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

Wan Zhao, Junjie Zhu, Hong Lu, Jiaming Zhu, Fei Jiang, Wei Wang, Lan Luo, Le Kang, Feng Cui

PDF(13484 KB)
PDF(13484 KB)
Protein Cell ›› 2022, Vol. 13 ›› Issue (5) : 360-378. DOI: 10.1007/s13238-021-00822-1
RESEARCH ARTICLE
RESEARCH ARTICLE

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

Author information +
History +

Abstract

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.

Keywords

rice stripe virus / nucleocapsid protein / nuclear localization / importinα / YY1

Cite this article

Download citation ▾
Wan Zhao, Junjie Zhu, Hong Lu, Jiaming Zhu, Fei Jiang, Wei Wang, Lan Luo, Le Kang, Feng Cui. The nucleocapsid protein of rice stripe virus in cell nuclei of vector insect regulates viral replication. Protein Cell, 2022, 13(5): 360‒378 https://doi.org/10.1007/s13238-021-00822-1

References

[1]
Ashour J, Laurent-Rolle M, Shi PY, García-Sastre A (2009) NS5 of dengue virus mediates STAT2 binding and degradation. J Virol 83:5408–5418
CrossRef Google scholar
[2]
Audsley MD, Jans DA, Moseley GW (2016) Roles of nuclear trafficking in infection by cytoplasmic negative-strand RNA viruses: paramyxoviruses and beyond. J Gen Virol 97:2463–2481
CrossRef Google scholar
[3]
Austen M, Luscher B, Luscher-Firzlaff JM (1997) Characterization of the transcriptional regulator YY1. The bipartite transactivation domain is independent of interaction with the TATA box-binding protein, transcription factor IIB, TAFII55, or cAMP-responsive element-binding protein (CPB)-binding protein. J Biol Chem 272:1709–1717
CrossRef Google scholar
[4]
Bhuvanakantham R, Chong MK, Ng ML (2009) Specific interaction of capsid protein and importin-alpha/beta influences West Nile virus production. Biochem Biophys Res Commun 389:63–69
CrossRef Google scholar
[5]
Bień K, Sokołowska J, Bąska P, Nowak Z, Stankiewicz W, Krzyzowska M (2015) Fas/FasL pathway participates in regulation of antiviral and inflammatory response during mousepox infection of lungs. Mediators Inflamm 2015:281613
CrossRef Google scholar
[6]
Blanc S, Gutierrez S (2015) The specifics of vector transmission of arboviruses of vertebrates and plants. Curr Opin Virol 15:27–33
CrossRef Google scholar
[7]
Bonamassa B, Ciccarese F, Antonio VD, Contarini A, Palù G, Alvisi G (2015) Hepatitis C virus and host cell nuclear transport machinery: a clandestine affair. Front Microbiol 6:619
CrossRef Google scholar
[8]
Byk LA, Gamarnik AV (2016) Properties and functions of the dengue virus capsid protein. Annu Rev Virol 3:263–281
CrossRef Google scholar
[9]
Chen Q, Zheng L, Mao Q, Liu J, Wang H, Jia D, Chen H, Wu W, Wei T (2019) Fibrillar structures induced by a plant reovirus target mitochondria to activate typical apoptotic response and promote viral infection in insect vectors. PLoS Pathog 15:e1007510
CrossRef Google scholar
[10]
Chen XF, Yu JT, Wang W, Lu H, Kang L, Cui F (2020) A plant virus ensures viral stability in the hemolymph of vector insects through suppressing prophenoloxidase activation. mBio 11: e01453-20.
CrossRef Google scholar
[11]
Davis ME, Gack MU (2015) Ubiquitination in the antiviral immune response. Virology 479–480:52–65
CrossRef Google scholar
[12]
Dixit E, Boulant S, Zhang Y, Lee AS, Odendall C, Shum B, Hacohen N, Chen ZJ, Whelan SP, Fransen M, Nibert ML, Superti-Furga G, Kagan JC (2010) Peroxisomes are signaling platforms for antiviral innate immunity. Cell 141:668–681
CrossRef Google scholar
[13]
Eng MW, van Zuylen MN, Severson DW (2016) Apoptosis-related genes control autophagy and influence DENV-2 infection in the mosquito vector, Aedes aegypti. Insect Biochem Mol Biol 76:70–83
CrossRef Google scholar
[14]
Falcón V, Acosta-Rivero N, Chinea G, de la Rosa MAC, Menéndez I, Dueñas-Carrera S, Gra B, Rodriguez A, Tsutsumi V, Shibayama M (2003) Nuclear localization of nucleocapsid-like particles and HCV core protein in hepatocytes of a chronically HCVinfected patient. Biochem Biophys Res Commun 310:54–58
CrossRef Google scholar
[15]
Gao R, Liu P, Wong SM (2012) Identification of a plant viral RNA genome in the nucleus. PLoS One 7:e48736
CrossRef Google scholar
[16]
Garcia-Sastre A (2002) Mechanisms of inhibition of the host interferon alpha/beta-mediated antiviral responses by viruses. Microbes Infect 4:647–655
CrossRef Google scholar
[17]
Gordon S, Akopyan G, Garban H, Bonavida B (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene 25:1125–1142
CrossRef Google scholar
[18]
Grant A, Ponia SS, Tripathi S, Balasubramaniam V, Miorin L, Sourisseau M, Schwarz MC, Sanchez-Seco MP, Evans MJ, Best SM (2016) Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe 19:882–890
CrossRef Google scholar
[19]
Hamamatsu C, Toryama S, Toyoda T, Ishihama A (1993) Ambisense coding strategy of the rice stripe virus genome: in vitro translation studies. J Gen Virol 74:7
CrossRef Google scholar
[20]
Hannemann H, Sung PY, Chiu HC, Yousuf A, Bird J, Lim SP, Davidson AD (2013) Serotype-specific differences in dengue virus non-structural protein 5 nuclear localization. J Biol Chem 288:22621–22635
CrossRef Google scholar
[21]
Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 5:119–127
CrossRef Google scholar
[22]
Hiscox JA, Wurm T, Wilson L, Britton P, Cavanagh D, Brooks G (2001) The coronavirus infectious bronchitis virus nucleoprotein localizes to the nucleolus. J Virol 75:506–512
CrossRef Google scholar
[23]
Huang HJ, Bao YY, Lao SH, Huang XH, Ye YZ, Wu JX, Xu HJ, Zhou XP, Zhang CX (2015) Rice ragged stunt virus-induced apoptosis affects virus transmission from its insect vector, the brown planthopper to the rice plant. Scientific Rep 55:11413
CrossRef Google scholar
[24]
Ivanov KI, Eskelin K, Lõhmus A, Mäkinen K (2014) Molecular and cellular mechanisms underlying potyvirus infection. J Gen Virol 95:1415–1429
CrossRef Google scholar
[25]
Jakob R (1993) Nucleolar accumulation of core protein in cells naturally infected with Semliki Forest virus: Quantitative aspects. Virus Res 30:145–160
CrossRef Google scholar
[26]
Kim Jd, Kim J (2009) YY1’s longer DNA-binding motifs. Genomics 93:152–158
CrossRef Google scholar
[27]
Kim SH, Macfarlane S, Kalinina NO, Rakitina DV, Ryabov EV, Gillespie T, Haupt S, Brown JWS, Taliansky M (2007) Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc Natl Acad Sci U S A 104:11115–11120
CrossRef Google scholar
[28]
Kong L, Wu J, Lu L, Xu Y, Zhou X (2014) Interaction between Rice stripe virus disease-specific protein and host PsbP enhances virus symptoms. Mol Plant 7:691–708
CrossRef Google scholar
[29]
Liu H, Wei C, Zhong Y, Li Y (2007) Rice black-streaked dwarf virus minor core protein P8 is a nuclear dimeric protein and represses transcription in tobacco protoplasts. FEBS Letters 581:2534–2540
CrossRef Google scholar
[30]
Ly HJ, Ikegami T (2016) Rift Valley fever virus NSs protein functions and the similarity to other bunyavirus NSs proteins. Virol J 13:118
CrossRef Google scholar
[31]
Marusawa H, Hijikata M, Chiba T, Shimotohno K (1999) Hepatitis C virus core protein inhibits Fas- and tumor necrosis factor alphamediated apoptosis via NF-kB activation. J Virol 73:8
CrossRef Google scholar
[32]
Michel MR, Elgizoli M, Dai Y, Jakob R, Koblet H, Arrigo AP (1990) Karyophilic properties of Semliki Forest virus nucleocapsid protein. J Virol 64:5123–5131
CrossRef Google scholar
[33]
Mitchell C, de Andrade-Rozental AF, Souto-Padron T, da Costa MGCarvalho (1997) Identification of mayaro virus nucleocapsid protein in nucleus of Aedes albopictus cells. Virus Res 47:11
CrossRef Google scholar
[34]
O’Neill K, Olson BJSC, Huang N, Unis D, Clem RJ (2015) Rapid selection against arbovirus-induced apoptosis during infection of a mosquito vector. Proc Natl Acad Sci U S A 112:E1152–E1161
CrossRef Google scholar
[35]
Reyes-Ruiz JM, Osuna-Ramos JF, Cervantes-Salazar M, Lagunes Guillen AE, Chavez-Munguia B, Salas-Benito JS, Del Angel RM (2018) Strand-like structures and the nonstructural proteins 5, 3and 1 are present in the nucleus of mosquito cells infected with dengue virus. Virology 515:74–80
CrossRef Google scholar
[36]
Richardson J, Sylvester ES (1968) Further evidence of multiplication of sowthistle yellow vein virus in its aphid vector, Hyperomyzus lactucae. Virology 35:347–355
CrossRef Google scholar
[37]
Rowland RR, Kervin R, Kuckleburg C, Sperlich A, Benfield DA (1999) The localization of porcine reproductive and respiratory syndrome virus nucleocapsid protein to the nucleolus of infected cells and identification of a potential nucleolar localization signal sequence. Virus Res 64:1–12
CrossRef Google scholar
[38]
Ryabov EV, Kim SH, Taliansky M (2004) Identification of a nuclear localization signal and nuclear export signal of the umbraviral long-distance RNA movement protein. J Gen Virol 85:1329–1333
CrossRef Google scholar
[39]
Sangiambut S, Keelapang P, Aaskov J, Puttikhunt C, Kasinrerk W, Malasit P, Sittisombut N (2008) Multiple regions in dengue virus capsid protein contribute to nuclear localization during virus infection. J Gen Virol 89:1254–1264
CrossRef Google scholar
[40]
Sasaki T, Burr B (2000) International rice genome sequencing project: the effort to completely sequence the rice genome. Curr Opin Plant Biol 3:138–142
CrossRef Google scholar
[41]
Segura MF, Sole C, Pascual M, Moubarak RS, Jose Perez-Garcia M, Gozzelino R, Iglesias V, Badiola N, Bayascas JR, Llecha N (2007) The long form of Fas apoptotic inhibitory molecule is expressed specifically in neurons and protects them against death receptor-triggered apoptosis. J Neurosci 27:11228–11241
CrossRef Google scholar
[42]
Thurmond S, Wang B, Song J, Hai R (2018) Suppression of type I interferon signaling by Flavivirus NS5. Viruses 10:712
CrossRef Google scholar
[43]
Toriyama S (1986) Rice stripe virus: prototype of a new group of viruses that replicate in plants and insects. Microbiol Sci 3:347–351
[44]
Vaidyanathan R, Scott TW (2006) Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11:1643–1651
CrossRef Google scholar
[45]
Walubo A (2007) The role of cytochrome P450 in antiretroviral drug interactions. Expert Opin Drug Metab Toxicol 3:583–598
CrossRef Google scholar
[46]
Wang W, Zhao W, Li J, Luo L, Kang L, Cui F (2017) The c-Jun N-terminal kinase pathway of a vector insect is activated by virus capsid protein and promotes viral replication. Elife 6:26591
CrossRef Google scholar
[47]
Wang X, Wang W, Zhang W, Li J, Cui F, Qiao L (2019) Immune function of an angiotensin-converting enzyme against Rice stripe virus infection in a vector insect. Virology 533:137–144
CrossRef Google scholar
[48]
Wang Y, Tzfira T, Gaba V, Citovsky V, Palukaitis P, Gal-On A (2004) Functional analysis of the Cucumber mosaic virus 2b protein: pathogenicity and nuclear localization. J Gen Virol 85:3135–3147
CrossRef Google scholar
[49]
Wei TY, Yang JG, Liao FR, Gao FL, Lu LM, Zhang XT, Li F, Wu ZJ, Lin QY, Xie LH (2009) Genetic diversity and population structure of rice stripe virus in China. J Gen Virol 90:1025–1034
CrossRef Google scholar
[50]
Xiong R, Wu J, Zhou Y, Zhou X (2009) Characterization and subcellular localization of an RNA silencing suppressor encoded by Rice stripe tenuivirus. Virology 387:29–40
CrossRef Google scholar
[51]
Yang M, Xu Z, Zhao W, Liu Q, Li Q, Lu L, Liu R, Zhang X, Cui F (2018) Rice stripe virus-derived siRNAs play different regulatory roles in rice and in the insect vector Laodelphax striatellus. BMC Plant Biol 18:219
CrossRef Google scholar
[52]
Zhao W, Yang P, Kang L, Cui F (2016a) Different pathogenicities of Rice stripe virus from the insect vector and from viruliferous plants. New Phytol 210:196–207
CrossRef Google scholar
[53]
Zhao W, Lu L, Yang P, Cui N, Kang L, Cui F (2016b) Organ-specific transcriptome response of the small brown planthopper toward rice stripe virus. Insect Biochem Mol Biol 70:60–72
CrossRef Google scholar
[54]
Zhao W, Wang Q, Xu Z, Liu R, Cui F (2019) Distinct replication and gene expression strategies of the Rice Stripe virus in vector insects and host plants. J Gen Virol 100:877–888
CrossRef Google scholar
[55]
Zhao W, Xu Z, Zhang X, Yang M, Kang L, Liu R, Cui F (2018) Genomic variations in the 3’-termini of Rice stripe virus in the rotation between vector insect and host plant. New Phytol 219:1085–1096
CrossRef Google scholar
[56]
Zheng L, He J, Ding Z, Zhang C, Meng R (2018) Identification of functional domain(s) of fibrillarin interacted with p2 of Rice stripe virus. Can J Infect Dis Med Microbiol: 8402839.
CrossRef Google scholar
[57]
Zheng L, Zhang C, Shi C, Yang Z, Wang Y, Zhou T, Sun F, Wang H, Zhao S, Qin Q (2017) Rice stripe virus NS3 protein regulates primary miRNA processing through association with the miRNA biogenesis factor OsDRB1 and facilitates virus infection in rice. PLoS Pathog 13:e1006662
CrossRef Google scholar
[58]
Zhou YJ, Shuo L, Cheng ZB, Zhou T, Fan YJ (2012) Research advances in rice stripe disease in China. Jiangsu J of Agr Sci 28:9
[59]
Zhu J, Eid FE, Tong L, Zhao W, Wang W, Heath LS, Kang L, Cui F (2020) Characterization of protein-protein interactions between rice viruses and vector insects. Insect Sci. https://doi.org/10.1111/1744-7917.12840
CrossRef Google scholar
[60]
Zhu J, Jiang F, Wang X, Yang P, Bao Y, Zhao W, Wang W, Lu H, Wang Q, Cui N (2017) Genome sequence of the small brown planthopper, Laodelphax striatellus. Gigascience 6:1–12
CrossRef Google scholar

RIGHTS & PERMISSIONS

2021 The Author(s)
AI Summary AI Mindmap
PDF(13484 KB)

Accesses

Citations

Detail

Sections
Recommended

/