Hijacking of host cellular components as proviral factors by plant-infecting viruses

Hyodo, Kiwamu; Okuno, Tetsuro

doi:10.1016/bs.aivir.2020.04.002

Cited by 40 publications

(27 citation statements)

References 265 publications

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“…Moreover, oxidative stress induction can benefit hepatitis C virus replication (Anticoli et al , 2019), blocking mitochondrial ROS levels inhibits respiratory syncytial virus multiplication (Hu et al , 2019b). In plant, red clover necrotic mosaic virus (the genus Dianthovirus in the family Tombusviridae ) replication requires RBOHB‐mediated ROS production, the replication protein p27 hijacking ROS‐generating machinery for efficient viral RNA replication (Hyodo et al , 2017; Hyodo & Okuno, 2020). Collectively, these studies, together with our results, indicate that viruses utilize distinct strategies to create an oxidative microenvironment for viral replication.…”

Section: Discussionmentioning

confidence: 99%

“…Low ROS levels serve as a secondary messenger to regulate the stromule biogenesis (Caplan et al , 2015) or plant growth and development (Zhao et al , 2021), but excessive ROS causes oxidative stress and damages intracellular macromolecular substances and other cellular processes (Choudhury et al , 2017; Waszczak et al , 2018). To avoid toxic effects, plants have evolved specific ROS‐generating and ROS‐scavenging systems to maintain cellular homeostasis under various oxidative stresses (Noctor et al , 2018; Qi et al , 2018; Fichman & Mittler, 2020; Hyodo & Okuno, 2020). The ROS‐scavenging enzymes in plant antioxidant systems include superoxide dismutase (SOD), catalase (CAT), peroxidase (Prx), ascorbate peroxidase (APX), glutathione S‐transferase (GST), and glutathione peroxidase (GPX; Waszczak et al , 2018).…”

Section: Introductionmentioning

confidence: 99%

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Barley stripe mosaic virus γb protein disrupts chloroplast antioxidant defenses to optimize viral replication

et al. 2021

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The plant antioxidant system plays important roles in response to diverse abiotic and biotic stresses. However, the effects of virus infection on host redox homeostasis and how antioxidant defense pathway is manipulated by viruses remain poorly understood. We previously demonstrated that the Barley stripe mosaic virus (BSMV) γb protein is recruited to the chloroplast by the viral αa replicase to enhance viral replication. Here, we show that BSMV infection induces chloroplast oxidative stress. The versatile γb protein interacts directly with NADPH‐dependent thioredoxin reductase C (NTRC), a core component of chloroplast antioxidant systems. Overexpression of NbNTRC significantly impairs BSMV replication in Nicotiana benthamiana plants, whereas disruption of NbNTRC expression leads to increased viral accumulation and infection severity. To counter NTRC‐mediated defenses, BSMV employs the γb protein to competitively interfere with NbNTRC binding to 2‐Cys Prx. Altogether, this study indicates that beyond acting as a helicase enhancer, γb also subverts NTRC‐mediated chloroplast antioxidant defenses to create an oxidative microenvironment conducive to viral replication.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Barley stripe mosaic virus γb protein disrupts chloroplast antioxidant defenses to optimize viral replication

et al. 2021

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“…Biogenesis of VROs is a major activity within infected cells. VRO formation requires subversion of several membranous compartments and vesicles as well as numerous co-opted cytosolic host proteins [2,3,[5][6][7][8][71][72][73][74]. Indeed, tombusviruses co-opt cellular membranous carriers, such as retromer-based tubular carriers, COPII vesicles and their selected cargoes via p33-based targeting of cellular membrane proteins, such as Rab1 and Rab5 small GTPases or the retromer complex and delivering them to the VROs for various functions and membrane modifications and membrane proliferation [51,52,[75][76][77].…”

Section: Discussionmentioning

confidence: 99%

A novel viral strategy for host factor recruitment: The co-opted proteasomal Rpn11 protein interaction hub in cooperation with subverted actin filaments are targeted to deliver cytosolic host factors for viral replication

2021

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Positive-strand (+)RNA viruses take advantage of the host cells by subverting a long list of host protein factors and transport vesicles and cellular organelles to build membranous viral replication organelles (VROs) that support robust RNA replication. How RNA viruses accomplish major recruitment tasks of a large number of cellular proteins are intensively studied. In case of tomato bushy stunt virus (TBSV), a single viral replication protein, named p33, carries out most of the recruitment duties. Yet, it is currently unknown how the viral p33 replication protein, which is membrane associated, is capable of the rapid and efficient recruitment of numerous cytosolic host proteins to facilitate the formation of large VROs. In this paper, we show that, TBSV p33 molecules do not recruit each cytosolic host factor one-by-one into VROs, but p33 targets a cytosolic protein interaction hub, namely Rpn11, which interacts with numerous other cytosolic proteins. The highly conserved Rpn11, called POH1 in humans, is the metalloprotease subunit of the proteasome, which couples deubiquitination and degradation of proteasome substrates. However, TBSV takes advantage of a noncanonical function of Rpn11 by exploiting Rpn11’s interaction with highly abundant cytosolic proteins and the actin network. We provide supporting evidence that the co-opted Rpn11 in coordination with the subverted actin network is used for delivering cytosolic proteins, such as glycolytic and fermentation enzymes, which are readily subverted into VROs to produce ATP locally in support of VRO formation, viral replicase complex assembly and viral RNA replication. Using several approaches, including knockdown of Rpn11 level, sequestering Rpn11 from the cytosol into the nucleus in plants or temperature-sensitive mutation in Rpn11 in yeast, we show the inhibition of recruitment of glycolytic and fermentation enzymes into VROs. The Rpn11-assisted recruitment of the cytosolic enzymes by p33, however, also requires the combined and coordinated role of the subverted actin network. Accordingly, stabilization of the actin filaments by expression of the Legionella VipA effector in yeast and plant, or via a mutation of ACT1 in yeast resulted in more efficient and rapid recruitment of Rpn11 and the selected glycolytic and fermentation enzymes into VROs. On the contrary, destruction of the actin filaments via expression of the Legionella RavK effector led to poor recruitment of Rpn11 and glycolytic and fermentation enzymes. Finally, we confirmed the key roles of Rpn11 and the actin filaments in situ ATP production within TBSV VROs via using a FRET-based ATP-biosensor. The novel emerging theme is that TBSV targets Rpn11 cytosolic protein interaction hub driven by the p33 replication protein and aided by the subverted actin filaments to deliver several co-opted cytosolic pro-viral factors for robust replication within VROs.

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“…PVC/MVB/LE serve as intermediate compartments between the TGN/EE and the vacuole, and enable proteins to recycle before fusion with the vacuole [2]. Plant viruses are obligate parasites with genomes that encode very few proteins and they exploit the host intracellular machinery to establish infection [3][4][5]. In the past decade, an essential role for the endomembrane system (including related host factors) in plant virus infection has been recognised [6][7][8][9][10][11][12][13][14][15][16][17][18][19][20].…”

Section: Introductionmentioning

confidence: 99%

Turnip mosaic virus co-opts the vacuolar sorting receptor VSR4 to promote viral genome replication in plants by targeting viral replication vesicles to the endosome

Jia

Ding

et al. 2022

PLoS Pathog

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Accumulated experimental evidence has shown that viruses recruit the host intracellular machinery to establish infection. It has recently been shown that the potyvirus Turnip mosaic virus (TuMV) transits through the late endosome (LE) for viral genome replication, but it is still largely unknown how the viral replication vesicles labelled by the TuMV membrane protein 6K2 target LE. To further understand the underlying mechanism, we studied the involvement of the vacuolar sorting receptor (VSR) family proteins from Arabidopsis in this process. We now report the identification of VSR4 as a new host factor required for TuMV infection. VSR4 interacted specifically with TuMV 6K2 and was required for targeting of 6K2 to enlarged LE. Following overexpression of VSR4 or its recycling-defective mutant that accumulates in the early endosome (EE), 6K2 did not employ the conventional VSR-mediated EE to LE pathway, but targeted enlarged LE directly from cis-Golgi and viral replication was enhanced. In addition, VSR4 can be N-glycosylated and this is required for its stability and for monitoring 6K2 trafficking to enlarged LE. A non-glycosylated VSR4 mutant enhanced the dissociation of 6K2 from cis-Golgi, leading to the formation of punctate bodies that targeted enlarged LE and to more robust viral replication than with glycosylated VSR4. Finally, TuMV hijacks N-glycosylated VSR4 and protects VSR4 from degradation via the autophagy pathway to assist infection. Taken together, our results have identified a host factor VSR4 required for viral replication vesicles to target endosomes for optimal viral infection and shed new light on the role of N-glycosylation of a host factor in regulating viral infection.

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Hijacking of host cellular components as proviral factors by plant-infecting viruses

Cited by 40 publications

References 265 publications

Barley stripe mosaic virus γb protein disrupts chloroplast antioxidant defenses to optimize viral replication

Barley stripe mosaic virus γb protein disrupts chloroplast antioxidant defenses to optimize viral replication

A novel viral strategy for host factor recruitment: The co-opted proteasomal Rpn11 protein interaction hub in cooperation with subverted actin filaments are targeted to deliver cytosolic host factors for viral replication

Turnip mosaic virus co-opts the vacuolar sorting receptor VSR4 to promote viral genome replication in plants by targeting viral replication vesicles to the endosome

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