Canine Respiratory Coronavirus, Bovine Coronavirus, and Human Coronavirus OC43: Receptors and Attachment Factors
<p>Phylogenetic tree of <span class="html-italic">Orthocoronavirinae</span>. The evolutionary history was inferred based on the sequences of the complete spike gene by using the Maximum Likelihood method based on General Time Reversible model [<a href="#B7-viruses-11-00328" class="html-bibr">7</a>]. The tree with the highest log likelihood-33860.47) is shown. The percentage of trees in which the associated taxa clustered together is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using the Maximum Composite Likelihood (MCL) approach, and then selecting the topology with superior log likelihood value. Discrete Gamma distribution was used to model evolutionary rate differences among sites (5 categories (+G, parameter = 3.0783)). The rate variation model allowed for some sites to be evolutionarily invariable ([+I], 5.04% sites). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 11 nucleotide sequences. All positions containing gaps and missing data were eliminated. There was a total of 3117 positions in the final dataset. Evolutionary analyses were conducted in MEGA7 [<a href="#B8-viruses-11-00328" class="html-bibr">8</a>]. <span class="html-italic">Alphacoronavirus</span>: Human coronavirus 229E (HCoV-229E; NC_002645); <span class="html-italic">Deltacoronavirus</span>: Wigeon coronavirus HKU20 (NC_016995); <span class="html-italic">Gammacoronavirus</span>: Beluga Whale coronavirus SW1 (NC_010646); BCoV: Bovine coronavirus (NC_003045); CRCoV: Canine respiratory coronavirus (JX860640); HCoV-OC43: Human coronavirus OC43 (NC_006213); HCoV-HKU1: Human coronavirus HKU1 (NC_006577); <span class="html-italic">Hibecovirus</span>: Bat Hp-betacoronavirus/Zhejiang2013 (NC_025217); <span class="html-italic">Merbecovirus</span>: Middle East respiratory syndrome coronavirus (NC_019843); <span class="html-italic">Nobecovirus</span>: Bat coronavirus HKU9 (NC_009021); <span class="html-italic">Sarbecovirus</span>: SARS coronavirus (NC_004718).</p> "> Figure 2
<p>HCoV-OC43 VR-1558, BCoV and CRCoV agglutinate erythrocytes. Representative picture of hemagglutination assay results is shown. Mouse erythrocyte suspension was mixed with viral stocks and incubated at room temperature for 1 h. Influenza A H3N2 reported to hemagglutinate erythrocytes [<a href="#B36-viruses-11-00328" class="html-bibr">36</a>] and HCoV-NL63 which does not bind to sialic acids (SAs) [<a href="#B33-viruses-11-00328" class="html-bibr">33</a>] were used as control samples.</p> "> Figure 3
<p>Removal of SAs from the surface of the cell limits attachment of HCoV-OC43 VR-1558, BCoV, and CRCoV to different extent. Cells pretreated with type II neuraminidase (NA, 200 mU/mL) were overlaid with HCoV-OC43, BCoV, and CRCoV stocks, incubated for 2 h at 4 °C, fixed, and immunostained. Viral capsids are presented in green, while blue denotes DNA. Scale bar 10 µm. Data were collected from a minimum of 12 fields of view, from at least three different samples. (<b>A</b>) virus inoculated, control cells; (<b>B</b>) virus inoculated, NA treated cells; (<b>C</b>) mock inoculated, non-treated cells; (<b>D</b>) FACS analysis of viral attachment in the presence of NA. Graph shows mean fluorescence normalized to control. The data is presented as mean ± SD from at least three experiments in triplicate. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 4
<p>SAs removal does not affect HCoV-OC43 VR-1558, BCoV, or CRCoV replication. Cells pretreated with type II neuraminidase (NA, 200 mU/mL) were overlaid with HCoV-OC43 VR-1558, BCoV and CRCoV stocks (at TCID<sub>50</sub> of 400 per milliliter, which approximately corresponds to M.O.I. = 0.0007) and incubated for 2 h at optimal temperature (see <span class="html-italic">Viral stocks</span>). Subsequently unbound virions were washed off and the cells were further incubated at optimal temperature for five days. (<b>A</b>) virus yield assessed by RT-qPCR. (<b>B</b>) NA effect on cell viability, as determined by an XTT assay. (<b>C</b>) The proportion of infected cells in the whole population normalized to control (flow cytometry). All data is presented as mean ± SD from at least three experiments in triplicate. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 5
<p>Soluble SAs limits attachment of HCoV-OC43 VR-1558, BCoV, and CRCoV but does not affect their replication. (<b>A</b>) Cells were overlaid with HCoV-OC43 VR-1558, BCoV, and CRCoV stocks preincubated with <span class="html-italic">N</span>-acetylneuraminic acid (Neu5Ac), incubated for 2 h at 4 °C, fixed, and immunostained. Graph shows results of flow cytometry analysis of viral attachment; data are presented as mean fluorescence normalized to control. (<b>B</b>) Cells overlaid with viral stocks (at TCID<sub>50</sub> of 400 per milliliter, which approximately corresponds to M.O.I. = 0.0007) exposed to Neu5Ac were incubated for 2 h at temperature optimal for particular virus. Subsequently, unbound virions were washed off and cells were incubated for 5 days in the presence of Neu5Ac. The data is presented as mean ± SD of virus yield in cell culture supernatant (RT-qPCR) from at least three experiments in triplicate. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 6
<p>Activity of neuraminidase and sialyltransferases. (<b>A</b>) HRT-18G cells were treated with type II neuraminidase (NA, 500 mU/mL) and overlaid with α-2,3-sialyltransferase (α2,3-ST) or α-2,6-sialyltransferase (α2,6-ST) in the presence of 1 mM cytidine-5′-monophospho-<span class="html-italic">N</span>-acetylneuraminic acid for 2 h at 37 °C. Following treatment, cells were fixed, and SAs were visualized with <span class="html-italic">sambucus nigra</span> lectin (α-2,3-SAs specific) labelled with fluorescein (in green) or <span class="html-italic">maackia amurensis</span> lectin (α-2,6-SAs specific) labelled with Cy3 (in red). Scale bar 10 µm. Data were collected from a minimum of 12 fields of view, from at least three different samples. (<b>B</b>) Graphs present corrected total cell fluorescence calculated by subtracting the product of multiplying the cell surface and the mean background fluorescence from total cell fluorescence. The data is presented as mean ± SD from at least one hundred cells per condition. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 7
<p>Resialylation restores CRCoV attachment to SAs-depleted cells. Cells treated with type II neuraminidase (NA, 500 mU/mL) and overlaid with α-2,3-sialyltransferase (α2,3-ST) or α-2,6-sialyltransferase (α2,6-ST) in the presence of 1 mM cytidine-5′-monophospho-<span class="html-italic">N</span>-acetylneuraminic acid for 2 h at 37 °C. Next, cells were overlaid with iodixanol-concentrated CRCoV, incubated for 2 h at 4 °C, fixed and immunostained. (<b>A</b>) Confocal analysis of CRCoV attachment in presence of NA and STs. Virions are presented in green, while blue denotes DNA. Scale bar 10 µm. Data were collected from a minimum of 12 fields of view, from at least two different samples. (<b>B</b>) FACS analysis of viral attachment in presence of NA and STs. Graph shows median fluorescence normalized to control. All data is presented as mean ± SD from at least three experiments in triplicates. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 8
<p>Resialylation restores HCoV-OC43 VR-1558 attachment to SAs-depleted cells. Cells treated with type II neuraminidase (NA, 500 mU/mL) and overlaid with α-2,3-sialyltransferase (α2,3-ST) or α-2,6-sialyltransferase (α2,6-ST) in the presence of 1 mM cytidine-5′-monophospho-<span class="html-italic">N</span>-acetylneuraminic acid for 2 h at 37 °C. Next, cells were overlaid with iodixanol-concentrated HCoV-OC43 VR-1558, incubated for 2 h at 4 °C, fixed, and immunostained. (<b>A</b>) Confocal analysis of HCoV-OC43 attachment in presence of NA and STs. Virions are presented in green, while blue denotes DNA. Scale bar 10 µm. Data were collected from a minimum of 12 fields of view, from at least two different samples. (<b>B</b>) FACS analysis of viral attachment in presence of NA and STs. Graph shows median fluorescence normalized to control. All data is presented as mean ± SD from at least three experiments in triplicates. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 9
<p>Resialylation restores BCoV attachment to SAs-depleted cells. Cells treated with type II neuraminidase (NA, 500 mU/mL) and overlaid with α-2,3-sialyltransferase (α2,3-ST) or α-2,6-sialyltransferase (α2,6-ST) in the presence of 1 mM cytidine-5′-monophospho-<span class="html-italic">N</span>-acetylneuraminic acid for 2 h at 37°C. Next, cells were overlaid with iodixanol-concentrated BCoV, incubated for 2 h at 4 °C, fixed and immunostained. (<b>A</b>) Confocal analysis of BCoV attachment in presence of NA and STs. Virions are presented in green, while blue denotes DNA. Scale bar 10 µm. Data were collected from a minimum of 12 fields of view, from at least two different samples. (<b>B</b>) FACS analysis of viral attachment in presence of NA and STs. Graph shows median fluorescence normalized to control. All data is presented as mean ± SD from at least three experiments in triplicates. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 10
<p>Human leukocyte antigen (HLA) class I as entry receptor for betacoronaviruses. Cells infected with HCoV-OC43 VR-1558, BCoV and CRCoV (at TCID<sub>50</sub> of 400 per milliliter, which approximately corresponds to M.O.I. = 0.0007) in the presence of HLA class I antibodies were incubated for five days at optimal temperature. (<b>A</b>) The proportion of virus infected cells determined with flow cytometry normalized to control. (<b>B</b>) Cytotoxicity of antibodies determined with XTT assay. All data is presented as mean ± SD. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 11
<p>Heparan sulfate (HS) as attachment receptor for HCoV-OC43 VR-1558, BCoV, and CRCoV. (<b>A</b>) FACS analysis of viral attachment in the presence of HS. Cells were overlaid with HCoV-OC43 VR-1558, BCoV, and CRCoV stocks in the presence of HS, incubated for 2 h at 4 °C, fixed, and immunostained. Graph shows mean fluorescence normalized to control. (<b>B</b>) Analysis of viral entry in the presence of HS. Cells were overlaid with HCoV-OC43, BCoV, and CRCoV stocks (at TCID<sub>50</sub> of 400 per milliliter, which approximately corresponds to M.O.I. = 0.0007) in the presence of HS and incubated for 2 h at optimal temperature. Subsequently unbound virions were washed off and the cells were further incubated at optimal temperature in the presence of HS. Virus yield was assessed by RT-qPCR at 5th day p.i. All data is presented as mean ± SD from at least three experiments in triplicate. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> "> Figure 12
<p>Attachment and replication of HCoV-OC43 0500 in human airway epithelium (HAE) cultures. (<b>A</b>) SAs serve as entry receptors for HCoV-OC43 0500. Influence of NA (200 mU/mL), HS (200 µg/mL), Neu5Ac (20–80 mM), and HLA class I specific antibodies (0.5 µg/mL) on HCoV-OC43 0500 infection. Viral yield was assessed by RT-qPCR 5 days p.i. The data is presented as mean ± SD from at least two experiments in duplicates. (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001). (<b>B</b>) SAs serve as attachment receptors for HCoV-OC43 0500. Confocal analysis of NA (200 mU/mL), Neu5Ac (40–80 mM) and HS (200 µg/mL) effect on HCoV-OC43 0500 attachment. Viral capsids are presented in green, blue denotes DNA and red represents actin. Scale bar 10 µm. (<b>C</b>) Quantification of virus attachment. A number of viral particles that attached to the surface of fully differentiated HAE culture was graphed. Data were collected from a minimum of 12 fields of view, from at least two different samples. Number of particles and number of cells were quantified using ImageJ Fiji built in tool “3D Objects Counter”. Results are presented as min-max graph with line corresponding to the mean value (* <span class="html-italic">p</span> < 0.05; ** <span class="html-italic">p</span> < 0.01; *** <span class="html-italic">p</span> < 0.001; **** <span class="html-italic">p</span> < 0.0001).</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cells
2.2. Viral Stocks
2.3. Purification of CRCoV
2.4. Antibodies to CRCoV N Protein
2.5. Western Blot Analysis
2.6. Hemagglutination Assay
2.7. Virus Attachment
2.8. Confocal Microscopy
2.9. Flow Cytometry
2.10. Virus Replication
2.11. Reverse Transcription Quantitative PCR (RT-qPCR)
2.12. Resialylation
2.13. Data Analysis
2.14. Ethics Statement
3. Results
3.1. HCoV-OC43, BCoV, and CRCoV Use SAs to Attach to Target Cells
3.2. SAs Did Not Facilitate Entry of CRCoV, BCoV, and HCoV-OC43 VR-1558 to HRT-18G Cells
3.3. Restoration of SAs on the Cell Surface Rescues Attachment of CRCoV, BCoV, and HCoV-OC43 VR-1558
3.4. Interaction with HLA-I Molecules
3.5. Involvement of HS and Lectins
3.6. Attachment Receptors and Adaptation during Cell Culture
4. Discussion
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Virus | Probe Sequence | Fluorescent Dyes | Forward Primer Sequence (5’→3’) | Reverse Primer Sequence (5’ → 3’) | Amplification Program | PCR Product Sequence |
---|---|---|---|---|---|---|
HCoV-OC43 | TGACATTGTCGATCGGGACCCAAGTA | FAM (6- carboxyfluorescein) and TAMRA (6- carboxytetramethyl-rhodamine) | AGCAACCAGGCTGATGTCAATACC | AGCAGACCTTCCTGAGCCTTCAAT | 50 °C for 2 min, 92 °C for 10 min, 40 cycles of 92 °C for 15 s and 60 °C for 1 min | AGCAACCAGGCTGATGTCAATACCCCGGCTGACATTGTCGATCGGGACCCAAGTAGCGATGAGGCTATTCCGACTAGGTTTCCGCCTGGCACGGTACTCCCTCAGGGTTACTATATTGAAGGCTCAGGAAGGTCTGCT |
CRCoV and BCoV | AGATCTACTTCACGCGCATCCAGT | FAM and TAMRA | CAGGAAGGTCTGCTCCTAATTC | GTTGCCAGAATTGGCTCTACTA | 95 °C for 5 min, 30 cycles of 95 °C for 15 s and 60 °C for 30 s | CAGGAAGGTCTGCTCCTAATTCCAGATCTACTTCACGCGCATCCAGTAGAGCCTCTAGTGCAGGATCGCGTAGTAGAGCCAATTCTGGCAAC |
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Szczepanski, A.; Owczarek, K.; Bzowska, M.; Gula, K.; Drebot, I.; Ochman, M.; Maksym, B.; Rajfur, Z.; Mitchell, J.A.; Pyrc, K. Canine Respiratory Coronavirus, Bovine Coronavirus, and Human Coronavirus OC43: Receptors and Attachment Factors. Viruses 2019, 11, 328. https://doi.org/10.3390/v11040328
Szczepanski A, Owczarek K, Bzowska M, Gula K, Drebot I, Ochman M, Maksym B, Rajfur Z, Mitchell JA, Pyrc K. Canine Respiratory Coronavirus, Bovine Coronavirus, and Human Coronavirus OC43: Receptors and Attachment Factors. Viruses. 2019; 11(4):328. https://doi.org/10.3390/v11040328
Chicago/Turabian StyleSzczepanski, Artur, Katarzyna Owczarek, Monika Bzowska, Katarzyna Gula, Inga Drebot, Marek Ochman, Beata Maksym, Zenon Rajfur, Judy A Mitchell, and Krzysztof Pyrc. 2019. "Canine Respiratory Coronavirus, Bovine Coronavirus, and Human Coronavirus OC43: Receptors and Attachment Factors" Viruses 11, no. 4: 328. https://doi.org/10.3390/v11040328