Small RNA sequencing analysis reveals regulation of microRNA expression in Madin-Darby canine kidney epithelial cells infected with Canid alphaherpesvirus 1.
Canid alphaherpesvirus 1
Innate immunity
Small RNA-seq
miRNA
Journal
Virus genes
ISSN: 1572-994X
Titre abrégé: Virus Genes
Pays: United States
ID NLM: 8803967
Informations de publication
Date de publication:
17 Jul 2024
17 Jul 2024
Historique:
received:
27
04
2024
accepted:
09
07
2024
medline:
17
7
2024
pubmed:
17
7
2024
entrez:
17
7
2024
Statut:
aheadofprint
Résumé
Canid alphaherpesvirus 1 (CHV-1) infection can cause spontaneous abortions in pregnant dams, and in young puppies, fatal systemic infections are common. MicroRNAs (miRNAs) affect viral infection by binding to messenger RNAs, and inhibiting expression of host and/or viral genes. We conducted deep sequencing of small RNAs in CHV-1-infected and mock-infected Madin-Darby Canine Kidney (MDCK) epithelial cells, and detected sequences corresponding to 282 cellular miRNAs. Of these, 18 were significantly upregulated at 12 h post-infection, most of which were encoded on the X chromosome. We next quantified the mature forms of several of the miRNAs using stem loop RT-qPCR. Our results revealed a discordance between the levels of small RNAs corresponding to canine miRNAs, and levels of the corresponding mature miRNAs, which suggests a block in miRNA biogenesis in infected cells. Nevertheless, we identified several mature miRNAs that exhibited a statistically significant increase upon infection. These included cfa-miR-8908b, a miRNA of unknown function, and cfa-miR-146a, homologs of which target innate immune pathways and are known to play a role in other viral infections. Interestingly, ontology analysis predicted that cfa-miR-8908b targets factors involved in the ubiquitin-like protein conjugation pathway and peroxisome biogenesis among other cellular functions. This is the first study to evaluate changes in miRNA levels upon CHV-1 infection. Based on our findings, we developed a model whereby CHV-1 infection results in changes in levels of a limited number of cellular miRNAs that target elements of the host immune response, which may provide clues regarding novel therapeutic targets.
Identifiants
pubmed: 39017941
doi: 10.1007/s11262-024-02091-6
pii: 10.1007/s11262-024-02091-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Natural Sciences and Engineering Research Council of Canada
ID : RGPIN/06475-2016
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Dempsey DM et al (2020) Changes to virus taxonomy and the statutes ratified by the international committee on taxonomy of viruses (2020). Adv Virol 165(11):2737–2748. https://doi.org/10.1007/s00705-020-04752-x
doi: 10.1007/s00705-020-04752-x
Carmichael LE, Squire RA, Krook L (1965) Clinical and pathologic features of a fatal viral disease of newborn pups. Am J Vet Res 26(113):803–814
pubmed: 5892835
Appel MJ, Menegus M, Parsonson IM, Carmichael LE (1969) Pathogenesis of canine herpesvirus in specific-pathogen-free dogs: 5 to 12-week-old pups. Am J Vet Res 30(12):2067–2073
pubmed: 4311021
Ledbetter EC, da Silva EC, Kim SG, Dubovi EJ, Schwark WS (2012) Frequency of spontaneous canine herpesvirus-1 reactivation and ocular viral shedding in latently infected dogs and canine herpesvirus-1 reactivation and ocular viral shedding induced by topical administration of cyclosporine and systemic administration of corticosteroids. Am J Vet Res 73(7):1079–1084. https://doi.org/10.2460/ajvr.73.7.1079
doi: 10.2460/ajvr.73.7.1079
pubmed: 22738061
Evermann JF, Ledbetter EC, Maes RK (2011) Canine reproductive, respiratory, and ocular diseases due to canine herpesvirus. Vet Clin North Am Small Anim Pract 41(6):1097–1120. https://doi.org/10.1016/j.cvsm.2011.08.007
doi: 10.1016/j.cvsm.2011.08.007
pubmed: 22041206
pmcid: 7114841
Hashimoto A, Hirai K, Yamaguchi T, Fujimoto Y (1982) Experimental transplacental infection of pregnant dogs with canine herpesvirus. Am J Vet Res 43(5):844–850
pubmed: 6283965
Decaro N, Martella V, Buonavoglia C (2008) Canine adenoviruses and herpesvirus. Vet Clin North America Small Anim Pract 38(4):799–814. https://doi.org/10.1016/j.cvsm.2008.02.006
doi: 10.1016/j.cvsm.2008.02.006
Eisa M, Loucif H, van Grevenynghe J, Pearson A (2021) Entry of the Varicellovirus Canid herpesvirus 1 into Madin-Darby canine kidney epithelial cells is pH-independent and occurs via a macropinocytosis-like mechanism but without increase in fluid uptake. Cell Microbiol 23(12):e13398. https://doi.org/10.1111/cmi.13398
doi: 10.1111/cmi.13398
pubmed: 34697890
Miyoshi M, Ishii Y, Takiguchi M, Takada A, Yasuda J, Hashimoto A et al (1999) Detection of canine herpesvirus DNA in the ganglionic neurons and the lymph node lymphocytes of latently infected dogs. J Vet Med Sci / Japanese Soc Vet Sci 61(4):375–379
doi: 10.1292/jvms.61.375
Okuda Y, Ishida K, Hashimoto A, Yamaguchi T, Fukushi H, Hirai K, Carmichael LE (1993) Virus reactivation in bitches with a medical history of herpesvirus infection. Am J Vet Res 54(4):551–554
doi: 10.2460/ajvr.1993.54.04.551
pubmed: 8387252
Gilden DH, Vafai A, Shtram Y, Becker Y, Devlin M, Wellish M (1983) Varicella-zoster virus DNA in human sensory ganglia. Nature 306(5942):478–480. https://doi.org/10.1038/306478a0
doi: 10.1038/306478a0
pubmed: 6316159
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233. https://doi.org/10.1016/j.cell.2009.01.002
doi: 10.1016/j.cell.2009.01.002
pubmed: 19167326
pmcid: 3794896
Bartel DP (2018) Metazoan MicroRNAs. Cell 173(1):20–51. https://doi.org/10.1016/j.cell.2018.03.006
doi: 10.1016/j.cell.2018.03.006
pubmed: 29570994
pmcid: 6091663
Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15(8):509–524. https://doi.org/10.1038/nrm3838
doi: 10.1038/nrm3838
pubmed: 25027649
Bofill-De Ros X, Vang Orom UA (2024) Recent progress in miRNA biogenesis and decay. RNA Biol 21(1):1–8. https://doi.org/10.1080/15476286.2023.2288741
doi: 10.1080/15476286.2023.2288741
pubmed: 38031325
Drury RE, O’Connor D, Pollard AJ (2017) The clinical application of MicroRNAs in infectious disease. Front Immunol 8:1182. https://doi.org/10.3389/fimmu.2017.01182
doi: 10.3389/fimmu.2017.01182
pubmed: 28993774
pmcid: 5622146
Barbu MG, Condrat CE, Thompson DC, Bugnar OL, Cretoiu D, Toader OD et al (2020) MicroRNA involvement in signaling pathways during viral infection. Front Cell Dev Biol 8:143. https://doi.org/10.3389/fcell.2020.00143
doi: 10.3389/fcell.2020.00143
pubmed: 32211411
pmcid: 7075948
Pan D, Flores O, Umbach JL, Pesola JM, Bentley P, Rosato PC et al (2014) A neuron-specific host microRNA targets herpes simplex virus-1 ICP0 expression and promotes latency. Cell Host Microbe 15(4):446–456. https://doi.org/10.1016/j.chom.2014.03.004
doi: 10.1016/j.chom.2014.03.004
pubmed: 24721573
pmcid: 4142646
Sun B, Yang X, Hou F, Yu X, Wang Q, Oh HS et al (2021) Regulation of host and virus genes by neuronal miR-138 favours herpes simplex virus 1 latency. Nat Microbiol 6(5):682–696. https://doi.org/10.1038/s41564-020-00860-1
doi: 10.1038/s41564-020-00860-1
pubmed: 33558653
pmcid: 8221016
Ru J, Sun H, Fan H, Wang C, Li Y, Liu M, Tang H (2014) MiR-23a facilitates the replication of HSV-1 through the suppression of interferon regulatory factor 1. PLoS ONE 9(12):e114021. https://doi.org/10.1371/journal.pone.0114021
doi: 10.1371/journal.pone.0114021
pubmed: 25461762
pmcid: 4252059
Xie Y, He S, Wang J (2018) MicroRNA-373 facilitates HSV-1 replication through suppression of type I IFN response by targeting IRF1. Biomed Pharmacother Biomed Pharmacother 97:1409–1416. https://doi.org/10.1016/j.biopha.2017.11.071
doi: 10.1016/j.biopha.2017.11.071
pubmed: 29156530
Lagos D, Pollara G, Henderson S, Gratrix F, Fabani M, Milne RS et al (2010) miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat Cell Biol 12(5):513–519. https://doi.org/10.1038/ncb2054
doi: 10.1038/ncb2054
pubmed: 20418869
Motsch N, Pfuhl T, Mrazek J, Barth S, Grasser FA (2007) Epstein-Barr virus-encoded latent membrane protein 1 (LMP1) induces the expression of the cellular microRNA miR-146a. RNA Biol 4(3):131–137. https://doi.org/10.4161/rna.4.3.5206
doi: 10.4161/rna.4.3.5206
pubmed: 18347435
Hou J, Wang P, Lin L, Liu X, Ma F, An H et al (2009) MicroRNA-146a feedback inhibits RIG-I-dependent Type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J Immunol 183(3):2150–2158. https://doi.org/10.4049/jimmunol.0900707
doi: 10.4049/jimmunol.0900707
pubmed: 19596990
Papageorgiou KV, Suarez NM, Wilkie GS, McDonald M, Graham EM, Davison AJ (2016) Genome sequence of canine herpesvirus. PLoS ONE 11(5):e0156015. https://doi.org/10.1371/journal.pone.0156015
doi: 10.1371/journal.pone.0156015
pubmed: 27213534
pmcid: 4877106
Kozomara A, Birgaoanu M, Griffiths-Jones S (2019) miRBase: from microRNA sequences to function. Nucleic Acids Res 47(D1):D155–D162. https://doi.org/10.1093/nar/gky1141
doi: 10.1093/nar/gky1141
pubmed: 30423142
Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT et al (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33(20):e179. https://doi.org/10.1093/nar/gni178
doi: 10.1093/nar/gni178
pubmed: 16314309
pmcid: 1292995
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Agarwal V, Bell GW, Nam JW, Bartel DP (2015) Predicting effective microRNA target sites in mammalian mRNAs. Elife. https://doi.org/10.7554/eLife.05005
doi: 10.7554/eLife.05005
pubmed: 26274565
pmcid: 4566075
McGeary SE, Lin KS, Shi CY, Pham TM, Bisaria N, Kelley GM, Bartel DP (2019) The biochemical basis of microRNA targeting efficacy. Science. https://doi.org/10.1126/science.aav1741
doi: 10.1126/science.aav1741
pubmed: 31806698
pmcid: 7051167
Chen Y, Wang X (2020) miRDB: an online database for prediction of functional microRNA targets. Nucleic Acids Res 48(D1):D127–D131. https://doi.org/10.1093/nar/gkz757
doi: 10.1093/nar/gkz757
pubmed: 31504780
Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC et al (2022) DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res 50(W1):W216–W221. https://doi.org/10.1093/nar/gkac194
doi: 10.1093/nar/gkac194
pubmed: 35325185
pmcid: 9252805
Abdel Motaleb FI, Nabih ES, Mohamed SM, Abd Elhalim NS (2017) Up-regulation of circulating miRNA146a correlates with viral load via IRAK1 and TRAF6 in hepatitis C virus-infected patients. Virus Res 238:24–28. https://doi.org/10.1016/j.virusres.2017.05.026
doi: 10.1016/j.virusres.2017.05.026
pubmed: 28587864
Selvamani SP, Mishra R, Singh SK (2014) Chikungunya virus exploits miR-146a to regulate NF-kappaB pathway in human synovial fibroblasts. PLoS ONE 9(8):e103624. https://doi.org/10.1371/journal.pone.0103624
doi: 10.1371/journal.pone.0103624
pubmed: 25083878
pmcid: 4118904
Pan D, Li G, Morris-Love J, Qi S, Feng L, Mertens ME et al (2019) Herpes simplex virus 1 lytic infection blocks MicroRNA (miRNA) biogenesis at the stage of nuclear export of Pre-miRNAs. MBio. https://doi.org/10.1128/mBio.02856-18
doi: 10.1128/mBio.02856-18
pubmed: 31337724
pmcid: 6650555
Lee S, Song J, Kim S, Kim J, Hong Y, Kim Y et al (2013) Selective degradation of host MicroRNAs by an intergenic HCMV noncoding RNA accelerates virus production. Cell Host Microbe 13(6):678–690. https://doi.org/10.1016/j.chom.2013.05.007
doi: 10.1016/j.chom.2013.05.007
pubmed: 23768492
Hennig T, Prusty AB, Kaufer BB, Whisnant AW, Lodha M, Enders A et al (2022) Selective inhibition of miRNA processing by a herpesvirus-encoded miRNA. Nature 605(7910):539–544. https://doi.org/10.1038/s41586-022-04667-4
doi: 10.1038/s41586-022-04667-4
pubmed: 35508655
Golani-Zaidie L, Borodianskiy-Shteinberg T, Bisht P, Das B, Kinchington PR, Goldstein RS (2019) Bioinformatically-predicted varicella zoster virus small non-coding RNAs are expressed in lytically-infected epithelial cells and neurons. Virus Res 274:197773. https://doi.org/10.1016/j.virusres.2019.197773
doi: 10.1016/j.virusres.2019.197773
pubmed: 31614167
Di Palo A, Siniscalchi C, Salerno M, Russo A, Gravholt CH, Potenza N (2020) What microRNAs could tell us about the human X chromosome. Cell Mol Life Sci 77(20):4069–4080. https://doi.org/10.1007/s00018-020-03526-7
doi: 10.1007/s00018-020-03526-7
pubmed: 32356180
pmcid: 7854456
Forrest AR, Kanamori-Katayama M, Tomaru Y, Lassmann T, Ninomiya N, Takahashi Y et al (2010) Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 24(2):460–466. https://doi.org/10.1038/leu.2009.246
doi: 10.1038/leu.2009.246
pubmed: 19956200
Care A, Bellenghi M, Matarrese P, Gabriele L, Salvioli S, Malorni W (2018) Sex disparity in cancer: roles of microRNAs and related functional players. Cell Death Differ 25(3):477–485. https://doi.org/10.1038/s41418-017-0051-x
doi: 10.1038/s41418-017-0051-x
pubmed: 29352271
pmcid: 5864217
Sun H, Zhang Q, Jing YY, Zhang M, Wang HY, Cai Z et al (2017) USP13 negatively regulates antiviral responses by deubiquitinating STING. Nat Commun 8:15534. https://doi.org/10.1038/ncomms15534
doi: 10.1038/ncomms15534
pubmed: 28534493
pmcid: 5457515
Xu S, Han L, Wei Y, Zhang B, Wang Q, Liu J et al (2022) MicroRNA-200c-targeted contactin 1 facilitates the replication of influenza A virus by accelerating the degradation of MAVS. PLoS Pathog 18(2):e1010299. https://doi.org/10.1371/journal.ppat.1010299
doi: 10.1371/journal.ppat.1010299
pubmed: 35171955
pmcid: 8849533
Zhang Z, Fang X, Wu X, Ling L, Chu F, Li J et al (2020) Acetylation-dependent deubiquitinase OTUD3 controls MAVS activation in innate antiviral immunity. Mol Cell 79(2):304-319.e7. https://doi.org/10.1016/j.molcel.2020.06.020
doi: 10.1016/j.molcel.2020.06.020
pubmed: 32679077
Teo QW, Wong HH, Heunis T, Stancheva V, Hachim A, Lv H et al (2023) Usp25-Erlin1/2 activity limits cholesterol flux to restrict virus infection. Dev Cell 58(22):2495-2509.e6. https://doi.org/10.1016/j.devcel.2023.08.013
doi: 10.1016/j.devcel.2023.08.013
pubmed: 37683630
pmcid: 10914638
Xu Z, Asahchop EL, Branton WG, Gelman BB, Power C, Hobman TC (2017) MicroRNAs upregulated during HIV infection target peroxisome biogenesis factors: Implications for virus biology, disease mechanisms and neuropathology. PLoS Pathog 13(6):e1006360. https://doi.org/10.1371/journal.ppat.1006360
doi: 10.1371/journal.ppat.1006360
pubmed: 28594894
pmcid: 5464672
Gonugunta VK, Sakai T, Pokatayev V, Yang K, Wu J, Dobbs N, Yan N (2017) Trafficking-mediated STING degradation requires sorting to acidified endolysosomes and can be targeted to enhance anti-tumor response. Cell Rep 21(11):3234–3242. https://doi.org/10.1016/j.celrep.2017.11.061
doi: 10.1016/j.celrep.2017.11.061
pubmed: 29241549
pmcid: 5905341
Ritter JL, Zhu Z, Thai TC, Mahadevan NR, Mertins P, Knelson EH et al (2020) Phosphorylation of RAB7 by TBK1/ikkepsilon regulates innate immune signaling in triple-negative breast cancer. Can Res 80(1):44–56. https://doi.org/10.1158/0008-5472.CAN-19-1310
doi: 10.1158/0008-5472.CAN-19-1310
Husebye H, Aune MH, Stenvik J, Samstad E, Skjeldal F, Halaas O et al (2010) The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes. Immunity 33(4):583–596. https://doi.org/10.1016/j.immuni.2010.09.010
doi: 10.1016/j.immuni.2010.09.010
pubmed: 20933442
pmcid: 10733841
Oussaief L, Fendri A, Chane-Woon-Ming B, Poirey R, Delecluse HJ, Joab I, Pfeffer S (2015) Modulation of MicroRNA cluster miR-183-96-182 expression by Epstein-Barr virus latent membrane protein 1. J Virol 89(23):12178–12188. https://doi.org/10.1128/JVI.01757-15
doi: 10.1128/JVI.01757-15
pubmed: 26401047
pmcid: 4645329
Venuti A, Musarra-Pizzo M, Pennisi R, Tankov S, Medici MA, Mastino A et al (2019) HSV-1\EGFP stimulates miR-146a expression in a NF-kappaB-dependent manner in monocytic THP-1 cells. Sci Rep 9(1):5157. https://doi.org/10.1038/s41598-019-41530-5
doi: 10.1038/s41598-019-41530-5
pubmed: 30914680
pmcid: 6435682
Zubchenko S, Maruniak S, tYuriev S, Sharikadze O (2019) Peculiarities of Mir-146a and Mir-155 expression in patients with allergopathy in combination with chronic Epstein-Barr virus infection in latent and active phases. Georgian Med News 290:69–73