In vitro Inhibition of HIV-1 by Cyclotide-Enriched Extracts of Viola tricolor
Tóm tắt
Since viral infectious diseases continue to be a global health threat, new antiviral drugs are urgently needed. A unique class of therapeutic compounds are antimicrobial peptides (AMPs). They can be found in humans, bacteria and plants. Plants express a wide variety of such defense peptides as part of their innate immune system to protect from invading pathogens. Cyclotides are non-classical AMPs that share a similar structure. Their unique topology consists of a circular peptide backbone and disulfide bonds. In previous studies they have been attributed to a wide range of biological activities. To identify novel cyclotides with antiviral activity, we established a library of plant extracts largely consisting of cyclotide-rich species and screened them as inhibitors of HIV-1 infection. Subsequent extraction and fractionation revealed four cyclotide-containing subfractions from
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Al Musaimi, 2021, 2020 FDA TIDES (Peptides and Oligonucleotides) Harvest, Pharm. (Basel), 14, 145, 10.3390/ph14020145
Álvarez, 2018, Identification of Peptides in Flowers of Sambucus Nigra with Antimicrobial Activity against Aquaculture Pathogens, Molecules, 23, 1, 10.3390/molecules23051033
Atanasov, 2021, Natural Products in Drug Discovery: Advances and Opportunities, Nat. Rev. Drug Discov., 20, 200, 10.1038/s41573-020-00114-z
Bokesch, 2001, A Novel Anti-HIV Macrocyclic Peptide from Palicourea Condensata, J. Nat. Prod., 64, 249, 10.1021/np000372l
Browne, 2020, A New Era of Antibiotics: The Clinical Potential of Antimicrobial Peptides, Int. J. Mol. Sci., 21, 1, 10.3390/ijms21197047
Brügger, 2006, The HIV Lipidome: A Raft with an Unusual Composition, Proc. Natl. Acad. Sci. U. S. A., 103, 2641, 10.1073/pnas.0511136103
Burman, 2015, Distribution of Circular Proteins in Plants: Large-Scale Mapping of Cyclotides in the Violaceae, Front. Plant Sci., 6, 855, 10.3389/fpls.2015.00855
Cai, 2020, Griffithsin with A Broad-Spectrum Antiviral Activity by Binding Glycans in Viral Glycoprotein Exhibits Strong Synergistic Effect in Combination with A Pan-Coronavirus Fusion Inhibitor Targeting SARS-CoV-2 Spike S2 Subunit, Virol. Sin., 35, 857, 10.1007/s12250-020-00305-3
Clark, 2006, Structural Plasticity of the Cyclic-Cystine-Knot Framework: Implications for Biological Activity and Drug Design, Biochem. J., 394, 85, 10.1042/BJ20051691
Colgrave, 2004, Thermal, Chemical, and Enzymatic Stability of the Cyclotide Kalata B1: The Importance of the Cyclic Cystine Knot, Biochemistry, 43, 5965, 10.1021/bi049711q
Cranfield, 2017, Kalata B1 and Kalata B2 Have a Surfactant-like Activity in Phosphatidylethanolomine-Containing Lipid Membranes, Langmuir, 33, 6630, 10.1021/acs.langmuir.7b01642
Cushnie, 2020, Bioprospecting for Antibacterial Drugs: a Multidisciplinary Perspective on Natural Product Source Material, Bioassay Selection and Avoidable Pitfalls, Pharm. Res., 1, 10.1007/s11095-020-02849-1
Daly, 2006, Kalata B8, a Novel Antiviral Circular Protein, Exhibits Conformational Flexibility in the Cystine Knot Motif, Biochem. J., 393, 619, 10.1042/BJ20051371
Daly, 2004, The Role of the Cyclic Peptide Backbone in the Anti-HIV Activity of the Cyclotide Kalata B1, FEBS Lett., 574, 69, 10.1016/j.febslet.2004.08.007
de Veer, 2019, Cyclotides: From Structure to Function, Chem. Rev., 119, 12375, 10.1021/acs.chemrev.9b00402
Dijksteel, 2021, Review: Lessons Learned from Clinical Trials Using Antimicrobial Peptides (AMPs), Front. Microbiol., 12, 616979, 10.3389/fmicb.2021.616979
Esmaeili, 2016, Viola Plant Cyclotide Vigno 5 Induces Mitochondria-Mediated Apoptosis via Cytochrome C Release and Caspases Activation in Cervical Cancer Cells, Fitoterapia, 109, 162, 10.1016/j.fitote.2015.12.021
Fahradpour, 2017, Cyclotides Isolated from an Ipecac Root Extract Antagonize the Corticotropin Releasing Factor Type 1 Receptor, Front. Pharmacol., 8, 1, 10.3389/fphar.2017.00616
Gerlach, 2019, The Membrane-Active Phytopeptide Cycloviolacin O2 Simultaneously Targets HIV-1-Infected Cells and Infectious Viral Particles to Potentiate the Efficacy of Antiretroviral Drugs, Med. (Basel), 6, 33, 10.3390/medicines6010033
Gerlach, 2013, Cycloviolacin O2 (CyO2) Suppresses Productive Infection and Augments the Antiviral Efficacy of Nelfinavir in HIV-1 Infected Monocytic Cells, Biopolymers, 100, 471, 10.1002/bip.22325
Göransson, 2004, Reversible Antifouling Effect of the Cyclotide Cycloviolacin O2 against Barnacles, J. Nat. Prod., 67, 1287, 10.1021/np0499719
Gruber, 2008, Distribution and Evolution of Circular Miniproteins in Flowering Plants, Plant Cell, 20, 2471, 10.1105/tpc.108.062331
Gründemann, 2019, T20K: An Immunomodulatory Cyclotide on its Way to the Clinic, Int. J. Pept. Res. Ther., 25, 9, 10.1007/s10989-018-9701-1
Gustafson, 1994, Circulins A and B. Novel Human Immunodeficiency Virus (HIV)-Inhibitory Macrocyclic Peptides from the Tropical Tree Chassalia Parvifolia, J. Am. Chem. Soc., 116, 9337, 10.1021/ja00099a064
Hashempour, 2013, Characterizing Circular Peptides in Mixtures: Sequence Fragment Assembly of Cyclotides from a Violet Plant by MALDI-TOF/TOF Mass Spectrometry, Amino Acids, 44, 581, 10.1007/s00726-012-1376-x
He, 2013, Novel Inhibitor Cystine Knot Peptides from Momordica Charantia, PLoS One, 8, e75334, 10.1371/journal.pone.0075334
Hellinger, 2019, Peptide-based Protease Inhibitors from Plants, Drug Discov. Today, 24, 1877, 10.1016/j.drudis.2019.05.026
Hellinger, 2014, Immunosuppressive Activity of an Aqueous Viola Tricolor Herbal Extract, J. Ethnopharmacol., 151, 299, 10.1016/j.jep.2013.10.044
Hellinger, 2015, Peptidomics of Circular Cysteine-Rich Plant Peptides: Analysis of the Diversity of Cyclotides from Viola Tricolor by Transcriptome and Proteome Mining, J. Proteome Res., 14, 4851, 10.1021/acs.jproteome.5b00681
Henriques, 2012, Importance of the Cell Membrane on the Mechanism of Action of Cyclotides, ACS Chem. Biol., 7, 626, 10.1021/cb200395f
Henriques, 2012, Phosphatidylethanolamine Binding Is a Conserved Feature of Cyclotide-Membrane Interactions, J. Biol. Chem., 287, 33629, 10.1074/jbc.M112.372011
Henriques, 2011, Decoding the Membrane Activity of the Cyclotide Kalata B1: The Importance of Phosphatidylethanolamine Phospholipids and Lipid Organization on Hemolytic and Anti-HIV Activities, J. Biol. Chem., 286, 24231, 10.1074/jbc.M111.253393
Huan, 2020, Antimicrobial Peptides: Classification, Design, Application and Research Progress in Multiple Fields, Front. Microbiol., 11, 1, 10.3389/fmicb.2020.582779
Ireland, 2006, A Novel Suite of Cyclotides from Viola Odorata: Sequence Variation and the Implications for Structure, Function and Stability, Biochem. J., 400, 1, 10.1042/BJ20060627
Jackman, 2018, Therapeutic Treatment of Zika Virus Infection Using a Brain-Penetrating Antiviral Peptide, Nat. Mat., 17, 971, 10.1038/s41563-018-0194-2
Jennings, 2001, Biosynthesis and Insecticidal Properties of Plant Cyclotides: The Cyclic Knotted Proteins from Oldenlandia Affinis, Proc. Natl. Acad. Sci. U. S. A., 98, 10614, 10.1073/pnas.191366898
Karpyuk, 2015, HPLC Determination of Free and Bound Amino Acids in Bryonia Alba, Chem. Nat. Compd., 51, 399, 10.1007/s10600-015-1298-4
Kawano, 2019, Development of a Membrane Curvature-Sensing Peptide Based on a Structure-Activity Correlation Study, Chem. Pharm. Bull. (Tokyo), 67, 1131, 10.1248/cpb.c19-00465
Koehbach, 2013, Cyclotide Discovery in Gentianales Revisited-Iidentification and Characterization of Cyclic Cystine-Knot Peptides and Their Phylogenetic Distribution in Rubiaceae Plants, Biopolymers, 100, 438, 10.1002/bip.22328
Kuroki, 2021, Broad-Spectrum Antiviral Peptides and Polymers, Adv. Healthc. Mat., 10, e2101113, 10.1002/adhm.202101113
Lau, 2018, Therapeutic Peptides: Historical Perspectives, Current Development Trends, and Future Directions, Bioorg Med. Chem., 26, 2700, 10.1016/j.bmc.2017.06.052
Lazzaro, 2020, Antimicrobial Peptides: Application Informed by Evolution, Science, 368, 368, 10.1126/science.aau5480
Lee, 2019, Griffithsin, a Highly Potent Broad-Spectrum Antiviral Lectin from Red Algae: From Discovery to Clinical Application, Mar. Drugs, 17, 10.3390/md17100567
Li, 2021, Plant Antimicrobial Peptides: Structures, Functions, and Applications, Bot. Stud., 62, 5, 10.1186/s40529-021-00312-x
Liu, 2014, A Cyclotide against Influenza A H1N1 Virus from Viola Yedoensis, Yao Xue Xue Bao, 49, 905
Liu, 2017, Expansion and Evolutionary Patterns of Cysteine-Rich Peptides in Plants, BMC Genomics, 18, 610, 10.1186/s12864-017-3948-3
Mahlapuu, 2016, Antimicrobial Peptides: An Emerging Category of Therapeutic Agents, Front. Cell. Infect. Microbiol., 6, 1, 10.3389/fcimb.2016.00194
Mammari, 2021, Plant-derived Antimicrobial Peptides as Potential Antiviral Agents in Systemic Viral Infections, Pharm. (Basel), 14, 1, 10.3390/ph14080774
Mott, 2014, Peptides and Small Molecules of the Plant-Pathogen Apoplastic Arena, Front. Plant Sci., 5, 1, 10.3389/fpls.2014.00677
Mücksch, 2019, Quantification of Phosphoinositides Reveals Strong Enrichment of PIP2 in HIV-1 Compared to Producer Cell Membranes, Sci. Rep., 9, 1, 10.1038/s41598-019-53939-z
Münch, 2007, Semen-Derived Amyloid Fibrils Drastically Enhance HIV Infection, Cell, 131, 1059, 10.1016/j.cell.2007.10.014
Muratspahić, 2021, Plant-Derived Cyclotides Modulate κ-Opioid Receptor Signaling, J. Nat. Prod., 84, 2238, 10.1021/acs.jnatprod.1c00301
Nguyen, 2013, Discovery of Linear Cyclotides in Monocot Plant Panicum Laxum of Poaceae Family Provides New Insights into Evolution and Distribution of Cyclotides in Plants, J. Biol. Chem., 288, 3370, 10.1074/jbc.M112.415356
Nii-Trebi, 2017, Emerging and Neglected Infectious Diseases: Insights, Advances, and Challenges, Biomed. Res. Int., 2017, 5245021, 10.1155/2017/5245021
Nishad, 2020, Modulation of Plant Defense System in Response to Microbial Interactions, Front. Microbiol., 11, 1, 10.3389/fmicb.2020.01298
Papkalla, 2002, Nef Enhances Human Immunodeficiency Virus Type 1 Infectivity and Replication Independently of Viral Coreceptor Tropism, J. Virol., 76, 8455, 10.1128/jvi.76.16.8455-8459.2002
Park, 2019, Comparing the Membrane-Interaction Profiles of Two Antiviral Peptides: Insights into Structure-Function Relationship, Langmuir, 35, 9934, 10.1021/acs.langmuir.9b01052
Patel, 2017, Ethanolamine and Phosphatidylethanolamine: Partners in Health and Disease, Oxid. Med. Cell. Longev., 2017, 1, 10.1155/2017/4829180
Pinto, 2018, Inhibition of Breast Cancer Cell Migration by Cyclotides Isolated from Pombalia Calceolaria, J. Nat. Prod., 81, 1203, 10.1021/acs.jnatprod.7b00969
Poth, 2011, Discovery of Cyclotides in the Fabaceae Plant Family Provides New Insights into the Cyclization, Evolution, and Distribution of Circular Proteins, ACS Chem. Biol., 6, 345, 10.1021/cb100388j
Poth, 2012, Cyclotides Associate with Leaf Vasculature and Are the Products of a Novel Precursor in Petunia (Solanaceae), J. Biol. Chem., 287, 27033, 10.1074/jbc.M112.370841
Retzl, 2020, Discovery of a Beetroot Protease Inhibitor to Identify and Classify Plant-Derived Cystine Knot Peptides, J. Nat. Prod., 83, 3305, 10.1021/acs.jnatprod.0c00648
Schmidt, 2008, A Natural History of Botanical Therapeutics, Metabolism, 57, S3, 10.1016/j.metabol.2008.03.001
Shikov, 2021, Medicinal Plants from the 14th Edition of the Russian Pharmacopoeia, Recent Updates, J. Ethnopharmacol., 268, 113685, 10.1016/J.JEP.2020.113685
Shikov, 2014, Medicinal Plants of the Russian Pharmacopoeia; Their History and Applications, J. Ethnopharmacol., 154, 481, 10.1016/J.JEP.2014.04.007
Shikov, 2017, Traditional and Current Food Use of Wild Plants Listed in the Russian Pharmacopoeia, Front. Pharmacol., 8, 841, 10.3389/FPHAR.2017.00841/BIBTEX
Silverstein, 2007, Small Cysteine-Rich Peptides Resembling Antimicrobial Peptides Have Been Under-predicted in Plants, Plant J., 51, 262, 10.1111/j.1365-313X.2007.03136.x
Slazak, 2021, Cyclotide Host-Defense Tailored for Species and Environments in Violets from the Canary Islands, Sci. Rep., 11, 12452, 10.1038/s41598-021-91555-y
Slazak, 2018, How Does the Sweet Violet (Viola Odorata L.) Fight Pathogens and Pests - Cyclotides as a Comprehensive Plant Host Defense System, Front. Plant Sci., 9, 1296, 10.3389/fpls.2018.01296
Strömstedt, 2017, Bactericidal Activity of Cyclotides where Phosphatidylethanolamine-Lipid Selectivity Determines Antimicrobial Spectra, Biochim. Biophys. Acta Biomembr., 1859, 1986, 10.1016/j.bbamem.2017.06.018
Tang, 2010, Isolation and Characterization of Cytotoxic Cyclotides from Viola Tricolor, Peptides, 31, 1434, 10.1016/j.peptides.2010.05.004
Wang, 2008, Anti-HIV Cyclotides from the Chinese Medicinal Herb Viola Yedoensis, J. Nat. Prod., 71, 47, 10.1021/np070393g
Wang, 2014, Molecular Grafting onto a Stable Framework Yields Novel Cyclic Peptides for the Treatment of Multiple Sclerosis, ACS Chem. Biol., 9, 156, 10.1021/cb400548s
Wang, 2007, CyBase: a Database of Cyclic Protein Sequences and Structures, with Applications in Protein Discovery and Engineering, Nucleic Acids Res., 36, D206, 10.1093/nar/gkm953
Wang, 2022, Therapeutic Peptides: Current Applications and Future Directions, Sig Transduct. Target Ther., 7, 10.1038/s41392-022-00904-4
Wei, 2002, Emergence of Resistant Human Immunodeficiency Virus Type 1 in Patients Receiving Fusion Inhibitor (T-20) Monotherapy, Antimicrob. Agents Chemother., 46, 1896, 10.1128/AAC.46.6.1896-1905.2002
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