Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera

Yuan, Chengye; Xing, Longsheng; Wang, Manli; Wang, Xi; Yin, Mengyi; Wang, Qianran; Zou, Zhen

doi:10.1371/journal.ppat.1006645

Cited by 87 publications

(99 citation statements)

References 55 publications

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“…Similarly, cotton bollworm caterpillars were more susceptible to entomoviruses when they consumed corn than when they consumed cotton . In fact, such differences in susceptibility are closely related to insect immunity . Before an entomovirus kills an insect host, it must invade and overcome host immune responses.…”

Section: Introductionmentioning

confidence: 99%

“…Entomovirus indirectly affects the melanization of insect herbivores by reducing the melanization enzyme activity in insect hemolymph. For instance, inhibition of melanization by NPV infection in cotton bollworm caterpillars was due to reduced levels of PO activity in the infected host hemolymph . However, whether host plants affect the inhibition of melanization by NPV infection remains largely unexplored.…”

Section: Introductionmentioning

confidence: 99%

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Immunity of an insect herbivore to an entomovirus is affected by different host plants

Wang

Zhang

Siemann

et al. 2019

Pest Management Science

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BACKGROUND Interactions between herbivorous insects and entomoviruses may depend on host plant, perhaps mediated through changes in herbivore innate immunity. RESULTS Caterpillars (Spodoptera exigua) fed Glycine max had high viral loads and low melanization rates together with low melanization enzyme [PO, DDC, TH] activities and gene expressions. Caterpillars fed Ipomoea aquatica had low viral loads and high melanization, gene activities and gene expressions while those fed Brassica oleracea or artificial diet had intermediate levels of each. Melanization rates were negatively correlated with viral loads and positively correlated with activity and expression of each of the three enzymes. Some diet effects on enzymes were constitutive because the same diets led to low (G. max) or high (I. aquatica) melanization related gene activities and expressions without infection. CONCLUSION Diet influences the interactions between insect herbivores and viruses by shaping the innate immune response both at the onset of infection and afterwards as viral loads accumulate over a period of days. In addition, diets that lead to low viral loads are associated with high activities and gene expressions of a variety of melanization related enzymes suggesting a common causative mechanism. © 2019 Society of Chemical Industry

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Immunity of an insect herbivore to an entomovirus is affected by different host plants

Wang

Zhang

Siemann

et al. 2019

Pest Management Science

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“…For instance, V‐ATPase and lipase were found in the MEbrown module (resistant), and previous studies have shown that V‐ATPase and lipase are involved in the silkworm defence response against BmNPV infection (Ponnuvel et al ., ; Lü et al ., ). Serpin‐5 was present in the MEsalmon module (susceptible), and previous research has indicated that overexpression of serpin‐5 promoted Helicoverpa armigera nucleopolyhedrovirus infection (Yuan et al ., ). Apart from the identification of potential antiviral genes, our data revealed potential insights into the underlying antiviral mechanisms.…”

Section: Discussionmentioning

confidence: 97%

Specific genes related to nucleopolyhedrovirus in Bombyx mori susceptible and near‐isogenic resistant strains through comparative transcriptome analysis

Chen

Tan

et al. 2019

Insect Molecular Biology

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Bombyx mori nucleopolyhedrovirus (BmNPV) is one of the primary pathogens that causes severe economic losses to sericulture. Comparative transcriptomics analysis has been widely applied to explore the antiviral mechanism in resistant strains. Here, to identify genes involved in BmNPV infection, we identified differentially expressed genes (DEGs) and performed weighted gene co‐expression network analysis (WGCNA) between two Bombyx mori strains: strain 871 (susceptible to BmNPV infection) and the near‐isogenic strain 871C (resistant to BmNPV). Our results showed that 400 genes were associated with resistance in strain 871C, and 76 genes were related to susceptibility in strain 871. In addition, the correlation analysis of DEGs and WGCNA showed that 40 genes related to resistance were highly expressed in the resistant strain. Among them, gene BGIBMGA004291 was the most noticeable. We further identified the effect of gene BGIBMGA004291, which encoded a multiprotein bridge factor 2 (MBF2) family member (MBF2‐10), on viral infection in cells. Our data suggested that MBF2‐10 inhibited viral infection. Taken together, this study showed specific module trait correlations related to viral infection in strains 871 and 871C, and we identified a resistance‐related gene. These findings suggested promising candidate genes with antiviral activity, aiding in the analysis of the antiviral molecular mechanisms in resistant strains.

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“…These results indicated that Spn-2 may be involved in the B. mori antiviral response. Additionally, serpin-5 and serpin-9 can promote baculovirus infection by inhibiting melanizationin in Helicoverpa armigera [63]. Based on these findings, we speculated that the down-regulation of expression of Spn in resistant strains or following BmNPV infection might lead to inhibition of serine proteases and enhance host melanization to suppress infection by BmNPV in resistant strains.…”

Section: Non-enzymatic Proteins Response To Bmnpv Infection In Midgutmentioning

confidence: 92%

Quantitative label-free proteomic analysis reveals differentially expressed proteins in the digestive juice of resistant versus susceptible silkworm strains and their predicted impacts on BmNPV infection

Zhang

Wang

Zhu

et al. 2020

Journal of Proteomics

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Bombyx mori nucleopolyhedrovirus (BmNPV) is a major pathogen causing severe economic loss. Previous studies have revealed that some proteins in silkworm digestive juice show antiviral activity. In this study, antiviral activity examination of different resistant strains showed that the digestive juice of the resistant strain (A35) had higher inhibition to virus than the susceptible strain (P50). Subsequently, the label-free quantitative proteomics was used to study the midgut digestive juice response to BmNPV infection in P50 and A35 strains. A total of 98 proteins were identified, of which 80 were differentially expressed proteins (DEPs) with 54 enzymes and 26 nonenzymatic proteins by comparing the proteomes of infected and non-infected P50 and A35 silkworms. These DEPs are mainly involved in metabolism, proteolysis, neuroactive ligand receptor interaction, starch and sucrose metabolism and glutathione metabolism. After removing the genetic background and individual immune stress response proteins, 9 DEPs were identified potentially involved in resistance to BmNPV. Further studies showed that a serine protease, an alkaline phosphatase and serine protease inhibitor 2 isoform X1 were differentially expressed in A35 compared to P50 or post BmNPV infection. Taken together, these results provide insights into the potential mechanisms for silkworm digestive juice to provide resistance to BmNPV infection.Signifcance: Bombyx mori nucleopolyhedrovirus (BmNPV) is highly pathogenic, which has a great impact on the sericulture. BmNPV entered the midgut lumen and exposed to digestive juices after oral infection. Previous studies have revealed that some proteins in silkworm digestive juice show antiviral activity, however, current information on the digestive juice proteome of high resistant silkworm strain after BmNPV challenge compared to susceptible strain is incomprehensive. Here, we combined label-free quantification method, bioinformatics, RT-qPCR and western blot analysis and found that BmNPV infection causes some protein changes in the silkworm midgut digestive juice. The DEPs were identified in the digestive juices of different resistant strains following BmNPV infection, and screened out some proteins potentially related to resistance to BmNPV. Three important differentially expression proteins were validated by independent approaches. These findings uncover the potential role of silkworm digestive juice in providing resistance to BmNPV and supplemented the profile of the proteome of the digestive juices in B. mori.

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Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera

Cited by 87 publications

References 55 publications

Immunity of an insect herbivore to an entomovirus is affected by different host plants

Immunity of an insect herbivore to an entomovirus is affected by different host plants

Specific genes related to nucleopolyhedrovirus in Bombyx mori susceptible and near‐isogenic resistant strains through comparative transcriptome analysis

Quantitative label-free proteomic analysis reveals differentially expressed proteins in the digestive juice of resistant versus susceptible silkworm strains and their predicted impacts on BmNPV infection

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