MicroRNA expression profiling of goat peripheral blood mononuclear cells in response to peste des petits ruminants virus infection

Springer Science and Business Media LLC - Tập 49 - Trang 1-10 - 2018
Xuefeng Qi1, Ting Wang1, Qinghong Xue2, Zhen Li1, Bo Yang1, Jingyu Wang1
1College of Veterinary Medicine, Northwest A&F University, Yangling, China
2China Institute of Veterinary Drug Control, Beijing, China

Tóm tắt

Peste des petits ruminants virus (PPRV) belongs to the genus Morbillivirus that causes an acute and highly contagious disease in goats and sheep. Virus infection can trigger the change in the cellular microRNA (miRNA) expression profile, which play important post-transcriptional regulatory roles in gene expression and can greatly influence viral replication and pathogenesis. Here, we employed deep sequencing technology to determine cellular miRNA expression profile in goat peripheral blood mononuclear cells (PBMC) infected with Nigeria 75/1 vaccine virus, a widely used vaccine strain for mass vaccination programs against Peste des petits ruminants. Expression analysis demonstrated that PPRV infection can elicit 316 significantly differentially expressed (DE) miRNA including 103 known and 213 novel miRNA candidates in infected PBMC at 24 hours post-infection (hpi) as compared with a mock control. Target prediction and functional analysis of these DEmiRNA revealed significant enrichment for several signaling pathways including TLR signaling pathways, PI3K-Akt, endocytosis, viral carcinogenesis, and JAK-STAT signaling pathways. This study provides a valuable basis for further investigation of the roles of miRNA in PPRV replication and pathogenesis.

Tài liệu tham khảo

Banyard AC, Parida S, Batten C, Oura C, Kwiatek O, Libeau G (2010) Global distribution of peste des petits ruminants virus and prospects for improved diagnosis and control. J Gen Virol 91:2885–2897 Gibbs EP, Taylor WP, Lawman MJ, Bryant J (1979) Classification of peste des petits ruminants virus as the fourth member of the genus Morbillivirus. Intervirology 11:268–274 Kumar KS, Babu A, Sundarapandian G, Roy P, Thangavelu A, Kumar KS, Arumugam R, Chandran ND, Muniraju M, Mahapatra M, Banyard AC, Manohar BM, Parida S (2014) Molecular characterisation of lineage IV peste des petits ruminants virus using multi gene sequence data. Vet Microbiol 174:39–49 Kumar N, Maherchandani S, Kashyap SK, Singh SV, Sharma S, Chaubey KK, Ly H (2014) Peste des petits ruminants virus infection of small ruminants: a comprehensive review. Viruses 6:2287–2327 Albina E, Kwiatek O, Minet C, Lancelot R, Servan de Almeida R, Libeau G (2013) Peste des petits ruminants, the next eradicated animal disease? Vet Microbiol 165:38–44 Diallo A, Minet C, Le Goff C, Berhe G, Albina E, Libeau G, Barrett T (2007) The threat of peste des petits ruminants: progress in vaccine development for disease control. Vaccine 25:5591–5597 Saravanan P, Sen A, Balamurugan V, Rajak KK, Bhanuprakash V, Palaniswami KS, Nachimuthu K, Thangavelu A, Dhinakarraj G, Hegde R, Singh RK (2010) Comparative efficacy of peste des petits ruminants (PPR) vaccines. Biologicals 38:479–485 Diallo A, Barrett T, Barbron M, Subbarao SM, Taylor WP (1989) Differentiation of rinder pest and peste des petits ruminants viruses using specific cDNA clones. J Virol Methods 23:127–136 Pawar RM, Dhinakar Raj G, Balachandran C (2008) Relationship between thelevel of signaling lymphocyte activation molecule mRNA and replication of Peste-des-petits-ruminants virus in peripheral blood mononuclear cells of host animals. Acta Virol 52:231–236 Bolt G, Berg K, Blixenkrone-Moller M (2002) Measles virus-induced modulation of host-cell gene expression. J Gen Virol 83:1157–1165 Iwasa T, Suga S, Qi L, Komada Y (2010) Apoptosis of human peripheral blood mononuclear cells by wild-type measles virus infection is induced by interaction of hemagglutinin protein and cellular receptor, SLAM viacaspase-dependent pathway. Microbiol Immunol 54:405–416 Dhanasekaran S, Biswas M, Vignesh AR, Ramya R, Raj GD, Tirumurugaan KG, Raja A, Kataria RS, Parida S, Subbiah E (2014) Toll-like receptor responses to Peste des petits ruminants virus in goats and water buffalo. PLoS One 9:e111609 Manjunath S, Kumar GR, Mishra BP, Mishra B, Sahoo AP, Joshi CG, Tiwari AK, Rajak KK, Janga SC (2015) Genomic analysis of host–Peste des petits ruminants vaccine viral transcriptome uncovers transcription factors modulating immune regulatory pathways. Vet Res 46:15 Manjunath S, Mishra BP, Mishra B, Sahoo AP, Tiwari AK, Rajak KK, Muthuchelvan D, Saxena S, Santra L, Sahu AR, Wani SA, Singh RP, Singh YP, Pandey A, Kanchan S, Singh RK, Kumar GR, Janga SC (2017) Comparative and temporal transcriptome analysis of peste des petits ruminants virus infected goat peripheral blood mononuclear cells. Virus Res 229:28–40 Axtell MJ, Westholm JO, Lai EC (2011) Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12:221 Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233 Shukla GC, Singh J, Barik S (2011) MicroRNAs: processing, maturation, target recognition and regulatory functions. Mol Cell Pharmacol 3:83–92 Haasnoot J, Berkhout B (2011) RNAi and cellular miRNAs in infections bymammalian viruses. Methods Mol Biol 721:23–41 Sharma N, Singh SK (2016) Implications of non-coding RNAs in viral infections. Rev Med Virol 26:356–368 Shrinet J, Jain S, Jain J, Bhatnagar RK, Sunil S (2014) Next generation sequencing reveals regulation of distinct Aedes microRNAs during chikungunya virus development. PLoS Negl Trop Dis 8:e2616 Skovgaard K, Cirera S, Vasby D, Podolska A, Breum SO, Durrwald R, Schlegel M, Heegaard PM (2013) Expression of innate immune genes, proteins and microRNAs in lung tissue of pigs infected experimentally with influenza virus (H1N2). Innate Immun 19:531–544 Slonchak A, Hussain M, Torres S, Asgari S, Khromykh AA (2014) Expression of mosquito microRNA Aae-miR-2940-5p is downregulated in response to West Nile virus infection to restrict viral replication. J Virol 88:8457–8467 Zhang Y, Jing J, Li X, Wang J, Feng X, Cao R, Chen P (2015) Integration analysis of miRNA and mRNA expression profiles in swine testis cells infected with Japanese encephalitis virus. Infect Genet Evol 32:342–347 Qi X, Qin L, Du R, Chen Y, Lei M, Deng M, Wang J (2017) Lipopolysaccharide upregulated intestinal epithelial cell expression of Fn14 and activation of Fn14 signaling amplify intestinal TLR4-mediated inflammation. Front Cell Infect Microbiol 7:315 Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, Finn RD (2015) Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43:D130–D137 Dong Y, Xie M, Jiang Y, Xiao N, Du X, Zhang W, Tosser-Klopp G, Wang J, Yang S, Liang J, Chen W, Chen J, Zeng P, Hou Y, Bian C, Pan S, Li Y, Liu X, Wang W, Servin B, Sayre B, Zhu B, Sweeney D, Moore R, Nie W, Shen Y, Zhao R, Zhang G, Li J, Faraut T, Womack J, Zhang Y, Kijas J, Cockett N, Xu X, Zhao S, Wang J, Wang W (2013) Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus). Nat Biotechnol 31:135–141 Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714 Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297 Schmittgen TD, Lee EJ, Jiang J, Sarkar A, Yang L, Elton TS, Chen C (2008) Real-time PCR quantification of precursor and mature microRNA. Methods 44:31–38 Lai F, Zhai H, Cheng M, Ma J, Cheng S, Ge W, Zhang G, Wang J, Zhang R, Wang X, Min L, Song J, Shen W (2016) Whole-genome scanning for the litter size trait associated genes and SNPs under selection in dairy goat (Capra hircus). Sci Rep 6:38096 Liu Y, Zhou Y, Wu J, Zheng P, Li Y, Zheng X, Puthiyakunnon S, Tu Z, Chen XG (2015) The expression profile of Aedes albopictusmiRNAs is altered by dengue virus serotype- 2 infection. Cell Biosci 5:16 Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P (2005) Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309:1577–1581 Norman KL, Sarnow P (2010) Modulation of hepatitis C virus RNA abundance and the isoprenoid biosynthesis pathway by microRNA miR-122 involves distinct mechanisms. J Virol 84:666–670 Ghosh Z, Mallick B, Chakrabarti J (2009) Cellular versus viral microRNAs in host-virus interaction. Nucleic Acids Res 37:1035–1048 Lu LF, Gasteiger G, Yu IS, Chaudhry A, Hsin JP, Lu Y, Bos PD, Lin LL, Zawislak CL, Cho S, Sun JC, Leslie CS, Lin SW, Rudensky AY (2015) A singlemiRNA-mRNA interaction affects the immune response in a context-and cell-type-specific manner. Immunity 43:52–64 Samir M, Vaas LA, Pessler F (2016) MicroRNAs in the host response to viral infections of veterinary importance. Front Vet Sci 3:86 Girardin SE, Sansonetti PJ, Philpott DJ (2002) Intracellular vs extracellular recognition of pathogens—common concepts in mammals and flies. Trends Microbiol 10:193–199 Gack MU, Diamond MS (2016) Innate immune escape by Dengue and West Nile viruses. Curr Opin Virol 20:119–128 Schwartz-Cornil I, Mertens PP, Contreras V, Hemati B, Pascale F, Breard E, Mellor PS, MacLachlan NJ, Zientara S (2008) Bluetongue virus: virology, pathogenesis and immunity. Vet Res 39:46 Vitour D, Doceul V, Ruscanu S, Chauveau E, Schwartz-Cornil I, Zientara S (2014) Induction and control of the type I interferon pathway by Bluetongue virus. Virus Res 182:59–70 Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O, Brummelkamp TR, Fleming MD, Camargo FD (2008) Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 451:1125–1129 Liu G, Friggeri A, Yang Y, Park YJ, Tsuruta Y, Abraham E (2009) miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci U S A 106:15819–15824 Pandey A, Sahu AR, Wani SA, Saxena S, Kanchan S, Sah V, Rajak KK, Khanduri A, Sahoo AP, Tiwari AK, Mishra B, Muthuchelvan D, Mishra BP, Singh RK, Gandham RK (2017) Modulation of host miRNAs transcriptome in lung and spleen of Peste des petits ruminants virus infected sheep and goats. Front Microbiol 8:1146 Wu J, Shen L, Chen J, Xu H, Mao L (2015) The role of microRNAs in enteroviral infections. Braz J Infect Dis 19:510–516 Chinnakannan SK, Nanda SK, Baron MD (2013) Morbillivirus v proteins exhibit multiple mechanisms to block type 1 and type 2 interferon signalling pathways. PLoS One 8:e57063 Ma X, Yang X, Nian X, Zhang Z, Dou Y, Zhang X, Luo X, Su J, Zhu Q, Cai X (2015) Identification of amino-acid residues in the V protein of peste des petits ruminants essential for interference and suppression of STAT-mediated interferon signaling. Virology 483:54–63 Sanz Bernardo B, Goodbourn S, Baron MD (2017) Control of the induction of type I interferon by Peste des petits ruminants virus. PLoS One 12:e0177300 Baron J, Bin-Tarif A, Herbert R, Frost L, Taylor G, Baron MD (2014) Early changes in cytokine expression in peste des petits ruminants disease. Vet Res 45:22–33 Gao Z, Dou Y, Chen Y, Zheng Y (2014) MicroRNA roles in the NF- kappaB signaling pathway during viral infections. Biomed Res Int 2014:436097 Hoesel B, Schmid JA (2013) The complexity of NF-kappaB signaling in inflammation and cancer. Mol Cancer 12:86 Mondal B, Sreenivasa BP, Dhar P, Singh RP, Bandyopadhyay SK (2001) Apoptosis induced by peste des petits ruminants virus in goat peripheral blood mononuclear cells. Virus Res 73:113–119 Zhang Y, Wu S, Lv J, Feng C, Deng J, Wang C, Yuan X, Zhang T, Lin X (2013) Peste des petits ruminants virus exploits cellular autophagy machinery for replication. Virology 437:28–38