MicroRNA miR-320a and miR-140 inhibit mink enteritis virus infection by repression of its receptor, feline transferrin receptor

Virology Journal

Weiquan Liu¹  Yaping Mao¹  Qiang Hou¹  Bao Yi¹  Zhili Li¹  Daoli Yuan¹  Shuang Wang¹  Jigui Wang¹  Jia-zeng Sun¹ 

[1] State Key Laboratory of Agrobiotechnology, Department of Biochemistry and Molecular Biology, College of Biological Sciences, China Agricultural University, No. 2 Yuanmingyuan West Road, Haidian District, Beijing 100193, China

关键词: Transferrin receptor (TfR);    miR-140;    miR-320a;    Mink enteritis virus (MEV);   

Others  :  1131080
DOI  :  10.1186/s12985-014-0210-3

 received in 2014-09-15, accepted in 2014-11-19,  发布年份 2014

【 摘 要 】

Mink enteritis virus (MEV) is one of the most important pathogens in the mink industry. Recent studies have shed light into the role of microRNAs (miRNAs), small noncoding RNAs of length ranging from 18–23 nucleotides (nt), as critical modulators in the host-pathogen interaction networks. We previously showed that miRNA miR-181b can inhibit MEV replication by repression of viral non-structural protein 1 expression. Here, we report that two other miRNAs (miR-320a and miR-140) inhibit MEV entry into feline kidney (F81) cells by downregulating its receptor, transferrin receptor (TfR), by targeting the 3′ untranslated region (UTR) of TfR mRNA, while being themselves upregulated.

【 授权许可】

   
2014 Sun et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Park GS, Best SM, Bloom ME: Two mink parvoviruses use different cellular receptors for entry into CRFK cells. Virology 2005, 340:1-9.
• [2]Rivera E, Karlsson KA, Bergman R: The propagation of feline panleukopenia virus in microcarrier cell-culture and use of the inactivated virus in the protection of mink against viral-enteritis. Vet Microbiol 1987, 13:371-381.
• [3]Schofield FW: Virus enteritis in mink. North Amer Vet 1949, 30:651-654.
• [4]Zhang DL: Studies on isolation, serum-free cultivation and manufacture of mink enteritis virus optimized for vaccine preparation. Biologicals 1997, 25:103-111.
• [5]Zuo J, Rao J, Xu H, Ma L, Li B, Wang Y, Cai X, Han W, Lei L, Liu B: Analysis of the vp2 gene sequence of a new mutated mink enteritis parvovirus strain in PR China. Virol J 2010, 7:124-129. BioMed Central Full Text
• [6]Ambros V: The functions of animal microRNAs. Nature 2004, 431:350-355.
• [7]Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
• [8]Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function (Reprinted from Cell 116, 281–297, 2004). Cell 2007, 131:11-29.
• [9]Krol J, Loedige I, Filipowicz W: The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11:597-610.
• [10]Cameron JE, Yin Q, Fewell C, Lacey M, McBride J, Wang X, Lin Z, Schaefer BC, Flemington EK: Epstein-Barr virus latent membrane protein 1 induces cellular MicroRNA miR-146a, a modulator of lymphocyte signaling pathways. J Virol 2008, 82:1946-1958.
• [11]Scaria V, Hariharan M, Maiti S, Pillai B, Brahmachari SK: Host-virus interaction: a new role for microRNAs. Retrovirology 2006, 3:68-76. BioMed Central Full Text
• [12]Grey F, Tirabassi R, Meyers H, Wu G, McWeeney S, Hook L, Nelson JA: A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′ UTRs. PLoS Pathog 2010, 6:e1000967.
• [13]Motsch N, Pfuhl T, Mrazek J, Barth S, Graesser FA: Epstein-Barr virus-encoded latent membrane protein 1 (LMP1) induces the expression of the cellular microRNA miR-146a. RNA Biol 2007, 4:131-137.
• [14]Ahluwalia JK, Khan SZ, Soni K, Rawat P, Gupta A, Hariharan M, Scaria V, Lalwani M, Pillai B, Mitra D, Brahmachari SK: Human cellular microRNA hsa-miR-29a interferes with viral nef protein expression and HIV-1 replication. Retrovirology 2008, 5:117-126. BioMed Central Full Text
• [15]Barth S, Pfuhl T, Mamiani A, Ehses C, Roemer K, Kremmer E, Jäker C, Höck J, Meister G, Grässer FA: Epstein-Barr virus-encoded microRNA miR-BART2 down-regulates the viral DNA polymerase BALF5. Nucleic Acids Res 2008, 36:666-675.
• [16]Lung RWM, Tong JHM, Sung YM, Leung PS, Ng DCH, Chau SL, Chan AWH, Ng EKO, Lo KW, To KF: Modulation of LMP2A expression by a newly identified Epstein-Barr virus-encoded microRNA miR-BART22. Neoplasia 2009, 11:1174-U1189.
• [17]Song L, Liu H, Gao S, Jiang W, Huang W: Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells. J Virol 2010, 84:8849-8860.
• [18]Sun JZ, Wang J, Yuan D, Wang S, Li Z, Yi B, Mao Y, Hou Q, Liu W: Cellular microRNA miR-181b inhibits replication of mink enteritis virus by repression of non-structural protein 1 translation. PLoS ONE 2013, 8:e81515.
• [19]Goodman LB, Lyi SM, Johnson NC, Cifuente JO, Hafenstein SL, Parrish CR: Binding site on the transferrin receptor for the parvovirus capsid and effects of altered affinity on cell uptake and infection. J Virol 2010, 84:4969-4978.
• [20]Hueffer K, Govindasamy L, Agbandje-McKenna M, Parrish CR: Combinations of two capsid regions controlling canine host range determine canine transferrin receptor binding by canine and feline parvoviruses. J Virol 2003, 77:10099-10105.
• [21]Hueffer K, Palermo LM, Parrish CR: Parvovirus infection of cells by using variants of the feline transferrin receptor altering clathrin-mediated endocytosis, membrane domain localization, and capsid-binding domains. J Virol 2004, 78:5601-5611.
• [22]Mellman I: Endocytosis and molecular sorting. Annu Rev Cell Dev Biol 1996, 12:575-625.
• [23]Palermo LM, Hafenstein SL, Parrish CR: Purified feline and canine transferrin receptors reveal complex interactions with the capsids of canine and feline parvoviruses that correspond to their host ranges. J Virol 2006, 80:8482-8492.
• [24]Parker JSL, Murphy WJ, Wang D, O’Brien SJ, Parrish CR: Canine and feline parvoviruses can use human or feline transferrin receptors to bind, enter, and infect cells. J Virol 2001, 75:3896-3902.
• [25]Glazov EA, Cottee PA, Barris WC, Moore RJ, Dalrymple BP, Tizard ML: A microRNA catalog of the developing chicken embryo identified by a deep sequencing approach. Genome Res 2008, 18:957-964.
• [26]Pontius JU, Mullikin JC, Smith DR, Lindblad-Toh K, Gnerre S, Clamp M, Chang J, Stephens R, Neelam B, Volfovsky N, Schäffer AA, Agarwala R, Narfström K, Murphy WJ, Giger U, Roca AL, Antunes A, Menotti-Raymond M, Yuhki N, Pecon-Slattery J, Johnson WE, Bourque G, Tesler G, O’Brien SJ: Initial sequence and comparative analysis of the cat genome. Genome Res 2007, 17:1675-1689.
• [27]Pontius JU, O’Brien SJ: Genome annotation resource Fields-GARFIELD: a genome browser for Felis catus. J Hered 2007, 98:386-389.
• [28]Li R, Li Y, Kristiansen K, Wang J: SOAP: short oligonucleotide alignment program. Bioinformatics 2008, 24:713-714.
• [29]Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P: CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 2007, 8:209-216. BioMed Central Full Text
• [30]Krueger J, Rehmsmeier M: RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res 2006, 34:W451-W454.
• [31]Huang HY, Chien CH, Jen KH, Huang HD: RegRNA: an integrated web server for identifying regulatory RNA motifs and elements. Nucleic Acids Res 2006, 34:W429-W434.
• [32]Yang CH, Yue J, Fan M, Pfeffer LM: IFN induces miR-21 through a signal transducer and activator of transcription 3-dependent pathway as a suppressive negative feedback on IFN-induced apoptosis. Cancer Res 2010, 70:8108-8116.
• [33]Bookout AL, Cummins CL, Mangelsdorf DJ, Pesola JM, Kramer MF: High-throughput real-time quantitative reverse transcription PCR. Curr Protoc Mol Biol 2006, Chapter 15:Unit 15.8.
• [34]Sun JZ, Wang J, Wang S, Yuan D, Birame BM, Li Z, Yi B, Liu W: MicroRNA profile analysis of a feline kidney cell line before and after infection with mink enteritis virus. Gene 2014, 539:224-229.
• [35]Otsuka M, Jing Q, Georgel P, New L, Chen J, Mols J, Kang YJ, Jiang Z, Du X, Cook R, Das SC, Pattnaik AK, Beutler B, Han J: Hypersusceptibility to vesicular stomatitis virus infection in Dicer1-deficient mice is due to impaired miR24 and miR93 expression. Immunity 2007, 27:123-134.
• [36]Chen Y, Shen A, Rider PJ, Yu Y, Wu K, Mu Y, Hao Q, Liu Y, Gong H, Zhu Y, Liu F, Wu J: A liver-specific microRNA binds to a highly conserved RNA sequence of hepatitis B virus and negatively regulates viral gene expression and replication. FASEB J 2011, 25:4511-4521.
• [37]Huang Y, Shen XJ, Zou QA, Wang SP, Tang SM, Zhang GZ: Biological functions of microRNAs: a review. J Physiol Biochem 2011, 67:129-139.
• [38]Lecellier CH, Dunoyer P, Arar K, Lehmann-Che J, Eyquem S, Himber C, Saib A, Voinnet O: A cellular MicroRNA mediates antiviral defense in human cells. Science 2005, 308:557-560.
• [39]Nathans R, Chu CY, Serquina AK, Lu CC, Cao H, Rana TM: Cellular microRNA and P bodies modulate host-HIV-1 interactions. Mol Cell 2009, 34:696-709.
• [40]Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, David M: Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 2007, 449:919-U913.
• [41]Aisen P: Transferrin receptor 1. Int J Biochem Cell B 2004, 36:2137-2143.
• [42]Cheng Y, Zak O, Alsen P, Harrison SC, Walz T: Structure of the human transferrin receptor-transferrin complex. Cell 2004, 116:565-576.
• [43]Kwok JC, Richardson DR: The iron metabolism of neoplastic cells: alterations that facilitate proliferation? Crit Rev Oncol Hemat 2002, 42:65-78.
• [44]Gatter KC, Brown G, Trowbridge IS, Woolston RE, Mason DY: Transferrin receptors in human-tissues - their distribution and possible clinical relevance. J Clin Pathol 1983, 36:539-545.
• [45]Chitambar CR, Massey EJ, Seligman PA: Regulation of transferrin receptor expression on human-leukemic cells during proliferation and induction of differentiation - effects of gallium and dimethylsulfoxide. J Clin Invest 1983, 72:1314-1325.
• [46]Larrick JW, Cresswell P: Modulation of cell-surface iron transferrin receptors by cellular density and state of activation. J Supramol Struct 1979, 11:579-586.
• [47]Neckers LM, Trepel JB: Transferrin receptor expression and the control of cell-growth. Cancer Invest 1986, 4:461-470.
• [48]Op De Beeck A, Caillet-Fauquet P: Viruses and the cell cycle. Prog Cell Cycle Res 1997, 3:1-19.
• [49]Tattersall P: Replication of the parvovirus MVM 1. Dependence of virus multiplication and plaque-formation on cell-growth. J Virol 1972, 10:586-590.
• [50]Davidson BL, McCray PB Jr: Current prospects for RNA interference-based therapies. Nat Rev Genet 2011, 12:329-340.
• [51]Geisbert TW, Lee ACH, Robbins M, Geisbert JB, Honko AN, Sood V, Johnson JC, de Jong S, Tavakoli I, Judge A, Hensley LE, MacLachlan I: Postexposure protection of non-human primates against a lethal Ebola virus challenge with RNA interference: a proof-of-concept study. Lancet 2010, 375:1896-1905.
• [52]Li BJ, Tang QQ, Cheng D, Qin C, Xie FY, Wei Q, Xu J, Liu YJ, Zheng BJ, Woodle MC, Zhong NS, Lu PY: Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in rhesus macaque. Nat Med 2005, 11:944-951.
• [53]Palliser D, Chowdhury D, Wang QY, Lee SJ, Bronson RT, Knipe DM, Lieberman J: An siRNA-based microbicide protects mice from lethal herpes simplex virus 2 infection. Nature 2006, 439:89-94.
• [54]Tompkins SM, Lo CY, Tumpey TM, Epstein SL: Protection against lethal influenza virus challenge by RNA interference in vivo. Proc Natl Acad Sci U S A 2004, 101:8682-8686.