A serine protease inhibitor from the hornfaced bee, Osmia cornifrons, exhibits antimicrobial activities

Lee, Kyeong Yong; Kim, Bo Yeon; Lee, Kwang-Sik; Yoon, Hyung Joo; Jin, Byung Rae

doi:10.1016/j.aspen.2015.06.004

Cited by 9 publications

(3 citation statements)

References 36 publications

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“…CvT-serpin21 was clustered with serpins involved in modulating melanization such as CvT-serpin6, Pp-serpin1O, Of-serpin3, Ag-serpin2, and Dm-serpin27A ( Ligoxygakis et al 2002 ; Chu et al 2015 ; Yan et al 2017 ; Zhang et al 2021b ; Gu et al 2022 ). In addition, the clade of (CvT-serpin3, CvT-serpin5, CvT-serpin15, CvT-serpin16, CvT-serpin18) was clustered with both anti-melanization and antimicrobial serpins ( Song et al 2008 ; Jiang et al 2009 ; Pan et al 2009 ; An et al 2012 ; Lee et al 2015 ; Liu et al 2015a ; Gu et al 2021 ; Morrow et al 2021 ; Teng et al 2022 ; Zhou et al 2023 ). CvT-serpin8 and 10, whose RCL sequences were clustered in the same branch of human alpha-1 antitrypsin, suggest that they might be related to metabolic regulation ( Rabekova et al 2021 ; O’Brien et al 2022 ).…”

Section: Resultsmentioning

confidence: 99%

Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

Wu,

Yuan,

et al. 2023

Molecular Biology and Evolution

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Parasitoids introduce various virulence factors when parasitism occurs, and some taxa generate teratocytes to manipulate the host immune system and metabolic homeostasis for the survival and development of their progeny. Host-parasitoid interactions are extremely diverse and complex, yet the evolutionary dynamics are still poorly understood. A category of serpin genes, named CvT-serpins, was discovered to be specifically expressed and secreted by the teratocytes of Cotesia vestalis, an endoparasitoid of the diamondback moth Plutella xylostella. Genomic and phylogenetic analysis indicated that the C. vestalis serpin genes are duplicated and most of them are clustered into 1 monophyletic clade. Intense positive selection was detected at the residues around the P1–P1′ cleavage sites of the Cv-serpin reactive center loop domain. Functional analyses revealed that, in addition to the conserved function of melanization inhibition (CvT-serpins 1, 16, 18, and 21), CvT-serpins exhibited novel functions, i.e. bacteriostasis (CvT-serpins 3 and 5) and nutrient metabolism regulation (CvT-serpins 8 and 10). When the host-parasitoid system is challenged with foreign bacteria, CvT-serpins act as an immune regulator to reprogram the host immune system through sustained inhibition of host melanization while simultaneously functioning as immune effectors to compensate for this suppression. In addition, we provided evidence that CvT-serpin8 and 10 participate in the regulation of host trehalose and lipid levels by affecting genes involved in these metabolic pathways. These findings illustrate an exquisite tactic by which parasitoids win out in the parasite–host evolutionary arms race by manipulating host immune and nutrition homeostasis via adaptive gene evolution and neofunctionalization.

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Section: Resultsmentioning

confidence: 99%

Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

Wu,

Yuan,

et al. 2023

Molecular Biology and Evolution

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“…In insects, serpins play a critical role in physiological processes and immune responses by regulating serine protease activities [14][15][16]. With the completion of insect genome sequencing projects, more and more serpin genes have been identified in insects.…”

Section: Introductionmentioning

confidence: 99%

A Genome-Wide Analysis of Serine Protease Inhibitors in Cydia pomonella Provides Insights into Their Evolution and Expression Pattern

Wu,

Xing,

et al. 2023

IJMS

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Serine protease inhibitors (serpins) appear to be ubiquitous in almost all living organisms, with a conserved structure and varying functions. Serpins can modulate immune responses by negatively regulating serine protease activities strictly and precisely. The codling moth, Cydia pomonella (L.), a major invasive pest in China, can cause serious economic losses. However, knowledge of serpin genes in this insect remain largely unknown. In this study, we performed a systematic analysis of the serpin genes in C. pomonella, obtaining 26 serpins from the C. pomonella genome. Subsequently, their sequence features, evolutionary relationship, and expression pattern were characterized. Comparative analysis revealed the evolution of a number of serpin genes in Lepidoptera. Importantly, the evolutionary relationship and putative roles of serpin genes in C. pomonella were revealed. Additionally, selective pressure analysis found amino acid sites with strong evidence of positive selection. Interestingly, the serpin1 gene possessed at least six splicing isoforms with distinct reactive-center loops, and these isoforms were experimentally validated. Furthermore, we observed a subclade expansion of serpins, and these genes showed high expression in multiple tissues, suggesting their important roles in C. pomonella. Overall, this study will enrich our knowledge of the immunity of C. pomonella and help to elucidate the role of serpins in the immune response.

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“…It had been widely reported that serpins are involved in humoral immunity. Besides, there are reports of serpins from species of crustacean and hymenoptera insects showing antimicrobial activity, indicating that they may function as direct effectors interacting with pathogens 34,35 …”

Section: Introductionmentioning

confidence: 99%

A serpin (CvT‐serpin15) of teratocytes contributes to microbial‐resistance in Plutella xylostella during Cotesia vestalis parasitism

Zhou

et al. 2021

Pest Management Science

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BACKGROUND Parasitic wasps are an important group of entomophagous insects for pest control. As parasitic wasps often lay eggs on or into their associated hosts, parasitoids evolve to utilize several factors including venom, polydnavirus (PDV) to alter host physiology for successful parasitism. Some taxa of endoparasitoids produce teratocytes, which are a type of cell that is released into host insects when wasp eggs hatch. Teratocytes display multifunction in parasitism such as host nutritional exploration, immune and developmental regulation, by secreting plenty of proteins into host hemocoel. RESULTS A serpin (CvT‐serpin15) secreted by teratocytes was characterized. QPCR results showed the expressional level of CvT‐serpin15 was upregulated following bacterial challenges. Enzyme activity experiment indicated the recombinant CvT‐serpin15 protein could interfere with the growth of Gram‐positive bacteria Staphylococcus aureus. The survival rate assay demonstrated CvT‐serpin15 increased survival rate of Plutella xylostella infected by S. aureus. CONCLUSION CvT‐serpin15 secreted by teratocytes would boost the host immune system when pathogens invade host hemocoel during parasitism, and ultimately protect the development of wasp larva from bacterial infection. © 2021 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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A serine protease inhibitor from the hornfaced bee, Osmia cornifrons, exhibits antimicrobial activities

Cited by 9 publications

References 36 publications

Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

Parasitoid Serpins Evolve Novel Functions to Manipulate Host Homeostasis

A Genome-Wide Analysis of Serine Protease Inhibitors in Cydia pomonella Provides Insights into Their Evolution and Expression Pattern

A serpin (CvT‐serpin15) of teratocytes contributes to microbial‐resistance in Plutella xylostella during Cotesia vestalis parasitism

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