Heterogeneous nuclear ribonucleoprotein A3 binds to the internal ribosomal entry site of enterovirus A71 and affects virus replication in neural cells.

IRES‐transacting factors enterovirus A71 hnRNP A3 internal ribosome entry site neural cell

Journal

Journal of cellular biochemistry
ISSN: 1097-4644
Titre abrégé: J Cell Biochem
Pays: United States
ID NLM: 8205768

Informations de publication

Date de publication:
09 May 2024
Historique:
revised: 15 04 2024
received: 08 11 2023
accepted: 22 04 2024
medline: 9 5 2024
pubmed: 9 5 2024
entrez: 9 5 2024
Statut: aheadofprint

Résumé

Enterovirus A71 (EV-A71) belongs to the genus Enterovirus of the Picornaviridae family and often causes outbreaks in Asia. EV-A71 infection usually causes hand, foot, and mouth disease and can even affect the central nervous system, causing neurological complications or death. The 5'-untranslated region (5'-UTR) of EV-A71 contains an internal ribosome entry site (IRES) that is responsible for the translation of viral proteins. IRES-transacting factors can interact with the EV-A71 5'-UTR to regulate IRES activity. Heterogeneous nuclear ribonucleoprotein (hnRNP) A3 is a member of the hnRNP A/B protein family of RNA-binding proteins and is involved in RNA transport and modification. We found that hnRNP A3 knockdown promoted the replication of EV-A71 in neural calls. Conversely, increasing the expression of hnRNP A3 within cells inhibits the growth of EV-A71. HnRNP A3 can bind to the EV-A71 5'-UTR, and knockdown of hnRNP A3 enhances the luciferase activity of the EV-A71 5'-UTR IRES. The localization of hnRNP A3 shifts from the nucleus to the cytoplasm of infected cells during viral infection. Additionally, EV-A71 infection can increase the protein expression of hnRNP A3, and the protein level is correlated with efficient viral growth. Based on these findings, we concluded that hnRNP A3 plays a negative regulatory role in EV-A71 replication within neural cells.

Identifiants

pubmed: 38720641
doi: 10.1002/jcb.30575
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Ministry of Science and Technology, Taiwan
ID : 111-2320-B-182-023
Organisme : Ministry of Science and Technology, Taiwan
ID : 112-2320-B-182-048-MY3
Organisme : Chang Gung University, Taiwan
ID : BMRPB33
Organisme : Chang Gung Memorial Hospital, Taiwan
ID : CMRPD1M0931
Organisme : Chang Gung Memorial Hospital, Taiwan
ID : CMRPD1M0932

Informations de copyright

© 2024 Wiley Periodicals LLC.

Références

Schmidt NJ, Lennette EH, Ho HH. An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis. 1974;129(3):304‐309. doi:10.1093/infdis/129.3.304
Puenpa J, Wanlapakorn N, Vongpunsawad S, Poovorawan Y. The history of enterovirus A71 outbreaks and molecular epidemiology in the Asia‐Pacific region. J Biomed Sci. 2019;26(1):75. doi:10.1186/s12929-019-0573-2
Ho M, Chen ER, Hsu KH, et al. An epidemic of enterovirus 71 infection in Taiwan. N Engl J Med. 1999;341(13):929‐935. doi:10.1056/NEJM199909233411301
Chang LY, Lin HY, Gau SSF, et al. Enterovirus A71 neurologic complications and long‐term sequelae. J Biomed Sci. 2019;26(1):57. doi:10.1186/s12929-019-0552-7
Lee KY. Enterovirus 71 infection and neurological complications. Korean J Pediatr. 2016;59(10):395‐401. doi:10.3345/kjp.2016.59.10.395
Khong WX, Yan B, Yeo H, et al. A non‐mouse‐adapted enterovirus 71 (EV71) strain exhibits neurotropism, causing neurological manifestations in a novel mouse model of EV71 infection. J Virol. 2012;86(4):2121‐2131. doi:10.1128/JVI.06103-11
Yan JJ, Wang JR, Liu CC, Yang HB, Su IJ. An outbreak of enterovirus 71 infection in Taiwan 1998: a comprehensive pathological, virological, and molecular study on a case of fulminant encephalitis. J Clin Virol. 2000;17(1):13‐22. doi:10.1016/s1386-6532(00)00067-6
Brown BA, Pallansch MA. Complete nucleotide sequence of enterovirus 71 is distinct from poliovirus. Virus Res. 1995;39(2‐3):195‐205. doi:10.1016/0168-1702(95)00087-9
Holcik M, Sonenberg N. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol. 2005;6(4):318‐327. doi:10.1038/nrm1618
Faye MD, Holcik M. The role of IRES trans‐acting factors in carcinogenesis. Biochim Biophys Acta. 2015;1849(7):887‐897. doi:10.1016/j.bbagrm.2014.09.012
Tolbert M, Morgan CE, Pollum M, et al. HnRNP A1 alters the structure of a conserved enterovirus IRES domain to stimulate viral translation. J Mol Biol. 2017;429(19):2841‐2858. doi:10.1016/j.jmb.2017.06.007
Lin JY, Shih SR, Pan M, et al. hnRNP A1 interacts with the 5′ untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J Virol. 2009;83(12):6106‐6114. doi:10.1128/JVI.02476-08
Luo Z, Dong X, Li Y, et al. PolyC‐binding protein 1 interacts with 5′‐untranslated region of enterovirus 71 RNA in membrane‐associated complex to facilitate viral replication. PLoS One. 2014;9(1):e87491. doi:10.1371/journal.pone.0087491
Lin JY, Li ML, Brewer G. mRNA decay factor AUF1 binds the internal ribosomal entry site of enterovirus 71 and inhibits virus replication. PLoS One. 2014;9(7):e103827. doi:10.1371/journal.pone.0103827
Lin JY, Li ML, Huang PN, Chien KY, Horng JT, Shih SR. Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 5′ untranslated region and participates in virus replication. J Gen Virol. 2008;89(Pt):2540‐2549. doi:10.1099/vir.0.2008/003673-0
Dreyfuss G, Matunis MJ, Pinol‐Roma S, Burd CG. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem. 1993;62:289‐321. doi:10.1146/annurev.bi.62.070193.001445
Dreyfuss G, Kim VN, Kataoka N. Messenger‐RNA‐binding proteins and the messages they carry. Nat Rev Mol Cell Biol. 2002;3(3):195‐205. doi:10.1038/nrm760
Reed R, Hurt E. A conserved mRNA export machinery coupled to pre‐mRNA splicing. Cell. 2002;108(4):523‐531. doi:10.1016/s0092-8674(02)00627-x
Shih SR, Chiang C, Chen TC, et al. Mutations at KFRDI and VGK domains of enterovirus 71 3C protease affect its RNA binding and proteolytic activities. J Biomed Sci. 2004;11(2):239‐248. doi:10.1007/BF02256567
Lin JY, Huang HI. Autophagy is induced and supports virus replication in enterovirus A71‐infected human primary neuronal cells. Sci Rep. 2020;10(1):15234. doi:10.1038/s41598-020-71970-3
Huang HI, Chang YY, Lin JY, et al. Interactome analysis of the EV71 5′ untranslated region in differentiated neuronal cells SH‐SY5Y and regulatory role of FBP3 in viral replication. Proteomics. 2016;16(17):2351‐2362. doi:10.1002/pmic.201600098
Yu J, Zhang L, Ren P, et al. Enterovirus 71 mediates cell cycle arrest in S phase through non‐structural protein 3D. Cell Cycle. 2015;14(3):425‐436. doi:10.4161/15384101.2014.980631
McMinn P, Stratov I, Nagarajan L, Davis S. Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin Infect Dis. 2001;32(2):236‐242. doi:10.1086/318454
You L, Chen J, Liu W, et al. Enterovirus 71 induces neural cell apoptosis and autophagy through promoting ACOX1 downregulation and ROS generation. Virulence. 2020;11(1):537‐553. doi:10.1080/21505594.2020.1766790
Huang HI, Lin JY, Chen SH. EV71 infection induces IFNβ expression in neural cells. Viruses. 2019;11(12):1121. doi:10.3390/v11121121
Rattanakomol P, Srimanote P, Tongtawe P, Khantisitthiporn O, Supasorn O, Thanongsaksrikul J. Host neuronal PRSS3 interacts with enterovirus A71 3A protein and its role in viral replication. Sci Rep. 2022;12(1):12846. doi:10.1038/s41598-022-17272-2
Zhong M, Wang H, Yan H, et al. Effects and mechanism of Aβ1−42 on EV‐A71 replication. Virol J. 2022;19(1):151. doi:10.1186/s12985-022-01882-3
Bampton A, Gittings LM, Fratta P, Lashley T, Gatt A. The role of hnRNPs in frontotemporal dementia and amyotrophic lateral sclerosis. Acta Neuropathol. 2020;140(5):599‐623. doi:10.1007/s00401-020-02203-0
Bekenstein U, Soreq H. Heterogeneous nuclear ribonucleoprotein A1 in health and neurodegenerative disease: from structural insights to post‐transcriptional regulatory roles. Mol Cell Neurosci. 2013;56:436‐446. doi:10.1016/j.mcn.2012.12.002
Clarke JP, Thibault PA, Salapa HE, Levin MC. A comprehensive analysis of the role of hnRNP A1 function and dysfunction in the pathogenesis of neurodegenerative disease. Front Mol Biosci. 2021;8:659610. doi:10.3389/fmolb.2021.659610
Low YH, Asi Y, Foti SC, Lashley T. Heterogeneous nuclear ribonucleoproteins: implications in neurological diseases. Mol Neurobiol. 2021;58(2):631‐646. doi:10.1007/s12035-020-02137-4
Pingale KD, Kanade GD, Karpe YA. Heterogeneous nuclear ribonucleoproteins participate in hepatitis E virus replication. J Mol Biol. 2020;432(7):2369‐2387. doi:10.1016/j.jmb.2020.02.025
Wang J, Sun D, Wang M, et al. Multiple functions of heterogeneous nuclear ribonucleoproteins in the positive single‐stranded RNA virus life cycle. Front Immunol. 2022;13:989298. doi:10.3389/fimmu.2022.989298
Zhang A, Sun Y, Jing H, et al. Interaction of HnRNP F with the guanine‐rich segments in viral antigenomic RNA enhances porcine reproductive and respiratory syndrome virus‐2 replication. Virol J. 2022;19(1):82. doi:10.1186/s12985-022-01811-4
Ou MY, Ju XC, Cai YJ, et al. Heterogeneous nuclear ribonucleoprotein A3a controls mitotic progression of neural progenitors via interaction with cohesin. Development. 2020;147(10). doi:10.1242/dev.185132
Davidson YS, Flood L, Robinson AC, et al. Heterogeneous ribonuclear protein A3 (hnRNP A3) is present in dipeptide repeat protein containing inclusions in frontotemporal lobar degeneration and motor neurone disease associated with expansions in C9orf72 gene. Acta Neuropathol Commun. 2017;5(1):31. doi:10.1186/s40478-017-0437-5
Mailliot J, Martin F. Viral internal ribosomal entry sites: four classes for one goal. WIREs RNA. 2018;9(2):1458. doi:10.1002/wrna.1458
Martinez‐Salas E, Francisco‐Velilla R, Fernandez‐Chamorro J, Embarek AM. Insights into structural and mechanistic features of viral IRES elements. Front Microbiol. 2018;8:2629. doi:10.3389/fmicb.2017.02629
Sweeney TR, Abaeva IS, Pestova TV, Hellen CUT. The mechanism of translation initiation on type 1 picornavirus IRESs. EMBO J. 2014;33(1):76‐92. doi:10.1002/embj.201386124
Lin JY, Li ML, Shih SR. Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation. Nucleic Acids Res. 2009;37(1):47‐59. doi:10.1093/nar/gkn901
Gherzi R, Lee KY, Briata P, et al. A KH domain RNA binding protein, KSRP, promotes ARE‐directed mRNA turnover by recruiting the degradation machinery. Mol Cell. 2004;14(5):571‐583. doi:10.1016/j.molcel.2004.05.002
Gratacós FM, Brewer G. The role of AUF1 in regulated mRNA decay. WIREs RNA. 2010;1(3):457‐473. doi:10.1002/wrna.26
Wong J, Si X, Angeles A, et al. Cytoplasmic redistribution and cleavage of AUF1 during coxsackievirus infection enhance the stability of its viral genome. FASEB J. 2013;27(7):2777‐2787. doi:10.1096/fj.12-226498
Huang PN, Lin JY, Locker N, et al. Far upstream element binding protein 1 binds the internal ribosomal entry site of enterovirus 71 and enhances viral translation and viral growth. Nucleic Acids Res. 2011;39(22):9633‐9648. doi:10.1093/nar/gkr682
Xi J, Ye F, Wang G, et al. Polypyrimidine tract‐binding protein regulates enterovirus 71 translation through interaction with the internal ribosomal entry site. Virol Sin. 2019;34(1):66‐77. doi:10.1007/s12250-019-00089-1
Kim CS, Seol SK, Song OK, Park JH, Jang SK. An RNA‐binding protein, hnRNP A1, and a scaffold protein, septin 6, facilitate hepatitis C virus replication. J Virol. 2007;81(8):3852‐3865. doi:10.1128/JVI.01311-06
Li HP, Zhang X, Duncan R, Comai L, Lai MMC. Heterogeneous nuclear ribonucleoprotein A1 binds to the transcription‐regulatory region of mouse hepatitis virus RNA. Proc Natl Acad Sci USA. 1997;94(18):9544‐9549. doi:10.1073/pnas.94.18.9544
Gustin KE. Effects of poliovirus infection on nucleo‐cytoplasmic trafficking and nuclear pore complex composition. EMBO J. 2001;20(1‐2):240‐249. doi:10.1093/emboj/20.1.240
Zhang YZ, Gan X, Song J, et al. (2013). The 2A protease of enterovirus 71 cleaves nup62 to inhibit nuclear transport. Bing Du Xue Bao, 29(4), 421‐425.
Feuer R, Mena I, Pagarigan R, Slifka MK, Whitton JL. Cell cycle status affects coxsackievirus replication, persistence, and reactivation in vitro. J Virol. 2002;76(9):4430‐4440. doi:10.1128/jvi.76.9.4430-4440.2002
Glaser W, Skern T. Extremely efficient cleavage of eIF4G by picornaviral proteinases L and 2A in vitro. FEBS Lett. 2000;480(2‐3):151‐155. doi:10.1016/s0014-5793(00)01928-1
Dave P, George B, Sharma DK, Das S. Polypyrimidine tract‐binding protein (PTB) and PTB‐associated splicing factor in CVB3 infection: an ITAF for an ITAF. Nucleic Acids Res. 2017;45(15):9068‐9084. doi:10.1093/nar/gkx519
Lee KM, Wu CC, Wu SE, et al. The RNA‐dependent RNA polymerase of enterovirus A71 associates with ribosomal proteins and positively regulates protein translation. RNA Biol. 2020;17(4):608‐622. doi:10.1080/15476286.2020.1722448

Auteurs

Jhao-Yin Lin (JY)

Department of Medical Biotechnology and Laboratory Science, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Research Center for Emerging Viral Infections, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.

Jing-Yi Lin (JY)

Department of Clinical Laboratory Sciences and Medical Biotechnology, College of Medicine, National Taiwan University, Taipei, Taiwan.
Department of Laboratory Medicine, National Taiwan University Hospital, Taipei, Taiwan.

Rei-Lin Kuo (RL)

Department of Medical Biotechnology and Laboratory Science, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Research Center for Emerging Viral Infections, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.

Hsing-I Huang (HI)

Department of Medical Biotechnology and Laboratory Science, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Research Center for Emerging Viral Infections, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Tao-Yuan, Taiwan.
Department of Pediatrics, Chang Gung Memorial Hospital, Linkou, Taiwan.

Classifications MeSH