimp, L. vannamei. (Ng et al, 2015) in vitro, with the bacteria Listonella anguillarum and Escherichia coli, respectively, ensnared on the extruded DNA. The study on shrimp did not define which haemocyte type(s) display the response, but with C. maenas, the use of separated haemocyte populations in vitro has revealed that only the agranular hyaline haemocytes and the semi-granular haemocytes show the response (Robb et al, 2014).…”

Section: Role In Microbial Trapping and Encapsulationmentioning

confidence: 99%

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Antimicrobial proteins: From old proteins, new tricks

Smith

Dyrynda

2015

Molecular Immunology

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This review describes the main types of antimicrobial peptides (AMPs) synthesised by crustaceans, primarily those identified in shrimp, crayfish, crab and lobster. It includes an overview of their range of microbicidal activities and the current landscape of our understanding of their gene expression patterns in different body tissues. It further summarises how their expression might change following various types of immune challenges. The review further considers proteins or protein fragments from crustaceans that have antimicrobial properties but are more usually associated with other biological functions, or are derived from such proteins. It discusses how these unconventional AMPs might be generated at, or delivered to, sites of infection and how they might contribute to crustacean host defence in vivo. It also highlights recent work that is starting to reveal the extent of multi-functionality displayed by some decapod AMPs, particularly their participation in other aspects of host protection. Examples of such activities include proteinase inhibition, phagocytosis, antiviral activity and haematopoiesis.

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Section: Role In Microbial Trapping and Encapsulationmentioning

confidence: 76%

Section: Role In Microbial Trapping and Encapsulationmentioning

confidence: 79%

Section: Role In Microbial Trapping and Encapsulationmentioning

confidence: 99%

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Antimicrobial proteins: From old proteins, new tricks

Smith

Dyrynda

2015

Molecular Immunology

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“…ROS production is a signal that triggers ET formation in mammals [85] and lophotrochozoans [84]. In shrimp, haemocytes also release ETs in response to ROS inducers [83]. It will be of great interest to identify the haemocyte types that are involved in ETosis and determine whether the AMPs that are stored in haemocytes, such as penaeidins, contribute to the antimicrobial activity of shrimp ETs.…”

Section: (C) Shrimp Amps Encrypted In Multifunctional Proteins (I) Hamentioning

confidence: 99%

“…ETs have now been described in deuterostomes [81] and protostomes, including species of Ecdysozoa (insects [82], crustaceans [83]) and Lophotrochozoa (molluscs [84]). This process is triggered by infection and/or tissue damage.…”

Section: (C) Shrimp Amps Encrypted In Multifunctional Proteins (I) Hamentioning

confidence: 99%

Antimicrobial peptides in marine invertebrate health and disease

Destoumieux-Garzón

Rosa

Schmitt

et al. 2016

Phil. Trans. R. Soc. B

120

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One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Aquaculture contributes more than one-third of the animal protein from marine sources worldwide. A significant proportion of aquaculture products are derived from marine protostomes that are commonly referred to as 'marine invertebrates'. Among them, penaeid shrimp (Ecdysozosoa, Arthropoda) and bivalve molluscs (Lophotrochozoa, Mollusca) are economically important. Mass rearing of arthropods and molluscs causes problems with pathogens in aquatic ecosystems that are exploited by humans. Remarkably, species of corals (Cnidaria) living in non-exploited ecosystems also suffer from devastating infectious diseases that display intriguing similarities with those affecting farmed animals. Infectious diseases affecting wild and farmed animals that are present in marine environments are predicted to increase in the future. This paper summarizes the role of the main pathogens and their interaction with host immunity, with a specific focus on antimicrobial peptides (AMPs) and pathogen resistance against AMPs. We provide a detailed review of penaeid shrimp AMPs and their role at the interface between the host and its resident/pathogenic microbiota. We also briefly describe the relevance of marine invertebrate AMPs in an applied context. This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

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Antimicrobial Microwebs of DNA–Histone Inspired from Neutrophil Extracellular Traps

et al. 2019

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with antimicrobial protein granules and enzymes. [5] NETs have been observed to be lethal to a number of bacteria, [6] fungi, [7] viruses, [8] and parasites, [9] yet some pathogenic bacteria can evade NET-induced killing. [10,11] Accumulation of excessive NETs in vivo is also associated with pathology of bacterial biofilm, autoimmune disease, and even cancer. [12] These complex and sometimes contradictory observations highlight the need to investigate NET-related physiological interactions with simpler but defined NET-like biomaterials. Isolation of NETs from neutrophils requires repeated centrifugation and washing steps, [13] which often causes unpredictable loss of proteins. Moreover, NETs can be triggered via chemical stimulus, [14] virulence factors, [15] and bacteria [16] under different pathways, yielding 33 common proteins and as much as 50 variable proteins. [12] While the existing antibodies and inhibitors are employed to block and characterize the function of specific NET components, their high complexity imposes limitations. [17] Here, we take a bottom-up approach of synthesizing NET-like materials with defined composition, termed "microwebs," through sonochemical complexation of lambda phage DNA and histone in aqueous solutions. Lambda phage DNA can spontaneously polymerize into networks in the presence of histone, [18] which facilitates formation of web-like structure. Escherichia coli UTI89 was used as a model pathogen Neutrophil extracellular traps (NETs) are decondensed chromatin networks released by neutrophils that can trap and kill pathogens but can also paradoxically promote biofilms. The mechanism of NET functions remains ambiguous, at least in part, due to their complex and variable compositions. To unravel the antimicrobial performance of NETs, a minimalistic NET-like synthetic structure, termed "microwebs," is produced by the sonochemical complexation of DNA and histone. The prepared microwebs have structural similarity to NETs at the nanometer to micrometer dimensions but with welldefined molecular compositions. Microwebs prepared with different DNA to histone ratios show that microwebs trap pathogenic Escherichia coli in a manner similar to NETs when the zeta potential of the microwebs is positive. The DNA nanofiber networks and the bactericidal histone constituting the microwebs inhibit the growth of E. coli. Moreover, microwebs work synergistically with colistin sulfate, a common and a last-resort antibiotic, by targeting the cell envelope of pathogenic bacteria. The synthesis of microwebs enables mechanistic studies not possible with NETs, and it opens new possibilities for constructing biomimetic bacterial microenvironments to better understand and predict physiological pathogen responses. Biomimetics Nature uses a variety of extracellular nanofibers, such as cobwebs, [1] amyloid plaques, [2] and fibrin clots [3] to capture invading microbes. As part of human innate immunity, neutrophils squirt decondensed chromatin networks to capture and disarm bacteria and fungi-a host defense pro...

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The DNA fibers of shrimp hemocyte extracellular traps are essential for the clearance of Escherichia coli

Cited by 27 publications

References 30 publications

Antimicrobial proteins: From old proteins, new tricks

Antimicrobial proteins: From old proteins, new tricks

Antimicrobial peptides in marine invertebrate health and disease

Antimicrobial Microwebs of DNA–Histone Inspired from Neutrophil Extracellular Traps

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