In Vitro Antiviral Activity of Kalanchoe daigremontiana Extract against Human Herpesvirus Type 1
<p>Images of <span class="html-italic">Kalanchoe daigremontiana</span> with a list of some compounds with virucidal potential based on chromatographic analysis. Photos by Dr. Sylwia Nowak; models of compounds - gray indicates carbon atoms, red indicates oxygen and white indicates hydrogen atoms; <a href="https://pubchem.ncbi.nlm.nih.gov/" target="_blank">https://pubchem.ncbi.nlm.nih.gov/</a>, accessed on 10 May 2024. Components with potential antiviral activity were selected on the basis of literature data [<a href="#B5-ijms-25-07507" class="html-bibr">5</a>,<a href="#B6-ijms-25-07507" class="html-bibr">6</a>,<a href="#B7-ijms-25-07507" class="html-bibr">7</a>,<a href="#B8-ijms-25-07507" class="html-bibr">8</a>,<a href="#B9-ijms-25-07507" class="html-bibr">9</a>,<a href="#B10-ijms-25-07507" class="html-bibr">10</a>,<a href="#B11-ijms-25-07507" class="html-bibr">11</a>,<a href="#B12-ijms-25-07507" class="html-bibr">12</a>,<a href="#B13-ijms-25-07507" class="html-bibr">13</a>,<a href="#B14-ijms-25-07507" class="html-bibr">14</a>].</p> "> Figure 2
<p>UHPLC-DAD-MS chromatograms of <span class="html-italic">K. daigremontiana</span> extract.</p> "> Figure 3
<p>Cell viability after exposure to <span class="html-italic">K. daigremontiana</span> extract was evaluated using cell proliferation WST-1 assay: (<b>A</b>) Vero 76 cell line; (<b>B</b>) HaCaT cell line. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test with * <span class="html-italic">p</span> ≤ 0.05, ** <span class="html-italic">p</span> ≤ 0.01, and extremely significant **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 4
<p>The anti-HHV-1 activity of <span class="html-italic">K. diagremontiana</span> extract. Virus titration in Vero 76 cells (<b>A</b>) and HaCat cells (<b>B</b>) (24 h p.i.). Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test with extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 5
<p><span class="html-italic">K. daigremontiana</span> extract blocks HHV-1 entry into the Vero 76 and HaCaT cells. Schematic representation of test procedures (<b>A</b>); inhibition of virus entry in Vero76 (<b>B</b>,<b>C</b>) and HaCaT (<b>D</b>,<b>E</b>) cell cultures with <span class="html-italic">K. daigremontiana</span> extract. At 2 and 4 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as means ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001.</p> "> Figure 6
<p><span class="html-italic">K. diagremontiana</span> extract inhibits HHV-1 attachment in Vero 76 and HaCaT cells. Schematic representation of test procedures (<b>A</b>); inhibition of virus attachment in Vero76 (<b>B</b>) and HaCaT (<b>C</b>) cell cultures with <span class="html-italic">K. daigremontiana</span> extract. At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as means ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05, ** <span class="html-italic">p</span> ≤ 0.01, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 7
<p><span class="html-italic">K. diagremontiana</span> extract inhibits HHV-1 penetration in Vero 76 and HaCaT cells. Schematic representation of test procedures (<b>A</b>); inhibition of virus penetration in Vero (<b>B</b>) and HaCaT (<b>C</b>) cell cultures with <span class="html-italic">K. daigremontiana</span> extract. At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 8
<p>Efficiency of pretreatment with <span class="html-italic">K. daigremontiana</span> extract. Schematic representation of test procedures (<b>A</b>); Vero76 cell line (<b>B</b>) and HaCaT cell line (<b>C</b>). At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05, ** <span class="html-italic">p</span> ≤ 0.01, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 9
<p>Efficiency of pretreatment with <span class="html-italic">K. daigremontiana</span> extract for the release of effective virions. Schematic representation of test procedures (<b>A</b>); At 24 h p.i., cells media from Vero 76 were subjected to HHV-1 copies titration by qPCR (<b>B</b>). Plaque inhibition rate on Vero 76 cell line. The experiment used cell media from culture-treated <span class="html-italic">K. daigremontiana</span> (<b>C</b>). Representative images of the cytopathic effect caused by HHV-1—plaque and diffuse cytopathic effect (microscope magnification 400×) (<b>D</b>). Representative images of crystal violet-stained HSV-1-infected Vero 76 cultures with visible cytopathic effect (PFU) wells, treated <span class="html-italic">K. daigremontiana</span> extracts (microscope magnification 100×) (<b>E</b>). Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001.</p> "> Figure 10
<p>Extract from <span class="html-italic">K. daigremontiana</span> affects expression of immediate early and late HHV-1 genes in Vero 76 cells. Schematic representation of test procedures (<b>A</b>). Relative expression of <span class="html-italic">gB</span> (<b>B</b>). Relative expression of <span class="html-italic">icp0</span> (<b>C</b>). Relative expression of <span class="html-italic">icp27</span> (<b>D</b>). Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001.</p> "> Figure 11
<p>Extract from <span class="html-italic">K. daigremontiana</span> affects expression of immediate early and late HHV-1 genes in HaCat cells. Schematic representation of test procedures (<b>A</b>). Relative expression of <span class="html-italic">gB</span> (<b>B</b>). Relative expression of <span class="html-italic">icp0</span> (<b>C</b>). Relative expression of <span class="html-italic">icp27</span> (<b>D</b>). Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test * <span class="html-italic">p</span> ≤ 0.05 or ** <span class="html-italic">p</span> ≤ 0.01.</p> "> Figure 12
<p>Efficiency of post-treatment with <span class="html-italic">K. daigremontiana</span> extract. Schematic representation of test procedures (<b>A</b>); Vero 76 cell line (<b>B</b>) and HaCaT cell line (<b>C</b>). At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test ** <span class="html-italic">p</span> ≤ 0.01, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 13
<p>Efficiency of combined therapy (pretreatment) with <span class="html-italic">K. daigremontiana</span> extract and ACV. Schematic representation of test procedures (<b>A</b>); Vero 76 cell line (<b>B</b>) and HaCaT cell line (<b>C</b>). At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test ** <span class="html-italic">p</span> ≤ 0.001, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 14
<p>Efficiency of combined therapy (post-entry treatment) with <span class="html-italic">K. daigremontiana</span> extract and ACV. Schematic representation of test procedures (<b>A</b>); Vero 76 cell line (<b>B</b>) and HaCaT cell line (<b>C</b>). At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test ** <span class="html-italic">p</span> ≤ 0.001, and extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 15
<p>Efficiency of combined therapy (preincubation) with <span class="html-italic">K. daigremontiana</span> extract and ACV. Schematic representation of test procedures (<b>A</b>); Vero 76 cell line (<b>B</b>) and HaCaT cell line (<b>C</b>). At 24 h p.i., cells were subjected to HHV-1 copies titration by qPCR. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test ** <span class="html-italic">p</span> ≤ 0.001 and extremely significant at **** <span class="html-italic">p</span> ≤ 0.0001.</p> "> Figure 16
<p>High-content imaging screening assay for HHV-1 antigens after treatment with the <span class="html-italic">K. daigremontiana</span> extract. Schematic representation of test procedures (<b>A</b>); dose-dependent anti-HHV-1 effects of <span class="html-italic">K. daigremontiana</span> extract using HCS spot detector protocols (the software counts the spot corresponding to the viral antigens) (<b>B</b>); representative images from analysis (green—HHV-1—red arrows; blue—DNA) (<b>C</b>), magnification 20×. Data from three independent experiments are presented as mean ± SEM. Tukey’s multiple comparison test at extremely significant at *** <span class="html-italic">p</span> ≤ 0.001 or **** <span class="html-italic">p</span> ≤ 0.0001.</p> ">
Abstract
:1. Introduction
2. Results
2.1. Chemical Characteristics of the Extract from K. daigremontiana
2.2. Effects of Aqueous Extract of K. daigremontiana on Cell Viability
2.3. Antiviral Assays with Extract of K. daigremontiana against HHV-1
2.4. The High-Content Imaging Screening Assay
3. Discussion
4. Materials and Methods
4.1. Plant Materials and Extraction
4.2. UHPLC-DAD-MS Analysis
4.3. Cell Lines and Virus Strains
4.4. Cytotoxicity Assay
4.5. Plaque Assay
4.6. Antiviral Test
4.7. Real-Time PCR (qPCR)
4.8. High-Content Screening Assay (HCS)
4.9. Statistical Evaluation
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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No | Compound Name | Rt [min] | UV-Vis Max [nm] | [M-H]− m/z | MS² Ions (−) | Ref. |
---|---|---|---|---|---|---|
1 | Undefined compound | 3.3 | 268 | 267 | 221b | |
2 | Undefined phenolic acid derivative | 11.2 | 300, 313 | 355 | 209, 191b | - |
3 | Undefined phenolic acid derivative | 11.8 | 300sh, 312 | 355 | 209, 191 | |
4 | Undefined compound | 13.8 | 294 | 451 | 405b | - |
5 | Undefined phenolic acid derivative | 15.6 | 225, 287sh, 312 | 355 | 337, 209, 191 | - |
6 | Undefined compound | 17.9 | 274 | 655 | - | - |
7 | Undefined compound | 20.9 | 230 | 431 | 385b, 205 | - |
8 | Undefined compound | 22.9 | 216, 292 | 449 | 287b, 269, 259 | - |
9 | kaempferol 3-O-β-D-xylopyranosyl-(1→2)-α-L-rhamnopyranoside-7-O-β-D-glucopyranoside | 27.9 | 264, 340 | 725 | 563b, 431, 413, 339, 285, 284, 255 | [15] |
10 | Undefined compound | 28.7 | 260 | 611 | 449, 431b, 251, 189 | - |
11 | Undefined compound | 31.5 | 261 | 449 | 269b, 207 | - |
12 | quercetin 3-O-α-L-arabinopyranosyl-(1→2)-α-L-rhamnopyranoside | 256, 263sh, 343 | 579 | 475,447, 429, 411, 383, 355, 300b, 271, 255, 229 | [16] | |
13 | Daigremontianin isomer | 41.2 | 298 | 531a | 485b, 455 | - |
14 | Bryophyllin a | 42.3 | 299 | 517a | 471b, 387 | [2] |
15 | Kapinnatoside (kaempferol 3-O-α-L-arabinopyranosyl-(1→2)-α-L-rhamnopyranoside) | 42.3 | 264, 341 | 563 | 460, 431, 413, 327, 309, 285, 284b, 255 | [16] |
16 | Bersaldegenin-1-acetate | 46.1 | 299 | 519a | 473, 459, 441, 413b, 395, 369 | [2] |
17 | Bersaldegenin-2-acetate | 47.2 | 298 | 519a | 473, 414, 305, 343b | [2] |
18 | Daigremontianin | 48.4 | 298 | 531a | 485b, 407 | [2] |
19 | Undefined compound | 50.8 | 269 | 971 | 791, 748b, 702, 634, 568, 478, 408 | - |
20 | Undefined compound | 51.5 | 227 | 327 | 292, 229b, 211, 171 | - |
21 | Undefined compound | 55.4 | 228 | 329 | 293, 229b, 211 | - |
22 | Undefined compound | 57.0 | 285 | 483 | 437, 377b, 333, 281, 237, 185 | - |
23 | Bersaldegenin-1,3,5-orthoacetate | 59.7 | 299 | 501a | 339b | [2] |
Cell Line | Antiviral Test | CC50 a | EC50 b | SI c |
---|---|---|---|---|
Vero 76 | attachment | 0.69 | 0.0095 | 72.63 |
penetration | 0.0184 | 37.5 | ||
pretreatment | 0.0062 | 111.29 | ||
post-entry treatment | 0.0028 | 246.42 | ||
HaCat | attachment | 0.48 | 0.0153 | 31.3 |
penetration | 0.0067 | 71.64 | ||
pretreatment | 0.0319 | 15.04 | ||
post-entry treatment | 0.0069 | 69.56 |
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Chodkowski, M.; Nowak, S.; Janicka, M.; Sobczak, M.; Granica, S.; Bańbura, M.W.; Krzyzowska, M.; Cymerys, J. In Vitro Antiviral Activity of Kalanchoe daigremontiana Extract against Human Herpesvirus Type 1. Int. J. Mol. Sci. 2024, 25, 7507. https://doi.org/10.3390/ijms25147507
Chodkowski M, Nowak S, Janicka M, Sobczak M, Granica S, Bańbura MW, Krzyzowska M, Cymerys J. In Vitro Antiviral Activity of Kalanchoe daigremontiana Extract against Human Herpesvirus Type 1. International Journal of Molecular Sciences. 2024; 25(14):7507. https://doi.org/10.3390/ijms25147507
Chicago/Turabian StyleChodkowski, Marcin, Sylwia Nowak, Martyna Janicka, Marcin Sobczak, Sebastian Granica, Marcin W. Bańbura, Malgorzata Krzyzowska, and Joanna Cymerys. 2024. "In Vitro Antiviral Activity of Kalanchoe daigremontiana Extract against Human Herpesvirus Type 1" International Journal of Molecular Sciences 25, no. 14: 7507. https://doi.org/10.3390/ijms25147507