Immune function of an angiotensin-converting enzyme against Rice stripe virus infection in a vector insect

Wang, Xue; Wang, Wei; Zhang, Wenzhong; Li, Jing; Cui, Feng; Qiao, Luqin

doi:10.1016/j.virol.2019.05.007

Cited by 6 publications

(5 citation statements)

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“…RSV activates the c-Jun N-terminal kinase (JNK) signaling pathway to promote viral replication in planthoppers (Wang et al, 2017 ). However, RSV significantly upregulates the expression of an angiotensin-converting enzyme, which has negative effects on RSV SP expression (Wang et al, 2019 ). The results of our recent study has provided basic clues regarding the interaction between the NP of RSV and an importin α protein of planthoppers (Zhu et al, 2020 ), suggesting that RSV or at least its NP can enter vector nuclei through the importin α/β pathway to influence immune reactions.…”

Section: Introductionmentioning

confidence: 99%

The nucleocapsid protein of rice stripe virus in cell nuclei of vector insect regulates viral replication

et al. 2021

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Rice stripe virus (RSV) transmitted by the small brown planthopper causes severe rice yield losses in Asian countries. Although viral nuclear entry promotes viral replication in host cells, whether this phenomenon occurs in vector cells remains unknown. Therefore, in this study, we systematically evaluated the presence and roles of RSV in the nuclei of vector insect cells. We observed that the nucleocapsid protein (NP) and viral genomic RNAs were partially transported into vector cell nuclei by utilizing the importin α nuclear transport system. When blocking NP nuclear localization, cytoplasmic RSV accumulation significantly increased. In the vector cell nuclei, NP bound the transcription factor YY1 and affected its positive regulation to FAIM. Subsequently, decreased FAIM expression triggered an antiviral caspase-dependent apoptotic reaction. Our results reveal that viral nuclear entry induces completely different immune effects in vector and host cells, providing new insights into the balance between viral load and the immunity pressure in vector insects.

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Section: Introductionmentioning

confidence: 99%

The nucleocapsid protein of rice stripe virus in cell nuclei of vector insect regulates viral replication

et al. 2021

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“…Interestingly, research conducted by Macours et al 117 showed that ACE can be important for haemocyte activity because bacterial infection led to the increased expression of a gene for ACE in the haemocytes of desert locust. Wang et al 116 supported these results experimentally and showed elevated transcript levels of the ACE gene in the fat body during viral infection. Additionally, the application of 10 –6 M Tenmo-TRP-7 after 24 h caused an increase in the expression levels of genes encoding ACE and ACE2 (Table 3 ).…”

Section: Resultsmentioning

confidence: 81%

“…Angiotensin converting enzyme (ACE), which is closely associated with the regulation of reproduction, development and hormone biosynthesis 116 , was overexpressed. Interestingly, research conducted by Macours et al 117 showed that ACE can be important for haemocyte activity because bacterial infection led to the increased expression of a gene for ACE in the haemocytes of desert locust.…”

Section: Resultsmentioning

confidence: 99%

Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L.

Urbański

Johnston

Bittermann

et al. 2022

Sci Rep

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Tachykinins (TKs) are a group of conserved neuropeptides. In insects, tachykinin-related peptides (TRPs) are important modulators of several functions such as nociception and lipid metabolism. Recently, it has become clear that TRPs also play a role in regulating the insect immune system. Here, we report a transcriptomic analysis of changes in the expression levels of immune-related genes in the storage pest Tenebrio molitor after treatment with Tenmo-TRP-7. We tested two concentrations (10–8 and 10–6 M) at two time points, 6 and 24 h post-injection. We found significant changes in the transcript levels of a wide spectrum of immune-related genes. Some changes were observed 6 h after the injection of Tenmo-TRP-7, especially in relation to its putative anti-apoptotic action. Interestingly, 24 h after the injection of 10–8 M Tenmo-TRP-7, most changes were related to the regulation of the cellular response. Applying 10–6 M Tenmo-TRP-7 resulted in the downregulation of genes associated with humoral responses. Injecting Tenmo-TRP-7 did not affect beetle survival but led to a reduction in haemolymph lysozyme-like antibacterial activity, consistent with the transcriptomic data. The results confirmed the immunomodulatory role of TRP and shed new light on the functional homology between TRPs and TKs.

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“…It is well established that ACE is an essential enzyme in many organisms; the knockout of ACE or its homologs in other species has severe negative effects on health in mammals and is lethal in Drosophila and C. elegans ( Tatei et al, 1995 ; Esther et al, 1996 ; Brooks et al, 2003 ; Kumar et al, 2016 ; Nichols et al, 2016 ). ACE likely evolved in a hypothesized most recent common ancestor of the Bilaterian clade; since that time functional ACE homologs have been retained in such diverse phyla as insects ( Lamango and Isaac, 1994 ; Cornell et al, 1995 ; Wijffels et al, 1996 ; Wijffels et al, 1997 ; Loeb et al, 1998 ; Isaac et al, 1999 ; Vandingenen et al, 2001 ; Vandingenen et al, 2002 ; Ekbote et al, 2003a ; Ekbote et al, 2003b ; Nathalie et al, 2003 ; Burnham et al, 2005 ; Lemeire et al, 2008 ; Wang et al, 2015 ; Abu Hasan et al, 2017 ; Nagaoka et al, 2017 ; Wang et al, 2019 ), crustaceans ( Smiley and Doig, 1994 ; Kamech et al, 2007 ; Sook Chung and Webster, 2008 ), mollusks ( Laurent et al, 1997 ; Riviere et al, 2011 ), annelids ( Rivière et al, 2004 ), nematodes ( Brooks et al, 2003 ; Kumar et al, 2016 ; Metheetrairut et al, 2017 ; Kucuktepe, 2021 ), and vertebrates (reviewed in ( Lv et al, 2018 )). Metalloprotease activity, predicted by the highly conserved histidine-rich HEXXH motif, is retained in all known organisms with an active ACE other than nematode ACN-1, indicating a high degree of evolutionary selective pressure to retain this motif.…”

Section: Discussionmentioning

confidence: 99%

Control of aging by the renin–angiotensin system: a review of C. elegans, Drosophila, and mammals

et al. 2022

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The free-living, non-parasitic nematode Caenorhabditis elegans is a premier model organism for the study of aging and longevity due to its short lifespan, powerful genetic tools, and conservation of fundamental mechanisms with mammals. Approximately 70 percent of human genes have homologs in C. elegans, including many that encode proteins in pathways that influence aging. Numerous genetic pathways have been identified in C. elegans that affect lifespan, including the dietary restriction pathway, the insulin/insulin-like growth factor (IGF) signaling pathway, and the disruption of components of the mitochondrial electron transport chain. C. elegans is also a powerful system for performing drug screens, and many lifespan-extending compounds have been reported; notably, several FDA-approved medications extend the lifespan in C. elegans, raising the possibility that they can also extend the lifespan in humans. The renin–angiotensin system (RAS) in mammals is an endocrine system that regulates blood pressure and a paracrine system that acts in a wide range of tissues to control physiological processes; it is a popular target for drugs that reduce blood pressure, including angiotensin-converting enzyme (ACE) inhibitors and angiotensin II receptor blockers (ARBs). Emerging evidence indicates that this system influences aging. In C. elegans, decreasing the activity of the ACE homolog acn-1 or treatment with the ACE-inhibitor Captopril significantly extends the lifespan. In Drosophila, treatment with ACE inhibitors extends the lifespan. In rodents, manipulating the RAS with genetic or pharmacological interventions can extend the lifespan. In humans, polymorphisms in the ACE gene are associated with extreme longevity. These results suggest the RAS plays a conserved role in controlling longevity. Here, we review studies of the RAS and aging, emphasizing the potential of C. elegans as a model for understanding the mechanism of lifespan control.

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Immune function of an angiotensin-converting enzyme against Rice stripe virus infection in a vector insect

Cited by 6 publications

References 40 publications

The nucleocapsid protein of rice stripe virus in cell nuclei of vector insect regulates viral replication

The nucleocapsid protein of rice stripe virus in cell nuclei of vector insect regulates viral replication

Tachykinin-related peptides modulate immune-gene expression in the mealworm beetle Tenebrio molitor L.

Control of aging by the renin–angiotensin system: a review of C. elegans, Drosophila, and mammals

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