Insect Immunity: Evolution, Genomics and Physiology

A topical collection in Insects (ISSN 2075-4450). This collection belongs to the section "Insect Physiology, Reproduction and Development".

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Editor


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Guest Editor
Department of Plant Pathology, Entomology and Microbiology, Iowa State University, Ames, IA 50011, USA
Interests: mosquito innate immunity; Plasmodium parasites; arbovirus; eicosanoids; insect neuropeptides

Topical Collection Information

Dear Colleagues,

Innate immunity mediated by humoral and cellular components plays a pivotal role in combating infectious pathogens and sustaining life throughout all organisms, including insects. Insect genome studies have revealed that many immune molecules have been evolutionally conserved between insects and vertebrates. While insect immune responses result from the orchestration of immune molecules, insects can maintain immunological homeostasis to control immune processes and minimize devastating effects on survival and reproduction through the coordination of multiple signal pathways. Recent studies demonstrate that insect immune systems are more complex than previously thought, and unveiling the mechanisms of insect immune systems provides a unique opportunity to better understand insect biology.

Dr. Hyeogsun Kwon
Guest Editor

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Keywords

  • insect innate immunity
  • immunophysiology
  • insect–pathogen interactions
  • conserved immune molecules
  • immune crosstalk

Published Papers (7 papers)

2024

Jump to: 2023

12 pages, 1590 KiB  
Article
BmToll9-1 Is a Positive Regulator of the Immune Response in the Silkworm Bombyx mori
by Jisheng Liu, Weijian Chen, Jinrong Situ, Jiaxuan Li, Jiahua Chen, Minchun Lai, Fengyi Huang and Baoqi Li
Insects 2024, 15(9), 643; https://doi.org/10.3390/insects15090643 - 27 Aug 2024
Viewed by 864
Abstract
Toll receptors are involved in the development and innate immunity of insects. BmToll9-1 is an important immune receptor in the Toll pathway. Previous studies have focused on its role as a receptor in immune response. In this study, we aimed to investigate the [...] Read more.
Toll receptors are involved in the development and innate immunity of insects. BmToll9-1 is an important immune receptor in the Toll pathway. Previous studies have focused on its role as a receptor in immune response. In this study, we aimed to investigate the role of BmToll9-1 as a regulator in the immune response. The expression profiles demonstrated that BmToll9-1 was predominantly expressed in the midgut. RNA interference (RNAi) of BmToll9-1 was found to be effective in the midgut via the injection of dsRNA, which resulted in smaller and lighter larvae and cocoons. Most signaling genes in the Toll pathway and downstream effector genes were downregulated after the RNAi of BmToll9-1. The hemolymph from BmToll9-1-silenced larvae showed decreased antibacterial activity against Escherichia coli, either in growth curve or inhibition zone experiments. The above results indicate that BmToll9-1 might be positively involved in the immune pathway of silkworm. As a positive regulator, BmToll9-1 might function mainly in the gut to maintain microbial homeostasis to regulate the growth of silkworms. Silencing of BmToll9-1 downregulates the signaling genes in the Toll pathway and antimicrobial peptide (AMP) production, resulting in decreased antibacterial activity in the hemolymph. Full article
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13 pages, 1563 KiB  
Article
Drosophila melanogaster Limostatin and Its Human Ortholog Promote West Nile Virus Infection
by Ezra B. Mead, Miyoung Lee, Chasity E. Trammell and Alan G. Goodman
Insects 2024, 15(6), 446; https://doi.org/10.3390/insects15060446 - 12 Jun 2024
Viewed by 1335
Abstract
The arbovirus West Nile virus (WNV) is a danger to global health. Spread primarily by mosquitoes, WNV causes about 2000 cases per year in the United States. The natural mosquito immune response controls viral replication so that the host survives but can still [...] Read more.
The arbovirus West Nile virus (WNV) is a danger to global health. Spread primarily by mosquitoes, WNV causes about 2000 cases per year in the United States. The natural mosquito immune response controls viral replication so that the host survives but can still transmit the virus. Using the genetically malleable Drosophila melanogaster model, we previously dissected innate immune pathways used to control WNV infection. Specifically, we showed that insulin/IGF-1 signaling (IIS) activates a JAK/STAT-mediated immune response that reduces WNV. However, how factors that regulate IIS in insects control infection has not been identified. D. melanogaster Limostatin (Lst) encodes a peptide hormone that suppresses insulin secretion. Its mammalian ortholog, Neuromedin U (NMU), is a peptide that regulates the production and secretion of insulin from pancreatic beta cells. In this study, we used D. melanogaster and human cell culture models to investigate the roles of these insulin regulators in immune signaling. We found that D. melanogaster Lst mutants, which have elevated insulin-like peptide expression, are less susceptible to WNV infection. Increased levels of insulin-like peptides in these flies result in upregulated JAK/STAT activity, leading to protection from infection. Treatment of human cells with the insulin regulator NMU results in increased WNV replication. Further investigation of methods to target Lst in mosquitoes or NMU in mammals can improve vector control methods and may lead to improved therapeutics for human and animal infection. Full article
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19 pages, 4256 KiB  
Article
The Lifespan of D. melanogaster Depends on the Function of the Gagr Gene, a Domesticated gag Gene of Drosophila LTR Retrotransposons
by Yevgenia Balakireva, Maria Nikitina, Pavel Makhnovskii, Inna Kukushkina, Ilya Kuzmin, Alexander Kim and Lidia Nefedova
Insects 2024, 15(1), 68; https://doi.org/10.3390/insects15010068 - 17 Jan 2024
Cited by 1 | Viewed by 1943
Abstract
(1) Background: The Gagr gene in Drosophila melanogaster’s genome originated from the molecular domestication of retrotransposons and retroviruses’ gag gene. In all Drosophila species, the Gagr protein homologs exhibit a conserved structure, indicative of a vital role. Previous studies have suggested a [...] Read more.
(1) Background: The Gagr gene in Drosophila melanogaster’s genome originated from the molecular domestication of retrotransposons and retroviruses’ gag gene. In all Drosophila species, the Gagr protein homologs exhibit a conserved structure, indicative of a vital role. Previous studies have suggested a potential link between the Gagr gene function and stress responses. (2) Methods: We compared flies with Gagr gene knockdown in all tissues to control flies in physiological tests and RNA-sequencing experiments. (3) Results: Flies with the Gagr gene knockdown exhibited shorter lifespans compared to control flies. Transcriptome analysis revealed that Gagr knockdown flies showed elevated transcription levels of immune response genes. We used ammonium persulfate, a potent stress inducer, to elicit a stress response. In control flies, ammonium persulfate activated the Toll, JAK/STAT, and JNK/MAPK signaling pathways. In contrast, flies with the Gagr gene knockdown displayed reduced expression of stress response genes. Gene ontology enrichment analysis identified categories of genes upregulated under ammonium persulfate stress in control flies but not in Gagr knockdown flies. These genes are involved in developmental control, morphogenesis, and central nervous system function. (4) Conclusion: Our findings indicate the significance of the Gagr gene in maintaining immune response and homeostasis. Full article
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2023

Jump to: 2024

17 pages, 3111 KiB  
Article
The Effects of Diet on the Immune Responses of the Oriental Armyworm Mythimna separata
by Lizhen Zhou, Li Ma, Lu Liu, Shaolei Sun, Xiangfeng Jing and Zhiqiang Lu
Insects 2023, 14(8), 685; https://doi.org/10.3390/insects14080685 - 3 Aug 2023
Cited by 2 | Viewed by 1692
Abstract
Nutrients can greatly affect host immune defenses against infection. Possessing a simple immune system, insects have been widely used as models to address the relationships between nutrition and immunity. The effects of high versus low protein-to-carbohydrate ratio (P:C) diets on insect immune responses [...] Read more.
Nutrients can greatly affect host immune defenses against infection. Possessing a simple immune system, insects have been widely used as models to address the relationships between nutrition and immunity. The effects of high versus low protein-to-carbohydrate ratio (P:C) diets on insect immune responses vary in different studies. To reveal the dietary manipulation of immune responses in the polyphagous agricultural pest oriental armyworm, we examined immune gene expression, phenoloxidase (PO) activity, and phagocytosis to investigate the immune traits of bacteria-challenged oriental armyworms, which were fed different P:C ratio diets. We found the oriental armyworms that were fed a 35:7 (P:C) diet showed higher phenoloxidase (PO) activity and stronger melanization, and those reared on a 28:14 (P:C) diet showed higher antimicrobial activity. However, different P:C diets had no apparent effect on the hemocyte number and phagocytosis. These results overall indicate that high P:C diets differently optimize humoral immune defense responses in oriental armyworms, i.e., PO-mediated melanization and antimicrobial peptide synthesis in response to bacteria challenge. Full article
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15 pages, 1115 KiB  
Review
Colonization Resistance of Symbionts in Their Insect Hosts
by Zhengyan Wang, Hanzi Yong, Shan Zhang, Zhiyuan Liu and Yaru Zhao
Insects 2023, 14(7), 594; https://doi.org/10.3390/insects14070594 - 30 Jun 2023
Cited by 7 | Viewed by 2282
Abstract
The symbiotic microbiome is critical in promoting insect resistance against colonization by exogenous microorganisms. The mechanisms by which symbionts contribute to the host’s immune capacity is referred to as colonization resistance. Symbionts can protect insects from exogenous pathogens through a variety of mechanisms, [...] Read more.
The symbiotic microbiome is critical in promoting insect resistance against colonization by exogenous microorganisms. The mechanisms by which symbionts contribute to the host’s immune capacity is referred to as colonization resistance. Symbionts can protect insects from exogenous pathogens through a variety of mechanisms, including upregulating the expression of host immune-related genes, producing antimicrobial substances, and competitively excluding pathogens. Concordantly, insects have evolved fine-tuned regulatory mechanisms to avoid overactive immune responses against symbionts or specialized cells to harbor symbionts. Alternatively, some symbionts have evolved special adaptations, such as the formation of biofilms to increase their tolerance to host immune responses. Here, we provide a review of the mechanisms about colonization resistance of symbionts in their insect hosts. Adaptations of symbionts and their insect hosts that may maintain such symbiotic relationships, and the significance of such relationships in the coevolution of symbiotic systems are also discussed to provide insights into the in-depth study of the contribution of symbionts to host physiology and behavior. Full article
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17 pages, 5101 KiB  
Article
Two Alimentary Canal Proteins, Fo-GN and Fo-Cyp1, Act in Western Flower Thrips, Frankliniella occidentalis TSWV Infection
by Falguni Khan, David Stanley and Yonggyun Kim
Insects 2023, 14(2), 154; https://doi.org/10.3390/insects14020154 - 3 Feb 2023
Cited by 4 | Viewed by 2188
Abstract
Tomato spotted wilt virus (TSWV) is a plant virus that causes massive economic damage to high-valued crops. This virus is transmitted by specific thrips, including the western flower thrips, Frankliniella occidentalis. TSWV is acquired by the young larvae during feeding on infected host [...] Read more.
Tomato spotted wilt virus (TSWV) is a plant virus that causes massive economic damage to high-valued crops. This virus is transmitted by specific thrips, including the western flower thrips, Frankliniella occidentalis. TSWV is acquired by the young larvae during feeding on infected host plants. TSWV infects the gut epithelium through hypothetical receptor(s) and multiplies within the cells for subsequent horizontal transmission to other plant hosts via the salivary glands during feeding. Two alimentary canal proteins, glycoprotein (Fo-GN) and cyclophilin (Fo-Cyp1), are thought to be associated with the TSWV entry into the gut epithelium of F. occidentalis. Fo-GN possesses a chitin-binding domain, and its transcript was localized on the larval gut epithelium by fluorescence in situ hybridization (FISH) analysis. Phylogenetic analysis indicated that F. occidentalis encodes six cyclophilins, in which Fo-Cyp1 is closely related to a human cyclophilin A, an immune modulator. The Fo-Cyp1 transcript was also detected in the larval gut epithelium. Expression of these two genes was suppressed by feeding their cognate RNA interference (RNAi) to young larvae. The RNAi efficiencies were confirmed by the disappearance of the target gene transcripts from the gut epithelium by FISH analyses. The RNAi treatments directed to Fo-GN or Fo-Cyp1 prevented the typical TSWV titer increase after the virus feeding, compared to control RNAi treatment. Our immunofluorescence assay using a specific antibody to TSWV documented the reduction of TSWV in the larval gut and adult salivary gland after the RNAi treatments. These results support our hypothesis that the candidate proteins Fo-GN and Fo-Cyp1 act in TSWV entry and multiplication in F. occidentalis. Full article
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13 pages, 3044 KiB  
Article
Overcoming Immune Deficiency with Allogrooming
by Mark S. Bulmer, Bruno A. Franco, Aditi Biswas and Samantha F. Greenbaum
Insects 2023, 14(2), 128; https://doi.org/10.3390/insects14020128 - 26 Jan 2023
Cited by 2 | Viewed by 1789
Abstract
Allogrooming appears to be essential in many social animals for protection from routine exposure to parasites. In social insects, it appears to be critical for the removal of pathogenic propagules from the cuticle before they can start an infectious cycle. For subterranean termites, [...] Read more.
Allogrooming appears to be essential in many social animals for protection from routine exposure to parasites. In social insects, it appears to be critical for the removal of pathogenic propagules from the cuticle before they can start an infectious cycle. For subterranean termites, this includes fungal spores commonly encountered in the soil, such as Metarhizium conidia, that can quickly germinate and penetrate the cuticle. We investigated whether there is a difference in reliance on social and innate immunity in two closely related subterranean termites for protection from fatal infections by two locally encountered Metarhizium species. Our results indicate that relatively weak innate immunity in one termite species is compensated by more sustained allogrooming. This includes enhanced allogrooming in response to concentrations of conidia that reflect more routine contamination of the cuticle as well as to heavy cuticular contamination that elicits a networked emergency response. Full article
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