Short ‘1.2× Genome’ Infectious Clone Initiates Kolmiovirid Replication in Boa constrictor Cells
<p>Schematic representation of the “1.2× genome” kolmiovirid inserts in forward (FWD)/genomic orientation. We cloned the 1.2× genome of the displayed kolmiovirid: Swiss snake colony virus 1 (SwSCV-1, GenBank accession: NC_040729.1, 1.15× genome), human hepatitis D virus genotype 1 (HDV-1, M21012.1, 1.16× genome), Tome’s spiny rat virus 1 (TSRV-1, MK598005.2, 1.13× genome), Dabbling duck virus 1 (DabDV-1, NC_040845.1, 1.17× genome), and Chusan Island toad virus 1 (CITV-1, MK962760.1, 1.22× genome) into pCAGGS/MCS plasmid, both in genomic (FWD—shown in this figure) and in antigenomic (REV) orientation. Each of the inserts, approximately 1.2× of the genome size, contains a single copy of the genomes flanked from each end by both the genomic and antigenomic ribozymes. The images were created using SnapGene Viewer (<a href="https://www.snapgene.com/snapgene-viewer/" target="_blank">https://www.snapgene.com/snapgene-viewer/</a>; accessed on 14 October 2019).</p> "> Figure 2
<p>SwSCV-1 DAg antiserum cross-reactivity with the DAg of different kolmiovirids. (<b>A</b>) I/1Ki cells transfected with 1.2× SwSCV-1, HDV-1, TSRV-1, DabDV-1, and CITV-1 REV constructs were stained for the DAg at 4 days post transfection using rabbit α-SwSCV-1 DAg antiserum (1:100 dilution). (<b>B</b>) I/1Ki cells transfected with 1.2× SwSCV-1, HDV-1, TSRV-1, DabDV-1, and CITV-1 FWD constructs and clean cell control were stained for the DAg 4 days post transfection using rabbit α-SwSCV-1 DAg antiserum (1:100 dilution). Hoechst 33342 served for detection of the nuclei (<b>left panels</b>), and AlexaFluor 488-labeled donkey anti-rabbit IgG as the secondary antibody for DAg detection (<b>middle panels</b>). The (<b>right panels</b>) show overlay of the nuclear and DAg staining. The images were captured using Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) with 20× objective. (<b>C</b>) I/1Ki cells transfected with 1.2× SwSCV-1, HDV-1, TSRV-1, DabDV-1, and CITV-1 REV constructs (<b>left panel</b>) and FWD constructs (<b>right panel</b>) were submitted for western blot at 4 days post transfection. The samples were separated on 4–20% Mini-PROTEAN TGX gels (Bio-Rad, Hercules, CA, USA), transferred onto nitrocellulose, and the membranes were probed with rabbit α-SwSCV-1 DAg antiserum and affinity purified α-HDAg antibody. We loaded 1/3 volume of the 1.2× SwSCV-1 REV and FWD samples. The bands corresponding to the different DAgs are marked with the black rectangle. The results were recorded using Odyssey Infrared Imaging System (LI-COR Biosciences, Lincoln, NE, USA).</p> "> Figure 3
<p>Expression of DAg in I/1Ki cells following transfection with 2× and 1.2× genome SwSCV-1 FWD and REV plasmids. I/1Ki cells transfected with 2× and 1.2× SwSCV-1 FWD and REV plasmids were fixed and stained for the DAg using rabbit α-SwSCV-1 DAg antiserum at 1–4 days post transfection. AlexaFluor 488-labeled donkey anti-rabbit IgG served as the secondary antibody for DAg detection. The images were captured using Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) with 20× objective.</p> "> Figure 4
<p>Western blot of I/1Ki cells after transfection with 2× and 1.2× SwSCV-1 (2×Δ and 1.2×Δ, respectively) FWD and REV constructs. (<b>A</b>) Samples of I/1Ki cells transfected with 2×Δ-FWD, 2×Δ-REV, 1.2×Δ-FWD, and 1.2×Δ-REV constructs collected at 1–4 days post transfection were separated on 4–20% Mini-PROTEAN TGX gels (Bio-Rad, Hercules, CA, USA), transferred onto nitrocellulose, and the membranes were probed with rabbit α-SwSCV-1 DAg antiserum and mouse monoclonal anti-pan actin antibody. The left panel shows 2× and the right panel 1.2× genome constructs. The results were recorded using Odyssey Infrared Imaging System (LI-COR Biosciences, Lincoln, NE, USA). (<b>B</b>) Samples of I/1Ki cells transfected with 2×Δ-FWD, 2×Δ-REV, 1.2×Δ-FWD, and 1.2×Δ-REV constructs collected at 5 days, analyzed as described in (<b>A</b>). (<b>C</b>) RNA isolated from I/1Ki cells transfected with 2×Δ-FWD, 2×Δ-REV, 1.2×Δ-FWD, and 1.2×Δ-REV constructs at 3 and 6 days post transfection were analyzed by qRT-PCR targeting genomic SwSCV-1 RNA. In vitro transcribed RNA target served for obtaining a standard curve to convert cycle threshold values into copy numbers. qRT-PCR targeting GAPDH mRNA served for normalizing the results between samples. The y-axis shows copy numbers/reaction. The error bars represent standard deviation.</p> "> Figure 5
<p>Superinfection of 2× and 1.2× SwSCV-1 FWD transfected I/1Ki cells leads to infectious particle production. (<b>A</b>) Supernatants collected at 3, 6, and 9 days post HISV-1 superinfection from I/1Ki cells—transfected with 2× and 1.2× SwSCV-1 FWD constructs two weeks earlier—were used to inoculate clean I/1Ki cells. At four days post inoculation, the cells were fixed and stained using rabbit α-SwSCV-1 DAg antiserum and Alexa Fluor 488-labeled donkey anti-rabbit secondary antibody. Hoechst 33342 served for staining the nuclei. The top panels show clean I/1Ki cells infected with 100-fold diluted supernatant originating from HISV-1 superinfected 2× SwSCV-1 FWD transfected cells, and the bottom panels with supernatant originating from HISV-1 superinfected 1.2× SwSCV-1 FWD transfected cells. Undiluted supernatant from non-superinfected cells served as a control. The images were captured using Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) with 20× objective. (<b>B</b>) Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) served to count the number of infected cells in (<b>A</b>), which enabled the quantification of infectious particles per milliliter of growth medium in terms of fluorescent focus-forming units (FFFUs—displayed on y-axis). The error bars represent standard deviation.</p> "> Figure 6
<p>Comparison of persistently SwSCV-1-infected I/1Ki cells generated following transfection with 2× and 1.2× SwSCV-1 FWD constructs by immunofluorescence, and western and northern blot. The 2× SwSCV-1 (I/1Ki-2×Δ) cell line was analyzed at approximately 2.5 years and the 1.2× SwSCV-1 (I/1Ki-1.2×Δ) at approximately 8 months after initial transfection, during which the cell lines were passaged at 1–2 week interval. (<b>A</b>) Rabbit α-SwSCV-1 DAg antiserum and Alexa Fluor 488-labeled donkey anti-rabbit secondary antibody served for IF staining of the fixed cells, and Hoechst 33342 for staining the nuclei. The top panels show staining of I/1Ki-2×Δ cells, and the bottom panels the staining of I/1Ki-1.2×Δ cells. The left panels show staining of nuclei in blue, the middle panels show DAg staining in green, and the right panels show an overlay. The images were captured using Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) with 20× objective. (<b>B</b>) Samples of naïve I/1Ki cells, I/1Ki-2×Δ cells, I/1Ki-1.2×Δ cells, and the brain homogenates of SwSCV-1-infected boa constrictors (F18-4 and F-18-5, of [<a href="#B15-viruses-14-00107" class="html-bibr">15</a>]) were separated on 4–20% Mini-PROTEAN TGX gels (Bio-Rad, Hercules, CA, USA), transferred onto nitrocellulose, and the membranes probed with rabbit α-SwSCV-1 DAg antiserum and mouse monoclonal anti-pan actin antibody. The results were recorded using Odyssey Infrared Imaging System (LI-COR Biosciences, Lincoln, NE, USA). (<b>C</b>) Indicated amounts of total RNA isolated from I/1Ki-2×Δ, I/1Ki-1.2×Δ, and clean I/1Ki cells and an in vitro-transcribed control RNA (~850 nucleotides long) were prepared using two different loading dyes (2X RNA loading dye [NEB] or “in-house” loading dye prepared according to Mansour and Pestov [<a href="#B43-viruses-14-00107" class="html-bibr">43</a>]), separated on agarose gel and transferred onto nylon membrane. Probes were targeting SwSCV-1 genomic RNA and SwSCV-1 DAg mRNA (left and middle panels) and antigenomic RNA and SwSCV-1 DAg mRNA (right panel); the bands of the marker served for visualizing the RNA targets. The results were recorded using Odyssey Infrared Imaging System (LI-COR Biosciences, Lincoln, NE, USA).</p> "> Figure 7
<p>Demonstration of circular SwSCV-1 genome in persistently infected cells using two-step RT-PCR. (<b>A</b>) We transcribed cDNA with primers targeting the genomic RNA upstream of either both genomic and antigenomic ribozyme (RT primer 1) or just the antigenomic ribozyme (RT primer 2) to include the putative cleavage sites of the genomic RNA. The subsequent PCR employed three different primer pairs (PP1–PP3) targeting the DAg ORF to amplify the nearly complete SwSCV-1 genome. The figure shows the location of primers in the SwSCV-1 genome map. (<b>B</b>) The PCR products with PP1 to PP3 from templates produced from the RNAs extracted from I/1Ki-2×Δ and I/1Ki-1.2×Δ in the presence (left half of both gels) or absence (right side of both gels) of RT enzyme. The top panel shows PCR products with RT primer 1 and the bottom with RT primer 2 separated on 1.2% agarose gel with GelRed for visualization of the bands, the expected size of the amplicons is roughly 1650 nt.</p> "> Figure 8
<p>SwSCV-1 infection on naïve I/1Ki cells. Supernatants from I/1Ki cells transfected six months ago with 1.2× or 2× SwSCV-1 FWD were collected three days post superinfection with HISV-1 and subsequently used to inoculate naïve I/1Ki cells at 1:5 and 1:100 dilutions. (<b>A</b>) Rabbit α-SwSCV-1 DAg antiserum and Alexa Fluor 488-labeled donkey anti-rabbit secondary antibody served for IF staining of the fixed cells, and Hoechst 33,342 for staining the nuclei. The left panels show an overlay of DAg (green) and nuclear (blue) staining of I/1Ki-2×Δ cells and the right panels the staining of I/1Ki-1.2×Δ cells fixed at 3, 6, or 9 dpi. The images were captured using Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) with 20× objective. (<b>B</b>) Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) served for enumerating the number of infected cells at each time point. The dark bars represent cells inoculated with 1:5 dilution of HISV-1 superinfected 2× SwSCV-1 and the light bars cells inoculated with 1:5 dilution of HISV-1 superinfected 1.2× SwSCV-1 cell culture supernatant. (<b>C</b>) RT-PCR served to quantify the amount of SwSCV-1 RNA in the cells at each time point. The number of SwSCV-1 RNA copies in the reaction (corresponding to 1/20 of RNA extracted from cells of a single 24-well plate well) normalized against housekeeping gene (GAPDH). (<b>D</b>) Samples of cells inoculated with 1:5 or 1:100 diluted supernatant collected from HISV-1 superinfected 2× SwSCV-1 FWD or 1.2× SwSCV-1 FWD transfected cells were separated on 4–20% Mini-PROTEAN TGX gels (Bio-Rad, Hercules, CA, USA), transferred onto nitrocellulose, and the membranes probed with rabbit α-SwSCV-1 DAg antiserum, rabbit α-HISV NP antiserum, and mouse monoclonal anti-pan actin antibody. The top panels show the results recorded using Odyssey Infrared Imaging System (LI-COR Biosciences, Lincoln, NE, USA), and the bottom panels show results for the quantification (using Image Studio Lite Ver 2) of the HISV NP and DAg bands normalized against the actin signal.</p> "> Figure 8 Cont.
<p>SwSCV-1 infection on naïve I/1Ki cells. Supernatants from I/1Ki cells transfected six months ago with 1.2× or 2× SwSCV-1 FWD were collected three days post superinfection with HISV-1 and subsequently used to inoculate naïve I/1Ki cells at 1:5 and 1:100 dilutions. (<b>A</b>) Rabbit α-SwSCV-1 DAg antiserum and Alexa Fluor 488-labeled donkey anti-rabbit secondary antibody served for IF staining of the fixed cells, and Hoechst 33,342 for staining the nuclei. The left panels show an overlay of DAg (green) and nuclear (blue) staining of I/1Ki-2×Δ cells and the right panels the staining of I/1Ki-1.2×Δ cells fixed at 3, 6, or 9 dpi. The images were captured using Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) with 20× objective. (<b>B</b>) Opera Phenix High Content Screening System (PerkinElmer, Waltham, MA, USA) served for enumerating the number of infected cells at each time point. The dark bars represent cells inoculated with 1:5 dilution of HISV-1 superinfected 2× SwSCV-1 and the light bars cells inoculated with 1:5 dilution of HISV-1 superinfected 1.2× SwSCV-1 cell culture supernatant. (<b>C</b>) RT-PCR served to quantify the amount of SwSCV-1 RNA in the cells at each time point. The number of SwSCV-1 RNA copies in the reaction (corresponding to 1/20 of RNA extracted from cells of a single 24-well plate well) normalized against housekeeping gene (GAPDH). (<b>D</b>) Samples of cells inoculated with 1:5 or 1:100 diluted supernatant collected from HISV-1 superinfected 2× SwSCV-1 FWD or 1.2× SwSCV-1 FWD transfected cells were separated on 4–20% Mini-PROTEAN TGX gels (Bio-Rad, Hercules, CA, USA), transferred onto nitrocellulose, and the membranes probed with rabbit α-SwSCV-1 DAg antiserum, rabbit α-HISV NP antiserum, and mouse monoclonal anti-pan actin antibody. The top panels show the results recorded using Odyssey Infrared Imaging System (LI-COR Biosciences, Lincoln, NE, USA), and the bottom panels show results for the quantification (using Image Studio Lite Ver 2) of the HISV NP and DAg bands normalized against the actin signal.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Culture and Superinfection
2.2. Plasmids and Cloning
2.3. Transfection
2.4. Western Blot (WB)
2.5. Immunofluorescence Staining
2.6. Detection of Circular RNA Genome
2.7. Quantitative Reverse Transcription PCR (qRT-PCR)
2.8. Near-Infrared Fluorescent Northern Blot
2.9. SwSCV-1 Infection Dynamics in Naïve I/1Ki Cells
3. Results
3.1. Transfection with 1.2× Genome Construct Initiates Replication of Kolmiovirids
3.2. The 1.2× and 2× SwSCV-1 Genome Infectious Clones Induce Similar Infection as Judged by Antigen Expression and Replication
3.3. Superinfection of Cells Transfected with 1.2× SwSCV-1 FWD Construct Induces Infectious Particle Formation
3.4. Transfection of Cells with the 1.2× SwSCV-1 Construct Results in Persistent Infection
3.5. Inoculation of Naïve I/1Ki Cells with SwSCV-1 Results in Productive
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Szirovicza, L.; Hetzel, U.; Kipar, A.; Hepojoki, J. Short ‘1.2× Genome’ Infectious Clone Initiates Kolmiovirid Replication in Boa constrictor Cells. Viruses 2022, 14, 107. https://doi.org/10.3390/v14010107
Szirovicza L, Hetzel U, Kipar A, Hepojoki J. Short ‘1.2× Genome’ Infectious Clone Initiates Kolmiovirid Replication in Boa constrictor Cells. Viruses. 2022; 14(1):107. https://doi.org/10.3390/v14010107
Chicago/Turabian StyleSzirovicza, Leonora, Udo Hetzel, Anja Kipar, and Jussi Hepojoki. 2022. "Short ‘1.2× Genome’ Infectious Clone Initiates Kolmiovirid Replication in Boa constrictor Cells" Viruses 14, no. 1: 107. https://doi.org/10.3390/v14010107