Inhibition of HIV Budding by a Genetically Selected Cyclic Peptide Targeting the Gag−TSG101 Interaction
Open accessAbstract
The egress of HIV particles from virus-infected cells is accomplished by the recruitment of proteins that normally mediate host cell endocytic functions. This process requires interaction of the HIV Gag protein with the host protein TSG101 (tumor susceptibility gene 101). Here, we report the use of a bacterial reverse two-hybrid system to identify cyclic peptides that interfere with the Gag-TSG101 interaction and the finding that a five amino acid peptide discovered by this approach can disrupt the interaction and consequently inhibit HIV egress. The inhibiting molecule, which was selected from a cyclic peptide library containing approximately 3.2 x 10(6) members, differs in primary sequence from the interacting sites of either TSG101 or Gag. Addition of cyclic peptide tagged with an HIV Tat sequence, which previously has been shown to enhance protein translocation across plasma membranes, to cultured human cells inhibited the production of virus-like particles (VLPs) by these cells (IC(50) of 7 microM), and this inhibition occurred in the absence of adverse affects on normal endocytic functions mediated by TSG101. A mutant Gag protein not dependent on TSG101 for release was unaffected by the cyclic peptide. Our findings, which suggest that interference with the TSG101-Gag interaction by cyclic peptides may be of practical use in the treatment of HIV infections, identify a specific cyclic peptide that reduces VLP release by this mechanism; they also demonstrate that the efficiency of interference with protein-protein interactions by cyclic peptides can be enhanced by tagging the peptides with translocation-promoting sequences. Collectively our results support the notion that small molecule therapeutics that inhibit specific interactions between viral and host proteins may have general applicability in antiviral therapy.
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Cites
Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding
Garrus, J. E., von Schwedler, U. K., Pornillos, O. W., Morham, S. G., Zavitz, K. H., Wang, H. E., Wettstein, D. A., Stray, K. M., Côté, M., Rich, R. L., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00506-2 · Cited by 1,369 · see citing works
Receptor downregulation and multivesicular-body sorting
Katzmann, D. J., Odorizzi, G., & Emr, S. D. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm973 · Cited by 1,201 · see citing works
Clavel, F., & Hance, A. J. (2004) · New England Journal of Medicine · doi:10.1056/nejmra025195 · Cited by 787 · see citing works
Martin-Serrano, J., Zang, T., & Bieniasz, P. D. (2001) · Nature Medicine · doi:10.1038/nm1201-1313 · Cited by 710 · see citing works
Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release
Göttlinger, H. G., Dorfman, T., Sodroski, J. G., & Haseltine, W. A. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.8.3195 · Cited by 647 · see citing works
VerPlank, L., Bouamr, F., LaGrassa, T. J., Agresta, B., Kikonyogo, A., Leis, J., & Carter, C. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131059198 · Cited by 584 · see citing works
Haldimann, A., & Wanner, B. L. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.21.6384-6393.2001 · Cited by 578 · see citing works
Morita, E., & Sundquist, W. I. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.010403.102350 · Cited by 574 · see citing works
Huang, M., Orenstein, J. M., Martin, M. A., & Freed, E. O. (1995) · Journal of Virology · doi:10.1128/jvi.69.11.6810-6818.1995 · Cited by 486 · see citing works
Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes
Bache, K. G., Brech, A., Mehlum, A., & Stenmark, H. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302131 · Cited by 470 · see citing works
Freed, E. (2002) · Journal of Virology · doi:10.1128/jvi.76.10.4679-4687.2002 · Cited by 444 · see citing works
Li, L.-M., & Cohen, S. N. (1996) · Cell · doi:10.1016/s0092-8674(00)81111-3 · Cited by 354 · see citing works
Self-citationTSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation
Lu, Q., Hope, L. W., Brasch, M. A., Reinhard, C., & Cohen, S. N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0932599100 · Cited by 319 · see citing works
Self-citationHermida-Matsumoto, L., & Resh, M. D. (2000) · Journal of Virology · doi:10.1128/jvi.74.18.8670-8679.2000 · Cited by 265 · see citing works
HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein
Pornillos, O., Higginson, D. S., Stray, K. M., Fisher, R. D., Garrus, J. E., Payne, M., He, G.-P., Wang, H. E., Morham, S. G., & Sundquist, W. I. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302138 · Cited by 258 · see citing works
Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein
Pornillos, O., Alam, S. L., Davis, D. R., & Sundquist, W. I. (2002) · Nature Structural Biology · doi:10.1038/nsb856 · Cited by 243 · see citing works
Rossi, J. J., June, C. H., & Kohn, D. B. (2007) · Nature Biotechnology · doi:10.1038/nbt1367 · Cited by 233 · see citing works
Smith, A. J., Cho, M. I., Hammarskjöld, M., & Rekosh, D. M. (1990) · Journal of Virology · doi:10.1128/jvi.64.6.2743-2750.1990 · Cited by 179 · see citing works
Split-intein mediated circular ligation used in the synthesis of cyclic peptide libraries in E. coli
Tavassoli, A., & Benkovic, S. J. (2007) · Nature Protocols · doi:10.1038/nprot.2007.152 · Cited by 171 · see citing works
Self-citationGöttlinger, H. G. (2001) · AIDS · doi:10.1097/00002030-200100005-00003 · Cited by 124 · see citing works
Role of HIV-1 Gag domains in viral assembly
Scarlata, S., & Carter, C. (2003) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/s0005-2736(03)00163-9 · Cited by 111 · see citing works
A systematic method for identifying small-molecule modulators of protein–protein interactions
Horswill, A. R., Savinov, S. N., & Benkovic, S. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406999101 · Cited by 110 · see citing works
Self-citationTsg101 Control of Human Immunodeficiency Virus Type 1 Gag Trafficking and Release
Goff, A., Ehrlich, L. S., Cohen, S. N., & Carter, C. (2003) · Journal of Virology · doi:10.1128/jvi.77.17.9173-9182.2003 · Cited by 105 · see citing works
Self-citationStructural requirements for the biosynthesis of backbone cyclic peptide libraries
Scott, C. P., Abel‐Santos, E., Jones, A. D., & Benkovic, S. J. (2001) · Chemistry & Biology · doi:10.1016/s1074-5521(01)00052-7 · Cited by 101 · see citing works
Self-citationGenetically Selected Cyclic‐Peptide Inhibitors of AICAR Transformylase Homodimerization
Tavassoli, A., & Benkovic, S. J. (2005) · Angewandte Chemie International Edition · doi:10.1002/anie.200500417 · Cited by 93 · see citing works
Self-citationHIV-1 and the host cell: an intimate association
Freed, E. O. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.02.001 · Cited by 92 · see citing works
HIV–host interactions: vital to the virus and key to its inhibition
Trkola, A. (2004) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.08.001 · Cited by 41 · see citing works
SAR by Oxime‐Containing Peptide Libraries: Application to Tsg101 Ligand Optimization
Liu, F., Stephen, A. G., Waheed, A. A., Aman, M. J., Freed, E. O., Fisher, R. J., & Burke, T. R. (2008) · ChemBioChem · doi:10.1002/cbic.200800281 · Cited by 29 · see citing works
HIV–host interactions: vital to the virus and key to its inhibition
Trkola, A. (2004) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.06.002 · Cited by 26 · see citing works
Liu, F., Stephen, A. G., Fisher, R. J., & Burke, T. R. (2008) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2007.12.003 · Cited by 21 · see citing works
Mechanisms of enveloped virus release
Freed, E. O. (2004) · Virus Research · doi:10.1016/j.virusres.2004.08.006 · Cited by 18 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
New developments in RiPP discovery, enzymology and engineering
Montalbán‐López, M., Scott, T. A., Ramesh, S., Rahman, I. R., van Heel, A. J., Viel, J. H., Bandarian, V., Dittmann, E., Genilloud, O., Goto, Y., et al. (2020) · Natural Product Reports · doi:10.1039/d0np00027b · Cited by 775 · see citing works
Understanding Cell Penetration of Cyclic Peptides
Dougherty, P. G., Sahni, A., & Pei, D. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.9b00008 · Cited by 581 · see citing works
Modulators of Protein–Protein Interactions
Milroy, L.-G., Grossmann, T. N., Hennig, S., Brunsveld, L., & Ottmann, C. (2014) · Chemical Reviews · doi:10.1021/cr400698c · Cited by 497 · see citing works
Inteins: nature's gift to protein chemists
Shah, N. H., & Muir, T. W. (2014) · Chem. Sci. · doi:10.1039/c3sc52951g · Cited by 404 · see citing works
Cyclic Peptides as Therapeutic Agents and Biochemical Tools
Joo, S. H. (2012) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2012.20.1.019 · Cited by 359 · see citing works
Modulating protein–protein interactions: the potential of peptides
Nevola, L., & Giralt, E. (2014) · Chemical Communications · doi:10.1039/c4cc08565e · Cited by 291 · see citing works
Sohrabi, C., Foster, A., & Tavassoli, A. (2020) · Nature Reviews Chemistry · doi:10.1038/s41570-019-0159-2 · Cited by 230 · see citing works
Self-citationSelection-Based Discovery of Druglike Macrocyclic Peptides
Passioura, T., Katoh, T., Goto, Y., & Suga, H. (2014) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060713-035456 · Cited by 221 · see citing works
Stynen, B., Tournu, H., Tavernier, J. H., & Dijck, P. V. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05021-11 · Cited by 204 · see citing works
Cardote, T. A. F., & Ciulli, A. (2015) · ChemMedChem · doi:10.1002/cmdc.201500450 · Cited by 189 · see citing works
Miranda, E., Nordgren, I. K., Male, A. L., Lawrence, C. E., Hoakwie, F., Cuda, F., Court, W., Fox, K. R., Townsend, P. A., Packham, G. K., et al. (2013) · Journal of the American Chemical Society · doi:10.1021/ja402993u · Cited by 185 · see citing works
Self-citationA lanthipeptide library used to identify a protein–protein interaction inhibitor
Yang, X., Lennard, K. R., He, C., Walker, M. C., Ball, A. T., Doigneaux, C., Tavassoli, A., & van der Donk, W. A. (2018) · Nature Chemical Biology · doi:10.1038/s41589-018-0008-5 · Cited by 153 · see citing works
Self-citationNovel approaches to inhibiting HIV-1 replication
Adamson, C. S., & Freed, E. O. (2009) · Antiviral Research · doi:10.1016/j.antiviral.2009.09.009 · Cited by 145 · see citing works
SICLOPPS cyclic peptide libraries in drug discovery
Tavassoli, A. (2017) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2017.02.016 · Cited by 139 · see citing works
Self-citationRapid selection of cyclic peptides that reduce α-synuclein toxicity in yeast and animal models
Kritzer, J. A., Hamamichi, S., McCaffery, J. M., Santagata, S., Naumann, T. A., Caldwell, K. A., Caldwell, G. A., & Lindquist, S. L. (2009) · Nature Chemical Biology · doi:10.1038/nchembio.193 · Cited by 138 · see citing works
Lian, W., Upadhyaya, P., Rhodes, C. A., Liu, Y., & Pei, D. (2013) · Journal of the American Chemical Society · doi:10.1021/ja405106u · Cited by 129 · see citing works
Cell-Permeable Bicyclic Peptide Inhibitors against Intracellular Proteins
Lian, W., Jiang, B., Qian, Z., & Pei, D. (2014) · Journal of the American Chemical Society · doi:10.1021/ja503710n · Cited by 128 · see citing works
Evolution of cyclic peptide protease inhibitors
Young, T. S., Young, D. D., Ahmad, I., Louis, J. M., Benkovic, S. J., & Schultz, P. G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108045108 · Cited by 128 · see citing works
Self-citationOwens, A. E., Iannuzzelli, J. A., Gu, Y., & Fasan, R. (2020) · ACS Central Science · doi:10.1021/acscentsci.9b00927 · Cited by 115 · see citing works
Lombardi, L., Genio, V. D., Alberício, F., & Williams, D. R. (2025) · Chemical Reviews · doi:10.1021/acs.chemrev.4c00989 · Cited by 126 · see citing works
Bouřa, E., Różycki, B., Herrick, D. Z., Chung, H. S., Večeř, J., Eaton, W. A., Cafiso, D. S., Hummer, G., & Hurley, J. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101763108 · Cited by 109 · see citing works
Cyclic Peptides: Promising Scaffolds for Biopharmaceuticals
Gang, D., Kim, D.-W., & Park, H.-S. (2018) · Genes · doi:10.3390/genes9110557 · Cited by 103 · see citing works
Han, Z., Lu, J., Liu, Y., Davis, B., Lee, M. S., Olson, M. A., Ruthel, G. T., Freedman, B. D., Schnell, M. J., Wrobel, J. E., et al. (2014) · Journal of Virology · doi:10.1128/jvi.00591-14 · Cited by 100 · see citing works
Peptide drugs to target G protein-coupled receptors
Bellmann‐Sickert, K., & Beck‐Sickinger, A. G. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.06.003 · Cited by 95 · see citing works
Host proteins involved in HIV infection: new therapeutic targets.
Arhel, N., & Kirchhoff, F. (2010) · Biochimica et Biophysica Acta · doi:10.1016/j.bbadis.2009.12.003 · Cited by 133 · see citing works
Birts, C. N., Nijjar, S. K., Mardle, C. A., Hoakwie, F., Duriez, P. J., Blaydes, J. P., & Tavassoli, A. (2013) · Chemical Science · doi:10.1039/c3sc50481f · Cited by 85 · see citing works
Self-citationHIV Type 1 Gag as a Target for Antiviral Therapy
Waheed, A. A., & Freed, E. O. (2011) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2011.0230 · Cited by 81 · see citing works
Garcia, A., & Camarero, J. A. (2010) · Current Molecular Pharmacology · doi:10.2174/1874-470211003030153 · Cited by 78 · see citing works
Therapeutic Application of Lantibiotics and Other Lanthipeptides: Old and New Findings
Staden, A. D. P. V., van Zyl, W. F., Trindade, M., Dicks, L. M. T., & Smith, C. (2021) · Applied and Environmental Microbiology · doi:10.1128/aem.00186-21 · Cited by 76 · see citing works
Crystallographic and Functional Analysis of the ESCRT-I /HIV-1 Gag PTAP Interaction
Im, Y. J., Kuo, L. S., Ren, X., Burgos, P. V., Zhao, X. Z., Liu, F., Burke, T. R., Bonifacino, J. S., Freed, E. O., & Hurley, J. H. (2010) · Structure · doi:10.1016/j.str.2010.08.010 · Cited by 76 · see citing works
Peptides Come Round: Using SICLOPPS Libraries for Early Stage Drug Discovery
Lennard, K. R., & Tavassoli, A. (2014) · Chemistry - A European Journal · doi:10.1002/chem.201403117 · Cited by 75 · see citing works
Self-citationVirus maturation as a new HIV-1 therapeutic target
Adamson, C. S., Salzwedel, K., & Freed, E. O. (2009) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903039714 · Cited by 72 · see citing works
Mechanistic Studies on the Substrate-Tolerant Lanthipeptide Synthetase ProcM
Mukherjee, S., & van der Donk, W. A. (2014) · Journal of the American Chemical Society · doi:10.1021/ja504692v · Cited by 68 · see citing works
Spurr, I. B., Birts, C. N., Cuda, F., Benkovic, S. J., Blaydes, J. P., & Tavassoli, A. (2012) · ChemBioChem · doi:10.1002/cbic.201200279 · Cited by 68 · see citing works
Self-citationProline‐Rich Regions and Motifs in Trafficking: From ESCRT Interaction to Viral Exploitation
Ren, X., & Hurley, J. H. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01208.x · Cited by 65 · see citing works
Synthetic Genomics and Synthetic Biology Applications Between Hopes and Concerns
König, H., Frank, D. O., Heil, R., & Coenen, C. (2013) · Current Genomics · doi:10.2174/1389202911314010003 · Cited by 63 · see citing works
Hepatitis E Virus Drug Development
Kinast, V., Burkard, T. L., Tödt, D., & Steinmann, E. (2019) · Viruses · doi:10.3390/v11060485 · Cited by 63 · see citing works
Han, Z., Madara, J. J., Herbert, A. S., Prugar, L. I., Ruthel, G. T., Lu, J., Liu, Y., Liu, W., Liu, X., Wrobel, J. E., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005220 · Cited by 55 · see citing works
Tsg101 chaperone function revealed by HIV-1 assembly inhibitors
Strickland, M., Ehrlich, L. S., Watanabe, S. M., Khan, M. B., Strub, M., Luan, C.-H., Powell, M. D., Leis, J. P., Tjandra, N., & Carter, C. A. (2017) · Nature Communications · doi:10.1038/s41467-017-01426-2 · Cited by 55 · see citing works
Targeting the ubiquitin–proteasome system to activate wild-type p53 for cancer therapy
Allende-Vega, N., & Saville, M. K. (2009) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2009.10.004 · Cited by 51 · see citing works
Ahsanullah, A., & Rademann, J. (2010) · Angewandte Chemie International Edition · doi:10.1002/anie.200904980 · Cited by 51 · see citing works
Fu, Y., Jaarsma, A. H., & Kuipers, O. P. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03759-0 · Cited by 48 · see citing works
Synthetic biology approaches in drug discovery and pharmaceutical biotechnology
Neumann, H., & Neumann‐Staubitz, P. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2578-3 · Cited by 49 · see citing works
BK Polyomavirus Hijacks Extracellular Vesicles for En Bloc Transmission
Handala, L., Blanchard, E., Raynal, P. I., Roingeard, P., Morel, V., Descamps, V., Castelain, S., François, C., Duverlie, G., Brochot, É., et al. (2020) · Journal of Virology · doi:10.1128/jvi.01834-19 · Cited by 48 · see citing works
Kenney, S. P., Wentworth, J. L., Heffron, C. L., & Meng, X.-J. (2015) · Virology · doi:10.1016/j.virol.2015.09.012 · Cited by 39 · see citing works
Sancheti, H., & Camarero, J. A. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.07.003 · Cited by 45 · see citing works
Antiviral strategies for hepatitis E virus
Debing, Y., & Neyts, J. H. (2013) · Antiviral Research · doi:10.1016/j.antiviral.2013.12.005 · Cited by 45 · see citing works
David, F., Davis, A. M., Gossing, M., Hayes, M. A., Romero, E., Scott, L. H., & Wigglesworth, M. J. (2021) · SLAS DISCOVERY · doi:10.1177/24725552211000669 · Cited by 45 · see citing works
Split Inteins: Nature’s Protein Ligases
Shah, N. H., & Muir, T. W. (2011) · Israel Journal of Chemistry · doi:10.1002/ijch.201100094 · Cited by 44 · see citing works
Frost, J. R., Jacob, N. T., Papa, L. J., Owens, A. E., & Fasan, R. (2015) · ACS Chemical Biology · doi:10.1021/acschembio.5b00119 · Cited by 42 · see citing works
Methods for the Creation of Cyclic Peptide Libraries for Use in Lead Discovery
Foster, A. D., Ingram, J. D., Leitch, E. K., Lennard, K. R., Osher, E. L., & Tavassoli, A. (2015) · SLAS DISCOVERY · doi:10.1177/1087057114566803 · Cited by 42 · see citing works
Self-citationProtein splicing: A versatile tool for drug discovery☆
Cheriyan, M., & Perler, F. B. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.04.021 · Cited by 41 · see citing works
Ribosomal synthesis of backbone macrocyclic peptides
Katoh, T., Goto, Y., Reza, M. S., & Suga, H. (2011) · Chemical Communications · doi:10.1039/c1cc12647d · Cited by 39 · see citing works
Ribosomal Synthesis of Natural‐Product‐Like Bicyclic Peptides in Escherichia coli
Bionda, N., & Fasan, R. (2015) · ChemBioChem · doi:10.1002/cbic.201500179 · Cited by 38 · see citing works
Anang, S., Kaushik, N., Hingane, S., Kumari, A., Gupta, J., Asthana, S., Shalimar, S., Nayak, B., Ranjith-Kumar, C. T., & Surjit, M. (2018) · Journal of Virology · doi:10.1128/jvi.00684-18 · Cited by 35 · see citing works
Expanding the Chemical Diversity of Genetically Encoded Libraries
Iskandar, S. E., Haberman, V. A., & Bowers, A. A. (2020) · ACS Combinatorial Science · doi:10.1021/acscombsci.0c00179 · Cited by 35 · see citing works
Protein Engineering in Ribosomally Synthesized and Post-translationally Modified Peptides (RiPPs)
Do, T., & Link, A. J. (2022) · Biochemistry · doi:10.1021/acs.biochem.1c00714 · Cited by 35 · see citing works
Deschuyteneer, G., Garcia, S., Michiels, B., Baudoux, B., Degand, H., Morsomme, P., & Soumillion, P. (2010) · ACS Chemical Biology · doi:10.1021/cb100072u · Cited by 33 · see citing works
Ball, A. T., Mohammed, S., Doigneaux, C., Gardner, R. M., Easton, J. W., Turner, S. J., Essex, J. W., Pairaudeau, G., & Tavassoli, A. (2024) · Journal of the American Chemical Society · doi:10.1021/jacs.3c10508 · Cited by 32 · see citing works
Self-citationEmerging Strategies to Access Peptide Macrocycles from Genetically Encoded Polypeptides
Smith, J. M., Frost, J. R., & Fasan, R. (2013) · The Journal of Organic Chemistry · doi:10.1021/jo400119s · Cited by 32 · see citing works
Recent Advances in Synthesis and Identification of Cyclic Peptides for Bioapplications
Ong, Y. S., Gao, L., Kalesh, K., Yu, Z., Wang, J., Liu, C., Li, Y., Sun, H., & Lee, S. S. (2017) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026617666170224121658 · Cited by 32 · see citing works
TSG101: a novel anti-HIV-1 drug target.
Chen, H., Liu, X.-Y., Li, Z.-Y., Zhan, P., & Clercq, E. D. (2010) · Current Medicinal Chemistry · doi:10.2174/092986710790514444 · Cited by 37 · see citing works
Matrix Proteins of Nipah and Hendra Viruses Interact with Beta Subunits of AP-3 Complexes
Sun, W., McCrory, T. S., Khaw, W. Y., Petzing, S. R., Myers, T., & Schmitt, A. P. (2014) · Journal of Virology · doi:10.1128/jvi.02103-14 · Cited by 31 · see citing works
Liu, Y., Lee, M. S., Olson, M. A., & Harty, R. N. (2011) · Advances in Virology · doi:10.1155/2011/341816 · Cited by 31 · see citing works
Development of peptide inhibitors of HIV transmission
Shi, S., Nguyen, P. K., Cabral, H., Diez-Barroso, R., Derry, P. J., Kanahara, S. M., & Kumar, V. (2016) · Bioactive Materials · doi:10.1016/j.bioactmat.2016.09.004 · Cited by 31 · see citing works
When membranes need an ESCRT: endosomal sorting and membrane remodelling in health and disease
Alfred, V., & Vaccari, T. (2016) · Swiss Medical Weekly · doi:10.4414/smw.2016.14347 · Cited by 31 · see citing works
A Review: The Antiviral Activity of Cyclic Peptides
Chia, L. Y., Kumar, P. V., Maki, M. A. A., Ravichandran, G., & Thilagar, S. (2022) · International Journal of Peptide Research and Therapeutics · doi:10.1007/s10989-022-10478-y · Cited by 29 · see citing works
Targeting the protein–protein interactions of the HIV lifecycle
Tavassoli, A. (2010) · Chemical Society Reviews · doi:10.1039/c0cs00092b · Cited by 29 · see citing works
Self-citationHIV-1 Gag as an Antiviral Target: Development of Assembly and Maturation Inhibitors
Spearman, P. W. (2015) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026615666150902102143 · Cited by 29 · see citing works
Recent advances in HIV-1 Gag inhibitor design and development
Dick, A., & Cocklin, S. (2020) · Molecules · doi:10.3390/molecules25071687 · Cited by 28 · see citing works
Selection for constrained peptides that bind to a single target protein
King, A. M., Anderson, D. A., Glassey, E., Segall-Shapiro, T. H., Zhang, Z., Niquille, D. L., Embree, A., Pratt, K., Williams, T. L., Gordon, D. B., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26350-4 · Cited by 27 · see citing works
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Male, A. L., Forafonov, F., Cuda, F., Zhang, G., Zheng, S., Oyston, P. C. F., Chen, P. R., Williamson, E. D., & Tavassoli, A. (2017) · Scientific Reports · doi:10.1038/s41598-017-03253-3 · Cited by 23 · see citing works
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Chung, B. K. W., Hickey, J. L., Scully, C. C. G., Zaretsky, S., & Yudin, A. K. (2013) · MedChemComm · doi:10.1039/c3md00054k · Cited by 18 · see citing works
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Self-citationRosa, S., Tagliani, A., Bertaso, C., Tadini, L., Visentin, C., Gourlay, L. J., Pricl, S., Feni, L., Pellegrino, S., Pesaresi, P., et al. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1017757 · Cited by 13 · see citing works
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Waheed, A. A., & Freed, E. O. (2008) · ACS Chemical Biology · doi:10.1021/cb800296j · Cited by 13 · see citing works
Siarot, L., Chutiwitoonchai, N., Sato, H., Chang, H., Sato, H., Fujino, M., Murakami, T., Aono, T., Kodama, E. N., Kuroda, K., et al. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.08.079 · Cited by 12 · see citing works
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Chen, X., & Wang, X. (2024) · Retrovirology · doi:10.1186/s12977-024-00633-2 · Cited by 12 · see citing works
Ahsanullah, A., & Rademann, J. (2010) · Angewandte Chemie · doi:10.1002/ange.200904980 · Cited by 12 · see citing works
Wang, J., & Holmes, M. C. (2016) · Cytotherapy · doi:10.1016/j.jcyt.2016.07.007 · Cited by 12 · see citing works
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Strickland, M., Nyenhuis, D. A., Watanabe, S. M., Tjandra, N., & Carter, C. A. (2021) · Viruses · doi:10.3390/v13061147 · Cited by 11 · see citing works
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Bowers, A. A. (2012) · MedChemComm · doi:10.1039/c2md20068f · Cited by 11 · see citing works
Liu, F., Stephen, A. G., Waheed, A. A., Freed, E. O., Fisher, R. J., & Burke, T. R. (2009) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2009.10.105 · Cited by 10 · see citing works
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Barreto, K., & Geyer, C. R. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-0799-1_21 · Cited by 10 · see citing works
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Briant, L., Gay, B., Devaux, C. A., & Chazal, N. (2011) · World Journal of AIDS · doi:10.4236/wja.2011.14017 · Cited by 9 · see citing works
Extensions to amino acid description
Gottfries, J., & Eriksson, L. (2009) · Molecular Diversity · doi:10.1007/s11030-009-9204-2 · Cited by 9 · see citing works
Miranda, E., Forafonov, F., & Tavassoli, A. (2011) · Molecular BioSystems · doi:10.1039/c0mb00318b · Cited by 8 · see citing works
Self-citation
- Authors
- Tavassoli, A., Lu, Q., Gam, J., Pan, H., Benkovic, S. J., & Cohen, S. N.
- Affiliations
- University of Southampton (GB)
- Harvard University (US)
- Pennsylvania State University (US)
- Stanford Medicine (US)
- Corresponding author
- Benkovic, Stephen J.
- Cohen, Stanley N.
- Venue
- ACS Chemical Biology
- Publisher
- American Chemical Society (ACS)
- Published
- 2008-11-24
- Volume
- 3
- Issue
- 12
- Pages
- 757-764
- ISSN
- 1554-8929 (ISSN-L)
- 1554-8937
- OpenAlex
- W2052497243
- Cited by
- 153
- References
- 31
- Citations by year
- 2026: 8 · 2025: 3 · 2024: 8 · 2023: 7 · 2022: 8 · 2021: 10 · 2020: 9 · 2019: 6 · 2018: 8 · 2017: 6 · 2016: 5 · 2015: 9 · 2014: 11 · 2013: 15 · 2012: 5
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- ACS Chemical Biology (publishedVersion, other-oa)
- PubMed (publishedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- Funders
- Defense Advanced Research Projects Agency
- Defense Threat Reduction Agency
- Topics
- Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chemical Synthesis and Analysis
- Health Sciences › Medicine › Infectious Diseases › HIV/AIDS drug development and treatment
- Keywords
- HIV budding, cyclic peptides, protein-protein interaction inhibition, TSG101, HIV gag protein, virus-like particles, plasma membrane translocation, antiviral therapy, host-virus interaction
- MeSH terms
- Tsg101 Protein, Cells, Cultured, DNA-Binding Proteins, Escherichia coli, Humans, Ligands, Peptides, Cyclic, Protein Binding, Structure-Activity Relationship, Transcription Factors, Molecular Structure, HIV-1, Peptide Library, Anti-HIV Agents, Two-Hybrid System Techniques, gag Gene Products, Human Immunodeficiency Virus, Endosomal Sorting Complexes Required for Transport
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