Natural Bioactive Compounds from Fungi as Potential Candidates for Protease Inhibitors and Immunomodulators to Apply for Coronaviruses
Abstract
:1. Introduction
2. Protease Inhibitor Drugs for CoVs
3. Potential of Fungal Antiviral Bioactive Compounds as Protease Inhibitors to Treat CoVs
3.1. HIV-1 Protease Inhibitors Isolated from Fungi
3.2. HCV NS3/4A Protease Inhibitors Isolated from Fungi
4. Potential of Fungal Bioactive Compounds for Immunomodulators
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Source | Bioactive Agent | Efficacy* | Reference |
---|---|---|---|
Endophytic fungi in genera Alternaria, Aspergillus, Beauveria, Cladosporium, Chaetomella, Fusarium, Guignadia, Monochaetia, Nodulisporium, Pestlotia, Pestalotiopsis, Pithomyces, Penicillium, Phomopsis, Phyllostica, Sporormia, Taxomyces, Trichoderma, Trichothecium, Tubercularia and Xylaria | Paclitaxel | 20 μg/mL, viral inhibition was similar to positive control pepstatin A (80 μg/mL). CC50 > 50 μg/mL in human embryonic kidney 293 (HEK-293) cells | [61,62,63,64,65,66,67,68,69,70,71,74] |
Chrysosporium merdarium | Semicochliodinol A | IC50 = 0.37 μM CC50 = 0.84 μM in human lung fibroblast cells | [75,76] |
Semicochliodinol B | IC50 > 0.5 μM | [77] | |
Didemethylasterriquinone D | IC50 = 0.24 μM | [77] | |
Ganoderma lucidum | Ganolucidic acid A | IC50 = 70 μM | [78] |
Ganoderic acid A | IC50 = 430 μM CC50 > 62.5 μM on normal human fibroblast BJ cells | [78,79] | |
Ganoderic acid B | IC50 = 140 μM | [80] | |
Ganoderic acid C1 | IC50 = 240 μM | [80] | |
Ganoderic acid β | IC50 = 20 μM | [80] | |
Ganodermanondiol | IC50 = 90 μM | [80] | |
Ganodermanontriol | IC50 = 70 μM | [80] | |
Lucidumol B | IC50 = 50 μM | [80] | |
3β-5α-dihydroxy-6β-methoxyergosta-7,22-diene | IC50 = 7.8 µg/mL | [80] | |
Ganomycin B | IC50 = 7.5 µg/mL | [81,82] | |
Ganoderma colosum | Ganomycin I | IC50 = 1 µg/mL | [81,82] |
Colossolactone A | IC50 = 39 µg/mL | [81] | |
Colossolactone E | IC50 = 8 µg/mL | [81] | |
Colossolactone G | IC50 = 5 µg/mL | [81] | |
Colossolactone V | IC50 = 9 µg/mL | [81] | |
Colossolactone VII | IC50 = 13.8 µg/mL | [81] | |
Colossolactone VIII | IC50 = 31.4 µg/mL | [81] | |
Ganoderma sinnense | Ganoderic acid GS-1 | IC50 = 58 μM | [83] |
Ganoderic acid GS-2 | IC50 = 30 μM | [83] | |
Ganoderic acid DM | IC50 = 38 μM | [83] | |
Ganoderic acid β | IC50 = 116 μM | [83] | |
Ganoderiol A | IC50 = 80 μM | [83] | |
Ganoderiol F | IC50 = 22 μM | [83] | |
Ganodermadiol | IC50 = 29 μM | [83] | |
Ganodermanontriol | IC50 = 65 μM | [83] | |
Lucidumol A | IC50 = 99 μM | [83] | |
20-hydroxylucidenic acid N | IC50 = 25 μM | [83] | |
20(21)-dehydrolucidenic acid N | IC50 = 48 μM | [83] | |
Lignosus rhinocerus | Heliantriol F | Binding energy −12.57 kcal/mol | [84] |
Auricularia polytricha | Hexane extract fraction | 0.80 ± 0.08 mg/ml | [85] |
Russula paludosa | 4.5 kDa protein | IC50 = 0.25 mg/mL | [86] |
Cordycep militaris | Adenosine | No quantifiable results | [87] |
iso-sinensetin | No quantifiable results | [87] |
Source | Bioactive Agent | Efficacy* | Reference |
---|---|---|---|
Agaricus bisporus | Aqueous extract with low molecular weight (< 3 kDa) faction | 20.5 µg/mL, viral inhibition = 67.2–87.7% | [88] |
Alternaria alternata | Alternariol | IC50 = 52.0 ± 4.4 µg/mL IC50 = 52.0 ± 4.4 µg/mL CC50 > 10 µg/mL on human bronchial epithelial BEAS-2B cells | [89,90,91] |
Alternariol-9-methyl- ether-3-O-sulphate | IC50 = 32.3 ± 2.6 µg/mL | [89] | |
Alternariol-9-methyl ether | IC50 = 12.0 ± 3.8 µg/mL CC50 > 7.7 µg/mL on human bone osteosarcoma epithelial U-2 OS cells | [89,92] | |
Antrodia cinnamomea | Antrodin A | IC50 = 0.9 µg/mL | [97] |
Antrodin C | IC50 = 2.9 µg/mL | [97] | |
Antrodin D | IC50 = 20.0 µg/mL | [97] | |
Antrodin E | IC50 = 20.1 µg/mL | [97] | |
Aspergillus ochraceus | Mellein | IC50 = 35 μM | [96] |
Aspergillus versicolor | (−)-Curvularin | IC50 = 37.5 ± 3.6 µg/mL | [103] |
Cyclo(L-Pro-L-Ile) | IC50 = 13.7 ± 3.3 µg/mL | [103] | |
Cyclo(L-Tyr-L-Pro) | IC50 = 8.2 ± 1.7 µg/mL | [103] | |
Cyclo(L-Phe-L-Pro) | IC50 = 88.8 ± 4.5 µg/mL | [103] | |
Cyclo- (Phenylalanyl-Pro-Leu-Pro) | IC50 = 95.3 ± 2.7 µg/mL | [103] | |
Emericella nidulans | Cordycepin | IC50 = 24.5 ± 2.3 µg/mL CC50 > 3.2 µg/mL on human umbilical vein endothelial cells and > 100 µg/mL on HEK 293 cells | [98,99,100] |
Emericellin | IC50 = 50.0 ± 3.8 µg/mL | [98] | |
Ergosterol peroxide | IC50 = 47.0 ± 3.4 µg/mL CC50 95 µg/mL on normal lung BEAS-2B cells and > 26.7 µg/mL normal human fibroblast BJ cells | [98,101] | |
Myristic acid | IC50 = 51.0 ± 2.6 µg/mL CC50 > 50 µg/mL on human dermal fibroblast cells | [98,102] | |
Sterigmatocystin | IC50 = 48.5 ± 4.2 µg/mL | [98] | |
Fusarium equiseti | Griseoxanthone C | IC50 = 19.88 ± 1.45 μM | [93] |
ω-Hydroxyemodin | IC50 = 10.7 μM | [93] | |
Cyclo-L-ALA-L-Leu | IC50 = 58.33 ± 3.51 μM | [93] | |
Cyclo(L-Pro-L-Val) | IC50 = 23.29 ± 1.23 μM | [93] | |
Thymine | IC50 = 51.82 ± 2.49 μM | [93] | |
Cyclo-(Phenylalanyl-Pro-Leu-Pro) | IC50 = 29.45 ± 1.98 μM | [93] | |
17-Demethyl-2,11-dideoxy-rhizoxin | IC50 = 34.42 ± 1.44 μM | [93] | |
Ergostra-5,7-dien-3β-ol | IC50 = 77.14 ± 4.55 μM | [93] | |
3-O-β-Glucosylsitosterol | IC50 = 76.56 ± 3.78 μM | [93] | |
5-Chloro-3,6-dihydroxy-2-methyl-1,4-benzoquinone | IC50 = 35.15 ± 3.92 μM | [93] | |
Cyclo(L-Tyr-L-Pro) | IC50= 18.20 ± 1.7 μM | [93] | |
Perlolyrine | IC50 = 37.89 ± 2.11 μM | [93] | |
Cordycepin | IC50 = 22.35 ± 3.12 μM CC50 > 3.2 µg/mL on human umbilical vein endothelial cells and > 100 µg/mL on HEK 293 cells | [93] | |
Ara-A | IC50 = 24.53 ± 2.3 μM | [93] | |
Fusarium oxysporum | H1-A | VX950 inhibitory constant value was 3.5 μmol/L | [94] |
Penicillium chrysogenum | Alatinone | IC50 = 370 μM | [104] |
Emodin | IC50 = 80 μM | [104] | |
ω-Hydroxyemodin | IC50 = 30 μM | [104] | |
Penicillium griseofulvum | Patulin | IC50 = 24.7 µM | [95] |
Category | Bioactive Agent | Source | Immune Effects | Reference |
---|---|---|---|---|
Lectins | Concanavalin A | Volvariella volvacea | Activating T lymphocytes | [130] |
Ricin-B-like lectin (CNL) | Clitocybe nebularis | Stimulating dendritic cells (DCs) and cytokines | [131] | |
TML-1, TML-2 | Tricholoma mongolicum | Macrophages activator (TNF-α, Nitrite ions) | [132] | |
Fungal immunomodulatory proteins (FIPs) | FIP-fve | Flammulina velutipes | Stimulating lymphocyte mitogenesis, enhancing transcription of IL-2, IFN- γ, and TNF-α | [133,134] |
Fip-gat | Ganoderma atrum | Inducing apoptosis via autophagy | [135] | |
Fip-gts | Ganoderma tsugae | Inducing apoptosis via autophagy | [136] | |
FIP-gsi | Ganoderma sinensis | Cytokines regulation (IL-2, IL-3, IL-4, IFN- γ, TNF-α) | [137] | |
Fip-lti1, Fip-lti2 | Lentinus tigrinus | Cytokines regulation (TNF-α, IL-1β, and IL-6) | [138] | |
FIP-ppl | Postia placenta | Enhancing interleukin-2 (IL-2) | [139] | |
FIP-SJ75 | Ganoderma lucidum, Flammulina velutipes, Volvariella volvacea | Activating macrophage M1 polarization and initiating pro-inflammatory response | [121] | |
Fip-vvo | Volvariella volvacea | Lymphocytes activator, cytokine regulation | [140] | |
GMI | Ganoderma microsporum | Inducing apoptosis via autophagy | [141] | |
Ling Zhi-8 (Lz-8) | Ganoderma lucidum | T cell and macrophages activator, cytokine regulation | [142,143] | |
Polysaccharides | α- and β-glucans | Agaricus bisporus, Agaricus brasiliensis, Ganoderma lucidum | Inducing synthesis of IFN-γ | [144] |
β-glucan | Grifola frondosa | Activating macrophages, NK cells, lymphokines and cytokines | [145,146] | |
Polysaccharides | Galactomannan | Morchella esculenta, Morchella conica | Activating macrophages and cytokines | [147,148] |
Grifolan | Grifola frondosa | Activating macrophages and lymphokines | [149] | |
Lentinan | Lentinus edodes | T-cell-oriented adjuvant | [149] | |
PS-G | Ganoderma lucidum | Activating macrophages and T lymphocytes | [135,136] | |
Schizophyllan | Schizophyllum commune | Activating T cell, increasing interleukin and TNF-α production | [150] | |
Terpenoids | Exobiopolymers | Ganoderma applanatum | Activating NK cell | [128] |
Ganolucidoid A and B | Ganoderma lucidum | NO production, anti-inflammatory activities | [130] | |
Lanostane | Hypholoma fasciculare | NO production, anti-inflammatory activities | [151] |
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Suwannarach, N.; Kumla, J.; Sujarit, K.; Pattananandecha, T.; Saenjum, C.; Lumyong, S. Natural Bioactive Compounds from Fungi as Potential Candidates for Protease Inhibitors and Immunomodulators to Apply for Coronaviruses. Molecules 2020, 25, 1800. https://doi.org/10.3390/molecules25081800
Suwannarach N, Kumla J, Sujarit K, Pattananandecha T, Saenjum C, Lumyong S. Natural Bioactive Compounds from Fungi as Potential Candidates for Protease Inhibitors and Immunomodulators to Apply for Coronaviruses. Molecules. 2020; 25(8):1800. https://doi.org/10.3390/molecules25081800
Chicago/Turabian StyleSuwannarach, Nakarin, Jaturong Kumla, Kanaporn Sujarit, Thanawat Pattananandecha, Chalermpong Saenjum, and Saisamorn Lumyong. 2020. "Natural Bioactive Compounds from Fungi as Potential Candidates for Protease Inhibitors and Immunomodulators to Apply for Coronaviruses" Molecules 25, no. 8: 1800. https://doi.org/10.3390/molecules25081800