Reoviruses hijack the SMARCB1-MYC transcriptional regulation complex to activate autophagy for persistent viral infection in leafhopper vector
Autophagy plays a crucial role in virus-host interactions, as viral components and particles can be degraded by the host’s autophagic machinery. Additionally, some viruses can hijack autophagy for their own benefit. However, the mechanisms underlying the transcriptional regulation of autophagy by ar...
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| Published in: | PLoS pathogens Vol. 21; no. 10; p. e1013569 |
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| Main Authors: | , , , , , , |
| Format: | Journal Article |
| Language: | English |
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| ISSN: | 1553-7374, 1553-7366, 1553-7374 |
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| Abstract | Autophagy plays a crucial role in virus-host interactions, as viral components and particles can be degraded by the host’s autophagic machinery. Additionally, some viruses can hijack autophagy for their own benefit. However, the mechanisms underlying the transcriptional regulation of autophagy by arboviruses in insect vectors remain largely unexplored. In this study, we found that rice dwarf virus (RDV) infection activates the autophagy pathway in the leafhopper vector, Nephotettix cincticeps , and this autophagy activation also facilitates viral infection in the leafhopper. We identified that MYC transcription factor regulates the expression of autophagy proteins ATG5 and ATG8 by directly targeting their promoters. A transcription regulator SMARCB1 binds to MYC and impedes its recognition of the ATG5 and ATG8 promoters, thus negatively regulating their expression. Moreover, NcSMARCB1 negatively regulates ATG5 expression by directly binding to its promoter. RDV major outer capsid protein P8 blocks the nuclear translocation of SMARCB1, disrupting the SMARCB1-MYC interaction and thereby relieving the transcriptional inhibition of ATG5 and ATG8, which leads to autophagy activation. Furthermore, major outer capsid protein P8 of rice gall dwarf virus (RGDV), same to RDV belonging to plant reoviruses, also interacts with SMARCB1 in leafhopper Recilia dorsalis , preventing its nuclear translocation. Similarly, suppression of SMARCB1 expression enhances autophagy formation and promotes RGDV infection. These findings highlight the critical role of insect vector SMARCB1 and MYC in regulating autophagy in response to arbovirus infection. |
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| AbstractList | Autophagy plays a crucial role in virus-host interactions, as viral components and particles can be degraded by the host’s autophagic machinery. Additionally, some viruses can hijack autophagy for their own benefit. However, the mechanisms underlying the transcriptional regulation of autophagy by arboviruses in insect vectors remain largely unexplored. In this study, we found that rice dwarf virus (RDV) infection activates the autophagy pathway in the leafhopper vector, Nephotettix cincticeps , and this autophagy activation also facilitates viral infection in the leafhopper. We identified that MYC transcription factor regulates the expression of autophagy proteins ATG5 and ATG8 by directly targeting their promoters. A transcription regulator SMARCB1 binds to MYC and impedes its recognition of the ATG5 and ATG8 promoters, thus negatively regulating their expression. Moreover, NcSMARCB1 negatively regulates ATG5 expression by directly binding to its promoter. RDV major outer capsid protein P8 blocks the nuclear translocation of SMARCB1, disrupting the SMARCB1-MYC interaction and thereby relieving the transcriptional inhibition of ATG5 and ATG8, which leads to autophagy activation. Furthermore, major outer capsid protein P8 of rice gall dwarf virus (RGDV), same to RDV belonging to plant reoviruses, also interacts with SMARCB1 in leafhopper Recilia dorsalis , preventing its nuclear translocation. Similarly, suppression of SMARCB1 expression enhances autophagy formation and promotes RGDV infection. These findings highlight the critical role of insect vector SMARCB1 and MYC in regulating autophagy in response to arbovirus infection. Autophagy plays a crucial role in virus-host interactions, as viral components and particles can be degraded by the host's autophagic machinery. Additionally, some viruses can hijack autophagy for their own benefit. However, the mechanisms underlying the transcriptional regulation of autophagy by arboviruses in insect vectors remain largely unexplored. In this study, we found that rice dwarf virus (RDV) infection activates the autophagy pathway in the leafhopper vector, Nephotettix cincticeps, and this autophagy activation also facilitates viral infection in the leafhopper. We identified that MYC transcription factor regulates the expression of autophagy proteins ATG5 and ATG8 by directly targeting their promoters. A transcription regulator SMARCB1 binds to MYC and impedes its recognition of the ATG5 and ATG8 promoters, thus negatively regulating their expression. Moreover, NcSMARCB1 negatively regulates ATG5 expression by directly binding to its promoter. RDV major outer capsid protein P8 blocks the nuclear translocation of SMARCB1, disrupting the SMARCB1-MYC interaction and thereby relieving the transcriptional inhibition of ATG5 and ATG8, which leads to autophagy activation. Furthermore, major outer capsid protein P8 of rice gall dwarf virus (RGDV), same to RDV belonging to plant reoviruses, also interacts with SMARCB1 in leafhopper Recilia dorsalis, preventing its nuclear translocation. Similarly, suppression of SMARCB1 expression enhances autophagy formation and promotes RGDV infection. These findings highlight the critical role of insect vector SMARCB1 and MYC in regulating autophagy in response to arbovirus infection.Autophagy plays a crucial role in virus-host interactions, as viral components and particles can be degraded by the host's autophagic machinery. Additionally, some viruses can hijack autophagy for their own benefit. However, the mechanisms underlying the transcriptional regulation of autophagy by arboviruses in insect vectors remain largely unexplored. In this study, we found that rice dwarf virus (RDV) infection activates the autophagy pathway in the leafhopper vector, Nephotettix cincticeps, and this autophagy activation also facilitates viral infection in the leafhopper. We identified that MYC transcription factor regulates the expression of autophagy proteins ATG5 and ATG8 by directly targeting their promoters. A transcription regulator SMARCB1 binds to MYC and impedes its recognition of the ATG5 and ATG8 promoters, thus negatively regulating their expression. Moreover, NcSMARCB1 negatively regulates ATG5 expression by directly binding to its promoter. RDV major outer capsid protein P8 blocks the nuclear translocation of SMARCB1, disrupting the SMARCB1-MYC interaction and thereby relieving the transcriptional inhibition of ATG5 and ATG8, which leads to autophagy activation. Furthermore, major outer capsid protein P8 of rice gall dwarf virus (RGDV), same to RDV belonging to plant reoviruses, also interacts with SMARCB1 in leafhopper Recilia dorsalis, preventing its nuclear translocation. Similarly, suppression of SMARCB1 expression enhances autophagy formation and promotes RGDV infection. These findings highlight the critical role of insect vector SMARCB1 and MYC in regulating autophagy in response to arbovirus infection. |
| Author | Wang, Hui Li, Bozhong Liu, Runfa Wei, Taiyun Xiao, Guangming Li, Yanan Chen, Qian |
| Author_xml | – sequence: 1 givenname: Hui surname: Wang fullname: Wang, Hui – sequence: 2 givenname: Runfa surname: Liu fullname: Liu, Runfa – sequence: 3 givenname: Guangming surname: Xiao fullname: Xiao, Guangming – sequence: 4 givenname: Yanan surname: Li fullname: Li, Yanan – sequence: 5 givenname: Bozhong surname: Li fullname: Li, Bozhong – sequence: 6 givenname: Qian surname: Chen fullname: Chen, Qian – sequence: 7 givenname: Taiyun orcidid: 0000-0002-0732-9752 surname: Wei fullname: Wei, Taiyun |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/41066408$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1016/j.ymeth.2015.01.008 10.1016/S0021-9258(18)54636-6 10.1038/ncb2788 10.1099/vir.0.81425-0 10.1080/15548627.2021.1954773 10.1128/MCB.24.10.4476-4486.2004 10.1016/j.dci.2022.104406 10.1371/journal.ppat.1003032 10.1038/s41467-019-10022-5 10.1016/j.chom.2014.04.004 10.1126/science.1193497 10.1038/nature06639 10.1371/journal.ppat.1011134 10.1093/hmg/ddt381 10.1007/978-1-59745-157-4_4 10.1080/15548627.2016.1192749 10.1016/j.tibs.2014.02.003 10.1089/ars.2011.4394 10.1111/ajco.13449 10.1038/ng.3958 10.1371/journal.ppat.1006727 10.1146/annurev-phyto-080615-095900 10.1038/8811 10.1172/JCI62973 10.1111/j.1750-3639.1991.tb00058.x 10.1098/rstb.2018.0320 10.1080/15548627.2022.2091904 10.1038/s41419-023-06248-3 10.1128/JVI.02167-05 10.3390/cells2010083 10.1080/15548627.2022.2115830 10.1016/j.tim.2023.06.008 10.1080/15384101.2016.1146836 10.1073/pnas.1332764100 10.1074/jbc.M702824200 10.1038/nmicrobiol.2017.25 10.1038/nature18014 10.1016/j.cell.2010.01.028 10.3390/ijms22168527 10.1128/JVI.00050-07 10.14336/AD.2023.0520 10.7150/thno.34887 10.1016/j.cell.2014.11.006 10.2147/OTT.S210575 10.1080/15548627.2023.2200352 |
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| SubjectTerms | Animals Autophagy - physiology Hemiptera - metabolism Hemiptera - virology Insect Vectors - virology Plant Diseases - virology Proto-Oncogene Proteins c-myc - genetics Proto-Oncogene Proteins c-myc - metabolism Reoviridae - pathogenicity Reoviridae - physiology SMARCB1 Protein - genetics SMARCB1 Protein - metabolism |
| Title | Reoviruses hijack the SMARCB1-MYC transcriptional regulation complex to activate autophagy for persistent viral infection in leafhopper vector |
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