MicroRNA miR-320a and miR-140 inhibit mink enteritis virus infection by repression of its receptor, feline transferrin receptor
© Sun et al.; licensee BioMed Central Ltd. 2014
Received: 15 September 2014
Accepted: 19 November 2014
Published: 3 December 2014
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.
Mink enteritis virus (MEV) is an autonomous parvovirus that causes important disease in mink, leading to huge economic losses worldwide. MEV is a single-stranded negative sense DNA virus belonging to the family Parvoviridae, with a genome of about 5 kb containing 2 main open reading frames (ORFs). MEV, a variant of feline panleukopenia virus (FPV) and highly homologous with canine parvovirus (CPV), causes a highly infectious acute disease of mink characterized by extensive virus replication in mesenteric lymph nodes and intestinal crypt epithelial cells, with an associated loss of intestinal mucosa, diarrhea, and a high rate of morbidity and mortality -.
MicroRNAs (miRNAs) are endogenous and highly conserved small noncoding RNAs of length 18–23 nucleotides (nt), which have gained widespread attention as critical modulators in many biological processes including cell proliferation and differentiation, development and apoptosis. In animals, miRNAs are imprecisely complimentary to their mRNA targets and act by repression of target gene expression -.
Attention has also been paid to the role of miRNAs as effectors in host-virus interaction networks ,, either by targeting cellular factors useful for virus replication , or by directly targeting virus mRNAs -. We have recently reported that a cellular miRNA miR-181b inhibits MEV infection by repression of viral non-structural protein 1 expression , which indicates that cellular miRNAs may play a direct role on viral mRNAs themselves.
For many animal viruses, cell entry and infection are initiated by receptor-mediated endocytosis involving specific cellular surface components. Transferrin receptor (TfR), is required for the import of iron into the cell, and is regulated by intracellular iron concentration. It has also been reported to be a receptor for MEV, controlling the first step in the viral infection process. TfR can be considered a model for the endocytosis and recycling of receptor-ligand complexes: it is excluded from lipid raft domains in the plasma membrane and is taken up rapidly from the cell surface via clathrin-mediated endocytosis ,-. Since TfR plays an important role in MEV infection, we therefore investigated whether miRNAs participate in the host-virus interaction by modulating its activity.
Materials and methods
Cell culture and MEV infection
Feline F81 cells, obtained from the American Type Culture Collection (ATCC), were cultured as monolayers in minimum essential medium (MEM) (Gibco, CA) containing 10% FBS (Hyclone, Logan, UT), and 1% penicillin-streptomycin (Gibco) at 37°C in a 5% CO2 atmosphere. MEV strain L was originally isolated from an infected animal in a mink farm, Liaoning province, China. The whole viral genome has been sequenced in our laboratory and found to have high identity with MEV strain Abashiri (GenBank accession, D00765.1). For infection, F81 cell monolayers were first dispersed by 0.25% trypsin and virus was added to the suspension before incubation in the original plates.
Deep sequencing of small RNAs and analysis of the sequencing data 
F81 cells cultured in 6-well plates (Costar) were infected with MEV at an input multiplicity (MOI) of 1 pfu/cell. Uninfected cells were maintained as a control. Twenty-four h later, the triplicate cultures were pooled, total RNA was extracted by Trizol reagent (Invitrogen) and small RNAs with length of 18–30 nt were separated by PAGE. Ten μg samples of the isolated RNAs were submitted to Solexa (Illumina) for sequencing as cDNA libraries. Duplicate sequences were eliminated from the initial data set. The resulting sets of unique reads were mapped onto the feline genome , using the program Short Oligonucleotide Analysis Package (SOAP) . Perfectly matched reads were also mapped onto the miRNAs of six reference species (Homo sapiens, Canis familiaris, Mus musculus, Rattus norvegicus, Bos taurus and Sus scrofa) listed in the Sanger miRBase (Release 18) using the Patscan tool  to identify homologs of known miRNAs.
Prediction of miRNA targets in feline TfR mRNA 3′UTR
RNAhybrid tools (http://bibiserv.techfak.uni-bielefeld.de/rnahybrid/submission.html/)  were used to predict miRNA targets in TfR mRNA 3′UTR following the rules of no mismatch and G/U complementarity in miRNA seed sequences. RegRNA tools (http://vita.mbc.nctu.edu.tw/)  were also used to predict regulatory RNA motifs in the TfR mRNA 3′UTR. TargetScan (http://www.targetscan.org/) tools were used to predict conservative miRNA targets in the TfR mRNA 3′UTRs of different species.
The luciferase expression vector pGL3-control (Promega) was used for construction of predicted miRNA candidate targets containing a luciferase reporter gene, with pRL-TK (Promega) as control. Sequences containing part of the TfR 3′UTR and candidate targets of miRNAs were amplified by RT-PCR and directionally inserted into the 3′UTR of the luciferase gene in the pGL3-control vector, generating pGL3-TfR 3′UTR. To facilitate cloning, the first PCR product amplified by the first pair of primers (5′-ATGTGGTACCTATACTTATATGAGAAC-3′ and 5′-TCCGTGTTCAAGCATTTTATTAAATC-3′) was used as a template and an Xba I restriction site (italics) was added to the 5’- (5′-GCTCTAGA ATGTGGTACCTATACTTATATGAGAACAGC-3′) and 3′- (5′-GCTCTAGA TCCGTGTTCAAGCATTTTATTAAATCAG-3′) secondary pair of primers. To further ascertain that the binding sites of the predicted miRNAs in TfR 3′UTR indeed existed, tetranucleotide mutations were generated in the two potential target sites of pGL3-TfR 3′UTR using PCR, resulting in mut320a-pGL3-TfR 3′UTR (5′-CACTAGATTTCTTTAGGCAGCACGAA TTAATACAGGGTAGGTAC-3′ and 5′-GTACCTACCCTGTATTAATTCG TGCTGCCTAAAGAAATCTAGTG-3′) and mut140-pGL3-TfR 3′UTR (5′-CTTCAAGTTAAAGTGAATAAGGTG TTAAAAATGTTCATGATAGAATC-3′ and 5′-GATTCTATCATGAACATTTTTAACACC TTATTCACTTTAACTTGAAG-3′). Mutant plasmids were generated by PCR using PrimeSTAR MAX DNA Polymerase (TaKaRa), 50 ng of the parent vectors as templates and the complementary primers under the following conditions: 98°C for 3 min, followed by 30 cycles of 98°C for 10 s, 55°C for 15 s and 72°C for 90 s, followed by 72°C 10 min. The resulting products were digested with 1 μl Dpn-1 for 1 h at 37°C to remove the parental DNA. The remaining DNA was used to transform competent DH5α cells, and a number of colonies containing mutant plasmids were obtained and confirmed by sequencing (Shanghai Sangong Co.).
miRNA mimics and inhibitors
The miR-320a, miR-320b, miR-140, miR-145, miR-152, miR-182 and miR-194 mimics and inhibitors, mut miR-320 mimics (in which the tetranucleotide mutation was complementary to mut320 pGL3-TfR 3′UTR) and mut miR-140 mimics (in which the tetranucleotide mutation was complementary to mut140 pGL3-TfR 3′UTR) were synthesized by GenePharma, Shanghai. All mimics were double-stranded RNA oligos, while inhibitors were single-stranded. Negative control mimics and inhibitors were also synthesized for control experiments. The inhibitors were modified by 2′-O-methylation. All sequences of mimics and inhibitors are listed below (italic letters are mutated bases):
miR-320a mimics: 5′-AAAAGCUGGGUUGAGAGGGCGA-3′
miR-320a inhibitors: 5′-UCGCCCUCUCAACCCAGCUUUU-3′
miR-320b mimics: 5′-AAAAGCUGGGUUGAGAGGGCAA-3′
miR-320b inhibitors: 5′-UUGCCCUCUCAACCCAGCUUUU-3′
miR-140 mimics: 5′-CAGUGGUUUUACCCUAUGGUAG-3′
miR-140 inhibitors: 5′-CUACCAUAGGGUAAAACCACUG-3′
miR-145 mimics: 5′-GUCCAGUUUUCCCAGGAAUCCCU-3′
miR-145 inhibitors: 5′-AGGGAUUCCUGGGAAAACUGGAC-3′
miR-152 mimics: 5′-UCAGUGCAUGACAGAACUUGG-3′
miR-152 inhibitors: 5′-CCAAGUUCUGUCAUGCACUGA-3′
miR-182 mimics: 5′-UUUGGCAAUGGUAGAACUCACACU-3′
miR-182 inhibitors: 5′-AGUGUGAGUUCUACCAUUGCCAAA-3′
miR-194 mimics: 5′-UGUAACAGCAACUCCAUGUGGA-3′
miR-194 inhibitors: 5′-UCCACAUGGAGUUGCUGUUACA-3′
Mut miR-320a mimics: 5′-AAUUCG UGGGUUGAGAGGGCGA-3′
Mut miR-140 mimics: 5′-CACACC UUUUACCCUAUGGUAG-3′
Negative control (NC) mimics: 5′-UUCUCCGAACGUGUCACGUTT-3′
Negative control (NC) inhibitors: 5′-CAGUACUUUUGUGUAGUACAA-3′
To screen for selected miRNAs to downregulate the expression of TfR, F81 cells, at a confluence of 60-70% in 24-well plates (Costar), were transfected with mimics or inhibitors (10 nM) using Lipofectamine 2000 transfection reagent (Invitrogen). NC mimics and inhibitors were used as controls. To further determine whether the screened miRNAs could modulate the expression of TfR, F81 cells were transfected with the mimics in a dose-dependent manner. The cells were collected for TfR mRNA qPCR assay at 36 h post-transfection and western blot analysis and flow cytometry assay at 48 h.
To determine whether the selected miRNAs play a direct role in repression of luciferase expression from pGL3-TfR 3′UTR, 24-well plates seeded with F81 cells at 60-70% confluence were co-transfected with a mixture of pGL3-TfR 3′UTR (4 μg/ml) and pRL-TK vector (4 μg/ml) together with mimics (10 nM). The mut320a or mut140 pGL3-TfR 3′UTR and pRL-TK together with mimics (10 nM) were co-transfected to verify accuracy of the seed sequence. NC mimics were used as negative controls. After 36 h, the cells were harvested for relative luciferase activity assay.
To determine the effects of the selected miRNAs on MEV infection, F81 cells, at a confluence of 60-70% in 24-well plates, were transfected with mimics (10 nM). After 48 h, the cells were dispersed with 0.25% trypsin and infected with MEV (MOI = 0.1). Virus infection was measured by qPCR and flow cytometric analysis at the indicated times.
To quantify the relative luciferase activity, a dual-luciferase reporter assay system kit (Promega) was used according to the manufacturer’s protocol. Co-transfected cells with a mixture of luciferase reporter plasmids were washed with cold phosphate-buffered saline (PBS). Passive lysis buffer (Promega: 100 μl) was then added to the cells in each well. After 10 min, the supernatants were clarified by centrifugation at 12,000 g for 30 s, and the luciferase activity was measured using a Modulus single-tube multimode reader (Promega). Relative luciferase expression was calculated as the expression of firefly luciferase (pGL3-control vector) divided by that of Renilla luciferase (pRL-TK).
Real-time quantitative PCR (qPCR) analysis
To detect whether selected miRNAs can downregulate the expression of TfR, qPCR analysis was performed. After transfection of F81 cells with miRNA mimics or inhibitors, NC mimics or inhibitors as controls, total RNA was extracted and digested with DNase I (Takara). Two μg total RNA of each sample was reverse transcribed using M-MLV reverse transcriptase (Promega) according to the manufacturer’s protocol. The β-actin mRNA level was measured as a control. Primers used for amplification were: β-actin, 5′-CGGGACCTGACGGACTACCT-3′ and 5′-GGCCATCTCCTGCTCAAAAT-3′ and TfR, 5′-ATGATTGGCTACTTGGGCTATTG-3′ and 5′-CCTGATGGTGCTGGTGAACTC-3′.
To detect the viral genomic DNA quantitative level in F81 cells, total DNA was extracted and the concentration was measured. PCR amplication of a fragment of viral genomic DNA (5′-GCTTACGCTGCTTATCTTCGC-3′, 5′-TAATGTCCTATTTTCCCCCCC-3′) was performed.
To determine the expression level of miRNAs in F81 cells, total RNA was extracted, and 2 μg was polyadenylated using E. coli poly (A) polymerase according to the manufacturer’s protocol (Promega). The poly (A) reaction product was then reverse transcribed using M-MLV reverse transcriptase (Promega) and an adaptor primer  (5′-GCGAGCACAGAATTAATACGACTCACTATAGGTTTTTTTTTTTTVN-3′) according to the manufacturer’s protocol. PCR amplication was carried out using the specific miRNAs primers (miR-320a, 5′-AAAAGCGGGGAGAGGGCG-3′ and 5′-GCGAGCACAGAATTAATACGACTCAC-3′ and miR-140, 5′-CAGTGGTTTTACCCTATGGTAGAAA-3′ and 5′-GCGAGCACAGAATTAATACGACTCAC-3′). U6 small RNA expression level was measured as a control using primers 5′-CTCGCTTCGGCAGCACA-3′ and 5′-AACGCTTCACGAATTTGCGT-3′. Cycling conditions for qPCR using FastSYBR Mixture (CWBIO) and the ViiA™ 7 real-time PCR System (Applied Biosystems) were 95°C for 20 s, followed by 35 cycles of 95°C for 3 s and 60°C for 30 s. The data were analyzed by the ΔΔCt method .
Western blot assay
F81 cells transfected with mimics in a 24-well plate were washed 3 times with cold PBS, a mixture of 100 μl RIPA lysis buffer (HX-BIO) and 0.5 mM PSMF was added and the cells were harvested into Eppendorf tubes. After 30 min on ice and centrifugation at 12,000 g for 30 min, 25 μl supernatant was mixed with 25 μl each 2 × SDS sample buffer and boiled for 5 min. Samples were subjected to 10% SDS-PAGE gel and transferred to a nitrocellulose membrane (PALL Life Science). The membranes were blocked with 5% nonfat dry milk for 1 h, then incubated for 1 h at room temperature with purified primary mouse antibody CD71 (H68.4) (Santa Cruz: 1:500 dilution) or anti-β-actin antibody (MBL: 1:1,000 dilution) in nonfat milk. After 3 washes with Tris-buffered saline containing 0.05% Tween-20 (TBST), the membranes were incubated for 1 h at ambient temperature with the appropriate horseradish peroxidase-conjugated secondary antibody (MBL: 1:5,000 dilution) in TBST. Protein bands were visualized using ECL western blot substrate (Thermo), with β-actin as a control.
Treated F81 cell monolayers were dispersed with 0.25% trypsin, harvested and fixed in 4% paraformaldehyde. After 3 washes with PBS and incubation for 1 h at 37°C with anti-CD71 mouse antibody (1:2500) or anti-MEV rabbit polyclonal antibody (prepared in this laboratory) at 1:100, the cells were washed 3 times with PBS, incubated with fluorescein isothiocyanate (FITC)-conjugated goat anti-mouse or anti-rabbit IgG antibody (MBL: 1:100 dilution) for 1 h at 37°C, washed another 3 times with PBS and analysed by BD FACSCalibur flow cytometry. Nonspecific rabbit polyclonal antibody (iso) (prepared in this laboratory) was used as an isotype control. The data were analyzed using BD CellQuest software.
Argonaute 2 (Ago2) co-immunoprecipitation
Human anti-Ago2 antibody (Abnova) was first bound to protein A/G-Agarose (Abmart) in PBS for 30 min at 4°C. Treated F81 cells were harvested, washed and solubilized in RIPA lysis buffer (HX-BIO) and PSMF for 30 min on ice, then centrifuged at 12,000 g for 30 min to clarify the supernatant. The latter was then added to the Ago2/Agarose conjugate and incubated for 4 h at 4°C. Incubation of the supernatant with normal mouse IgG (MBL) was used as a negative control. RNA bound to the Ago2 protein was dissociated with Trizol reagent and reverse transcribed. TfR, miR-320a and miR-140 were quantified by qPCR analysis, with β-actin and U6 small RNA as internal controls.
Data were analysed statistically using GraphPad software, as described in the figure legends.
Screening of miRNAs targeting TfR mRNA 3′UTR
MEV infection leads to cellular miR-320a and miR-140 upregulation and TfR downregulation
Expression level of the predicted miRNAs of the two libraries
Rds numain mock infected cells
Rds num in MEV infected cells
TPMbin mock infected cells
TPM in MEV infected cells
MiR-320a and miR-140 target the 3′UTR of TfR and physically bind to TfR mRNA in the RISC
MiR-320a and miR-140 inhibit MEV infection by preventing the virus from entering cells
MiR-320a and miR-140 play roles on TfR and MEV in a synergistic manner
Host cellular miRNAs have frequently been reported to interact with viruses during infection ,,-. We recently showed that miR-181b inhibited MEV replication by repression of its non-structural protein 1 expression . Here, we report that other miRNAs, miR-320a and miR-140, inhibit MEV entry into F81 cells by downregulating its receptor, TfR, through targeting the 3′UTR of TfR mRNA.
A number of reports have shown that TfR, as a cell surface receptor, is required for iron delivery to cells. Indeed, TfR has been established as a gatekeeper for regulating iron uptake by most cells, and the transferring-to-cell endocytic pathway has been characterized in detail . TfR is central to the uptake of iron-loaded transferrin  which is post-transcriptionally regulated via iron-responsive elements present in its 3′UTR . In addition to its role in erythropoiesis, TfR is also overexpressed in the majority of malignancies  and is directly linked to cell proliferation -. Studies have demonstrated that parvovirus replication is dependent on host cellular division and proliferation (; Tattersa ) and vigorous proliferative activity of host cells promotes parvoviral replication. Reduction in cellular metabolic activity, therefore, may explain why downregulation of TfR inhibits MEV replication. There may, however, be another mechanism. TfR is necessary for MEV uptake by host cells: downregulation may therefore render infected cells less susceptible to superinfection with additional MEV particles. While it may take only one virion to establish a primary infection, a multiply-infected cell may produce more infectious progeny. Downregulation of TfR on the cell surface, therefore, may result in diminished production of virus.
Since miR-320a and miR-140 have been shown to inhibit MEV entry into host cells and might also affect virus replication, it may find application as an antiviral therapeutic for MEV-induced mink enteritis. As several reports have shown -, siRNAs can be used to control virus diseases in vivo; however, little attention has so far been paid to the possibility of using endogenous miRNAs as an antivirus tool. Compared with siRNAs, endogenous miRNAs may be safer and induce fewer side-effects. More extensive studies are merited to determine if the two miRNAs described here can be used as antiviral tools.
In conclusion, our work has shown that two miRNAs (miR-320a and miR-140) inhibit MEV entry into the F81 cells by downregulating its specific receptor TfR through targeting the 3′UTR of TfR mRNA in a synergistic manner, while the two miRNAs were upregulated through MEV infection. As summarized in Figure 7, a simple pathway of host-virus interaction network involving TfR and miRNAs has been deduced. These results provide further understanding of the mechanisms in MEV infection and may be helpful for development of endogenous miRNA antiviral therapy strategies.
This work was supported by 863 Project (2011AA10A213) and National Key Scientific Foundation (2009ZX08006-010B).
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