DNA extracellular traps are part of the immune repertoire of Periplaneta americana

Abstract

Extracellular traps (ETs), web-like structures composed of DNA and histones, are released by innate immune cells in a wide range of organisms. ETs capture microorganisms, thereby avoiding their spread, and also concentrate antimicrobial molecules, which helps to kill microbes. Although vertebrate innate immune systems share homology with the insect immune system, ETosis have yet to be characterized in insects. Here, we report that the hemocytes of the hemimetabolous insect Periplaneta americana release ETs upon in vitro stimulation. We further discuss the relationship between ETs and nodulation and in controlling bacterial spread in vivo.

Galleria mellonella (Lepidoptera: Pyralidae) Hemocytes Release Extracellular Traps That Confer Protection Against Bacterial Infection in the Hemocoel

“…6 [online only] ). These findings, in addition to studies mentioned previously, indicate that extracellular DNA release may be common in insects and can be induced by different types of microbes (e.g., bacteria and fungi) ( Altincicek et al 2008 , Nascimento et al 2018 , Grahl et al 2020 ). Future studies are required to determine the prevalence and specificity of extracellular DNA release in insects.…”

“…Hemolymph coagulation potentially enhanced EPEC killing by increasing local concentration of ROS and cytotoxic quinones produced by melanization and granule contents (e.g., lysozyme) released by the degranulation of granulocytes ( Chain and Anderson 1983 , Nappi et al 1995 ). A recent study found that Periplaneta americana hemocytes may also release DNA ex vivo which immobilize bacteria ( Nascimento et al 2018 ). However, release of ETs has not previously been documented in vivo in insects to our knowledge and represents a novel form of insect immune response against microbial pathogens in addition to the typical insect antimicrobial immune responses (i.e., melanization, hemolymph coagulation, AMP production, phagocytosis, and nodulation).…”

“…However, evidence of ETosis in insects, the most diverse group of animals, remains ambiguous. A study reported extracellular DNA release by Periplaneta americana hemocytes ex vivo after stimulation with delipidated lipopolysaccharide (LPS) and DH5α Escherichia coli (Migula) (Enterobacterales: Enterobacteriaceae) ( Nascimento et al 2018 ). However, the study lacked controls (i.e., blank stimulation) to account for potential experimental artifacts (e.g., mechanical lysis of hemocytes during handling and spontaneous DNA release) and the hemocyte type(s) involved remain unknown.…”

Structure-Function Insights of Jaburetox and Soyuretox: Novel Intrinsically Disordered Polypeptides Derived from Plant Ureases

“…Another important immune response is the release of extracellular nucleic acid traps [96]. This immune mechanism of vertebrates and invertebrates is characterized by ROS-dependent release of chromatin into the cytoplasm, promoting the association of the nuclear material with antimicrobial proteins.…”

“…This immune mechanism of vertebrates and invertebrates is characterized by ROS-dependent release of chromatin into the cytoplasm, promoting the association of the nuclear material with antimicrobial proteins. Thereafter, this complex is released to the extracellular medium to withstand infections [96,97]. In this context, considering the changes in gene expression and nuclear condensation induced by Jaburetox in R. prolixus, experiments were designed to evaluate the impact of Jaburetox on the interactions of nucleic acids (DNA and RNA) extracted from the same insect species and used to mimic extracellular nucleic acid traps.…”