Tomato yellow leaf curl virus confronts host degradation by sheltering in small/midsized protein aggregates

Macroautophagy/autophagy plays an important role against pathogen infection in mammals and plants. However, little has been known about the role of autophagy in the interactions of insect vectors with the plant viruses, which they transmit. Begomoviruses are a group of single-stranded DNA viruses and are exclusively transmitted by the whitefly Bemisia tabaci in a circulative manner. In this study, we found that the infection of a begomovirus, tomato yellow leaf curl virus (TYLCV) could activate the autophagy pathway in the Middle East Asia Minor 1 (MEAM1) species of the B. tabaci complex as evidenced by the formation of autophagosomes and ATG8-II. Interestingly, the activation of autophagy led to the subsequent degradation of TYLCV coat protein (CP) and genomic DNA. While feeding the whitefly with 2 autophagy inhibitors (3-methyladenine and bafilomycin A 1 ) and silencing the expression of Atg3 and Atg9 increased the viral load; autophagy activation via feeding of rapamycin notably decreased the amount of viral CP and DNA in the whitefly. Furthermore, we found that activation of whitefly autophagy could inhibit the efficiency of virus transmission; whereas inhibiting autophagy facilitated virus transmission. Taken together, these results indicate that TYLCV infection can activate the whitefly autophagy pathway, which leads to the subsequent degradation of virus. Furthermore, our report proves that an insect vector uses autophagy as an intrinsic antiviral program to repress the infection of a circulative-transmitted plant virus. Our data also demonstrate that TYLCV may replicate and trigger complex interactions with the insect vector.

show abstract

“…52 Increased understanding of this process will greatly improve our knowledge of the pathogenesis of plant virus. 53 …”

Section: 46mentioning

confidence: 99%

The autophagy pathway participates in resistance to tomato yellow leaf curl virus infection in whiteflies

et al. 2016

View full text Add to dashboard Cite

show abstract

“…The large CP aggregates, which can be compared with VFs in animal cells (Wileman, 2006, 2007), is a major feature of a successful TYLCV infection. The role of small/mid-size aggregates in sheltering TYLCV components and protecting them from host degradation has been shown in plant and in insect cells (Gorovits et al, 2016). In both hosts, the proteolytic activities in the small/mid-size aggregates were low.…”

Section: Tylcv Interactions With Plant Host and Insect Vector Heat Shmentioning

confidence: 99%

The Involvement of Heat Shock Proteins in the Establishment of Tomato Yellow Leaf Curl Virus Infection

Gorovits

Czosnek

2017

Front. Plant Sci.

Self Cite

View full text Add to dashboard Cite

Tomato yellow leaf curl virus (TYLCV), a begomovirus, induces protein aggregation in infected tomatoes and in its whitefly vector Bemisia tabaci. The interactions between TYLCV and HSP70 and HSP90 in plants and vectors are necessity for virus infection to proceed. In infected host cells, HSP70 and HSP90 are redistributed from a soluble to an aggregated state. These aggregates contain, together with viral DNA/proteins and virions, HSPs and components of the protein quality control system such as ubiquitin, 26S proteasome subunits, and the autophagy protein ATG8. TYLCV CP can form complexes with HSPs in tomato and whitefly. Nonetheless, HSP70 and HSP90 play different roles in the viral cell cycle in the plant host. In the infected host cell, HSP70, but not HSP90, participates in the translocation of CP from the cytoplasm into the nucleus. Viral amounts decrease when HSP70 is inhibited, but increase when HSP90 is downregulated. In the whitefly vector, HSP70 impairs the circulative transmission of TYLCV; its inhibition increases transmission. Hence, the efficiency of virus acquisition by whiteflies depends on the functionality of both plant chaperones and their cross-talk with other protein mechanisms controlling virus-induced aggregation.

show abstract

“…Indeed, HCV particle production was more efficient in cells transfected with GDP-locked Rab32-T39N than in cells transfected with an empty vector. Notably, viral proteins in functional complexes could counter the host defense mechanism by sheltering in aggregated structures (46)(47)(48). Interestingly, in the present study, we showed that the GDP-but not GTP-bound form of Rab32 specifically interacted with HCV core protein and enriched core in Rab32-derived perinuclear aggregated structures and resulted in a high level of core protein expression.…”

Section: Discussionmentioning

confidence: 45%

Hepatitis C Virus-Induced Rab32 Aggregation and Its Implications for Virion Assembly

Pham

Tran

Lim

et al. 2017

J Virol

View full text Add to dashboard Cite

Hepatitis C virus (HCV) is highly dependent on cellular factors for viral propagation. Using high-throughput next-generation sequencing, we analyzed the host transcriptomic changes and identified 30 candidate genes which were upregulated in cell culture-grown HCV (HCVcc)-infected cells. Of these candidates, we selected Rab32 for further investigation. Rab32 is a small GTPase that regulates a variety of intracellular membrane-trafficking events in various cell types. In this study, we demonstrated that both mRNA and protein levels of Rab32 were increased in HCV-infected cells. Furthermore, we showed that HCV infection converted the predominantly expressed GTP-bound Rab32 to GDP-bound Rab32, contributing to the aggregation of Rab32 and thus making it less sensitive to cellular degradation machinery. In addition, GDP-bound Rab32 selectively interacted with HCV core protein and deposited core protein into the endoplasmic reticulum (ER)-associated Rab32-derived aggregated structures in the perinuclear region, which were likely to be viral assembly sites. Using RNA interference technology, we demonstrated that Rab32 was required for the assembly step but not for other stages of the HCV life cycle. Taken together, these data suggest that HCV may modulate Rab32 activity to facilitate virion assembly. IMPORTANCE Rab32, a member of the Ras superfamily of small GTPases, regulates various intracellular membrane-trafficking events in many cell types. In this study, we showed that HCV infection concomitantly increased Rab32 expression at the transcriptional level and altered the balance between GDP-and GTP-bound Rab32 toward production of Rab32-GDP. GDP-bound Rab32 selectively interacted with HCV core protein and enriched core in the ER-associated Rab32-derived aggregated structures that were probably necessary for viral assembly. Indeed, we showed that Rab32 was specifically required for the assembly of HCV. Collectively, our study identifies that Rab32 is a novel host factor essential for HCV particle assembly.

show abstract

Tomato yellow leaf curl virus confronts host degradation by sheltering in small/midsized protein aggregates

Cited by 30 publications

References 41 publications

The autophagy pathway participates in resistance to tomato yellow leaf curl virus infection in whiteflies

The autophagy pathway participates in resistance to tomato yellow leaf curl virus infection in whiteflies

The Involvement of Heat Shock Proteins in the Establishment of Tomato Yellow Leaf Curl Virus Infection

Hepatitis C Virus-Induced Rab32 Aggregation and Its Implications for Virion Assembly

Contact Info

Product

Resources

About